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Presumed reactive polyarthritis and granulomatous vasculitis in a Mississippi sandhill crane (Grus canadensis pulla).

Abstract: A 1.5-year-old female Mississippi sandhill crane (Grus canadensis pulla) was presented and managed for a polyarthritis of the intertarsal and tarsophalangeal articulations. Results of aerobic bacterial cultures, Mycoplasma species culture, and polymerase chain reaction testing of articular fluid did not identify any causative organisms. Results of radiographs and cytologic examination of articular fluid were consistent with an inflammatory, nonerosive polyarthritis. The arthritis did not improve with systemic anti-inflammatory and antibiotic treatment and with joint lavage. A large necrotic granulomatous mass was detected on the right shoulder area from which Staphylococcus aureus and Enterococcus species were isolated as opportunistic pathogens. Two days after surgical resection of the mass, the distal polyarthritis resolved. Histopathologic examination of the mass was consistent with granulomatous vasculitis with abscess formation of unknown origin. In this crane, the unresponsiveness to standard therapy, the presence of an infected and inflammatory mass, and the resolution of the polyarthritis after the resection of the mass strongly supported a diagnosis of reactive immune-mediated nonerosive polyarthritis. Analysis of this case suggests that immune-mediated idiopathic arthritis should be a differential diagnosis of distal polyarthritis in cranes and that an inciting source remote from the joints should be investigated in case of lack of response to standard therapy.

Key words: polyarthritis, idiopathic arthritis, reactive arthritis, avian, Mississippi sandhill crane, Grus canadensis pulla

Clinical Report

A 1.5 year-old female Mississippi sandhill crane (Grus canadensis pulla) was presented to the veterinary staff of the Freeport-McMoran Audubon Species Survival Center (New Orleans, LA, USA) because of a swollen right hock and lameness. The crane was housed in an outdoor pen and fed a pelleted crane diet supplemented with monensin at 90 g/ton. The bird was part of a colony of Mississippi sandhill cranes and whooping cranes (Grus americana) used for a conservation and reintroduction program in the southern United States. In this colony, routine prophylaxis included annual physical examination, blood tests, fecal examination, and vaccination for West Nile virus and eastern equine encephalitis virus. Intertarsal joint problems are commonly diagnosed in cranes at this center, and most are traumatic in nature. The medical history of this crane included toe curling and intestinal coccidiosis while a chick.

The crane was hand captured and hooded, and a physical examination was performed on site. The right intertarsal joint was severely enlarged, warm, and edematous. No sign of trauma was noticed, and the other joints of the legs appeared normal. A blood sample was taken from the right jugular vein and submitted for complete blood cell count (CBC) and plasma biochemical profile. The bird was started on meloxicam (0.3 mg/kg PO ql2h; Metacam, Boehringer Ingelheim, St Joseph, MO, USA). Results of the CBC revealed a moderate heterophilic and lymphocytic leucocytosis, with a total white blood cell count (WBC) of 50 x [10.sup.3]/[micro]L (reference interval, 6.2-22.6 x [10.sup.3]/[micro]L), (1) heterophil count of 36 x [10.sup.3]/[micro]L, and lymphocyte count of 13.5 x [10.sup.3]/[micro]L. Results of the plasma biochemical profile were within reference intervals.

Although a mild reduction of the swelling was initially noted, at the 2-week recheck, the contralateral left intertarsal articulation and the right tarsophalangeal articulations also were swollen (Fig 1). After aseptically preparing the right intertarsal area, an arthrocentesis was performed with a 25-gauge needle and a 2.5-mL syringe. A whitish, viscous fluid compatible with synovial fluid was recovered from the joint and was submitted for aerobic bacterial and mycoplasmal cultures. Several slides also were prepared for cytologic examination of the articular fluid. Analysis of the results revealed the presence of mostly heterophils and macrophages in a proteinaceous background, with no organisms observed, which was consistent with a granulocytic and heterophilic exudate. The volume of exudate recovered was too low to be submitted for fluid analysis. Another blood sample was collected from the right jugular vein. At this time, the bird was placed on enrofloxacin (15 mg/kg PO ql2h; Baytril, Bayer Healthcare, Wayne, N J, USA) because of its broad antimicrobial spectrum, oral acceptability by the cranes, and adequate therapeutic levels usually achieved in joint fluid. The meloxicam also was continued. The CBC results showed lower WBC (30 x [10.sup.3] cells/[micro]L) and heterophil counts (24.9 x [10.sup.3] cells/[micro]L). Results of the plasma biochemical profile were normal, and bacterial and mycoplasmal cultures did not isolate any organisms.

The next week, because of the unresponsiveness of the posterior limbs polyarthritis to nonsteroidal anti-inflammatory therapy, further diagnostic tests were planned with the crane under general anesthesia. The bird was premedicated with butorphanol (1 mg/kg IM; Fort Dodge Animal Health, Fort Dodge, IA, USA) and mask induced with 5% isoflurane. The crane was intubated with a 4.5-mm uncuffed endotracheal tube and maintained on 2%-3% isoflurane throughout the procedure. Radiographs of the intertarsal and tarsophalangeal articulations did not reveal any articular erosion or bony changes, which was consistent with a nonerosive inflammatory polyarthritis. Thoracoabdominal radiographs also were unremarkable. Serosanguinous fluid was removed from the intertarsal articulations by arthrocentesis and placed in a blood culture media in an attempt to improve culture sensitivity. (2) A sample of the joint fluid also was submitted for Mycoplasma species polymerase chain reaction (PCR) testing. Two 20-gauge indwelling catheters were placed in each articulation, and joints were lavaged with 1030 mL of warm sterile 0.9% NaC1 solution. Ticarcillin-clavulanate (100 mg/kg; Timentin, GlaxoSmithKline, Philadelphia, PA, USA) also was infused in each joint. These antibiotics were chosen because of a low propensity of local and joint adverse effects. An additional dose of ticarcillin-clavulanate (200 mg/kg) was given intravenously in the left ulnar vein. A transcoelomic cardiac ultrasound examination also was performed and did not show any abnormalities or evidence of vegetative endocarditis, which could have been a potential source for bacterial emboli. The bird then was recovered and released back into its pen later on that day. The oral treatment regimen was left unchanged. The aerobic culture did not grow any bacteria, and results of PCR testing for mycoplasma were negative.

Two days later (3 weeks after the initial presentation), the caretakers reported that feathers appeared misaligned on the right shoulder area. Closer examination and palpation revealed the presence of a 7 x 5-cm ulcerated mass on the dorsocaudal aspect of the right proximal humeral area that seemed to be adherent to underlying structures. A large amount of necrotic tissue and feathers were covering the mass. When considering the size and nature of the mass, it was likely present since the initial presentation. Surprisingly, the mass was not previously noticed despite a complete physical examination with the bird under manual restraint, later repeated with the bird under general anesthesia. The location of the mass, close restraint of the bird with its right side against the handler's body, and the humeral feather tract in the area that covered the mass likely contributed to this omission. Because of the size of the bird, the area also was not present on the radiographic images. Nevertheless, the bird was reanesthetized for further workup of the mass. Radiographs of the mass area did not reveal any bony involvement, and the tarsal joints were still markedly swollen. The mass was asceptically prepared, and punch biopsy samples were collected and submitted for histopathologic examination and bacterial culture. Culture isolated a Staphylococcus aureus and an Enterococcus species, with no significant resistance pattern. Histopathologic findings were consistent with ulcerated granulation tissue. Because we suspected that the arthritis could have developed in reaction to the necrotic and infected mass, complete surgical excision was planned for the next week.

The crane was anesthetized as described previously and given an intramuscular injection of butorphanol (1 mg/kg) for pain management. A blood sample was collected for a WBC. A left brachial plexus block was performed with lidocaine (1 mg/kg). An indwelling 22-gauge catheter was placed into the left ulnar vein, and the bird was infused with isotonic fluids (lactated Ringer's solution) at a rate of 10 mL/kg/h during surgery. Cefazolin (100 mg/kg IV) was administered every 90 minutes for perioperative antibiotic prophylaxis. The core body temperature was maintained by using a heating blanket, and arterial pulse was monitored with a Doppler unit. The right dorsocaudal area over the mass was plucked and surgically prepared. A circumferential incision was made around the mass approximately 2 cm from the margins. During dissection, the mass was found to originate from deep within the muscle belly of the triceps brachii. The mass along with the major part of the triceps brachii down to the mid humeral area were removed by a combination of sharp and blunt dissection (Fig 2). Hemostasis was achieved by using a monopolar electrocautery and hemoclips (Hemoclip, Weck, Teleflex Medical, Research Triangle Park, NC, USA). The surgical site was flushed with 300 mL of warm sterile 0.9% NaC1 solution, and the skin was closed by using 2-0 PDS (Ethicon, Somerville, NJ, USA) in a simple interrupted pattern. A figure-of-eight bandage was applied to the wing, and the bird was recovered. Postoperative analgesia consisted of meloxicam (0.5 mg/kg PO ql2h) and 2 additional doses of butorphanol (1 mg/kg IM q4h). Enrofloxacin was continued at the previous dosage. The CBC results revealed a WBC of 18 x [10.sup.3] cells/[micro]L, which was within reference intervals. The surgical wound healed slowly over several weeks and exhibited mild serosanguineous drainage and dehiscence, possibly caused by electrosurgical debridement and skin tension. At this time, the wound was treated by secondary intention with every-other-day bandage change, cleaning, and topical silver sulfadiazine ointment. The wing was kept wrapped for several weeks because the bird appeared unable to maintain adequate flexion of the elbow. Clindamycin (50 mg/kg PO ql2h) also was added to the bird's treatment regimen for a week because of its good distribution in skin, muscle, and bones, and its excellent spectrum against gram-positive and anaerobic bacteria. The surgical wound was cultured later and did not isolate any aerobic bacterial pathogens. Two days after the mass removal, the polyarthritis resolved.

On histopathologic examination of the mass, extensive abscess formation was associated with large numbers of degenerative macrophages and granulocytes admixed with necrotic cell debris. The deep dermis and panniculus adjacent to the abscessed region had numerous foci of granulomatous inflammation within and around the small arteries and veins. Inflammation in these areas was predominantly histiocytic, with occasional multinucleated cells and fewer lymphocytes. Acid-fast and fungal stains were negative. No coccidial sporozoites or merozoites were observed in the examined sections. Results of the Fite acid-fast, Gram's, and Grocott methenamine silver stains were negative for bacteria and fungi. Transmission electron microscopy was performed on formalinfixed tissue and identified intracytoplasmic particles compatible with rickettsia-like organisms. Paraffin-embedded tissue was submitted for PCR testing for Chlamydophila psittaci and Rickettsia species by using universal primers, the results of which were negative. These findings were consistent with severe granulomatous vasculitis of unknown cause with associated abscess formation.

The bird developed a tracheal stenosis secondary to the intubation approximately 2 weeks after the surgery, which was successfully managed with tracheal resection and anastomosis. Over the next 7 months, no recurrence of the polyarthritis was noticed. In addition, the crane was able to breathe normally but showed some permanent voice changes, with a loss of the vibrato typical of gruidae calls. A definitive cause of the brachial granulomatous vasculitis that led to tissue necrosis, inflammation, and infection was not found. The resolution of the posterior limb polyarthritis 2 days after excision of the infected and necrotic mass strongly supports a reactive nonerosive, immunemediated polyarthritis.

Discussion

This report documents the diagnosis and management of a presumed reactive polyarthritis to a brachial granulomatous mass in a Mississippi sandhill crane. Intertarsal and tarsophalangeal articulations injuries are common in cranes and other long-legged birds such as other members of gruiformes, ciconiiformes, otidiformes, and phenicopteriformes that are kept in a captive environment. (1,3-5) At the International Crane Foundation (Baraboo, WI, USA), the 1-year incidence rate of intertarsal joint trauma was estimated at 4%. (6) These joints have limited soft-tissue protection and are distant from the body and, therefore, are relatively exposed to external trauma. Growing gruidae also are predisposed to leg and joint abnormalities in captivity, in particular, when hand-raised. (3,7) These developmental leg problems may make these birds more susceptible to lameness and joint injuries as adults.

Common causes for arthritis of posterior limb joints in cranes include trauma, infectious causes, arthritis secondary to developmental conditions, degenerative osteoarthritis, tendinitis, gout, pododermatitis, tendon rupture, luxations, and fractures. (1,3,4,6) Similar causes are found in other birds. Common bacterial pathogens known to cause arthritis and polyarthritis in birds are S aureus, Streptococcus species, Escherichia coli, Salmonella species, Pasteurella species, Mycoplasma species, C psittaci, and Mycobacterium species. (8,9) In this crane, no infectious agents could be isolated after multiple cultures by using different transport media. Mycoplasma species has been strongly associated with polyarthritis in black vultures (Coragyps atratus), and large colonies of black vultures are in the vicinity of the Freeport-McMoran Audubon Species Survival Center. (10) Because of that concern, culture and molecular diagnostics for mycoplasma were performed from the joint fluid in this crane, and the results were negative. Other infectious agents that potentially cause arthritis in birds are viruses such as reovirus as a cause of arthritis in chickens, fungi such as Aspergillus species, and parasites such as filarioids. (11-15) However, these agents have not been documented as a cause of arthritis in cranes. A rickettsial organism found in the formalin-fixed tissues raised suspicions, but tissues could not be submitted in electron microscopy fixative, and the organism could not be confirmed by PCR because PCR sensitivity on paraffin-embedded tissues is low. Furthermore, rickettsial infection has not been documented in cranes and is an unlikely cause of primary arthritis in this crane because of the lack of erosive lesions on radiographs.

Immune-mediated polyarthritis is another cause of inflammatory joint disease that can be accompanied by systemic clinical signs and usually is divided into erosive and nonerosive (idiopathic) polyarthritis. (16) In mammals, polyarthritis is further classified into 4 categories. (17) Type I includes idiopathic uncomplicated polyarthritis. Type II is associated with an infectious process and is also known as reactive arthritis. Type III or enteropathic arthritis is linked to gastrointestinal diseases. Finally, type IV is related to a neoplasia and also is qualified as arthritis of malignancy. Type I idiopathic polyarthritis is the most common form of polyarthritis in dogs. (16,17) In addition, nonerosive, immune-mediated arthritis can develop subsequent to vaccination or drug reactions or as part of specific syndromes, for example, systemic lupus erythematosus. (17) The exact cause is unknown, but proposed mechanisms are immune complex disease with immune complex formation in response to an inciting cause (eg, infection) and their subsequent deposition into the synovium and periarticular tissues, or antibody formation against specific infectious agents that cross-react with cartilage components. (16,17) The treatment usually consists of immunosuppressive medications and removal of the inciting cause, if identified. (16) Idiopathic, reactive, and immune-mediated arthritis undoubtedly develop in birds but has not clearly been documented. In poultry, distal immune-mediated polyarthritis can occur spontaneously as part of a systemic sclerodermalike syndrome in the University of CaliforniaDavis-200/206 lines of chickens. (18) In our case, the inflammatory nature of the mass with secondary bacterial infection and the resolution of the arthritis only 2 days after excising the mass, after previous medical treatment, strongly support a diagnosis of presumed immune-mediated polyarthritis that could be consistent with type I or II of the mammalian classification.

The necrotic and inflammatory mass was secondary to a granulomatous vasculitis of unknown cause. Reported causes of granulomatous vasculitis in birds include infections caused mostly by Mycobacterium and Aspergillus species. (19) In cranes, visceral coccidiosis caused by Eimeria gruis and Eimeria reichenowi also can cause granulomatous responses in any part of the body, and sporozoites and merozoites have been seen in vascular tissues and blood. (20) Moreover, coccidial granulomatous nodules are frequently associated with veins, especially in the liver. (20) However, the examined histologic sections of the mass in this crane were negative for acid-fast and fungal organisms. Moreover, no coccidial sporozoites, merozoites, or oocysts were observed in the histologic sections of the mass, no oral granulomas were seen in the bird, fecal parasitologic test results were negative, and this crane colony had no history of visceral coccidiosis. Polymerase chain reaction testing of tissues from the mass for mycobacteria and coccidia were not performed and could have helped to clarify its underlying cause. Nevertheless, regardless of the cause of the mass, the secondary infection and extensive inflammatory reaction were likely responsible for triggering an immune-mediated distal polyarthritis in this crane.

Tracheal stenosis secondary to intubation has been reported in other birds. (21-26) Reported causes of postintubation tracheal stenosis in birds are mechanical or chemical trauma, tube friction, pressure necrosis, local infection, tissue reaction to plastic material, multiple intubations, and the position of the neck during the procedure. (21-26) The underlying reasons for the occurrence of this complication were unknown in this crane because the same intubation procedure had been performed in multiple cranes in the past without inducing tracheal stenosis, and the position of the neck was carefully monitored. The interesting aspect of the management of the tracheal trauma in this crane was the permanent loss of its characteristic call pattern, probably due to laryngeal trauma, trauma to the recurrent nerves (which innervate the tracheal and syringeal muscles but not the larynx in birds), (27) or changes in the tracheal airflow.

This case illustrates that reactive or idiopathic polyarthritis should be considered in the differential diagnosis of posterior limb polyarthritis in cranes. In addition, in cases that exhibit a lack of response to standard therapy, the potential for an inciting source remote from the joints should be investigated.

Acknowledgments: We thank the staff of the Freeport-McMoRan Audubon Species Survival Center, in particular, the persons taking care of the cranes, Amanda Franklin, for her invaluable help managing this case, and Kirk Ryan, DVM, Dipl ACVIM, from the Louisiana State University, School of Veterinary Medicine for his useful comments on the manuscript.

References

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Robert MacLean, DVM, Hugues Beaufrere, DrMedVet, PhD, Dipl ABVP (Avian), Dipl ECZM (Avian), Brittany Heggem-Perry, DVM, Cara Field, DVM, PhD, and Michael Garner, DVM, Dipl ACVP

From the Freeport-McMoran Audubon Species Survival Center--Audubon Nature Institute, 6500 Magazine St, New Orleans, LA 70118, USA (MacLean, Field); the Department of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Skip Bertman Dr, Baton Rouge, LA 70808, USA (Beaufrere, Heggem); and Northwest ZooPath, 654 W Main, Monroe, WA 98272, USA (Garner). Present address (Beaufrere): Ontario Veterinary College, University of Guelph, 50 Stone Rd, Guelph, Ontario N1G 2W1, Canada.
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Author:MacLean, Robert; Beaufrere, Hugues; Heggem-Perry, Brittany; Field, Cara; Garner, Michael
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Dec 1, 2013
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