Osteoporosis in an Asian small-clawed otter (Aonyx cinereus Illiger, 1815)

Abstract

Osteoporosis is a skeletal disease that occurs in many mammals. Our report describes osteoporosis in an Asian small-clawed otter (Aonyx cinereus). Gross, histological, and radiographic observations showed that all of the bones had numerous pockmarks on their surfaces. Histologically, the pockmarks were filled with fibrous tissue without inflammation. However, the spongy bone was normal according to the histological and radiographic results. Overall, the results showed that this was a case of osteoporosis that mainly involved external rather than internal surfaces.

The Asian small-clawed otter is the smallest otter in the family Mustelidae. Its distribution in Asia is broad, ranging from southeast China to India, the Indochina Peninsula, and Borneo Island in Indonesia. It is 45–61 cm in body length and weighs 1–5 kg [1, 3]. This otter species feeds on mussels, shellfish, crabs, and frogs living in rivers, creeks, and along coastlines [1, 3]. Bone disease has been reported in the sixth lumbar vertebra; right ischial osteolysis caused by a malignant lymphangiosarcoma that led to paresis was also reported [7]. However, to our knowledge, detailed information on other bone diseases afflicting this otter species is not available. The carcass of a 4-year-old male Asian small-clawed otter, stored at −15°C after death, was recently donated to our laboratory for educational purposes.

The otter weighed 2.08 kg, had a body length of 41 cm, and a tail of 26 cm. For more than 1 month before his death, the otter spent more time alone than with the group, and about 10 days before dying, he developed dysphagia. We found that both epihyoid bones were broken during the dissection and the carpal bone had lesions on the synovial cartilaginous surface (Fig. 1a). For general histological observation of the lesions, the right epihyoid bone, right radiointermediate carpal bone and second carpal bone, and left fabella were fixed and decalcified in commercial decalcification solution (OSTEOMOLL^®; Merck, Darmstadt, Germany) at room temperature for 4 days. The other bones were treated with 4% sodium decahydrate tetraborate at 90°C for 20 hr, and then dried in room air after washing in running water. This treatment was modified from a previous report [6]. The skeleton was treated with a 2% H₂O₂ solution for 48 hr and dried in room air. The main organs, including the liver, kidney, testis, and digestive tract, did not show any lesions, based on the gross findings. However, the lung and visceral pleura showed purulent necrotic foci.

Fig. 1.

Gross findings of the synovial joint and bones of an Asian small-clawed otter. Some lesions (arrows) on the synovial cartilage surface were found in the antebrachiocarpal joint. RIRC, right intermedioradial carpal bone. Proximal view (1a). The penile bone was deformed, with a deviated fusion line after fracture (1b). Numerous pockmarks created a rough bone surface. Several pockmarks on opposing surfaces were on the verge of joining together to form holes and the spine of the scapula was deviated (arrow) (1c, 1d). (1c) Dorsal view of the skull; (1d) Lateral view of the right scapula.

All bones were adult and had rough pockmarks (or pits) on their surfaces, even on the articular surface. These abnormalities were also found in the cranial and caudal extremities of the vertebrae, and on the attachment sites of the muscle tendons. The cortical bone of the thin skeleton, including the scapulae and skull, were characterized by several pockmarks on opposing surfaces that were on the verge of joining together to form holes (Fig. 1c, 1d). The scapular spine was deviated (Fig. 1d). The penile bone (os penis) was deformed, showing a deviated fusion line after fracture (Fig. 1b). Radiography (EcoRay E7239X; Toshiba, Tokyo, Japan; <40 kV, 200 mA, 3.6 mAs/msec) of the skull, and of the scapulae, humeri, femurs, tibias, and fibulae, was performed; the skull image revealed many thin and porous areas and the radiographs of the long bones of the limbs revealed well-developed cancellous bone with marrow cavities on their extremities, except near the greater trochanter of the femur. Trabecular bone was present between the epiphysis and the area between the metaphysis and diaphysis. The external contours of the bones were normal. Histologically, the epihyoid bone showed discontinuity of the cortical bone and a fracture space filled with a hematoma and fibrous tissue (Fig. 2a). Many osteoclasts were found in both the periosteum and endosteum. Fibrous tissue, cartilage, and osteoclasts filled the space between the articular surface and the marrow space in the right second carpal bone (Fig. 2b, 2c). The trabecular bone tissue was normal, with osteoblasts but no inflammation.

Fig. 2.

Histological findings of the right epihyoid bone (2a) and right second carpal bone (2b, 2c). Hematoxylin-eosin stain. Fracture sites (arrow) and regions with no cortical bone (arrowheads) are readily seen on the epihyoid bones (2a). (2c) A magnified view of the box in (2b). Many osteoclasts (arrows) were observed in front of the fibrous tissue, which contacted the bone tissue shown in (2c). Scale bars are 500 µm in (2a) and (2b) and 100 µm in (2c).

There were numerous pockmarks on the bone surfaces, indicating bone mass loss and bone fracture. Based on these findings, the otter was diagnosed with osteoporosis. The main causes of osteoporosis in animals are calcium deficiency due to starvation or malnutrition, vitamin D deficiency, decreased estrogen levels after menopause, hypogonadism, and chronic administration of glucocorticoids [2, 5]. Osteoporosis has been reported in humans and domestic animals, including rats, dogs, pigs, and primates [2, 5]. However, there has been no report of osteoporosis in an Asian small-clawed otter. Osteoporosis caused by bone resorption primarily affects the surface of the endosteum; extensive trabecular bone loss occurs first, and cortical bone thinning occurs gradually thereafter. Both of these events are caused by hyperactivity of osteoclasts and decreased activity of osteoblasts [4]. In the male Asian small-clawed otter in this study, extensive external, rather than internal, bone resorption had occurred, including in the articular surface. The endosteum exhibited osteoblasts and trabecular bone appeared in the metaphysis. Therefore, we ruled out several possible causes of osteoporosis, such as malnutrition and decreased estrogen levels.

Fibrous osteodystrophy lesions are very similar in histological terms to the features of this case. Fibrous osteodystrophy develops due to primary and secondary hyperparathyroidism or pseudohyperparathyroidism [2]. This abnormality has several characteristics. Bone resorption, caused by osteoclasts, is extensive, and the resorption sites are filled with fibrous and bony tissue. However, this metabolic disorder does not affect the articular cartilage, growth plates, or secondary ossification centers. In cases of fibrous osteodystrophy, bone resorption begins in the endosteum, not the periosteum, in cortical bone. Occasionally, the fibrous tissue proliferation is so extensive that the external dimensions of the bone are increased, and the bone is flexible or weakened. This process is most commonly seen in the maxilla and mandible [2]. The case reported here is consistent with fibrous osteodystrophy, in that the lesions were extensive and fibrous tissue filled the bone resorption sites. However, there were also features different from those of fibrous osteodystrophy: bone resorption occurred on all external surfaces, including the articular surface, resulting in pockmarks on the outer surfaces of the dried bones, the external contours of the bones, including the maxilla and mandible, appeared normal, and bone size was not increased.

Another bone disease potentially present in our case is renal osteodystrophy. Chronic renal failure can lead to hyperparathyroidism, and osteodystrophy might occur secondarily [2]. To establish the presence of renal osteodystrophy, laboratory data on parathyroid hormone, blood urea nitrogen, creatinine, calcium, and phosphate levels, and histological data on the kidney and parathyroid gland, are required. However, we did not perform these tests because the main goal was to examine the skeleton for anatomical education purposes. The carcass, which was stored in a refrigerator, contained only coagulated blood, which is not suitable for hematological tests. At dissection, we did not observe any abnormalities of the kidneys or endocrine organs, including the thyroid and parathyroid glands; thus, histological observations of these organs were not performed. The symptoms of renal osteodystrophy are similar to those of fibrous osteodystrophy, including lameness, loss of teeth, and deformity of the maxilla and mandible [2], none of which were observed in this case. In addition, bone disorders in an Asian small-clawed otter with renal disease have never been reported previously [8, 9]. Taken together, our gross data and histological observations do not support signs of renal osteodystrophy in this case.

In summary, this report describes osteoporosis in a male Asian small-clawed otter, in which hyperactive bone and cartilage resorption by osteoclasts was seen in various bone sites, and in the joint cartilage, resulting in pockmarks on the surfaces of all bones.