Asian Pac J Trop Biomed 2014; 4(Suppl 1): S62-S65 S62

Asian Pacific Journal of Tropical Biomedicine

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Document heading doi:10.12980/APJTB.4.2014C915 2014 by the Asian Pacific Journal of Tropical Biomedicine. All rights reserved. 襃 Fatal hemorrhagic-necrotizing pancreatitis associated with pancreatic and hepatic lipidosis in an obese Asian palm civet (Paradoxurus hermaphroditus) 1 2 2 1 2 Bongiovanni Laura *, Di Girolamo Nicola , Montani Alessandro , Della Salda Leonardo , Selleri Paolo 1Faculty of Veterinary Medicine, University of Teramo, Teramo, Italy 2Clinica per Animali Esotici, Centro Veterinario Specialistico, Via Sandro Giovannini 53, Rome, Italy

PEER REVIEW ABSTRACT

Peer reviewer Paradoxurus hermaphroditus Asian palm civets ( ), or toddy cats, belong to the family Viverridae. Dr. Changbo Ou, Department of Little is known about the pathology of these animals and few articles have been published, Preventive Veterinary Medicine, mainly concerning their important role as wild reservoir hosts for severe infectious diseases of College of Animal Science, Henan domestic animals and human beings. A 4-year-old, female Asian palm civet was found dead Institute of Science and Technology, by the owner. At necropsy, large amount of adipose tissue was found in the subcutis and in the Xinxiang 453000, Henan Province, peritoneal cavity. Most of the pancreas appeared red, translucent. Hepatomegaly, discoloration China. of the liver were evident, with multifocal areas of degeneration, characterized by white nodular E-mail: [email protected] lesions. Histologically, the pancreas showed severe interstitial and perilobular necrosis and Comments extensive haemorrhages, with separation of the interstitium, mild reactive inflammation at the periphery of the pancreatic lobules. Liver showed multifocal foci of vacuolar degeneration, The work sounds like interesting and lipidic accumulation, sometimes associated to hepatocyte necrosis. A diagnosis of acute severe it was basic work for the research. We hemorrhagic-necrotizing pancreatitis (or acute pancreatic necrosis) associated with pancreatic could learn the pathological changes and hepatic lipidosis was made. To the best of our knowledge, this represents the first case about pancreatitis in a palm civet report of acute lethal pancreatitis in an Asian palm civet. Although the exact cause of the disease from the paper. Moreover, the author remains undetermined, a hypothesis of the cause and pathogenesis is discussed, pointing out thought diet and overweight might be dietary indiscretion and consequent overweight as possible important risk factors. the key causes for the disease. The research deserved our attentions. Details on Page S64

KEYWORDS Necrotizing pancreatitis, Civet, Viverridae, Diet

1. Introduction originated from the South and Southeast Asia, but they can be found throughout South-Western Europe, Asia, the East Paradoxurus hermaphroditus Asian palm civets ( ), or Indies, Africa, and Madagascar[1]. toddy cats, belong to the family Viverridae, together with Little is known about the pathology of these animals. other civets, genets and lisangs, for a total of 71 different Most of the published studies refer to the importance species. They are small mammals, nocturnal frugivores, of this animal as wild reservoir of important infectious

C B L F V M A * orresponding author: ongiovann–i aura, aculty of eterinary edicine, rticle history: University of Teramo, piazza Aldo Moro, 45 64100 Teramo, Italy. Received 26 Jan 2014 Tel: 0039 0861266890 Received in revised form 5 Feb, 2nd revised form 10 Feb, 3rd revised form 15 Feb 2014 E-mail: [email protected] Accepted 2 Mar 2014 Available online 5 Apr 2014 Bongiovanni Laura et al./Asian Pac J Trop Biomed 2014; 4(Suppl 1): S62-S65 S63 diseases, such as distemper[2,3], rabies[4-6], severe acute examined using haematoxylin and eosin (H-E) staining respiratory syndrome (SARS coronavirus)[7,8], avian influenza and visualized by light microscope. In order to confirm the H5N1[9], parvovirosis[10]. Interestingly, in a recent paper, presence of lipid within pancreatic acinar cells, samples civets have been identified as an important new reservoir from the formalin fixed pancreas were also taken, washed Bartonella henselae for playing a role as potential sources in tape water for 2 h, and then fixed by immersion in OCT ° of human infection[11]. Compound (EMS 62550-01) for snap-freezing in a -80 C Asian palm civets are frugivorous carnivoras[12,13], using freezer. The obtained frozen samples were then cryostat µ fruits as a major food source, even if they also eat small sectioned, and 7 m-thick sections were stained with Oil mammals and insects[1]. In captivities, overweight and red O (Fluka 75087, cf 25 g), specific for lipids. obesity are common problems because of lack of exercise Histologically, the pancreas showed severe interstitial and difficulty to find an appropriated diet[14]. Indeed, and perilobular necrosis, oedema and extensive the food used for these animals are often adapted from haemorrhages, with separation of the interstitium (Figure commercial diet designed for other species, with the 1C) and mild reactive inflammation at the periphery of the possibility to induce nutritional imbalances. pancreatic lobules, characterized by the presence of few To the best of our knowledge, this is the first case report neutrophils. Necrotic areas were characterized by pale of acute lethal pancreatitis in an Asian palm civet. Even eosinophilic, finely fibrillar or homogeneous material, though, in the present case, the exact cause of the disease admixed with free erythrocytes. Multifocally, small vessels remains unknown, a hypothesis of the pathogenesis is showed fibrinoid necrosis of the vessel wall and were discussed. surrounded by numerous erythrocytes. Multifocal aspects of fat necrosis were also evident in the surrounding adipose tissue. At the periphery of the pancreatic lobules, 2. Case report beside areas of liquefaction, there were features of early modifications of the parenchyma, consisting of small foci of Paradoxurus A 4-year-old, female Asian palm civet ( coagulative necrosis, where acinar cells appear shrunken hermaphroditus ) was found dead by the owner (Figure 1A), and acidophilic. Duct system, endocrine pancreas, which referred the animal as apparently healthy in the centrilobular parenchyma, as well as large vessels and morning of the same day. The animal lived in a closed nerves, were spared. In the spared portions of pancreatic enclosure with a male. The diet consisted mainly in dry cat parenchyma, and within the islets of langerhans, multifocal food, with two times per week raw egg, and rarely chicks, haemorrhages and scattered single or small clusters of mice and rats. round cells, with large clear cytoplasm and central nuclei (lipidic macrophages) were found (Figure 1, right inset). The presence of these cells and lipidic accumulation also within the acinar cells was confirmed by red oil staining on frozen sections (Figure 1, left inset). Multifocal post-mortem

A B C autolysis processes were also evident, due to the fact the Figure 1. A) Pictures of the Asian palm civet found dead; B) Pancreas: animal was found death by the owner, and some time most of the organ appeared red, translucent, with more evident lobulated; C) passed between death and necropsy. Histological features of pancreas. Haematoxylin and eosin: severe interstitial Liver showed multifocal foci of vascular degeneration, and perilobular necrosis and extensive haemorrhages and oedema, with lipidic accumulation, sometimes associated with hepatocyte separation of the interstitium. 4伊. Inset: scattered single or small clusters of round cells, with large clear cytoplasm and central hyperchromatic nuclei necrosis. In the spleen, multifocal foci of extramedullary (lipidic macrophages) found in the pancreatic parenchyma. 40伊. hematopoiesis were evident. The kidney showed multifocal interstitial infiltration of lymphocytes. At necropsy, large amount of adipose tissue was On the basis of the gross and histological features, found in the subcutis and in the peritoneal cavity. Most a diagnosis of acute severe haemorrhagic-necrotizing of the pancreas appeared red, translucent (Figure 1B). pancreatitis (or acute pancreatic necrosis) associated with Hepatomegaly and discoloration of the liver were evident, pancreatic and hepatic lipidosis was made. with multifocal areas of degeneration, characterized by white nodular lesions. All the other organs were grossly 3. Discussion normal. Samples from pancreas, liver, spleen and kidney were taken and routinely fixed in 10% neutral buffered formalin, Unfortunately, the palm civet was found dead, and no µ embedded in paraffin wax, and 5 m-thick sections were haemato-biochemical diagnostic tests were performed, Bongiovanni Laura et al./Asian Pac J Trop Biomed 2014; 4(Suppl 1): S62-S65 S64 in order to define the metabolic profile of the animal a lesion described as a consequence of pancreatitis in cat and identify eventual metabolic dysfunctions (such as and often related to a worse prognosis when associated hyperadrenocorticism, hypothyroidism, hypercalcemia, with concurrent acute pancreatitis[16,23]. Noteworthy, two uraemia) known to increase risk of acute pancreatitis in animals were kept in the same environments, fed with the domestic animals[15]. Abdominal trauma, described as a same food, but only one developed the disease. This would cause of acute necrotizing pancreatitis in cat was ruled let to suppose that other concomitant risk factors and/or a out[16], based on the anamnesis and the necropsy findings specific predisposition could have played a role. Inherited i.e. ( , the lack of haemorrhages or fractured bones). No alterations in genes encoding pancreatitis enzyme or their obstruction was found in the pancreatic duct system, nor inhibitors, as described at the basis of the human hereditary evident signs of ischemic injury from shock, thrombosis, or idiopathic pancreatitis, could have not been ruled out. embolism or vasculitis, as possible primary underlying A condition characterized by homozygosis for a mutation causes[15]. in the lipoprotein lipase gene and hyperlipoproteinemia Actually, very little is known about the pathology of palm has been recently described in young mink, representing civets and viverrids. A more wide veterinary and human a valid model for the study of the corresponding human literature was then considered to discuss the possible hyperlipoproteinemia type I[17,24]. causes underlying the observed pathological features, Although the definitive cause of the pancreatitis remains also considering that inflammatory lesions of the exocrine undetermined, dietary indiscretion (high-fat, high- pancreas are not as common in domestic animals as in energy) and consequent overweight are considered possible humans[17]. Although pancreatitis has occasionally been important risk factors in determining the disease outcome, reported in a number of animal species (most dogs and cats), raising concerns on how these animals are kept in captivity. information on causal factors is sparse and incompletely understood[15]. Conflict of interest statement Some considerations were made about diet and the nutritional status of the animal, which showed abundant adipose tissue in the subcutis and in the peritoneal We declare that we have no conflict of interest. cavity. Obesity has been considered a predisposing factor Acknowledgements for acute pancreatitis in both human and animals[15,18], often associated with pancreatic steatosis and a worse prognosis[19,20]. Recent studies in human medicine The authors would like to thank Marina Baffoni for the demonstrated that obesity can act creating an environment technical support. that favours the induction and the progression of pancreatic disease by a promotion of inflammation and inhibition Comments or deregulation of autophagy[20]. Despite the relative frequency of acute pancreatitis in human beings, the Background precise underlying mechanisms are unknown. Experiments on animal models were indispensable in providing insight Asian palm civet is an important animal as wild reservoir in pathophysiology and treatment of acute pancreatitis[21]. of many infectious diseases such as rabies, severe acute In this respect, particular attention should be paid to the respiratory syndrome, avian influenza virus, parvovirosis diseases of these animals, since palm civet would represent and so on. However, there was little knowledge about a potential suitable model for the study of some important histological and pathological changes of pancreatitis about human conditions, such as diet-induced pancreatitis. it. In viverrids in captivity, overweight and obesity are Research frontiers common problems because of lack of exercise and dietary errors[14]. Indeed, the diets used for these animals are not This paper is the first case report on acute lethal specific, often adapted from commercial diet designed for pancreatitis in an Asian palm civet and the author other species. In the present case, the civet was kept in described its necropsy and histological changes in detail. a closed enclosure and mainly fed with dry cat food, with Meanwhile, it pointed out that dietary indiscretion and two times per week raw egg, and rarely chicks, mice and overweight might be the important risk factors. rats. Considering their natural habits[1,13,22], the diet of Related reports Asian palm civets should include a major percentage of fruits. Furthermore, hepatic lipidosis was also observed, Asian palm civets normally live in primary forests, parks Bongiovanni Laura et al./Asian Pac J Trop Biomed 2014; 4(Suppl 1): S62-S65 S65 and suburban gardens with mature fruit trees. Takashi 1729-1732. et al. Matsumoto (2011) reported that a novel sylvatic rabies [10] C hen XY, Xie ZJ, Zhao ZP, Jiang SJ, Zhao HK, Zhu YL, et al. virus variant was detected in a golden palm civet in Sri Genetic diversity of parvovirus isolates from dogs and wild J Wildl Dis 47 Lanka and the virus diverged from canine rabies viruses. animals in China. 2011; (4): 1036-1039. [11] S ato S, Kabeya H, Shigematsu Y, Sentsui H, Une Y, Minami M, Innovations and breakthroughs et al. Small Indian mongooses and masked palm civets serve Bartonella henselae This is the first case report of acute lethal pancreatitis as new reservoirs of and potential sources Clin Microbiol Infect 19 in an Asian palm civet and it could teach us to know some of infection for humans. 2013; (12): 1181- pathological knowledge on the civet. 1187. [12] G rassman LI. Movements and fruit selection of two Paradoxurinae Applications Small species in a dry evergreen forest in southern Thailand. Carnivore Conserv 19 – From the paper, we could know something about lethal 1998; : 25 29. pancreatitis in a palm civet and it facilitated the diagnosis [13] N akabayashi M, Bernard H, Nakashima Y. An observation of Paradoxurus hermaphroditus in the near future. several common palm civets at Endospermum diadenum a fruting tree of in Tabin Wildlife Peer review Reserve, Sabah, Malaysia: comparing feeding patterns of Small Carnivore Conserv 47 The work sounds like interesting and it was basic work for frugivorous carnivorans. 2012; : 42-45. The the research. We could learn the pathological changes about [14] W emmer C. Civets and genets. In: Macdonald DW, editor. encyclopaedia of mammals pancreatitis in a palm civet from the paper. Moreover, the . Oxford, UK: Oxford University Press; author thought diet and overweight might be the key causes 1984, p. 136-143. Jubb, Kennedy for the disease. The research deserved our attentions. [15] C harles JA. Pancreas. 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