Pododermatitis, often called ‘sore hocks’, is a chronic, granulomatous, ulcerative dermatitis which most commonly affects the plantar aspect of the caudal metatarsal and tarsal areas. Pododermatitis is a common clinical finding in the pet rabbit population, but no data is available regarding the actual prevalence of this condition in the UK pet rabbit population or possible husbandry-related factors which may predispose pet rabbits to development of this condition. It was the aim of this study to determine the prevalence of pododermatitis within a sample pet rabbit population, and study possible correlations with husbandry, sex, breed and origin of the rabbits. Findings suggested that young rabbits are at a lower risk of pododermatitis compared with older rabbits; female domestic rabbits are more predisposed to pododermatitis than males; and 100 per cent of the neutered females examined showed clinical evidence of pododermatitis. The effect that different types of bedding may have on the prevalence of pododermatitis was also investigated. This study also produced a scoring system which can be used to score clinical cases. Our study is of clinical importance because it helps to recognise many of the factors which predispose pet rabbits to pododermatitis, representing the first step towards increased awareness of this extremely common problem.
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Pododermatitis, often called ‘sore hocks’, is a chronic, granulomatous, ulcerative dermatitis which most commonly affects the plantar aspect of the caudal metatarsal and tarsal areas (Harkness and others 2010). Less frequently, the palmar aspect of the metacarpal and phalangeal surfaces of the front feet may be also involved, often occurring secondary to a shift of the rabbit's weight from the hind to the front feet in an attempt to relieve the pain associated with this condition (Harkness and others 2010).
Rabbits are now becoming very popular pets, but the majority of the publications on pododermatitis in this species have been derived from studies performed in animals kept under laboratory or farm conditions. Rosell and others (2000) and Mirabito and Delbreil (1997) observed a mean prevalence of sore hocks of between 7.5 per cent and 12.5 per cent in intensive production farms in Spain and France. In laboratory settings, however, the rabbit population is composed of relatively few breeds, and animals are housed under controlled conditions. This situation is in contrast with that of pet rabbits presenting to a local veterinary practice for routine care. Furthermore, in the laboratory situation, many rabbits are sacrificed at an early age, whereas the normal life span of a pet rabbit can now reach on average up to 9–11 years (Carey and Judge 2000). The aim of this research was therefore to acquire data applicable to pet rabbits. For commercial rabbits, factors predisposing to pododermatitis include: animal origin, weight, body condition, age, sex and concurrent diseases (Rosell and others 2000, Rosell and de la Fuente 2004, Rosell and de la Fuente 2008). Hago and others (1987) attributed pododermatitis to primary pasteurellosis and to conformational defects, but in more recent years, major risk factors have been identified in farmed animals. Pododermatitis, in animals kept in intense farmed conditions, is therefore now considered mainly secondary to physical/conformational or husbandry-related problems. These occur when animals are confined in small cages with hard or wire flooring, because the trauma due to persistent contact with various types of rough, dirty flooring can lead to ischaemia and avascular necrosis of the plantar surface of the foot (Rommers and Meijerhof 1996). It has been speculated that this may also occur in obese rabbits (Drescher and Sclender-Böbbis 1996, Harcourt-Brown 2002), in larger breeds and those with thin, long fur or that lack plantar/palmar protective hairs, such as Angora, Rex or Flemish giant breeds (Harkness and others 2010). Clinical conditions resulting in musculoskeletal pain and altered weightbearing can also increase the susceptibility to this condition. Deep pyoderma and cellulitis may result, followed by abscessation, osteomyelitis and synovitis with loss of function of the superficial digital flexor tendon in extreme and severe cases (Harcourt-Brown 2002, Keeble 2006).
At rest, rabbits bear their weight on the area between the hock and the hind claws but during locomotion they are digitigrade, placing their weight on the digits and claws rather than on the metatarsi and hocks. Rabbits do not have footpads to protect the plantar aspect of the hind feet, like dogs and cats, but only thick fur, and the thin skin associated with this area is adhered to the underlying tissues (Harcourt-Brown 2002).
Any condition which compromises locomotion and the mechanism of weightbearing, can ultimately increase the pressure on the thin, soft skin and the underlying bones of the feet, resulting in ischaemia and avascular necrosis (Harcourt-Brown 2002, Oglesbee 2006). Conditions that have been associated with this include obesity, spinal pain, lack of exercise or immobility due to other causes, hard or wire flooring, or clipping the fur around the foot (Richardson 2000). Focal hair loss, erythema, scaling, ulceration of the skin of the plantar surface over the bony prominence of the metatarsus are frequently seen initial clinical signs (Richardson 2000). Locally applied pressure, friction and shearing forces with subsequent ischaemia-reperfusion and tissue necrosis are considered predisposing factors for development of pressure ulcers (bedsores or decubitus ulcers) in human beings (Nguyen and others 2008). Harcourt-Brown (2002) hypothesised that the predisposing factors leading to ulcerative pododermatitis may be similar in rabbits, and Liu and others (2009) investigated the effects of two types of intermittent pressure on the formation of pressure ulcers in Japanese white rabbits in laboratory conditions.
Harcourt-Brown (2002) stated, and it is also the authors' personal experience, that pododermatitis is a common clinical finding in the pet rabbit population, but no data is available regarding the actual prevalence of this condition in the UK pet rabbit population or possible husbandry-related factors which may predispose pet rabbits to development of this condition. It was therefore the aim of this study to determine the prevalence of pododermatitis within a sample pet rabbit population, and study possible correlations with husbandry, sex, breed and origin of the rabbits.
Materials and methods
Over a seven-month period (April 2012–November 2012), all owners presenting a rabbit to the Exotic Animal and Wildlife Service of The Royal (Dick) School of Veterinary Studies, University of Edinburgh, were invited to participate in the survey. Owners were asked to complete a questionnaire which covered details of their rabbit's signalment and husbandry (eg, sex, age, breed, substrate, indoor/outdoor enclosure, diet). A full history was obtained, and a complete physical examination was carried out on every rabbit. Results were recorded, including weight and body condition score (BCS) using a five-point scale, with three being the optimum (Courcier and others 2012). Rabbits were checked for pododermatitis and were clinically scored from 0 to 6 based on the degree of pododermatitis present (Figs 1⇓⇓⇓⇓–6). This grading scale (PRPSS (The Pet Rabbit Pododermatitis Scoring System)), with a macroscopic description of the pododermatitis lesions, can be found in Table 1.
Photographs of the left and right hocks of every rabbit examined were taken during the consultation with a digital camera (Canon SX210IS 14× Optical zoom). The photographs, in a random order, were divided into those which showed the hocks clearly and those which were unclear. The photos determined to be clear enough for grading were then blindly scored by four different clinicians.
Collected data was analysed at the end of the study by use of two commercially available software programmes (Minitab V.16; Minitab, Coventry, UK and R V.2.12.1; The R Foundation for Statistical computing) and a P value of <0.05 was taken to indicate statistical significance. A χ2 test and standard logistic regression with ORs and 95% CIs were calculated to evaluate the potential risk factors for occurrence of pododermatitis. Rabbits with pododermatitis were then divided into those presenting with major pododermatitis (clinical scores of 2/6 and above) and those with minor pododermatitis (clinical scores of 1/6) to enable statistical analysis. For the group of rabbits with major pododermatitis, the risk factors associated with the presence of more severe pododermatitis were examined using the same logistic regression techniques as above. Incomplete questionnaires were included in data analysis which accounts for the differences in numbers of rabbits analysed for each risk factor.
A total of 179 domestic rabbits were surveyed. These consisted of 49 entire females, 42 neutered females, 34 entire males and 54 neutered males ranging in age from two months to nine years. One hundred and three rabbits were owned, and 76 were currently held in a rescue centre. Breeds included: Lop (n=68), Crossbreed (n=60), Lionhead (n=21), Netherland dwarf (n=12), Rex (n=6), Dutch (n=5), Continental giant (n=4), and English (n=3), (Fig 7).
Out of the 179 rabbits surveyed, 11 showed no signs of pododermatitis, with the remaining 168 rabbits showing varying degrees of lesions (Fig 8). Of these 168 rabbits, 73 had major pododermatitis (score >1) and 94 had minor pododermatitis (score 1).
Risk factors for the presence of pododermatitis
A statistically significant association was found between age and presence of pododermatitis with the odds of being positive for pododermatitis being higher at 3.67 (0.94 to 14.41) for rabbits >12 months compared with younger rabbits (Table 2).
There was also a statistically significant association between sex and the presence of pododermatitis, with the odds of being positive for pododermatitis being higher if female at 5.07 (1.06 to 24.17) compared to males. All neutered females had detectable pododermatitis.
Pododermatitis was also detected in all rabbits not bedded on hay. There were, however, no statistically significant associations between the presence of pododermatitis and whether carpet or hard flooring formed part of the substrate (P>0.057). The association between origin of the rabbit and presence of pododermatitis was not statistically significant (P=0.095). However, 100 per cent of the rabbits from breeders, or home bred, were positive for pododermatitis.
There were no statistically significant associations between the presence of pododermatitis and whether a rabbit was currently held in a rescue centre or not, housing, diet, body condition or weight (P>0.095) (see Table 2). It was not possible to analyse the association between breed and presence of pododermatitis, as the large variety of rabbit breeds seen, the relatively small numbers within each group, and the large number of crossbreed rabbits precluded statistical analysis.
Risk factors for the presence of major pododermatitis
The association between the presence of major pododermatitis (scores of 2/6 or above) and the various risk factors was then examined in only those 168 rabbits with clinical lesions. A statistically significant association was found between age and presence of major pododermatitis (χ21=21.9, P<0.001, Table 3), with the odds of being positive for major pododermatitis being higher at 5.43 (2.56 to 11.52) for rabbits >12 months compared to younger rabbits. There was also a statistically significant association between the rabbit's sex and the presence of major pododermatitis, with the odds of being positive for entire rabbits being less, at 0.25 (0.1 to 0.6) for female entire and 0.53 (0.21 to 1.36) for male entire rabbits, compared with neutered rabbits. There were no statistically significant associations between the presence of major pododermatitis and breed, origin of the rabbit, whether it was currently in a rescue centre or not, housing, bedding, diet, body condition or weight (P>0.057, Table 3).
Each clinician's scores of the pododermatitis photos were examined with 73 per cent (72/99) agreement between clinicians. Ninety-nine photos were determined to be clear enough for grading and these were blindly scored by four different clinicians. When dividing photos into those in which pododermatitis was present and those in which it was not, there was 99 per cent (98/99) agreement.
Ulcerative pododermatitis is a serious and painful condition which can rapidly progress and potentially compromise the welfare of pet rabbits (Webster 2001). Our survey showed that pododermatitis is frequently encountered with 93.8 per cent prevalence in the sampled pet rabbit population in the UK.
The factors affecting the prevalence of pododermatitis have been previously investigated in rabbits kept in intensive farmed conditions and in laboratory settings, and it has been suggested that husbandry set-up may play a role in influencing the development of lesions (Rommers and Meijerhof 1996, Rosell and others 2000). Harkness and others (2010) reported that the incidence of pododermatitis in the laboratory environment increases with age and weight (more than 3 kg), with humid weather, and in males compared to immature animals, whereas, light-weight breeds seem to be less frequently affected. In our study, involving 179 domestic pet rabbits, the relationship between the prevalence of pododermatitis and several possible risk factors including sex, neutered status, age, breed, weight and BCS was examined to assess their relevant effect.
Our findings suggest that young rabbits are at a lower risk of pododermatitis compared to older rabbits. This would be consistent with the theory that pressure-related ulcers are the product of compression over a period of time (Kosiak 1961).
A mean prevalence of sore hocks of 9.1 per cent for female and 7.5 per cent for male rabbits in farm conditions has been previously reported (Rosell and others 2000). Females had a higher prevalence of pododermatitis compared to males (10.4 per cent and 5.7 per cent, respectively) in 130 Spanish rabbitries (Rosell 2003). The result of our study on pet rabbits is in agreement with these previous reports on farmed rabbits. Female domestic rabbits are more predisposed to pododermatitis than males, with a prevalence of 97.8 per cent compared to 89.7 per cent, respectively. Furthermore, we investigated the effect that neutering may have on the incidence of pododermatitis and we found that 100 per cent of the neutered females examined showed clinical evidence of pododermatitis. Among the 73 rabbits examined with a score >1 (major pododermatitis), a similar significant effect of sex and neutered status on the incidence of pododermatitis was found. Neutered females had a higher prevalence of major pododermatitis compared to entire females (54.7 per cent and 23.4 per cent, respectively). Similarly, neutered males had a 54.9 per cent prevalence of clinically major lesions compared to entire males (39.2 per cent). A recent communication by Courcier and others (2012) suggested that female rabbits and/or rabbits that had been neutered were more likely to be overweight. The incidence of pododermatitis has been clearly linked to body weight (Rosell and others 2000, Harcourt-Brown 2002) and body condition in farmed rabbits (Rosell and de la Fuente 2008). It has also been suggested that this is also the case in pet rabbits (Harcourt-Brown 2002). In this study, those in the overweight category (BCS>3) did have a higher prevalence of pododermatitis at 97.4 per cent compared to those rabbits considered to be at an ideal weight and those considered to be underweight (93.8 per cent and 91.7 per cent, respectively), but differences were not found to be statistically significant. It can be speculated that neutered female rabbits were more likely to be less active and more overweight and, therefore, more predisposed to pododermatitis development. Further studies would be needed to evaluate the effect that activity levels would have on the development of such condition and the correlation with sex. The effect that different types of bedding may have on the prevalence of pododermatitis in commercial rabbits has been extensively studied (Rommers and Meijerhof 1996, Harcourt-Brown 2002, De Jong and others 2008, Rosell and De la Fuente 2008). It is generally accepted that the type of substrate on which a rabbit is housed has a great impact on the development of sore hocks (Rommers and Meijerhof 1996), as it can affect the weight distribution allowing most of the weight to be borne by the metatarsi. Furthermore, many types of flooring are abrasive and can cause friction and increased shearing forces, increasing the likelihood of sore hocks developing (Harcourt-Brown 2002). Our survey showed that hay, compared with other types of bedding, is associated with a reduced incidence of pododermatitis. There was no statistically significant correlation between carpet, hard flooring or other types of bedding (including newspaper, straw, shavings, towels, blankets, recycled paper bedding, carpet or foam mats) and the presence of pododermatitis, as 100 per cent of the rabbits housed on these beddings presented various degree of major pododermatitis (scores >1). These findings further confirm the fact that house rabbits which, in the majority of cases, are kept on rough carpeting or hard flooring are equally more susceptible to developing pododermatitis compared to those that spend most of their time sitting on hay. Furthermore, no statistically significant association was found between the type of housing (whether the rabbit was being kept indoor or outdoor, in a hutch or in a cage) and the prevalence of pododermatitis (P>0.169). Whether exercise was part of the daily routine of the rabbits examined was not taken into consideration in our preliminary study. Nevertheless, it would have been interesting to assess the impact that exercise each day may have on the development of hock lesions. The type of housing did not represent an increased risk factor for the incidence of sore hocks in those animals presenting major pododermatitis (P>0.232). In contrast with Rosell and de la Fuente (2004) for which the origin of the rabbit was a predisposing risk factor, the results of our study showed no statistically significant association between the origin of the rabbit, whether from a breeder, home-bred, or from a rescue centre or a pet shop, and the incidence of pododermatitis (P=0.09). Nevertheless, 100 per cent of the rabbits that were home-bred or from a breeder presented with pododermatitis. Around 67,000 rabbits end up in rescue centres in UK every year according to figures released by the Rabbit Welfare Association and Fund (RWAF 2012). Our study showed that 58 per cent rabbits examined were in fact acquired as ‘rescues’. These may have been related to the fact that the owners of the 179 rabbits surveyed volunteered to take part in the study. Therefore, it is possible that our survey attracted particularly keen and dedicated owners. Similarly, there was a high proportion of rabbits acquired from a breeder or were home-bred (19 per cent), which may have been associated with those owners more keen to own a specific breed or obtain a rabbit from known parents. Pet shops supplied 23 per cent of the rabbits examined. However, there was also no statistically significant difference between the origin of the rabbit examined and the presence of major pododermatitis (P=0.9).
Our results showed a large variety of rabbit breeds being presented to the practice. This reflects the wide range of breeds that have become available in the pet trade. The British Rabbit Council (www.thebrc.org/standards.htm) recognises many different breeds and over 500 varieties of rabbits in the UK, which constantly evolve due to selective breeding practices (Meredith 2006). Many pet rabbits are now crossbreeds (Meredith 2006), and our survey confirmed this observation, as the large majority of rabbits seen were crossbreed (n=60). Lop rabbits were also present in large numbers (n=68), followed by Lionhead (n=21), Netherland dwarf (n=12), Rex (n=6), Dutch (n=5), Continental giant (n=4) and English (n=3). Previous literature, involving commercial pet, recognised Angora and Rex rabbits as being more predisposed to developing pododermatitis due to their fine sparse hair which offers limited protection to the metatarsi (Harcourt-Brown 2002, Harkness and others 2010). Flemish Giant and other giant breeds are also considered more susceptible due to their increased weight (Harkness and others 2010). However, in our study, it was not possible to analyse the association between breed and presence of pododermatitis as the large variety of rabbit breeds seen, with relatively small numbers within each group, and the large number of crossbreed rabbits precluded statistical analysis.
The correlation between diet and incidence of pododermatitis has been previously investigated in laboratory settings (Sanchez and others 2012). In laboratory rabbits, female rabbits consuming a more caloric diet presented with a greater BCS and were, therefore, more prone to pododermatitis due to increased weight. Inappropriate diets may predispose to obesity and may be a reflection of inappropriate husbandry which ultimately can lead to an increased incidence of pododermatitis. A direct link between diet and the prevalence of pododermatitis was investigated in our study, but no statistically significant relationship was found between diet (P>0.207 and P=0.59, respectively) and the presence of pododermatitis or major pododermatitis. A scoring system for pododermatitis has been previously proposed for commercial rabbit does (Rommers and Meijerhof 1996) and in a rabbit model of compression-induced ear lobe ulcers (Niitsuma and others 2003). The extent and severity of lesions presented by the rabbits examined during our study were clinically scored by adapting these previous systems to produce the PRPSS. In this scoring system, dermatologic signs were scored for severity from 0 (no evidence of pododermatitis), 1 (mild), 2–3 (moderate), 4–5 (severe) to 6 (loss of pedal function). Each grade was also associated with a macroscopic description of the dermatologic lesions observed at the metatarsi (‘sore hocks’) (Table 1). More recently, Olivas and others (2013) proposed a scoring system for breeding does taking into account different aspects and characteristics of the lesions. Although the authors recommend a simple system with only a three- or four-point scale to provide a more consistent and reliable scoring method to be applied in practice, it is these authors' opinion that a higher level of details may also help in better identifying different stages of the lesions. Identification of early stages, for example, may induce to enforcing husbandry changes, thus preventing development of more severe lesions.
The digital images obtained for each hock examined were then blindly scored in a randomised order and a 73 per cent agreement was obtained. Nevertheless, when images clearly showing lesions of pododermatitis were selected and blindly scored, the agreement was 99 per cent between the four clinicians permitting further validation of our scoring system.
According to Webster (2001), sore hocks compromise the rabbit's health and welfare by causing chronic pain and suffering. Drescher and Schlender-Böbbis (1996) also stated that welfare is decreased when a callus is present on the footpads (Grade 1 in our study). Other authors (De Jong and others 2008) questioned whether a grade I lesion is associated with pain in rabbits, but they underlined how callus formation may increase the risks of more severe abnormalities occurring, and correspondingly higher scores (Grades 3 and 4 of our PRPSS), which pose a clear welfare issue. From our data, it appears that many of the risk factors previously identified as potentially increasing the incidence of pododermatitis in commercial animals, are similar for pet rabbits. This provides clear evidence that husbandry and captive management have a great impact on the development of this condition. Nevertheless, a larger study allowing investigation of a greater sample population and the identification of further risk factors is recommended by the authors. This would significantly aid our understanding of the aetiology of pododermatitis in pet rabbits and enable the production of clear recommendations for the prevention and management of this serious condition in pet rabbits. This study has also produced a clear scoring system which can now be used for future studies on a larger population of rabbits and by veterinarians in practice to score clinical cases and help in their decision making on treatment recommendations. Our study is therefore of clinical importance because it helps to recognise many of the factors which predispose pet rabbits to pododermatitis. Our results also represent the first step towards increased awareness of this extremely common problem that many pet rabbit owners are unaware of and which is often underestimated by many veterinarians.
The authors would like to kindly thank the nursing staff for their assistance. This work would not have been possible without Darren J Shaw BSc PhD who greatly helped with his advice and knowledge.
Provenance: not commissioned; externally peer reviewed
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