Bone fractures are an important clinical condition in rabbits; however, little information has been published regarding causes and treatments of naturally occurring fractures in rabbits kept as pets.1 Rabbits might have a higher risk for skeletal fractures than do other companion animal species because their bones comprise a lower proportion of their total body weight.2
Radiographic examination is usually performed to help diagnose fractures in companion animals. However, radiographic images are generally insufficient for fracture assessment and treatment planning when fractures are comminuted or involve complicated structures such as the pelvis, vertebrae, and skull. Computed tomography can be used to obtain more detailed imaging information for fracture evaluation in dogs and cats.3,4 Multiplanar reformation images and volume-rendered 3-D images are particularly helpful in characterization of complicated anatomic abnormalities.5,6 However, CT cannot be used to detect small orthopedic lesions in smaller companion animal species such as rodents and rabbits, and the need for anesthesia to keep patients motionless during the scanning process makes CT even less suitable for these species.
Development of imaging techniques such as micro-CT has enabled more detailed assessment of bone diseases in small animals.7–9 Micro-CT involves use of a microfocal source (range in slice thickness, 30 to 150 μm), and 2-D or 3-D spatial resolution is possible independent of patient body position. Compared with conventional multislice CT scanning, micro-CT scanning requires much shorter patient exposure times (fastest scanning time, 10 to 18 seconds). These advantages suggest that micro-CT could be used to obtain highdefinition images to aid diagnosis of fractures in rabbits. The objective of the study reported here was to characterize bone fractures in a large group of rabbits with respect to age at onset, cause, and site of origin. We also sought to evaluate a new method for imaging fractures via micro-CT and compare results with those of radiography.
Materials and Methods
Case selection—A database of patients evaluated at the Kitasuma Animal Hospital was reviewed to identify pet rabbits evaluated for bone fractures from 2007 through 2013. To be included in the study, rabbits were required to have had fractures that were diagnosed on the basis of clinical signs and radiographic or micro-CT findings.
Medical records review—Data extracted from the medical records included rabbit age, sex, breed, and body weight; cause of fracture if known; and anatomic site of fracture origin. Long-bone fractures were classified by the investigators on the basis of anatomic site of origin (humerus, 1; radius, 2; femur, 3; and tibia, 4), position (proximal region, 1; diaphysial region, 2; and distal region, 3), and severity (mild, A; medium, B; and severe, C) in accordance with the Unger classification system.10 For example, a simple fracture of the shaft of the femur was classified as 32-A.
Imaging of fractures had been performed by use of conventional radiographic,a digital radiographic,b or micro-CTc,d devices. Choice of micro-CT device had been made on the basis of the seating capacity of the signal bridge (device 1 was used for rabbits with a body weight < 2 kg [4.4 lb], and device 2 was used for heavier rabbits). Micro-CT device 1c had a 512 × 512 display matrix with an x-ray tube (5-μm focus; 1 rotation = 17 seconds) and 2-D flat panel detector with rotary arm. Slice thicknesses were 150 and 120 μm. Scanning conditions included a tube voltage of 90 kV, tube electric current of 160 μA, and focal-spot size of 27 μm. Images were obtained with a minimum voxel size of 10 μm, and the anatomic region of suspected fractures was imaged at 512 × 512 × 384 pixels with an exposure duration of 18 or 120 seconds. Scan region dimensions were 73 mm in diameter and 60 or 120 mm in height. For micro-CT device 2,d 512 image slices were acquired with an x-ray tube (33-μm focus; 1 rotation = 18 seconds) and 2-D flat panel detector and rotary arm. Slice thickness ranged from 60 to 440 μm. Scanning conditions included a tube voltage of 80 kV, tube electric current of 400 μA, and focal-spot size of 33 μm. Images were obtained with a minimum voxel size of 60 μm, and the region of suspected fractures was imaged at 512 × 512 × 512 pixels with an exposure duration of 18 or 150 seconds. Scan region ranged from 30 mm in diameter × 30 mm in height (minimum) to 220 mm in diameter × 118 mm in height (maximum). Detection involved use of an amorphous silicon pattern, and reconstruction was performed by use of the Feldkamp-Davis-Kress algorithm method in a manner synchronous with respiratory cycle.
Statistical analysis—Continuous data are reported as median and range, and categorical data are reported as number and percentage. Median age at which fractures occurred was compared between rabbits with fractures attributed and not attributed to neoplasia by use of the Mann-Whitney U test. Distributions of fractures attributed or not attributed to neoplasia were compared between sexes by use of the Fisher exact test. All analyses were performed with the aid of statistical software.e Values of P < 0.05 were considered significant.
Results
Animals—A total of 211 rabbits had a diagnosis of fracture during the study period. One rabbit with multiple fractures of all limbs was excluded from the study, leaving 210 rabbits for analysis. All but 2 (1%) of the included rabbits had single fractures. Of the 2 rabbits with multiple fractures, 1 had bilateral radial fractures and the other had bilateral calcaneal fractures.
One hundred fifteen (54.8%) rabbits were male, and 95 (45.2%) were female. Median age was 3.1 years (range, 0.3 to 11.9 years), and median body weight was 1.6 kg (3.5 lb; range, 0.3 to 3.0 kg [0.7 to 6.6 lb]). Breeds included Dwarf (n = 147 [70.0%]), Netherland Dwarf (33 [15.7%]), Holland Lop (16 [7.6%]), American Fuzzy Lop (5 [2.4%]), Japanese White (4 [1.9%]), Lepus (2 [1.0%]), and Himalayan, Jersey Wooly, and Mini Rex (1 [0.5%] each). Distributions of fracture types were summarized by year of age, revealing that 1-year-old rabbits were the most common age group in the study sample (Figure 1). Almost half (n = 95 [47.7%]) of fractures were in rabbits < 3 years old.
Distribution of sites of bone fracture origin by year of age in 210 pet rabbits. Site of origin was determined by review of radiographic and micro-CT images. Two (1%) rabbits had multiple fractures.
Citation: Journal of the American Veterinary Medical Association 246, 12; 10.2460/javma.246.12.1339
Causes of fractures—The most common cause of fractures was accidental fall due to human error (n = 52 [24.8%] rabbits) or other reasons (48 [22.9%]). Other causes included hopping when in cage (12 [5.7%]), neoplasia (12 [15.7%]), handling error unrelated to accidental fall (9 [4.3%]), veterinarian error (6 [2.9%]), hopping when outside cage (5 [2.4%]), trampling by humans (5 [2.4%]), trapping by closing door (4 [1.9%]), and miscellaneous (eg, bitten by dog, injured by falling object, abscess formation, or trapped in cage; 22 [10.5%]). Cause of fracture for 35 (16.7%) rabbits was unknown (not seen by owners or not recorded in medical record).
Types of neoplasia in the 12 affected rabbits included metastasis of uterine adenocarcinoma to bone tissue (7), confirmed osteosarcoma (2), extraskeletal osteosarcoma (1), rhabdomyosarcoma (1), and suspected osteosarcoma (1). Median age of this subgroup was significantly (P < 0.001) higher than that of rabbits with fractures not attributed to neoplasia (Table 1). Median body weight of the subgroup did not differ significantly from the median body weight for other rabbits with fractures. Females were significantly (P = 0.02) more likely to have a fracture attributed to neoplasia than were males. Fracture by metastasis of uterine adenocarcinoma was identified in 7 of 79 (8.9%) unneutered female rabbits.
Median (range) age and body weight and number (%) of males and females for pet rabbits with fractures attributed (n = 12 rabbits) or not attributed (198) to neoplasia.
| Variable | No neoplasia | Neoplasia |
|---|---|---|
| Age (y) | 3.0 (0.3–11.9) | 7.5 (4.3–9.5)* |
| Body weight (kg) | 1.5 (0.3–3.0) | 1.8 (1.3–2.3) |
| Sex | ||
| Males | 113 (98.3) | 2 (1.7) |
| Females | 85 (89.5) | 10 (10.5)† |
Value differs significantly (P < 0.001) from value for rabbits without neoplasia (Mann-Whitney U test).
Value differs significantly (P = 0.02) from value for rabbits without neoplasia (Fisher exact test).
Two (1%) rabbits had multiple fractures.
Sites of fracture origin—Sites of fracture origin in the 198 rabbits with fractures not attributed to neoplasia were vertebral column (46 [23.2%]), tibia (45 [22.7%]), femur (26 [13.1%]), radius (23 [11.6%]), pelvis (ie, ilium, coxa, or ischium; 14 [7.1%]), humerus (9 [4.5%]), mandible or maxilla (9 [4.5%]), metatarsal bone (7 [3.0%]), metacarpal bone (6 [3.5%]), talus (4 [2.0%]), phalanges of the forelimb and hind limb (3 [1.5%] each), and coccyx (1 [0.5%]). Fractures involved multiple sites in 3 (1.5%) rabbits. Limb fractures were identified in 126 (63.6%) rabbits, with 94 (47.4%) of those fractures in 1 of 3 bone types (ie, radius, tibia, and femur). The ratio of forelimb to hind limb fractures was 1:2. The most common types of long-bone fractures not attributed to neoplasia were simple fractures of the tibial shaft (42-A), radial shaft (22-A), and femoral shaft (32-A) and segmental fractures of the tibial shaft (42-C) and femoral shaft (32-C; Figure 2). In the 12 rabbits with fractures attributed to neoplasia (5 caused by metastasis of uterine adenocarcinoma and the remainder caused by other tumors), limbs were also the most common site of fracture origin.
Distribution of location and severity of 103 long-bone fractures with nonneoplastic causes in 103 pet rabbits. Fractures were classified by investigators on the basis of anatomic site of origin (humerus, 1; radius, 2; femur, 3; tibia, 4), position (proximal aspect, 1; diaphysial region, 2; distal aspect, 3), and severity (mild, A; medium, B; severe, C).13 See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 246, 12; 10.2460/javma.246.12.1339
Sites of fracture origin in the 46 rabbits with vertebral fractures not attributed to neoplasia were in the T9-L7 region. The L4-L7 region was a common fracture site (n = 37 [80.4%] rabbits; Figure 3). Vertebral fractures in the 2 rabbits with metastasis of uterine adenocarcinoma occurred in the region of vertebrae C5 and L2, respectively.
Distribution of sites of origin for 46 vertebral fractures with nonneoplastic causes in 46 pet rabbits. See Figure 1 for remainder of key.
Citation: Journal of the American Veterinary Medical Association 246, 12; 10.2460/javma.246.12.1339
Usefulness of micro-CT imaging—Information from the 3-D surface rendering images obtained via micro-CT was detailed. Tertiary structures of complicated fractures were clearly visible in micro-CT images of rabbits with humeral and tibial fractures. Fractures of the maxilla that were difficult to detect in detail in both conventional and digital radiographic images were clearly visible in micro-CT images, which lacked the interference from a shadow that arose from the lateral aspect of the opposite maxilla in radiographic images (Figure 4). In rabbits with fractures of the lumbar vertebrae, the exact nature of the fractures was difficult to identify in radiographic images because of overlapping tertiary structures. Three-dimensional volume rendering provided more information than did radiographic examination. With micro-CT, it was also possible to clearly identify fractures of the distal region of the femur attributed to neoplasia (Figure 5). Evidence of metastasis of uterine adenocarcinoma to cervical vertebrae could not be easily detected in radiographic images but was visible in micro-CT images.
Images of bone fractures in 4 pet rabbits obtained via micro-CT (A,B,D,F) and conventional radiography (C,E). Micro-CT 3-D surface rendering images of the humerus (A) and tibia (B) reveal details of comminuted fractures. A mandibular fracture that is difficult to identify in a left lateral radiographic image of the skull (C) is clearly visible in a 3-D surface rendering image (D). The tertiary structure of a complicated lumbar vertebral fracture is difficult to identify in a left lateral radiographic image of the vertebral column (E) and is more easily identified in a 3-D volume rendering image (F). Arrows indicate fracture sites.
Citation: Journal of the American Veterinary Medical Association 246, 12; 10.2460/javma.246.12.1339
Images of bone fractures in 3 pet rabbits obtained via micro-CT (A,B,D,E) and conventional radiography (C). A micro-CT 3-D surface rendering image of the lateral aspect of the stifle joint reveals a fracture in the distal aspect of the femur that occurred when the rabbit was accidentally dropped by its owner (A). A 3-D surface rendering image of the distal aspect of the stifle joint in another rabbit reveals a fracture and osteolytic lesions (arrowheads) attributed to neoplasia (B). The fracture site in another rabbit with uterine adenocarcinoma that metastasized to the cervical vertebrae is difficult to identify in a right lateral radiographic image of the vertebral column (C). Greater detail is seen in a 3-D surface rendering image of a similar view of the same rabbit as in panel C, which reveals severe osteolysis with a collapsing fracture and shortening of the C6 vertebral body (D). A 3-D surface rendering image of the ventral aspect of the vertebral column in the same rabbit as in panel C reveals additional detail of the fracture (E).
Citation: Journal of the American Veterinary Medical Association 246, 12; 10.2460/javma.246.12.1339
Discussion
The present study was conducted to characterize bone fractures in a large sample of pet rabbits. The age at which the most fractures occurred was 1 year, which is the age during which rabbits might be most active because of reaching sexual maturity. To the authors’ knowledge, this was the first study in which age distribution of rabbits with fractures was determined. In contrast to common causes of the fractures in dogs and cats (road accidents, falls, and crushing injuries),11,12 the predominant causes of fractures in the study rabbits were spontaneous accidents and unidentified incidents. Also unlike dogs and cats, rabbits are prey animals that, in the authors’ experience, startle easily and are highly sensitive to perceived threats. Accidental fall was the most common cause of fracture in our study. Therefore, opportunities exist for veterinarians to educate rabbit owners on safe handling techniques.
Overall, 5.7% of rabbits with fractures were confirmed to have tumors in the present study. A few reports13–15 of osteosarcoma in rabbits exist, but there has been only 1 report16 of fractures attributed to metastases of uterine adenocarcinoma to bone tissue. Four types of tumor-associated fractures were identified in the study rabbits; 7 fractures were attributed to metastasis of uterine adenocarcinoma. The prevalence of uterine adenocarcinoma is reportedly high in female rabbits ≥ 3 years old and even higher in rabbits ≥ 7 years old.1,17 In most affected rabbits, tumors are metastatic. Uterine adenocarcinoma is primarily diagnosed on the basis of clinical signs such as hematuria, anorexia, and abdominal distension. Rabbits without these signs but with metastasis to lungs, bones, and intra-abdominal organs have a poor prognosis by the point clinical signs develop and a diagnosis is confirmed.1,17 In the present study, a rabbit with neurologic signs had a vertebral fracture attributed to metastasis of uterine adenocarcinoma. Such fractures could develop in middle-aged and older, unneutered female rabbits.16 In addition to osteosarcoma, metastasis of uterine adenocarcinoma should be included in the list of differential diagnoses when evaluating rabbits for lameness or fractures, particularly when rabbits are ≥ 7 years old.
Limb fractures accounted for 63.6% of all fractures in the present study. The tibia was the most commonly affected site, accounting for 22.7% of all fractures. Segmental fractures were more common in the study rabbits than in dogs.10,11 Bone weight accounts for only 7% to 8% of total body weight in rabbits, and this proportion is lower than that in dogs and cats (12% to 13%).2 Rabbits move forcefully, and their powerful kicks exert considerable force on the hind limbs, putting the hind limbs at greater risk for fracture development than forelimbs. Researchers in another study11 classified 386 limb fractures in dogs by use of the Unger system and found that simple fractures of the diaphyseal region (including the radius, femur, and tibia) were common. On the other hand, several types of tibial fractures (simple and segmental) were represented in the rabbits of the present study in addition to segmental fractures of the femur and radius. Rabbits with humeral, femoral, or pelvic fractures were of a wide age range. Although obesity, decrease in muscle mass, and age-related weakening of bones were not evaluated in our study, fractures in older rabbits might have been influenced by these factors.
Vertebral fracture was identified in 46 of 198 (23.2%) rabbits in the present study with fractures not attributed to neoplasia, and the cause involved human error. This finding was similar to that in a previous report18 in which inappropriate handling was identified as the primary factor responsible for vertebral fracture in rabbits. Our study revealed that the L5 vertebra was the most commonly affected site for vertebral fracture, contrary to published information1 that the L7 vertebra and L6-L7 region are the most common sites in rabbits. Fractures in the L4-L7 region may have serious consequences for affected rabbits, including neurapraxia of the hindquarters and injury of the spinal cord. Vertebral injuries associated with hind limb paralysis may also cause severe hemorrhage, intense pain, difficulty with defecation or urination, and death. These findings once again emphasized the importance of stressing safe handling to any individual caring for pet rabbits.
Computed tomographic devices designed for use in human medicine have been used to obtain CT images of rabbits.18 In the present study, the usefulness of images obtained via micro-CT was compared with the usefulness of radiographic images in the diagnosis of fractures in rabbits. Because of the high resolution that results from the tiny focal spot obtained with a micro-CT device, micro-CT was predicted to be useful as a diagnostic tool for the rabbits in our study. Indeed, detailed information was obtained through examination of micro-CT images that could not be obtained with radiographic images. Comminuted fractures of long bones and fractures of the structurally complex skull, pelvis, and vertebrae were clearly visible in micro-CT images. In many rabbits, fracture lines (or fractures) that could not be confirmed by examination of radiographic images (eg, differentiation of tumor-associated fractures and small lesions such as those identified in the vertebrae of rabbits with metastatic uterine adenocarcinoma) were visible in micro-CT images. Images obtained with 3-D surface and volume rendering allowed identification of positional relationships among bony structures and extent of damage from the injury. Findings of other studies9–11 indicated that detailed information could be obtained by means of micro-CT that was suitable for evaluation of small bone fractures in small rabbits (mean weight, 1.6 kg [3.5 lb]) and for evaluation of fractures in any anatomic region (eg, skull, vertebrae, pelvis, and bones of the extremities). The radiation dose associated with micro-CT is < 10 mGy, which is much lower than the dose that adversely affects the immune system of mice.19 Our findings suggested that micro-CT techniques can contribute considerably to detection of lesions in rabbits that cannot be clearly identified via radiography, providing detailed images to inform diagnosis and treatment.
Kodak MIN-R, Eastman Kodak Co, Rochester, NY.
Canon CXDI-70C, Canon Inc, Tokyo, Japan.
R_mCT2, Rigaku Co, Tokyo, Japan.
R_mCTAX, Rigaku Co, Tokyo, Japan.
Ekuseru-Toukei 2012, Social Survey Research Information Co, Tokyo, Japan.
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