Signalment:  

African jacana bird (Actophilornis africanus), female 12+ years old, 251 g, wild- caught long-term captiveA keeper found this bird dead near a stream in its exhibit. It had been moved from a nearby exhibit onto the current exhibit approximately 40 days prior. Following the move it had been eating well, and was approaching the keepers and taking food items at each feed-out.

Gross Description:  

At necropsy, this jacana was moderately autolyzed, and had adequate adipose stores and pectoral muscle mass. Multiple enlarged, firm interphalangeal joints were present on both feet. The nail was absent from the right first digit and the distal aspect was swollen to greater than 1 cm in diameter. The dorsolateral lung fields were mottled dark red. Approximately 50 petechial hemorrhages were present in the subepicardium of the heart and subserosal surface of the proventriculus. The spleen was diffusely swollen, soft, and dark pink-gray. Impression smears of the lung, spleen, and intestine yielded mixed inflammatory cells and large numbers of gram-positive rod bacteria which were often within inflammatory cells, particularly histiocytes.

Histopathologic Description:

Kidney: Multifocally throughout the sections glomerular capillaries and small-caliber, thin-walled intertubular vessels are expanded by dense aggregates of tightly packed dark blue bacterial colonies which occasionally completely occlude vessel lumina. In these areas, the bacterial colonies are often observed to be contained within the cytoplasm of large irregular cells with eccentrically displaced nuclei. Medium and occasionally larger caliber veins and smaller arterioles contain moderately increased numbers of large blue-gray histiocytic cells. In some vessels these cells form small aggregates or dense sheets and contain small to large clusters of dark blue rod bacteria similar to those observed in the capillaries. In the most severely affected areas of some sections, occasional individual proximal tubules are lined by dissociated epithelial cells with hypereosinophilic hyalinized to clumped cytoplasm and pyknotic to fragmented nuclei (necrosis). Multifocally collecting ducts are mildly to markedly dilated and contain pale blue granular to fibrillar material admixed with amorphous basophilic debris. Low numbers of lymphocytes, heterophils, plasma cells and histiocytes are scattered throughout the sections. Rarely, random individual tubules are mineralized, and infrequently dark orange-brown granular material is present in the cytoplasm of tubular epithelium. The intracellular bacteria were strongly grampositive with Goodpastures Gram stain.

Other tissues: Large intracytoplasmic aggregates of bacteria similar to those in the kidney were present in phagocytic cells within vessels of most tissues. These were associated with hemorrhage and necrosis in the heart, spleen, and intestine. Histiocytosis was especially prominent in the spleen and was accompanied by a remarkably large number of intracellular bacteria. Multiple fibrinocellular thrombi were also present in the lung. Proliferative and ulcerative pododermatitis (bumblefoot) was confirmed and gram-positive and gram-negative rod bacteria, grampositive coccoid bacteria and superficial fungal hyphae were present in the ulcerated areas. Supplemental digital images include a composite of affected heart in which a vessel contains histiocytes with intracytoplasmic grampositive rod bacterial colonies.

Morphologic Diagnosis:  

1. Kidney: intravascular histiocytosis with intracellular gram-positive rod bacteria

2. Kidney: mild to moderate multifocal acute tubular necrosis, mild multifocal granulocytic and lymphocytic interstitial nephritis, and moderate multifocal collecting duct ectasia with urate accumulation (not present in all sections)

Lab Results:  

Bacterial cultures of postmortem kidney samples preserved at -70 C yielded 3+ growth of Erysipelothrix rhusiopathiae, and 1+ growth each of Escherichia coli and Enterococcus sp.

Condition:  

Erysipelothrix rhusiopathae

Contributor Comment:  

The bacterium Erysipelothrix rhusiopathiae is a cosmopolitan gram-positive, nonspore- forming, facultative anaerobe with numerous serotypes and variable virulence. (1, 8, 9) It has been documented to cause severe disease in a wide variety of animals including domestic and wild birds, mammals ranging from whales to mice, and occasional reptiles. It is also a common commensal on aquatic and marine fishes and invertebrates.

Infection of livestock with E. rhusiopathiaeresults in significant financial losses, particularly in swine and turkey production units. E. rhusiopathiae is considered normal pharyngeal flora in up to 50% of swine and bacteria also cause significant disease, most commonly septicemia, polyarthritis, and endocarditis.(8) The septicemic form in swine often leads to disseminated intravascular coagulation with classic cutaneous manifestations characterized by diamond-shaped pink to purple raised foci commonly referred to as diamond skin disease.(8) It causes a rapidly fatal septicemia in turkeys and other birds with inapparent to generalized petechiation in multiple organs and fibrinopurulent exudate on organ surfaces and joints.(1) In many cases there are limited histologic lesions, with colonies of intravascular bacteria with little or no inflammation as the primary feature.(3,11) While it may cause sporadic disease in a variety of wildlife, it is notable that E. rhusiopathiae has caused multiple significant mass mortality events involving hundreds of wild eared grebes in Nevada and brown pelicans in California, nearly an entire group of released captive raised kakapo in New Zealand, and one of 60 remaining Hawaiian -�-�Alala crows. (3,4,5,10)

Due to the ubiquitous nature of the bacteria, the potential for mass mortality events in birds, and the ability to infect individual birds of high value, E. rhusiopathiae should be considered as a potential cause of sudden death or sepsis in birds in zoological collections. The jacana in this case was wild caught in Tanzania and retained in the collection for approximately 12 years in multiple enclosures, most recently with a long-term mate, and had successfully raised several clutches of chicks. She had a history of proliferative pododermatitis lesions dating back to approximately 1 year after entering the collection. At necropsy the digital articular and skin lesions were chronic and proliferative, but also ulcerated and heavily colonized with opportunistic fungi and mixed bacteria. It hypothesized that infection in this case occurred via the skin wounds. An outbreak of E. rhusiopathiae affecting more than 300 chuckars was attributed to foot trauma caused by relocation from enclosures with solid flooring to wire-bottomed flooring.(2) Exposure to bedding material previously used by swine was the suspected source of the E. rhusiopathiae in the chukars. Disease in the jacana was suspected to have resulted from contamination of plantar skin wounds by bacteria in soil or enclosure bedding, water, mud, or other aquatic source associated with the stream. Bacteriologic surveys for potential sources were not evaluated in this case however, and dietary or other alternative sources including rodents or stray wildlife could not be ruled out.

JPC Diagnosis:  

Kidney: Glomerulitis and nephritis, necrotizing and histiocytic, multifocal, moderate, with numerous intravascular bacterial colonies.

Conference Comment:  

The degree of autolysis present in the sections hampers thorough interpretation of some of the pathologic tubular changes in this interesting case. Erysipelothricosis in birds is often has such an acute course that the animal dies before many appreciable pathologic lesions occur(7).

Erysipelothrix rhusiopathiae adheres to cells by producing neuraminidase, an enzyme that cleaves alpha glycosidic linkages in neuraminic acid, a reactive mucopolysaccharide in cell membranes. Erysipelothrix rhusiopathiae has hemagglutinating activity that can result in complement-dependent hemolysis in severe acute disease. The hemagglutinating activity is believed due to the high neuraminidase activity in virulent strains(6, 10).

Acute to subacute systemic erysipelothricosis causes generalized septicemia and endothelial swelling of capillaries and venules, leading to adherence of monocytes to vascular walls and thus vascular fibrinoid necrosis, fibrin thrombosis, and invasion of vascular endothelium by bacteria. Chronic erysipelothricosis leads to polyarthritis, synovitis, fibrosis and articular cartilage destruction. Vegetative valvular endocarditis frequently occurs, resulting in vasculitis, myocardial infarcts, destruction of valve endocardium, and splenic and renal infarcts(6, 10). Erysipelothrix rhusiopathiae is on a short list of gram positive bacilli important in veterinary medicine; others include Actinomyces spp., which are filamentous, Corynebacterium spp., and Listeria monocytogenes.

References:

1. Bricker JM, Saif YM. Erysipelas. In: Calnek BW, ed. Diseases of poultry. 10th ed. Ames, IA: Iowa State University Press; 1997; 302313.
2. Butcher G, Panigrahy B. An Outbreak of Erysipelas in Chukars. Avian Dis. 1985;29(3):843-845
3. Franson JC, Galbreath EJ, Wiemeyer SN, et al. Erysipelothrix rhusiopathiae Infection in a Captive Bald Eagle (Haliaeetus leucocephalus). J Zoo Wildl Med. 1994;25(3):446-448.
4. Gartrell BD, Alley MR, Mack H, et al. Erysipelas in the critically endangered kakapo (Strigops habroptilus). Avian Pathol. 2005;34(5):383-7.
5.Jensen WI, Cotter SE. An outbreak of erysipelas in eared grebes (Podiceps nigricollis). J Wildl Dis. Oct 1976;12(4):583-586.
6. Maxie MG, Robinson WF: Cardiovascular system. In: Jubb, Kennedy, and Palmer's Pathology of Domestic Animals, ed. Maxie MG, 5th ed., vol. 3, pp. 27-29. Academic Press, San Diego, California, 2007
7. Mazaheri A, Lierz M, Hafez HM: Investigations on the pathogenicity of Erysipelothrix rhusiopathiae in laying hens. Avian Diseases 49(4): 574-576, 2005
8. Qinning Wang Q, Chang B, Riley T. Review: Erysipelothrix rhusiopathiae Vet Micro. 2010;140: 405417.
9. Shibatani M, Suzuki T, Chujo M, Nakamura K. Disseminated intravascular coagulation in chickens inoculated with Erysipelothrix rhusiopathiae. J Comp Pathol. 1997;117(2):147-156.
10. Thompson K: Bones and joints. In: Jubb, Kennedy, and Palmer's Pathology of Domestic Animals, ed. Maxie MG, 5th ed., vol. 1, pp. 163-164. Academic Press, San Diego, California, 2007
11. Work TM, A Donna Ball, B and Mark Wolcott Erysipelas in a Free-ranging Hawaiian Crow (Corvus hawaiiensis) Avian Dis. 1999; 43:338-341.

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3-1. Lung

3.2. Kidney

3.3 Heart

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