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Research Article

The effects of assistance dogs on psychosocial health and wellbeing: A systematic literature review

Roles Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Supervision, Writing – original draft, Writing – review & editing

* E-mail: [email protected]

Current address: Human-Animal Bond in Colorado, School of Social Work, Colorado State University, Fort Collins, Colorado, United States of America

Affiliation Center for the Human-Animal Bond, College of Veterinary Medicine, Purdue University, West Lafayette, Indiana, United States of America

Roles Data curation, Formal analysis, Investigation, Methodology, Writing – review & editing

Affiliation Vassar College, Poughkeepsie, New York, United States of America

Roles Data curation, Investigation, Methodology, Writing – review & editing

Affiliation Purdue University Libraries, Purdue University, West Lafayette, Indiana, United States of America

Roles Conceptualization, Supervision, Writing – review & editing

Roles Conceptualization, Data curation, Project administration, Supervision, Writing – review & editing

• Kerri E. Rodriguez, 
• Jamie Greer, 
• Jane K. Yatcilla, 
• Alan M. Beck, 
• Marguerite E. O’Haire

• Published: December 2, 2020
• https://doi.org/10.1371/journal.pone.0243302
• Peer Review
• Reader Comments

9 Aug 2021: Rodriguez KE, Greer J, Yatcilla JK, Beck AM, O’Haire ME (2021) Correction: The effects of assistance dogs on psychosocial health and wellbeing: A systematic literature review. PLOS ONE 16(8): e0256071. https://doi.org/10.1371/journal.pone.0256071 View correction

Beyond the functional tasks that assistance dogs are trained for, there is growing literature describing their benefits on the psychosocial health and wellbeing of their handlers. However, this research is not only widely disparate but, despite its growth, has not been reviewed since 2012. Our objective was to identify, summarize, and methodologically evaluate studies quantifying the psychosocial effects of assistance dogs for individuals with physical disabilities. Following PRISMA guidelines, a systematic review was conducted across seven electronic databases. Records were independently screened by two authors. Studies were eligible for inclusion if they assessed outcomes from guide, hearing, medical, or mobility service dogs, if they collected original data on handlers’ psychosocial functioning, and if the outcome was measured quantitatively with a validated, standardized measure. Studies on psychiatric service dogs, emotional support dogs, and pet dogs were excluded. Of 1,830 records screened, 24 articles were identified (12 publications, 12 theses) containing 27 studies (15 cross-sectional, 12 longitudinal). Studies assessed the effects of mobility (18), hearing (7), guide (4), and medical (2) assistance dog partnerships with an average sample size of N = 83. An analysis of 147 statistical comparisons across the domains of psychological health, quality of life, social health, and vitality found that 68% of comparisons were null, 30% were positive in the hypothesized direction, and 2% were negative. Positive outcomes included significant effects of having an assistance dog on psychological wellbeing, emotional functioning, self-esteem, and vitality. However, it is of note that several methodological weaknesses of the studies make it difficult to draw any definitive conclusions, including inadequate reporting and a failure to account for moderating or confounding variables. Future research will benefit from stronger methodological rigor and reporting to account for heterogeneity in both humans and assistance dogs as well as continued high-quality replication.

Citation: Rodriguez KE, Greer J, Yatcilla JK, Beck AM, O’Haire ME (2020) The effects of assistance dogs on psychosocial health and wellbeing: A systematic literature review. PLoS ONE 15(12): e0243302. https://doi.org/10.1371/journal.pone.0243302

Editor: Geilson Lima Santana, University of Sao Paulo Medical School, BRAZIL

Received: July 22, 2020; Accepted: November 18, 2020; Published: December 2, 2020

Copyright: © 2020 Rodriguez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper and its Supporting information files.

Funding: The authors received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

Introduction

The roles of dogs to assist in improving human wellbeing continue to expand. Not only are companion dogs prevalent in modern society, but dogs are also often intentionally incorporated into therapeutic processes in the contexts of animal-assisted activities (AAA) and animal-assisted therapy [AAT; 1]. In other contexts, dogs can be specially trained to provide specific benefits to individuals with impairments, disabilities, or chronic conditions as trained assistance animals. Assistance dog placements and roles have grown rapidly in recent decades, especially in the United States, Canada, and Europe [ 2 ].

Assistance Dogs International (ADI) defines three types of assistance dogs, of which we use as terminology in this review: guide dogs who assist individuals with visual impairments, hearing dogs who assist individuals with hearing impairments, and service dogs who assist individuals with disabilities other than blindness or deafness [ 3 ]. Service dogs can assist individuals with physical disabilities (e.g. performing mobility-related tasks such as pulling a wheelchair or retrieving dropped items), individuals with medical conditions (e.g. alerting or responding to medical crises such hypoglycemia or seizures), and individuals with mental health disorders (e.g. psychiatric service dogs for posttraumatic stress disorder or autism spectrum disorder). Under the Americans with Disabilities Act of 1990, a United States law, an assistance dog must do work or perform tasks for the benefit of an individual with a physical, sensory, psychiatric, intellectual, or other mental disability in order to receive public access rights [ 4 ]. While there are no legal requirements specifying that an assistance dog must be certified, registered, or receive any specialized training to receive public access rights, independent organizations such as ADI, the International Association of Assistance Dog Partners (IAADP), and the International Guide Dog Federation (IGDF) define a set of minimum training and behavior standards for public access that help guide the assistance dog industry.

In parallel with an increasing amount of research quantifying the therapeutic benefits of companion dogs and therapy dogs on human health and wellbeing [ 5 , 6 ], there has been an increased focus on quantifying the physical, psychological, and social effects that assistance dogs may have on their handlers [ 7 – 9 ]. Research has indicated that beyond the physical or tangible benefits that an assistance dog is trained to provide (e.g. route finding, retrieving dropped items, alerting to a seizure), the assistance dog’s companionship, emotional and social support, and social facilitation effects in public may be particularly salient to improving the quality of life of individuals with disabilities [ 7 – 9 ]. After receiving an assistance dog, individuals retrospectively report increases to their social, emotional, and psychological health [e.g., 10 – 12 ]. Longitudinal studies have found that individuals report improvements to their emotional wellbeing, social functioning, and quality of life just 3 to 6 months after receiving an assistance dog [ 13 – 15 ]. Compared to those on the waitlist, individuals with an assistance dog report better psychosocial functioning and wellbeing [ 16 , 17 ]. Additionally, research suggests the relationship between an assistance dog and its owner may also serve as a reciprocal attachment and caregiving relationship characterized by secure and strong attachments [ 18 , 19 ].

To date, there have been several reviews summarizing the literature on the psychosocial effects of assistance dogs on their handlers. One of the first reviews published by Modlin in 2000 [ 7 ] summarized nine published quantitative and qualitative studies on the benefits of guide dogs, hearing dogs, and mobility service dogs on their handlers (omitting unpublished theses). Another early review published by Sachs-Ericsson and colleagues in 2002 [ 8 ] summarized 14 quantitative studies on both standardized and nonstandardized outcomes following mobility service dog or hearing dog placement (omitting guide dogs). Neither of these early reviews employed a formal methodological assessment of studies, but limitations were listed for each included study. While both reviews found mostly positive findings regarding mobility, guide, and hearing dogs’ effects on their handlers’ health and wellbeing, social interactions, and activity participation [ 7 , 8 ], it was concluded that “the small number of studies and methodological limitations of these studies preclude any clear conclusions” [ 8 ].

A more recent systematic review published by Winkle and colleagues in 2012 [ 9 ] summarized 12 published quantitative studies on both standardized and nonstandardized outcomes following mobility service dog placement (omitting guide dogs, hearing dogs, and unpublished theses). The scientific rigor of each study was rated according to a 5-level system while the methodological quality of each study was scored on a 7-point scale. While results described positive effects of service dogs in terms of social, psychological, and functional benefits for their handlers, it was concluded that all 12 of the studies had weak study designs with limitations including lack of comparison groups, inadequate description of the service dog intervention, and nonstandardized outcome measures. The authors concluded that although results are promising, “conclusions drawn from the results must be considered with caution” [ 9 ].

Because medical service dogs are a relatively new category of assistance dog placements [ 2 ], there has been less research on the psychosocial effects of medical alert and response service dogs on their handlers. However, a recent 2018 review summarized five published quantitative studies describing outcomes from seizure alert and seizure response service dogs. The authors found three studies reporting an association between having a seizure alert or response dog and improvements to quality of life and wellbeing, concluding a need for more research.

Research in the field of human-animal interaction (HAI) and assistance dogs is not only rapidly growing but is often disparately published across multidisciplinary journals and outlets. Conducting periodic systematic reviews of this research is crucial to both disseminate knowledge as well as to identify knowledge gaps for future studies [ 20 ]. As research on the assistance animal-handler relationship continues to increase, there is a need for an updated, comprehensive collation of the literature encompassing studies on the effects of all varieties of assistance dogs (guide dogs, hearing dogs, and both mobility and medical service dogs) including both published studies and unpublished theses and dissertations. Further, as researchers increasingly incorporate standardized outcome measures into this research, collating and pooling findings will allow researchers to compare outcomes across different populations and interventions while estimating the magnitude of effects across domains.

This research aimed to conduct a systematic assessment of the current state of knowledge regarding the potential benefits of assistance dogs on standardized outcomes of the health and wellbeing of individuals with disabilities. Specifically, this review sought to systematically identify, summarize, and evaluate studies assessing psychosocial outcomes from owning an assistance dog (including service, guide, hearing, and/or medical alert or response dogs) with measures tested for reliability and validity among individuals with physical disabilities. The specific aims were to (1) describe the key characteristics of studies (2) evaluate the methodological rigor of studies (3) summarize outcomes.

Materials and methods

The systematic literature review was conducted according to The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [ 21 ]. A study protocol was designed a-priori to define the search strategy, inclusion and exclusion criteria, and items for data extraction.

Search procedure

As the field of animal-assisted intervention is multidisciplinary, a wide and extensive search was conducted encompassing medical and scientific databases. Further, as publication bias and the “file-drawer effect” is an often referenced weakness of the HAI literature [ 22 ], two dissertation and thesis databases and abstracts of two conferences were searched for unpublished studies.

A health information specialist (JY) constructed and executed comprehensive search strategies in six electronic databases: MEDLINE (PubMed platform), Cumulative Index to Nursing and Allied Health Literature (CINAHL) (EBSCOhost platform), ERIC (EBSCOHost), Web of Science Core Collection (Web of Science), PsycINFO (EBSCOhost), and PsycARTICLES (EBSCOhost). The electronic searches were performed on July 23, 2018, and updated on January 23, 2019. The complete MEDLINE search strategy, which was adapted for the other databases, is shown in S1 Table . Grey literature was addressed by searching ProQuest Dissertations and Theses (ProQuest) and WorldCatDissertations and hand searching the abstracts of the International Society for Anthrozoology and International Association of Human Animal Interactions Organizations conferences.

Article selection

Studies were eligible for inclusion if they met the following criteria: (1) The study population consisted of current or prospective owners/handlers of an assistance dog (including service, guide, hearing, and/or medical alert or response dogs) with a physical disability or chronic condition in which the assistance dog is trained to do work or perform tasks directly related to the disability or condition [ 4 ]; (2) The study collected original data on the effect of the assistance dog on their handler with at least one psychosocial outcome, including those quantifying aspects of mental health, social health, and health-related quality of life; and (3) The psychosocial outcome(s) were collected via a standardized measure tested for validity and reliability. The rationale for excluding studies on emotional service dogs and psychiatric service dogs is that the primary benefits of these dogs are psychological in nature, rather than physical or medical, which complicated comparisons of their psychosocial effects. The rationale for excluding qualitative studies from inclusion was to focus on outcomes using standardized measures to facilitate quantitative comparisons across studies.

Article screening

All articles were screened by two independent reviewers (authors KR and JG) using Covidence systematic review software (Veritas Health Innovation, Melbourne, Australia). In the case of disagreements, inclusion or exclusion was resolved by discussion and consultation with a third independent reviewer (author MO). After removing duplicate articles in EndNote following a validated protocol [ 23 ], articles were screened based on their title and abstract. At this stage, articles were excluded if they were (1) non-English; (2) written for a magazine or other non-peer-reviewed source; (3) book reviews, book chapters, editorials, letters, or opinion papers that did not collect original data; (4) conference abstracts or proceedings; (5) studies assessing companion, therapy, or emotional support animals that were not trained for tasks or work related to a specific disability.

After the initial title and abstract review, articles were screened based on full text. Exclusion criteria were then used to select articles based on the following (in order): (1) irrelevant to study topic; (2) assessed an excluded study population (psychiatric service dogs, therapy dogs, emotional support dogs, or companion dogs); (3) did not report quantitative outcomes from assistance dog placement (literature reviews, instrument development, not original research); (4) reported unrelated outcomes (puppy raising, service dog training, or animal-related outcomes); (5) reported only non-psychosocial outcomes (medical or physical); (6) methodological exclusions (qualitative, case studies, single-subject design); (7) no full text available.

Data extraction

Articles were extracted for information based on three aims to describe study characteristics, assess methodological rigor, and summarize outcomes. To describe study characteristics, extracted items included participant characteristics (sample size, age, gender, country of origin), assistance dog characteristics (type and provider), and details of the study (design, measurement time points, comparison conditions). To assess methodological rigor, a total of 15 extracted items were sourced from methodological assessment tools including the National Institutes of Health (NIH) Study Quality Assessment Tools [ 24 ], the Consolidated Standards of Reporting Trials (CONSORT) checklist [ 25 ], the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) checklists [ 26 ], and the Specialist Unit for Review Evidence (SURE) Checklists [ 27 ]. Authors JG and KR independently coded 20% of the included articles to establish adequate inter-rater reliability (alpha = 0.822). Author KR then coded 100% of articles. To examine the relationship between methodological rigor score and year of publication as well as sample size, bivariate correlations were performed. To compare methodological rigor by study design, an independent t-test was used to compare mean scores across longitudinal and cross-sectional designs.

To summarize study outcomes, extracted items included statistical comparisons for any psychosocial outcomes from included studies. Because of the broad inclusion criteria, the 27 studies were widely varied in terms of human and dog participants, assessment time points, statistical analyses, and standardized outcomes. Therefore, due to observed heterogeneity, a meta-analysis was not pursued. We also planned to extract or manually calculate effect sizes to create funnel plots to investigate potential publication biases. However, due to large heterogeneity and poor reporting of effect sizes and raw data, a narrative synthesis of findings in comparison to unpublished theses and published articles was pursued instead.

A total of 1,830 records were screened via title and abstract in which 1,576 records were excluded due to irrelevancy (see Fig 1 for PRISMA diagram). A total of 254 records were screened via full text, of which 230 were excluded. Exclusions included those based on population, outcomes, and methodology. The final sample included 24 articles (12 peer-reviewed publications, 12 unpublished theses/dissertations) containing 27 individual studies. Articles were published from 1994–2018 with publication dates in the 1990s (5), 2000s (9), and 2010s (10) indicating an increasing publication rate on this topic over time.

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Study characteristics

To achieve the first aim of the review–to describe study characteristics–we extracted several features of from each study and article ( Table 1 ).

https://doi.org/10.1371/journal.pone.0243302.t001

Study designs.

Of 27 studies, 15 were cross-sectional and 12 were longitudinal. Studies compared outcomes of individuals with an assistance dog to before they received the dog (six longitudinal studies), to participants on the waitlist to receive an assistance dog (five longitudinal and seven cross-sectional studies), or to participants without an assistance dog (eight cross-sectional studies). Longitudinal assessment time points were varied. Most longitudinal studies (8/12) assessed participants at two time points: at baseline prior to receiving an assistance dog, and an average of 5.8 +/- 3.3 months after participants received an assistance dog (range of 3–12 months follow-up). The remaining four longitudinal studies assessed participants 3–5 times with final follow-up ranging from 9–24 months after receiving an assistance dog.

Study participants.

Most studies (15/27; 56%) were conducted in the United States, followed by the United Kingdom (6/27; 22%). Other countries where studies took place included Canada (3), Japan (2), New Zealand (1), and Sweden (1). A majority of studies (18/27; 67%) assessed outcomes from mobility service dogs for individuals with physical disabilities. These 18 studies recruited study populations with a range of physical impairments including para- or quadriplegia, musculoskeletal disorders, and neuromuscular disorders. Other studies assessed outcomes from hearing dogs (7/27; 26%), guide dogs (4/27; 15%), and medical alert/response service dogs (2/27; 7%). Human participants in these studies included those with hearing or visual impairments, diabetes, and seizure disorders. Most studies (24/27; 89%) assessed outcomes from a single type of assistance dog (e.g. mobility or guide), thus restricting human participants to a single category of impairments. However, three studies collapsed analyses across several types of assistance dogs and impairments. Most studies (17/27; 63%) recruited from a single assistance dog provider organization, while the remaining studies recruited from a range of providers (7/27; 26%) or did not report the source of the assistance dogs in the study (3/27; 11%). The most common provider organizations represented were Canine Companions for Independence (CCI; six mobility service dog studies), Paws with a Cause (four mobility service dog studies), and Hearing Dogs for Deaf People (HDDP; four hearing dog studies).

Samples sizes ranged from 10 to 316 participants with an average sample size across all studies of N = 83 +/- 74 participants and a median sample size of N = 53. Seven studies (26%) had sample sizes less than or equal to N = 20, all of which were longitudinal. However, more than half of all studies (16/27; 59%) had sample sizes greater than or equal to N = 50. Cross-sectional studies had the highest sample sizes with an average sample size of N = 126 +/- 73 participants (range of N = 38–316), while longitudinal studies averaged N = 29 +/- 18 participants (range of N = 10–55). Only a single study [ 16 ] assessed outcomes from child participants under the age of 18 (an additional study [ 38 ] had a minimum inclusion age of 16, but the youngest participant was 19). Average age across all studies was 42 +/- 13 years old. Samples ranged from 15% male to 85% male, with an average of 42% male participants across all studies.

Study methodologies

To achieve the second aim of the review–to evaluate the methodological rigor of studies–each study was assessed if they met a set of 15 methodological rating items using a scale of yes, no, or N/A ( Table 2 ). Fig 2 displays the total scores across each of the 15 items, separated by introduction, methods, results, and discussion sections (see S2 Table for individual study scores). Overall, studies addressed an average of 62% of methodological consideration items with a range of 23% (3/13) to 100% (15/15; denominators were variable as there were two items not applicable to all study designs). Longitudinal studies addressed an average of 59% of methodological items while cross-sectional studies averaged 65%. However, methodological rigor did not significantly differ by study design ( t (25) = -0.940, p = 0.356). Methodological rigor also did not significantly correlate with year of publication ( r = 0.327, p = 0.096) nor total sample size ( r = 0.258, p = 0.194).

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In introduction sections, all studies described an objective, but only 17/27 (63%) of studies stated a directional hypothesis. In methods sections, only 16/27 (59%) of studies indicated whether ethical approval for conducting human subjects research was sought and received. Most studies reported adequate detail on participant demographics such as age and sex or gender identity (23/27; 85%) as well as disability characteristics such as primary diagnoses or severity (22/27; 81%). However, inclusion and exclusion criteria were less commonly described (17/27; 63%). Only 5/27 studies (19%) described dogs’ breeds and sources. Finally, most studies (21/27;78%) compared outcomes to a control or comparison condition.

In results sections, 15/21 studies with a control or comparison condition (71%) demonstrated that participants in each condition were comparable on demographic variables. This occurred by either matching groups on select criteria or statistically comparing groups’ demographic characteristics before performing main analyses. When reporting statistical results, 78% of studies (21/27) provided estimates of variability for outcomes, including confidence intervals, standard deviations, or standard error of the mean. However, only 44% (12/27) of studies reported statistical values (e.g. t , F , or B values) and only 55% (15/27) of studies reported exact probability values from analyses. Only 6/27 (22%) reported any estimates of effect size in their results. Of 15 cross-sectional studies that surveyed individuals who owned assistance dogs for variable periods of time, 4/15 studies (27%) considered length of time of assistance dog ownership as a potential explanatory or moderating variable in analyses. Finally, in discussion sections, most studies (22/27; 81%) stated at least two limitations of their study.

Study outcomes

To achieve the third aim of the review–to summarize outcomes–psychosocial outcomes within each study were extracted. Studies made an average of 5.4 statistical comparisons on psychosocial outcomes, ranging from 1–15 comparisons. In total, 147 comparisons were made across the 27 studies that examined the effect of having an assistance dog on a standardized scale or sub-scale on a psychosocial outcome: 58 (39%) psychological outcomes, 43 (29%) social outcomes, 34 (23%) quality of life outcomes, and 12 (8%) energy/vitality outcomes. Of 147 comparisons, 44 (30%) were positive (improved or better functioning in comparison to pre- or control conditions), 100 (68%) were null (no observed difference), and 3 (2%) were negative (decreased or worse functioning in comparison to pre- or control conditions). Of the 44 positive comparisons, 36 (82%) were from published papers and 8 (18%) were from unpublished theses. Of the 100 null comparisons, 43 (43%) were from published papers and 57 (57%) were from unpublished theses.

Psychological outcomes.

Table 3 summarizes psychological outcomes across studies in terms of general psychological health, emotional health, mental health, and self-evaluation. Of 27 studies, 20 (74%) assessed a psychological outcome with a total of 24 different standardized measures. Of 58 total psychological outcomes, 21 (37%) were positive (improved or better psychological health in comparison to pre- or control conditions), 37 (63%) were null (no difference), and zero (0%) were negative (decreased or worse functioning in comparison to pre- or control conditions).

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For general psychological health, 5/11 (45%) outcomes were significant across group or condition. Six studies used standardized measures to assess general health and health symptoms, three of which [ 17 , 28 , 35 ] reported null findings on the general health domain of the RAND 36-Item Short Form Health Survey [SF-36; 47 ]. However, Lundqvist et al. [ 35 ] found increased SF-36 health transition scores after 3-months of having a mobility, hearing, or medical service dog, while Guest [ 13 ] found an increase in general health 3-months after receiving a hearing dog using the 30-item General Health Questionnaire [GHQ-30; 48 ]. Three studies found positive findings on measures of overall psychological wellbeing or psychosocial health, including increased psychological wellbeing 3-months after receiving a mobility, hearing, or medical service dog [ 35 ], 6-months after receiving a mobility service dog [ 14 ], and better overall psychosocial health in those with a mobility or medical service dog compared to a control group [ 16 ]. On the other hand, Spence [ 34 ] found no improvement to a composite score of psychological health 12-months after receiving a mobility service dog.

Regarding emotional health, 7/15 (46%) outcomes were significant across group or condition. Yarmolkevich [ 46 ] found a significant effect of having a guide dog on positive affect using the Scale of Positive and Negative Experience [SPANE; 49 ] compared to a control group, while others studies found no effect of having a hearing dog [ 29 ] or mobility service dog [ 39 ] on affect via the Positive and Negative Affect Scale [PANAS; 50 ]. Guest [ 13 ] used the Profile of Mood States Scale [POMS; 51 ], finding less overall mood disturbance, less tension, and less confusion 3-months after hearing dog placement. In terms of emotional functioning, two studies found positive results using the SF-36 role emotional domain; Lundqvist et al. [ 35 ] found increased functioning 3-months after receiving a mobility, hearing, or medical service dog, while Shintani et al. [ 17 ] found better functioning among those with a mobility service dog compared to a control group. On the other hand, Donovan [ 28 ] found no change in emotional functioning 4-months after receiving mobility service dog. Using a different measure of emotional functioning, Rodriguez et al. [ 16 ] found higher emotional functioning in those with a mobility or medical service dog compared to a control group.

A total of 13 mental health outcomes were assessed in which 4 (31%) were significant across group or condition. Of 5 studies that used the mental health domain of the SF-36 or the shorter 12-Item Short Form Health Survey (SF-12), only Shintani et al. [ 17 ] found an effect of having an assistance dog on mental health. The other four studies reported no changes in participants’ mental health 3-months after receiving a mobility, hearing, or medical service dog [ 35 ], 4-months after receiving a mobility service dog [ 28 ], and 7-months after receiving a hearing or mobility service dog [ 32 ]. Six comparisons were made to measure the effect of having an assistance dog on clinical measures of depression or anxiety. However, none of the four studies using the Center for Epidemiologic Studies Depression Scale [CES-D; 52 ] found significant differences in self-reported depression among those with a mobility service dog compared to a control group [ 39 – 41 ] or after 4-months with a mobility service dog [ 28 ]. However, Guest et al. found significantly lower depression and anxiety using the POMS and GHQ-30, respectively, 6-months after receiving a hearing dog [ 13 ].

In the self-evaluation subcategory, 5/19 (26%) outcomes found a significant effect of having an assistance dog on standardized measures of self-esteem, self-concept, and other measures of self-evaluation. Nine studies assessed self-esteem as a primary outcome, with four studies [ 14 , 32 , 36 , 46 ] finding a significant effect of having a guide, hearing, mobility, or medical service dog on self-esteem as measured by the Rosenberg Self Esteem Scale [RSES; 53 ]. However, other studies reported no relationship between having a mobility service dog and self-esteem via the RSES [ 39 , 41 ] or other standardized measures of self-esteem [ 15 , 28 , 36 ]. Using the Psychosocial Impact of Assistive Devices Scale [PIADS; 54 ], Vincent et al. [ 15 ] found no difference in self-esteem, adequacy, or competency over 12-months following receiving a mobility service dog. Other self-evaluation outcomes assessed with null findings included no differences in self-concept between control groups and those with mobility service dogs [ 37 ] or guide dogs [ 46 ], no differences in attitude towards a disability 4-months after receiving a mobility service dog [ 28 ] or among guide dog users compared to a control group [ 38 ], and no differences in flourishing among guide dog users compared to a control group [ 46 ]. The only other positive outcome was from Allen et al. [ 14 ] which found significantly higher internal locus of control 6-months after receiving a mobility service dog.

Social outcomes.

Table 4 summarizes the social outcomes across studies within the sub-categories of general social functioning, loneliness, and social participation. Of 27 studies, 18 (67%) reported outcomes a standardized measure of social health with a total of 18 different standardized measures. Of 43 total social outcome comparisons, 7 (16%) were positive (improved or better social health in comparison to pre- or control conditions), 36 (84%) were null (no difference) and zero (0%) were negative (decreased or worse social health in comparison to pre- or control conditions).

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In terms of general social functioning, 2/10 comparisons made were significant. Three studies using SF-36 failed to find significant effects on the social domain; Lundqvist et al. [ 35 ] found no improvement 3-months after receiving a mobility, hearing, or medical service dog, Donovan [ 28 ] found no improvement 4-months after receiving a mobility service dog, and Shintani et al. [ 17 ] found no difference among mobility service dog users compared to controls. However, on different measures of social functioning Rodriguez et al. found better social functioning in those with a mobility or medical service dog compared to a control group [ 16 ] while Guest found improved social functioning 3- and 12-months after receiving a hearing dog [ 13 ]. In addition, null findings were reported on standardized measures of family role 3-, 6-, and 12-months after receiving a mobility service dog [ 15 ], discrimination and social inclusion 12-months after receiving a mobility service dog [ 34 ], and family and social self-concept among mobility dog users compared to a control group [ 37 ].

The sub-category of loneliness had 19 comparisons in which only 1/19 (5%) was significant. Of five studies using a version of the UCLA Loneliness Scale [ 55 ] only Yarmolkevich [ 46 ] found significantly lower self-reported loneliness in those with a guide dog compared to a control group. Four studies found no effect of having a hearing dog [ 29 ] or mobility service dog [ 39 , 41 ] on the UCLA Loneliness Scale. Two studies from the a single thesis [ 29 ] made the remaining 14 comparisons on measures of loneliness distress and complementary loneliness, finding no significant changes to loneliness six months after receiving a hearing dog and no significant group differences in loneliness compared to those without a hearing dog.

Regarding social participation, 14 comparisons were made in which 4/14 were significant (29%). Two studies found increased social participation 3-, 6-, and 12-months [ 15 ] as well as 7-months [ 33 ] after receiving a mobility service dog, while Donovan [ 28 ] found no change in social participation 4-months receiving a mobility service dog. Other studies found increased social connectedness 3-months after receiving a mobility or hearing dog [ 31 ] and increased community integration 6, 12, 18, and 24 months after receiving a mobility service dog [ 14 ]. Using the CHART, both Milan [ 41 ] and Davis [ 44 ] found no group differences in social integration among those with a mobility service dog control groups. Other null findings included no effect of having a guide dog on social conflict stress and interactions with others [ 42 ], no improvement in social relationships 12-months after receiving a mobility service dog, and null findings regarding self-reported friendship and companionship with a mobility or medical service dog [ 16 ] or 4-months after receiving a mobility service dog [ 28 ].

Quality of life outcomes.

Table 5 displays all quality of life outcomes across studies within the sub-categories of overall quality of life, life satisfaction, and independence. Of 27 studies, 19 (70%) reported outcomes a quality of life measure with a total of 13 different standardized measures used. Of 34 total quality of life outcomes, 9 (26%) were positive (improved or better quality of life in comparison to pre- or control conditions), 22 (65%) were null (no difference) and 3 (9%) were negative (decreased or worse quality of life in comparison to pre- or control conditions).

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In the overall quality of life sub-category, 2/8 (25%) comparisons were significant. Lundqvist et al. [ 35 ] found higher health-related quality of life 3-months after receiving a mobility, hearing, or medical service dog on one of three measures used [EuroQol Visual Analog Scale; 56 ]. Hall et al. [ 45 ] found higher health-related quality of life among those with a mobility service dog compared to a control group, but not among those with a hearing dog. Other studies found no effect of having a mobility service dog on quality of life including more specific measures such as physical and environmental quality of life [ 33 , 34 ].

In the next sub-category, six studies assessed life satisfaction outcomes using Satisfaction with Life Scale [SWLS; 57 ]. However, only 1/6 (17%) found a significant effect, in which Yarmolkevich found higher life satisfaction among those with a guide dog compared to a control group. The other five studies found no effect of having a mobility service dog [ 32 ], hearing dog [ 29 , 32 ], or guide dog [ 38 ] on life satisfaction using SWLS.

In the sub-category of independence, a total of 20 comparisons were made in which 9 (45%) were significant, but 3 (15%) were in the negative direction. The most commonly used measure was the Craig Handicap Assessment and Reporting Technique [CHART; 58 ] which assesses how people with disabilities function as active members of their communities. Using the occupation domain of the CHART, Rintala et al. [ 32 ] found no difference in occupational functioning 7-months after receiving a mobility service dog and Milan [ 41 ] found no group difference in those with and without a mobility service dog. However, 2 studies found worse occupational functioning in terms of employment, schooling, or homemaking. Rintala et al. [ 32 ] found that participants reported worse occupational functioning 7-months after receiving a hearing dog while Davis [ 44 ] found that individuals with a mobility service dog reported worse occupational functioning compared to a control group.

In the economic domain of the CHART, which assesses socio-economic independence, Davis [ 44 ] again found that those with a mobility service dog reported worse economic functioning than controls while two mobility dog studies reported null findings [ 30 , 41 ]. In the mobility domain, only Milan [ 41 ] found a significant effect of having a mobility service dog on the CHART mobility domain (which includes hours per day out of bed and days per week out of the house) while Davis [ 44 ] and Rintala et al. [ 32 ] reported no relationship between the mobility domain and having a service dog or hearing dog. Using other standardized measures of independence, Matsunaka & Koda [ 42 ] found that those with guide dogs reported and lower stress while being mobile. Similarly, Crudden et al. [ 43 ] found that individuals who had guide dogs reported less stress while walking, but not while using public transportation. Using the Reintegration to Normal Living Index [RNLI; 59 ], Hubert found improvements in the ability to return to ‘normal life’ after 7-months with a mobility service dog while Vincent et al. [ 15 ] found improvements to daily work activities 3- and 12-months after receiving mobility service dog (but not in self-care or dealing with life events). Finally, Rodriguez et al. [ 16 ] found that those with a mobility or medical service dog reported significantly higher work/school functioning than a control group.

Vitality outcomes.

Table 6 summarizes vitality outcomes across studies within the sub-categories of general energy/vitality and sleep. Of 27 studies, 7 (26%) reported outcomes from at least one standardized measure of vitality with a total of five different standardized measures. Of 12 total vitality comparisons, 6 (50%) were positive (improved or better vitality in comparison to pre- or control conditions), 6 (50%) were null (no difference) and zero (0%) were negative (decreased or worse vitality in comparison to pre- or control conditions).

https://doi.org/10.1371/journal.pone.0243302.t006

In terms of general vitality and energy, four studies used the SF-36 to measure the effect of having an assistance dog on the vitality domain. Only Vincent et al. [ 15 ] found a significant increase in pep, energy, and feeling less worn out 3- and 6-months after receiving a mobility service dog while three studies found no relationship between the vitality domain and having a mobility service dog [ 17 , 28 ] or a mobility, hearing, or medical service dog [ 35 ]. Using the Profile of Mood States Scale [POMS; 51 ], Guest found increased self-reported vigor 3- and 12-months after receiving a hearing dog and less fatigue 3-months after receiving a hearing dog. Using another measure of energy and fatigue, Craft [ 40 ] found no difference in those with or without a mobility service dog. Regarding sleep, Guest found better self-reported sleep quality 3- and 12-months after receiving a hearing dog while Rodriguez et al. [ 16 ] found no difference in sleep disturbance between individuals with mobility or medical service dog and a control group.

This systematic review summarized the current state of knowledge regarding the effects of owning an assistance dog (including service, guide, hearing, and/or medical alert or response dogs) on standardized outcomes of psychosocial health and wellbeing of individuals with disabilities. Our search procedure identified 24 articles containing 27 studies assessing psychosocial outcomes from a wide variety of human and assistance dog populations. These studies were reviewed to complete three specific aims: to describe the key characteristics of studies, to evaluate the methodological rigor of studies, and to summarize outcomes. The discussion section aims to review the findings from each aim and to provide targeted suggestions for future research.

Our first aim was to describe study characteristics of the literature. We found that most studies were conducted in either the United States or the United Kingdom, but there was international representation of the research in Canada, Sweden, New Zealand, and Japan. Most articles were published in the 2010s, indicating an increasing publication interest in this topic over time. In fact, nine new articles were identified (three theses, six publications) that had been published since the last review on this topic in 2012 [ 9 ]. Increased research on this topic is likely in parallel with the increased roles and demands for different types of assistance dogs worldwide [ 2 ] as well as increased interest in the benefits of animal interaction for human health and wellbeing [ 60 ]. The most commonly studied type of assistance dog was mobility service dogs, followed by hearing dogs. Guide dogs were only assessed in four studies (all of which were cross-sectional, and one of which was an unpublished thesis [ 46 ]). The lack of guide dog-specific research is especially surprising given that guide dogs not only have the longest history of any type of assistance dog [ 61 ] but are also the most commonly placed assistance dog placed by professional facilities worldwide [ 2 ]. Future longitudinal research in this population is necessary to understand the complex psychosocial and physical roles that guide dogs play in the lives of their handlers. Medical service dogs for diabetes and seizure alert/response were rarely studied [ 16 , 35 ], and were assessed in conjunction with mobility service dogs rather than on their own. However, these are relatively new categories of assistance dogs [ 2 ], many of which may also be self-trained [ 62 ], and it appears that emerging research on this population has centered on medical benefits [ 63 ] rather than psychosocial. Future research should focus on assessing outcomes from these medical alert and response assistance dogs and how their roles may be similar or different than mobility, guide, or hearing dogs.

Study designs included both cross-sectional and longitudinal studies, with only one randomized longitudinal study identified [ 14 ]. However, it should be noted that this study by Allen & Blascovich has received considerable critique due to incredibly large effect sizes, unrealistic retention and response rates, and severe methodological omissions including a lack of reporting on recruitment, funding, or where assistance dogs were sourced and trained [despite repeated requests for clarification; 64 , 65 ]. The remaining studies were quasi-experimental in that they did not use randomized assignment to treatment or control groups. Therefore, the current literature is limited to correlational, rather than causal conclusions regarding the benefits of assistance dogs on the psychosocial health of their owners. Overall, sample sizes were higher than what is usually observed in targeted animal-assisted intervention studies with dogs (e.g. [ 66 , 67 ]) but smaller than that of pet dog research [ 68 ]. Interestingly, only one included study [ 16 ] assessed outcomes from participants under the age of 18. Although outcomes from assistance dog placement for children and adolescents have been quantified with qualitative [e.g., 69 – 71 ] and observational [e.g., 72 ] study designs, effects on standardized measures of psychosocial wellbeing including social functioning have not been explored. Therefore, future studies are warranted that specifically assess health and wellbeing using validated parent-proxy or self-report measures to fully understand the potential effects that assistance dogs can have on children and adolescents with disabilities.

Methodological rigor

Our second aim was to evaluate the methodological rigor of studies. We found that similar to the range of study characteristics observed, there was considerable variation in the methodological rigor of included studies. The most notable weaknesses included a lack of adequate reporting in the methodological sections, which not only limits interpretation of findings but prevents reproducibility. First, only 59% of studies stated whether ethical approval for human subjects was sought and received. Future research should specify not only ethical protocols for human subjects research, but also for animal subjects, which is often underutilized and/or underreported in AAI research [ 73 ]. Second, only 63% of studies described inclusion and/or exclusion criteria of recruited participants, and some studies did not report all demographic or disability characteristics of participants. Future studies should provide detailed researcher-specified criteria for participation as well as organizational-specified criteria for placing/receiving an assistance dog, if applicable. For example, organizations that place assistance dogs may have housing, familial, physical, or even financial requirements for potential recipients that should be subsequently reported in the manuscript to fully define the population. It is unreasonable to assume that the changes to an individual’s life following receipt of an assistance dog is identical for all ages, gender identities, backgrounds, and disabilities. Therefore, detailed descriptions of study populations is critical for helping the field understand for whom assistance dogs are beneficial regarding social, emotional, or psychological health and under what contexts or conditions [ 74 ].

Finally, one of the most notable examples of poor methodological reporting across studies was the omission of information regarding assistance dogs’ sources (e.g. purpose-bred from a provider, self-trained) and breeds (e.g., Labrador Retriever, Golden Retriever, Mixes). As the assistance dog itself is the key component of the intervention, details regarding the dog’s breeding, rearing, selection, and training, as well as the assistance dog-handler matching process are critical to disentangling potential mechanisms [ 75 ]. In addition, reporting detailed information on assistance dogs allows for the consideration of the dogs as individual agents in the therapeutic process rather than as uniform tools [ 1 , 74 ].

In addition to poor methodological reporting, many studies were restrained by statistical weaknesses. Many studies did not confirm that participants across groups were statistically equivalent on key demographic variables such as age and sex/gender before conducting statistical analyses. This poses a severe threat to the validity of findings as group differences in outcomes could be caused by underlying differences in certain demographics or characteristics and cannot be confidently attributed to the presence of the assistance dog. Secondly, many studies did not report sufficient detail in results in terms of estimates of variability and effect size. Thorough reporting in terms of the magnitude and variability of effects observed will allow researchers to make informed comparisons across populations and interventions and conduct critically needed meta-analyses in the field.

The third aim of the review was to summarize psychosocial outcomes of studies. We found that studies reported mostly psychological outcomes (74%), followed by social outcomes (67%), quality of life outcomes (70%), and vitality (26%) outcomes. Overall, most (68%) of comparisons made across studies were null in which no statistical difference was found in the outcome compared to before getting an assistance dog or compared to a control group. Importantly, only a few comparisons were made in the negative direction (2%) indicating that there is limited reason to believe that acquiring an assistance dog is associated with worse functioning. A total of 30% of comparisons made were positive in which having an assistance dog was associated with improved psychosocial functioning among individuals with disabilities. In fact, positive findings were identified in all domains and sub-domains of psychosocial health and wellbeing. Promising areas include psychological wellbeing, emotional wellbeing, and social participation in which several positive outcomes were identified. However, almost all positive findings were accompanied by a null finding using the same or similar standardized measure in a different study. The below discussion considers various potential explanations for the inconsistencies in findings across studies.

Variability in assessment times.

One of the main considerations in understanding the potential variability across findings is the aspect of time since assistance dog placement. In longitudinal studies, the first follow-up time point varied from 3- to 12-months after receiving an assistance dog. Within cross-sectional studies, number of years since first partnering with an assistance dog ranged from 6-months to 45 years with means ranging from 2–9 years. This variation in assessment times makes it difficult to draw definitive conclusions on conflicting findings. Further, the number of years spent with the assistance dog at the time of surveying was unknown for half of the cross-sectional studies [ 29 , 37 , 40 , 42 – 45 ]. Therefore, in the cases where positive outcomes were reported in these studies, it is unknown what amount of time with an assistance dog the finding was associated with (and therefore difficult to compare to findings from other studies).

Variability in interventions.

Another potential explanation for inconsistent findings across studies lies in the inherent variability of the assistance dog intervention itself. Assistance dog categories (guide, hearing, mobility, and medical) were collapsed for the purposes of this review, but undoubtedly contribute to the lives of individuals with disabilities in diverse ways. However, even within a single category, there are differences in assistance dog breeds, temperaments, and training that may significantly contribute to observed variance across studies. Second, there is inherent variation in both the quality and quantity of interactions from one assistance dog-owner pair to the next. In addition to the different human and dog phenotypes that contribute to this heterogeneity, there are likely differences in the strength of the human-animal bond and attachment relationships formed between assistance dogs and handlers [ 19 , 76 ]. Moderator analyses will be useful in determining the potential explanatory effects that handler-service dog relationships have on psychosocial outcomes.

Variability in standardized measures.

Another potential reason for the inconsistencies in findings from studies assessing the same construct is disparities across standardized measures. Measures of the same outcome not only can have different wording and items, but also can measure functioning over different time periods or contexts. In one example, four studies included in this review failed to find significant results in comparisons of depression using the CES-D [ 28 , 39 – 41 ]. However, positive findings were found in depression using the POMS by a different study [ 13 ]. The CES-D asks participants to rate how often they had experienced 20 depressive symptoms in the prior week using statements such as “I thought my life had been a failure,” while the POMS asks participants to rate from not at all to extremely how they feel right now using single words such as “sad” and “unhappy.” It is also possible that some standardized measures do not capture the intended effects from having an assistance dog. One author argued that an “important methodological issue is the absence of appropriate measures” in measuring the effect of an assistance dog on recipients’ lives [ 32 ]. Future research is necessary to determine if in fact some measures are inappropriate to measure change following an assistance dog, which may be addressed using interviewing and focus group techniques among assistance dog handlers. The replicated measures identified in this review can serve as a basis for future researchers to collate the existing literature when making assessment choices.

Variability in study rigor.

A final potential reason for outcome discrepancies is variation in methodological rigor across studies. In particular, not only did studies vary largely in terms of sample size, but they also varied in the manner in which statistical analyses were conducted. As mentioned above, a surprisingly high number of studies did not ensure that assistance dog and control groups were statistically equal across demographic and disability characteristics prior to outcome analyses. In these studies, positive findings (i.e., better social functioning in those with an assistance dog compared to a control group) may be partially attributed to an unmeasured variable driving the group difference [ 77 ]. In addition, many studies did not account for confounding variables such as having a pet dog, the progressiveness or type of disability, or relationship status.

Other considerations.

An important finding from this review was that most positive findings were reported in published studies, while unpublished theses were more likely to report null findings. This pattern suggests a potential publication bias present in which disproportionately more positive findings are in the published studies than the unpublished theses [ 78 ]. Importantly, unpublished theses had a similar average sample size as published studies, with similar power to detect effects compared to published studies. Thus, this pattern may be better explained by the “file drawer effect” in which there is a bias towards publishing positive findings over null findings [ 79 ]. Although this tendency occurs in many fields, the file-drawer bias may especially be prevalent in human-animal interaction research due to the preconceived notion that animals are beneficial for humans [ 80 ]. In fact, positive, null, and negative findings are equally instrumental in understanding the complexities of the role that assistance dogs play in the lives of individuals with physical disabilities. As Serpell and colleagues point out, individuals that don’t benefit from animal-assisted interventions may be just as informative from a scientific perspective as the ones that do, and “the entire field potentially suffers when these sorts of contrary or ambiguous findings get buried or ignored” [ 74 ]. Therefore, future efforts should be made to publish null findings in peer-reviewed journals and to encourage scientific transparency [ 80 ].

As a final consideration, it is possible that assistance dogs may not confer significant psychosocial benefits as quantified by some of the standardized measures used. First, there may be ceiling effects present whereby individuals are functioning at initially healthy levels of the measured construct (e.g., depression, self-esteem) prior to receiving an assistance dog and thus may not significantly improve on these measures. This effect may be compounded by the possibility that those who apply for an assistance dog may inherently have certain positive characteristics (e.g., stable housing, stable finances, has a familial support system) that contribute to overall psychosocial health. Further, in contrast to a psychiatric service dog or an emotional support dog, the assistance dogs in this review are not explicitly trained for mental health-related support and their effects on the psychosocial health of their handlers may be variable rather than population-wide. For example, the benefits of an assistance dog for a socially isolated individual who experiences periodic anxiety and depression may be significantly different than an individual without these characteristics. An important question for the field moving forward will be to determine for whom an assistance dog may confer the most significant psychosocial health benefits for, and under what contexts or conditions.

Conclusions

This systematic review identified 24 articles containing 27 studies that assessed a psychosocial outcome of having an assistance dog (guide dog, hearing dog, mobility service dog, or medical service dog). Included studies assessed psychosocial outcomes via standardized measures from assistance dogs that were trained for functional tasks related to a physical disability or medical condition (omitting psychiatric service dogs or emotional support dogs). Despite the purpose of these assistance dogs specifically for physical tasks, positive outcomes were noted in psychological, social, quality of life, and vitality domains. However, results suggested that for most outcomes, having an assistance dog had no effect on psychosocial health and wellbeing. Methodological weaknesses including poor reporting of assistance dog interventions and statistical limitations prevent any clear conclusions made regarding the psychosocial effects of assistance dogs on individuals with disabilities. Inconsistencies in findings were discussed in terms of wide variability in assessment times, interventions, measures, and rigor, and recommendations were made to contribute to the knowledge of this growing application of the human-animal bond. Continued efforts are required to improve methodological rigor, conduct replicable research, and account for heterogeneity in both humans and animals to advance the state of knowledge in this field.

Supporting information

S1 checklist. prisma 2009 checklist..

https://doi.org/10.1371/journal.pone.0243302.s001

S1 Table. MEDLINE search terms and search strategy.

The search strategy was adapted to the other databases, including mapping terms to each database’s thesaurus or prescribed vocabulary, as appropriate.

https://doi.org/10.1371/journal.pone.0243302.s002

S2 Table. Summary of methodological rating scores by each of the N = 27 individual studies.

Studies are organized by design (longitudinal or cross-sectional).

https://doi.org/10.1371/journal.pone.0243302.s003

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• Published: 14 October 2020

Unravelling the health status of brachycephalic dogs in the UK using multivariable analysis

• D. G. O’Neill 1 ,
• C. Pegram 1 ,
• P. Crocker 1 ,
• D. C. Brodbelt 1 ,
• D. B. Church 2 &
• R. M. A. Packer 2  

Scientific Reports volume  10 , Article number:  17251 ( 2020 ) Cite this article

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Brachycephalic dog breeds are regularly asserted as being less healthy than non-brachycephalic breeds. Using primary-care veterinary clinical data, this study aimed to identify predispositions and protections in brachycephalic dogs and explore differing inferences between univariable and multivariable results. All disorders during 2016 were extracted from a random sample of 22,333 dogs within the VetCompass Programme from a sampling frame of 955,554 dogs under UK veterinary care in 2016. Univariable and multivariable binary logistic regression modelling explored brachycephaly as a risk factor for each of a series of common disorders. Brachycephalic dogs were younger, lighter and less likely to be neutered than mesocephalic, dolichocephalic and crossbred dogs. Brachycephalic differed to non-brachycephalic types in their odds for 10/30 (33.33%) common disorders. Of these, brachycephalic types were predisposed for eight disorders and were protected for two disorders. Univariable and multivariable analyses generated differing inference for 11/30 (30.67%) disorders. This study provides strong evidence that brachycephalic breeds are generally less healthy than their non-brachycephalic counterparts. Results from studies that report only univariable methods should be treated with extreme caution due to potential confounding effects that have not been accounted for during univariable study design or analysis.

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Introduction.

Issues relating to the health and welfare concerns for brachycephalic dogs have become an increasingly high profile topic in veterinary medicine in the UK 1 , 2 and internationally 3 , 4 over the past decade. Controversy surrounds these much cherished but often debated breeds, with marked rises in their popularity 5 set against a backdrop of increasing evidence of the health compromises associated with their exaggerated body morphology 6 , 7 . Indeed, some veterinarians now consider the health and welfare of several popular brachycephalic breeds too compromised to justify their continued breeding 8 . A growing body of evidence is accumulating to suggest that brachycephalic breeds are strongly predisposed to a range of disorders intrinsically related to their typical conformations, including respiratory disease 9 , 10 , eye disease 11 , 12 , dystocia 13 , 14 , spinal disease 15 , heat stroke and pneumonia 16 . Brachycephalic breeds are also reported with significantly shorter lifespans (median longevity: 8.6 years) than moderate and non-brachycephalic dogs (median 12.7 years) 17 .

To date, a priori exploration of brachycephalic health has often compared brachycephalic and non-brachycephalic dogs for individual disorders selected based on prior belief of a brachycephalic predisposition e.g. upper respiratory tract disease 9 . An alternative approach that encompasses a wider spectrum of disorders has been to report prevalence within key individual brachycephalic breeds such as French Bulldogs, Bulldogs and Pugs but without directly including a comparator group of dogs for reference 18 , 19 , 20 . While both approaches are useful, inference from these approaches is limited to the specific disorder or breed under study, and it is challenging to draw the deeper conclusions across the spread of disorders and breeds that are needed to fully evaluate health associations for brachycephalic dogs. To date, an analysis of pet insurance data in the United States of America is the only study to have directly compared the overall health of brachycephalic versus non-brachycephalic dogs overall across a range of common disorders simultaneously 16 . That insurance study reported higher prevalence in brachycephalic dogs for many health problems. However, these data were derived from an inherently biased subset of the overall population that were insured and formal statistical methods such as multivariable analysis to account for potential confounding variables such as differing age and neutering structures between the groups in the study population were not applied 21 .

In the UK, the brachycephalic population of dogs has some unique demographic features compared with non-brachycephalic dogs. Rapid popularity increases over the past decade for some brachycephalic breeds such as French Bulldog and Pug have led to disproportionate numbers of younger animals representing these breeds 18 , 19 . Age is consistently shown as one of the most important risk factors for disease; young animals show higher rates of infectious disease rates 22 but lower rates of neoplastic (e.g. lymphoma 23 ), musculoskeletal (e.g. elbow joint disease 24 ) and degenerative disease (e.g. osteoarthritis 25 ). As such, univariable analyses of brachycephalic health parameters are likely to be highly confounded by age and therefore it seems sensible to account for potential confounders in analyses of breed health as a general rule 21 .

Much of the previous veterinary literature on breed predispositions reported findings from univariable analyses that compared breed effects without accounting for other differences such as age 7 . It is possible this approach may lead to false positive and false negative findings 26 . Many of the more recent VetCompass studies of canine health have highlighted the complexity underlying disorder risk, with variables such as age, bodyweight, neutering and insurance status commonly associated with disease risk factors in addition to breed effects 14 , 24 , 27 , 28 , 29 . As such, the secondary aim of the study was to compare the consistency of findings between univariable versus multivariable analyses to assist in gaining a deeper understanding of the reliability of univariable analyses for robust inference on factors related to dog health.

The VetCompass Programme that collects anonymised data from primary-care veterinary practices was used to compare overall health between large groups of dogs 30 . VetCompass has previously been applied to report that purebred dogs had higher prevalence than crossbreds for 3/20 of the most-frequently recorded disorders, although these analyses were limited to univariable statistical methods 31 . A similarly holistic approach, but extended to include multivariable methods, could compare health between brachycephalic versus non-brachycephalic dogs to investigate whether brachycephalic dogs are predisposed or protected to common disorders after accounting for other demographic factors. The findings from such an approach would offer further insights into both the challenges, and indeed potential benefits, to health and welfare from being a brachycephalic breed. With this background, using anonymised veterinary clinical data from the VetCompass Programme 30 , the primary aim of the current study was to compare the general demography and prevalence of common disorders between brachycephalic dogs compared with mesocephalic and dolichocephalic types under primary veterinary care in the UK during 2016 and specifically to identify disorders with predisposition and protection in the brachycephalic dogs compared with non-brachycephalic dogs. A secondary aim was to explore differences in the results from univariable compared with multivariable risk factor analyses in order to better understand the value of accounting for confounding in breed health studies. These results could assist welfare scientists, breeders, kennel clubs, veterinary practitioners, owners and other stakeholder with an evidence base on the health of the wider general population of brachycephalic dogs that could assist to predict, prevent and manage key health and welfare opportunities for brachycephalic dog types.

The study included a random sample of 22,333 dogs attending 784 veterinary clinics from an overall population of 955,554 dogs under veterinary care in 2016. The analysis included 22,248/22,333 (99.62%) dogs with breed information available. These dogs included 4,169 (18.74%) brachycephalic, 10,341 (46.48%) mesocephalic, 1,744 (7.84%) dolichocephalic and 5,994 (26.94%) crossbred types. At a more summarised level, there were 4,169 (18.74%) brachycephalic and 18,079 (81.26%) non-brachycephalic types (Table 1 ).

The median age of brachycephalic dog types was 3.31 years (IQR 1.40–6.24, range 0.15–19.54). Brachycephalic dog types were younger than mesocephalic types (median 5.33 years, IQR 2.33–8.98, range 0.01–20.46) ( P  < 0.001), dolichocephalic types (5.07 years, IQR 2.23–8.49, range 0.20–18.33) ( P  < 0.001) and crossbred types (3.74 years, IQR 1.68–7.34, range 0.01–19.49) ( P  < 0.001). The median adult bodyweight of brachycephalic dog types was 8.75 kg (IQR 6.29–12.18, range 1.52–80.63). Brachycephalic dog types were lighter than mesocephalic types (median 16.98 kg, IQR 8.93–25.95, range 1.41–83.70) ( P  < 0.001), dolichocephalic types (25.80 kg, IQR 10.30–33.78, range 2.20–76.77) ( P  < 0.001) and crossbred types (13.80 kg, IQR 8.43–23.34, range 2.10–85.00) ( P  < 0.001). There was no overall association between sex and the skull conformation group ( P  = 0.069). Pairwise proportional neutering was lower in brachycephalic types (number neutered 1,526, 36.70%) than mesocephalic types (4,756, 46.13%) ( P  < 0.001), dolichocephalic types (807, 46.43%) ( P  < 0.001) and crossbred types (2,985, 49.95%) ( P  < 0.001). Pairwise proportional insurance did not differ between brachycephalic (478, 11.47%) and crossbreds (752, 12.55%) ( P  = 0.101) but insurance was lower for brachycephalic types than for mesocephalic (1,466, 14.18%) ( P  < 0.001) or dolichocephalic types (280, 16.06%) P  < 0.001) (Table 2 ).

The brachycephalic group included 34 individual breeds, the mesocephalic group included 169 individual breeds and the dolichocephalic group included 66 individual breeds (Supplementary A). The most common brachycephalic breeds were Chihuahua (n = 955, 22.91%), Shih-tzu (795, 19.07%) and Cavalier King Charles Spaniel (435, 10.43%). The most common mesocephalic breeds were Labrador Retriever (1462, 14.14%), Staffordshire Bull Terrier (1304, 12.61%) and Jack Russell Terrier (1190, 11.51%). The most common dolichocephalic breeds were German Shepherd Dog (546, 31.31%), Greyhound (149, 8.54%) and Whippet (117, 6.71%). The most common crossbred types were non-designer type crossbreds (4699, 78.4%), Cockapoo (478, 7.97%) and Labradoodle (175, 2.92%). The 15 most common breeds within each skull shape group comprised a greater proportion of the brachycephalic dog types (4,101/4,169, 98.37%) than mesocephalic types (8,654/10,341, 83.69%) ( P  < 0.001) or dolichocephalic types (1,432/1,744, 82.11%) ( P  < 0.001) (Table 2 ).

Precise diagnoses

In the overall study sample, there were 14,704 (65.84%) dogs with at least one disorder during the 12-month interval from January to December 2016. The proportion of dogs with at least one disorder recorded during 2016 for the skull shape conformation were: brachycephalic dog types n = 2,769 (66.42%), mesocephalic types n = 6,868 (66.42%), dolichocephalic types n = 1,160 (66.51%) and crossbred types n = 3,866 (64.50%). Univariable logistic regression modelling showed that brachycephalic (odds ratio [OR] 1.09 (95% confidence interval [CI] 1.00–1.18, P  = 0.045) and mesocephalic (OR 1.09, 95% CI 1.02–1.16, P  = 0.013) types had higher odds of having at least one disorder compared with crossbred types, whereas no difference was identified for dolichocephalic types (OR 1.09, 95% CI 00.98–1.22, P  = 0.120). Multivariable logistic regression modelling (adjusting for adult bodyweight, bodyweight relative to breed/sex mean, age, sex, neuter and insurance) revealed an increased odds of having at least one disorder in brachycephalic types (OR 1.27, 95% confidence interval [CI] 1.13–1.43, P  < 0.001) compared with crossbred types. However, mesocephalic types (OR 0.95, 95% CI 0.87–1.04, P  = 0.285) and dolichocephalic types (OR 0.96, 95% CI 0.83–1.12, P  = 0.625) were not significantly different to crossbreds. The 95% CI for mesocephalic and dolichocephalic dogs did not overlap the 95% CI for brachycephalic dogs, indicating that brachycephalic dogs also had increased odds of having at least one disorder compared with mesocephalic and dolichocephalic dogs.

The median count of disorders in the overall study sample during 2016 was 1 (interquartile range [IQR] 0–2, range 0–17). Univariable Poisson regression modelling showed that brachycephalic (disorder count risk ratio [DCRR] 1.13, 95% CI 1.10–1.17, P  < 0.001), mesocephalic (DCRR 1.13, 95% CI 1.10–1.16, P  < 0.001) and dolichocephalic types (DCRR 1.11. 95% CI 1.06–1.16, P  < 0.001) had higher disorder count risk ratios than crossbred types. Multivariable Poisson regression modelling (adjusting for adult bodyweight, bodyweight relative to breed/sex mean, age, sex, neuter and insurance) showed an increased disorder count risk ratio for brachycephalic types (DCRR 1.24, 95% CI 1.19–1.29, P  < 0.001) and a decreased disorder count risk ratio for mesocephalic types (DCRR 1.04, 95% CI 1.01–1.08, P  = 0.007) compared to crossbreds. Dolichocephalic types (DCRR 1.04. 95% CI 0.99–1.10, P  = 0.124) were no longer significantly different to crossbreds.

The most common precise disorders (i.e. greatest prevalence) in the brachycephalic types were periodontal disease (n = 485, prevalence = 11.63%), otitis externa (303, 7.27%), obesity (266, 6.38%), anal sac impaction (249, 5.97%), overgrown nail(s) (212, 5.09%), diarrhoea (143, 3.43%) and heart murmur (3.43%). There were eight precise disorders with the higher odds in multivariable logistic regression analysis (i.e. disorder predisposition) for brachycephalic types compared with non-brachycephalic types: corneal ulceration (OR 8.40, 95% confidence interval [CI] 5.21–13.56, P  < 0.001), heart murmur (OR 3.52, 95% CI 2.70–4.60, P  < 0.001), umbilical hernia (OR 3.16, 95% CI 1.94–5.18, P  < 0.001), pododermatitis (OR 1.66, 95% CI 1.20–2.28, P  = 0.002), skin cyst (OR 1.52, 95% CI 1.04–2.22, P  = 0.029), patellar luxation (OR 1.40, 95% CI 1.02–1.93, P  = 0.038), otitis externa (OR 1.29, 95% CI 1.10–1.51, P  = 0.002) and anal sac impaction (OR 1.24, 95% CI 1.03–1.50, P  = 0.021). Two precise disorders had reduced odds for brachycephalic types in multivariable analysis: undesirable behaviour (OR 0.52, 95% CI 0.34–0.81, P  = 0.003) and claw injury (OR 0.45, 95% CI 0.29—0.70, P  < 0.001) (Table 3 ).

Based on the multivariable logistic regression analysis results for the individual precise disorders, the odds of ten of the thirty (10/30; 33.33%) disorders differed between brachycephalic and non-brachycephalic types, with 8/10 disorders showing higher odds in brachycephalic types while 2/10 disorders had lower odds in brachycephalic types. Review of the univariable logistic regression analyses identified 17/30 (56.67%) precise disorders with differing odds between brachycephalic and non-brachycephalic types, with 8/17 disorders showing higher odds in brachycephalic types while 9/17 disorders had lower odds in brachycephalic types. Univariable and multivariable analyses generated differing inference on disorder predisposition between brachycephalic and non-brachycephalic types for 11/30 (30.67%) common precise disorders (Table 3 ).

Grouped diagnoses

The most common grouped disorders in the brachycephalic types were dermatological (n = 587, prevalence = 14.08%), dental (583, 13.96%), enteropathy (424, 10.17%), ophthalmological (393, 9.43%) and aural (342, 8.2%). There were six grouped disorders with the higher odds in multivariable logistic regression analysis for brachycephalic types compared with non-brachycephalic types: cardiac (OR 4.06, 95% CI, 3.18–5.18, P  < 0.001), ophthalmologic (OR 1.80, 95% CI 1.53–2.11, P  < 0.001), upper respiratory tract (OR 1.62, 95% CI 1.30–2.03, P  < 0.001), aural (OR 1.33, 95% CI 1.14–1.55, P  < 0.001), dermatologic (OR 1.32, 95% CI 1.16–1.50, P  < 0.001) and anal sac (OR 1.33, 95% CI 1.12–1.58, P  = 0.001). One grouped disorder had reduced odds for brachycephalic types in multivariable analysis: behavioural (OR 0.73, 95% CI 0.59—0.90, P  = 0.004). (Table 4 ).

Based on the multivariable logistic regression analysis results for the individual grouped disorders, the odds of seven of the sixteen (7/16; 43.75%) disorders differed between brachycephalic and non-brachycephalic types, with 6/7 disorders showing higher odds in brachycephalic types while 1/7 disorders had lower odds in brachycephalic types. Review of the univariable logistic regression analyses identified 10/16 (62.50%) grouped disorders with differing odds between brachycephalic and non-brachycephalic types, with 5/10 disorders showing higher odds in brachycephalic types and 5/10 disorders with lower odds in brachycephalic types. Univariable and multivariable analyses generated differing inference on disorder predisposition between brachycephalic and non-brachycephalic types for 5/16 (31.25%) common grouped disorders (Table 4 ).

This study is the first large-scale direct comparison of the health of brachycephalic versus non-brachycephalic dogs using veterinary clinical records. The results provide strong evidence to support the position that brachycephalic dogs have reduced health overall compared with non-brachycephalic dogs based on the current evaluation of the most common conditions observed in dogs attending primary care practices. Brachycephalic dogs had higher odds of having at least one disorder diagnosed compared with mesocephalic, dolichocephalic or crossbred dogs. Among the thirty individual precise disorders, brachycephalic types showed predispositions for 8/30 disorders compared with protections for just 2/30 disorders. At the more general grouped level of disorders, brachycephalic types showed predispositions in 6/16 disorders compared with protection in just 1/16 disorder. This study focused on common problems because these contribute substantially to the overall disease burden and therefore should be considered as priority issues for these breeds 32 . The power of the current study for reliable inference on the relative health status of brachycephalic dogs is strengthened by the relatively large sample size, the breadth of clinical disorders included, access to diagnoses recorded directly by veterinary professionals and the availability of health information on non-brachycephalic dogs for comparison 33 . The majority of previous studies on breed health tended to focus primarily on identification of disorder predispositions but the current study expanded this approach by also aiming to identify disorder protections as a relatively new concept in companion animal epidemiology 7 .

As well as reporting disorder predispositions, the current study also explored disorder occurrence across the types of skull shape at a more general level by comparing the counts of disorders recorded annually in the dogs of each group. Multivariable Poisson regression modelling showed that brachycephalic types had the highest disorder count risk ratio of the four skull shape groups assessed (DCRR 1.24 compared with crossbreds). Although disorder count as a welfare metric does not consider the contribution of disorder severity and duration to the overall welfare impact 32 , 34 , the elevated risk for overall disorder occurrence shown in the current study provides additional support that brachycephalic types in general have reduced health compared to other types.

It is noteworthy that rising popularity and ownership over the past decade of the Pug 20 , French Bulldog 18 and Bulldog 19 in particular has been at the heart of the growing concerns about brachycephalic health issues in dogs 35 , 36 . This phenomenon may give the impression that these breeds dominate the brachycephalic dog population overall. However, in contrast, the current study shows that the most common brachycephalic breeds in 2016 in the UK were the Chihuahua, Shih-tzu and Cavalier King Charles Spaniel, whereas the Pug, French Bulldog and Bulldog were just the fourth, fifth and eight most common breeds respectively. This apparent paradox may be explained by rising popularity being reflected by increasing numbers of very young dogs being added to the overall population but that it can take a decade for these new additions to overtake the counts of pre-exiting popular brachycephalic breeds.

Although the current results reflect the relative risk for brachycephalic types overall, application of the findings for health reforms based on the individual disorders will require deeper understanding of pathogenetic pathways that lead to these disorders. Vulnerability in the brachycephalic group of dogs to disease risk can be directly related to the brachycephalic skull conformation itself or may instead be associated with alternative factors such as other conformational features typically linked with brachycephaly, specific predisposition in some common brachycephalic breeds or even lifestyle differences between brachycephalic and other dog types. Several of the disorders identified with predisposition in brachycephalic dogs in the current study have causative links associated with the brachycephalic skull conformation. These disorders include upper respiratory tract disorders 10 and corneal ulcers 11 . However, there are many others where the underlying pathophysiological pathway may not be directly linked with brachycephalism itself but happen to be very common in some brachycephalic breeds, for example heart murmurs in Cavalier King Charles Spaniels 37 , or where no clear rationale for the increased risk in brachycephalic types is clear, such as umbilical hernia, otitis externa or anal sac impaction. As such, decision-making on the most effective potential solutions and strategies to reduce the prevalence of the predisposed disorders identified here will likely differ by breed. Promotion of widespread change to average breed conformations may reduce the frequency or severity of those disorders inherently linked to specific morphological features, for example, an increased muzzle length to move a breed away from the exaggerations of the brachycephalic category would likely reduce the risk or severity of BOAS in French Bulldogs 10 , 38 . In contrast, changing skull shape may offer little direct improvement to the prevalence of other predisposed disorders such as patellar luxation which appears to be associated with miniaturization of breeds (especially those < 10 kg) 39 . Miniaturisation and association with patellar luxation has been a feature for several breeds included in this study including Chihuahua (brachycephalic) as well as the Pomeranian and Yorkshire Terrier (mesocephalic) 40 .

The degree (or severity) of brachycephaly varies between breeds (a bulldog may be considered as more severely brachycephalic than a Cavalier King Charles Spaniel) but there can also be considerable variation in brachycephaly within breeds 41 . Shifting the median severity of brachycephaly towards a longer skull shape within breeds has been suggested as one option to reduce the prevalence of disorders directly linked to brachycephaly while still retaining these breeds within the overall dog population 10 , 11 , 42 . Detrimental effects from skull shape on health may be affected by other modifiable variables (risk factors) which may vary between populations of brachycephalic dogs and over time. These differences also offer opportunities to reduce the negative welfare impact of brachycephalism if carefully managed. For example, obesity has been identified as a risk factor for Brachycephalic Obstructive Airway Syndrome (BOAS) 10 , 43 , with bodyweight control likely to be, in part, dependent on provision of appropriate diet and exercise by individual dog owners 44 . Although the current study did not identify higher odds of obesity in brachycephalic dogs overall, the results did highlight obesity as the third most common disorder in brachycephalic dogs which suggests there is ample scope to reduce obesity in these breeds and therefore to positively impact on the respiratory compromise shown by many of these dogs. Certain popular brachycephalic breeds, such as Pugs, have also previously been reported to be at particularly high risk of obesity 20 , suggesting that effective bodyweight control may be of additional benefit to the health of specific brachycephalic breeds.

The breed-related normalisation phenomenon describes a cognitive bias whereby humans readily accept certain clinical attributes that are typical for the breeds as falling within the domain of ‘good health’ within these breeds whereas these same clinical attributes would not be accepted as consistent with ‘good health’ in dogs in general 45 , 46 . The belief that clinical conditions that are overwhelmingly common in certain breeds must, de facto, also be normal and therefore acceptable has been suggested to explain the reduced frequency for presentation of dogs affected with these breed-typical conditions for veterinary care 47 . Studies in the UK indicate that over half of dogs with BOAS are not presented for veterinary investigation of this disorder because their owners perceive these clinical signs (e.g. increased respiratory noise) as ‘normal for the breed’ 38 , 48 . The common current perception by owners and veterinary professionals alike that common breed-related traits such as snoring/snorting, drooling and exercise intolerance are somehow normal and therefore consistent with health in certain breeds could be considered as a modifiable risk factor with the potential to improve welfare in brachycephalic breeds. In humans, health is defined as a ‘state of complete physical, mental and social well-being and not merely the absence of disease or infirmity’ 49 . Breed and kennel clubs, the veterinary profession and welfare bodies, as key opinion leaders, should emphasise that attributes inconsistent with good health in dogs overall (for example, noisy laboured breathing at rest) should not be acceptable as consistent with good health in individual breeds; and that any exceptions to this rule should be considered as a deviation from good health.

Normalisation of expectations of health can lead to other phenomena that promote diagnostic biases between breeds. Veterinarians in clinical practice often tend to rely on intuitive methods such as pattern recognition for speedy diagnosis-making rather than following a more labour-intensive process of problem-based inductive clinical reasoning 50 . Script theory proposes a rationale for how clinicians store sets of pre-compiled knowledge called ‘illness scripts’ as mental models of real-world disorders; these illness scripts then influence the probability of certain diagnoses being reached 51 . Since illness scripts depend heavily on prior knowledge and beliefs, it stands to reason that increasing awareness of heightened risk of certain disorders such as corneal ulceration 12 or dystocia 13 , 14 in brachycephalic breeds will bias the probability of such diagnoses in these breeds.

The current study highlights that the 2016 UK population of brachycephalic dogs were demographically different to their mesocephalic, dolichocephalic and crossbreed counterparts in many characteristics that may be associated with health outcomes. Brachycephalic dogs were generally younger and lighter than the other three groups. The probability of the occurrence of many disorders in dogs is strongly associated with age and bodyweight; for example osteoarthritis, heart disease, lipoma, hyperadrenocorticism, urinary incontinence, dystocia, cruciate disease and patellar luxation 12 , 24 , 25 , 27 , 28 , 40 , 52 , 53 , 54 , 55 , 56 , 57 , 58 . Confounders are defined as factors associated with both the risk factor and the outcome of interest but that are not on the causal pathway 21 . Age and bodyweight are therefore likely to act as confounders in analyses that aim to compare effects between brachycephalic and other skull shape groups but to date many studies have been reported using only univariable methods that fail to account for confounding and therefore potentially may report results that are heavily confounded and misleading.

The median age of any group of breeds is strongly influenced by whether the predominant breeds in the group are increasing or decreasing in popularity; increasing popularity will promote the introduction of many new puppies into the population and therefore shift the median age downwards with proportionately more younger dogs entering than there are older dogs dying 7 . The past decade has seen marked increases in popularity for several brachycephalic breeds in the UK, with proportional ownership of Chihuahua 59 , French Bulldog 18 and Pug 20 rising steeply. These rapid increases in popularity of these breeds contribute to a lowered median age of brachycephalic dogs overall. Although the median age of the brachycephalic group (3.31 years) was statistically lower than each of the other three groups, it is noteworthy that the median ages for crossbreds (3.74 years) was numerically much closer and younger than the median ages for mesocephalic (5.33 years) and dolichocephalic (5.07 years) types. The relative youth of the crossbred group may reflect the recent surge in popularity of designer crosses such as labradoodle and cockapoo that will have had the effect of pulling the median age of the overall crossbred group downwards 60 .

In addition to age and bodyweight differences, brachycephalic breeds were less likely to be neutered than the other three skull shape groups and also had some differential insurance status effects, suggesting that neutering and insurance should also be considered a priori as potential confounders. Associations between neutering have been reported for many disorders including urinary incontinence, cancer, joint disease and some behavioural consequences 61 , 62 , 63 , 64 , 65 , 66 , 67 , 68 , 68 . Proportional uptake of pet insurance is associated with the probability of diagnosis for several disorders including corneal ulceration, hyperadrenocorticism, cruciate disease, mast cell tumour, chronic kidney disease and patellar luxation 12 , 40 , 54 , 55 , 57 , 69 . Access to the financial support of pet insurance may reduce diagnostic constraints for both owners and veterinarians to promote greater clinical freedom and hence higher levels of diagnosis 70 .

This study revealed profound differences in inference when the same core data were analysed using either univariable or multivariable methods. Several findings were identified from multivariable methods that would have been missed if only univariable testing had been applied, including that brachycephalic dogs show increased odds of having at least one disorder compared to crossbreed types and two precise term disorders (otitis externa, skin cyst) that were at increased odds in brachycephalic breeds. Conversely, there were eight confounded findings that would have been accepted as significant if only univariable analysis had been applied but that did not show associations after accounting for confounding in multivariable analysis: periodontal disease, obesity, overgrown nail(s), retained deciduous tooth, lameness, skin mass, osteoarthritis and lipoma. Reporting false positive and false negative results in scientific studies carries increasingly detrimental risks for dog welfare as we move into the era of evidence based veterinary medicine and policy 70 , 71 . Results from canine health studies influence breed club health initiatives, research funding, animal charity campaigning and government policy 36 , 73 , 74 , 75 and thus the reliability of research findings are critical if we are to optimise decision-making on future dog welfare strategies. Publishing results that are heavily confounded, especially where this form of bias is not explicitly acknowledged, also contributes to the current ‘reproducibility crisis’ in scientific reporting and promotes a more general distrust in scientific outputs and quality 76 , 77 .

The findings of the current study confirm that there are substantially different inferences gained from multivariable analysis compared with univariable analysis. This suggests that multivariable methods should be considered as the gold standard when analysing canine health data and that key confounding variables including bodyweight, age, sex, neuter and insurance status should be considered as standard default covariables in these analyses unless there is evidence to justify exclusion of these from analyses. Additionally, the results of previous breed predisposition studies that did not include multivariable methods should now be viewed with a more critical eye, given that these findings may harbour false positive and/or negative inferences that are challenging to now identify. This need for later re-analysis of previous studies also highlights the importance of depositing research data along with relevant confounding variables in open access repositories so that results can be retrospectively verified if authors choose to publish only univariable analyses of their data initially 78 .

In the current study, undesirable behaviour (precise level disorder) and behavioural disorders (group level disorder) showed decreased odds in brachycephalic breeds compared to non-brachycephalic breeds. Several factors may influence this finding, including both actual differences in the frequency of undesirable (and desirable) behaviours between breed types, but also differing perceptions and expectations by owners about what is normal, or desirable within these breeds. The current allure to ownership of brachycephalic breeds is partly based on perceived breed-associated positive behavioural factors, namely making good companion dogs, and being good breeds for households with children 79 . Owner expectations of what is ‘normal’ or ‘good’ behaviour for their breed is likely to influence the likelihood of veterinary presentation for perceived undesirable behaviour. In a recent study of brachycephalic ownership experiences, one-fifth of owners reported their dog behaved better than expected, and two-thirds met expectations, suggesting that the majority of brachycephalic dog owners appear satisfied with their dog’s behaviour 80 . Studies that explore actual behavioural differences (positive or negative traits) between brachycephalic and non-brachycephalic breeds are in their relative infancy compared to studies on physical health differences. However, initial findings suggest some potential divergences between these breed types, particularly in relation to dog–human communication and affiliation. Evidence suggests that brachycephalic dogs are more affectionate, cooperative and interactive with unfamiliar humans than dogs with relatively longer skulls 81 , 82 .

There are limitations to the current study. Breed status was assigned at the discretion of the owner and the veterinary team without validation based on pedigree records, so some breed misclassification was possible. The generalisability of the current results to countries outside of the UK and over time may vary. The median bodyweight of the brachycephalic and the non-brachycephalic groups will be heavily influenced by the dominant breeds within each group, which is liable to geographical variation, and demographic trends 83 . The distribution of breeds within the brachycephalic group in the current study is highly skewed towards a smaller number of very popular breeds in the UK, such as the Chihuahua, Shih Tzu, Cavalier King Charles Spaniel, French Bulldog and Pug, with these five breeds alone representing 71.87% of all dogs in this category. As such, more general characteristics of the overall brachycephalic group may be obscured by these breeds and biased towards small-medium brachycephalic dogs rather than less common, larger brachycephalic breeds such as the Dogue De Bordeaux and Bullmastiff. Future work specifically aimed at subsets of smaller and larger sized brachycephalic breeds can help to improve clarity based on body size. Research findings can be reported at differing levels of abstraction ranging from high abstraction (such as skull conformation) to moderate abstraction (such as breed) to precise abstraction (such as specific subsets of breeds) 84 . Research at different levels of abstraction offers differing advantages and drawbacks, and there is no single ideal abstraction level that answers research question. Research at very precise abstraction offers advantages of tighter application to well defined phenotypes of dogs (such as one specific disorder in one sex of one breed in one country) but conversely limits the proportion of overall dogs that are covered. Alternatively, higher levels of abstraction can assist our understanding of broader concepts such as skull conformation, but may be criticised for offering less rigour in relation to each of the many subtypes of dogs within these broad skull conformational groups. Consequently, although the current study applied a high level of abstraction to explore associations between general health and skull conformation, the cautious reader should not interpret this to infer that every breed or subtype of dog in each skull conformation category carries equal risk for these disorders. This study was based on the general population of dogs under primary-veterinary care in the UK but was unable to differentiate between Kennel Club registered and non-Kennel Club registered dogs which may differ in health status. The Kennel Club has recently made efforts to reduce points of concern for individual breeds, with brachycephalic breeds as a priority, using the Breed Watch scheme 85 and is also working with the relevant breed clubs on defined breed health strategies within its Breed Health and Conservation Plans 73 . It is also noteworthy that this study explores effects associated with brachycephalism overall but the ecological fallacy phenomenon suggests that these effects may not necessarily apply to all breeds within these groups 86 . For example, brachycephalic dogs had 3.46 higher odds of heart murmur compared to non-brachycephalic types. However, over 10% of the brachycephalic group were Cavalier King Charles Spaniels, a breed highly predisposed to heart murmurs with a reported prevalence of 30.9% 37 . Although the results of the current study may assist to generate an overall view of the impact from brachycephalism on dog health, it is also clear that a breed-by-breed approach is additionally required to tackle specific problems that may differ in predisposition between breeds even within the brachycephalic group, for example corneal disorders in Pugs 20 and skin fold pyoderma in Bulldogs 19 . Further than this, there is additionally wide variation in health status between individual dogs within each breed and thus ultimately each dog should be considered on its own individual merits for breeding, beyond the label of its breed. The grouping of dogs into skull categories, and the choice of categorisation scheme is another potential limitation of this work. Breeds were categorised by the authors based on typical breed-related skull-shape conformation but this process did not include measurements of individual skull conformation 11 or apply format cut-points for category boundaries based on cephalic index 87 or other skull metrices including craniofacial ratio 11 , craniofacial angle 88 , and skull index 89 . Supplementary A shows the breed categorisation that was used in the study. There is currently no standardised classification system that comprehensively links the spectrum of dog breeds to skull shape. The classification (Appendix A) used in the current study is the result of work by the authors over the past several years but is still open to update based on new information and opinions. Although brachycephalic, mesocephalic and dolichocephalic are useful classifiers to capture the wide variety in dog skull shapes, they have been criticised as overly simplistic and likely to miss subtle differences in head shape within each category 90 . Indeed, recent studies have identified more subtle elements of skull conformation that are risk factors for disorders such as syringomyelia 91 . Although potentially hampered by these limitations, the methods used in the current study are bolstered by the application of the big data approach, which has the power to identify differences between these groups and generate hypotheses for further, more in-depth studies. The results of the many specific statistical comparisons reported in the current study should be taken as exploratory rather than confirmatory; the authors were aiming to explore general principles of comparison between the skull shape categories and between univariable versus multivariable methods rather than to confirm predispositions for the specific disorders.

This study provides strong evidence to support the common assertion that brachycephalic breeds are generally less healthy than their non-brachycephalic counterparts in relation to total disorder counts and specific common conditions recorded. Potential solutions to some of these health problems are likely to require conformational change to current skull shapes averages for many breeds; however, many other health problems will require targeted action at the individual breed level, owing to large differences in individual breed predispositions to disorders. Results from studies that report only univariable methods should be treated with extreme caution due to potential confounding effects that have not been accounted for during study design or analysis.

The study population included all available dogs under primary veterinary care at clinics distributed across the entire of the UK that were participating in the VetCompass Programme during 2016. Dogs under veterinary care were defined as those with either a) at least one electronic patient record (EPR) (free-text clinical note, treatment or bodyweight) recorded during 2016 or b) at least one EPR recorded during both 2015 and 2017. VetCompass collates de-identified EPR data from primary-care veterinary practices in the UK for epidemiological research 30 . Data fields available to VetCompass researchers include a unique animal identifier along with species, breed, date of birth, sex, neuter status, insurance status and bodyweight, and clinical information from free-form text clinical notes and treatment with relevant dates.

A cross-sectional analysis using cohort clinical data was used to estimate the one-year (2016) period prevalence of the most commonly diagnosed disorders in brachycephalic, mesocephalic and dolichocephalic dog types 92 . Sample size calculations estimated that approximately 3,346 brachycephalic types and 13,384 non-brachycephalic types would be needed to detect an odds ratio ≥ 1.50 for any disorder with ≥ 1.50% prevalence in the non-brachycephalic group, assuming 1:4 ratio of brachycephalic to non-brachycephalic dog types (80% power and 95% confidence) 93 . Ethics approval was obtained from the RVC Ethics and Welfare Committee (Reference SR2018-1652). All methods were performed in accordance with the relevant guidelines and regulations. Informed consent for use of the clinical data of the study dogs was obtained from all of the participating clinics and the animal owners.

Breed status was assigned by the participating practices based on information provided by the owners in combination with the opinion of the veterinary professional teams. The recorded breed status could be updated over time in the clinical records. The latest available breed status was used in the current study, based on the assumption that accuracy would improve over time. Breed status was cleaned and mapped to a VetCompass breed list derived and extended from the VeNom Coding breed list 94 . Breeds were categorised by the authors into four groups based on typical skull-shape conformation 41 : brachycephalic, mesocephalic, dolichocephalic and crossbred dog types (Supplementary A). Crossbred dogs included all dogs that were not recorded with a standard recognised breed name 41 , 95 ; crossbreds included genuine ‘mixed-breed’ mongrels as well as dogs where some breed parentage information was recorded including those that are so-called designer types such as labradoodle and cockapoo 60 . Mesocephalic, dolichocephalic and crossbred dog types were further grouped as non-brachycephalic types for the purposes of disease risk analyses. Neuter and insurance status were defined by the final available EPR value. Adult bodyweight was defined as the mean of all bodyweight (kg) values recorded for each dog after reaching 18 months old and was categorised: ≤ 5.0, 5.0 to < 10.0, 10.0 to < 15.0, 15.0 to < 20.0, 20.0 to < 25.0, 25.0 to < 30.0, 30.0 to < 35.0, 35.0 to < 40.0 and ≥ 40.0. Mean adult bodyweight was calculated for each breed/sex combination with adult bodyweight available for ≥ 100 dogs. Individual dogs were categorised as “at or above the breed/sex mean”, “below the breed/sex mean” and “no recorded bodyweight” compared with the relevant breed/sex category. Age (years) was defined at December 31, 2016 and categorised: ≤ 1.0, 1.0 to < 2.0, 2.0 to < 4.0, 4.0 to < 6.0, 6.0 to < 8.0, 8.0 to < 10.0, 10.0 to < 12.0 and ≥ 12.0.

The list of unique animal identification numbers was randomly ordered and the clinical records of a randomly selected subset of animals were reviewed in detail to extract the most definitive diagnoses recorded for all disorders with clinical evidence of existence during 2016 31 . For the current study, disorders were defined as conditions that show deviation from good health and are often characterised by functional impairment 96 . Elective (e.g. neutering) or prophylactic (e.g. vaccination) clinical events were not included. No distinction was made between pre-existing and incident disorders. Disorders described within the clinical notes using presenting sign terms (e.g. ‘vomiting’ or 'vomiting and diarrhoea'), but without a formally recorded clinical diagnostic term, were included using the first sign listed (e.g. vomiting). The extracted diagnosis terms were mapped to a dual hierarchy of diagnostic precision for analysis: precise terms and grouped terms as previously described 31 . Briefly, precise terms described the original extracted terms at the maximal diagnostic precision recorded within the clinical notes (e.g. inflammatory bowel disease would remain as inflammatory bowel disease ). Grouped-level precision terms mapped the original diagnosis terms to a general level of diagnostic precision (e.g. inflammatory bowel disease would map to gastro-intestinal ).

Following internal validity checking and data cleaning in Excel (Microsoft Office Excel 2013, Microsoft Corp.), analyses were conducted using Stata Version 13 (Stata Corporation). The sex, neuter status, insurance status, age, adult bodyweight and breed composition for common breeds were described and the one-year period prevalence values were reported with 95% confidence intervals (CI) that described the probability of diagnosis at least once during 2016 for brachycephalic, mesocephalic, dolichocephalic and crossbred dog types under veterinary care during 2016. The CI estimates were derived from standard errors based on approximation to the binomial distribution 97 .

Direct comparisons between variables other than disorders used the chi-square test to evaluate categorical variables (Fisher’s exact test was used if at least one of the reported cells was under 5) and the Mann–Whitney U test to evaluate binary categorical variables for association with continuous variables 97 . The odds of disorder occurrence were estimated using binary logistic regression. Univariable risk factor analyses directly compared the odds for each disorder between brachycephalic and non-brachycephalic dogs. Multivariable risk factor analyses applied mixed effects multivariable binary logistic regression modelling to evaluate associations between each disorder and the brachycephalic/non-brachycephalic factor of main interest along with a fixed set of covariables included to account for confounding ( adult bodyweight category, bodyweight relative to breed/sex mean, age category, sex, neuter and insurance ). Breed and clinic attended were included as a random effects 21 . Decision-making on which variables to include in these standard models used an ‘information theory’ approach to include a priori variables that the authors considered as potential confounders for outcome associations with the skull conformation variable that was of primary interest 98 . Multivariable Poisson regression modelling was used to evaluate associations between the skulls shape factor of main interest (brachycephalic, mesocephalic, dolichocephalic and crossbred) along with the same fixed set of covariables ( adult bodyweight category, bodyweight relative to breed/sex mean, age category, sex, neuter and insurance) and the numerical outcome of the count of disorders recorded during 2016. Statistical significance was set at the 5% level. Only the results for the brachycephalic/non-brachycephalic factor of main interest are reported from each regression model.

Ethics approval

Ethics approval was granted by the RVC Ethics and Welfare Committee (reference number SR2018-1652).

Consent for publication

The Royal Veterinary College has provided permission to publish this paper. The manuscript number is PPH_02188.

Data availability

Original data used for the current study will be made freely available on the Royal Veterinary College Data Repository.

Abbreviations

Confidence interval

Disorder count risk ratio

Electronic patient record

Interquartile range

The Kennel Club

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Acknowledgements

Thanks to Noel Kennedy (RVC) for VetCompass software and programming development. We are grateful to the following researchers who assisted with data collection during this project: Alice Ashworth, Alison Toetz, Bethany Allen, Eleanor White, Elizabeth Ainsworth, Jasmine Broomhead, Joanne Humphrey and Teresa Soares. We acknowledge the Medivet Veterinary Partnership, Vets4Pets/Companion Care, Goddard Veterinary Group, CVS Group, IVC Evidensia, Linnaeus Group, Beaumont Sainsbury Animal Hospital, Blue Cross, Vets Now and the other UK practices who collaborate in VetCompass. We are grateful to The Kennel Club Charitable Trust, Agria Pet Insurance and The Kennel Club for supporting VetCompass.

This study was supported at the RVC by an award from the Kennel Club Charitable Trust and Agria Pet Insurance. Neither the Kennel Club Charitable Trust, Agria Pet Insurance or the Kennel Club had any input in the design of the study, the collection, analysis and interpretation of data or in writing the manuscript.

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D.O.N., C.P. and P.C. were responsible for the conception and design, acquisition and extraction of data. D.O.N. carried out the analysis. D.O.N., R.P. and C.P. were mainly responsible for drafting the manuscript. D.O.N., R.P., C.P., P.C., D.C. and D.B. were involved in interpreting the results, revising the manuscript and gave final approval of the version to be published. D.O.N., R.P., C.P., P.C., D.C. and D.B. agree to be accountable for all aspects of the accuracy and integrity of the work.

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Correspondence to D. G. O’Neill .

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O’Neill, D.G., Pegram, C., Crocker, P. et al. Unravelling the health status of brachycephalic dogs in the UK using multivariable analysis. Sci Rep 10 , 17251 (2020). https://doi.org/10.1038/s41598-020-73088-y

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Article Contents

Introduction, regulatory definitions of natural, natural beyond the regulatory definitions, impact on pet health, the future of natural pet nutrition, literature cited.

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Natural pet food: A review of natural diets and their impact on canine and feline physiology

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P. R. Buff, R. A. Carter, J. E. Bauer, J. H. Kersey, Natural pet food: A review of natural diets and their impact on canine and feline physiology, Journal of Animal Science , Volume 92, Issue 9, September 2014, Pages 3781–3791, https://doi.org/10.2527/jas.2014-7789

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The purpose of this review is to clarify the definition of “natural” as it pertains to commercial pet food and to summarize the scientific findings related to natural ingredients in pet foods and natural diets on the impact of pet health and physiology. The term “natural,” when used to market commercial pet foods or pet food ingredients in the United States, has been defined by the Association of American Feed Control Officials and requires, at minimum, that the pet food be preserved with natural preservatives. However, pet owners may consider natural as something different than the regulatory definition. The natural pet food trend has focused on the inclusion of whole ingredients, including meats, fruits, and vegetables; avoiding ingredients perceived as heavily processed, including refined grains, fiber sources, and byproducts; and feeding according to ancestral or instinctual nutritional philosophies. Current scientific evidence supporting nutritional benefits of natural pet food products is limited to evaluations of dietary macronutrient profiles, fractionation of ingredients, and the processing of ingredients and final product. Domestic cats select a macronutrient profile (52% of ME from protein) similar to the diet of wild cats. Dogs have evolved much differently in their ability to metabolize carbohydrates and select a diet lower in protein (30% of ME from protein) than the diet of wild wolves. The inclusion of whole food ingredients in natural pet foods as opposed to fractionated ingredients may result in higher nutrient concentrations, including phytonutrients. Additionally, the processing of commercial pet food can impact digestibility, nutrient bioavailability, and safety, which are particularly important considerations with new product formats in the natural pet food category. Future opportunities exist to better understand the effect of natural diets on health and nutrition outcomes and to better integrate sustainable practices in the production of natural pet foods.

Throughout history, humans have associated with dogs and cats in various ways, including protection, rodent control, hunting, and companionship. Diets of dogs and cats have shifted, as a result of domestication, from hunting and scavenging to diets formulated for their specific nutritional requirements. Changes in human diets through the development of agricultural practices have fostered this shift. In the United States, 63% of pet owners consider their pets to be family members ( AVMA, 2012b ). Anthropomorphism of dogs and cats has resulted in pet owner preference for pet foods containing ingredients that they find in their own diet and processed in a way to maintain the nutritional integrity of the ingredients and ensure food safety. Contemporary trends in human diets in developed regions of the world are including more fresh fruits and vegetables ( Barnard, 2010 ) and whole grains ( Griffiths, 2010 ). This paradigm has resulted in the emergence of the natural pet food segment. The natural pet food segment in the United States has grown steadily, from US$2.0 billion in 2008 to $3.9 billion in 2012 ( Lummis, 2012 ).

The expansion of the natural pet food segment has led to a wide spectrum of products with different nutritional strategies applied across brands and introducing unique philosophies on what defines a natural pet food product ( Lummis, 2012 ). This variability has led to confusion and disagreement as to the true definition of natural pet foods and natural pet nutrition. Additionally, the application of human food trends often is used to support functional health benefits of natural pet food products despite limited scientific evidence supporting the benefits in companion animals. Therefore, the purpose of this review is to clarify the definition of natural as it pertains to commercially manufactured pet foods and summarize the scientific findings regarding natural ingredients used regarding their impact on pet health and physiology. It should be noted, however, that although home-prepared diets may meet certain definitions of natural, they will not be discussed here because these are not officially recognized by any regulatory agency.

Pet food manufacturers must meet the regulatory definition of natural to market a pet food as natural. The definition of natural applies to both pet food ingredients and pet food products. However, regulatory agencies internationally disagree on the definition of natural. Consider, for example, differences that exist between the United States and European definitions of natural as it applies to pet food ingredients or products. In the United States, the regulatory definition of natural has been developed by the Association of American Feed Control Officials ( AAFCO ), a voluntary membership association of state feed officials charged with developing model regulations to be adopted by states to regulate animal feeds and animal drug remedies. The AAFCO definition of natural states the following:

…A feed or ingredient derived solely from plant, animal or mined sources, either in its unprocessed state or having been subject to physical processing, heat processing, rendering, purification, extraction, hydrolysis, enzymolysis or fermentation, but not having been produced by or subject to a chemically synthetic process and not containing any additives or processing aids that are chemically synthetic except in amounts as might occur unavoidably in good manufacturing practices. ( AAFCO, 2013 )

Synthetic trace nutrients are allowed by the AAFCO in natural pet foods as long as they have nutritive value. In this case, a disclaimer on the package is used to inform the consumer that the vitamins, minerals, or other trace nutrients are not natural ( AAFCO, 2013 ). This enables the formulation of complete and balanced natural pet food products. A complete and balanced diet should have all essential nutrients in the proper amount and proportions based on authoritative recommendations, such as the NRC ( NRC, 2006 ). Guidelines for nutrient profiles for both dogs and cats by which a food may be considered complete and balanced are provided by the AAFCO (2013) . The complete and balanced statement on the label indicates the formula provides all the essential nutrients necessary to maintain life (except water) when fed as the sole source of energy in the diet.

The European Union use of the term natural is defined by The European Pet Food Industry Federation ( FEDIAF ) and states

The term “natural” should be used only to describe pet food components (derived from plant, animal, microorganism or minerals) to which nothing has been added and which have been subjected only to such physical processing as to make them suitable for pet food production and maintaining the natural composition. ( FEDIAF, 2011 )

Processing of components including freezing, concentration, extraction (without chemicals), drying, pasteurization, or smoking (without chemicals) is acceptable as far as is maintains the natural composition. Microbiological and enzymatic processes, hydrolysis, or natural fermentation processes (without the use of genetically modified organisms) are acceptable with the use of the term natural ( FEDIAF, 2011 ). Similar to the AAFCO definition, the FEDIAF definition allows the use of synthetic vitamins and minerals with an appropriate disclaimer. Additionally, guidelines for nutrient profiles for both dogs and cats by which a food may be considered complete and balanced are provided by the FEDIAF (2011) .

Given the above definitions, it is noteworthy that there are distinct differences between the AAFCO and FEDIAF approaches to defining natural. While both allow many of the same processes, the FEDIAF definition excludes the use of chemical processing aids and requires that processing does not change the natural composition of the ingredient. For example, under the AAFCO definition, hexane-extracted soybean oil is considered a natural pet food ingredient since the hexane is not present in the final ingredient except in amounts as might occur unavoidably in good manufacturing practices. However, according to the FEDIAF definition, hexane-extracted oil would not be considered natural since it uses chemical extraction. Conversely, cold pressed oil would be considered natural according to the FEDIAF definition because it does not use chemical extraction. An example of an instance where the natural composition of an ingredient is not maintained is carrot pulp from which carotene has been extracted. According to the FEDIAF definition, this would not be considered a natural ingredient because the natural composition has changed; however, this may be considered a natural ingredient according to the AAFCO definition. Another difference in regulatory definitions is that the use of genetically modified ingredients in natural products is currently not addressed in the AAFCO definition of natural but is excluded by the FEDIAF definition. The difference between these definitions is instrumental to defining natural ingredients in today's global marketplace and underscores both the functional and regulatory characterizations of natural pet foods for dogs and cats. As such, it presents an ongoing challenge for natural pet food product formulation because it necessitates a different approach to product formulation in different regions of the world.

Inconsistencies in the definition of natural among international regulatory agencies and the lack of visibility and understanding of regulatory definitions by pet owners have contributed to misperceptions about natural pet food products. Therefore, many natural pet food consumers seek out products or ingredients with claims of human-grade, organic, holistic, ancestral, or instinctual and avoid ingredients perceived as fillers or byproducts ( Shmalberg, 2013 ); however, these terms are not addressed in the current regulatory definitions of natural.

Each step of the manufacturing process of pet food can positively or negatively affect the naturalness of the final product, including crop and livestock production activities, ingredient processing and preservation, and kibble extrusion or canning of final product ( Fig. 1 ). Consequently, various steps of the manufacturing process are considered by pet owners, manufacturers, nutritionists, or regulatory agencies when determining if an ingredient or product is natural. For example, the AAFCO definition of natural primarily considers ingredient processing, whereas consumers may impose additional selection criteria based on opinions and beliefs, such as exclusion of ingredients perceived as having low nutritional value. On the other hand, consumers, nutritionists, or manufacturers that determine a natural diet based on pet physiology or pet preference may consider nutrient composition, food format, or ingredient origin (e.g., plant vs. animal).

Pet food manufacturing process steps considered by different entities for defining “natural.” Labels within a circle represent the regulatory consideration of the Association of American Feed Control Officials definition of natural, consumer perspectives of natural, and natural pet nutrition concepts based on pet physiology and preferences.

Differences in natural ingredient processing highlight the difficulties in classifying ingredients or pet food products as natural. Therefore, identifying natural ingredients is a complex process in which it is critical to have a thorough understanding of ingredients through their production, preparation, processing, and preservation. Even within ingredient processing techniques, there is a continuum of what may be considered more or less natural ( Fig. 2 ). For example, an identical raw material can be processed either as a whole ingredient, fractionated to isolate specific parts of the ingredient, or stabilized by adding synthetic preservatives. According to the AAFCO definition of natural, the whole cooked ingredient and fractionated ingredients would be considered natural but the synthetically preserved ingredient would not. However, from a consumer standpoint the defining of the ingredient as natural may not be as clear-cut. Many consumers would consider the whole cooked ingredient as natural but not the fractionated or synthetically preserved ingredient.

The continuum of natural ingredients. The Association of American Feed Control Officials (AAFCO) and The European Pet Food Industry Federation (FEDIAF) regulatory definitions of natural are highlighted along the continuum. Examples of pet food ingredients are given for each step of the continuum. GM = Genetically Modified.

Natural Diets

Natural diets, including instinctual or ancestral diets, are based on feeding pets according to their physiological capabilities or preferences, rather than simply meeting the regulatory definition of a natural pet food product. Instinctual diets are based on the philosophy of feeding pets according to their innate preferences, with the assumption that animals will self-select foods to meet their nutritional needs. Ancestral diets are based on the philosophy of feeding pets a diet similar to evolutionary ancestors, with the assumption that such a diet aligns with the physiological needs and metabolic capabilities of companion animals. Regardless of philosophical basis, both instinctual and ancestral diets typically contain higher protein and lower carbohydrate concentrations than the majority of dry pet foods on the market. There are no regulatory definitions of instinctual or ancestral diets; therefore, the nutrient composition of commercial pet food products may not accurately apply to instinctual or ancestral nutritional philosophies.

Instinctual Diets.

Recent research using nutritional geometry in a controlled environment has demonstrated that dogs of various breeds select a macronutrient profile in which 30% of their ME comes from protein, 63% from fat, and 7% from carbohydrates ( Hewson-Hughes et al., 2013 ). Similar research in cats indicates they select 52% of their ME from protein, 36% from fat, and 12% from carbohydrates ( Hewson-Hughes et al., 2011 ). Given their strict carnivorous nature, it is not surprising that cats show a preference for higher protein diets compared to omnivorous dogs. By contrast, dogs apparently find dietary fat particularly palatable, which is consistent with minimal adverse health effects of high fat diets in healthy populations of dogs ( Bauer, 2006 ). However, it is unknown whether the above distributions of macronutrients would provide optimal nutrition, given that the preferred macronutrient levels are substantially different than minimal requirements or recommended allowances outlined by the NRC ( NRC, 2006 ).

Ancestral Diets.

It is recognized that domesticated dogs evolved from wolves ( Canis lupus lupus ; Serpell, 1995 ). From archeological evidence, it is believed dogs were the first animal to be domesticated by humans around 14,000 yr ago ( Clutton-Brock, 1995 ). Domestication of cats is more recent than dogs, as remains of cats dating back 6,000 yr ago have been found in Cyprus ( Serpell, 2000 ). Consequently, some natural dog foods are marketed based on high meat and protein formulations believed suitable for wolves due to their evolutionary connection and genetic similarities. However, domesticated dogs are no longer wolves because domestication as Canis lupus familiaris has modified not only their social and cognitive attributes but also the types of foodstuffs that are suitable for them ( Hemmer, 1990 ). Recent evidence has been reported in which candidate mutations in key genes of dogs compared to wolves provide functional support for increased capability for starch digestion ( Axelsson et al., 2013 ) compared to the carnivorous wolf diet ( Stahler et al., 2006 ). This supports a previous report by Serpell (1995) that dogs descended from a subset of wolves that had been more socially adapted to human contact. These data help explain the omnivorous nature of domestic dogs versus carnivorous wolves.

In nature, it appears the primary component of the canine diet is animal protein, but as noted above, domestic canines can obtain nutritional requirements from plant sources as well. Feral dogs are known to hunt in packs, similar to wild canines, and eat a wide variety of foods. The diet of wolves consists primarily of animal protein and they typically hunt larger prey, such as elk, eating the nutrient-dense organs first followed by muscle tissue ( Stahler et al., 2006 ). Analysis of 50 diets consumed by wolves revealed average nutrient intake of 35.5 g protein, 13.2 g fat, and 0.8 g carbohydrate per MJ ME, which reflects a macronutrient profile of 52% ME from protein, 47% ME from fat, and 1% ME from carbohydrate ( Hendriks, 2013 ). Feral dogs typically hunt small prey and forage on berries and some plants ( Boitani and Ciucci, 1995 ). Jackals ( Canis aureus ) often raid stores of cultivated fruit and consume large quantities of grass ( Ewer, 1973 ). Wild canines and feral dogs must exert a considerable amount of energy to acquire food and therefore consume foods that are more easily available in the environment in which they live. This evidence supports the hypothesis that canine species are highly adaptable to various diets, and the diet they choose is dictated by the environment in which they live.

Through mitochondrial DNA analysis, it has been reported that the domestic cat ( Felis catus ) is most closely related to the European wildcat ( Felis silvestris ), the African wildcat ( Felis libyca ), and the sand cat ( Felis nigripes ; Johnson and O'Brien, 1997 ). These species of wild cats closely resemble the domestic cat in appearance, and African wildcats have been kept as pets ( Smithers, 1968 ). Many of the behavioral signs observed in domestic cats, such as purring, meowing, hissing, and spitting, have been observed in most wild species ( Serpell, 2000 ).

The natural diet of feral cats consists primarily of small mammals, birds, fish, reptiles, and invertebrates, with a macronutrient profile of 52% ME from protein, 46% ME from fat, and 2% ME from carbohydrate ( Plantinga et al., 2011 ). Studies on the preferred macronutrient profile of domestic cats indicate the instinctual dietary preference of domestic cats closely resembles the nutrient composition of cats in the wild ( Hewson-Hughes et al., 2011 ). Studies have been conducted comparing the digestibility of various raw meat based diets of captive exotic felids to domestic cats. Vester et al. (2010) reported apparent total tract digestibility in cheetahs ( Acinonyx jubatus ), jaguars ( Panthera onca ), Malayan tigers ( Panthera tigris corbetti ), Amur tigers ( Panthera tigris altaica ), and domestic short hair cats ( F. catus ) consuming 2 different raw meat based diets. These investigators found no differences in digestibility measure between the captive exotic felids. Differences between domestic cats and jaguars were observed for DM, CP, fat, and GE digestibilities ( P < 0.05). Differences were also observed between domestic cats and Amur tigers for DM, OM, CP, fat, and GE digestibility ( P < 0.05). Additionally, differences were observed between domestic cats and Malayan tigers for CP, fat, and GE digestibilities ( P < 0.05). No differences were observed between domestic cats and cheetahs. A later report from the same laboratory ( Kerr et al., 2013 ) compared total tract digestibility of domestic cats, African wildcats ( Felis silvestris tritrami ), jaguars, and Malayan tigers fed meat based raw diets. In this study, there were no observed differences between species for total tract DM, OM, and GE digestibilities. However, they did find differences between apparent total tract CP digestibility between domestic cats and Malayan tigers, but no differences in CP digestibility were observed between domestic cats and other species in this study. Unlike the evolution of dogs, cats appear to have retained much of the dietary preference, behavioral attributes, and physiological digestive function as the wild species. More research needs to be conducted to determine impact of ancestral diets on health of pets.

Pet Physiology and Metabolism.

The basis behind feeding natural diets, including instinctual and ancestral diets, is to meet nutritional needs and align with physiological and metabolic capabilities to promote health in companion animals. Therefore, to better evaluate the extent to which such diets are appropriate for companion animals, some appreciation of both dog and cat digestive physiology is important.

Both dogs and cats have the ability enzymatically (maltase, sucrose, and lactase) to digest carbohydrates ( Hore and Messer, 1968 ). Morris et al. (1977) showed cats are able to efficiently digest glucose, sucrose, lactose, dextrin, and starch (apparent digestibility 94–100%). Additionally, cats have been reported to have lower enzymatic activities for carbohydrate digestion compared to other species ( Kienzle, 1993a , b , c , d ) and physiologic responses differ by carbohydrate type and thermal processing ( Kienzle, 1994 ). These results indicate that although cats have the ability to efficiently digest carbohydrates, their capacity for carbohydrate digestion may be limited, as evidenced by digestive disorders, such as diarrhea, flatulence, and bloating, when high concentrations of carbohydrates (>5 g/kg BW) are fed ( Kienzle, 1993b ).

Relative to humans, dogs have an increased capacity for fat oxidation, generating twice the amount of energy from fat oxidation at rest and during exercise ( McClelland et al., 1994 ). However, dogs have responses similar to humans in carbohydrate metabolism following a meal, with carbohydrate amount and type dictating glycemic response ( Nguyen et al., 1998 ; Carciofi et al., 2008 ; Elliott et al., 2012 ). For example, when 12 working hounds were fed a high protein (49%), low carbohydrate (13%) diet they had a delayed peak glucose concentration and sustained glucose response compared to when fed a lower protein (22%), higher carbohydrate (45%) diet ( Hill et al., 2009 ).

The metabolism of cats is adapted for gluconeogenesis rather than glucose clearance, including no detectable hepatic glucokinase activity and higher activities of pyruvate carboxylase, fructose-1,6-biphosphatase, and glucose-6-phosphatase in feline compared to canine livers ( Washizu et al., 1999 ; Tanaka et al., 2005 ). However, there is currently limited evidence to suggest that moderate concentrations of carbohydrates in the diet are detrimental to the metabolism or health of cats ( Verbrugghe et al., 2012 ). For example, both high (47% energy from carbohydrate compared to 26–27%) or low (7% energy from carbohydrate compared to 25–29%) concentrations of dietary carbohydrate reduce insulin sensitivity in cats ( Farrow et al., 2002 ; Verbrugghe et al., 2010 ). Additionally, while protein intake of 48 versus 28% energy from protein does not affect insulin sensitivity ( Leray et al., 2006 ), high concentrations of dietary fat (51% energy from fat compared to 33%) reduces glucose tolerance in cats ( Thiess et al., 2004 ).

Although protein or essential AA intakes beyond the recommended allowance ( NRC, 2006 ) have not been reported to provide added benefit for pets requiring maintenance nutrient needs, there is evidence to suggest a benefit during physiological states other than adult maintenance, such as obesity and athletic training. High protein diets (>100 g crude protein/1,000 kcal ME) have been shown to effectively facilitate weight loss in obese dogs while maintaining lean body mass ( Diez et al., 2002 ; Blanchard et al., 2004 ; German et al., 2010 ). Hoenig et al. (2007) investigated effects of a high-carbohydrate/low-protein (28% protein/38% carbohydrate) and a high-protein/low-carbohydrate (45% protein/25% carbohydrate) diet during weight loss. Weight loss modified selected hormones and other metabolites independent of diet. These investigators also found that the high protein diet was beneficial in cats to maintain normal insulin sensitivity of fat metabolism during caloric restriction. It should be noted that studies showing beneficial effects of higher protein diets in overweight or obese companion animals also used caloric restriction and often lower fat concentrations than natural diets to achieve these benefits.

Diets high in protein (>30% ME from protein) or fat (>50% ME from fat) have been shown to have a beneficial effect on exercise performance in dogs. Fat adaptation to greater than 50% of ME from fat was found to improve aerobic performance ( Downey et al., 1980 ) and to spare glycogen utilization in dogs ( Reynolds et al., 1995 ). Beagles ran for 20 miles (140 min) when fed high fat (53–67% of energy) diets but became exhausted after only 15 miles (100 min) when fed a moderate fat (29% of energy) diet ( Downey et al., 1980 ). A high carbohydrate (60% ME from carbohydrate), low fat (15% ME from fat) diet fed to sled dogs resulted in higher ( P < 0.05) resting muscle glycogen concentrations compared with a high fat (60% ME from fat), low carbohydrate (15% ME from carbohydrate) diet, but the rate of glycogen utilization was greater ( P < 0.05) during an anaerobic exercise bout; therefore, the final muscle glycogen concentration was unchanged ( Reynolds et al., 1995 ). In racing sled dogs, protein concentration is also important, given there is progressive development of stress anemia below 32% ME from protein ( Kronfeld et al., 1994 ). Conversely, moderate protein and fat (24% ME from protein, 33% ME from fat, and 43% ME from carbohydrate) has been shown to be more beneficial for sprint performance in dogs, as indicated by faster racing times (32.43 ± 0.48 vs. 32.61 ± 0.50 s; P < 0.05) over a 500-m distance ( Hill et al., 2001 ).

The studies described above support the premise that canine and feline physiological and metabolic capabilities align with the preferred macronutrient levels of instinctual nutrition, which is particularly evident under physiological conditions of stress, such as aerobic exercise training. For cats, this also aligns with the macronutrient concentrations of ancestral nutrition. However, for dogs, ancestral nutrition specified by the diets of wolves is higher in protein and lower in fat and carbohydrates than preferences or physiology.

Further evidence is needed to support health benefits of natural diets for healthy, adult companion animals with maintenance requirements. There is a wide range of nutrient concentrations that may support optimal nutrition ( Kronfeld et al., 1994 ). When the effect of increasing a selected nutrient on some specific performance measure is determined, an optimal plateau is often observed before declining at yet higher concentrations. Furthermore, the optimal range of a nutrient is broader during undemanding physiological states, such as maintenance, but becomes narrower during states of physiological stress, such as growth or exercise training. This is evident in dogs' and cats' ability to effectively and safely use a wide range of macronutrient levels, including higher carbohydrate and lower fat or protein than those specified by instinctual or ancestral nutrition.

Adjusting macronutrient levels to provide optimal nutrition is particularly relevant considering modern pet lifestyles, in which companion animals live primarily indoors and are less active than their wild predecessors. Feeding management becomes a critical issue in feeding natural diets high in protein and fat to sedentary pets, given the substantial evidence for negative health effects of weight gain ( Lund et al., 2005 , 2006 ). Additionally, feeding foods containing high concentrations of animal based protein negatively impacts the environmental sustainability of a diet ( Reijnders and Soret, 2003 ). Including carbohydrate in pet foods aligns with the concept of nutritional sustainability by reducing the environmental impact of pet foods while supporting pet health and nutritional needs (for a complete review of this topic see Swanson et al., 2013 ). Partially meeting energy needs from carbohydrates while still meeting AA and fatty acid requirements allows for the moderate inclusion of more environmentally and economically costly protein and/or fat sources in a pet food, especially in cases where there is competition of certain sources for human food ingredients. Therefore, the potential health benefits of feeding natural diets, specific to an individual pet's lifestyle and health status, should be weighed against the potential health and environmental concerns of feeding a natural diet high in protein and fat Finally, where pet food manufacture is concerned, owner lifestyle must be matched against pet nutritional needs and feeding management. For example, some pets may be indoors for lengthy periods of time while owners are away. Therefore, physiologic patterns of defecation and urination may, of necessity, be different depending on a food's nutrient composition.

Whole Ingredients

Pet foods have historically been formulated based on nutrient content, given that animals have specific requirements for nutrients and not ingredients. However, in the natural pet food segment, there is an increased focus by consumers and pet food manufacturers on ingredients, especially whole ingredients. As it pertains to pet food ingredients, “whole” is defined as a physical form that is “complete, entire” ( AAFCO, 2013 ). Consequently, a growing trend for natural pet foods to contain more whole ingredients, such as meat instead of meat meals, whole grains instead of refined grains, and fruit and vegetable inclusions, has emerged ( Lummis, 2012 ).

The theory behind the beneficial health effects of whole ingredients is described by the concept of food synergy. Food synergy is based on the proposition that the action of the food matrix (i.e., the composite of naturally occurring food components) on biological systems is greater than or different from the corresponding actions of the individual food components ( Jacobs et al., 2009 ). It stems from the idea that we do not have complete knowledge of food composition and some health effects may result from unidentified or underappreciated components. In this way, whole ingredients may provide health benefits that the individual fractionated ingredients or single nutrients cannot provide. Although the term food synergy may not be well known by consumers, the concept of whole ingredients providing health benefits has likely contributed to the interest in natural pet foods by pet owners and hence the increased market demand for whole ingredients in pet foods.

The health benefit in humans of phytonutrients from fruits and vegetables is an example of food synergy. Epidemiological studies in humans indicate associations between fruit and vegetable intake with lower risk of cardiovascular disease in women ( Liu et al., 2000 ). In a human population study, consumption of foods rich in phytonutrients as measured by phytonutrient index has been shown to decrease weight gain and adiposity ( Mirmiran et al., 2012 ) and risk for metabolic syndrome ( Bahadoran et al., 2012 ). Rodent and in vitro models have shown positive effects of food synergy from fruits on antiproliferative and anticarcinogenic activities ( Jacobs et al., 2009 ). Drug-induced mammary tumor incidence in rats was reduced more by using the whole apple than only the flesh without the skin ( Liu et al., 2005 ). Similarly, whole pomegranates had greater in vitro antiproliferative effects than did some of their individual constituents ( Seeram et al., 2005 ). Importantly, as fruits and vegetables and their constituents are incorporated in pet foods, additional research is needed to understand the potential impact on pet health and well-being and the effect of processing on phytonutrient stability ( Tiwari and Cummins, 2013 ).

Whole grains are added to pet food formulations to provide digestible carbohydrates and dietary fiber ( de Godoy et al., 2013 ). The effects of whole grains as they relate to pet health and well-being have not been thoroughly evaluated. Of interest is that whole grains have greater concentrations of many nutrients, including fiber, vitamins, minerals, and phytonutrients, compared to refined grains ( Okarter and Liu, 2010 ; Jonnalagadda et al., 2011 ). For example, nutrient analysis of whole brown rice and brewers' rice used in pet food revealed higher ( P < 0.05) concentrations of ether extract fat, crude fiber, phosphorus, and potassium in whole brown rice compared to brewers' rice ( Table 1 ). This may seem irrelevant given that the dietary formulation of pet foods is intended to account for total nutrient needs especially when similar nutrient concentrations in can be achieved with supplemental fiber and synthetic vitamins and mineral source. However, as in fruits and vegetables, grains contain many unique phytonutrients. Recent studies by Forster et al. (2012a) demonstrated excellent digestibility and acceptability in dogs fed a dry-extruded diet when substituting some wheat and corn with 25% cooked navy bean powder while controlling both macronutrient and micronutrient contents. In addition, these workers also observed similar whole dry cooked bean powder containing diets to provide nutritional weight loss therapy while regulating serum lipids and biochemical analytes in overweight and obese dogs ( Forster et al., 2012b ). In humans, whole grain consumption has been associated with lower risk of certain cancers such as colon cancer. Phytonutrients, such as ferulic acid, have been implicated in the mechanism behind this lower risk ( Jonnalagadda et al., 2011 ). To date, this is an unexplored area for pet nutrition and additional studies are needed

Nutrient analysis (mean ± SD) of brewers' rice and whole brown rice

1 Independent t test.

The trend to include more whole ingredients in natural pet foods has also led to an increase in the inclusion of raw animal protein products as opposed to rendered animal protein products. Rendered products can have a wide range of nutritional variability, which is dependent on byproduct inclusion and processing of the product. For example, feed-grade poultry byproduct meal inclusive of feathers and heads had more variable nutrient content than pet-food grade poultry byproduct meal that did not contain feathers or heads ( Dozier et al., 2003 ). In a study using roosters to measure true AA digestibility, rendered animal meals generally had lower AA digestibility than raw animal products, with lamb meal having the poorest AA digestibility and pork livers (raw animal product) having the greatest AA digestibility ( Cramer et al., 2007 ). In a separate study, rendering of poultry, but not beef, seemed to have a slight negative influence on ileal, but not total tract, digestibility by dogs ( Murray et al., 1997 ). It should be noted, however, that handling, processing, and preservation by an ingredient supplier is a large contributor to the variability in nutritional value of animal products ( Parsons et al., 1997 ), and therefore ingredient supplier practices may be more important than ingredient type (i.e., raw vs. rendered) when assessing quality or nutritional value of animal products.

Ingredient and Product Processing

Processing can have either a positive or negative effect on nutritional value, depending on the processing method and outcomes measured. For example, the degree of gelatinization of wheat starch is positively associated with in vitro digestibility and plasma glucose and insulin responses in rats ( Holm et al., 1988 ), indicating increased digestible carbohydrate bioavailability with processing. Additionally, starch gelatinization degree and reactive lysine in a canine diet increased with increasing extrusion temperatures up to 150°C compared to untreated control ( Lankhorst et al., 2007 ). Conversely, increasing time of heat treatment during canning of cat food was associated with a decrease in true ileal AA digestibility in rats ( Hendriks et al., 1999 ). Higher drying temperatures (200°C) of an extruded canine diet resulted in lower lysine, reactive lysine, reactive to total lysine ratio, linolenic acid, and linoleic acid concentrations compared to lower drying temperatures (≤160°C) in 4 mm kibbles ( Tran et al., 2011 ). These examples of processing influencing the quality and nutritional value of an ingredient or final product highlight the importance of quality control outcomes in ingredient selection and final product processing.

Processing method also influences nutritional value by affecting the moisture content of the final product. From a nutritional perspective, foods with moisture content similar to animal prey would better align with a natural pet nutrition philosophy compared to dry foods. While there is limited evidence to demonstrate a health benefit of high dietary moisture intake in dogs, there have been demonstrated effects in cats on urinary tract health and weight management. Feeding diets containing 73% moisture reduced ( P < 0.05) the calcium oxalate relative super saturation from 1.14 ± 0.21 compared with the 6 (2.29 ± 0.21) and 53% (2.06 ± 0.21) moisture diets and reduced ( P < 0.001) specific gravity from 1.036 ± 0.002 compared with the 6, 25, and 53% moisture diets (1.052–1.054 ± 0.002) while increasing ( P < 0.001) total water intake of cats to 144.7 ± 5.2 mL compared with diets containing 6, 25, or 53% moisture (98.6–104.7 ± 5.3 mL; Buckley et al., 2011 ). Another study found that ad libitum ingestion of a 40% hydrated diet compared to a dry diet with 12% moisture following weight loss caused cats to eat less (77 ± 10.8 vs. 86 ± 18.4 g/d; P < 0.05), with a trend to gain less BW (312 ± 95.9 g vs. 368 ± 120.7 g; P = 0.28), and increased their activity level ( P < 0.001; Cameron et al., 2011 ). Although these findings may be specific to the diets evaluated, given the ubiquitous nature of urinary related syndromes in cats, the potential health benefits of feeding pet food with higher moisture content (e.g., pasteurized/refrigerated, raw, frozen, or canned) that typically contain 70 to 85% moisture should be noted.

There are reports in the literature evaluating the digestibility of raw diets in feline species that have been discussed above. However, Kerr et al. (2012) evaluated the performance of extruded cat food versus a beef based diet fed either raw or cooked. These investigators found the apparent total tract digestibility to be greater ( P < 0.001) in both the raw and cooked form of the beef based diet than the extruded diet. There were no differences in apparent digestibility between the raw and cooked beef based diet. The differences observed in this study could be due to the ingredient composition as well as processing method. Given the level of ingredient processing required before extrusion, it would be difficult to design a study using ingredients in the same physical form with and without extrusion.

Processing method is also an important influencer of food safety. With respect to food processing, unpasteurized raw foods would most closely match wild prey and therefore align with a natural pet nutrition philosophy. However, there are safety concerns with the pathogenic bacteria found in many raw meats. Studies have demonstrated that raw or undercooked animal-source protein may be contaminated with a variety of pathogenic organisms, including Salmonella spp., Campylobacter spp., Clostridium spp., Escherichia coli , Listeria monocytogenes , and enterotoxigenic Staphylococcus aureus ( Freeman and Michel, 2001 ; LeJeune and Hancock, 2001 ; Joffe and Schlesinger, 2002 ; Stiver et al., 2003 ; Weese et al., 2005 ; Finley et al., 2006 ). In a cohort of 200 therapy dogs, the incidence rate of Salmonella shedding in the raw meat-fed dogs was 0.61 cases/dog–year, compared with 0.08 cases/dog–year in dogs that were not fed raw meat ( P < 0.001; Lefebvre et al., 2008 ). This poses a risk of foodborne illness to the pets eating the contaminated food and of secondary transmission to humans, especially children, older persons, and immunocompromised individuals ( LeJeune and Hancock, 2001 ; Joffe and Schlesinger, 2002 ). Given these health risks, the American Veterinary Medical Association, American Animal Hospital Association, and U.S. Food and Drug Administration have issued statements on the avoidance and safe handling practices of raw foods ( AAHA, 2011 ; AVMA, 2012a ; FDA, 2013 ). The American College of Veterinary Nutrition also has endorsed a publication on the potential risks vs. benefits of pets consuming raw meat based diets ( Freeman et al., 2013 ). Furthermore, raw food diets can pose risk for metabolic disease depending on the parts of the animal used in the diet. For example, clinical cases of dietary hyperthyroidism have been reported in dogs fed bone and raw food diets, which was reversed by feeding commercial pet food ( Kohler et al., 2012 ). To reduce safety concerns, minimal processing may be applied, such as pasteurization of raw animal products, or comprehensive microbiological testing of product may be used.

The natural segment of manufactured pet food has grown in recent years driven by consumer demand. The increased demand for these products has centered on the consumer belief that these products are of high quality and safe, made from ingredients that fit an individual's concept of natural, and provide functional health benefits. Different regulatory definitions have been described by the AAFCO and FEDIAF for natural pet food ingredients and products; however, most consumers have their own perceptions of what should be considered natural based on personal experiences, biases, or preferences. In the absence of data on the impact of natural pet food on pet health, some pet food companies target diet formulation and ingredients based on teleological reasoning that dogs and cats should eat a diet resembling that of related wild species. Many opportunities exist for research involving natural pet foods and natural diets to understand their effects on growth and performance, nutrient availability, digestibility, and product safety among other health and nutrition parameters. Future opportunities also include the integration of sustainability with natural pet foods ( Swanson et al., 2013 ). The challenge is to match consumer demand and provide natural nutrition to pets while reducing impact on the environment. With the increasing trend of anthropomorphism of pets and interest in ancestral or instinctual diets, challenges of particular interest to the natural pet food segment include competition with the human food chain and the high use of animal protein sources.

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Dogs play a key role in veterinary college’s brain cancer trial

• Marjorielee Christianson

21 May 2024

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Lucy, with her boundless puppy-like energy even at 12 years old, is more than just a pet to Susan Ketcham. She's now part of a research project that could transform the way we treat brain cancer – in both dogs and humans.

This study at Virginia Tech's Virginia-Maryland College of Veterinary Medicine explores an innovative therapy called histotripsy. It's a leap forward from traditional cancer treatments, harnessing the power of focused ultrasound to break down tumors with precision. 

When Lucy began experiencing seizures last July, Ketcham, a clinical nurse specialist, knew something more serious was the cause. The diagnosis of a brain tumor was devastating, but Ketcham was determined to explore all treatment options available. She discovered the histotripsy trial during her search and quickly reached out.

"Being in human medicine myself," said Ketcham. "I work in operating rooms and am very familiar with focused ultrasound, so I was eager to learn more."

Collaborative mission, translational impact

The trial is led by John Rossmeisl , the Dr. and Mrs. Dorsey Taylor Mahin Professor of Neurology and Neurosurgery, and Rell Parker , an iTHRIV scholar and assistant professor of neurology and neurosurgery.

Also on the team is Lauren Ruger , a postdoctoral associate in Eli Vlaisavljevich’s lab in the Department of Biomedical Engineering and Mechanics where histotripsy is extensively researched. She's adapting the equipment used in the study to make it safe and effective for their canine patients.

“I had wanted to be a veterinarian when I was younger before deciding to become an engineer,” said Ruger. “So I love having the opportunity to use my skills as an engineer to influence animal health.”

This trial offers an essential stepping stone in developing less invasive treatment options for brain cancer and is supported by the Focused Ultrasound Foundation and the Canine Health Foundation, highlighting the widespread commitment to results across species.

Hope for histotripsy

“Histotripsy uses acoustic energy, or sound waves, to modify tissue,” said Rossmeisl. “The intent is to cause a mechanical disruption of the tissue – killing cancer cells." 

The technology was developed by researchers at the University of Michigan in the early 2000s. 

The advantage is precision. Unlike traditional surgery, histotripsy can focus its impact on the tumor itself. "We could potentially treat these hard-to-reach brain tumors we normally can’t access with traditional surgery,” said Parker.

"We really don't have great ways to treat brain cancers in patients,” said Rossmeisl. “Even when you do surgery, radiation, or chemotherapy alone or in combination, usually, you're not creating a cure." 

However, there is hope that histotripsy could be used to activate the body’s immune response and have it attack cancer cells, called the abscopal effect. Clinicians also see fewer side effects compared to other traditional treatment options.

About the procedure

The study currently still involves surgery to access brain tumors, which is the gold standard of care for this type of diagnosis. This allows for direct targeting of the tumor with the histotripsy transducer, delivering focused sound waves for precise treatment.

“When we do the surgery, we can see the tumor via ultrasound,” Parker said. “We can see that we're treating the appropriate cells, and then we also do an MRI to ensure that we've targeted the right area.” 

After the histotripsy treatment, surgeons carefully remove the treated tumor. This tissue provides crucial insights into the technique's effect on cancer cells, helping researchers refine the technology for future applications.

“It gives us the advantage of being able to look at the tissue that's been broken down to ensure that we're getting the desired effect from the histotripsy therapy,” said Ruger.

While the science is complex, the stories of patients like Lucy are reminders of why this work matters. "The recovery was quick, the incision was small," Ketcham said. "She's back to her playful self, and knowing she's helped advance science and technology is amazing."

Parker added: "We’re happy to say that the procedure has been safe for our patients, and we've been able to treat them appropriately."

Looking toward the future of treatment

A long-term goal of this study is to develop a completely non-invasive treatment that would eliminate the need for surgery. The team is in the early stages of exploring this possibility, citing several challenges to realizing a solution that could be widely available. 

“Transmitting ultrasound through the bones of the skull is very difficult,” said Ruger. “And then accurately focusing it in only the areas you want to treat with histotripsy adds another layer of complexity.”

However, the technique can be successfully applied through the skin, explained Rossmeisl. "That would be a paradigm changer. We would make surgically treating tumors a lot more widely available.”

“Even though I love neurosurgery,” he added. “Anytime I can do something that doesn't require putting the patient through a complex and invasive procedure and get them home quicker, that's always a good thing.”

To learn more about eligibility criteria or enroll your dog in the trial, please contact John Rossmeisl at [email protected] or 540-231-4621 or Mindy Quigley, clinical trials coordinator at  [email protected] or 540-231-1363.  

Andrew Mann

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Original research article, assisting decision-making on age of neutering for 35 breeds of dogs: associated joint disorders, cancers, and urinary incontinence.

• 1 Department of Anatomy, Physiology and Cell Biology, School of Veterinary Medicine, University of California, Davis, Davis, CA, United States
• 2 Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, Davis, CA, United States
• 3 Department of Statistics, University of California, Davis, Davis, CA, United States

Neutering (including spaying) of male and female dogs in the first year after birth has become routine in the U.S. and much of Europe, but recent research reveals that for some dog breeds, neutering may be associated with increased risks of debilitating joint disorders and some cancers, complicating pet owners' decisions on neutering. The joint disorders include hip dysplasia, cranial cruciate ligament tear or rupture, and elbow dysplasia. The cancers include lymphoma, mast cell tumor, hemangiosarcoma, and osteosarcoma. In previous studies on the Golden Retriever, Labrador Retriever and German Shepherd Dog, neutering before a year of age was associated with increased risks of one or more joint disorders, 2–4 times that of intact dogs. The increase was particularly seen with dogs neutered by 6 months of age. In female Golden Retrievers, there was an increase in one or more of the cancers followed to about 2–4 times that of intact females with neutering at any age. The goal of the present study was to expand and use the same data collection and analyses to cover an additional 29 breeds, plus three varieties of Poodles. There were major breed differences in vulnerability to neutering, both with regard to joint disorders and cancers. In most cases, the caregiver can choose the age of neutering without increasing the risks of these joint disorders or cancers. Small-dog breeds seemed to have no increased risks of joint disorders associated with neutering, and in only two small breeds (Boston Terrier and Shih Tzu) was there a significant increase in cancers. To assist pet owners and veterinarians in deciding on the age of neutering a specific dog, guidelines that avoid increasing the risks of a dog acquiring these joint disorders or cancers are laid out for neutering ages on a breed-by-breed and sex basis.

Introduction

In the U.S. and much of Europe, the practice of neutering male and spaying female dogs (herein both referred to as neutering) has become routine ( 1 ) and is increasingly being performed at, or before, 6 months of age. At the same time, several investigations have revealed that joint disorders and some cancers may increase in association with neutering of males and/or females. For example, in studies that did not focus on specific breeds or ages of neutering, one found that hip dysplasia and cranial cruciate ligament tears or ruptures were significantly more likely in neutered than intact males and females ( 2 ). Another study found that neutering was associated with a 3-fold increase in excessive tibial plateau angle ( 3 ), which is a risk factor for development of cranial cruciate ligament tears or rupture. Neutering is reported to be a risk factor for canine intervertebral disc herniation in Dachshunds ( 4 ). Certain cancers are also known to be more likely in neutered than intact dogs. The occurrence of lymphoma was found to be higher in spayed than intact females ( 5 ), as was the occurrence of mast cell tumors ( 6 ) and hemangiosarcoma ( 7 ). A study of over 40,000 dogs utilizing the Veterinary Medical Database found that neutered males and females were more likely to die of cancer than intact dogs ( 8 ). A recent finding was that the absence of estrogen from spaying females was associated with accelerated brain aging ( 9 ). Another recent report from the Golden Retriever Lifetime Project is that neutering at <6 months increases the risk of cranial cruciate ligament injury ( 10 ). Most of the studies cited above offer no useful clinical information or guidelines with regard to the various diseases that may occur in association with neutering in a specific breed.

In an attempt to address the absence of breed-specific information on joint disorders and cancers associated with neutering, we undertook a project focusing on various specific breeds using data collection and analyses with our extensive veterinary hospital database where the same diagnostic criteria could be applied to all breeds. We started with popular breeds well-represented in the database, initially with the Golden Retriever ( 11 , 12 ), Labrador Retriever ( 12 ) and German Shepherd Dog ( 13 ). The joint disorders examined included cranial cruciate ligament tears or rupture (CCL), hip dysplasia (HD) and elbow dysplasia (ED). The cancers examined, which previous studies found could be affected by neutering, were lymphoma/lymphosarcoma (LSA), hemangiosarcoma (HSA), mast cell tumors (MCT), and osteosarcoma (OSA).

In the Labrador Retrievers, Golden Retrievers, and German Shepherd Dogs, there was an increase in the incidence of one or more of the joint disorders with neutering in the first year in males and females to 2–4 times >3–5% incidence in intact dogs. In female Golden Retrievers, neutering at any age was associated with an occurrence of one or more of the cancers followed to 2–4 times higher than the 5 percent incidence in intact females. But in male Golden Retrievers, and in male and female Labrador Retrievers and German Shepherd Dogs, there was no evident increase in cancers above that of the dogs left intact. Preliminary analyses from some small-dog breeds revealed no apparent increased risks of joint disorders with neutering. Thus, the research that had been undertaken revealed a wide range of breed-specific differences in disease vulnerability to neutering.

The purpose of this study was to analyze, in a variety of additional breeds, the increased risks, if any, of the above specified joint disorders and cancers associated with neutering male and female dogs at various ages, so as to increase the information available to pet owners and veterinarians for consideration when making decisions regarding neutering specific dogs. We added 29 new breeds to the study, separating three varieties of Poodles, for a total of 32 breed groups (referred to as breeds); this made a total of 35 breeds with the Goldens, Labs and German Shepherds included. The goal was to use the same veterinary hospital database and diagnostic criteria for the diseases as was used with the published studies on the retrievers and German Shepherds so as to allow for direct comparisons among various breeds. The primary purpose was to offer readers some evidence-based information on breed-specific differences with vulnerability to neutering, including suggested guidelines for neutering ages to avoid increasing long-term health risks of neutering, if any. A secondary, unforeseen, purpose was to document breed-specific differences in the increases in some cancers associated with removal of gonadal hormones, as an area for possible research on genetic aspects of cancer occurrence.

Ethics Statement

Hospital records of the Veterinary Medical Teaching Hospital (VMTH) provided the retrospective dataset used. In conformity with the campus policy, faculty of the University of California-Davis, School of Veterinary Medicine, are allowed use of the record system for research purposes. No animal care and use committee approval was required, and strict confidentiality of the owners and their dogs was maintained.

Subjects Breed Categories

In addition to the Golden Retriever, Labrador Retriever, and German Shepherd Dog, the other breeds chosen for this project included those most frequently occurring in the database and those chosen to obtain a sampling of giant breeds or small-dog breeds. The final list of 35 (including three varieties of Poodle) represented in the present study are, alphabetically, the: Australian Cattle Dog, Australian Shepherd, Beagle, Bernese Mountain Dog, Border Collie, Boston Terrier, Boxer, Bulldog, Cavalier King Charles Spaniel, Chihuahua, Cocker Spaniel, Collie, Corgi (Pembroke and Cardigan combined), Dachshund, Doberman Pinscher, English Springer Spaniel, German Shepherd Dog, Golden Retriever, Great Dane, Irish Wolfhound, Jack Russell Terrier, Labrador Retriever, Maltese, Miniature Schnauzer, Pomeranian, Poodle-Miniature, Poodle-Standard, Poodle-Toy, Pug, Rottweiler, Saint Bernard, Shetland Sheepdog, Shih Tzu, West Highland White Terrier, and Yorkshire Terrier.

Study Parameters

The present study examined the occurrence in both sexes of the joint disorders: HD, CCL and ED. Also examined in both sexes were the cancers LSA, HSA, MCT, and OSA, because these had been shown in some multi-breed studies to be increased in risks with neutering. In addition, mammary cancer (MC), pyometra (PYO), and urinary incontinence (UI) were examined in female dogs. Of interest was the possible association of early neutering and the occurrence of intervertebral disc disorders (IDD) in the Corgi and Dachshund, two breeds known to be at risk for these diseases. All of the above diseases were examined with regard to dogs neutered in one of the age periods of: <6 mo., 6–11 mo., 1 year (12 to <24 mo.) or 2–8 years, or left intact. The diseases were tracked until the dogs were last seen at the hospital, or through 11 years of age, if seen past their 12th birthday.

Mammary cancer is a late occurring cancer with the median age of diagnosis being 10.1 years in one study ( 14 ). Tracking cancers through 11 years of age would be presumably sufficient to catch most cases of MC if the case record had information extending to that age. However, most case records did not extend to that age. As an additional point of comparison, percentages of MC occurrence were looked at in just females tracked through 8 years of age or beyond, including diagnosed MC cases beyond the 12th birthday cut-off, which was the cut-off used for all other data.

Data Collection and Presentation

The computerized hospital record system of the VMTH provided the dataset. The hospital, with currently over 50,000 cases admitted per year, is a secondary and tertiary facility as well as being a primary care facility. The statistical evaluations, with standardized diagnostic criteria applied to various diseases and taking into account sex and different ages of neutering, required a large database with a computerized record system. The study focused on proportional differences in disease occurrences between the neuter age groups and intact dogs of the same breed and sex.

The study period represented 15 years of data for most breeds. The inclusion criteria were date of birth, age at neutering (if neutered), and age of diagnosis or onset of clinical signs for diseases of interest. As mentioned, age at neutering was designated as <6 mo., 6–11 mo., 1 year (12 to <24 mo.), and 2–8 years (2 to <9 years). The term “early neutering” is sometimes used below to refer to neutering in the first year, combining cases for both the <6 mo. and 6–11 mo. neuter periods. For MC, PYO, and UI, only females were examined. While UI does occur in males, it is predominantly an issue in females.

For all neutered dogs that developed a disease of interest, records were examined to confirm that the dog was neutered prior to the diagnosis or signs of the disease. If the dog developed signs of the disease prior to neutering, the dog was considered intact for analysis of that disease. However, for any disease that occurred after neutering, the dog was considered neutered for analysis of that disease. For any disease of interest that occurred before 12 months of age, the dog was removed from that disease analysis, but included in analyses of other diseases. Therefore, the number of cases for various diseases varied in the analyses for different disease occurrences.

The age at neutering was sometimes not included in the hospital records, so telephone calls to the referring veterinarians were made to obtain the neutering dates or ages. Nonetheless, there were many neutered dogs where age at neutering was not available from the VMTH records or the referring veterinarian, so these dogs were excluded from the study. Of course, this was not an issue with the sample of intact dogs, so there were proportionately more intact cases in the final dataset for each breed than would be expected in the general population. However, the proportion of dogs with a disease, whether intact or neutered, was not affected by the overrepresentation of intact dogs in the database.

The criteria for disease diagnoses were the same as in previous studies on the retrievers and German Shepherd Dog ( 11 – 13 ). A dog was considered as having a disease of interest if the diagnosis was made at the VMTH, or by a referring veterinarian and later confirmed at the VMTH. For joint disorders (HD, ED, and/or CCL), dogs typically presented with signs of lameness, difficulty in moving, and/or joint pain. The diagnosis was confirmed by orthopedic examination, radiographic evidence, and/or surgery. In Dachshunds and Corgis, where intervertebral disc disorders (IDD) is a concern, the diagnosis included herniation, rupture, extrusion, protrusion, fracture, compression, stenosis, or spinal cord injury. For cancers (LSA, HSA, MCT, OSA, MC), the diagnosis was based on the presence of a tissue mass, lumps on the skin or enlarged lymph nodes, and confirmed by chemical panels, appropriate blood cell analyses, imaging, histopathology, and/or cytology. PYO was confirmed by ultrasonic evidence and/or post-surgically after removal of the uterus. UI was confirmed by clinical signs of abnormally frequent urination, urinalyses and exclusion of urinary tract infection and/or other disease. If a diagnosis was listed in the record as “suspected” based on some clinical signs but not confirmed, the case was excluded from the analysis for that specific disease, but the dog was included in other disease analyses.

Although body condition scores have been reported to be a factor in the occurrence of joint disorders ( 3 , 15 ), our previous studies on the retrievers and German Shepherd Dog found no significant relationship when body condition scores were compared between dogs with and without a joint disorder. Therefore, in the current paper the body condition score is not reported for each breed.

Statistical Analyses

Survival analysis was used to test for differences with respect to the hazard of a disease in the neutered and intact groups, while adjusting for the differences in time at risk for a disease. The groups were initially compared using a Kaplan Meier life table analysis. Post-hoc comparisons among the subgroups were based on least squares means of the hazard within each subgroup. For comparisons where the Kaplan Meier test showed significance at the p <0.05 level, both the log-rank and Wilcoxon tests were used for further analyses. Because joint disorders are expected to be seen at a similar risk throughout a dog's lifespan, regardless of age, the log-rank test was used initially for the joint disorders. If the log-rank test did not show significance but the Wilcoxon test did for joint disorders, the Wilcoxon test result was reported with significance level and an asterisk. The reverse rule of thumb was used with cancers where the first test examined was the Wilcoxon test, since the risk of cancer is expected to be higher in older dogs. If the Wilcoxon test did not show significance but the log-rank test did for cancers, the log-rank test result was reported with significance level and an asterisk. For all statistical tests, the two-tailed statistical level of significance was set at p <0.05 and reported as either p < .05 or p <0.01. Each breed was analyzed separately, and there were no statistical comparisons between breeds. However, the overall findings with each breed allow for some general comparisons.

Data Presentation

For each breed represented on a separate page in Appendix 1 , the numbers of intact and neutered males and females are given. In the tables, the percentage of dogs with each of the diseases and the percentage having at least one of the joint disorders and at least one of the cancers (except MC) was calculated for intact males and intact females as well as those neutered at various age ranges. Statistical analyses compared the occurrences of joint disorders and cancers between each neuter period and intact dogs. If the comparison was significant at either the p <0.05 or p <0.01 level, the data were bolded and the p -value was given. The detailed datasets are available online (Figshare, doi: 10.6084/m9.figshare.7231010 ). Three breeds for which findings have been previously published (Golden Retriever, Labrador Retriever, German Shepherd Dog) are included to present an overall picture in the same Appendix 1 . The data for these three breeds were expanded through 11 years of age, to provide continuity among breeds and diseases.

For each breed, a short paragraph summarizes the main findings on joint disorders (HD, CCL, ED), cancers (LSA, HSA, MCT, OSA) for both males and females, and MC, PYO and UI for females. For Dachshunds and Corgis, the occurrence of IDD is listed for both sexes. Survival analyses were not done on IDD occurrence because the condition represented so many different disease diagnoses. Also included in the breed summary information is a suggested guideline for neutering age for males and females to avoid increasing the risks of a disease under consideration. When there was no noticeable occurrence of an increase in joint disorders or cancers with neutering, the guideline statement was made that those wishing to neuter should decide on the appropriate age (or briefly stated as choice in Table 1 ). When neutering at <6 months was associated with an increased disease risk but no increased risk was evident with neutering beyond 6 months, the default recommended guideline was neutering beyond, 6 months.

Table 1 . Suggested Guidelines by Breed for Age of Neutering.

The breed-by-breed findings are presented in four different formats. One format, seen in this section below, is a short paragraph for each breed. The occurrence of the joint disorders and the cancers followed is reported for the intact and neutered dogs, and the increase in the two disease types over that of the intact dogs, if significant, is reported. Other findings are also mentioned if appropriate, such as IDD occurrence in Dachshunds and Corgis. A second format, represented in Table 1 , is a very brief summary of spaying and neutering guidelines based on findings regarding joint disorders and cancers for each breed, allowing the reader to quickly scroll through the various breeds. In the third format, the data-based findings, with statistical notations for each breed, are reported in Appendix 1 . In the fourth format, the raw data allowing the reader to perform their own calculations, if desirable, is available in Figshare.

The mean age of last entry was calculated for intact and neutered males and females for each breed and presented in Appendix 2 . Across all breeds the mean age of last entry in the record for neutered males was 5.5 years (range 3.71–6.54), for neutered females 5.7 years (range 4.21–6.97), for intact males 4.9 (range 4.15–7.11), and intact females 4.7 (range 3.41–6.32). Upon perusal of the data, it is evident that the mean age of data entry for intact dogs was younger than that of neutered dogs, especially for females, where there is disparity of almost 1 year. To address the issue of whether the lower age of last entry for intact dogs could have resulted in a lower rate of disease occurrence in intact dogs in either joint disorders or cancers, we examined data of dogs where the last entry was at 8 years or beyond. We looked at three breeds with the largest databases (Golden Retrievers, Labrador Retrievers, and German Shepherd Dogs) and where there were significant differences in disease diagnoses between early neutered and intact dogs. Using these parameters, the occurrences of joint disorders in Golden Retrievers for those neutered at ≤ 6mo. vs. intact, in males, there was a 6-fold difference (18% vs. 3%) and in females 3-fold (25 vs. 8%). For male Labrador Retrievers, the figures were 22 vs. 8% and in females 33 vs. 10%. For male German Shepherd Dogs, the figures were 33 vs. 2% and for females, 29 vs. 9%. For cancers in female Goldens, the figures were 26 vs. 14%. The incidence figures, although not sufficient for meaningful statistical analyses, are consistent with the larger database where all ages are included. Thus, while the age of the last visit is a limitation for analyses on late-occurring cancers and joint disorders, the examples chosen for dogs seen at the age of 8 years or beyond are consistent with the overall results presented here; these results appear to represent what would be seen in the general situation.

General Findings

Looking at the occurrences of these joint disorders and cancers, it is clear that most breeds are unaffected for these diseases by age of neutering. Vulnerability to joint disorders associated with neutering is generally related to body size. Small-dog breeds – Boston Terrier, Cavalier King Charles Spaniel, Chihuahua, Corgi, Dachshund, Maltese, Pomeranian, Poodle-Toy, Pug, Shih Tzu, Yorkshire Terrier – do not appear to have an increased risk in joint disorders with neutering compared to the breeds of larger size. However, in the breeds of larger body size there were differences among the breeds with the two giant breeds – Great Danes and Irish Wolfhounds – showing no indication of increase in one or more joint disorders with neutering at any age.

Although the occurrence of MC was tracked, the female mean age at the last hospital visit for all breeds ended short of the reported, late-onset mean age of MC occurrence in intact female dogs. Thus, the low occurrence of MC in intact females (typically under 6 percent) cannot be expected to represent the actual incidence over a female's lifetime. When the percentage of MC was calculated for only those dogs seen through 8 years of age or older (including cases diagnosed past the 12th birthday), the results did not appear appreciably different than the percentages seen using the study age range. However, the number of dogs seen through age 8 or beyond was fairly small, so the analysis results might change with an increased sample size of these older dogs.

The following are brief summaries for each of the breeds along with suggested guidelines for age of neutering. See Appendix 1 for the complete data set, including statistical analyses for each breed.

Australian Cattle Dog

The study population was 61 intact males, 58 neutered males, 48 intact females, and 70 spayed females for a total of 237 cases. In this sample, 5 percent of intact males and 2 percent of intact females were diagnosed with one or more joint disorders. Neutering males was not associated with any increased risk in joint disorders, but there was an association with spaying females at <6 mo. where the risk of a joint disorder increased to 15 percent ( p <0.05). The occurrence of cancers was low for males and females left intact (0 and 3 percent, respectively). There were no evident occurrences of the cancers in dogs neutered at various ages. The occurrence of MC in intact females was 6 percent and in those spayed at 2–8 years, 6 percent. For females left intact, 4 percent were reported with PYO. UI was not reported in any of the spayed or intact females. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males, those wishing to neuter should decide on the appropriate age. In females, the increased risk of a joint disorder with spaying occurred only at the <6 mo. range, so the suggested guideline is spaying at, or beyond, 6 months.

Australian Shepherd

The study population was 93 intact males, 135 neutered males, 76 intact females, and 136 spayed females for a total of 440 cases. In this sample, 3 percent of intact males and 4 percent of intact females were diagnosed with one or more joint disorders. Neutering males and females was not associated with any evident increased risk in joint disorders. The occurrence of cancers was 9 percent for intact males and, in contrast, only about 1 percent for intact females. Neutering males did not appear to be associated with an overall increased risk of cancers above the rather high level of intact males. However, spaying females at 6–11 mo. and at 2–8 years was associated with a 7–8 percent risk in cancers which may have reached significance with a larger sample size. The occurrence of MC in intact females was zero, but was 8 percent in females spayed at 2–8 years. For females left intact, 5 percent were reported with PYO. UI was reported in just 1 percent of early-spayed females. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males, those wishing to neuter should decide on the appropriate age. The guideline for females is the same while also maintaining vigilance for the cancers which may be associated with spaying beyond 6 months, or else leaving the female intact and being vigilant for MC.

The study population was 42 intact males, 82 neutered males, 45 intact females and 87 spayed females for a total of 256 cases. Just 2 percent of intact males were diagnosed with one or more joint disorders, but with neutering at 6–11 mo. joint disorders increased 7-fold to 15 percent, which may have reached significance with a larger sample size. None of the females left intact or spayed had a joint disorder. None of the intact males or females was diagnosed with any of the cancers followed. There was no evident increased occurrence of cancers in neutered males and females. There was no occurrence of MC in intact or late-spayed females. There was 1 case of PYO in intact females (2 percent). UI was reported in only 2 percent of early-spayed females.

For males, in light of a possible increase in joint disorders for those neutered at 6–11 mo., the suggested guideline is to delay neutering males until beyond a year of age. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered females, those wishing to neuter should decide on the appropriate age.

Bernese Mountain Dog

The study population was 59 intact males, 74 neutered males, 37 intact females, and 65 spayed females for a total of 235 cases. The percentage of intact males with at least one joint disorder was 4 percent and for intact females, 11 percent. Neutering males any time prior to 2 years of age was associated with a significant increase in at least one joint disorder to 23–24%, about a 6-fold increase over intact males ( p <0.01). Spaying females before 6 mo. increased the likelihood of a joint disorder to over 3-fold that of intact females, but this did not reach significance. The occurrence of one or more of the cancers followed was 9 percent for both intact males and intact females. There was no evident increase in cancer risk in males related to neutering, but with females, spaying at <6 mo. was associated with a 2-fold increase above that of intact females. There was no occurrence of MC in females, whether left intact or neutered at any age, and a 5 percent occurrence of PYO in intact females. There was no occurrence of UI in intact or spayed females. Reflecting the increased risk of joint disorders for males, the suggested guideline for neutering males is delaying neutering until well-beyond 2 years. Lacking a significant occurrence of increased joint disorders or cancers in neutered females, those wishing to neuter should decide on the appropriate age.

Border Collie

The study population was 105 intact males, 85 neutered males, 88 intact females, and 121 spayed females for a total of 399 cases. In this sample 2–3% of intact males and females were diagnosed with one or more joint disorders, and neutering males and females was not associated with any evident increased risk in joint disorders. The occurrence of one or more of the cancers followed in intact males was 2 percent and none for females left intact. For males, there was a significant increased risk in one or more of the cancers to 13 percent with neutering at 6–11 mo. ( p <0.05), and for females there was a significant increase in the cancers to 11 percent with spaying at 6–11 mo. ( p <0.01). The occurrence of MC in intact females was just 1 percent, and for PYO, 4 percent. UI was reported in just one spayed female. The suggested guideline for neutering, given the significant risk of cancers, is holding off neutering of both sexes until beyond a year of age.

Boston Terrier

The study population was 75 intact males, 67 neutered males, 54 intact females, and 96 spayed females for a total of 291 cases. None of the intact or neutered males or females was diagnosed with one or more joint disorders. For cancers, the story is a bit different in that 5 percent of intact males were diagnosed with one or more cancers and 10 percent of males neutered at <6 mo., and 12 percent of males neutered at 6–11mo. had cancers ( p <0.01, the two neuter periods combined). For females, 2 percent of intact females had one or more of the cancers and with spaying, there was no evident increase of cancers. The occurrence of MC in intact females was 2 percent and for PYO, 7 percent. UI was 2 percent in early-spayed females. In light of the significant increase in cancers in males with neutering through 11 months of age, the suggested guideline for males is delaying neutering to beyond a year of age. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered females, those wishing to neuter should decide on the appropriate age.

The study population was 220 intact males, 203 neutered males, 128 intact females, and 210 spayed females, for a sample size of 761 cases. Males and females left intact had just a 2 percent occurrence of joint disorders, with neutered males and females showing no apparent increase in this measure. The occurrence of one or more of the cancers followed in intact males was 17 percent, and for intact females, 11 percent. Neutering males before 2 years significantly raised the risk of a cancer over that of intact males to 32 percent ( p <0.01). The same pattern of increase in cancers was seen in spaying females with up to 20 percent of females having one or more of the cancers with spaying done before 2 years, an increase that was not significant, but with an expanded database may have been. There was no occurrence of MC in intact females. PYO was diagnosed in 2 percent of intact females. Just 1 percent of spayed females were diagnosed with UI. Given the risk of increased cancers, the suggested guideline for both sexes is to delay neutering until beyond 2 years of age.

The study population was 198 intact males, 156 neutered males, 90 intact females, and 114 spayed females for a sample of 558 cases. The occurrence of joint disorders in intact males was 7 percent and 5 percent in intact females. Neutering at <6 mo. raised the incidence to 15 percent for males and to 18 percent for females, which did not reach significance for either. The cancers followed occurred at the 6 to 7 percent level in intact males and females. There were no significant increases above this with neutering males or females. The occurrence of MC in females left intact was 1 percent and 2 percent with spaying at 2–8 years. There was a 2 percent occurrence of PYO in intact females and no UI in early spayed females. Lacking a significant occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age, but some people may wish to be cautious in view of the possible apparent risk in joint disorders.

Cavalier King Charles Spaniel

The study population was 51 intact males, 72 neutered males, 87 intact females, and 76 spayed females, for a sample size of 286 cases. For males and females left intact, the occurrences of one or more joint disorders were just 4 and 1 percent, respectively, and for both sexes neutering was not associated with any increase in this measure. The occurrences of cancers in intact males were 2 percent and zero for intact females. For both sexes neutering was not associated with any increase in this measure. The occurrence of MC in females left intact was zero. The occurrence of PYO was 2 percent in intact females. There was no occurrence of UI in spayed females. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age.

The study population was 261 intact males, 189 neutered males, 298 intact females, and 289 spayed females for a total sample of 1,037 cases. For both males and females, neither those left intact, nor those neutered at any age had a noteworthy occurrence of a joint disorder. The cancers followed in both intact and neutered males and females were <5 percent with no evident increase with neutering at any age. The occurrence of MC in females left intact was 1 percent, and in females neutered at 2–8 mo., 4 percent. In intact females, PYO was diagnosed in 2 percent. There was no UI diagnosed in any of the spayed females. Lacking a noticeable occurrence of increased joint disorders or cancers with neutering in either sex, those wishing to neuter should decide on the appropriate age.

Cocker Spaniel

The study population was 71 intact males, 112 neutered males, 61 intact females, and 127 spayed females, for a sample size of 369 cases. The occurrence of at least one joint disorder was seen in 1 to 3 percent of the intact males and females. Neutering males at <6 mo. was associated with a significant increase of this measure to 11 percent ( p <0.01). Spaying females was not associated with an increase in joint disorders. The occurrence of one or more of the cancers followed was 6 percent in intact males with no increase with neutering. Although there was no occurrence of cancers in intact females, this measure rose significantly to 17 percent in females spayed between 1 and 2 years of age ( p <0.01), entirely due to MCT. For females left intact, 11 percent were diagnosed with MC and 5 percent with PYO. None of the spayed females developed UI. The suggested guideline for males is neutering beyond 6 months of age. Given the increased cancer risk for females spayed at a year of age, the suggested guideline is delaying spaying until beyond 2 years of age.

The study population was 29 intact males, 26 neutered males, 24 intact females, and 37 spayed females, for a sample size of 116 cases. The occurrence of at least one joint disorder was seen in 7 percent of the intact males and in none of the intact females. None of the neutered males or females had a noteworthy occurrence of a joint disorder. The occurrence of one or more of the cancers followed was 11 percent for intact males and none for the intact females. There was no evident increase of cancers in males with neutering, and in females, there was an increase of cancer to 40 percent in those spayed at <6 mo., which may have reached significance with a larger sample size. For females left intact, 4 percent were diagnosed with MC, and 16 percent were diagnosed with PYO. Of females spayed at 6–11 mo., 13 percent had UI. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males, those wishing to neuter a male should decide on the appropriate age. For females, given the apparent risks of cancers with spaying at <6 mo. and UI with spaying at 6–11 mo., the guideline is to delay spaying until the female is a year old.

Corgi (Welsh), Pembroke and Cardigan

The study population was 42 intact males, 78 neutered males, 50 intact females, and 70 spayed females, for a total sample size of 240 cases. Although these are two breeds, they vary only a little in size, so these two breeds are combined for statistical analyses and display of data. The occurrence of at least one joint disorder in intact males was 5 percent and for intact females 6 percent. There was no significant increase in this measure in males or females with neutering. This is one of the breeds where intervertebral disc disorders are a concern, and in 3 percent of intact males and 8 percent of intact females, IDD was reported. In males neutered before 6 months, the occurrence of IDD reached 18 percent, and in females there was no increase with neutering. The occurrence of one or more of the cancers followed was 5 percent in intact males and 6 percent in intact females. In neutered males and females, there was no evident increase in cancers. For females left intact, the occurrence of MC was 8 percent, and there was zero occurrence of PYO. There was no diagnosis of UI in spayed females. The suggested guideline for age of neutering for males, given the increase in IDD with neutering at <6 mo., is beyond 6 months. Lacking a noticeable occurrence of increased joint disorders, IDD, or cancers with neutering females, those wishing to neuter a female should decide on the appropriate age.

The study population was 177 intact males, 170 neutered males, 99 intact females, and 212 spayed females, for a total sample size of 658 cases. Joint disorders were basically absent in males and females, left intact or neutered. This is a breed plagued by intervertebral disc disorders, and in this sample 53 percent of intact males and 38 percent of intact females were diagnosed with a form of IDD. There was no evident increase in this measure with neutering of males or females. The occurrence of the cancers followed was <1% in both intact males and females, with no indication of an increased risk with neutering. For females left intact, the occurrence of MC was 1 percent and for PYO, 4 percent. None of the spayed females developed UI. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age.

Doberman Pinscher

The study population was 109 intact males, 91 neutered males, 53 intact females, and 108 spayed females, for a sample size of 358 cases. The percentage of intact males with at least one joint disorder was 2 percent and 0 percent for intact females. There was no evident increase in this measure with neutering males. For females, spaying within 11 months resulted in an increase in joint disorders of 11 percent, which did not reach significance. The occurrence of one or more of the cancers followed for both intact males and intact females was 2 percent. In neutered males at the 1 year and 2–8 year periods, there was a non-significant increase in occurrence of cancers to 6 percent and 13 percent, respectively. For females, there was no noteworthy increase in cancers with spaying at any time. The occurrence of MC in females left intact was 2 percent and 4 percent for those spayed at 2–8 years. There was a 7 percent occurrence of PYO in intact females. UI was a significant risk in females spayed at any age up to 2 years, ranging from 25 percent in the females spayed at <6 mo. ( p <0.01) to 19 percent for those spayed between 1 and 2 years ( p <0.05). The suggested guideline, based on fragmentary results, for males is to leave the male intact or neuter before 1 year of age to avoid the possible increased risk of cancers seen in those neutered beyond a year of age. For females, the suggested guideline, also based on limited data, given the risk of UI in early spayed females, and the possible increased risk of a joint disorder, is to consider delaying spaying until beyond 2 years of age.

English Springer Spaniel

The study population was 52 intact males, 57 neutered males, 37 intact females, and 66 spayed females for a total sample of 212 cases. In males and females left intact, the occurrence of one or more joint disorders was 5 and 8 percent, respectively. Among males and females neutered at various ages, there were no noteworthy increases in joint disorders. The cancers followed occurred in the intact males and females at a 6 percent level, and neutering at any age was not associated with any evident increase in this measure in either sex. In intact females, MC was diagnosed in 6 percent, and for those spayed at 2–8 years, 15 percent. PYO was not reported in any of the intact females. Spaying females at 6–11 mo. was associated with a 13 percent occurrence of UI, which may have reached significance with a larger sample size. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males, those wishing to neuter should decide on the appropriate age. For females, given the increased risk of UI in those spayed before 1 year, the suggested guideline is to delay spaying until a year of age.

German Shepherd Dog

The study population was 514 intact males, 272 neutered males, 173 intact females, and 298 spayed females for a total of 1,257 cases. In males and females left intact, the occurrence of one or more joint disorders was 6 and 5 percent, respectively. Neutering males at <6 mo., 6–11 mo. and 1–2 years was associated with increased risks of this measure to 19, 18 and 9 percent, respectively ( p <0.01). Spaying females at <6 mo. and 6–11 mo. was associated with a 20 and 15 percent level of increased risk ( p <0.01), and spaying at 1–2 years with a 5 percent risk level ( p <0.05). The occurrence of one or more of the cancers followed for intact males and females was 3 percent and 2 percent, respectively. Neutering at the various ages was not associated with any appreciable increased risk in cancers followed. The occurrence of MC in intact females was 5 percent and for those spayed at 2–8 years, 6 percent. Of intact females, 3 percent were reported with PYO. UI ranged up to 9 percent for females spayed from <6 mo. through 1 year of age ( p <0.05–0.01). The suggested guideline for males, given the risks of joint disorders, is delaying neutering until over 2 years of age. For females, with the same joint issues as males plus the risks of UI, the suggested guideline is delaying spaying until over 2 years of age.

Golden Retriever

The study population was 318 intact males, 365 neutered males, 190 intact females, and 374 spayed females for a total of 1,247 cases. In intact males and females, the level of occurrence of one or more joint disorders was 5 percent and 4 percent, respectively. Neutering males at <6 mo. and at 6–11 mo. was associated with risks of 25 percent and 11 percent, respectively ( p <0.01). In females, spaying at <6 mo. and at 6–11 mo. was associated with risks of 18 percent and 11 percent ( p <0.01, when combined). The occurrence of one or more of the cancers followed in intact males was a high 15 percent and for intact females 5 percent. Neutering males at <6 mo. and at 6–11 mo. was associated with increased risks of cancers to 19 and 16 percent, respectively ( p <0.01). Spaying females at <6 mo. and at 6–11 mo., was associated with increases in cancers to 11 and 17 percent, respectively ( p <0.05, when combined) and spaying at 1 year and at 2–8 years was associated with increased risks of 14 percent ( p <0.01, when combined). The occurrence of MC in intact females was 1 percent and for those spayed at 2–8 years, 4 percent. For females left intact, 4 percent were reported with PYO. No cases of UI were reported in females spayed at any age. The suggested guideline for males, based on the increased risks of joint disorders and cancers, is delaying neutering until beyond a year of age. The suggested guideline for females, based on the increased occurrence of cancers at all spaying ages, is leaving the female intact or spaying at one year and remaining vigilant for the cancers.

The study population was 90 intact males, 103 neutered males, 69 intact females, and 91 spayed females for a total sample of 353 cases. This is a giant breed where one might expect a high risk of joint disorders. However, both intact males and females have low levels of joint disorders, just 1 and 2 percent, respectively. For both males and females, there was no evident increase in this measure with neutering. The occurrence of one or more of the cancers followed in intact males was 6 percent and for intact females, 3 percent. There was no evident increase in this measure of cancers with neutering in either sex. In intact females, MC was diagnosed in just 2 percent and PYO in 6 percent. In early-spayed females, no UI was reported. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age. However, given the large body size, and physiology of late musculoskeletal development, neutering well-beyond year 1 should be considered.

Irish Wolfhound

The study population was 30 intact males, 19 neutered males, 21 intact females, and 16 spayed females for a total of 86 cases. Even with the small number of cases, this breed was chosen for analyses because of the large body size: challenging the Great Dane for height, and where one might expect an increased risk of joint disorders. In this sample, 7 percent of intact males and none of the intact females had a joint disorder. No joint disorders were seen in neutered males or females. With the intact males and females, the incidences of one or more cancers were 8 percent and 21 percent, respectively. With neutering males at 1 year, there was an increase in cancer occurrence to 25 percent ( p <0.05). There was no evident increase in cancers in neutered females above the relatively high level in intact females. There was no occurrence of MC in intact females or those spayed late. For females left intact, 5 percent were reported with PYO. UI was not reported in any of the spayed or intact females. The suggested guidelines for males given the increased occurrence of cancers around at ages 1–2 years, is neutering beyond 2 years. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered females, those wishing to neuter should decide on the appropriate age. However, given the large body size, and physiology of late musculoskeletal development, some may want to consider neutering females well-beyond year 1.

Jack Russell Terrier

The study population was 92 intact males, 87 neutered males, 84 intact females, and 113 spayed females for a total sample of 376 cases. As in other small dogs, joint disorders were rare; none of the intact males, and just 2 percent of intact females had one or more joint disorders. Neutering was not associated with any increase in this measure in either sex. In intact males, 3 percent, and in intact females none, had one or more of the cancers followed. There was no evident increase in cancer occurrence in either sex with neutering at any age. In females left intact, MC was seen in 1 percent, as was PYO. In those spayed at 2–8 years, MC was diagnosed in 3 percent. UI was not diagnosed in any females. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age.

Labrador Retriever

The study population was 714 intact males, 381 neutered males, 400 intact females, and 438 spayed females for a total of 1,933 cases. One or more joint disorders were reported in 6 percent of both intact males and intact females. This measure was significantly increased to 13 percent for males neutered before 6 mo. ( p <0.01). In females spayed at <6 mo. and 6–11 mo., the risk of a joint disorder was 11–12 percent for each period ( p <0.01, spay periods combined). The occurrence of cancers followed was 8 percent and 6 percent, respectively, for intact males and females. Neutering at the various ages was not associated with any evident increased risk in the cancers. The occurrence of MC in intact females was 1 percent and for those spayed at 2–8 years, 2 percent. For females left intact, 2 percent were reported with PYO. UI was reported at a low rate (2–3%) in females spayed at various ages though 1 year. Given the significant occurrence of joint disorders in males neutered at <6 mo., the suggested guideline for males is neutering beyond 6 months. For females, given the increased risks of joint disorders with spaying through 11 months of age, the suggested guideline is delaying spaying until beyond a year of age.

The study population was 49 intact males, 72 neutered males, 65 intact females, and 86 spayed females for a total sample of 272 cases. As mentioned in Appendix 1 , the Maltese and Chihuahua vie for the smallest breeds and the Great Dane and Irish Wolfhound for the largest, but all four breeds share a low predisposition to joint disorders. For the Maltese in both sexes, there was no occurrence of joint disorders in either those left intact or neutered. Virtually the same picture emerges with cancers, with only one of 64 intact females being diagnosed with a cancer. There was no occurrence of MC in the intact females and only one case among the 19 females spayed at 2–8 years. PYO was seen in none of the intact females. UI did not occur in any of the females.

Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age.

Miniature Schnauzer

The study population for this small-dog breed was 47 intact males, 63 neutered males, 25 intact females and 96 spayed females for a total sample of 231 cases. There was virtually no occurrence of any joint disorders in males or females either left intact or neutered. The incidence of cancers in intact males was 4 percent and in females, zero percent. There was no indication of cancer increase related to neutering in either sex. There was no occurrence of MC in any of the females left intact or spayed, and a 4 percent occurrence of PYO in intact females. None of the females was diagnosed with UI. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age.

The study population was 84 intact males, 69 neutered males, 65 intact females, and 104 spayed females for a total sample of 322 cases. As with other dogs of small body size, both males and females had no occurrences of joint disorders in either those left intact or neutered. With regard to cancers, for both males and females left intact, the occurrence of cancers was zero, and there was no indication of increased cancer risk related to neutering in either sex. There was just one case of MC in females left intact, and 7 percent with PYO. None of the females was diagnosed with UI. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age.

Poodle, Toy

The study population was 49 intact males, 53 neutered males, 58 intact females, and 78 spayed females for a total sample of 238 cases. While the AKC registers all the Poodle varieties as the same breed, the three main varieties are dealt with separately here because of differences in size. In intact males, 4 percent had one or more joint disorders and in intact females there was no occurrence of a joint disorder. In neutered males and females, there was no evident increased risk of a joint disorder. There was a 2 percent occurrence of cancers in intact males and none in intact females. In neutered males and females, there was no noteworthy occurrence of cancers. In intact females, there was only a single case of MC and no case of PYO in intact females and no occurrence of UI in spayed females. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age.

Poodle, Miniature

The study population was 41 intact males, 60 neutered males, 30 intact females, and 69 spayed females for a total sample of 199 cases. The AKC registers the Toy, Miniature, and Standard Poodle varieties, all as the same breed. However, because of differences in size, the varieties of Poodles are dealt with separately here. There was no occurrence of a joint disorder in intact males or females. However, in males neutered at 6-11 mo., there was a significant 9 percent occurrence of joint disorders ( p <0.01), reflecting CCL. In spayed females, there was no occurrence of a joint disorder. In intact males and females, there was a 5 and zero percent occurrence of cancers, respectively. There was no indication of increased cancer occurrence related to neutering in either sex. The only occurrence of MC in females was one female that had been spayed at 2–8 years. Of intact females, 6 percent developed PYO. Just one female spayed at <6 mo. developed UI. The suggested guideline for males, based on the significant occurrence of a joint disorder with neutering at 6-11 mo., is delaying neutering until a year of age. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered females, those wishing to neuter should decide on the appropriate age.

Poodle, Standard

The study population was 47 intact males, 88 neutered males, 53 intact females, and 87 spayed females for a total sample of 275 cases. The AKC registers the Toy and Miniature, along with the Standard Poodle, as all being Poodles. However, because of differences in size, the varieties of Poodles are dealt with separately here. There was a 2 percent occurrence of joint disorders in both intact males and females. In males neutered at <6 mo., there was a non-significant increase to 8 percent, and in spayed females, there was no occurrence of joint disorders. The occurrences of cancers in intact males and females were 4 and 2 percent, respectively. In males neutered at 1 year of age, the occurrence of one or more cancers rose to a significant 27 percent ( p <0.01), all due to the increased risk of LSA. In females, there was no significant increase in cancers with spaying. There was a 4 percent occurrence of MC, and a 2 percent occurrence of PYO in the females left intact. Just one female spayed beyond 2 years later developed UI. The suggested guideline for males, based on the occurrence of one or more cancers with neutering at 1 year, is to delay neutering until 2 years of age. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered females, those wishing to neuter should decide on the appropriate age.

The study population was 96 intact males, 106 neutered males, 63 intact females, and 118 spayed females for a total sample of 383 cases. In intact males and females, the occurrences of joint disorders were zero and 2 percent, respectively. In neutered males and females, there was no evident increased occurrence of joint disorders. The level of occurrence of one or more cancers in intact males was 6 percent and in intact females, 8 percent. Neutering males and females did not lead to any evident increase in risk of a cancer. There were no cases of MC in females left intact or spayed at any time, and there was a 5 percent occurrence of PYO in the intact females. None of the females was diagnosed with UI. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age.

The study population was 315 intact males, 152 neutered males, 143 intact females, and 239 spayed females for a total sample of 854 cases. Joint disorders are a major concern in this breed with 8 percent of intact males and 16 percent of intact females having one or more joint disorders. In males, neutering at <6 mo. and at 6-11 mo. resulted in 10 percent and 22 percent occurrences (combined p <0.05). In females, spaying at <6 mo. resulted in a significant 43 percent occurrence ( p <0.05), the main joint disorder being CCL. The cancers followed occurred in the intact males and females at 16 and 11 percent, respectively. These relatively high occurrences of cancers in intact males and females were not increased by neutering at any age. Of females left intact or spayed at 2–8 years, 8 and 5 percent were diagnosed with MC, respectively. In intact females, 12 percent were diagnosed with PYO. With regard to UI, 1 percent of intact females had UI, and in females spayed at <6 mo. and 6-11 mo., 4 and 6 percent, respectively had UI. The suggested guideline for males, given the risk of joint disorders for those neutered at 6-11 mo. or earlier, is neutering beyond a year of age. For females, given the increased risk of joint disorders with neutering at <6 mo., the suggested guideline is spaying beyond 6 months.

Saint Bernard

The study population was 26 intact males, 27 neutered males, 18 intact females, and 23 spayed females for a total sample of 94 cases. This breed was chosen because of the large size. In intact males and females, the occurrences of one or more joint disorders were 8 percent and 6 percent, respectively. While there was no evident increase in joint disorders with neutering males, in females spayed at <6 mo., joint disorders increased to a significant 100 percent ( p <0.01). The cancers followed occurred in intact males and females at 4 and 11 percent, respectively. With neutering males and females, there were no noteworthy increases in cancers. There was no occurrence of MC in either the intact or spayed females. In intact females, PYO was diagnosed in 15 percent There was no occurrence of UI in spayed females. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males those wishing to neuter should decide on the appropriate age. The suggested guideline for females given in the increased risk of joint disorders with neutering at <6 mo., is neutering beyond 6 months. However, given the large body size, some may wish to consider neutering well-beyond 1 year of age.

Shetland Sheepdog

The study population was 31 intact males, 30 neutered males, 20 intact females, and 52 spayed females for a total sample of 133 cases. There were no joint disorders in intact males and just one in the intact females. In neutered males, the only joint disorder was in one of the males neutered at <6 mo. and in females there was no joint disorder associated with spaying. The occurrence of cancers in intact males was 6 percent and in intact females, zero. There were no evident increases in cancers in neutered males or females. There was no occurrence of MC in intact or spayed females and a 14 percent occurrence of PYO in intact females. Spaying at 6-11 mo. resulted in a 6 percent occurrence of UI, but at 1 year a 33 percent occurrence. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males, those wishing to neuter should decide on the appropriate age. However, to avoid the high level of UI occurrence in females, one could consider spaying females at, or beyond, 2 years.

The study population was 104 intact males, 112 neutered males, 77 intact females, and 139 spayed females for a total sample of 432 cases. In this small-dog breed there were no occurrences of joint disorders in either intact or neutered males and females, revealing virtually no vulnerability in this regard. There was no occurrence of the cancers followed in intact males and females. In neutered males there was no occurrence of cancers. However, in females, the occurrence of cancers for those spayed at 6-11 mo. was 7 percent and at 1 year this measure reached a significant 18 percent ( p <0.01). MC occurred in 3 percent of intact females. PYO occurred in 5 percent of intact females. UI was not reported in any females. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males, those wishing to neuter should decide on the appropriate age. The picture is very different for spaying females where the increased risk of cancers started with spaying at 6-11 mo., reaching 18 percent with spaying at year 1. The suggested guideline for females is to delay spaying until the female is 2 years of age. Another possibility is to spay a female a month or two before 6 months to avoid the increased risk of cancers.

West Highland White Terrier

The study population was 35 intact males, 33 neutered males, 28 intact females, and 46 spayed females for a total sample of 142 cases. Just one intact male had a joint disorder, and other than this, no joint disorders were reported in intact females or in neutered males or females. None of the intact males or females had any of the cancers followed. There were no noteworthy occurrences of the cancers in neutered males or females. There were no occurrences of MC in either intact or neutered females, and a 7 percent occurrence of PYO in intact females. The occurrence of UI was 14 percent for females spayed at <6 mo. and 6 percent at 6-11 mo. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age. However, for females, one could consider delaying spaying until a year of age to avoid the risk of UI.

Yorkshire Terrier

The study population was 134 intact males, 178 neutered males, 144 intact females, and 229 spayed females for a total sample of 685 cases. There were no joint disorders reported in intact males, and in intact females, just 1 percent. In neutered males and females there were no noteworthy occurrences of joint disorders. In intact males and intact females, just 1 percent were reported with at least one of the cancers followed. In both neutered males and females, none of the cancer occurrences was noteworthy. In intact females, the occurrence of MC was 1 percent as was the occurrence with spaying at 2–8 years. PYO was reported in 7 percent of intact females. No UI was reported in any of the intact or spayed females. Lacking a noticeable occurrence of increased joint disorders or cancers in neutered males or females, those wishing to neuter should decide on the appropriate age.

Since the reporting from this center of increased risks of joint disorders and some cancers in Golden Retrievers, Labrador Retrievers, and German Shepherd Dogs ( 11 – 13 ), the appropriate age of neutering has become a common point of discussion ( 16 – 18 ). With the evidence-based information on the risks, if any, of joint disorders, cancers, PYO and UI associated with neutering at different ages for males and females of various as dog breeds, dog owners, and their veterinarians, can use this information to select an age for neutering for the long-term health of their companion dogs on a case-by-case basis.

The overall major finding from the present study is that there are breed differences – and sometimes sex differences – with regard to the increased risks of joint disorders and cancers associated with neutering at various ages. For example, with the Boston Terrier, neutering females at the standard 6 month age did not increase the risks of joint disorders or cancers over that of dogs left intact, but with males, neutering before a year of age was associated with a significant increase in cancers. The opposite effect with genders was seen in the Cocker Spaniel where neutering at 6 months was not associated with an increase in joint disorders or cancers in males, but in females there was a significant increase in risk of cancers to 17 percent with neutering before 2 years.

Another important finding that holds across several breeds is that with the small-dog breeds – Cavalier King Charles Spaniel, Chihuahua, Corgi, Dachshund, Maltese, Pomeranian, Poodle-Toy, Pug, Shih Tzu, Yorkshire Terrier –the occurrences of joint disorders were close to zero in both the intact and neutered males and females. In these small-dog breeds, the occurrence of cancers was low in both those kept intact and neutered. Two exceptions were the Boston Terrier and Shih Tzu where there was there a significant increase in cancers with neutering.

As noted in the results section, the mean date of last entry per patient in the hospital record ranged from about 4.5 to 5.5 years, which means the data especially represent rather early-occurring joint disorders and cancers. The perspective taken here is that it is the early occurring joint disorders and cancers that are the most impactful on the human caregivers, both emotionally and financially, as well as their dogs. To just delay neutering by a year or so to lower the risk of a joint disorder or cancer in those breeds where the issue is relevant, is a noteworthy goal, making it worthwhile to discuss appropriate ages to neuter with caregivers who have a new puppy.

A suggested guideline for the use of the data presented here for those who may wish to focus on a breed or two, is to first scroll through Table 1 to peruse the breeds for a brief look at the neutering guidelines for the breeds of interest. The next step could be to refer to summary paragraphs in the Results section, which present the major findings with a suggested guideline for neutering age. Then for a third step, one could turn to Appendix 1 for detailed joint disorder and cancer tabular data as well as data on MC, PYO, and UI. Our intention is to offer readers data-based information to make case-by-case decisions about age of neutering. As is clearly evident in the breed-specific data presented, one cannot make a generalization for all dogs about age of neutering guidelines.

As mentioned, this study involved 35 breeds, counting the three varieties of Poodles as three breeds. Thus, most breeds registered by AKC or other comparable agencies were not covered. The breeds chosen were the most popular, and with the largest dataset in our records, or were included to sample the largest range of breed sizes as was feasible. Hence, some of the largest breeds (e.g., Great Dane, Irish Wolfhound) and smallest breeds (Miniature Schnauzer, West Highland White Terrier) were included despite lower numbers of patient records. While with some of the most popular breeds there were over 1,000 cases in the database, most breeds ended up with 200 to 500 cases which was sufficient for statistical analyses where the impact of neutering was substantial.

A suggestion for those interested in a breed not covered in this study is to find a breed or two closest genetically to the breed of their interest in order to get an estimate of the various disease risks, if any, associated with neutering. However, one needs to bear in mind that even genetically related breeds may vary a great deal. An example is seen when comparing Golden and Labrador Retrievers, using the data from this study, where in the Labrador, there was no increase in cancer risk above that of intact dogs with neutering, but in the female Golden, the risk of a cancer with neutering increased to 2–4 times that of the 5 percent level of intact females. The popular Poodle breed provides another example, where there are three major varieties in size, the Standard, Miniature, and Toy. In the Standard, neutering males at 1 year was associated with a highly significant increase in the risk of a cancer (mainly LSA) to over six times that of intact males, whereas in the Miniature, there was no increase in cancers with neutering but a significant increase in joint disorders (mainly CCL) with neutering at 6-11 mo.

A likely mechanism by which early neutering may lead to a joint disorder is related to disturbance of the closure of the long-bone growth plates by gonadal hormone secretion as the animal approaches maturity ( 19 , 20 ). We have proposed that neutering much before the closure of growth plates allows the long bones to grow a little longer than normal, and may sufficiently disturb joint alignments in some neutered dogs to lead to a clinically-apparent joint disorder.

Given the frequency with which early neutering is performed in dogs, it seems surprising that osteoporosis has not been examined given that in humans, chronic loss of gonadal hormones is associated with osteoporosis ( 21 ). It could be that the wolf ancestor of the dog had one breeding season and that the bone structure of mature dogs was not as affected by seasonal fluctuations of gonadal hormones as with a permanent gonadal hormonal loss in humans.

One of the frequently mentioned advantages of early neutering of female dogs is protection against MC ( 22 ). There may be important genetic, breed-line differences in the occurrence of MC that are not portrayed in our database. However, relevant to the discussion of MC is the recent meta-analysis of published studies on neutering females and MC, finding that the evidence linking neutering to a reduced risk of MC is weak ( 23 ). In the data gathered in this study, through 11 years of age, the occurrence of MC in females left intact was rarely above 6 percent and frequently 2 percent or less. For those neutered at <6 months, there was, as expected, no occurrence of MC. Obviously with most cases of intact females not followed through 11 years, and with the 12-year cut-off for those that were followed, many occurrences of MC were missed. However, it seems reasonable, that if MC was a common occurrence in intact females that this disease would have been more frequent in the intact females followed. Further, a very late onset of MC would seem less disturbing to pet owners than the much earlier onsets of joint diseases and other cancers.

For males, there is some concern that neutering beyond puberty will increase the likelihood of a problem behavior such as aggression. However, studies show that while neutering males can reduce aggression to people or other dogs in about 25 percent of males, neutering prior to puberty is no more effective in preventing this problem than is neutering in adulthood in resolving the problem ( 24 , 25 ).

This paper deals primarily with the risks of diseases that are seen within a given breed and sex. Comparisons between breeds are difficult to interpret, in part because of differences in developmental and physiological factors between breeds including those between smaller and larger breeds. In the text we have reported the occurrences of various diseases in percentages but in statistical analyses the actual data are used. When disease incidence is particularly low in one or more neutering subgroups, the ability to detect significant differences will be low, but there still could be differences which may or may not have been evident in the statistical analyses.

There are at least two major limitations to this study. First, relatively few breeds are covered compared to those included in the various breed registries of kennel clubs and canine organizations. This limitation was necessary so as to apply the same diagnostic criteria for diseases covered across all breeds, using the same database, and the necessity of having sufficient cases for analyses. Second, no information is available as to the reasons the owners or others chose to neuter, or not to neuter their dogs. In California, the vast majority of dogs are neutered, and since 2005 it is legally required for dogs to be neutered prior to adoption from an animal shelter or humane society ( 26 ); many breeders impose the same requirement.

In conclusion, the data presented should provide to veterinarians and interested puppy caregivers data-based information for the best age for neutering to avoid increasing the risk of joint disorders and some cancers beyond that of leaving the dog intact. Readers can note that an elevated risk for a joint disorder or cancer occurs in relatively few of these breeds. In other words, with most breeds or sexes, neutering can apparently be done without referral to a particular age, at least with regard to the joint disorders or cancers covered in this study. Of course, individual factors must be taken into account. For puppies of mixed breed, another paper that is currently in press provides data-based information dealing with age of neutering and the risk of one or more joint disorders as a function of the dog adult weight category ( 27 ). This information can also help inform decisions on age of recommended neuter in purebred dogs where the breed is not covered in our data.

Data Availability Statement

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found below: (Figshare, doi: 10.6084/m9.figshare.7231010 ).

Author Contributions

BH, LH, and AT: conceived and designed study, collected and complied, and analyzed data. NW: statistical analyses. BH, LH, AT, and NW: drafted and edited manuscript. All authors contributed to the article and approved the submitted version.

Supported by the Canine Health Foundation (#01488-A), the Center for Companion Animal Health, University of California, Davis (# 2009-54-F/M), and Versatility in Poodles.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

We wish to acknowledge the assistance of the following individuals in collecting the data: Siobhan Aamoth, Cristina Bustamante, Valerie Caceres, Rhoda Coscetti, Madeline Courville, Elvira Covarrubias, Aaron Frankel, Matthis Grupe, Vanessa Hsieh, Mi Hwangbo, Katrina Larkin, Arielle Merlos, Emily Parker, Roger Pender, Venus Pun, Emily Romanko, Sara Sewell, Sandra Walther, and Lexy Wetzel.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fvets.2020.00388/full#supplementary-material

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Keywords: elbow dysplasia, hip dysplasia, cranial cruciate tear, lymphoma, mast cell tumor, hemangiosarcoma, osteosarcoma

Citation: Hart BL, Hart LA, Thigpen AP and Willits NH (2020) Assisting Decision-Making on Age of Neutering for 35 Breeds of Dogs: Associated Joint Disorders, Cancers, and Urinary Incontinence. Front. Vet. Sci. 7:388. doi: 10.3389/fvets.2020.00388

Received: 02 April 2020; Accepted: 01 June 2020; Published: 07 July 2020.

Reviewed by:

Copyright © 2020 Hart, Hart, Thigpen and Willits. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Benjamin L. Hart, blhart@ucdavis.edu

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Dogs play a key role in veterinary college's brain cancer trial

by Virginia Tech

Lucy, with her boundless puppy-like energy even at 12 years old, is more than just a pet to Susan Ketcham. She's now part of a research project that could transform the way we treat brain cancer—in both dogs and humans.

This study at Virginia Tech's Virginia-Maryland College of Veterinary Medicine explores an innovative therapy called histotripsy. It's a leap forward from traditional cancer treatments, harnessing the power of focused ultrasound to break down tumors with precision.

When Lucy began experiencing seizures last July, Ketcham, a clinical nurse specialist, knew something more serious was the cause. The diagnosis of a brain tumor was devastating, but Ketcham was determined to explore all treatment options available. She discovered the histotripsy trial during her search and quickly reached out.

"Being in human medicine myself," said Ketcham, "I work in operating rooms and am very familiar with focused ultrasound, so I was eager to learn more."

Collaborative mission, translational impact

The trial is led by John Rossmeisl, the Dr. and Mrs. Dorsey Taylor Mahin Professor of Neurology and Neurosurgery, and Rell Parker, an iTHRIV scholar and assistant professor of neurology and neurosurgery.

Also on the team is Lauren Ruger, a postdoctoral associate in Eli Vlaisavljevich's lab in the Department of Biomedical Engineering and Mechanics where histotripsy is extensively researched. She's adapting the equipment used in the study to make it safe and effective for their canine patients.

"I had wanted to be a veterinarian when I was younger before deciding to become an engineer," said Ruger. "So I love having the opportunity to use my skills as an engineer to influence animal health."

This trial offers an essential stepping stone in developing less invasive treatment options for brain cancer .

Hope for histotripsy

"Histotripsy uses acoustic energy, or sound waves, to modify tissue," said Rossmeisl. "The intent is to cause a mechanical disruption of the tissue—killing cancer cells."

The technology was developed by researchers at the University of Michigan in the early 2000s.

The advantage is precision. Unlike traditional surgery , histotripsy can focus its impact on the tumor itself. "We could potentially treat these hard-to-reach brain tumors we normally can't access with traditional surgery," said Parker.

"We really don't have great ways to treat brain cancers in patients," said Rossmeisl. "Even when you do surgery, radiation, or chemotherapy alone or in combination, usually, you're not creating a cure."

However, there is hope that histotripsy could be used to activate the body's immune response and have it attack cancer cells, called the abscopal effect. Clinicians also see fewer side effects compared to other traditional treatment options .

About the procedure

The study currently still involves surgery to access brain tumors, which is the gold standard of care for this type of diagnosis. This allows for direct targeting of the tumor with the histotripsy transducer, delivering focused sound waves for precise treatment.

"When we do the surgery, we can see the tumor via ultrasound," Parker said. "We can see that we're treating the appropriate cells, and then we also do an MRI to ensure that we've targeted the right area."

After the histotripsy treatment, surgeons carefully remove the treated tumor. This tissue provides crucial insights into the technique's effect on cancer cells, helping researchers refine the technology for future applications.

"It gives us the advantage of being able to look at the tissue that's been broken down to ensure that we're getting the desired effect from the histotripsy therapy," said Ruger.

While the science is complex, the stories of patients like Lucy are reminders of why this work matters. "The recovery was quick, the incision was small," Ketcham said. "She's back to her playful self, and knowing she's helped advance science and technology is amazing."

Parker added, "We're happy to say that the procedure has been safe for our patients, and we've been able to treat them appropriately."

Looking toward the future of treatment

A long-term goal of this study is to develop a completely non-invasive treatment that would eliminate the need for surgery. The team is in the early stages of exploring this possibility, citing several challenges to realizing a solution that could be widely available.

"Transmitting ultrasound through the bones of the skull is very difficult," said Ruger. "And then accurately focusing it in only the areas you want to treat with histotripsy adds another layer of complexity."

However, the technique can be successfully applied through the skin, explained Rossmeisl. "That would be a paradigm changer. We would make surgically treating tumors a lot more widely available."

"Even though I love neurosurgery," he added, "anytime I can do something that doesn't require putting the patient through a complex and invasive procedure and get them home quicker, that's always a good thing."

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A doglike robot can navigate unknown obstacles using a simple algorithm that encourages forward progress with minimal effort.

Someday, when quakes, fires, and floods strike, the first responders might be packs of robotic rescue dogs rushing in to help stranded souls. These battery-powered quadrupeds would use computer vision to size up obstacles and employ doglike agility skills to get past them.

Toward that noble goal, AI researchers at Stanford University and Shanghai Qi Zhi Institute say they have developed a new vision-based algorithm that helps robodogs scale high objects, leap across gaps, crawl under thresholds, and squeeze through crevices – and then bolt to the next challenge. The algorithm represents the brains of the robodog.

“The autonomy and range of complex skills that our quadruped robot learned is quite impressive,” said Chelsea Finn , assistant professor of computer science and senior author of a new peer-reviewed paper announcing the teams’ approach to the world, which will be presented at the upcoming Conference on Robot Learning . “And we have created it using low-cost, off-the-shelf robots – actually, two different off-the-shelf robots.”

The key advance, the authors say, is that their robodog is autonomous – that is, it is able to size up physical challenges and imagine, then execute, a broad range of agility skills based simply on the obstacles it sees before it.

“What we’re doing is combining both perception and control, using images from a depth camera mounted on the robot and machine learning to process all those inputs and move the legs in order to get over, under, and around obstacles,” said Zipeng Fu, a doctoral candidate in Finn’s lab and first author of the study, along with Ziwen Zhuang of Shanghai Qi Zhi Institute.

Simplifying to optimize

Theirs is not the first robodog to demonstrate such agility – a class of athletics known as “parkour” – but it is first to combine self-sufficiency with a broad array of skills.

“Our robots have both vision and autonomy – the athletic intelligence to size up a challenge and to self-select and execute parkour skills based on the demands of the moment,” Fu said.

Existing learning methods are often based on complex reward systems that must be fine-tuned to specific physical obstacles. Accordingly, they don’t scale well to new or unfamiliar environments. Other related approaches learn using real-world data to imitate agility skills of other animals. These robodogs lack a broad skill set and don’t have the new robodogs’ vision capabilities. Both existing methods are also computationally “laggy” – in other words, slow.

This is the first open-source application to accomplish these goals with a simple reward system using no real-world reference data, the authors write in the study.

To succeed, they first synthesized and honed the algorithm using a computer model, then transferred it to two real-world robodogs. Next, in a process called reinforcement learning, the robots attempted to move forward in any way they saw fit and got rewarded based on how well they did. This is how the algorithm eventually learns the best way to approach a new challenge.

In practice, most existing reinforcement learning reward systems involve too many variables to be effective, slowing computational performance. This is what makes the streamlined reward process for robodog parkour exceptional, if also surprisingly straightforward.

“It’s actually fairly simple,” Finn said. “We based it mostly on how far forward the robot is moving and the amount of effort it has applied to do it. Eventually, the robot learns more complex motor skills that allow it to get ahead.”

Real-world tests

The team then performed extensive experiments using real-world robodogs to demonstrate their new agility approach in especially challenging environments using only those robodogs’ off-the-shelf computers, visual sensors, and power systems.

In raw numbers, the new-and-improved robodogs were able to climb obstacles more than one-and-a-half times their height, leap gaps greater than one-and-a-half times their length, crawl beneath barriers three-quarters of their height, and tilt themselves in order to squeeze through a slit thinner than their width.

Next up, the team hopes to leverage advances in 3D vision and graphics to add real-world data to its simulated environments to bring a new level of real-world autonomy to their algorithm.

Additional authors are from Shanghai Tech, Carnegie Mellon University, and Tsinghua University.

The project was supported financially by Shanghai Qi Zhi Institute and a grant from the Office of Naval Research (ONR).

Media Contacts

Jill Wu, Stanford University School of Engineering: (386) 383-6061;  [email protected]

When should you neuter or spay your dog? Researchers update guidelines

R esearchers at the University of California, Davis, have updated their guidelines on when to neuter 40 popular dog varieties by breed and sex. Their recent paper in Frontiers in Veterinary Science adds five breeds to a line of research that began in 2013 with a study that suggested that early neutering of golden retrievers puts them at increased risk of joint diseases and certain cancers.

That initial study set off a flurry of debate about the best age to neuter other popular breeds. Professors Lynette and Benjamin Hart of the School of Veterinary Medicine, the study's lead authors, set out to add more breed studies by examining more than a decade of data from thousands of dogs treated at the UC Davis veterinary hospital. Their goal was to provide owners with more information to make the best decision for their animals.

They specifically looked at the correlation between neutering or spaying a dog before 1 year of age and a dog's risk of developing certain cancers. These include cancers of the lymph nodes, bones, blood vessels or mast cell tumors for some breeds; and joint disorders such as hip or elbow dysplasia, or cranial cruciate ligament tears.

Joint disorders and cancers are of particular interest because neutering removes male and female sex hormones that play key roles in important body processes such as closure of bone growth plates.

For the most recent study, they focused on German short/wirehaired pointer, mastiff, Newfoundland, Rhodesian ridgeback and Siberian husky. Data was collected from the UC Davis veterinary hospital's records that included more than 200 cases for each of these five breeds weighing more than 20 kg (or 44 pounds), spanning January 2000 through December 2020.

The Harts said their updated guidelines emphasize the importance of personalized decisions regarding the neutering of dogs, considering the dog's breed, sex and context. A table representing guidelines reflecting the research findings for all 40 breeds that have been studied, including the five new breeds, can be found here .

Health risks different among breeds

"It's always complicated to consider an alternate paradigm," said Professor Lynette Hart. "This is a shift from a long-standing model of early spay/neuter practices in the U.S. and much of Europe to neuter by 6 months of age, but important to consider as we see the connections between gonadal hormone withdrawal from early spay/neuter and potential health concerns."

The study found major differences among these breeds for developing joint disorders and cancers when neutered early. Male and female pointer breeds had elevated joint disorders and increased cancers; male mastiff breeds had increased cranial cruciate ligament tears and lymphoma; female Newfoundland breeds had heightened risks for joint disorders; female Ridgeback breeds had heightened risks for mast cell tumors with very early neutering; and Siberian huskies showed no significant effects on joint disorders or cancers.

"We're invested in making contributions to people's relationship with their animals," said Benjamin Hart, distinguished professor emeritus. "This guidance provides information and options for veterinarians to give pet owners, who should have the final decision-making role for the health and well-being of their animal."

Other researchers on this UC Davis study include: Abigail Thigpen, Maya Lee, Miya Babchuk, Jenna Lee, Megan Ho, Sara Clarkson and Juliann Chou with the School of Veterinary Medicine; and Neil Willits with the Department of Statistics.

More information: Lynette Arnason Hart et al, Assisting decision-making on age of neutering for German Short/Wirehaired Pointer, Mastiff, Newfoundland, Rhodesian Ridgeback, Siberian Husky: associated joint disorders, cancers, and urinary incontinence, Frontiers in Veterinary Science (2024). DOI: 10.3389/fvets.2024.1322276

Provided by UC Davis

Pavlov’s Dogs Experiment and Pavlovian Conditioning Response

Saul Mcleod, PhD

Editor-in-Chief for Simply Psychology

BSc (Hons) Psychology, MRes, PhD, University of Manchester

Saul Mcleod, PhD., is a qualified psychology teacher with over 18 years of experience in further and higher education. He has been published in peer-reviewed journals, including the Journal of Clinical Psychology.

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Olivia Guy-Evans, MSc

Associate Editor for Simply Psychology

BSc (Hons) Psychology, MSc Psychology of Education

Olivia Guy-Evans is a writer and associate editor for Simply Psychology. She has previously worked in healthcare and educational sectors.

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Like many great scientific advances, Pavlovian conditioning (aka classical conditioning) was discovered accidentally. Ivan Petrovich Pavlov (1849–1936) was a physiologist, not a psychologist.

During the 1890s, Pavlov researched salivation in dogs in response to being fed. He inserted a small test tube into the cheek of each dog to measure saliva when the dogs were fed (with a powder made from meat).

Pavlov predicted the dogs would salivate in response to the food in front of them, but he noticed that his dogs would begin to salivate whenever they heard the footsteps of his assistant, who was bringing them the food.

When Pavlov discovered that any object or event that the dogs learned to associate with food (such as the lab assistant) would trigger the same response, he realized that he had made an important scientific discovery.

Accordingly, he devoted the rest of his career to studying this type of learning.

Pavlovian Conditioning: Theory of Learning

Pavlov’s theory of learning, known as classical conditioning, or Pavlovian conditioning, posits that behaviors can be learned through the association between different stimuli.

Classical conditioning (later developed by Watson, in 1913) involves learning to associate an unconditioned stimulus that already brings about a particular response (i.e., a reflex) with a new (conditioned) stimulus, so that the new stimulus brings about the same response.

Pavlov developed some rather unfriendly technical terms to describe this process:

• Neutral Stimulus (NS) : A stimulus that initially does not elicit a particular response or reflex action. In other words, before any conditioning takes place, the neutral stimulus has no effect on the behavior or physiological response of interest. For example, in Pavlov’s experiment, the sound of a metronome was a neutral stimulus initially, as it did not cause the dogs to salivate.
• Unconditioned Stimulus (UCS): This is a stimulus that naturally and automatically triggers a response without any learning needed. In Pavlov’s experiment, the food was the unconditioned stimulus as it automatically induced salivation in the dogs.
• Conditioned Stimulus (CS): This is a previously neutral stimulus that, after being repeatedly associated with an unconditioned stimulus, comes to trigger a conditioned response. For instance, in Pavlov’s experiment, the metronome became a conditioned stimulus when the dogs learned to associate it with food.
• Conditioned Response (CR): This is a learned response to the conditioned stimulus. It typically resembles the unconditioned response but is triggered by the conditioned stimulus instead of the unconditioned stimulus. In Pavlov’s experiment, salivating in response to the metronome was the conditioned response.
• Unconditioned Response (UR): This is an automatic, innate reaction to an unconditioned stimulus. It does not require any learning. In Pavlov’s experiment, the dogs’ automatic salivation in response to the food is an example of an unconditioned response.

Pavlov’s Dog Experiment

Pavlov (1902) started from the idea that there are some things that a dog does not need to learn. For example, dogs don’t learn to salivate whenever they see food. This reflex is ‘hard-wired’ into the dog.

Pavlov showed that dogs could be conditioned to salivate at the sound of a bell if that sound was repeatedly presented at the same time that they were given food.

Pavlov’s studies of classical conditioning have become famous since his early work between 1890 and 1930. Classical conditioning is “classical” in that it is the first systematic study of the basic laws of learning (also known as conditioning).

Pavlov’s dogs were individually situated in secluded environments, secured within harnesses. A food bowl was positioned before them, and a device was employed to gauge the frequency of their salivary gland secretions.

The data from these measurements were systematically recorded onto a rotating drum, allowing Pavlov to meticulously monitor the rates of salivation throughout the course of the experiments.

First, the dogs were presented with the food, and they salivated. The food was the unconditioned stimulus and salivation was an unconditioned (innate) response. (i.e., a stimulus-response connection that required no learning).

Unconditioned Stimulus (Food) > Unconditioned Response (Salivate)

In his experiment, Pavlov used a metronome as his neutral stimulus. By itself, the metronome did not elicit a response from the dogs. 

Neutral Stimulus (Metronome) > No Response

Next, Pavlov began the conditioning procedure, whereby the clicking metronome was introduced just before he gave food to his dogs. After a number of repeats (trials) of this procedure, he presented the metronome on its own.

As you might expect, the sound of the clicking metronome on its own now caused an increase in salivation.

Conditioned Stimulus (Metronome) > Conditioned Response (Salivate)

So, the dog had learned an association between the metronome and the food, and a new behavior had been learned.

Because this response was learned (or conditioned), it is called a conditioned response (and also known as a Pavlovian response). The neutral stimulus has become a conditioned stimulus.

Temporal contiguity

Pavlov found that for associations to be made, the two stimuli had to be presented close together in time (such as a bell).

He called this the law of temporal contiguity. If the time between the conditioned stimulus (bell) and the unconditioned stimulus (food) is too great, then learning will not occur.

‘Unconditioning’ through experimental extinction

In extinction, the conditioned stimulus (the bell) is repeatedly presented without the unconditioned stimulus (the food).

Over time, the dog stops associating the sound of the bell with the food, and the conditioned response (salivation) weakens and eventually disappears.

In other words, the conditioned response is “unconditioned” or “extinguished.”

Spontaneous recovery

Pavlov noted the occurrence of “spontaneous recovery,” where the conditioned response can briefly reappear when the conditioned stimulus is presented after a rest period, even though the response has been extinguished.

This discovery added to the understanding of conditioning and extinction, indicating that these learned associations, while they can fade, are not completely forgotten.

Generalization

The principle of generalization suggests that after a subject has been conditioned to respond in a certain way to a specific stimulus, the subject will also respond in a similar manner to stimuli that are similar to the original one.

In Pavlov’s famous experiments with dogs, he found that after conditioning dogs to salivate at the sound of a bell (which was paired with food), the dogs would also salivate in response to similar sounds, like a buzzer.

This demonstrated the principle of generalization in classical conditioning.

However, the response tends to be more pronounced when the new stimulus closely resembles the original one used in conditioning.

This relationship between the similarity of the stimulus and the strength of the response is known as the generalization gradient.

This principle has been exemplified in research, including a study conducted by Meulders and colleagues in 2013.

Impact of Pavlov’s Research

Ivan Pavlov’s key contribution to psychology was the discovery of classical conditioning, demonstrating how learned associations between stimuli can influence behavior.

His work laid the foundation for behaviorism, influenced therapeutic techniques, and informed our understanding of learning and memory processes.

Behaviorism: Pavlov’s work laid the foundation for behaviorism , a major school of thought in psychology. The principles of classical conditioning have been used to explain a wide range of behaviors, from phobias to food aversions.

Therapy Techniques: Techniques based on classical conditioning, such as systematic desensitization and exposure therapy , have been developed to treat a variety of psychological disorders, including phobias and post-traumatic stress disorder (PTSD).

In these therapies, a conditioned response (such as fear) can be gradually “unlearned” by changing the association between a specific stimulus and its response.

• Little Albert Experiment : The Little Albert experiment, conducted by John B. Watson in 1920, demonstrated that emotional responses could be classically conditioned in humans. A young child, “Little Albert,” was conditioned to fear a white rat, which generalized to similar objects. 

Educational Strategies: Educational strategies, like repetitive learning and rote memorization, can be seen as applications of the principles of classical conditioning. The repeated association between stimulus and response can help to reinforce learning.

Marketing and Advertising: Principles from Pavlov’s conditioning experiments are often used in advertising to build brand recognition and positive associations.

For instance, a brand may pair its product with appealing stimuli (like enjoyable music or attractive visuals) to create a positive emotional response in consumers, who then associate the product with it.

Critical Evaluation

Pavlovian conditioning is traditionally described as learning an association between a neutral conditioned stimulus (CS) and an unconditioned stimulus (US), such that the CS comes to elicit a conditioned response (CR). This fits many lab studies but misses the adaptive function of conditioning (Domjan, 2005).

From a functional perspective, conditioning likely evolves to help organisms effectively interact with biologically important unconditioned stimuli (US) in their natural environment.

For conditioning to happen naturally, the conditioned stimulus (CS) can’t be arbitrary, but must have a real ecological relationship to the US as a precursor or feature of the US object.

Pavlovian conditioning prepares organisms for important biological events by conditioning compensatory responses that improve the organism’s ability to cope.

The critical behavior change from conditioning may not be conditioned responses (CRs), but rather conditioned modifications of unconditioned responses (URs) to the US that improve the organism’s interactions with it.

Evidence shows conditioning occurs readily with naturalistic CSs, like tastes before illness, infant cues before nursing, prey sights before attack. This conditioning is more robust and resistant to effects like blocking.

Traditional descriptions of Pavlovian conditioning as simply the acquired ability of one stimulus to evoke the original response to another stimulus paired with it are inadequate and misleading (Rescorla, 1988).

New research shows conditioning is actually about learning relationships between events, which allows organisms to build mental representations of their environment.

Just pairing stimuli together doesn’t necessarily cause conditioning. It depends on whether one stimulus gives information about the other.

Conditioning rapidly encodes relations among a broad range of stimuli, not just between a neutral stimulus and one eliciting a response. The learned associations allow complex representations of the world.

Recently, Honey et al. (2020, 2022) presented simulations using an alternative model called HeiDI that accounts for Rescorla’s findings. HeiDI differs by allowing reciprocal CS-US and US-CS associations. It uses consistent learning rules applied to all stimulus pairs.

The simulations suggest HeiDI explains Rescorla’s results via two mechanisms:

• Changes in US-CS associations during compound conditioning, allowing greater change in some US-CS links
• Indirect influences of CS-CS associations enabling compounds to recruit associative strength from absent stimuli

HeiDI integrates various conditioning phenomena and retains key Rescorla-Wagner insights about surprise driving learning. However, it moves beyond the limitations of Rescorla-Wagner by providing a framework to address how learning translates into performance.

HeiDI refers to the authors of the model (Honey, Dwyer, Iliescu) as well as highlighting a key feature of the model – the bidirectional or reciprocal associations it proposes between conditioned stimuli and unconditioned stimuli.

H – Honey (the lead author’s surname), ei – Bidirectional (referring to the reciprocal associations), D – Dwyer (the second author’s surname), I – Iliescu (the third author’s surname).

• Domjan, M. (2005). Pavlovian conditioning: A functional perspective.  Annu. Rev. Psychol. ,  56 , 179-206.
• Honey, R.C., Dwyer, D.M., & Iliescu, A.F. (2020a). HeiDI: A model for Pavlovian learning and performance with reciprocal associations. Psychological Review, 127, 829-852.
• Honey, R. C., Dwyer, D. M., & Iliescu, A. F. (2022). Associative change in Pavlovian conditioning: A reappraisal .  Journal of Experimental Psychology: Animal Learning and Cognition .
• Meulders A, Vandebroek, N. Vervliet, B. and Vlaeyen, J.W.S. (2013). Generalization Gradients in Cued and Contextual Pain-Related Fear: An Experimental Study in Health Participants .  Frontiers in Human Neuroscience ,  7 (345). 1-12.
• Pavlov, I. P. (1897/1902). The work of the digestive glands. London: Griffin.
• Pavlov, I. P. (1928). Lectures on conditioned reflexes . (Translated by W.H. Gantt) London: Allen and Unwin.
• Pavlov, I. P. (1927). Conditioned Reflexes: An Investigation of the Physiological Activity of the Cerebral Cortex . Translated and edited by Anrep, GV (Oxford University Press, London, 1927).
• Rescorla, R. A. (1988). Pavlovian conditioning: It’s not what you think it is .  American Psychologist ,  43 (3), 151.
• Pavlov, I. P. (1955). Selected works . Moscow: Foreign Languages Publishing House.
• Watson, J.B. (1913). Psychology as the behaviorist Views It. Psychological Review, 20 , 158-177.
• Watson, J. B., & Rayner, R. (1920). Conditioned emotional reactions.  Journal of experimental psychology ,  3 (1), 1.

Further Reading

• Logan, C. A. (2002). When scientific knowledge becomes scientific discovery: The disappearance of classical conditioning before Pavlov. Journal of the History of the Behavioral Sciences, 38 (4), 393-403.
• Learning and Behavior PowerPoint

What was the main point of Ivan Pavlov’s experiment with dogs?

The main point of Ivan Pavlov’s experiment with dogs was to study and demonstrate the concept of classical conditioning.

Pavlov showed that dogs could be conditioned to associate a neutral stimulus (such as a bell) with a reflexive response (such as salivation) by repeatedly pairing the two stimuli together.

This experiment highlighted the learning process through the association of stimuli and laid the foundation for understanding how behaviors can be modified through conditioning.

What is Pavlovian response?

The Pavlovian response, also known as a conditioned response, refers to a learned, automatic, and involuntary response elicited by a previously neutral stimulus through classical conditioning. It is a key concept in Pavlov’s experiments, where dogs learned to salivate in response to a bell.

When did Pavlov discover classical conditioning?

Ivan Pavlov discovered classical conditioning during his dog experiments in the late 1890s and early 1900s. His seminal work on classical conditioning, often called Pavlovian conditioning, laid the foundation for our understanding of associative learning and its role in behavior modification.

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Effect of Music on Stress Parameters in Dogs during a Mock Veterinary Visit

Tammie king.

1 Waltham Petcare Science Institute, Freeby Lane, Waltham on the Wolds, Leicestershire LE14 4RT, UK; [email protected] (H.E.F.); [email protected] (A.B.G.H.); [email protected] (D.W.L.)

Hannah E. Flint

Alysia b. g. hunt, walter t. werzowa.

2 HealthTunes Inc., 1800 S. Brand Boulevard Suite 114, Glendale, CA 91204, USA; gro.senuthtlaeh@retlaw

Darren W. Logan

Associated data.

Data are contained within the article or Supplementary Materials .

Simple Summary

Visits to the vet are stressful for many pet dogs, but less is known about how measures of stress change over the course of a visit. Identifying appropriate measures of canine stress, along with successful interventions which alleviate stress in dogs during a veterinary visit, will be of great benefit to dogs and people. Music therapy has been successfully used to reduce stress and anxiety in people and other animals. Specifically, a process called entrainment, which involves playing music at a particular tempo aimed at synchronizing physiological responses, has been implemented with success in humans. The aim of this study was to examine a range of behavioral and physiological measures in dogs over the duration of a veterinary visit and to establish if bespoke music, which mimicked the tempo of their resting heart rate, could improve wellbeing. The results indicated that certain measures increased over time, indicating that dogs became increasingly stressed. Music was not shown to have a demonstrated effect across measures, suggesting that the stressor may be too extreme for this type of intervention to have a positive effect, or that music therapy requires modification before it can be successful in alleviating stress in dogs during a veterinary visit.

Veterinary visits can be stressful for dogs, but how their wellbeing changes during a visit is not well understood. Music therapy has been successfully used in clinical practice to alleviate stress and anxiety in people. The present study aimed to understand how canine stress changes during a veterinary visit, establish the effect of music, and highlight measures which may be of practical use. In a randomized crossover design, dogs were exposed to no music and a bespoke piece of classical music at a tempo designed to match their resting heart rate during a mock veterinary visit. Dogs were scored as more “afraid” during the physical examination compared to when they were in the hospital kennel ( p < 0.001). Salivary cortisol, IgA, and infrared temperature all increased significantly ( p < 0.05) from baseline to post-kennel and post-examination, with no effect of music treatment. Core body temperature ( p = 0.010) and the odds of ‘relaxed’ lips ( p = 0.020) were lower when dogs were exposed to music compared to control visits. Overall, dogs experienced changes in physiology and behavior, indicative of increased stress, over the course of the visit. Additional research is required to further understand the effect that bespoke music may have in alleviating canine stress during veterinary visits.

1. Introduction

Veterinary hospitals are considered stressful environments for dogs [ 1 , 2 , 3 , 4 , 5 , 6 ] as well as caregivers [ 7 ], and these negative experiences can have long-lasting effects on animals [ 8 ]. Although the mammalian stress response is an adaptive mechanism that allows animals to respond quickly to certain situations or stimuli, chronic or extreme stress, often categorized as distress, can be harmful to animals, resulting in poor welfare [ 9 ]. Although it is widely accepted by owners and practitioners that dogs experience stress and anxiety when visiting a veterinary clinic, to what extent a pet may be impacted is not fully understood. Possible reasons for this may be because there are no clear protocols specifying how canine stress can be accurately measured and monitored in clinical environments, along with the accompanying complexity of capturing data across different timepoints during a visit, and the inability to obtain output in a timely manner. Commonly, data are collected in “real-world” environments where standardization may be lacking and added variables, such as the presence of other pets, staff, and the owner, can influence measures. The experience and handling skills of both veterinary staff and pet owners may also influence pet behavior and physiology, along with the different types of treatment protocols and whether the dog is in pain. Traditional measures include owner or staff questionnaires [ 10 ], ratings of stress [ 5 ], and coding of specific behaviors, e.g., lip licking, whale eye, body posture, panting, and trembling [ 11 ], as well as a range of physiological parameters. These can include eye temperature using infrared thermography (IRT) [ 4 ], heart rate, heart rate variability, blood pressure, along with salivary or plasma cortisol and immune markers such as immunoglobulin A (IgA), as well as neutrophil–lymphocyte (N:L) ratios. (For a detailed overview of physiological measures of stress in dogs, see Hekman et al. [ 12 ]). Some parameters are difficult, costly and/or time consuming to capture and can be influenced by circadian rhythms, physical health, and activity [ 12 ]. For example, the collection of behavioral data via video recordings is relatively straightforward but resource intensive when objectively coding specific behaviors. Conversely, owner-directed questionnaires may be a relatively quick and easy means to obtain data; however, they are subjective in nature and therefore potentially inaccurate [ 11 ]. An increasingly popular approach is to use instruments that require ratings of specific behaviors or behavioral attributes that can be scored by an experimenter [ 13 ]. Qualitative Behavior Analysis (QBA) [ 14 ] yields accurate and repeatable results to infer animals’ affective states. Unlike specific coding of individual behaviors, QBAs act as a “whole-animal” measure which captures a holistic view of an individual’s demeanor [ 15 ]. However, to best understand an animal’s emotional state, the ideal approach is to combine easy-to-administer scales which evaluate behavior, along with a range of physiological parameters.

It would be beneficial to identify interventions that are easy to implement and supported by science that can improve pet wellbeing in a veterinary setting. This has the potential to be multi-beneficial. Caregivers are likely to feel more at ease and may therefore be more likely to return to a clinic that prioritizes their pet’s welfare. Animals who are less stressed, anxious, or afraid are less likely to exhibit aggressive behavior [ 16 ] which may result in staff injuries.

A range of strategies to make vet visits a more pleasant experience for pets are recommended by practitioners who take an interest in animal welfare, including low-stress handling techniques, appropriate waiting/consultation/hospital room layout, pheromonotherapy, lighting, and aromatherapy [ 8 , 17 , 18 ]. An approach which has not been widely recommended, employed, or empirically tested is the inclusion of music therapy in veterinary hospitals [ 19 ]. Often, veterinary clinics have a radio or television playing in their waiting rooms, and music may be played during surgical procedures, but this is generally for the benefit of staff or clients, rather than specifically to aid in pet welfare. Music has been used for centuries to influence human health [ 20 ], including as a form of alternative therapy to reduce patient pain [ 21 ], stress, and anxiety [ 22 ] and to improve staff and patient wellbeing [ 23 ]. The exact mechanisms of these therapies are not well understood, but one possible explanation is that music acts as a distractor stimulus, focusing the patient’s attention away from fear- or pain-inducing stimuli to something pleasant and enjoyable. Much less is known as to whether music has similar effects on non-human animals, such as cats and dogs, in clinical environments. Classical music, in particular, is thought to have positive effects in a veterinary setting, but empirical studies to support this tend to be weak [ 24 ]. Assumptions are often based on other studies which include healthy animals not representative of hospitalized patients or those within a clinical environment, sample sizes are often small, with lack of randomization and inconsistent treatment approaches. However, one study demonstrated that cats who are exposed to classical music whilst under anesthesia showed reduced respiratory rate and pupil diameter when undergoing painful surgical procedures [ 25 ]. Another study demonstrated that classical music improved owner satisfaction during a veterinary visit [ 26 ]. Other studies have focused on the effect music has on laboratory animals or livestock, concluding that some forms of music improve milk production and meat quality, while also decreasing potential indicators of stress, such as heart rate and blood pressure [ 27 ]. More commonly, research involving music and companion animals has focused on pet welfare in kenneled environments (working and shelter dog populations) [ 28 , 29 , 30 , 31 , 32 , 33 ]. Results from these studies have indicated that the type of auditory stimuli is important, with kenneled dogs showing more calm behaviors when exposed to classical music [ 33 ], and more active behaviors when exposed to heavy metal music [ 29 ]. A separate study found that kenneled dogs displayed more relaxed behavior when exposed to audiobooks than when exposed to any other auditory stimuli [ 30 ]. It may not necessarily be the classification of music that is important, but the structure of the piece of music related to its notes, tone, rhythm, and tempo [ 34 ], along with the individual dog’s previous associations with the music. A study which examined the effect certain music types had on felines showed that cats prefer species-specific music, so sounds that were at a higher pitch and tempo [ 35 ]. When tested in a clinical setting, cats were scored as being significantly less stressed and easier to handle compared to when they were exposed to classical music or no music [ 36 ]. In humans, music induces both arousal and relaxation effects, predominantly related to the tempo [ 37 ]. Slow or meditative music can induce a relaxing effect; relaxation is particularly evident during a musical pause, whereas faster rhythms concentrate attention [ 38 ]. Specifically, physiological measures including heart rate, blood pressure, and respiration modulate in response to music containing particular tempi. Another mechanism related to music tempo which has been demonstrated to positively affect humans is the process of entrainment. Entrainment describes a process whereby two or more rhythmic properties synchronize with one another [ 39 ]. Studies have demonstrated positive entrainment and stimulation caused by certain tempi and/or rhythms in chronic pain, sleep, anxiety, mobility, and heart rate treatments [ 40 , 41 ]. Rhythmic entrainment using music may also be beneficial in alleviating anxiety levels in dogs, attempting to synchronize biorhythms (such as heart rate) to bespoke music set to resting heart rate tempo.

To our knowledge, there have been no studies which examine the phenomena of music entrainment in dogs and its effect on reducing stress during a veterinary visit. To examine the topics of canine stress and music therapy in more detail, the present study was designed to address three key objectives. Firstly, to understand how specific measures of canine stress change during a mock veterinary visit, secondly, to establish the effect bespoke music has on stress parameters in a clinical environment, and thirdly, to provide recommendations on measures of canine stress for in-clinic use.

2. Materials and Methods

2.1. subjects.

Thirty-eight adult dogs, seventeen males and females of various breeds (14 Labrador Retrievers, 6 Beagles, 6 Petit Basset Griffon Vendéen, and 12 Norfolk Terriers), with a mean age (±sd) of 3.4 ± 1.9 years, ranging from 1 to 8.2 years, participated in the study. All dogs were housed in pairs within kennels at the Waltham Petcare Science Institute (Leicestershire, UK). Throughout the duration of the study, all dogs were provided with comprehensive training and socialization programs, adjusted to the needs of individual dogs as per the Institute’s standard pet keeping requirements. Prior to the study, dogs had been exposed to the testing environment and underwent basic mouth handling training to facilitate saliva sample collection.

2.2. Veterinary Clinic

The study was conducted in the veterinary suite located at the Waltham Petcare Science Institute between November and December 2019. The temperature-controlled veterinary clinic was a standard set-up including an office/foyer area, walk-in hospital kennels, consultation room, and surgery, along with diagnostic facilities and associated veterinary equipment. The experimental procedure was designed to simulate a veterinary clinic experience which comprised a period of “waiting” time in the hospital kennel area (1.59 m × 0.98 m), followed by a routine veterinary health examination in a consultation room (6.46 m × 2.94 m). The walk-in kennel had solid opaque walls with a transparent Perspex front door. Kennels faced into a hallway. No other animals or staff, other than those involved in the collection of data, were present in the veterinary clinic while the study was underway.

2.3. Study Design

Using a randomized crossover design, each dog experienced two mock veterinary visits which occurred at least two weeks apart, one where music was played and one without music. Bespoke pieces of classical music, composed by an experienced, professional music producer, were designed to match the tempo of the estimated resting heartbeat of each dog breed. In consultation with the site’s veterinarian, the heart rates of specific beats per minute (bpm) for small (120 (±20)), medium (100 (±20)), and large (95 (±20)) breeds included in the study were collected and used by the HealthTunes music producer when designing the music. Three curated playlists were provided for each of the dog sizes ( Audio S1; Audio S2; Audio S3 ). Each playlist contained solo-harp music arrangements of classical works. The dynamic range of the music was narrow (no sudden volume peaks/accents), the arrangements fluid (no sudden pattern changes), and the frequency band well balanced (mid-range frequency dominates and high/low frequency bands evenly audible). The music program was mastered at −0.1 dB. During the experimental procedure, music was delivered continuously through two SONOS One wireless audio speakers mounted on the walls within the testing environment during treatment sessions. One speaker was placed in the kennel room hallway and the other inside the consultation room and provided stereo sound with the same music quality in both locations.

The standardized mock veterinary visit was separated into two phases—waiting time in the kennel area followed by a physical examination in a consultation room.

Dogs entered the foyer of the building with a familiar handler at the same time each day for their test sessions. Immediately after entering, a series of baseline measures were collected by a researcher (T0). The dog was then led by the handler into the walk-in kennel, where they were left alone for a duration of 15 min and exposed to music or no music (Kennel). Additional data were collected immediately after the end of this session (T1), and the dog was then led by the handler into the consultation room, where a second researcher, acting as a mock veterinarian, performed a routine health examination (Consult). To ensure consistency, the same researcher was used throughout. The handler and “veterinarian” engaged in small talk to mimic what would occur during a routine clinic appointment. Small and medium dogs (<15 kg) were picked up by the handler and placed on the examination table to receive their health check, while large dogs (>15 kg) received their health examination on the floor. During the examination, which lasted approximately 10 min, the mock veterinarian, who wore a white laboratory coat, followed a standardized procedure and accompanying script where they spoke to the dog’s handler whilst completing a health exam. They checked the dog’s eyes, mouth, nose, and ears, palpated lymph nodes and the abdomen, then provided a foreleg and foot exam. They also took each dog’s heart rate, respiration rate, and finally, rectal temperature. If at any point the dog displayed signs of distress, the examination was modified to maintain dog welfare and ensure each dog could participate as much as possible. Distress was considered as the prolonged duration, intensity, or frequency of any stress-related behavior such as trembling, panting, cowering, vocalizing, low body posture, and avoidance. Directly after the examination, additional data were collected (T2) before the dog was led back to the foyer and collected by a member of staff, where they were then returned to their familiar housing.

The study was reviewed and approved by the Waltham Petcare Science Institute Animal Welfare and Ethical Review Board (study number PPM 63406).

2.4. Data Collection and Analysis

A range of data were collected at three sample points: T0—baseline (after entering the foyer/office), T1—after being left alone in the kennel, and T2—after the physical examination in the consultation room. Behavioral measures were collected later from video recordings of the dog in the kennel (Kennel) and during the health examination in the consultation room (Consult) ( Figure 1 ).

A range of physiological and behavioral data were collected at various timepoints during testing sessions.

2.4.1. Eye, Nose, and Ear Temperature

Infrared thermography (IRT) was used to capture the mean eye and nose temperature and maximum and mean ear temperature at T0, T1, and T2. A portable infrared thermal camera (FLIR T840, FLIR, Wilsonville, OR, USA) was used to capture all infrared images during the study with a thermal range of—20 to 150 °C and a resolution of 464 × 348 pixels. The value of emissivity was set at 1. All dogs were pictured with the camera at a 90° angle to the dog and from approximately 1 m away. Once collected, images were analyzed using FLIR Tools software (FLIR, Wilsonville, OR, USA). Using the software, the following temperatures were taken: the mean temperature of an ellipse drawn within the anterior surface region of the eye; the maximum and mean of an ellipse drawn within the surface of the ear flap; along with the mean of an ellipse drawn encompassing the anterior surface of the nose ( Figure 2 ).

Infrared thermal images of a Labrador Retriever with ellipses drawn for ( a ) the eye and nose and ( b ) the ear flap.

2.4.2. Salivary Cortisol and IgA

Saliva was collected at T0, T1, and T2 using SalivaBio Children’s Swabs (Salimetrics, Carlsbad, CA, USA) to measure cortisol and sIgA. No stimulus was provided (e.g., toys/food) to avoid impacting the measures collected. The swab was inserted briefly into the left-side buccal cavity area of the dog’s mouth for 30–60 s before the tip was cut off and placed into the collection tube. This was repeated with the other end of the swab for the right-side buccal cavity and below the tongue. Both tips were placed in the same tube. The collection tube was immediately placed on ice and transported to the onsite laboratory. Samples were centrifuged at 4 °C before being stored at −20 °C in preparation for later analyses. The expanded range high sensitivity salivary cortisol enzyme immunoassay kit by Salimetrics (Salimetrics, Carlsbad, CA, USA) was used as per the kit protocol with an intra-assay variation of 5.1% and a limit of quantification of >0.04 µL/dL. The sIgA was analyzed using the Abcam IgA Dog ELISA Kit with an intra-assay variation between 4.2 and 7.4% and a limit of quantification of 4.02 ng/mL.

2.4.3. Temperature, Pulse, and Respiration (TPR)

TPR measurements were collected by the mock veterinarian at the end of the physical examination within the consultation room. Rectal temperature was collected using a Genia Digiflash Thermometer, while pulse and respiration were collected using a stethoscope. Readings were documented on paper for each dog and later manually entered onto an electronic spreadsheet.

Dogs also wore PetPace TM (Burlington, MA, USA) monitors to automatically capture heart rate and vasovagal tonus index (VVTI), a measure of heart rate variability, at 2 min intervals throughout the entire vet visit. A PetPace TM monitor collar was placed on the dog whilst they were situated in their familiar housing, prior to being led by their handler to the veterinary suite. The collar was then removed immediately prior to leaving the veterinary suite upon the completion of testing.

2.4.4. Dog Behavior

Dog behavior was recorded during the kennel wait time (Kennel) and the physical examination (Consult) using GoPro Hero 7 cameras mounted on tripods. The cameras were positioned in a standardized position in front of the kennel and either on the floor or on the examination table in the consultation room to best capture each individual dog for the duration of the experimental procedure.

Behavioral data were coded from video footage from the kennel room and consultation room. A QBA previously developed to evaluate dog welfare in shelter dogs [ 15 ] was modified slightly to include an additional term, “calm”, and was used to collect behavioral data during the dogs’ time in the kennel and during the health examination. The final QBA consisted of a list of 21 terms with associated characteristics that scorers used to rate each dog ( Table 1 ).

Qualitative behavioral analysis used to measure dog behavior in the kennel area.

The QBA was used to assess the overall level of intensity at which certain attributes were present during the dog’s time alone in the kennel and throughout the physical examination. Three trained raters who were familiar with dog behavior and body language were randomly assigned videos so that the behavior of all dogs was scored. Each rater was provided with scoring sheets (one for each video clip) on which Visual Analogue Scales (VAS) with lengths of 125 mm were placed next to each term. Raters were instructed to independently score each dog on every qualitative term on the list. The left end of the VAS scale corresponded to the minimum score (0 mm), meaning the expressive quality indicated by the term was entirely absent in the dog, whereas the right end represented the maximum score (125 mm), meaning that the quality indicated by the term was strongly dominant in that dog. Raters watched each assigned video using their laptops, and after each clip, they were encouraged to score the dogs’ expressions on the rating scales as quickly as possible by marking a cross on the VAS at the point they felt was appropriate. A score was assigned to each term for each video by using a ruler to measure the distance in millimeters between the minimum point of the VAS and the point where the observer marked the line.

To capture additional behavioral data during the physical examination, a scale previously developed to specifically evaluate dog behavior during a veterinary consultation was used. The Clinic Dog Stress Scale (CDSS) [ 13 ] ( Table 2 ) originated as a way to measure a dog’s behavior during an examination and is designed to be scored by a veterinary nurse or technician. The chart evaluates body regions that are involved in the stress response. A total of 36 points is possible. Dogs with high scores show signs of stress and may be considered distressed, while dogs who score low may be mildly stressed. Dogs who score zero are considered calm and relaxed [ 13 ].

Clinic Dog Stress Scale (CDSS) used to measure dog behavior during the health examination.

The same three trained raters were also responsible for scoring behavior using the CDSS via video footage of dogs during the physical examination (Consult). The raters were randomly assigned videos and instructed to rate each dog between 0 and 4 on a stress level score, across a range of dog body regions, according to the associated definitions.

To assess inter-rater reliability for the behavioral ratings, 15 videos were randomly selected to be scored in common by all raters. This resulted in nine videos watched in common for the CDSS (physical examination only) and fifteen videos for the QBA (kennel and physical examination). To assess intra-rater reliability, each rater re-scored a random selection of 10 videos from those they had previously scored, which resulted in repeat scores on ten videos for the QBA (kennel and physical examination) and five videos for the CDSS (physical examination only).

2.5. Statistical Analysis

Cortisol, IgA, and IRT (ear, eye, and nose temperature) measures were fitted to a linear mixed effects model, with the parameter as the response variable, treatment, timepoint, and their interaction as the fixed effects, and the individual dog as the random effect. Since up to three replicates were run of cortisol and IgA at each sample point, these values were averaged for analysis. This was to limit any bias that might have been introduced as more samples had insufficient saliva for multiple replicates in the later timepoints. Due to the practical limitations of collecting salivary cortisol, many data were missing. The data that were collected were categorized within exposures as well as within each timepoint, and a chi-squared test was used to see if there were any significant differences within these groups for the amount of missing data. Only complete data were included in the linear mixed effects models.

TPR measures were all measured once during the consultation, and so, a linear mixed effects model was fitted with the parameter as the response variable, treatment as the explanatory variable, and dog as the random effect. Due to large amounts of missing heart rate data from the Petpace TM monitors, these measures were unable to be analyzed.

Dogs were scored using the QBA at two timepoints: while dogs were kenneled prior to the consultation (Kennel) and during the veterinary health exam (Consult). These data were composed of scores ranging from 0–125 for a series of 21 different terms. These scores were summarized using a Principal Component Analysis (PCA) to create component scores ( Table S1 ). The first three component scores were then analyzed using linear mixed effect models, with the component score as the response variable, treatment, location, and the interaction between treatment and location as the fixed effects, and dog and observer as random effects. Additionally, questions related to the dogs’ behavior were measured at a single timepoint during the vet consultation on a scale from 0 to 4 (Clinic Dog Stress Scale). These data were analyzed using Kruskal–Wallis rank sum tests to determine if there were any differences in scores based on treatment. Scores were also categorized to represent dogs that were not stressed (score 0) or stressed (score 1+) for each of the questions. These data were then analyzed using logistic mixed effects models, with the parameter as the response variable, treatment as the fixed effect, and dog and observer as random effects.

To assess the intra- and inter-rater reliability of the behavioral measures, Intraclass Correlation Coefficients (ICCs) using a two-way mixed effects model and consistency agreement were calculated for each behavior (Clinic Dog Stress Scale) and component score (QBA).

Finally, to assess the relationship between all the collected measures, a PCA was conducted. Measures taken at different timepoints were treated as separate variables for the purpose of analysis. Where multiple measures were available at each timepoint (e.g., replicates of cortisol and IgA measures, or ratings from multiple raters for behavioral measures), the mean of the values was used ( Table S2 ). Missing values were imputed by the mean of the variable. All measures were scaled to unit variance. The first three component scores were then analyzed using linear mixed effect models, with the component score as the response variable, treatment as the fixed effect, and the dog as the random effect.

For all models, residuals were visually inspected to assess model fit. If assumptions for normality or homoskedasticity were violated, the model was re-run with a log transformation, and back-transformed means and confidence intervals are reported. In addition, where appropriate, the Tukey method was used to adjust the p-value to account for multiple comparisons.

All analyses were performed using R version 4.0.4 [ 42 ].

3.1. Physiological and Behavioral Measures

3.1.1. eye, nose, and ear temperature.

The models of eye, nose, and ear temperature using IRT all met model assumptions, and therefore, no transformation was required. Timepoint was significant for all the models ( p < 0.001), with eye, nose, and ear temperatures all increasing significantly from baseline (T0) to the post-kennel (T1) and post-physical examination (T2) timepoints. However, there were no significant differences in eye, nose, and ear temperatures between the post-kennel and post-physical examination timepoints, or between the treatment and control groups at the post-kennel or post-consult timepoints ( Figure 3 ). Dogs had significantly higher mean nose ( p = 0.010), maximum ear ( p = 0.004), and mean ear ( p = 0.002) temperatures at baseline, upon entering the veterinary suite during control visits, when compared to treatment visits. These differences decreased to a tendency for mean nose ( p = 0.098), maximum ear ( p = 0.110), and mean ear ( p = 0.087) temperatures at the post-kennel timepoint, and were non-significant by the post-physical examination timepoint (mean nose: p = 0.515; max ear: p = 0.311; mean ear: p = 0.127).

Predicted mean eye ( top left ), mean nose ( top right ), maximum ear ( bottom left ), and mean ear ( bottom right ) temperature values (+95% CI) during a mock veterinary visit measured at baseline (T0), post-kenneling (T1), and post-consult (T2) for both control visits and visits where music treatment was provided.

3.1.2. Salivary Cortisol and IgA

Chi-square analysis of the frequency of missing data for salivary measures indicated no significant differences between treatment and control groups ( p = 0.224). However, there was a significant effect of timepoint, with fewer successful saliva collections occurring as time progressed ( p = 0.020). Since successful collection was not associated with treatment group, we proceeded with only complete data for this analysis. When salivary cortisol and IgA data were analyzed, the residuals demonstrated a skewed distribution and heteroskedasticity, so a log transformation was used and resulted in improved model fit. The results indicated that both cortisol and IgA measurements increased significantly from baseline (T0) to the post-kennel (T1) and post-physical examination (T2) timepoints. There were no significant differences in cortisol or IgA between the post-kennel and post-consult timepoints, or between the treatment and control visits ( Figure 4 ).

Predicted back-transformed mean cortisol ( left ) and IgA ( right ) values (+95% CI) during a mock veterinary visit measured at baseline (T0), post-kenneling (T1), and post-consult (T2) for both control visits and visits where music treatment was provided.

3.1.3. Temperature, Pulse and Respiration (TPR)

The models of rectal temperature and heart rate met model assumptions, and therefore, no transformation was required. The assumptions for normality and homoskedasticity were not met for the model of respiration rate, so a log transformation was used and resulted in improved model fit. Heart rate ( p = 0.901) and respiration rate ( p = 0.512) did not differ significantly between control and treatment visits. However, rectal temperature measured during the veterinary consult was significantly higher during the control visits when compared to the treatment visits when music was played ( p = 0.009) ( Figure 5 ).

Predicted mean rectal temperature values (+95% CI) during a mock veterinary visit for both control visits and visits where music treatment was provided.

3.1.4. Dog Behavior

Analysis of the QBA data using a PCA suggested three main components of interest based on the strength of loadings and the variance explained ( Table 3 ). The first component explained 32.2% of the total variance and was labeled “stressed/anxious”. It comprised positive loadings for “stressed”, “anxious”, “nervous” and “wary”, and negative loadings for “calm”, “comfortable”, and “relaxed”. The second component explained 20.0% of the total variance and was named “interacting/engaged”, as it comprised positive loadings for “interested”, “curious”, “excited”, “explorative”, “playful”, and “sociable”. The third component, which explained 11.3% of the total variance, was named “afraid”, and comprised positive loadings for “fearful”, “hesitant”, and “depressed”, and negative loadings for “alert”, “bored”, “reactive”, and “aggressive” did not load strongly on any of the identified components.

Components extracted by the Principal Component Analysis (PCA) of Qualitative Behavior Analysis (QBA) scores. Loadings ≥ |0.50| are in bold.

Inter-rater reliability between the three trained raters showed moderate agreement for scores generated for the three identified components: PC1—Stressed/Anxious (ICC = 0.69), PC2—Interacting/Engaged (ICC = 0.68), PC3—Afraid (ICC = 0.58). Intra-rater agreement demonstrated good to excellent agreement for PC1—Stressed/Anxious (ICC = 0.81–0.99), moderate to excellent agreement for PC2—Interacting/Engaged (ICC = 0.68–0.98), and poor to excellent agreement for PC3—Afraid (ICC = 0.70–0.99).

When the generated component scores were analyzed using linear mixed models, they met model assumptions, and therefore, no transformation was required. There were no significant differences between the control and treatment groups for any of the components ( Figure 6 ). Dogs scored significantly higher for the “interacting/engaged” component during the physical examination compared to when they were in the kennel ( p < 0.001). Additionally, dogs scored significantly higher for the “afraid” component during the physical examination compared to when they were in the kennel ( p < 0.001).

Predicted component scores (+95% CI) for ( a ) PC1—Stressed/Anxious, ( b ) PC2—Interacting/Engaged, ( c ) PC3—Afraid based on QBA ratings during a mock veterinary visit measured when kenneled (Kennel) and during a veterinary consultation (Consult) for both control visits (Control) and visits where music treatment was provided (Treatment).

The inter-rater reliability of the behaviors measured using the CDSS ranged from poor to good depending on the behavior. Ear posture (ICC = 0.43), lips (ICC = 0.42), and gaze (ICC = 0.16) had poor agreement, body posture (ICC = 0.59) and activity (ICC = 0.54) had moderate agreement, and vocalizations (ICC = 0.83) and respirations (ICC = 0.80) had good agreement. Intra-rater reliability demonstrated that all behaviors had good to perfect agreement across the three raters (ICC = 0.83–1.00), apart from body posture (ICC = 0.71–1.00) and respirations (ICC = 0.67–1.00), which had moderate agreement to perfect agreement depending on the rater.

No significant differences in behaviors measured using the CDSS were found between the control and treatment visits except for lips ( Figure 7 ). There was a significant Kruskal–Wallis rank sum test for the overall lips score ( p = 0.033), and dogs had higher odds of being scored as stressed for lips (>0) during visits with music compared to control visits ( p = 0.020).

Histogram of distributions of ratings of dog behavior using the Clinic Dog Stress Scale (CDSS) during the veterinary consult for both control and treatment visits for ( a ) body posture, ( b ) ear posture, ( c ) gaze, ( d ) respirations, ( e ) lips, ( f ) activity, and ( g ) vocalizations.

3.1.5. Behavioral and Physiological Measures Combined

All data captured across the various timepoints throughout the mock veterinary visit were combined using a PCA. Three main components of interest emerged based on the strength of loadings and the variance explained ( Table 4 ). The first component was labeled “temperature” and explained 20.9% of the total variance. This component comprised positive loadings for all IRT readings for mean nose, maximum ear, and mean ear temperatures, as well as rectal temperature as measured during the health examination. This component also comprised negative loadings for salivary IgA at T1 and T2.

Components extracted by the PCA of all measures combined. Loadings ≥ |0.50| are in bold.

The second component was labeled “consult stress” and explained 12.1% of the total variance. This component comprised positive loadings for the QBA “Stressed/Anxious” component during physical examination in the consultation room, the QBA “Afraid” component during consult, “activity”, “gaze”, and “body posture” from the CDSS, and salivary cortisol at T2. This component also comprised negative loadings for the QBA “Interacting/Engaged” component during the health examination.

The final component was named “kennel confidence” and explained 9.7% of the total variance. This component comprised positive loadings for IgA at T1, and negative loadings for the QBA “anxious” component during kenneling.

When the generated component scores were analyzed using linear mixed models, there were no significant differences between control and treatment groups for any of the components ( Figure 8 ). There was a tendency for dogs to score lower for the “temperature” component during treatment visits compared to control visits ( p = 0.099). Additionally, there was a tendency for dogs to score lower on the “kennel confidence” component during treatment visits compared to control visits ( p = 0.060). There was no significant effect of treatment on the “consult stress” component ( p = 0.874).

Predicted component scores (+95% CI) for ( a ) PC1—Temperature, ( b ) PC2—Consult Stress, ( c ) PC3—Kennel Confidence based all combined measures collected during a mock veterinary visit for both control visits (Control) and visits where music treatment was provided (Treatment).

4. Discussion

The aims of the present study were to understand how canine stress changes during a veterinary visit, establish the effect bespoke music has on dogs who may be experiencing stress in this environment, and highlight measures which may be of practical use to evaluate dog wellbeing within a clinical setting. Overall, the results indicated that various physiological and behavioral parameters of canine stress increased over the course of a veterinary visit. Additionally, being physically examined in a consultation room appeared to elicit more fear-related behaviors compared to when dogs were housed alone in a hospital kennel. Bespoke music designed to entrain physiological parameters did not consistently decrease measures of stress in dogs, though it was associated with a significant reduction in rectal temperature.

4.1. Dog Physiology during a Veterinary Visit

Several physiological measures (eye, nose, and ear temperature, salivary cortisol, and salivary sIgA) increased over time, suggesting that not only are visits to the veterinarian stressful for dogs, but they may be increasingly stressed over time. Interestingly, dogs in the control groups generally had higher baseline temperatures than the treatment groups, which is most likely a random effect due to outside temperature. This difference in temperature between groups decreased over time and was not significant at the post-kennel and post-consult timepoints. This is likely due to increased time spent indoors and the effect of stress from the veterinary examination overcoming the effect of outside temperature. To mitigate the effect of outside temperature in future studies, researchers should either measure and control for outside temperature or allow dogs to acclimate to a standardized inside temperature before taking the IRT reading. Infrared thermography has been used in other studies as a tool to evaluate canine stress in a variety of situations, from being separated from caregivers [ 43 ], to experiencing pain [ 44 ], as well as visits to the veterinarian [ 4 , 45 ]. However, there are inconsistencies as to whether an increase or decrease in temperature is related to negative or positive emotional valence. This may be dependent on what body part the temperature is being taken from and whether the stressor is acute or chronic. The results obtained from the present study support previous findings in which canine eye temperature increased significantly during a veterinary examination [ 4 , 45 ], but in contrast, another study showed ear temperature decreased [ 43 ] in response to stress caused by a separation event. To better understand whether IRT is of value as a measure of emotional wellbeing, it is necessary to further validate these measures against other stress parameters.

In the present study, both salivary cortisol and sIgA measures also significantly increased from baseline compared to post-kennel and post-consult. Again, there are challenges with how to interpret these results, as sIgA has also been shown to both increase and decrease in dogs when they have been subjected to stressful situations. For example, when exposed to loud, novel noises, sIgA concentration decreased significantly immediately after and 30 min after the noise stress [ 46 ], converse to what was observed in the current study, where sIgA concentrations increased significantly 15 min post-stressor, i.e., when left alone and being physically examined. SIgA has also been used to determine guide dog suitability, with low concentrations of sIgA being indicative of a stress response. Dogs who were considered suitable guide dog prospects had increased concentrations of sIgA over time, indicating they were better able to adapt to their surroundings and were less sensitive to stress, compared with rejected guide dogs [ 47 ]. Similarly, in a separate study, decreased levels of sIgA were observed 10 days after dogs had been introduced to novel kennel environments, and these were in the opposite direction to cortisol concentrations [ 48 ], suggesting low levels of sIgA in dogs are related to stress. However, another study demonstrated that low levels of sIgA were related to high levels of dog trainability [ 49 ], which is unlikely to be possible if individuals were experiencing stress. The measure appears to be influenced by the duration and type of stressor, as well as time of day, reflecting the complex immune response to stress. It has also been stated that the perception of the stimuli can influence results and if perceived negatively can lead to a short-term increase in sIgA concentration [ 50 ]. A recent study concluded that it is not clear whether sIgA is a useful short-term measure of stress in dogs [ 51 ]. As such, it appears more research is required to better understand this parameter.

Similarly, interpreting salivary cortisol measures can also be challenging due to the various factors that influence this parameter [ 49 , 52 ], but there appears to be more consistent responses whereby cortisol concentrations increase in response to stress reflecting the activation of the hypothalamic–pituitary–adrenal (HPA) axis [ 12 ]. As such, obtaining cortisol concentrations is a common method to measure stress responses in dogs [ 53 , 54 , 55 ] and although it is affected by a range of factors, it provides valuable information on how an animal may be feeling when used in conjunction with other physiological and behavioral markers of stress [ 56 ]. The increases in salivary cortisol concentrations over time in dogs seen in the present study are similar to what has been observed in other studies [ 57 , 58 , 59 , 60 ] and is considered indicative of an increased stressed response, which is aligned with the direction of the IRT measures, yet, somewhat surprisingly, also the sIgA measures. In this study, there were no significant differences in cortisol concentrations at any timepoints between the two groups. Similar findings were observed when shelter dogs were exposed to classical music or no music [ 28 ]. However, in contrast to the present study, the shelter dogs spent less time standing and barking when exposed to music, suggesting music may have had a positive effect in reducing stress despite no changes in cortisol concentrations.

Core body temperature captured during the physical examination was significantly lower in the treatment group compared with the control group. This result is consistent with other studies which have previously used this measure in a range of animal species. Stress-induced hyperthermia is a common response that many mammals experience when faced with stressful stimuli [ 61 ], and core body temperature is a measure that can aid in quantifying stress responses in a range of animal species [ 62 ]. The results of this study suggest that bespoke music therapy may be successful in influencing this physiological parameter during veterinary consultations, therefore suggesting that dogs may feeling less stressed. However, it should be noted that as there were baseline differences in surface body temperature identified between the treatment groups using IRT, this difference may be spurious and not due to the music treatment. Since core temperature was only collected at a single timepoint, it cannot be determined whether there were baseline differences between the groups. A similar study found no significant differences in rectal temperature in dogs who underwent a clinical examination between groups who had owners who provided tactile and verbal interaction or groups that were provided with no interaction [ 4 ]. Despite this measure being a reliable way to evaluate stress in dogs, it may be challenging to capture as the method used (i.e., rectal thermometer) is likely to elicit mild stress in most individuals. A less invasive method would be of value. It has been demonstrated that the temperature of the tympanic membrane and ear canal measured using an infra-red thermometer is related to core body temperature [ 63 ]. Interestingly, ear temperature captured in the present study did not differ significantly between groups. However, the current study measured the temperature of the ear pinna, rather than the ear canal, which likely did not have as strong a relationship to core body temperature.

Unfortunately, due to large amounts of missing heart rate data from the Petpace TM monitors, analyses of these measures were not possible. This was disappointing as these data could have provided insights as to whether the tempo of music influenced the sympathetic nervous system and entrained heart rate in dogs but also whether heart rate was related to other parameters of interest. Further research into this would be warranted, ideally with wearable devices that measures continuous heart rate and heart rate variability. Heart rate and respiration rate were also measured at a single timepoint as part of the physical examination. These measures did not differ significantly between treatment and control, suggesting there was no effect of the treatment. However, without baseline measurements, it is not known whether music affected the change in heart rate over time. Interestingly, measurements taken during the examination indicated that the mean heart rates were 103, 93, and 79 bpm for small, medium, and large dogs, respectively. These readings are all lower than the predicted heart rates used to select the music tempo and may have contributed to the music not having an anxiolytic effect. If the music was faster than the dog’s heart rate during a stress event, it is likely the process of entrainment would not have been effective in lowering the dog’s heart rate. Furthermore, the average resting heart rate estimates were selected by combining heart rate data from the relevant dog breeds used in the study at Waltham, not the specific individual dogs who participated in the study. Future studies examining music entrainment would likely benefit from capturing resting heart rate measures from the individuals being evaluated.

Despite significant changes in physiological measures over time, they are complex to interpret as various factors can influence the data which may impact how effectively canine emotional state can be inferred. As such, it is necessary to evaluate these measures in conjunction with other physiological and behavioral parameters, to better understand and assess the positive and negative valence of dogs.

4.2. Dog Behavior during a Veterinary Visit

Dog behavior was captured using a QBA during the veterinary visit and a qualitative scale designed to evaluate canine stress specifically during a veterinary consultation (CDSS). There are pros and cons of using such tools, and alternative ways to measure behavior are routinely employed, such as coding of specific behaviors; however, this approach can be time consuming and is not particularly feasible to conduct in real time, or to get timely feedback. QBA is a useful method to quickly capture a holistic view of how a dog may be feeling. Recent research has suggested QBA is a reliable way of capturing behavioral data without the need for time-consuming video coding [ 64 ]. The present study relied on two qualitive scales rather than time-intensive video coding. It has been demonstrated that QBAs correlate with objective behavioral data [ 64 ], so it may not always be necessary to resort to annotating video footage to capture a range of behavioral variables. Based on the findings from this study, a number of terms were loaded together on the “stressed/anxious” component, suggesting they all measured similar responses. Inter-rater reliability for these component scores was moderate, with intra-rater reliability ranging from poor to excellent, with reliability being the highest in the “stressed/anxious” component. While observer was included as a random effect in the models in order to account for some of these differences between observers, reliability issues would still have contributed additional variation to the results and may have masked differences between the control and treatment groups. Since the QBA was being administered during a situation expected to elicit stressed/anxious responses, it is possible that reliability in the other components was low due to the infrequent occurrence of those behaviors. As such, the QBA could be refined to only include terms relevant in the components of interest. Therefore, terms from the “stressed/anxious” and “afraid” components, so seven or four terms instead of twenty, could be used in future to evaluate canine stress in a veterinary setting. However, the training of observers would be required to increase reliability.

Using output from the QBA, dogs scored significantly higher on the “afraid” component during the physical examination compared to being left alone in the kennel. Other studies support the finding that being in the consultation room can elicit fear and stress in dogs [ 5 , 8 ]. This is likely due to the fear-inducing nature of being restrained by a person and examined [ 65 ]. Not surprisingly, dogs scored significantly higher for “interacting/engaged” during the physical examination compared to when they were left in the kennel, suggesting that human presence and contact influences behavior. However, there were no significant differences in scores on the “stressed/anxious” component, which consisted of terms such as “stressed”, “anxious”, and “nervous”, between when dogs were left in the kennel and when they were physically examined in the consultation room. It could be expected that the veterinary examination would be more stressful for dogs; however, it is not surprising that social isolation for the population of dogs who were tested was equally stressful. These dogs are always housed with conspecifics, have regular interactions with people, and are not routinely left alone. As such, being left in a kennel on their own is likely to have induced stress. In this study, it appears the two different stressors were of equal magnitude, as measured by QBA. Interestingly, there were no significant differences between the control and treatment groups for any of the components, suggesting that bespoke music did not have a positive effect in reducing behavioral indicators of stress or fear in dogs during a veterinary visit.

Another potential alternative to time-consuming video coding is the use of simple scales that can be measured live or from video to categorize stress behaviors. The CDSS is a tool that has been developed to quantify the level of stress dogs experience during veterinary visits and examinations [ 8 , 13 , 66 ]; however, to the authors’ knowledge, this tool has not previously been assessed for reliability or validity. In the current study, the inter-rater reliability of the behaviors measured using the CDSS ranged from poor to good depending on the behavior. The behaviors that had the worst agreement were ear posture, lips, and gaze, which may have potentially been due to limitations of video angle and quality. As with QBA, observer was included as a random effect within the logistic regression models; however, reliability issues likely contributed additional variation to the results and may have masked differences between the control and treatment groups. It is possible that higher agreements could have been achieved with live scoring. As one of the objectives was to identify measures that can be easily applied into clinical practice, it would be worthwhile for future studies to further assess the reliability of the CDSS following live scoring by raters who have received intensive training. Similar to QBA, there were no significant differences in behaviors measured using the CDSS between control and treatment visits except for lips, where dogs had higher odds of being scored as stressed for lips during veterinary visits when music was played. This is opposite to what we would have expected if positive entrainment was taking place and more relaxed behavior occurred as a result. It is unclear as to why this occurred, and could be a spurious result, or may be due to multiple possible contributors to lip licking, including anticipation of food, increased salivation, or social communication. Additionally, lips had poor inter-rater agreement, which may have also contributed to the findings. There were some slight differences in body posture and gaze, indicating more dogs scored highly in the control group. This would indicate these dogs were highly stressed, suggesting music may have had a positive effect. However, these differences were small and not statistically significant so may have been due to chance. Future studies using the CDSS should consider larger sample sizes to be able to have sufficient power to detect significant differences between groups. If this tool was to be used more broadly in clinics, it is important to be aware of its limitations as a measure of stress. Future research which investigates this tool further, along with the effect music has on dog behavior during a health examination, would be of value.

4.3. Combining Behavioral and Phsyiological Measures

To gain a holistic view of the effect of music on the emotional state of dogs in a clinical setting, as well as how the different measures relate to each other, a PCA was run combining all the measures. The output of this PCA identified three primary components labeled “temperature”, “consult stress”, and “kennel confidence”. The first component, “temperature”, indicated that core body temperature loaded positively, along with ear and nose temperature, while IgA loaded negatively. This suggests that these parameters are likely to be measuring the same thing, related to a physiological response, possibly due to stress, activity, or external temperature. There was a tendency for dogs to score higher on this measure during control visits, indicating a potential for music to have had a stress-reducing effect. As such, this may support the use of a less invasive approach to measuring body temperature to evaluate canine stress. Surprisingly, these measures did not load on other dimensions related to canine stress or anxiety, which may suggest they are instead indicative of differences between these groups for other confounding variables, such as external temperature.

The second component, “consult stress”, indicated that measures from the CDSS positively correlated with the QBA components “afraid” and “stressed/anxious”, along with cortisol measures, and negatively associated with “interacting/engaged”, suggesting all these measures were capturing an element of canine stress during a veterinary consultation. In line with the individual results for these measures, music did not have a significant effect on this component score, suggesting that the bespoke music was not sufficient to reduce signs of stress during the veterinary consultation.

The final component, “kennel confidence”, indicated that sIgA taken after dogs had spent time in the kennel loaded positively, while the QBA “stressed/anxious” component loaded negatively, suggesting lower levels of sIgA are related to stress, as supported by other research studies [ 46 ]. When the effect of music was analyzed, there was a tendency for dogs to score lower on this component when exposed to music, indicating higher levels of stress. The findings suggest canine stress is apparent during a mock veterinary visit, and the intensity can change depending on the event occurring during the visit. It is also important to recognize that some physiological measures, e.g., body temperature, may provide more reliable data than behavioral parameters which vary considerably between individuals [ 67 ] and therefore should be included in future studies examining the effect of interventions aimed at reducing canine stress.

Despite our hypothesis, there is limited evidence to suggest a significant positive effect of bespoke music treatment on any of the behavioral measures captured, and only one physiological measure differed significantly between the groups. These results may be due to the small sample size, the measures used, the intensity of the stressor, or that music did not have a calming effect. Similar results were obtained whereby no significant differences in behavior or physiology were observed between groups of dogs who were exposed to classical, dog relaxation music and no music within a veterinary hospital [ 26 ]. Further, it appears there is only weak evidence to suggest that classical music has the ability to reduce stress in dogs in a clinical setting [ 24 ]. Other reasons may be attributed to how the music was perceived by the dogs. This may be influenced by dog breed morphology, the shape of the dogs’ head and ears [ 19 ], as well as their hearing ability. Dogs’ hearing was not specifically tested during this study, which may have influenced the results. Additionally, surface materials, room dimensions, and room shape all influence auditory stimuli. Hard surfaces, especially metal and hard plastic, cause reflections, frequency shift with early reflections, and delays/echoes, and parallel walls induce more acoustic bounce back, which alters audio [ 66 ]. Indeed, recordings of the music being played in the kennel showed evidence of short room reverb and delays (echo effect), which could have impacted entrainment. Other clinics are likely to have similar environments and therefore would be likely to face similar limitations with acoustics.

4.4. The Future of Canine Stress Evaluation and Management in a Clinicial Setting

It would be of benefit to have pets wearing non-invasive devices that rely on technology to accurately measure a range of physiological and behavioral parameters. Unfortunately, in the present study, Petpace™ was unable to provide adequate readings for analyses. Technology is increasingly being used to monitor animal welfare; this is particularly evident within the livestock industry, where a range of monitoring systems are available to farmers as a way to evaluate their animals, ensuring optimal welfare and productivity [ 68 ]. Small devices such as accelerometers are also used in the pet industry. They commonly attach to collars and accurately capture location and movement and are being developed further using machine learning to accurately detect other behaviors [ 69 ]. Recent advances in pet technology mean that these types of devices, along with other types of wearables (harnesses, etc.), are likely to be readily available in future and capable of efficiently capturing a range of data from pets. Combined with owner and/or staff questionnaires, along with the use of machine learning to automatically quantify key behaviors via video, these approaches have the potential to provide accurate evaluations of pet emotional state in real time within the veterinary environment. As such, interventions aimed at alleviating canine fear and stress can be evaluated accordingly.

When considering music therapy as an intervention to improve pet wellbeing, it is important to be mindful of individual preferences. Some dogs may not like the music or have negative associations due to previous experiences, in which case, this could have a negative impact. One study demonstrated that auditory stimulation, in the form of classical music, improved HRV by a reduced RR variability, suggesting the novel music exposure may have had an excitatory rather than a calming effect [ 70 ]. Therefore, a more appropriate approach may be to first expose dogs to a particular type of music in a familiar and relaxing environment before they are subjected to a stressful event. For example, using the principal of classical conditioning, a neutral stimulus—music—could be played immediately prior and during activities that bring the individual pleasure and relaxation, e.g., feeding, playing, resting, and petting/attention. It could be expected that upon repeated exposures that music becomes a conditioned stimulus and produces feelings of pleasure, relaxation, and calmness. This approach has practical applications for pet owners who may wish to help calm their pet during a veterinary visit. This approach has been used with success in parents and children during a hospital visit [ 71 ] and also as a way to facilitate feeding in premature infants [ 72 ], but to our knowledge, has not been explored in detail in non-human animals. It is known that dogs’ experiences at the veterinary clinic will influence whether or not they are afraid or aggressive [ 73 ], so providing them with positive experiences will help to make them feel more relaxed. Enabling the choice to not listen to music would be of value in future studies aimed at ascertaining if music therapy (or not) improves dog welfare [ 19 ] and should be considered by professionals who currently use music in a clinical setting.

5. Conclusions

The present findings suggest being left alone in a kenneled area within a veterinary clinic and subsequently undergoing a heath examination appears to be stressful for a population of dogs and these events may elicit different levels of stress. It is important to understand how clinicians, staff, and caregivers can alleviate stress in dogs during veterinary visits. It is still unclear if bespoke music has a positive effect on dogs within a clinical setting, but when designing such studies, it is important to consider study design, ensuring adequate subjects are tested and appropriate measures are captured, along with how the testing environment may impact how music is perceived by the animals. Feasible measures that can provide the accurate, real-time assessment of canine stress will help clinicians better understand the effect interventions, such as music, have on improving canine emotional wellbeing in a veterinary environment.

Acknowledgments

The authors thank the staff and pets at the Waltham Petcare Science Institute for enabling this study. In particular, we thank Steph McKay, Laura Richardson, Quentin Garrigues, Beth Brougham, Emily Norton, Amelia Wagstaff, Hayley Mogg, Rachel Manning, and Natalie Hewitt for their technical support in collecting the data. We thank Emma McCluskey and Nathan Czyzewicz for laboratory analyses, along with Laura Carvell-Miller and Amandine Schmutz for statistical support, as well as Alex Peters for the infographic. Finally, we acknowledge Erika Csoltova for her assistance during the pilot study which preceded this main study.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ani12020187/s1 , Audio S1: SmallDogMusic; Audio S2: MedDogMusic; Audio S3: LargeDogMusic; Table S1: QBAData; Table S2: AllData. Additionally, music playlists can be accessed for free via HealthTunes https://www.healthtunes.org/signup (accessed on 28 November 2021) and visiting healthtunes.org/code (accessed on 28 November 2021) and entering code FH2021.

Author Contributions

Conceptualization, T.K.; methodology, T.K. and A.B.G.H.; formal analysis, H.E.F.; investigation, A.B.G.H.; resources, A.B.G.H. and W.T.W.; data curation, H.E.F.; writing—original draft preparation, T.K.; writing—review and editing, T.K., A.B.G.H., H.E.F., W.T.W., and D.W.L.; supervision, D.W.L. All authors have read and agreed to the published version of the manuscript.

This research was funded by Mars Petcare UK.

Institutional Review Board Statement

The study was reviewed by the Waltham Petcare Science Institute Animal Welfare and Ethical Review Board (study number PPM 63406). All dogs were housed and maintained according to the UK Code of Practice for the Housing and Care of animals bred, supplied, or used for scientific purposes.

Informed Consent Statement

Not applicable.

Data Availability Statement

Conflicts of interest.

The authors are employees of Mars Petcare (T.K., H.E.F., A.B.G.H., and D.W.L.), a provider of veterinary care, and HealthTunes Inc. (W.T.W.), an audio streaming service provider.

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