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Health survey of 167 pet rabbits (Oryctolagus cuniculus) in Finland
  1. J. Mäkitaipale, DVM, GPCert(SAS)1,
  2. F. M. Harcourt-Brown, BVSc, FRCVS, RCVS2 and
  3. O. Laitinen-Vapaavuori, Prof. Dipl ECVS1
  1. 1Department of Equine and Small Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, Helsinki, Finland
  2. 2Crab Lane Vets, Harrogate, North Yorkshire, UK
  1. E-mail for correspondence: johanna.makitaipale{at}helsinki.fi

Abstract

Only a limited amount of information is available about health status of pet rabbits. The aim of this study was to obtain data about the health status of pet rabbits considered healthy by the owners in Finland. Physical examination and lateral abdominal and lateral skull radiography were performed on 167 pet rabbits of which 118 (70.7 per cent) had abnormal findings in at least one examination. The most common findings were acquired dental disease (n=67, 40.1 per cent), vertebral column deformities and degenerative lesions (n=52, 31.1 per cent), skin disorders (n=28, 16.8 per cent) and eye disorders (n=12, 7.2 per cent). Vertebral column angulating deformities were significantly more common in dwarf lop rabbits (P≤0.001). The prevalence of health disorders was significantly higher in rabbits over three years of age of which 51 (82.3 per cent) had findings in at least one examination (P<0.05). Rabbits as prey animals hide their illness, which cause difficulties to owners to recognise health problems. Because of the high prevalence of clinical and radiological findings in apparently healthy pet rabbits, regular physical examinations are advised, especially for animals over three years old.

  • Rabbits
  • Health
  • Spine
  • Dentistry
  • Radiography
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Rabbits (Oryctolagus cuniculus) are the third most popular house pets in many countries (Borst and others 2011, SCB 2012, PFMA 2014). The exact number of pet rabbits in Finland is not known, but their amount as patients in veterinary clinics is increasing. In the last few years, rabbit medicine has advanced with new diagnostic procedures and treatments almost to the level of canine and feline medicine in many parts of Europe and the USA.

Rabbits are prey animals that hide signs of illness so they may have severe health problems before they are presented for veterinary treatment. A health survey of 102 pet rabbits in the UK by Mullan and Main (2006) revealed that 30 rabbits had dental disease and only six of their owners were aware of the problem. In the UK, many pet rabbits are vaccinated and examined regularly, but in Finland, there is no myxomatosis or RHD so pet rabbits do not visit veterinarians for vaccinations and regular examination, hence it is even more possible that serious health problems could go undiagnosed. To the authors’ knowledge, there are no reports on the health status of pet rabbits in Finland. The aim of the study was to obtain data on current health status of Finnish pet rabbits considered healthy by the owners by performing physical examination and lateral skull and lateral abdominal radiographic evaluation.

Materials and methods

This study was performed as part of the pet rabbit health research project in Finland. In total, 167 family-owned pet rabbits were recruited to the health survey by advertising over Finland. Rabbits needed to be considered healthy by the owners and not receiving any veterinary treatment at the time of the survey to be included to this study. Previous veterinary visits were not exclusive, but owner needed to assess the rabbit as basically healthy. The health survey was performed at the Small Animal Teaching Hospital of University of Helsinki during May 2012 and September 2013.

Physical examination was performed in all rabbits by the first author using the same protocol that included assessment of the skin, coat and perineal region, palpation of the skull and the visual examination of the eyes, ears, nares and incisors. The chest was auscultated for cardiac murmurs, dysrhythmias or abnormal respiratory sounds and abdomen was palpated. The posture was recorded as normal or abnormal and extremities were examined for abnormalities. Each rabbit was weighed. Once the physical examination was completed, 160 of the rabbits were sedated with the owner's consent using a standardised protocol of medetomidine 0.1 mg/kg (Cepetor; CP Pharma Handelsgesellschaft GmbH) and ketamine 5 mg/kg (Ketaminol; Intervet International BV) administered subcutaneously. The seven remaining rabbits were not sedated either because of the findings of the physical examination or because the owners did not consent to sedation. These rabbits were radiographed conscious.

Lateral abdominal and lateral skull radiographs of all rabbits were taken. For lateral abdominal radiography, the primary beam was centred on the last rib. In rabbits weighing <5 kg, the thorax was included on the radiograph. Under sedation the cheek teeth and oral cavity were examined with an otoscope. Conscious examination of oral cavity was performed in the unsedated rabbits. The dentition was graded using the grading system of progressive syndrome of acquired dental disease (PSADD) (Table 1) (Harcourt-Brown 1997). At the end of the procedure, atipamezole 0.25 mg/kg (Revertor, CP Pharma Handelsgesellschaft mbH) was given subcutaneously to the sedated rabbits to reverse the effects of medetomidine.

TABLE 1:

Grading of acquired dental disease (PSADD)

The lateral abdominal radiographs were initially evaluated by the first author before discussing any abnormal findings with the second author. The radiographs were examined in a systematic manner. The gastrointestinal tract was evaluated for any abnormal gas shadows, organ distensions or impacted contents. The liver was examined for abnormalities, such as enlargement and calcifications. Presence of renal or urinary calculus, sediment in the bladder or uterine enlargement was recorded in the evaluation of the genitourinary tract. The vertebral column was examined for changes in bone density, angulation deformities, narrowed intervertebral spaces, calcified intervertebral discs, facet joint osteoarthritis and spondylosis deformans. The whole abdomen was examined for abnormalities such as masses, mineralisation in the abdominal fat or aortic calcification.

The lateral skull radiographs were evaluated by the first two authors independently. The structures of the skull were examined for abnormalities, such as evidence of osteopenia, areas of calcification, osteolysis or proliferative bone. The shape, structure and occlusion of the teeth were examined closely. Both authors graded the radiographic dentition from 1 to 5 using a system that has been used to grade the progression of acquired dental disease previously (Table 1) (Harcourt-Brown 1997). Differing results in grading were discussed by the authors to produce an agreed result.

The information from the health examinations and radiographs was encoded into Numbers ‘09 (Apple) and were used as a base for the statistical analysis. Age was used as both a continuous variable and a dichotomised variable (<3 years, ≥3 years). Data analysis and statistics were carried out by using SPSS 22 TM. Fisher's exact and likelihood ratio tests were first used to evaluate the statistical significance of the association between the variables. The significance level of 0.05 was used for all analysis (P<0.05). Goodman and Kruskal's tau (GK#120591;) yielded the coefficients of determination for predicting the variances of the dependent variables and Cramér's V and Phi coefficient were calculated for possible meta analysis. OR for risk assessment was also calculated using Mantel-Haenszel test for 2×2 tables.

Results

In total, 167 pet rabbits from 64 different owners participated in the study (Table 2). Seventeen breeds were represented with dwarf lop as the largest group (n=47, 28.1 per cent). Mixed breed rabbits were the second largest (n=43, 25.7 per cent). The mean age of the rabbits was 2.8 years (range 0.3–9.3 years). Also, 83 rabbits (51.5 per cent) were females, of which 12 were neutered (14.0 per cent), and 81 (48.5 per cent) rabbits were males, of which 35 were neutered (43.2 per cent).

TABLE 2:

Breed, age and gender distribution of the 167 pet rabbits

The findings of the physical examination precluded sedation in four rabbits. These were stage III/VI heart murmur (n=1), dysrhythmia (n=1), emaciation (n=1) and suspected renal failure (n=1). One exceptional small young rabbit and two old rabbits were not sedated at the owners’ request.

The results of the physical and radiological examinations are listed in Table 3. Abnormalities were detected in 118 rabbits (70.7 per cent) either during physical or radiographic examination. In total, 105 rabbits (62.9 per cent) had radiographic findings and 76 rabbits (45.5 per cent) had findings in the physical examination. Sixty-three (37.7 per cent) rabbits had abnormal findings both in physical and radiographic examination. The findings were significantly more common in rabbits over three years old of which 51 (82.3 per cent) had finding in at least one examination (P<0.05, OR=2.6, 95% CI 1.23 to 5.64).

TABLE 3:

Results of the physical and lateral skull and lateral abdominal radiographic examination in 167 pet rabbits

Dental disease was the most common finding in both physical and radiographic examinations. The total prevalence of dental abnormalities, including hypodontia and incisor abnormalities, in the study was 45.5 per cent (n=76). The prevalence of PSADD detected by oral or radiographic examination was 40.1 per cent (n=67). PSADD was diagnosed during the physical examination in 36 rabbits (21.6 per cent) and in 64 rabbits (38.3 per cent) during radiographic evaluation. Diagnosis of PSADD in oral examination was strongly associated with PSADD diagnosed during radiographic examination (P<0.001), although, in two rabbits, mild molar teeth spurs and, in three rabbits, enamel hypoplasia of the incisors were seen during oral examination, but there was no sign of dental disease on the lateral skull radiograph. Conversely, radiographic signs of dental disease grade 2 were seen 31 rabbits (18.6 per cent) that showed no abnormality of their cheek teeth during oral examination. Apical elongation was evident on their radiographs (Fig 1). Also, 14 out of the 167 rabbits were graded differently by oral examination and evaluation of the lateral skull radiographs. All these rabbits had minor findings that placed them in grade 1 or 2 during the physical and radiographic examination.

FIG 1:

Lateral skull radiograph of a pet rabbit with mild elongation of molar rooths (progressive syndrome of acquired dental disease grade 2). The line of the alveolar bone at the apex of the tooth root is indistinct and the ventral border of the mandibular bone is thin (white arrow). No abnormalities were observed during the oral examination

Acquired dental disease (PSADD) was significantly more common in rabbits over three years old (P<0.05) and was equally observed in both genders (females 40.7 per cent, males 39.5 per cent). Frequency of PSADD was higher in lionhead rabbits compared with other breeds in this study (P<0.05). No association was seen between other breeds and dental disease.

Seven rabbits (4.2 per cent) had hypodontia, incisor or peg teeth malocclusion. Dental abscesses were diagnosed in five rabbits (3.0 per cent) by radiolucent areas in periapical area, pus in the gingival sulcus and irregularity and pain of the surrounding bone in the palpation.

Disorders of the vertebral column were the second most common finding of the study (n=52, 31.1 per cent). These were all detected by radiography. Degenerative lesions (spondylosis, calcified discs, narrowed disc spaces, facet joint arthritis) were diagnosed in 26 rabbits (15.6 per cent), spondylosis was the most common (n=20, 12 per cent). Narrowed intervertebral disc spaces (Fig 2a) were seen in eight rabbits (4.8 per cent), facet joint osteoarthritis in six rabbits (3.6 per cent) and one rabbit (0.6 per cent) had lumbar intervertebral disc calcification (Fig 2b). Degenerative vertebral lesions were observed in 35.5 per cent (n=22) of rabbits over three years old, which is significantly more often than in rabbit younger than three years old (P<0.001, OR=13.9, 95% CI 4.5 to 42.8). Prevalence was not associated with the breed or gender. Angulation deformities of the vertebral column (Fig 2c, d) were diagnosed in 30 rabbits (18.0 per cent) and deformities were significantly more common in dwarf lops (P<0.001, OR=7.0, 95% CI 3.0 to 16.5) of which 40.4 per cent (19 out of 47) were affected. Affected dwarf lops were owned by 15 different owners, 6 of those were breeding rabbits (4 males, 2 females), 3 were used for rabbit shows and 2 were show jumping rabbits. No differences between age or gender were noticed. Four rabbits were diagnosed with both degenerative disorders and angulation deformities. No association was found between degenerative lesions and deformities.

FIG 2:

Different vertebral column disorders in pet rabbits. (a) Narrowed intervertebral disc space and osteosclerosis of the vertebral endplates between thoracic vertebrae 9 and 10 (white arrow). (b) Calcified intervertebral discs between lumbar vertebrae L1–2 and L2–3 (white arrows). Facet joint osteoarthritis (facet joint of L1–2 marked with asterisk). (c) Mild deformity (lordosis) of the thoracic spine (Th 9–10) (white arrow). (d) Severe deformity (lordosis) of the thoracic spine (Th 8–10) (white arrow)

Skin disorders were the third most common finding (n=28, 16.8 per cent) and included scaling (n=10, 6.0 per cent) of which five rabbits were diagnosed with Cheyletiella parasitovorax, local alopecia due to self-mutilation or barbering by the other rabbits or animals (n=7, 4.2 per cent) and skin nodule (n=4, 2.4 per cent). Other skin pathologies included dermatitis (n=3, 1.8 per cent), mild pododermatitis (n=3, 1.8 per cent), perineal scalding (n=2, 1.2 per cent), accumulation of the faeces in the perineal region (n=2, 1.2 per cent) and bite wounds (n=1, 0.6 per cent). No association between skin disorders and dental diseases was noticed in this study.

Ocular disorders were found in 12 rabbits (7.2 per cent). Ocular discharge was seen in eight rabbits (4.8 per cent) of which seven had PSADD (grade 2, n=2; grade 3, n=2; grade 4, n=2; grade 5, n=1). Ocular discharge was strongly associated with PSADD diagnosed during the physical examination (P<0.01). Three rabbits were diagnosed with corneal scars (1.8 per cent), one rabbit with glaucoma (0.6 per cent) and another with persistent pupillary membrane (0.6 per cent).

Three rabbits (1.8 per cent) had healed fractures in the distal limbs, one (0.6 per cent) had tendon rupture in two digits and four (2.4 per cent) had osteoarthritis of the distal limbs (carpus, elbow, stifle, hock). Osteoarthritis was significantly more common in rabbits over three years old (P<0.05). Two rabbits (0.2 per cent) had an abnormally low standing position with the hind limbs in varus (cow-hocked) position, which was associated with lumbar vertebral deformity. One rabbit (0.6 per cent) had nail injury. Other findings were torticollis (n=1, 0.6 per cent), inguinal hernia (n=1, 0.6 per cent), nasal discharge (n=1, 0.6 per cent), emaciation and collapse (n=1, 0.6 per cent), sneezing (n=1, 0.6 per cent), heart murmur stage III/VI (n=1, 0.6 per cent) and arrhythmia (n=1, 0.6 per cent).

Fourteen rabbits (8.4 per cent) had calcified tissue in the abdomen on their radiographs. This was more common in older rabbits (P<0.05). It was the only finding in 5 of the 14 rabbits. In four cases, the calcified tissue was in the caudal abdomen of neutered female rabbits and was suspected to be calcification of the ligatures in the broad ligament. In two cases (1.2 per cent), the calcification was either similar to the calcified necrotic lipoma reported by Chitty (Lennox 2014) (Fig 3a) or the calcified lesion in the liver reported by Harcourt-Brown (Lennox 2014). In one case, the stomach was filled with fluid, gas and small calcified particles that appeared to be in the stomach contents (Fig 3b). Calcified particles appeared to be in the gastrointestinal tract in another five cases (3.9 per cent). Two rabbits (1.2 per cent), both aged 6 years, had a calcified mass in the uterus. Aortic calcification was seen in one rabbit (0.6 per cent) and calculi in the renal pelvis were seen in two rabbits (1.2 per cent) (Fig 3c). One rabbit (0.6 per cent) had obvious sediment in the urinary bladder. Other abdominal radiographic abnormalities included a rabbit with an obvious gas shadow surrounding the stomach contents. Another had an enlarged liver. On the skull radiographs, 10 rabbits (6.0 per cent) had mineralisation of the soft tissue in the nasal cavity.

FIG 3:

Findings in the abdominal radiographs of pet rabbits. (a) Calcified tissue in the abdomen (white arrows) similar to the calcified necrotic lipoma reported by Chitty (Lennox 2014). (b) Fluid and gas-filled stomach (asterisk) with small calcified particles inside (white arrow). (c) Nephrolithiasis (calculi in the renal pelvis) in a rabbit with chronic kidney disease (white arrows). Note marked osteosclerosis in all bones and spondylosis deformans between lumbar vertebrae (open arrow showing spondylosis deformans between lumbar vertebrae 1 and 2)

Discussion

This survey showed that abnormalities are common in pet rabbits that are believed to be healthy by the owners. Abnormalities were found during the physical and/or radiographic examination in 118 (70.7 per cent) of the 167 rabbits that were examined. Some of the abnormalities were severe. Voluntary participation to the survey could have affected disease incidence because many of the rabbits were owned by dedicated owners who looked after them well and fed them on a good diet so their rabbits may have been healthier than the pet rabbit population as a whole. Conversely, the health examination including radiography was free of charge. This may have attracted rabbit owners that suspected their rabbit was ill but claimed it was healthy in order to qualify for free investigations.

Acquired dental disease was most common finding and found in 67 (40.1 per cent) of all examined rabbits. The results are in accordance with previous studies where the reported prevalence of dental disease had varied between 6.7 and 38.1 per cent in different pet rabbit populations (Mullan and Main 2006, Jekl and others 2008, Mosallanejad and others 2010). In this study, dental disease was diagnosed by oral examination and lateral skull radiography. Ventrodorsal, oblique, rostrocaudal or intraoral radiographs, CT or endoscopic examination of the oral cavity could have increased the prevalence of dental disease and other dental abnormalities. The prevalence of PSADD grade 2 was 77.7 per cent higher when it was diagnosed from radiographs in comparison with oral inspection. Thirty-one rabbits without findings in the inspection of molar teeth had mild apical elongation of molar teeth root in the radiographs, which supports the finding that apical elongation is the initial stage of PSADD (Harcourt-Brown 1997).

Mullan and Main (2006) reported that owners were often unaware of their rabbit's dental problems, and this finding was also present in this study. Mosallanejad and others (2010) reported higher prevalence of acquired dental disease in rabbits over three years of age compared with younger rabbits, which also agree with this survey and makes sense as PSADD is a progressive and irreversible disease. Analysis of breed incidence showed that lionheads were significantly more affected by PSADD in comparison to other breeds although the total number of lionheads in this study was low (14), so the importance of this finding is unclear. Brachycephalism in dwarf breed rabbits, inherited mandibular prognathism and maxillary brachygnatism are reported causes of incisor malocclusion (Verstraete and Osofsky 2005, Reiter 2008), but, to the authors’ knowledge, no other breed-related risks are described in the literature. A study on dental disease among pet rabbits showed an association with dermatological disorders, but this was not observed in this survey (dOvidio and Santoro 2013).

Degenerative lesions and deformities of the vertebral column are frequent findings on lateral radiographs of rabbits (Hunt 2014), although, to the authors’ knowledge, there are no previous prevalence data published on vertebral column disorders in pet rabbits. In this survey, the prevalence of angulation vertebral deformities was 18.0 per cent and degenerative vertebral lesions (spondylosis, calcified discs, narrowed disc spaces, facet joint arthritis) 15.6 per cent. Most of the degenerative vertebral column lesions (84.6 per cent) were observed in rabbits older than three years old. As vertebral column radiographs including the whole spine in ventrodorsal or dorsoventral radiographic views were not taken, the true prevalence of vertebral column abnormalities could be much higher. Mild vertebral column abnormalities may be clinically insignificant, but more severe lesions can cause pain and affect the rabbits’ ability to reach the perineal region for grooming and consumption of caecotrophs (Hunt 2014). Increased prevalence of spinal deformities were observed in breeding does kept in small cages compared with bucks by Drescher and Loeffler (1996). They noticed an association with small cage size and attributed the spinal deformities to the abnormal low-standing position and lack of exercise, which decreased bone mineral density. Forces affecting the spine and high demand for calcium during pregnancy and lactation were considered to be additional factors.

In this study, narrowed intervertebral disc spaces were observed in eight rabbits and calcified intervertebral discs in one rabbit. Rabbits are popular animal models for intervertebral disc disease (IVDD), and age-related degeneration of intervertebral discs is reported in rabbits (Leung and others 2008). Clinical IVDD cases in pet rabbits are seldom reported but may be misdiagnosed if proper diagnostic imaging (myelography, CT, MRI) is not performed. Neurological signs are common in pet rabbits, and signs mimicking IVDD can be caused by several other diseases such as Encephalitozoon cuniculi infection, fracture and tumours (Harcourt-Brown 2002).

The incidence of uterine neoplasia in this study was low compared with prevalence of uterine tumours in literature (Greene 1941, Heatley and Smith 2004). Two cases were diagnosed by radiography and palpation. More cases could have been present because the diagnosis of uterine disorders often requires additional diagnostic procedures. None of the rabbits had sludgy urine or bladder stones.

Only two rabbits with perineal scalding and three rabbits with mild pododermatitis were recorded in this study. Ocular discharge was strongly associated with PSADD diagnosed in physical examination (P<0.01). Dental-related obstruction and infection of nasolacrimal duct are well known in rabbits, but there are other reasons for ocular discharge (Florin and others 2009, Saunders 2014). Further investigations, such as nasolacrimal duct irrigation, Jones test, dacryocystorhinography or bacterial culture of discharge, might have given more information but were not performed in this study.

Other limitations of the survey included the lack of other projections in the radiographic examination. Only a lateral abdominal view was taken, which limited the radiological interpretation and some abnormalities might have been missed. Also, the prevalence of ear disease was not studied in this survey. Accumulation of cerumen is common, especially in lop-eared rabbits due to the anatomy of the ear canal (Chitty 2014). Diagnosis of otitis would have needed sampling, cleaning of the ear canal for better visualisation and more precise imaging like CT to ensure the diagnosis. However, no abnormalities indicating ear canal diverticulosis or abscesses were observed during palpation.

The overall prevalence of abnormalities was significantly higher in older than in younger rabbits, altogether 82.3 per cent (n=51) of rabbits over three years old having findings in physical or radiographic examination. The average life expectancy in rabbits is increased within last years, and it is not uncommon to meet rabbits over 10 years of age especially in the case of medium-sized rabbits (Lennox 2010, Chitty 2014). Medium-sized rabbits may be considered geriatric at seven years of age, but dwarf and giant breeds have shorter life expectancy and geriatric diseases may be seen in these breeds at four to five years of age (Chitty 2014). Chitty (2014) and Lennox (2010) recommend regular physical examination twice yearly. Considering the results of this survey, regular physical examinations are advised specially for rabbits over three years of age.

Acknowledgments

The authors would like to thank Mr Vesa A. Niskanen (PhD, Associate Professor, Adjuct Professor Docent) for his help with the statistical analysis.

REFERENCES

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Footnotes

  • Provenance: not commissioned; externally peer reviewed

  • Ethics approval The national Animal Experiment Board of Finland (5562/04.10.03/2011).

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