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First Case of Echinococcus Multilocularis Infection in a Zoo-Housed

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First Case of Echinococcus Multilocularis Infection in a Zoo-Housed Advance Publication The Journal of Veterinary Medical Science Accepted Date: 7 Dec 2012 J-STAGE Advance Published Date: 21 Dec 2012 1 Category: Pathology 2 Note 3 4 First case of Echinococcus multilocularis infection in a zoo-housed 5 flying squirrel (Pteromys volans orii) 6 7 Eri Oikawa1), Ryoji Shimura2), Maki Nishimura3), Hidefumi Furuoka1) 8 9 1)Division of Pathobiological Science, Department of Basic 10 Veterinary Medicine and 3)National Research Center for Protozoan 11 Diseases, Obihiro University of Agriculture and Veterinary Medicine, 12 Obihiro 080-8555; 2)Kushiro City Zoo, Kushiro 085-0201, Japan 13 14 15 Correspondence to: Hidefumi Furuoka 16 Division of Pathobiological Science, Department of Basic Veterinary 17 Medicine, Obihiro University of Agriculture and Veterinary Medicine, 18 Obihiro 080-8555 19 E-mail: [email protected], 20 Phone: 0155-49-5360, 21 Fax: 0155-49-5359 22 23 24 25 26 Running head: ECHINOCOCCOSIS IN A FLYING SQUIRREL 27 ABSTRACT. A thirty-three month-old male flying squirrel kept in a 28 zoo developed progressive dyspnea and died. Macroscopically, the 29 liver and lung were enlarged with numerous nodular vesicles. 30 Histologically, these organs were replaced by numerous collapsed 31 vesicles demarcated by fibrous tissues. The cysts lined by a 32 cellular, germinal layer contained numerous brood capsules with 33 abundant production of well-developed protoscolices. Protoscolices 34 were about 80-100 μ m in diameter, and had hooks being visible as 35 refractive structures. This zoo locates in the east of Hokkaido 36 where is an endemic area of Echinococcus multilocularis infection. 37 From epidemiology and pathological findings, this animal was 38 diagnosed as E.multilocularis infection. This report describes the 39 pathology of the first case of E. multilocularis infection in a flying 40 squirrel. 41 42 Key words; Echinococcus multilocularis, flying squirrel, Hokkaido, 43 new host record, pathology 2 44 Echinococcosis, also known as hydatid disease, is one of the most 45 important zoonotic diseases, causing human morbidity and mortality 46 worldwide [3]. Generally, six species of Echinococcus are 47 recognized, and four of them are of public health concern: 48 Echinococcus granulosus, E. multilocularis, E. vogeli, and E. 49 oligarthrus [6, 9-11]. E.granulosus is characterized by the 50 presence of unilocular cysts. In contrast, E.multilocularis which 51 causes alveolar echinococcosis, and E.vogeli, and E.oligarthrus are 52 associated with the multicystic lesion. While E.vogeli and 53 E.oligarthrus are restricted to South and Central America [5], the 54 geographical distribution of E.granulosus is worldwide, and that of 55 E. multilocularis is wide in the northern hemisphere such as central 56 Europe, Russia, central Asia, China, Alaska and Canada [9-11]. The 57 life cycle of E. granulosus involves dogs and other canids as 58 definitive hosts, and domestic and wild ungulates as intermediate 59 hosts. Meanwhile E. multilocularis exploits predator-prey 60 relationships between canids and rodents [2]. In Hokkaido, an 61 endemic area of E. multilocularis in Japan, the Ezo red fox (Vulpes 62 vulpes chrenchki) and red-backed vole (Myodes rufocanus bedfordiae) 63 mainly maintain its life cycle [7]. In foreign countries, the common 64 vole (Microtus arvalis), the water vole (Arvicola terrestris) and 65 the muskrat (Ondatra zibethicus) are important intermediate host for 66 this species [2]. In addition to voles, grounds squirrels (Citellus 67 daurious, C. erythrogenys, C. ungugalatus and C. alashanicus), red 68 squirrel (Sciurus vulgaris), bobak marmot (Marmota bobak) and 69 Prevost’s squirrel belonging to the suborder Sciuromorpha have been 3 70 reported rarely as the intermediated host [2, 12, 13]. This paper 71 describes the first case of Ezo flying squirrel (Pteromys volans orii) 72 affected with larval E. multilocularis. 73 A thirty-three month-old male Ezo flying squirrel, which was born 74 and kept in the lair at a logged timber soon after birth to one 75 month-old, and then housed in a metal cage enclosure with an outdoor 76 area in Kushiro City Zoo. The animal developed progressive dyspnea 77 and died on three days after the onset of dyspnea, then dissected 78 by a zoo veterinarian. Main organs including liver, spleen, kidney, 79 heart, lung, colon and testes were fixed in 15% formalin and submitted 80 to our laboratory. Samples were embedded in paraffin wax, and 81 sections (4 μ m) were stained with hematoxylin and eosin (HE) or 82 periodic acid-Schiff (PAS). At necropsy, the thoracic cavity was 83 filled with enlarged lung containing vesicular cysts. One third of 84 the liver was replaced by a mass sized head of the thumb consisting 85 of conglomerate cysts (Fig.1). These cysts showed multilocular 86 vesiculation containing white to yellow gruel-like fluid. 87 Histologically, the liver and lung were replaced by numerous 88 collapsed vesicles demarcated by fibrous tissues (Fig. 2). These 89 fibrous tissues in both organs were not so broad, and thinned 90 especially at the periphery of the vesicles projecting to the 91 parenchyma. In the liver, fibrosis was associated with bile-duct 92 proliferation. The outermost of the vesicles was a homogeneous 93 layer in HE-stained sections, and stained strongly with PAS. This 94 structure showed often fragmentation and convolution. The inner 95 cavity of the vesicles lined by a cellular, germinal layer was 4 96 composed of plural brood capsules containing numerous protoscolices. 97 Protoscolices were about 80-100 μ m in diameter, and had hooks being 98 visible as refractive structures. Numerous calcareous corpuscles 99 were observed within the germinal layer as well as protoscolices (Fig. 100 3). A dense accumulation of germinal cells, showing budding form, 101 were sometimes observed (Fig. 4). Many multinucleated giant cells 102 being reactive to the vesicles were observed, associated with 103 numerous lymphocytes and foamy macrophages (Fig. 5). No 104 pathological lesions were observed in other organs. 105 In this study, alveolar echinococcosis was diagnosed in a flying 106 squirrel at postmortem examination. In Japan, Hokkaido, the 107 northern island, is the only region with documented endemic 108 occurrence of E. multilocularis [2]. Red foxes (Vulpues vulpes), 109 domestic dogs and raccoon-dogs (Nyctereutes procyonoides) have been 110 identified as definitive host in Hokkaido [7]. Macroscopical 111 finding showed marked enlargement of the liver and lung characterized 112 by polycystic or multiloculated-cystic structures, and were 113 consistent with alveolar echinococcosis. Histologically, 114 metacestode origin of these cysts showing multivesicular, 115 infiltrating structures consisted of a bladder with numerous 116 protoscoleces. In addition to the epidemiology, these morphological 117 criteria confirm the diagnosis of E. multilocularis infection. 118 E. multilocularis lesion is characterized by a granulomatous host 119 reaction that includes infiltration of cells including lymphocytes, 120 epithelioid cells and multinucleated giant cells and fibrosis [4, 121 13]. These periparasitic reactions surrounding the metacestode 5 122 vesicles were not markedly different in the small mammal intermediate 123 hosts including the experimental murine model and our flying squirrel 124 case [2, 8]. The metacestode evades immune responses and 125 proliferates progressively, and is capable to produce large numbers 126 of protoscoleces. The periparasitic granuloma and fibrosis protect 127 the host against the parasite’s growth. In experimental murine model 128 and human cases [4, 13], the correlation between resistance and 129 development of fibrosis suggests that fibrogenesis is an important 130 component of the immunologically mediated effector mechanisms that 131 limit larval growth. Since thin fibrosis in the periphery of the 132 metacestode expanding growth does not seem to inhibit the 133 infiltrative growth in this case, the flying squirrel may have high 134 susceptibility to infection. Although lung involvement is rare in 135 E. multilocularis infections in human [1], pulmonary lesions with 136 metacestode tissue are sometimes observed in the intermediate animals 137 [2]. In this animal, the pulmonary lesions caused by hematogenous 138 metastasizing spread from primary hepatic lesions induced clinically 139 breathing difficulty and cyanosis, and finally death. 140 Infection of intermediate hosts occurs by the ingestion of eggs. 141 The zoo maintaining a flying squirrel in this study is surrounded 142 by a fox-tight perimeter fence, and direct contact with foxes can 143 be excluded. Generally, metacestodes of E. multilocularis develop 144 rapidly in intermediate host animals, and death of the intermediate 145 host can occur, usually around five months after infection [2]. From 146 these findings, the infection route in this animal may be ingestion 147 of feeds or some branches from wild trees or shrubs contaminated by 6 148 E.multilocularis. 149 Based on the histological findings, flying squirrel may be one of 150 the most suitable intermediate hosts for E. multilocularis as 151 red-backed voles, and could contribute to the transmission of this 152 disease by chance. 153 7 154 REFERENCES 155 1. Czermak, B. V., Unsinn, K. M., Gotwald, T., Waldenberger, P., 156 Freund, M. C., Bale, R. J., Vogel, W. and Jaschke, W. R. 2001. 157 Echinococcus multilocularis revisited. Am. J. Roentgenol. 158 176:1207-1212. 159 2. Eckert, J., Rausch R. L., Gemmell, M. A., Giraudoux, P., Kamiya, 160 M., Liu, F.-J., Schaantz, P. M. and Romig, T. 2001. Epidemiology 161 of Echinococcus multilocularis, Echinococcus vogeli and 162 Echinococcus oligartbrus. Pp. 164-194. In: WHO/OIE Manual on 163 Echinococcosis in Humans and Animals:a Public Health Problem of 164 Global Concern (Eckert, J., Gemmell, M. A., Meslin, F. –X. and 165 Pawłowski, Z. S. eds.), World Organisation for Animal Health and 166 World Health Organization, Paris. 167 3. Eddi, C., Katalin, de B., Juan, L., William, A., Andrew, S., 168 Daniela, B. and Joseph, D. 2006. Veterinary public health 169 activities at FAO: cysticercosis and echinococcosis.
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