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West Highland White Terriers under primary veterinary care in the UK in 2016: demography, mortality and disorders

Background The West Highland White Terrier (WHWT) is a relatively common breed in the UK, although Kennel Club registrations have declined in recent years. The VetCompass™ Programme collates de-identified clinical data from primary-care veterinary practices in the UK for epidemiological research. Using VetCompass clinical data, this study aimed to characterise the demography, longevity and common disorders of WHWTs under primary veterinary care in the UK. Results WHWTs comprised 6605/905,544 (0.7%) dogs under veterinary care during 2016 from 886 clinics. Mean adult bodyweight was 9.6 kg (standard deviation [SD] 1.8 kg). Males (10.1 kg, SD 1.8 kg) were heavier than females (9.0 kg, SD 1.6 kg) (P < 0.001). Median age was 7.8 years (interquartile range [IQR] 4.3–11.1). Median longevity was 13.4 years (IQR 11.0–15.0). Males (13.8 years) outlived females (12.9 years) (P = 0.045). The most common grouped causes of death were lower respiratory tract (10.2, 95% CI: 5.5–16.7), neoplastic (10.2, 95% CI: 5.5–16.7) and spinal cord disorder (7.8, 95% CI: 3.8–13.9). Overall, 71.5% WHWTs had > 1 disorder recorded during 2016. The most prevalent specific disorders were periodontal disease (15.7, 95% CI: 14.1–17.3), otitis externa (10.6, 95% CI: 9.3–12.0), overgrown nails (7.2, 95% CI: 6.2–8.4), allergic skin disorder (6.5, 95% CI: 5.5–7.7) and obesity (6.1, 95% CI: 5.1–7.2). The most prevalent grouped disorders were cutaneous (22.7, 95% CI: 20.9–24.6), dental (17.8, 95% CI: 16.2–19.6) and aural (12.3, 95% CI: 11.0–13.8). The median age of dogs affected with the 27 most common disorders varied from 6.7 (pododermatitis) to 13.9 years for cataracts. Conclusions These findings highlight that, despite a recent decline in popularity, WHWTs are still relatively common in the UK. Dental disease, ear disease, overgrown nails, allergic skin disorder and obesity were identified as common health issues within the breed. Cutaneous disorders were the most common disorder group in the breed but showed a lower prevalence than might be expected. These results can be used by breeders, veterinary practitioners and owners as an evidence base to predict, prevent and manage key health and welfare issues for WHWTs.


Plain English Summary
West Highland White Terriers (WHWTs) are a relatively common dog breed in the UK, although Kennel Club registrations have declined in recent years. There are reported predispositions in WHWTs to 42 disorders, most notably skin disorders. However predisposition does not necessarily mean that a disease is common or even important for the breed. Using veterinary clinical data from the VetCompass™ Programme at the Royal Veterinary College, this study aimed to describe the demography and frequency of common disorders of WHWTs under primary veterinary care in the UK.
This study documents the WHWT as still being a relatively common dog breed in the UK, although its popularity is in steep decline. The WHWT is shown to be a long-lived breed. Dental disease, ear disease, overgrown nails, allergic skin disorder and overweight were identified as common health issues within the breed. Skin disorders were the most common health group issue. These results can provide useful evidence to veterinarians and owners in order to improve the health and welfare of WHWTs.

Background
The West Highland White Terrier (WHWT) was developed from a white strain of Cairn Terrier bloodlines in the mid-19th century in Argyllshire, Scotland. Over time, the breed gradually moved towards a shorter body and higher tail carriage than the traditional Cairn Terrier and was recognized formally as a distinct breed in 1907 by the Kennel Club (KC) [1]. Although still a relatively common breed in the UK, KC registrations for WHWTs have declined in recent years. During the 10-year period 2008-2017 inclusive, registrations decreased 70.8% from 2.7 to 0.9% of total KC registrations. In contrast, the same 10-year period oversaw substantial increases in registrations for some other similar-sized breeds to the WHWT, including the Pug, Bulldog, French Bulldog and Miniature Smooth Dachshund suggesting competing impacts from appeal for the same group of potential owners [2]. However, these data just describe the KC registered subset of the breed and do not take account of changing popularity among the wider, and often nonregistered, subset of the WHWT population that have been largely unaccounted to date.
The WHWT is considered a long-lived breed with a median longevity of 13.5 years that compares favourably with the median of 12.0 across all breeds [3]. A survey of owners of pedigree dogs in the UK identified the most common causes of death/reasons for euthanasia in WHWTs as old age (14.6%) and kidney failure (8.3%) [4]. This contrasts with an owner survey of the general population of WHWTs in the US that reported the most common diseases WHWTs died with as atopic dermatitis (31.1%), pulmonary fibrosis (10.5%) and congestive heart failure (9.1%) [5]. Despite impressive longevity, the WHWT is reportly predisposed to 42 disorders including aggression, atopic dermatitis, craniomandibular osteopathy, keratoconjunctivitis sicca and bronchiectasis [6]. The WHWT is reported as the dog breed with the second-lowest level of genetic heterozygosity in the UK suggesting a high level of inbreeding which may be associated with some of these disease predispositions, although there is not a clear correlation between heterozygosity and the level and severity of inherited disease overall within breeds [7,8]. In a WHWT health survey in the US, owners reported atopic dermatitis as the most common disease of this breed (23.2% affected) followed by luxated patella (5.5%) and aggression (3.9%) [5]. These results differ slightly to a KC breed health survey in the UK where the most commonly reported conditions were hypersensitivity (allergic) skin disorder (8.6%), dermatitis (4.7%), chronic itching (3.8%) and otitis externa (2.9%), although it is possible that many of these reported conditions were related to underlying allergic dermatitis and otitis [4]. Keratoconjunctivitis sicca (2.4%), cruciate disease (1.8%) and patellar luxation (1.8%) were other commonly recorded disorders in the UK [4].
The KC's Breed Watch scheme serves as an 'early warning system' to identify points of concern for individual breeds and classifies WHWT as a category 2 breed with two points of concern for special attention by judges: skin irritation and misplaced lower canines [9]. The WHWT has been identified world-wide as a breed predisposed to canine atopic dermatitis [10] albeit with some variability in the level of predisposition between populations in different geographic locations [10,11]. Atopic dermatitis is a chronic, inflammatory and pruritic skin disease with a complex pathogenesis that includes allergic pathways in the majority of affected dogs [12]. It is recognised that the life-long nature of the disease, its complications, and associated financial costs are challenging, even a burden, for affected dogs and their carers, and a challenge for clinicians [13,14], despite the expanding treatment options for this disease [15]. A recent study that developed a metric to summarise welfare compromise and total impact of disease in individual animals estimated that atopic dermatitis had by far the highest score out of the 10 canine diseases studied, even though euthanasia due to the disease was not factored into the estimate [16]. The documented breed predisposition and impact of this kind of allergic skin disease is reflected in the focus on skin disease by the KC as a priority for the WHWT, although much of the current evidence has been derived from referral veterinary care and owner survey data sources [9]. Clinical data derived from primary veterinary care databases has been suggested to offer an additional perspective that combines the strengths of veterinary-quality diagnoses with study populations that are representative of the wider population [17,18].
Using veterinary clinical data from the VetCompass™ Programme [19], this study aimed to characterise the demography, longevity and common disorders of West Highland White Terriers under primary veterinary care in the UK. The study placed special focus on exploration of health associations with age and sex. These results could assist breeders, veterinary practitioners and owners with an evidence base on the wider general population to predict, prevent and manage key health and welfare opportunities for WHWTs.

Materials and methods
The study population included all available dogs under primary veterinary care at clinics 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 electronic patient record (EPR) data from primary-care veterinary practices in the UK for epidemiological research [19]. Data fields available for the study included a unique animal identifier along with species, breed, date of birth, sex, neuter status and bodyweight, and also clinical information from free-form text clinical notes, summary diagnosis terms [20] and treatment with relevant dates.
A cohort study design was used to estimate the oneyear (2016) period prevalence of the most commonly diagnosed disorders [21]. Sample size calculations estimated that 2069 dogs would need to be sampled from a population of 6605 dogs in order to estimate the prevalence of a disorder affecting 3% of the dogs with 0.5% acceptable margin of error at a 95% confidence level [22]. Ethics approval was obtained from the RVC Ethics and Welfare Committee (reference number 2015/1369).
Dogs recorded as West Highland White Terrier breed were categorised as West Highland White Terrier and all remaining dogs were categorised as non-West Highland White Terrier. No distinction was made between Kennel Club registered and unregistered individuals. Adult Bodyweight described the mean bodyweight (Kg) recorded from all bodyweight data for dogs aged over 18 months at the time of weighing and was categorised into 5 groups (< 7.0, 7.0 to < 9.0, 9.0 to < 11.0, 11.0 to < 13.0, ≥ 13.0). Neuter described the status of the dog (entire or neutered) at the final EPR. Age described the age (years) at the final date under veterinary care during 2016 (December 31st, 2016) and was categorised into 5 groups (< 3.0, 3.0 to < 6.0, 6.0 to < 9.0, 9.0 to < 12.0, ≥ 12.0).
The list of unique West Highland White Terrier animal identification numbers was randomly ordered and the clinical records of a randomly selected sample of animals were reviewed manually in detail to extract the most definitive diagnoses for all disorders recorded as existing during 2016 as previously described [23]. Elective (e.g. neutering) or prophylactic (e.g. vaccination) clinical events were not included. No distinction was made between pre-existing and incident disorder presentations. Disorders described within the clinical notes using presenting sign terms (e.g. 'vomiting' or 'vomiting and diarrhoea'), but without a formally recorded biomedical diagnostic term, were included using the first sign listed (e.g. vomiting). Mortality data (recorded cause, date and method of death) were extracted on all deaths at any date during the available EPR data. The extracted diagnosis terms were mapped to a dual hierarchy of diagnostic precision for analysis: fine-level and grouped-level as previously described [23]. Briefly, fine-level 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 terms mapped the original diagnosis terms to a general level of diagnostic precision (e.g. inflammatory bowel disease would map to gastro-intestinal).
Following data checking for internal validity and cleaning in Excel (Microsoft Office Excel 2013, Microsoft Corp.), analyses were conducted using Stata Version 13 (Stata Corporation). The sex, neuter status, age and adult bodyweight for WHWTs under veterinary care during 2016 were described. Annual proportional birth rates described the relative proportion of WHWTs compared with all dogs that were born in each year from 2004 to 2015 from the cohort of dogs under veterinary care in 2016. All-age bodyweight data with associated dates were used to generate individual bodyweight growth curves for male and female WHWTs by plotting age-specific bodyweights and were overlaid with a cross medians line plot using the Stata mband command.
One-year period prevalence values were reported along with 95% confidence intervals (CI) that described the probability of diagnosis at least once during 2016. The CI estimates were derived from standard errors based on approximation to the binomial distribution [24]. The median age at the end of the study date range was reported for affected animals. Prevalence values were reported overall and also separately for males and females. The chi-square test was used to compare categorical variables and the Students t-test or Mann-Whitney U test to compare continuous variables as appropriate [24]. Statistical significance was set at the 5% level. The mean was reported for continuous data that were normally distributed; otherwise the median was reported [24].

Demography and mortality
The study population of 905,544 dogs under veterinary care attending 886 clinics in the vetCompass database during 2016 included 6605 (0.7%) WHWTs. Annual proportional birth rates showed that WHWTs decreased in popularity from 1.69% of the annual Vet-Compass birth cohort in 2004 to 0.43% in 2015 ( Fig. 1).

Discussion
This is the largest study to date using primary-care veterinary data to report on WHWT health. The study characterised the demography of 6605 dogs and the longevity and common disorders of 2058 WHWTs under primary veterinary care in the UK. The median age of WHWTs was 7.8 years, suggesting that this was an ageing population compared with previously reported median ages of Labrador Retrievers (4.9 years) [25], German Shepherd Dogs (4.7 years) [26] and Rottweilers (4.5 years) [27] which showed younger profiles. The most common causes of mortality were lower respiratory tract disease, neoplasia and spinal cord disorders. The most prevalent fine-level disorders of WHWTs were periodontal disease, otitis externa, overgrown nails, allergic skin disorder and obesity. At a grouped level, the most common disorders were cutaneous, dental, aural, claw/nail and musculoskeletal. These results reiterate the power of primary-care records to highlight common events within breeds and expand the evidence-base on breed-related health in dogs [18]. The findings can provide breeders, veterinary practitioners and owners with a generalisable evidence-base to improve health and welfare for WHWTs.
The WHWT showed a median longevity of 13.4 years in the current study, which is in line with a previous report of 13.5 years for the WHWT and higher than the median longevity of 12.0 years reported across all breeds [3]. As a smaller-sized breed, the longevity of the WHWT benefits from the inverse association between increasing bodyweight and longevity [3,28]. It is worth noting that longevity values using the methodology of the current study will be biased upwards for breeds such as the WHWT that are declining in popularity whereas the converse effect will occur for breeds that are rising in popularity [29]. The median longevity of males (13.8 years) was almost 1 year longer than females (12.9 years). This male longevity advantage in the WHWT is unusual across dog breeds and is in contrast to previous reports in individual breeds that reported no sex difference in Labrador Retrievers [25] or French Bulldogs [30] or that conversely showed a female advantage for Rottweilers  [27] and German Shepherd Dogs [26]. These contrasting results across breeds demonstrates that the female longevity advantage that has been previously reported in dogs is not universal across breeds and each breed needs to be considered individually in terms of sex-associated longevity [31]. It is important to distinguish between prevalence and predisposition when interpreting results from epidemiological studies [6]. Prevalence is an absolute value that defines the overall frequency of a condition whereas predisposition is a relative value that describes the risk in one group compared to another [32]. A disorder may be highly prevalent within a particular breed (i.e. the disorder is common in the breed) and therefore can be considered as an important issue for the welfare of the breed without necessarily exhibiting a specific predisposition (i.e. the disorder is no more common in this breed than in dogs overall). Conversely, the breed may be predisposed to the disorder (i.e. the breed has a much higher relative risk of the disorder than dogs overall) but without the disorder being common (i.e. it need not be important to the breed) [33]. For the purposes of the current paper, an increased probability of disease compared with dogs overall or with breeds of a similar body size was accepted as evidence of disease predisposition [6] and preference was given to discussion of disorders that were either or both common and predisposed.
Lower respiratory tract disease and neoplasia were the most common causes of death in WHWTs in the current study, each accounting for 10.2% of deaths. Given that neoplasia accounted for 16.5% of deaths in dogs overall and 14.7% of deaths in Miniature Schnauzers, a similar-sized breed to the WHWT, in previous VetCompass reports [3,33], the current study does not suggest that the WHWT is predisposed to neoplasia in general. The prevalence of lower respiratory tract disease, however, was much higher in the current study than a previous report estimating mortality due to respiratory conditions at 3.9% across all breeds [3]. This suggests that lower respiratory disease is a significant life-ending issue for the WHWT and this view is supported by the literature. An owner survey in the US reported that 10.5% of WHWTs died with pulmonary fibrosis [5]. Idiopathic pulmonary fibrosis (IPF) is a chronic, progressive interstitial lung disease that carries a poor prognosis and the WHWT has been reported as strongly predisposed [34,35]. Therefore, it is possible that IPF accounted for much of the mortality due to lower respiratory tract disease seen in the current study. The most prevalent fine-level disorder in the current study was periodontal disease, with 15.7% of WHWTs affected. This is comparable to results for the Cavalier King Charles Spaniel (15.2%) and Border Terrier (17.6%) but higher than values reported for larger sized breeds such as Labrador Retriever (4.2%) [25], German Shepherd Dog (4.1%) [26] and Rottweiler (3.1%) [27]. The prevalence of periodontal disease has been reported to increase with age, decrease with increasing body size [36] and increase with dental malocclusion [37]. The KC breed standard describes the WHWT with teeth "large for size of dog" [1] which could predispose to malocclusion and therefore promote dental disease. Indeed, misplaced lower canines are cited in the KC Breed Watch system as points of concern for special attention by judges [9]. Consequently, the ageing population in the current study, the smaller size of breed and the dental profile of WHWTs contribute to make the 15.7% prevalence of periodontal disease unremarkable and suggests that dental disease is a common and important disease for the WHWT but that the breed is not particularly predisposed to the condition compared with other similar sized breeds.
Six of the 27 most common fine-level disorders (otitis externa, allergic skin disorder, pododermatitis, pyoderma, atopic dermatitis and dermatitis) represent various clinical manifestations of inflammatory skin disease, and have a combined prevalence of 28%. Whilst otitis externa, pododermatitis and pyoderma may occur in isolation and may be aetiologically unrelated, they frequently represent manifestations or complications of an underlying allergic skin disease, specifically atopic dermatitis [38,39]. The terms allergic skin disease, atopic dermatitis and dermatitis represent differing levels of aetiological specificity [38]. If these six common finelevel disorders are thus viewed as related to each other within the context of allergic, and more specifically atopic, dermatitis, their combined prevalence in this study may conceal a higher prevalence of true atopic dermatitis in the UK population than the 2.5% prevalence of formally diagnosed atopic dermatitis reported in this study might suggest. Indeed, based on a systematic review of frequency data from different populations, the WHWT has been identified as globally predisposed to atopic dermatitis [10], and 23.2% of WHWTs in the US were described as affected in an owner reported survey [5]. Methodological differences between studies reporting disease frequency data render direct comparisons difficult [10]. Diagnostic term substitution can describe the phenomenon whereby multiple correct but varying alternative biomedical diagnostic terms may be recorded appropriately for any single disorder event. As described above, this phenomenon may result in apparent underrepresentation of a complicated disease such as atopic dermatitis in this study when many true instances of the disease may be recorded using other terms that fall under the diagnostic umbrella relating to allergic dermatitis. This phenomenon may also affect breeds differentially, as breed-specific phenotypes of atopic dermatitis are recognized [11,39]. WHWTs are reportedly more often affected with widespread skin lesions than other atopic dogs [39], and as a result may show underreporting of associated distinct disorders such as otitis externa. Otitis externa was the second most prevalent disorder diagnosed in WHWT, affecting 10.6% of the current study population which is comparable to the 10.2% prevalence reported in dogs overall [23]. A survey of owners conducted by the KC reported a much lower prevalence of 2.87% in the WHWT [4] although biases in owner reporting may in part account for this difference [40]. In summary, the complexity of allergic skin disease in terms of its aetiologies, diagnostic definitions, criteria and associated skin infections [12,38,41,42], in combination with the variable use of terminology in clinical practice, add to the challenge of accurately documenting the frequency of this group of disorders from primary care clinical records.
It is noteworthy that the prevalence of cutaneous disorders at a grouped level was 22.7%, which is higher than the 15.5% reported across all dogs [23] and also higher than previous reports on other similarly smallsized breeds including French Bulldog (17.9%) [30], Pug (15.6%) [43] and Border Terriers (10.2%) [44]. Therefore, this study supports the body of evidence that skin disorders are a significant health issue for the WHWT, albeit that the current study does not highlight the predisposition to be as marked as previously reported. This difference may relate to internationally differing disease profiles in breeds because many of the previous studies were conducted outside the UK. It is also possible that the decreasing popularity of the WHWT over the past decade may have reduced the selection pressure on the breed and allowed the use of genetically and physically healthier stock such that the dermatological health of the breed is genuinely improving.
In the current study, the prevalence of KCS was 2.0%, cruciate disease was 1.8% and diabetes mellitus was 1.2%. Although these conditions were not at the top of the list of the most common disorders within the breed, each of these results support a breed predisposition compared with prevalence values in other small sized breeds [30,33,43,44]. The results also suggest that these diseases are important clinically to the WHWT because of their reasonably high absolute prevalence values. For these reasons, these disorders warrant inclusion within the lists of priority disorders for control and management in the WHWT by breeders, veterinarians and owners. Some sex-related differences were identified in the WHWT in the current study. Male WHWTs were more likely than females to be diagnosed with otitis externa (12.2% vs 8.7% respectively) and aggression (2.8% vs 1.1% respectively). A sex-related difference in otitis externa has not been previously identified in breed studies that used a similar design to the current study [25][26][27]33]. However, a male predisposition to aggression is supported by a substantial body of evidence [26,27,48,49]. Conversely, females had a higher prevalence of periodontal disease than males (17.7% vs 14.0% respectively). A female predisposition to periodontal disease was also identified in the Miniature Schnauzer [33]. The discovery and reporting of sex-based prevalence differences highlight that certain disorders may benefit from specific focus on preventive and remedial control within sexes to optimise health and welfare improvements. No sex association was detected for atopic dermatitis, which is in agreement with a previous study exploring risk factors for the disease [50]. The ageing population in the current study, with a median age of 7.8 years for the WHWTs overall, reflects declining popularity of the breed in the wider general population of dogs. A similar pattern of declining KC registrations in recent years has been reported [2]. It is possible that the veterinary profession may have contributed to declining popularity of WHWTs by emphasising poor health in the breed to their clients, especially in relation to skin disease. However, the frequency of skin disease in the current study is not as marked as might be expected. It is possible that veterinary opinion has been influenced by an element of cognitive bias because veterinary clinicians are presented with the most severely affected and recurrent cases. The results of the current study might suggest that the decline in popularity of the breed has led to more regulated breeding and thus a reduction in inherited cutaneous disorders. This could be an area for future research and is relevant to breeds such as the Pug, French Bulldog and Bulldog, which are currently increasing in popularity, but may face declining populations in the future for similar health-associated reasons [30,43].
The application of "big data" using anonymized clinical records from primary-care veterinary practice is radically changing how epidemiological research on companion animals is conducted [19,[51][52][53]. Previously, much of the data used in companion animal research were sourced from referral practice, pet insurance databases or from questionnaires that are subject to substantial selection bias. Although useful, studies based on these resources often had limited scope to generalize results from these skewed populations under examination to the wider general population [18]. Although also not without limitations, primary-care data research offers much better generalizability. To date, primary-care clinical data on companion animals have offered opportunities for research on prevalence in species overall [23,54] as well as within individual breeds [33]. These data have also been used for studies to explore specific disorders [55,56], drug therapy [57], longevity [3], demography [58], methodology [18,[59][60][61] and human translational studies [62]. The current study adds to this increasing body of evidence derived from primary care clinical data that is providing a new perspective on the health and care of companion animals.
There were limitations to methodology in the current study, some of which have been explored previously [33,63]. A final biomedical diagnosis is not always reached, or often even required, in primarycare veterinary practice for successful clinical management [64,65]. Consequently, many 'diagnoses' reported in the current study were, in reality, presenting signs. As discussed above, fragmentation of disorders recorded across multiple terms may have resulted in under-estimation of some precise diagnostic terms such as atopic dermatitis. Analysis and reporting at the precision of both fine-level and grouped-level terms aimed to limit the inferential impact of this diagnostic hierarchical phenomenon [23]. There are a proportion of dogs in the general population that are not registered with, or likely to present to, primary-care veterinary practices. If the prevalence of, and risk factors for, disease in this group differs to the subset that are under veterinary care, then the results of the current study may not generalise well to this unrecorded group. As discussed, the median age of WHWTs in the current study was 7.8 years and therefore the results may be skewed towards disorders of older dogs.

Conclusion
This study of over 6,000 WHWTs under primary veterinary care highlighted that, despite a recent decline in popularity, the breed is still relatively common in the UK. The WHWT is a long-lived breed. Lower respiratory tract disease is a common cause of death and therefore warrants consideration as a significant health issue within the breed. The most prevalent disorders identified were periodontal disease, otitis externa, overgrown nails, allergic skin disorder and obesity. Some important sex-associated differences were identified, with males living significantly longer than females. Although cutaneous disorders were the most common disorder in the breed at a grouped level, their prevalence was lower than might be expected which may suggest that the negative impact of cutaneous disease on the breed is waning. The study reiterates the power of primary-care veterinary clinical records for research to help understand breed health in dogs and to support evidence based approaches towards improved health and welfare in dogs.