Herpetology Notes, volume 13: 449-450 (2020) (published online on 30 May 2020)

Suppurative pericarditis in Veiled ( calyptratus, Duméril & Duméril 1851) by Klebsiella oxytoca

Andreia Garcês1,*, Vanessa Soeiro2, Sara Lóio2, Filipe Silva3,4, and Isabel Pires3,4

Reports regarding cardiac diseases in are scarce colouration, and consolidated areas, while the liver was (Rishniw, 2008). Its nonspecific symptomatology, such enlarged with a pallid colour. Both kidneys were pallid as generalised weakness, exercise intolerance, anorexia, and contained a white powdery needle-like crystalline changes in colour of the skin or sudden death make it substance compatible with urate crystals (visceral difficult to premature diagnose (Mader, 2006). A large gout). A suppurative pericardial exudate with a yellow variety of bacterial pathogens have been associated colour (0.4 ml) was noted (Fig. 1A). Tissue specimens with cardiovascular diseases in reptiles Chlamydia were collected and fixed in 10% neutral buffered spp., Escherichia coli, Salmonella Arizona and Vibrio formaldehyde for histologic examination. Tissues were damsel, are some examples (Mader, 2006). processed using the standard methods (Mescher, 2013) In October 2015, an adult male Veiled Chameleon and stained with haematoxylin and eosin. Microscopic (Chamaeleo calyptratus, Duméril & Duméril 1851) examination revealed an infiltration with leukocytes, from the Parque Biologico de Gaia (Portugal), exhibited mostly neutrophils, with septic foci and emboli, in poor body condition and, motor disability. Moreover, pericardium, and adjacent myocardium (Fig. 1B). Other and when inspected by palpation, bones appeared microscopic findings include the presence of bacteria in soft, while manipulated articulations looked rigid and the lungs, hepatic lipidosis and kidney visceral gout. painful. Fluids (5 mL NaCl and Ringer Lactate, IP, b.i.d), The purulent exudate was collected and subjected to Carprofen, 1-4 mg/kg IM and calcium supplementation microbiological examination for the identification of of the diet were prescribed. However, despite treatment the etiological agent. The sample was plated onto solid the eventually died one week later. culture media (Blood BHI agar, Columbia CAN + 5% Post-mortem examination revealed that, the animal sheep blood MacConkey Agar) and incubated for 48 h presented dehydration, poor body conditions, pallid at 35-37 °C. Dome-shaped glistening white colonies mucosa’s, tail ulceration, missing nails on the five (2-3 mm in diameter) were observed on the Blood BHI fingers of the left forward limb and pododermatitis on the agar, while convex shaped pink mucoid colonies (1- right limb. When palpated, the bones were soft and the 2 mm in diameter) appeared on the McConkey Agar. articulations rigid, with oedema. An internal examination Gram-negative, encapsulated, non-motile and non- evidenced that, the lungs displayed a heterogeneous sporing bacilli were observed in the Gram staining from both media. The determination of the was made using the isolated colonies by VITEK® system (2 GN ID Car REF 21341, Biomérieux, France): the agent identified was Klebsiella oxytoca. In this study case, the animal presented a suppurated 1 Inno – Serviços Especializados em Veterinária, Rua Cândido pericarditis. However, due to the unspecific clinical de Sousa 15, 4710-300, Braga, Portugal. signs, pericarditis was only identified during the post- 2 Wildlife Rehabilitation Centre of Parque Biológico de Gaia, mortem exam. Purulent pericarditis can be originated Rua da Cunha, 152, Avintes, Portugal. by pyogenic bacteria or due to opportunistic infectious 3 Veterinary Science Department, University of Trás-os-Montes agents in cases of a previous fibrinous pericarditis and Alto Douro, Quinta dos Prados, 5000-801, Vila Real, (Maxie, 2015). K. oxytoca is a ubiquitous and Portugal. 4 CECAV- University of Trás-os-Montes and Alto Douro, Quinta opportunistic agent attacking the immune system of its dos Prados, 5000-801, Vila Real, Portugal. host especially when this is compromised or a primary * Corresponding author. E-mail: [email protected] infection occurs (Podschun and Ullmann, 1998). These 450 Andreia Garcês et al.

Figure 1. A- suppurative pericarditis with a yellow purulent exudate (indicated by the arrow) in a C. calyptratus individual; B- a microscopic image of the heart where it is possible to observe the pericarditis and myocardial calcification (H&E) in the same individual.

bacteria may be found in the water, soil, plants fluids, and INNO laboratory for the support in the execution of this animal mucosal membranes, and also as part of the oral work. and digestive flora of reptiles (Miller, 1998). In the case presented here, Klebsiella oxytoca probably occurred as References an opportunistic agent, secondary to a previous disease Jackson, K.A. (2016): Prevalence of Klebsiella oxytoca in Anolis like fibrinous pericarditis. This bacterium could have carolensis of Louisiana. Vector Borne Zoonotic Disease 16: been already be present in the chameleon’s body as a 800–801. commensal or been conveyed from the other chameleon Jacobson, E.R. (2007): Infectious diseases and pathology of that lived with him or by one of the zookeepers reptiles: color atlas and text. First edition. California, USA, Taylor & Francis. responsible for the cleaning of their habitat. Mader, D. (2006): Medicine and Surgery. Second edition. Septicaemia due to Klebsiella oxytoca has only been Missour, USA, Saunders. described in crocodiles (Jacobson, 2007), while in Maxie, M.G. (2015): Jubb, Kennedy, and Palmer’s pathology of mammals - humans included - this agent, which may domestic volume 3. Sixth edition. Missouri, USA, also occur as a commensal, may be responsible for a Saunders Ltd. variety of pathologies including nosocomial infections Mescher, A.L. (2013): Junqueira’s basic histology : text and atlas. Thirteenth edition. USA, McGraw-Hill Education. that may lead to hospital outbreaks (Jackson, 2016). Miller, H.A. (1998): Urinary Diseases of Reptiles : Pathophysiology To the author´s knowledge, this is the first ever reported and Diagnosis. Seminares in Avian and Exotic Pet Medicine 7: case of suppurative pericarditis by K. oxytoca not only in 93–103. Chamaeleo calyptratus, but also in the group of Podschun, R., Ullmann, U. (1998): Klebsiella spp. as Nosocomial (Order ). This record is key to improve our Pathogens: Epidemiology, , Typing Methods, and current understanding of pathogens and cardiac disease Pathogenicity Factors. Clinical Microbiology Review 11: 589– 603. in reptiles. Importantly, this case not only outlines the Rishniw, M. (2008) Reptile cardiology. 33rd Annual World Small role played by reptiles as reservoirs of zoonotic agents Animal Veterinary Assocation, Dublin, Ireland: WSAVA. but also the importance of zoological collections in the advancement of wild animal infectious diseases. Accepted by Saeed Hosseinian Yousefkhani Acknowledgements. We are grateful to Parque Biológico de Gaia, Laboratory of Histology and Anatomic Pathology of UTAD