Shih-Ping CHEN, Ming-Chung LEE, Yu-Fen SUN, Chi-Min CHEN, Ping-Chen YANG, * Ivan-Chen CHENG

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1 ij~~ifi~t; Taiwan VetJ 33 (3&4): , 2007 Short Communication: Malignant Catarrhal Fever Associated with Caprine Herpesvirus-2 Infection in Captive Formosan Sika Deer (Cervus Nippon Taiouanus) in Taiwan Shih-Ping CHEN, Ming-Chung LEE, Yu-Fen SUN, Chi-Min CHEN, Ping-Chen YANG, * Ivan-Chen CHENG Animal Technology Institute Taiwan, PO Box 23, Chunan, Miaoli, Taiwan Department of Animal Medicine, Animal Technology Institute Taiwan ( Received: December 13, Accepted: December 27, ) ABSTRACT Caprine herpesvirus-2 ( CpHV-2) infec tion in Formosan sika deer ( Cerv us nippon teiouanus ) with clinical sign s and pathologi cal changes of chronic malignant catarrhal fever ( MCF) detected by polymerase chain reaction ( PCR) and sequencing in Taiwan is reported here. During th e period of September 2002 and January 2003, 12 Formosan sika deer died with progressive weight loss; while 2 other deer in the same captive herd were subclinically infected. At necropsy, gross lesions were characte rized by marked arteriosclerosis in th e heart, mesentery, and kidneys were noted. Microscopi cally, all 12 animal s had seve re lympho cytic vas culitis with intimal hyperplasia that were consistent w ith th e lesions of chronic MCF. Antibody to MCF virus was detected in sera collected from all deer and goats housing in the same barn. Clinically normal goats, but not cattle, in the same barn were also PCR positive for CpHV-2. Subclinically CpHV-2-infected goats were considered to be the sourc e of infec tion in this incidence. [Shih-Ping CHEN, Ming-Chun g LEE, Yu-Fen SUN, Chi-Min CHEN, Ping-Chen YANG, *Ivan-Chen CHENG. Short Communication : Malignant catarrhal fever assoc i ated with caprine herpesvirus-2 infection in captive Formosa n sika deer ( Cervus nippon taiouanus ) in Taiwan. Taiwan Vet J 33(3&4): , *Corresponding author TEL: (037) , FAX: (037) , iccol@ma il.atit.org.tw] Keywords: Malignant catarrhal fever ( MCF), Caprine herpesvirus-2 ( CpHV-2), ( PCR) Polymerase chain reaction Malignant catarrhal fever ( MCF) is a serious and usually fatal infection of many species of ruminants throughout the world [9]. It is defined by the recog nition of characteristic wid espread Iymphoproliferation, vas culitis, and inflamma tion affecting many tissues. Moreover, it is generally characterized by low morbidity but high mortality. Captive deer, such as red deer, Pere David 's deer, white-tailed deer, and sika deer, are susce ptible to this disease. It has been described as one of the most imp ortant viral diseases in farm deer in New Zealand [I]. Two distinct herp esviru ses, alcelaphine herpesvirus 1 ( AHv -I) and ovine herpesviru s 2 ( OvHv -2 ), are capable ofinducing MCF. The AHv-I and OvHV-2 infections are endemi c in wildebeest and dom estic sheep, respectively, causing virt ually no clinic al disease in these species. Another MCF virus that is well adapted in dome stic goats has recently been identifi ed as caprine

2 Shih -Ping Chen et al 163 herpesvirus 2 ( CpHV-2) [4, 7,8]. Recent studies have and kidneys were affected the most. Other lesions in- shown that sika deer ( CervlIs nippon ) and white-tail- cluded petechial to paint brush hemorrhages along the ed deer ( Odocoileus virginianus ) cohabiting with in- coronary groove and in the left ventricle wall of the fected domestic goats can lead to the deve lopment of heart and in the serosa of small intestine and co lon. MCF in those deer [7, 8]. The detection of DNA of Multiple necrotic foci were seen in the liver. White CpHV-2 from perip heral blood leukocytes from sick spots on rena l cortex and conjunctival hyperemia were deer and clinically healthy domestic goats further stren- also observed. In addition, there were mucosal erosi- gthens the concept that goats are the reservoir for ons in ora l and nasal cavities and in rumen, omentum, CpHV-2 [4, 7, 8]. This report describes the first diag- and reticulum. nosis, by pathology, PCR and sequencing approaches, Microscopic lesions in the dead deer were severe, ofcphv-2 infec tion in a severe MCF incidence in For- extens ive, and consistent. There was marked Iy- mosan sika deer ( Cervus nippon taiouanus ) in Ta- mp hop lasmacytic meningoencephalitis in the cere - iwan. brum and cerebellum. Lymphocytic vasculitis to perifourteen 6-month-old Formosan sika deer were vasculitis ( Fig. 2 ) with fibrinoid mural necrosis and pu rchased from a captive deer fann in southern Ta- intimal hyperplasia was observed in the heart ( Fig. iwan in early Jul y The deer were then kept with 3 ), brain, kidneys, mesenteric lymph node, aboma- 16 catt le and 30 pregnant domestic goa ts that were either near term or kidding. These an imals were housed in separate pens in one bam without direct contact and were tended by an attendant. Twe lve of the 14 sika deer die d between September 2002 and January Clinical signs were anorexia, depression, seizures, we ight loses, mild ocular discharge, conjunctivitis, and corneal opacity. Death occ urred within 1 mon th of the onset of clinical signs. Two deer remained clinically normal until December Goats and cattle that shared housing with the Formosan sika deer also remained clinically norm al. At necropsy, the principal gross lesion was ma rkedly increased thickness of the arterial wall. The coronary arteries ( Fig. I ) and those in the mesentery Fig. 2 Microscopic lesions of Fig. 1. with severe intimal hyperp lasia of corona ry a rte ry ( Trichrome sta in ). X200. Fig. 1 Markedly thickened coronary arte ries as indicated by arrows ( inset: the cross section of a coronary a rte ry). Fig. 3 Severe arter itis with fibrinoid necrosis a nd marked perivas cular Iymphoplasma cytic cuffi ng in the mesente ry ( H&E ). X200

3 MCF associated with CpHV-2 in Formosan sika deer 164 sum, and ileum. Foc i of mineralization, associated with hemorrhages, were presented in the walls ofsome necrotic vessels and myocardium. Sero logy for antibodies to epizootic hemorrhagic disease and bluetongue viruses were negative, but were positive for MCF virus ( VMRD, Inc. ) in all deer and goats housing in the same barn. Samples of DNA ex tracted from the per ipheral blood lym phocytes ( PBL) of 7 deer; spleen and lymph nodes of all 12 affected deer, as well as samples of DNA from PBL of goa ts, cattle and the 2 alive sika deer were subjected to PCR am plification. The proce dures for DNA extrac tion using commercial kits were as described previous ly [7]. The purified DNA samples were store d at -20 o e until tested. The PCR was performed to identify the presence of MCF virus using the consensus primers [10] of a conserved reg ion of the herpesviral DNA polymerase gene and the primers [7] specific for CpHV-2. The consensus PCR produced a product of approximately 230 base pairs ( bp) ( Fig. 4 ) from PBL and tissues ofall 14 deer and all commingled goats. The PCR products from all positive animals were sequence d and exhi bited 100% iden tity. When the sequences were compared with that ofthe polymerase gene ofcphv bp M 1 2 Fig. 4 Herpesvirus consensus PCR products analyzed by agarose gel electrophoresis. Lane M. 100-bp DNA ladder; lanes 1-4. blood samples from dead Formosan sika deer; lane 5. positive control from sequenced MCF PCR product; lane 6. negative control bp _ M Fig. 5 Agarose gel electrophoresis of ethidium bromide-stained CpHV-2-specific PCR products. Lane M. 100-bp DNA ladder; lanes 1-4. blood samples from dead sika deer; lane 5. positive control from sequenced MCF PCR product; lane 6. negative control. from GeneBank ( AF ), they also matched 100% ( data not shown ). When primers specific for Cp HV-2 we re used, a produc t ofapproximately 108 bp ( Fig 5 ) was detected from the PBL or tissues of all 14 deer and all comming led goats. However, samples from the cattle showed negative for these two PCR assays ( data not show n ). Thi s is the first report ofgoa t-associated MCF in Taiwa n. The clinica l findings in the present study are simi lar to those of chronic goa t-associated MCF in sika deer [7] and wh ite-tai led deer [8] which had we ight loss and emaciation. This report confirms that goa t-associated MCF ca n cause chro nic infection in deer. A distinct feature in the present incidence different from the previous findings [4, 8] was that 2 of 14 deer with typical MCF, and 10 of 14 that survived for extended periods within 30 days. Meanwhile, 2 of 14 didn't showed any clin ical signs. In this incidence, serology indicated that all deer and goats in the same barn were infected by MCF. The mor tality was also as high as that described in sheep-associated MCF in white-tailed deer [2] with some deer recovered. There is no explanation for the different clinical outcomes among various animals with MCF in this incid ence, although there were reports of MCF in deer that recovered [5]. 5 6

4 165 Shih-Ping Chen et al Co meal ede ma, desc ribed in shee p-associated MCF in cattl e and cervid spec ies [9], has not been described in previous cases of goat-associated MCF [7, 8], but was observ ed in 2 of the diseased deer in this study. Th e current cases had mark edly thickened arterial wa ll, due to intima l hyperplasia and infiltrati on of lymphocytes and so me neutrophils, as described in axis deer [3]. Th e vascul ar lesions were abse nt in CpHV-2 infections of sik a deer [7] and white-tailed deer [8] ind icating that different clinical signs and lesions may be ob serv ed among different species affected by MCF. Me anwhil e, the ho st range ofcphv-2 rem ain s to be det ermined, However, in particular in the present incidenc e, cattl e showed no evidence of infection as indicated by the negative C-E LISA ( VMRD, Inc. ) and PCR results; even wh en they we re hou sed with goats and deer, Therefore, unli ke that found in sheep-associated MCF virus which caused infection in both deer and cattl e [6], cattl e are not susceptible to Cp HV-2 associated MCF by ind irect co ntac t. This rep ort shows that serious loss can occur in the outbreak of CpHV-2-associated MCF in deer and it also provid es further evidence that goats are the so u rce of infection. Since no va ccine is available for MCF, deer producers should try to avoid contact s betw een deer and go ats to prevent the infection of CpHV-2. REFERENCES 1. Audiqe L. Wilson PRo Morris RS. Disea se and mortalit y on red deer farms in New Zeal and. Vet Rec 148: Bro wn CC and Bloss LL. An epizootic of malignant ca tarrhal fever in a large ca ptive herd of white-tailed deer ( Odocoileus virginianus ). J Wildl Dis 28 : Clark J<A and Robinson RM. Maligna nt cararr hal fever in Texas cervids. J Wildl Dis 6: Crawf ord TB. Li H. Rosenburg SR. Norhausen RW. Garn er MM. Mural folliculitis and alopecia caused by infection with goat -a ssociated malignant catarrh al fever virus in two stk a deer. J Am Vet Med Assoc 22: Heuschele WP. Nielsen NO. Oosterhuis JE. Castro AE. Dexamethasone-induced re crudescen ce of malignant catarrhal fever and ass ociat ed lymphosarcoma and granulomatous disease in a Formosan slka deer ( Cervus nippon taiouanus ). Am J Vet Res 46: Imai 1<. Nishimori T. Horin o R. I<awashima 1<. Murata H. Tsunemitsu H. Saito T. I<atsura gi 1<. Yaegashi G. Experimental transmission of sheep- ass ociated malignant cat ar rhal f ever from sheep to Japanese deer ( Cervus nippon ) and cattle. Vet Microbiol 79: I<eel MI<. Patterson JG. Noon TH. Brad ley GA. Collins JI<. Capri ne herpesviru s-2 in association with naturally occ urring maligna nt catarrhal f ever in captive sika deer ( Cervus nippon ). J Vet Diagn Inve st 15: Li H. Wunschmann A. I<eller J. Hall G. Crawfo rd TB. Caprine herpesv iru s-2-associated malignant catarrhal feve r in white-tailed deer ( Odocoileus virginianus ). J Vet Diagn Inve st 15: Radostits OM. Gay CC. Blood DC. Hinchcliff I<W. Malignant cat arrhal fever. In: Veterinary Medicine. 9th ed. Harcourt Publishers Ltd. pp VanDevanter DR. Warrener P. Bennett L. Schu ltz ER. Coulter S. Garbe r RL. Rose TM. Detection and analysis of diverse herpesviral spec ies by consensus pr imer PCR. J Clin Microbiol 34:

5 MCF associated with CpHV-2 in Formo san sika deer 166 簡訊 : 台灣圈飼梅花鹿戚染山羊第二型宿疹病毒惡性卡他熱 陳世平李明昌孫 豫芬陳敢銘楊平政 * 鄭益謙 財團法人台灣動物科技研究所 苗果縣竹南郵政信箱 2 3 號 財團法人台灣動物科技研究所動物醫學組 ( 收稿日期 : 96 年 12 月 13 日 接受日期 : 96 年 12 月 2 7 日 ) ; 高要本篇報告為首次以眾合酹鏈反應及基因定序診斷台灣本地梅花鹿因成染山羊第二型泡疹病毒所引發 之慢性惡性卡他熱臨床症狀與病理特徵 在 年九月到 年元月間, 圈養在一起的鹿群中有叩頭死於 逐漸消瘦, 另外兩頭無可見病狀 剖檢肉眼病變有心 腸繫膜淋巴結與腎的明顯動脈硬化 ; 1 2 頭動物都有嚴 重淋巴球性血管炎, 伴隨血管內膜增生 與慢性惡性卡他熱吻合的顯微病理病變 成染鹿與圈飼於同舍不同 欄的山羊血清中, 均可驗出惡性卡他熱抗體, 這些外表健康的山羊於山羊第二型箔疹病毒的環合髓鏈反應按 測均呈陽性, 但圈飼於同舍不同欄的牛隻驗測結果則呈陰性 推測本案例中無臨床症狀 但為山羊第二型厄 疹病毒帶原者的健康山羊是造成鹿隻戚染發病的病毒來源 [ I 宋世平 李明昌 孫豫芬 陳屆主銘 楊平 政 * 鄭益謙 台灣國飼梅花鹿 0. 染山羊第二型疤疹病毒惡性卡他熱 a 台灣獸醫誌 3 3 (3&4): , 2007 * 聯絡人 TE L: (037) , FAX: (037) icco I@mail.atit.org.tw] 晶宮訝 : 是吉性表 f 世縛, 山芋第二 ff1f&, 彥府萃, ZZt 子 if~ 血事友應