Pathology in Practice

Shangzhe Xie Willowbrook Wildlife Center, 525 S Park Blvd, Glen Ellyn, IL 60137.

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 BSc, BVMS, MVS
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Jennifer Nevis Willowbrook Wildlife Center, 525 S Park Blvd, Glen Ellyn, IL 60137.

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 DVM
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Stephane Lezmi Department of Pathobiology, College of Veterinary Medicine, University of Illinois, Urbana, IL 61802.

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 DVM, PhD

History

An adult great horned owl (Bubo virginianus) of undetermined age and sex was brought to Willowbrook Wildlife Center after being found sitting at the side of a road.

Clinical and Gross Findings

On physical examination, the owl had poor body condition with mild cracks and dried blood on its beak as well as fluid buildup around the right elbow joint. The bird weighed 1.56 kg (3.43 lb). Radiography revealed multiple mineralized foci bilaterally in the scapulohumeral and stifle joints. Analysis of a sample of synovial fluid collected from the right elbow joint and left scapulohumeral joint also revealed mild mononuclear inflammation with a high number of activated macrophages as well as crystalline mineralization. Blood samples were also collected for a CBC and serum biochemical analysis, which revealed monocytosis, lymphocytopenia, high aspartate aminotransferase activity, low total protein concentration, and hyperuricemia acidemia.

After treatment with meloxicam (0.2 mg/kg [0.09 mg/lb], PO, q 24 h) for 1 week, the owl was very active, eating well, and gaining weight. It was moved to a larger enclosure for the next week. However, the owl had no flight ability and poor perching ability in the larger enclosure, despite continued oral treatment with meloxicam at the same dosage. The decision was made to surgically explore the stifle joints in an attempt to remove any free-floating material within the synovia and thereby improve the bird's mobility in a large cage setting. The owl was anesthetized with isoflurane, and bilateral arthrotomies were performed on the stifle joints. Multiple free-floating small round, smooth, white pieces of material (2 to 4 mm in diameter) were removed from the synovial space. Postoperative radiographic findings confirmed that the previously observed mineralized foci within the stifle joints were no longer present. To avoid prolonged duration of anesthesia, the scapulohumeral joints were not explored during this surgery. Following recovery from anesthesia, the owl was administered an injectable long-acting ceftiofura (10 mg/kg [4.5 mg/lb], IM, q 72 h) for 2 weeks and continued to receive oral treatment with meloxicam at the presurgical dosage.

Over a 2-week period after surgery, leg function improved considerably as evidenced by the owl's adequate perching ability. Flight ability remained severely limited, so a decision was made to surgically explore both scapulohumeral joints. However, during this second surgery, removal of the material within the synovia proved to be impossible because, in the scapulohumeral joints, the material was tightly adhered to other apparently normal tissues. Without flight, this bird could not be returned to the wild and the severe chronic pain associated with this condition negated the option of life in captivity; during anesthesia, the owl was euthanized by IV injection of pentobarbital sodium solution.

Postmortem exploration of the scapulohumeral joints revealed pieces of mineralized nodules closely adhered to connective tissues of the joints and invading the synovial space (Figure 1). The synovial surfaces appeared slightly roughened with some evidence of mild degenerative joint disease. The synovial fluid was not abnormal in color or viscosity and was present in apparently normal volumes within the synovial spaces. The mineralized nodules and portions of surrounding tissue were removed and submitted for histologic evaluation.

Figure 1—
Figure 1—

Photograph of the left scapulohumeral joint of an adult great horned owl (Bubo virginianus) of undetermined age and sex that was found sitting at the side of a road. Notice the large mineralized nodules (2 to 4 cm in diameter) closely adhered to connective tissues of the joint.

Citation: Journal of the American Veterinary Medical Association 245, 7; 10.2460/javma.245.7.767

Histopathologic Findings

At necropsy, the samples of mineralized nodules and portions of surrounding tissue were fixed in neutral-buffered 10% formalin, routinely processed after decalcification (immersion for 3 days in a bone decalcification solutiona), paraffin embedded, sectioned at 5 μm, and stained with H&E stain.

The periarticular connective tissue contained multilobular, irregular (maximum dimension, ≤ 1 cm) foci of deeply eosinophilic mature bone deposits (osseous metaplasia; Figure 2), which were associated with randomly distributed, mature, pale, fibrous, and hyaline cartilage deposits (chondroid metaplasia); chondrocytes were well differentiated. Within foci of osseous metaplasia, development of bone marrow was evident with areas containing mature adipocytes admixed with foci of mononuclear cells with frequent immature and mature heterophils (granulopoiesis). Numerous osteoblasts lined bone deposits and multinucleated osteoclasts were frequently observed, suggestive of an active bone remodeling process. Synovial membranes were variably thickened, forming papillary projections (synovial hyperplasia), and were infiltrated by numerous heterophils. These foci of bone and chondroid metaplasia were surrounded by a dense connective tissue (fibrosis) that extended to the margins of the tissue samples; at the periphery, a few striated muscle fibers were atrophied, necrotic, and embedded within a dense collagen stroma (interstitial fibrosis).

Figure 2—
Figure 2—

Photographs of sections of the periarticular connective tissue from the scapulohumeral joint of the owl in Figure 1. A—Notice the multifocal irregular foci of mature bone deposit (osseous metaplasia). H&E stain; bar = 1 mm. B—Multifocal irregular foci of mature bone deposit (osseous metaplasia) are admixed with mature cartilaginous material (chondroid metaplasia [arrows]). Within these foci are aggregates of mature and immature heterophils (blue star). H&E stain; bar = 500 μm. Inset—Higher magnification view of the aggregates of mature and immature heterophils. H&E stain; bar = 10 μm. C—Multifocal irregular foci of mature bone deposits are visible. Numerous osteoblasts line the bone deposits and multinucleated large osteoclasts are frequently observed, suggestive of an active bone remodeling process. H&E stain; bar = 50 μm. D—Synovial membranes are variably thickened (synovial hyperplasia) with infiltration of numerous heterophils. H&E stain; bar = 200 μm. In panels A through C, osseous metaplasia (yellow stars) is indicated.

Citation: Journal of the American Veterinary Medical Association 245, 7; 10.2460/javma.245.7.767

In the synovial membranes, a focal, dense extracellular eosinophilic material was observed that did not stain or appear birefringent (when viewed microscopically with polarized light) with Congo red stain, ruling out the presence of amyloid. Within the synovial membranes and in the neighboring connective tissue, few dark blue bacillus-like structures were observed with Giemsa stain, suggesting the presence of bacteria.

Morphologic Diagnosis and Case Summary

Morphologic diagnosis and case summary: chondro-osseous metaplasia consistent with synovial chondromatosis in a great horned owl.

Comments

For the bird of the present report, differential diagnoses initially included chronic arthritis, articular gout, and chondromatosis. Chondromatosis has been described in several species of domestic animals. It usually develops in older horses and dogs with osteoarthritis1 but has also been identified in great horned owls2,3 and a red-tailed hawk (Buteo jamaicensis).3 It has been suggested that chronic irritation may be the cause of the cartilaginous metaplasia.1 In raptors, the lesions are typically bilateral and are most frequently found in the scapulohumeral joints, followed by the sternocoracoid and femoroacetabular joints.3 All 14 great horned owls described in the previous reports2,3 had bilateral chondromatosis in the scapulohumeral joints; one also had bilateral chondromatosis in the stifle joints (as in the case described in the present report), and another had chondromatosis in only 1 stifle joint.3 The treatment of choice for chondromatosis in humans is removal of the excess cartilage in the joint and resection of the affected synovium2; such procedures were not possible in the owl of this report.

The actual etiopathogenesis of chondromatosis in avian species is unknown, and further research is warranted. In the case described in the present report, there was evidence of mild joint changes associated with degenerative joint disease; chronic inflammation of the joints may have resulted in the subsequent development of chondromatosis. The presence of bone marrow with granulopoiesis (heterophil production) may suggest that an infectious process was the main cause of chondromatosis in this owl. Indeed, the inflammatory reaction observed on the synovial membranes suggested that an infectious process was ongoing. On the other hand, bone marrow formation can be seen in areas of dural ossification in dogs and ossifying atherosclerotic lesions in other species without any relationship to an infectious process. In the owl of the present report, few bacillus-like organisms were observed in Giemsastained sections of the scapulohumeral synovial membranes and in the neighboring connective tissue. This finding differed from that for most of the great horned owls with chondromatosis described previously3 and could possibly indicate that bacterial arthritis was present in addition to chondromatosis in this case. However, bacterial culture results would be required before a diagnosis of bacterial arthritis could be made.

For the case described in the present report, an alternative hypothesis for the presence of these foci of metaplasia would be that they were derived from fragments of cartilage eroded from a damaged articular surface (so-called articular mice) as part of a preexisting joint disease.4 Such fragments might be capable of surviving and growing in the synovial fluid, which provides a nutritious culture medium. Some could attach and become embedded in the synovial membrane, where survival and proliferation of chondrocytes within fragments would also be expected as suggested for humans with chondromatosis.4

Through our communication with colleagues who have dealt with similar cases in the past, the most common outcome for raptors with chondromatosis appears to be euthanasia. However, this high euthanasia rate could perhaps be reduced if early detection became possible. It is our opinion that, with early detection, surgical removal of the excess cartilage would be easier and more likely to temporarily relieve signs of pain for raptors affected by the disease. Furthermore, bacterial cultures of synovial fluid or tissue samples from affected joints should be performed as part of the diagnostic assessment if possible to determine whether bacterial arthritis is part of the disease process.

a.

IHC-Tek Bone Decal Solution, IW-1900, IHC World LLC, Woodstock, Md.

References

  • 1. Pool RR. Tumors and tumor-like lesions of joints and adjacent soft tissues. In: Moulton JE, ed. Tumors in domestic animals. 3rd ed. Berkeley, Calif: University of California Press, 1990; 102156.

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  • 2. Howard MO, Nieves MA, Miles KG. Synovial chondromatosis in a great horned owl (Bubo virginianus). J Wildl Dis 1996; 32: 370372.

  • 3. Stone EG, Walser MM, Redig PT, et al. Synovial chondromatosis in raptors. J Wildl Dis 1999; 35: 137140.

  • 4. Bones and joints. In: Jubb, Kennedy & Palmer's pathology of domestic animals. 5th ed. St Louis: Elsevier Health Sciences, 2007; 134135.

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  • Figure 1—

    Photograph of the left scapulohumeral joint of an adult great horned owl (Bubo virginianus) of undetermined age and sex that was found sitting at the side of a road. Notice the large mineralized nodules (2 to 4 cm in diameter) closely adhered to connective tissues of the joint.

  • Figure 2—

    Photographs of sections of the periarticular connective tissue from the scapulohumeral joint of the owl in Figure 1. A—Notice the multifocal irregular foci of mature bone deposit (osseous metaplasia). H&E stain; bar = 1 mm. B—Multifocal irregular foci of mature bone deposit (osseous metaplasia) are admixed with mature cartilaginous material (chondroid metaplasia [arrows]). Within these foci are aggregates of mature and immature heterophils (blue star). H&E stain; bar = 500 μm. Inset—Higher magnification view of the aggregates of mature and immature heterophils. H&E stain; bar = 10 μm. C—Multifocal irregular foci of mature bone deposits are visible. Numerous osteoblasts line the bone deposits and multinucleated large osteoclasts are frequently observed, suggestive of an active bone remodeling process. H&E stain; bar = 50 μm. D—Synovial membranes are variably thickened (synovial hyperplasia) with infiltration of numerous heterophils. H&E stain; bar = 200 μm. In panels A through C, osseous metaplasia (yellow stars) is indicated.

  • 1. Pool RR. Tumors and tumor-like lesions of joints and adjacent soft tissues. In: Moulton JE, ed. Tumors in domestic animals. 3rd ed. Berkeley, Calif: University of California Press, 1990; 102156.

    • Search Google Scholar
    • Export Citation
  • 2. Howard MO, Nieves MA, Miles KG. Synovial chondromatosis in a great horned owl (Bubo virginianus). J Wildl Dis 1996; 32: 370372.

  • 3. Stone EG, Walser MM, Redig PT, et al. Synovial chondromatosis in raptors. J Wildl Dis 1999; 35: 137140.

  • 4. Bones and joints. In: Jubb, Kennedy & Palmer's pathology of domestic animals. 5th ed. St Louis: Elsevier Health Sciences, 2007; 134135.

    • Search Google Scholar
    • Export Citation

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