This study of over two thousand animals is the largest analysis of breed health in French Bulldogs based on primary-care veterinary records to date. The results highlight steeply rising French Bulldog ownership in the UK, with French Bulldogs comprising over 1.46% of all dogs born in 2013 attending veterinary practices, although not all of these may have been born in the UK. These findings are consistent with registration data from The Kennel Club that highlights the French Bulldog currently as the most rapidly rising pedigree breed in the UK, surpassing other popular small brachycephalic breeds such as the Pug. This trend has also been observed internationally, with shorter, smaller and flatter faced dog breeds also becoming more popular in Australia between 1986 and 2013 [25].
Both in the United States of America (USA) and the UK, breed popularity appears to lack direct associations with functional traits (e.g. health, trainability) [3, 26] whilst displaying a concerning tendency for more popular breeds to have greater numbers of inherited disorders [26]. For owners of small brachycephalic breeds including the French Bulldog, the breeds’ appearance, size being suited to the owners’ lifestyle and behavioural traits (good dog breed for children and good companion breed) have been reported as more highly influential to breed choice by owners than either health or longevity [5]. In addition, French Bulldog owners may represent examples of ‘extrinsically motivated’ owners, who acquire dogs as a means of obtaining status and attention from other people, due to the distinctiveness or ‘cuteness’ of the dog, and may often perceive their dog as helpless and in need of care and control [6]. With several of the most common disorders in French Bulldogs linked to their physical conformation (e.g. URT disease and ophthalmological conditions), the increasing popularity of this breed is not necessarily a benign phenomenon. Increased demand for dogs with extreme conformational features is suggested to be detrimental to these dogs’ welfare both because of directly linked disorder risk and also because steeply increasing demand may contribute to suboptimal breeding and welfare standards as breeders and suppliers rapidly attempt to fulfil the heightened consumer demand [27]. With dogs born in high-volume commercial breeding establishments experiencing an increased incidence of behavioural and emotional problems that cause distress in adulthood compared with dogs from other sources, dramatic increases in popularity are a welfare concern for any breed [28]. Consequently, surveillance of the health of the general population of French Bulldogs in the UK is of increasing importance to provide evidence on both breed and husbandry related welfare concerns.
The most common disorders identified in the current study for French Bulldogs were otitis externa, diarrhoea, conjunctivitis, overlong nails and skin fold dermatitis. These results provide a framework to identify health priorities from a prevalence perspective in French Bulldogs that can contribute positively to reforms that aim to improve health and welfare within the breed. Although longevity did not differ between males and females, marked sex differences in disorder prevalence were observed, with males were more likely than females to be diagnosed 8 of the 26 most common fine-level precision disorders, and 6 of the 15 most common grouped-level precision disorders. These additional sex-based prevalence data can highlight those disorders that would benefit from special focus within specific sexes in order to contribute to improved French Bulldog health and welfare as well as assisting decision-making by veterinarians and owners on the most appropriate sex selection [10]. The current study data do not provide a strong rationale to explain the disorder prevalence differences between males and females but these may be associated with differing body sizes (13.7 kg in males versus 11.5 kg in females) or hormonal profiles between the sexes [29]. Sex-associated differences in dogs for disorder prevalence in multi-disorder studies have also been reported for Rottweilers [30], Border Terriers [31] and German Shepherd Dogs [32] and may represent an under-explored area of research that could enhance our understanding of disease causality.
URT disorders were the fourth most common grouped-level disorder, reported in 12.7% of French Bulldogs. The most commonly recorded fine level disorders within the URT group included brachycephalic obstructive airway syndrome (BOAS) (2.4%), URT disorder (2.1%), and stenotic nares (1.7%). BOAS encompasses a range of primary or secondary disorders that may include stenotic nares, enlarged tonsils, elongated soft palate, everted lateral saccules of the larynx, narrowed rima glottides, collapse of the larynx and tracheal hypoplasia [33, 34]. BOAS is considered a major animal welfare concern, with the lives of affected animals negatively impacted both while awake and asleep by clinical signs including chronic breathlessness, exercise intolerance, eating difficulties and disrupted sleeping including periods of apnoea [35]. The relatively low prevalence of recorded diagnoses of BOAS and other respiratory problems in the current primary-care population using a retrospective observational study design is in sharp contrast with the findings from some other prospective clinical studies. A prospective study of BOAS in the UK reported that 70% of French Bulldogs attending a referral veterinary hospital and 75% of a general population of French Bulldogs had BOAS based on clinical history, owner questionnaire and clinical examination [7]. A UK clinical study using whole-body barometric plethysmography reported that 89.9% of French Bulldogs tested were affected by BOAS to some extent, with 53.9% exhibiting clinically relevant disease [9]. These latter data suggest that many truly BOAS-affected French Bulldogs may be accepted as ‘normal for breed’ by owner and the veterinary profession because the pervasively high true prevalence of the disorder may conflate perceptions of ‘typically expected’ and ‘desirably expected’. The authors would strongly encourage veterinarians, breeders and owners to avoid the use of the word ‘normal’ with its inference of acceptability in relation to breed-related health features and move instead to alternative terms such as ‘typical’ or ‘commonplace’. Indeed, only 42% of owners of dogs affected by BOAS perceive that their dog has a breathing problem; as such, it is possible that only the most severely affected cases may receive a formal BOAS diagnosis in the primary-care setting [36]. Psychological desensitisation in veterinarians to URT in brachycephalic dogs may result from chronic exposure to common clinical signs of BOAS (e.g. increased and/or abnormal respiratory noise) in brachycephalic breeds such as the French Bulldog that potentially leads to underreporting in clinical notes. Unfortunately, this may also contribute to the sub-optimal clinical management of individual affected dogs if the condition is under-recognised and not discussed with clients. An earlier VetCompass™ study reported that 20% of French Bulldogs had least one URT disorder recorded over a 4.5 year study period, compared to the one year period of the current study, so it is possible that more French Bulldogs in the current population would go on to be diagnosed with URT disorders with a longer study period [34]. The current study reports that older dogs are significantly more likely to have a diagnosis of BOAs than younger dogs and suggests that the UK population of French Bulldogs are likely to show substantially higher levels of BOAS as the current cohort of dogs ages.
Dermatological disorders were a commonly recorded grouped-level event in French Bulldogs, with 17.9% of the study population affected. At the fine-level of disorder reporting, skin fold dermatitis was the fifth most common disorder (3.0%), followed by pyoderma (2.7%), pododermatitis (2.5%) and atopic dermatitis (2.0%). Skin disease is well-recognised as a breed-specific issue in French Bulldogs, with both hair loss or scarring from previous dermatitis and signs of dermatitis in skin folds listed as points of concern in ‘Breed Watch’ for the breed [1]. Skin fold dermatitis may occur at any site on the body where excessive skin wrinkling causes skin-on-skin contact, including the facial region of brachycephalic dogs or in skin folds around absent, short or screw-tails [37]. Skin fold dermatitis (intertrigo) was also a common finding in a previous VetCompass™ study of Pugs [38], another brachycephalic breed where skin folds are common, particularly on the face (referred to as ‘over nose wrinkle’) [1]. Although an over nose wrinkle is not explicitly encouraged, The Kennel Club (UK) French Bulldog breed standard specifies that skin on the skull and forehead “should be supple enough to allow fine wrinkling” [1]; and the American Kennel Club breed standard describes “heavy wrinkles forming a soft roll over the extremely short nose” [39]. In addition to conformation-related skin disorders, the French Bulldog has also been reported as both predisposed to canine atopic dermatitis [40] and also reported as developing clinical signs of atopic dermatitis earlier than other breeds, which may suggest a higher genetic predisposition [41]. The median age of dogs affected with atopic dermatitis in the current study was 3.8 years and the condition was significantly more likely in dogs older than 2 years (Table 4). In a breed such as the French Bulldog where immune-mediated skin disease is common, ensuring their conformation does not exacerbate existing skin disorders, or directly cause skin disease in itself should be of priority for breed welfare. As proposed in the Independent Inquiry into Dog Breeding, “Where a problem within a breed already exists, the Breed Standard should be amended specifically to encourage the selection for morphologies that will improve the welfare status of the breed” [42]. Amending breed standards and breeding away from skin folds may go some way to encourage healthier skin conformation and improve breed health.
Ophthalmological disorders (10.5%) were the fifth most common grouped-level disorder for French Bulldogs, with conjunctivitis (3.2%), prolapsed nictitans gland (2.6%) and ulcerative keratitis (2.1%) in the top 20 most common fine-level disorders for the breed. A previous VetCompass™ study of corneal ulceration reported that French Bulldogs had the 8th highest breed prevalence for this disorder (prevalence: 1.87%) and had a five-times increased odds of diagnosis with corneal ulceration compared with crossbreeds [13]. The median age at diagnosis of corneal ulceration across all breeds in the UK has been reported as 4.9 years [13]. This value is higher than the median of 2.79 years reported in the current study and may reflect the relative youth of the French Bulldog population. A prospective clinical study reported that 15.4% of French Bulldogs were affected by corneal ulcers [8], with conformational risk factors for corneal ulcers across dog breeds also identified in the same study. These included the presence of a nasal fold, brachycephalic skull shape and wide eyelid openings, all of which are commonly observed in French Bulldogs [8]. The UK Kennel Club has taken efforts to redress these associations, with ‘excessively prominent eyes’ and ‘incomplete blink’ (lagophthalmos) identified as points of concern for the French Bulldog in Breed Watch [1]. Given that the canine cornea is densely innervated by nociceptive afferent axons and that in a previous study, 69.1% of canine corneal ulcers cases had either pain recorded in their notes and/or received pain management [13], ensuring that skull, eyelid and eye conformation do not predispose dogs to these welfare-relevant disorders is of major welfare importance.
Aggression was the thirteenth most common fine-level disorder recorded in French Bulldogs (2.3%). In contrast, aggression did not feature among the 25 most common fine-level disorders in Pugs in the UK [38]. The differing age distributions of the two study populations (3.0 years median age of Pug population versus 1.3 years median age in the current French Bulldog study) are unlikely to explain the differing aggression prevalence since the current study identified that aggression was more common in dogs older than 2 years compared with dogs younger than 2 years [43]. In addition, both studies had similar ratios of males and females overall. This relatively high level of aggression in the French Bulldog is somewhat surprising in light of the finding that owners of French Bulldogs were influenced to buy their breed by a perception that they were a ‘good companion breed’ and ‘good with children’ [5], with their temperament described as a ‘deeply affectionate’ in their UK breed standard [1]. As such, further data on the behaviour of French Bulldogs are required to more precisely characterise the types of aggression seen and explore the underlying motivation for these behaviours. As in previous studies, a higher male prevalence of aggression was observed in French Bulldogs (males 3.7% vs. females 0.8%), which may be related to androgens promoting competitive behaviour [44, 45].
During the one-year period of surveillance (2013) of this study, 27.6% of French Bulldogs 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 comparable with the 24% of dogs without any recorded disorders that was reported across a random sample of all breeds in the VetCompass™ database [46]. With well-documented health concerns in French Bulldogs, it is perhaps surprising that the proportion of French Bulldogs with at least one disorder recorded is not higher than for the overall population. However, this may be explained by the younger age of French Bulldogs in the current study (median age: 1.3 years) compared with the overall dog population in the previous study (median age: 4.5 years). It has previously been documented that French bulldogs are very young when they exhibit their first veterinary care event (less than two years compared to around five years for all breeds [6]), which may reflect that the health problems of the breed are more related to congenital disorders instead of acquired and age-related diseases [6]. The young median age of 1.3 years in the current study may also explain why periodontal disease, the second most common disorder affecting dogs overall in the UK [46] did not feature amongst the common disorders of French Bulldogs. In addition, although spinal cord disorders were a common cause of death in the current study, and Hansen type I disc herniation (IVDH) has been reported to be the most common neurological disease in French Bulldogs [15], spinal disorders did not feature amongst the most common disorders in the present study. This is again likely due to the young age of this study population, with 81% of French Bulldogs affected by IVDH aged 3 years old or more [15]. The current study identified that 38% of the common disorders recorded in French Bulldogs were associated with age with equal proportions showing higher prevalence in older and younger dogs. It is planned to repeat the current study in the future and this may identify shifting disorder profiles towards diseases of aging and away from disorders of youth assuming that breed popularity wanes over time.
The study had some limitations that have been previously reported [46]. The study was unable to segregate and compare between Kennel Club registered and unregistered dogs but ongoing efforts underway within the VetCompass™ Programme should enable such distinctions in the future and could contribute to greater clarity on the health comparisons between these two groups. 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 [47]. 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 [10].
