Degenerative Joint Disease in the Skeletal Remains of a Captive Bornean Sun Bear (Helarctos malayanus euryspilus)

Awang Hazmi Awang-Junaidi1, Yeoh Boon Nie2, Siew Te Wong2, Nur Nabila Sarkawi3, Wafeq Mu’izzadin Khairul Anuar1, Siti Mariam Zainal Ariffin1*

1Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia; 2Bornean Sun Bear Conservation Centre (BSBCC), PM 219, Elopura, 90000, Sandakan, Sabah, Malaysia; 3Sabah Wildlife Department, Block B, 5th Floor, Wisma Muis, 88100, Kota Kinabalu, Sabah, Malaysia.

Received | June 10, 2024; Accepted | August 30, 2024; Published | October 10, 2024

*Correspondence | Siti Mariam Zainal Ariffin, Faculty of Veterinary Medicine, Universiti Putra Malaysia, 43400 UPM Serdang, Selangor Darul Ehsan, Malaysia; Email: sitimariam_za@upm.edu.my

Citation | Awang-Junaidi AH, Yeoh BN, Wong ST, Sarkawi NN, Anuar WMK, Ariffin SMZ (2024). Degenerative joint disease in the skeletal remains of a captive bornean sun bear (Helarctos malayanus euryspilus). J. Anim. Health Prod. 12(4): 557-561.

DOI | http://dx.doi.org/10.17582/journal.jahp/2024/12.4.557.561

ISSN (Online) | 2308-2801

Copyright: 2024 by the authors. Licensee ResearchersLinks Ltd, England, UK.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

Introduction

Degenerative joint disease (DJD) is a progressive condition that affects any joint in the body. Based on the involvement of the joint, osteoarthritis (OA) specifically targets synovial joints, whereas spondylosis deformans (SD) refers to the degenerative changes occurring in the vertebral column, including intervertebral discs, vertebral bodies, and surrounding structures. Osteoarthritis is clinically manifested by primary symptoms such as pain, stiffness, and locomotor restrictions. Osteoarthritis results in the progressive loss of articular cartilage structure and function, osteophyte formation, subchondral bone sclerosis, and synovial inflammation (Kim et al., 2018). Spondylosis deformans is characterized by the formation of osteophytes along the edges of vertebral bodies in the spine. Although the exact cause is unknown, individual-level factors such as age, sex, obesity, genetics, and diet are well-documented as predictors of DJD. Likewise, joint-level factors such as injury, overuse, and malalignment may also contribute to the development of DJD (Palazzo et al., 2016). Degenerative joint disease has been reported not only in domestic animals (Anderson et al., 2019; Baccarin et al., 2022) but also in wildlife (Kalogeropoulu et al., 2023).

The Bornean sun bear is the smallest bear species in the world. It is the subspecies of the Malayan sun bear (Helarctos malayanus) and is endemic to the island of Borneo (Wong, 2002; Meijaard, 2004; Kunde, 2017). Habitat loss and activities such as illegal hunting and trading constitute a significant threat to the population of Bornean sun bears (Gomez et al., 2020). Conservation efforts for this small bear species include the establishment of rescue and rehabilitation facilities, such as in the states of Sabah and Sarawak (Malaysia) and Balikpapan province in East Kalimantan, Indonesia. The Bornean Sun Bear Conservation Centre (BSBCC) in Sabah is the world’s only sun bear rehabilitation centre. Degenerative joint disease is reported in Ursidae such as American black bears (Storms et al., 2004), sloth bears (Selvaraj et al., 2017), and brown bears (Witz et al., 2001; Aminkov et al., 2018; Hadziomerovic et al., 2019). An earlier study on palaeopathological examination revealed DJD in the dry skeleton of Malayan sun bears (Greer et al., 1977).

In this article, we report the presence of DJD in the skeletal remains of a captive Bornean sun bear from BSBCC in Sabah, Malaysia. To the best of our knowledge, this is the first documented report of DJD in this subspecies.

Materials and Methods

We examined the skeleton of a male Bornean sun bear named “Gutuk”, who was rescued in the year 2001 from illegal traffickers at an adult age and sent to Sepilok Orangutan Rehabilitation Centre, Sandakan, Sabah, Malaysia. Gutuk became a resident of the BSBCC after the sun bear center was established in 2008. Within the BSBCC, Gutuk was housed in a cemented cage (3m length x 2m width x 3m height). Dietary management consists of a variety of fruits, rice porridge, and cooked vegetables such as pumpkin, sweet potatoes, and mung beans. Health records indicated that the sun bear had partial blindness and chronic skin conditions, including dermatitis, alopecia, and pruritis. Neither locomotion difficulties nor lameness was observed before his death. In 2017, Gutuk experienced an injury and radiological findings revealed a comminuted fracture at the right carpus. Gutuk died a day after the general anaesthesia to assess the fracture condition. The carcass was macerated, and the bones were collected, dried, and kept at room temperature.

The skeletal remains were categorized and organized based on their anatomical regions, distinguishing between the appendicular and axial skeletons. The appendicular bones and vertebrae were examined macroscopically for evidence indicative of OA and SD, respectively. The presence of osteophyte formation, subchondral bone degradation, and joint remodelling was examined and recorded as present and absent for the available appendicular bones and vertebrae (Nganvongpanit et al., 2017). The width of the osteophytes extending from the bone surface was measured at its widest dimension using a ruler. All bones showing lesions were photographed.

Results and Discussion

Osteoarthritis was observed in multiple sites of the joint (i.e., hip joint, elbow joint, stifle joint, and carpal joint) with bilateral involvement. Specifically, OA lesions were identified in various appendicular bones, including the femur, pelvis, humerus, radius, ulna, and carpal bones. The osteophytes were observed as new bone formations around the periphery of the joint, ranging in size from 0.5 to 2.0 cm. Osteophyte formation was identified at the femoral head-neck junction (Figure 1), along the trochlear margin of the distal femur (Figure 1), around the acetabular margin (Figure 2), on the proximal and distal radius and the distal ulna (Figure 3). Evidence of subchondral bone degradation was observed on the entire surface of the left and right acetabulum (Figure 2), femoral head, right medial femoral condyle (Figure 1) and radius. Joint remodelling was identified by assessing changes in the bone shape, and the event was observed in the acetabulum and right femoral head; both of these bones had extensive osteophyte formation (Figures 1 and 2). The right femoral head depicted a flattened shape, compared with the rounded appearance observed in the left femoral head (Figure 1).

Spondylosis deformans lesion characterized by the formation of osteophytes was observed at the edge of the lateral and ventral vertebral body of C6-C7, C7-T1, and T12-T13 (Figure 4). The size of the osteophytes ranged from 0.5 to 1.0 cm. Bone degradation, characterized by erosion and roughened and irregular bone texture, was found on both the cranial and caudal intervertebral surfaces of all the affected vertebrae (Figure 4). Greer et al. (1977) reported DJD in wild mammals’ skeletons, including three Malayan sun bears. They found severe SD affecting the lumbar vertebrae, along with OA present in the carpal joints. Additionally, they described DJD in the sun bears as being characterized by osteophyte formation on the vertebrae, with the fusion of three lumbar vertebrae, and on the long bones, particularly at the distal ends of the ulna.

In this study, the most affected areas of SD in Bornean sun bear were the cervical and thoracic vertebrae with marked osteophyte formations at the edge of the lateral and ventral aspect of the vertebral body. The distribution pattern of osteophytes observed in Bornean sun bears in this study was similar to the pattern observed in both domestic animals and humans (Nganvongpanit et al., 2017).

In companion animals, the presence of SD in the caudal cervical spine may be associated with cervical instability (Walker, 2002). Spine instability can occur at any vertebra along the vertebral column, resulting from trauma, ligament laxity, degenerative changes, and congenital abnormalities. Sun bears, like other bear species, possess high mobility in both their skull and cervical vertebrae (Endo et al., 2001), enabling them to scan their surroundings and track movements while foraging for food, climbing, and swimming. If cervical instability occurs, increased activity in the cervical region of sun bears may trigger the development of spondylosis. Furthermore, in captivity, limited exercise and sub-optimal nutrition could exacerbate spondylosis development and progression (Wagner et al., 2005).

Sun bears are semi-arboreal animals as they spend a significant portion of their time in trees for feeding, resting, and avoiding dangers. The hindlimbs are specialized for this arboreal lifestyle by having strong muscles to push the body off the ground and propel themselves upward while climbing (Sasaki et al., 2005). Additionally, the flexible hindlimb joints allow for a wide range of motion, especially when navigating through the branches and the trunks. Consequently, OA in the hindlimb joints can significantly impair their mobility, overall health, and welfare. In this study, severe OA lesions were observed in the hip joints. The presence of large osteophyte formations at the acetabular margin and the head-neck junction of the femoral head is an attempt to compensate and stabilize the compromised hip joints by increasing the surface area of the degraded acetabular and femoral head cartilage lining. Moreover, it also contributes to enhancing support and joint incongruity, particularly during locomotion and climbing activities. Nevertheless, osteophytes can limit joint movement by encroaching on the joint space and irritating surrounding soft tissue, including ligaments, tendons, and nerves, leading to inflammation, pain, and discomfort. Examination of the skeleton also revealed subchondral bone degradation and joint remodelling, suggesting an advanced stage of joint degeneration. As cartilage deteriorates and exposes the underlying bone, the subchondral bone becomes susceptible to damage and degradation.

In this study, the sun bear experienced a fracture in the carpal region, ultimately leading to the development of secondary OA in the carpal joint. Osteoarthritis is a chronic progressive degenerative disease, and aging is recognized as a significant risk factor for its development in mammalian species (Baccarin et al., 2022). Changes associated with OA typically increase as animals age. At 17 years old at the time of its death, the sun bear may have developed OA at some point during its life, but no reports of chronic lameness were recorded previously. Wildlife can adapt to their environment and cope with injuries and discomfort. They appear to be moving normally or hide signs of lameness, making it difficult to recognize any joint issues (Bourne et al., 2010). As a result, OA may go undetected or be diagnosed at a later stage when clinical signs become more pronounced or when complications arise. The behaviour of bears with DJD often changes due to discomfort and limitation caused by the condition. Bears with DJD are less active, spend more time sleeping and resting, climb less frequently, and are more easily agitated (Bourne et al., 2010). Thus, monitoring the behavioural patterns can assist caretakers, researchers, and wildlife biologists in assessing the health and well-being of the bear population, both in captivity and in the wild.

Assessing lameness in bears involves understanding bear locomotion. Hunter-Ishikawa et al. (2023) developed a reliable Bear Lameness Scale for Asiatic black bears (Ursus thibetanus), and it has been used on other bear species, including the Malayan sun bear. The scale is based on visual observation of the bear’s locomotion during walking, running, and any alteration in the stride. Moreover, the scale can be easily used to monitor both acute and chronic lameness, as bears share similar anatomy and locomotion patterns (Amanat et al., 2020). Frequent visual assessment, physical examination, and regular radiographic evaluation enable early detection and monitoring of disease progression (Bourne et al., 2010).

Conclusions and Recommendations

Our study of DJD in skeletal remains of Bornean sun bears sheds light on the occurrence of this condition in these animals. The study identified characteristic signs of OA and SD, including osteophyte formation and changes in the bone morphology indicative of chronic joint pathology. Understanding the consequences of DJD in sun bears is crucial for their conservation and health management.

Acknowledgments

We thank the Bornean Sun Bear Conservation Centre for providing the funding that made these studies possible. We thank the staff at BSBCC for their kind cooperation.

Novelty Statement

By documenting species-specific patterns of joint degeneration, the study reveals how captivity and increased longevity impact the skeletal health of Bornean sun bear, which offering insights that were previously unexplored. The findings not only contribute to our understanding of the evolutionary and behavioural implications of joint disease in these animals but also have practical implications for improving conservation strategies and developing targeted geriatric care protocols for wildlife in captivity.

Author’s Contribution

STW, YBN, and NNS were involved in retrieving, cleaning, and preserving the skeletal remains. AHAJ, SMZA, and WMKA documented relevant information on each bone specimen and captured detailed photographs of the specimens. Authors AHAJ and SMZA wrote the first draft of the manuscript. Author SMZA edited the last manuscripts. All authors read and approved the final manuscript.

Conflict of interests

The authors have declared no conflict of interest.

References

Amanat S, Mayer J, Paracha H, Ali Z, Granatosky MC (2020). Bear locomotion: 1st edn. pp. 3986-4001. Springer International Publishing, Switzerland. https://doi.org/10.1007/978-3-319-47829-6_1707-1

Aminkov B, Nanev P, Aminkov K (2018). Radiographic findings in joint disease in three brown bears. Trad. Modern. Vet. Med., 3(4): 3-6.

Anderson KL, O’Neill DG, Brodbelt DC, Church DB, Meeson RL, Sargan D, Summer JF, Zulch H, Collins LM (2018). Prevalence, duration and risk factors for appendicular osteoarthritis in a UK dog population under primary veterinary care. Sci. Rep., 8: 5641. https://doi.org/10.1038/s41598-018-23940-z

Baccarin RYA, Seidel SRT, Michelacci YM, Tokawa PKA, Oliveira TM (2022). Osteoarthritis: A common disease that should be avoided in the athletic horse’s life. Anim. Front., 12(3): 25-36. https://doi.org/10.1093/af/vfac026

Bourne DC, Cracknell JM, Bacon HJ (2010). Veterinary issues related to bears (Ursidae). Int. Zoo Yearb., 44(1): 16–32. https://doi.org/10.1111/j.1748-1090.2009.00097.x

Endo H, Sasaki M, Hayashi Y, Koie H, Yamaya Y, Kimura J (2001). Carpal bone movements in gripping action of the giant panda (Ailuropoda melanoleuca). J. Anat., 198(2): 243-246. https://doi.org/10.1046/j.1469-7580.2001.19820243.x

Gomez L, Shepherd CR, Khoo MS (2020). Illegal trade of sun bear parts in the Malaysian states of Sabah and Sarawak. Endang. Species Res., 41: 279–287. https://doi.org/10.3354/esr01028

Greer M, Greer JK, Gillingham J (1977). Osteoarthritis in selected wild mammals. Proc. Oklahoma Acad. Sci., 57: 39-43.

Hadžiomerović N, Avdić R, Kovacevic S, Tandir F, Bejdić P (2019). Spondyloarthropathy in a captive female brown bear (Ursus arctos). J. Adv. VetBio Sci. Tech., 4(3): 130-133. https://doi.org/10.31797/vetbio.571424

Hunter-Ishikawa M, Nakatani JY, Miller DS. (2023). Modification of Domestic Animal Lameness Scales for Use in Asiatic Black Bears (Ursus thibetanus). Animals (Basel)., 13(21):3302. https://doi.org/10.3390/ani13213302.

Kalogeropoulu SK, Rauch-Schmücking H, Lloyd EJ, Stenvinkel P, Shiels PG, Johnson RJ, Fröbert O, Redtenbacher I, Burgener IA (2023). Formerly bile-farmed bears as a model of accelerated ageing. Sci. Rep., 13: 9691. https://doi.org/10.1038/s41598-023-36447-z

Kim JR, Yoo JJ, Kim HA (2018). Therapeutics in osteoarthritis based on an understanding of its molecular pathogenesis. Int. J. Mol. Sci., 19(3): 674. https://doi.org/10.3390/ijms19030674

Kunde MN (2017). Ex-situ and in-situ conservation approach for the Malayan sun bear (Helarctos malayanus). PhD thesis, Griffith University, Los Angelas, USA.

Meijaard E (2004). Craniometric differences among Malayan sun bears (Ursus malayanus); evolutionary and taxonomic implications. Raffles Bull. Zool., 52(2): 665-672.

Nganvongpanit K, Soponteerakul R, Kaewkumpai P, Punyapornwithaya V, Buddhachat K, Nomsiri R, Kaewmong P, Kittiwatanawong K, Chawangwongsanukun R, Angkawanish T, Thitaram C, Mahakkanukrauh P (2017). Osteoarthritis in two marine mammals and 22 land mammals: Learning from skeletal remains. J. Anat., 231(1): 140-155. https://doi.org/10.1111/joa.12620

Palazzo C, Nguyen C, Lefevre-Colau MM, Rannou F, Poiraudeau S (2016). Risk factors and burden of osteoarthritis. Ann. Phys. Rehabil. Med., 59(3): 134-138. https://doi.org/10.1016/j.rehab.2016.01.006

Sasaki M, Endo H, Wiig O, Derocher AE, Tsubota T, Taru H, Yamamoto M, Arishima K, Hayashi Y, Kitamura N, Yamada J (2005). Adaptation of the hindlimbs for climbing in bears. Ann. Anat., 187(2): 153-160. https://doi.org/10.1016/j.aanat.2004.10.001

Selvaraj I, Arun AS, Singh PK, Khadpekar Y (2017). Coxo-femoral osteoarthritis in a rescued dancing sloth bear (Melursus ursinus). Shanlax Int. J. Vet. Sci. Res., 4(4): 1-6.

Storms TN, Beazley SL, Schumacher J, Ramsay EC (2004). Thyroid cystadenoma, colloid goitre, and hypothyroidism in an American black bear (Ursus americanus). J. Zoo Wildl. Med., 35(1): 82-87. https://doi.org/10.1638/03-033

Wagner WM, Hartley M, Duncan N, Barrows M (2005). Spinal spondylosis and acute intervertebral disc prolapse in a European brown bear (Ursus arctos arctos). J. South Afr. Vet. Assoc., 76(2): 120-122. https://doi.org/10.4102/jsava.v76i2.410

Walker MA (2002). The vertebrae canine and feline- 4th edn. W.B. Saunders, USA. pp. 98-109.

Witz M, Lepage, OM, Lambert C, Couillerot D, Fau D, Rachail M, Troncy E (2001). Brown bear (Ursus arctos arctos) femoral head and neck excision. J. Med., 32(4): 494–499.

Wong ST (2002). The ecology of Malayan sun bears (Helarctos malayanus) in the lowland tropical rainforest of Sabah, Malaysian Borneo. Master Thesis, The University of Montana, Missoula, Montana.