Demography and health of Pugs under primary veterinary care in England

This study of over one thousand animals is the largest analysis of breed health in Pugs based on primary-care veterinary records to date. The results highlight steeply rising Pug ownership in England, with Pugs comprising over 2.5 % of all dogs attending veterinary practices that were born in 2013, although not all of these may have been born in the UK. The most common disorders identified in Pugs were overweight/obesity, corneal disorder and otitis externa and the most commonly affected body location was the head-and-neck region. These results provide a framework to identify health priorities in Pugs that can contribute positively to reforms to improve health and welfare within the breed.

A good understanding of demography is critical for optimal interpretation and generalization of canine health studies [25–27]. The current study identified a steep rise in Pug ownership in recent years. Annual proportional birth rates have risen almost three-fold from less than 1 % before 2008 to almost 3 % of the annual birth cohort born in 2013 (Fig. 2). These findings are consistent with registration data from the UK Kennel Club that recorded an increase of more than four-fold in Pug registrations between 2005 and 2014, [6]. Unfortunately the current study was unable to identify between Kennel Club registered and unregistered dogs but work is underway within the VetCompass Programme to enable such distinction and could contribute to greater clarity on the health comparisons between these two groups. The popularity of the Pug breed has been ascribed to anthropomorphic tendencies of owners who perceived as endearing their child-like or baby-like (paedomorphic) physical characteristics such as flat faces and large eyes [10, 28] and behaviours such as tractability, attention seeking, begging for food and waiting patiently [29–31]. Social effects such as celebrity endorsement and product advertising that features Pugs may also strongly influence breed selection decisions by prospective puppy buyers [32–36].

However, increasing popularity of individual breeds is not necessarily a benign phenomenon. Extreme conformational features of the Pug such as large dark round eyes and flat faces that are appealing to humans have been associated with welfare concerns for the dogs [10, 28, 37]. There are also fears that increased demand for Pugs may contribute to suboptimal breeding and welfare standards as breeders and suppliers rapidly attempt to fulfil the heightened consumer demand [38]. Large numbers of Pug puppies are reported to be imported into the UK, both legally and illegally, with consequent health and behavior risks to these puppies themselves as well as concerns about the introduction of non-endemic diseases such as rabies into the UK [39–41]. Consequently, surveillance of the health of the general population of Pugs in the UK is of increasing importance to support both dog welfare and UK national disease status activities.

Bodyweight growth curves are commonly used for health screening and surveillance in humans, especially because of increasing public health concern over childhood undernutrition and obesity [42] and may similarly contribute to improved nutritional health in dogs. However, diversity between dog breeds in their relative and absolute growth rates implies canine growth curves should be generated from populations that are representative by sex, breed and geography for the target animals for optimal reliability [43]. Unsurprisingly, the results confirmed that male Pugs (median bodyweight 8.9 kg) are heavier than female Pugs (median bodyweight 7.39 kg) and the current study provides exemplars of growth curves for the general population of male and female Pugs in England and could assist breeders and veterinarians to recognise individual animals that are over- or under-sized. Canine growth curves could also assist with estimation of age, for example in puppies presented for importation to the UK to validate the consistency between the stated age and bodyweight [40].

During the one year period of surveillance (2013) of this study, 32 % of Pugs under veterinary care did not have any disorders recorded and were instead either presented for routine or prophylactic veterinary care or did not attend the veterinary clinic at all. This value is higher than the 24 % of dogs without any recorded disorders that was reported across a random sample of all breeds in the VetCompass database [17]. The lower proportion of Pugs recorded with at least one disorder may partially be explained by the younger age of Pugs in the current study (median age: 3.0 years) compared with the the overall dog population in the previous study (median age: 4.5 years). However, these results also suggest that, despite well-documented health concerns in Pugs, many individuals in this breed are not diagnosed with illness over extended periods of observation and that gaining a full understanding of health issues in Pugs will be a complex undertaking that also requires data on disease duration and severity [7, 11].

A review of breed predispositions to disease identified 25 disorders have been reported as over-represented in Pugs [7]. A loose comparison between these breed predispositions and the current study identified just eight of the 25 over-represented disorders that were also among the 25 most common disorders recorded in Pugs shown in Table 2: corneal disorder, brachycephalic obstructive airway syndrome (BOAS), upper respiratory tract noise increased, intertrigo, respiratory noise increased, pruritus, keratoconjunctivitis sicca and coughing. This highlights the importance of generating both ‘between breed’ and ‘within breed’ evidence on disorder occurrence in order to facilitate disorder prioritisation based on both relative and absolute disorder burdens for individual breeds.

Overweight/obesity was the most common single disorder recorded in the current study, with 13 % of Pugs affected. By comparison, just 6 % of dogs across all breeds were recorded with overweight/obesity in a VetCompass study using a similar methodology [17]. Obesity has previously been recognised as a serious concern in Pugs. The Kennel Club cite being significantly overweight as a point of concern for special attention by show judges under its Breedwatch scheme [4]. In a study of show-visiting dogs, Pugs had the second highest mean body condition of 64 dog breeds evaluated [44]. Although the current study concurs with the literature that overweight/obesity is a common finding in Pugs, the true prevalence may be substantially under-estimated in the current retrospective study. Compared with retrospective studies, prospective studies of obesity in dogs generally report much higher overweight/obesity values ranging from 25 % to 41 % [45–47]. Obesity is a clinically relevant disorder in dogs because of associations with disorders including diabetes mellitus, cardiovascular, skin and musculoskeletal disease, exercise and heat intolerance, metabolic syndrome and increased surgical and anaesthetic risk [13, 47–49]. Overweight/obesity should be considered a health priority in Pugs because of the high prevalence, associated health problems and reversible nature of the disorder [50].

Corneal disorders were the second most common specific disorder recorded in the current study, with almost 9 % of Pugs affected during the study year. In contrast, corneal disorders did not rank among the top twenty disorders recorded across all dog breeds in England [17]. Corneal disorders cover a spectrum of presentations including pigmentation, opacity, vascularisation, scarring, erosion, ulceration and perforation, many of which are non-specific biological responses to various noxious stimuli, including mechanical abrasion, immune-mediated keratitis, trauma, and tear film disorders [51]. A high prevalence of primary periocular and ocular problems, including macroblepharon, entropion, distichiasis, ectopic cilia and keratoconjunctivitis sicca, has been previously documented in Pugs, and secondary corneal disease may ensue [52–56]. Selection towards exaggerated brachycephalic facial morphologies have been suggested to promote the occurrence of ocular disorders in Pugs [10, 37, 57, 58]. The UK Kennel Club has taken efforts to redress these associations by listing Pugs as a category 3 breed in their ‘Breed Watch’ system and has recently revised the Pug breed standard to discourage severe exaggeration [4, 8]. Given that the canine cornea is densely innervated by nociceptive afferent axons and that corneal damage is believed to cause substantial pain [59], the results from the current study showing that ophthalmological disorders were the most common grouped disorder in Pugs, with over 16 % of dogs affected, and that the head-and-neck was the most common body location for disorders, with over 40 % of dogs affected, suggest that prioritisation of the extent of brachycephaly for ongoing health surveillance and reform will be important to improve the health welfare of Pugs.

Brachycephalic obstructive airway syndrome (BOAS) defines variable clinical presentations resulting from underlying primary or secondary disorders that include stenotic nares, enlarged tonsils, elongated soft palate, everted lateral saccules of the larynx, narrowed rima glottides, collapse of the larynx and tracheal hypoplasia [60–62]. Dogs affected by BOAS often have severe dyspnoea and inspiratory stridor leading to exercise intolerance and potentially heat stress [62]. Unremitting or remitting breathlessness (‘air hunger’) can have severe welfare implications over prolonged proportions of the lives of affected dogs [61, 63], with severely affected animals being fully engaged in active breathing efforts to the detriment of other life activities [64]. In a prospective study of BOAS in Pugs, 88 % of Pugs attending a referral veterinary hospital and 91 % of a general population of Pugs were diagnosed with BOAS based on clinical history, owner questionnaire and clinical examination [14]. However, the current retrospective study using primary-care veterinary clinical records identified just over 5 % of Pugs that were specifically diagnosed with BOAS and 10 % of Pugs recorded with at least one upper respiratory disorder. These contrasting data suggest that many BOAS-affected Pugs may be accepted as ‘normal for breed’ because of the pervasive true prevalence of the disorder and that only the most severely affected cases may receive a formal BOAS diagnosis [65]. In support of this normalisation phenomenon, more than half of owners of dogs diagnosed with BOAS at a referral centre stated that their dog did not have breathing problems [66]. Such normalisation phenomena may blind owners and veterinarians to disorders in commonly affected breeds and constrain reforms intended to improve the welfare of affected breeds [61, 66, 67] as well as also contributing to the apparently low prevalence of BOAS and other respiratory problems recorded in the current study.

Two congenital or early-developmental disorders, retained deciduous teeth (3.0 %) and umbilical hernia (2.8 %), also featured amongst the most common disorders in Pugs. By contrast, neither disorder appeared in the top twenty disorders recorded across all breeds in a previous study [17]. This suggests that retained deciduous teeth and umbilical hernia may be more common in Pugs than in the general population of dogs. However, these findings need to be interpreted carefully because, as discussed above, the relative excess of younger individuals in the current study may positively confound the apparent risks for disorders that occur during the early life period.

The study had some limitations. Studies based on reviews of medical records of animals may under-estimate the true disease burden by predominantly including those more severely affected animals that warrant veterinary management and there may be reduced reporting of less severely affected animals that may be less likely to be clinically presented [61]. The practices participating in the study were situated mainly in central and south-east England and therefore may not be fully representative of the overall veterinary practice structure and caseloads in England. Case definitions and diagnosis recording relied heavily on the clinical acumen and note-making of attending practitioners [17]. The current study ranked disorders based on prevalence but additional data on duration and severity are also required for effective welfare prioritisation of disorders [68, 69]. Clinical variants of some diseases may be recorded using distinct disorder terms and therefore the overall prevalence for these diseases may be fragmented into separate prevalence values for each of multiple more-specific diagnostic term, giving the illusion of lower prevalence [17]. The current study attempted to overcome such artefacts by also providing grouped-level precision results for common disorders to improve interpretability. Reporting the maximum bodyweight recorded during the adult period of life may have upwardly biased the bodyweight results compared with average bodyweights of Pugs at any one point in time. Additionally, it is worth noting that bodyweight values may be poor proxy measures for obesity status.