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Case 1. Ursus ursinus Cuvier, 1823
A female Sloth bear Ursus ursinus, named ‘Frederica’, died in her sleep on 12 October 1995 at the Amsterdam zoo. She had arrived on 29 May 1965, at the age of six months, from the zoo of Calcutta, India, together with two other females and one male. Having reached almost 31 years of age, she was considered rather old for a Sloth bear: Jones (1982) gave a maximum life span of 28 years and Prater (1971) 40 years. She was the last of the four Sloth bears imported in 1965. The other three bears died of malignant tumors of the biliary system, which is a common cause of death for old zoo bears, especially Sloth bears (see e.g. Kingston & Wright, 1985; Canfield et al., 1990; Hellmann et al., 1991; Van der Hage & Dorrestein, 1994). Frederica gave birth to several pups between 1970 and 1987 (registration cards Natura Artis Magistra; Fig. 1).
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Fig. 1. Sloth bear Ursus ursinus ‘Sonja’ (daughter of ‘Frederica’), with pup born December 1987 in the Amsterdam Zoo ‘Artis’. Photo: Nationaal Foto-Persbureau B.V., Amsterdam). |
Autopsy was performed one day after death at the Veterinary Faculty of the University of Utrecht, The Netherlands. The abdominal cavity contained circa 25 litres of yellowish fluid. A mesothelioma was found. Ascites often complicated intra-abdominal malignancies (Kuntze, 1995). The colon showed a thickened red-coloured mucosa; from the contents, Proteus mirabilis, Proteus morganii, Escherichia coli, Streptococcus sp., and Enterobacteriaceae were cultured. A chronic colitis was suspected. Two specimens of the parasite Toxascaris transfuga were found in the stomach, which also contained an amount of blood. The cardia was thickened. Infection with Toxascaris transfuga is common in all species of Ursidae, but is rare in the Sloth bear (Kuntze, 1995).
The mounted skin and skeleton were saved for the collection of the Natural History Museum of Rotterdam (Natuurmuseum Rotterdam), The Netherlands (reg. no. 999000153). During preparation of the skeleton, severe pathological changes were found on the ventral and anterolateral sides of the lower thoracic and lumbar/sacral region of the vertebral column. The vertebral column was subsequently submitted to radiographic examination. After radiographs were made, the vertebral column was further dissected and the condition of the vertebral ligaments and the intervertebral disci were studied. The bones were then macerated in water, after which examination of the cleaned bones was possible. A preliminary report on this case was published by Kompanje & Klaver (1998)
Radiographic examination of the vertebrae
Radiographs were made of the entire vertebral column including the pelvis in ventrodorsal view. Radiographs in lateral view were made from the lumbar vertebrae. The cervical part showed some abnormalities. On the right anterolateral side of C2 new bone formation was visible as on the zyg-apophyseal joint between C5 and C6. The intervertebral disc space between C6 and C7 was narrowed. The radiograph of the lower thoracic and lumbar part showed typical nonmarginal syndesmophytes and paradiscal ossicles. On the radiograph in lateral view, large nonmarginal syndesmophytes were visible in the lower thoracic and upper lumbar region. The syndesmophytes along the lateral part of the vertebrae, also visible on the radiograph in ventrodorsal view, were vertically disposed and had a ‘bullhorn shape’ (Fig. 2). Sacroiliac fusion was evident in the upper region (Fig. 2). Calcification of the intervertebral disc was visible in the affected parts of the lumbar vertebrae on the radiograph in lateral view (Fig. 3). The costo-vertebral joints appeared to be normal.
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Fig. 2. Postmortem radiograph of the lower thoracic and lumbar vertebrae and pelvis of Ursus ursinus (case 1). Arrowheads indicate syndesmophytes; A = sacroiliac fusion. Spondyloarthropathy. |
Examination of the macerated skeleton
next sectionSkull. – The skull and dentition were as one should expect from an old zoo bear. Many teeth were lost during the bear’s lifetime and those remaining were severely worn. The canines showed signs of dental treatment. Surprisingly, all the apices of the canines were normal. No alveodental abscesses were found.
Forelimbs. – Both humeri and ulnae showed signs of osteoarthrosis (marginal osteophytes on the caput humeri and elbow joint) (Figs. 4 & 5). Some erosive lesions were found on the distal joint surfaces of both radii. Both scapulae showed features of osteoarthrosis on the margins of the glenoid fossa.
The middle three metacarpal bones of the right manus showed signs of healed fractures. The other two metacarpal bones, the carpal bones and phalanxes were normal, as were the bones of the left manus.
Hindlimbs. – Impressive features of osteoarthrosis were found on both caput femoris (eburnation, erosion, marginal osteophytes) (Fig. 6). The knee joint showed only mild features of osteoarthrosis. The right ankle joint showed a mixture of osteoarthrosis and erosive arthritis (the latter is a feature of spondyloarthropathy). The left one is only affected by osteoarthrosis. Large enthesophytes (calcifications of tendon attachments) were found on the dorsal side of the upper end of both tibiae (Fig. 7).
Severe erosive arthritis was found in the right subtalar and ankle joint. Erosions were also found between the third and fourth metatarsalia of the left foot. All the other bones of the feet were normal.
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Fig. 6. Capita femoris of Ursus ursinus (case 1) showing features of osteoarthrosis. A = erosion of the cortex; B = marginal osteophytes. |
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Fig. 7. Tibiae of Ursus ursinus (case 1) with (A) large enthesophytes on the dorsal side of the upper ends. |
Cervical vertebrae. – Arthrosis and erosion was found in all zygapophyseal joints, most severe between C5 and C6, already visible on the radiograph. Marginal osteophytes, a sign of discarthrosis, were found on the ventral margins of all vertebrae. A large nonmarginal syndesmophyte was found on the right anterolateral side of C2. Erosion was found on the caudal vertebral endplate of C3 and the cranial vertebral endplate of C4. Severe erosion was found on the caudal endplate of C6 and cranial endplate of C7 (Fig. 8); normal covering bone plate was completely absent.
Thoracic vertebrae. – Arthrosis was found in all zygapophyseal joints, but most severe between Th8-Th9 and Th9-Th10. The whole area of contact was covered with erosion and perforations of varying size and there was new bone formation and eburnation. On several vertebrae large nonmarginal syndesmophytes were found, the most severe being in the lower thoracic spine after Th9. On some of the vertebrae marginal osteophytes were found, as a sign of discarthrosis. Th3, Th4 and Th5 were completely normal.
Lumbar vertebrae. – Large nonmarginal syndesmophytes were found on the ventral and anterolateral sides of all lumbar vertebrae. Involvement of the zygapophyseal joints was visible (Fig. 9). Paradiscal ossicles were found on the ventral side between L1 and L2, also visible on the radiograph in lateral view (Fig. 3). Extensive erosions were found on the caudal endplate of L5. Between L6 and the sacrum, ankylosis was found. Large nonmarginal syndesmophytes were found in this region (Fig. 8).
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Fig. 9. Severe erosion of the zygapophyseal joints (arrowheads) in a lumbar vertebra of Ursus ursinus (case 1). |
Pelvis, sacrum, and caudal vertebrae. – The sacroiliac fusion was asymmetric, on the left side in ventral view more complete than on the right. On the dorsal side the fusion was complete on both sides (Fig. 10). Extensive osteoarthrosis was found in the hip joints.
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Fig. 10. Pelvis and sacrum of Ursus ursinus (case 1) showing sacroiliac fusion on both sides (arrowheads). Spondyloarthropathy. |
Comments on case 1
On the spine, osteophytes and syndesmophytes were found as features of two different conditions: discarthrosis (spondylosis deformans) and spondyloarthropathy. Mixtaosteophytes as a combination of arthritis and arthrosis were also recognized.
Initial alterations in spondyloarthropathy are apparent at the thoracolumbar and lumbosacral junctions, as is seen in this case. Asymmetric fusion of the sacroiliac joints is typical for spondyloarthropathy of Reiter’s type and for psoriatic arthritis. The syndesmophytes in this Sloth bear were mostly unilateral and asymmetric in distribution, looking broad and bulky, characteristic of Reiter’s syndrome (Kerr & Resnick, 1985).
