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Rabies and Rabies Virus in Wildlife in Mainland China, 1990–2013

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Rabies and Rabies Virus in Wildlife in Mainland China, 1990–2013 View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector International Journal of Infectious Diseases 25 (2014) 122–129 Contents lists available at ScienceDirect International Journal of Infectious Diseases jou rnal homepage: www.elsevier.com/locate/ijid Review Rabies and rabies virus in wildlife in mainland China, 1990–2013 a,b, a,b a,b Lihua Wang *, Qing Tang , Guodong Liang a State Key Laboratory for Infectious Disease Prevention and Control, Key Laboratory for Medical Virology, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, 155 Changbai St., Changping Dist., Beijing 102206, China b Collaborative Innovation Center for Diagnosis and Treatment of Infectious Diseases, Hangzhou, China A R T I C L E I N F O S U M M A R Y Article history: The number of wildlife rabies and wildlife-associated human and livestock rabies cases has increased in Received 6 March 2014 recent years, particularly in the southeast and northeast regions of mainland China. To better understand Received in revised form 17 April 2014 wildlife rabies and its role in human and livestock rabies, we reviewed what is known about wildlife Accepted 17 April 2014 rabies from the 1990s to 2013 in mainland China. In addition, the genetic diversity and phylogeny of Corresponding Editor: Eskild Petersen, available wildlife-originated rabies viruses (RABVs) were analyzed. Several wildlife species carry rabies Aarhus, Denmark including the bat, Chinese ferret badger, raccoon dog, rat, fox, and wolf. RABVs have been isolated or detected in the bat, Chinese ferret badger, raccoon dog, Apodemus, deer, and vole. Among them, the bat, Keywords: Chinese ferret badger, and raccoon dog may play a role in the ecology of lyssaviruses in mainland China. Wildlife rabies All wildlife-originated RABVs were found to belong to genotype 1 RABV except for a bat-originated Irkut Genetic diversity virus isolated in 2012. Several substitutions were found between the glycoprotein of wildlife-originated Phylogeny RABVs and vaccine strains. Whether these substitutions could affect the efficacy of currently used Mainland China vaccines against infections caused by these wildlife-originated RABVs needs to be investigated further. Phylogenetic analysis showed that RABVs in the bat, Chinese ferret badger, and raccoon dog were distinct from local dog-originated RABVs, and almost all collected wildlife-originated isolates were associated with older China clades II to V, suggesting the possibility of wildlife reservoirs in mainland China through the ages. ß 2014 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/3.0/). The role of the domestic dog in the spread of RABVs has been 1. Introduction established in China, and almost 95% of human cases have been 5–9 associated with dog transmission. However, the number of Rabies is one of the oldest diseases in recorded human history, wildlife rabies and wildlife-associated human and livestock rabies 1 dating back more than 4000 years. It occurs in over 150 countries cases has increased in recent years, particularly in the southeast 2 and territories. More than 70 000 human rabies deaths occur and northeast regions of China (Figure 1 and Table 1). The majority annually, and Asia accounts for approximately 80% of the have occurred in the most recent 10 years. Viruses have also been 3 worldwide total. Rabies was first reported in about 556 BC and isolated or detected in wildlife, including the bat, Chinese ferret has persisted in China for more than 2500 years. Rabies has been 10–20 badger, raccoon dog, Apodemus, deer, vole, and wolf. To better one of the most important infectious diseases in China since the understand wildlife rabies and its role in human and livestock 4,5 1950s. Although comprehensive preventive measures have been rabies, we reviewed what is known about wildlife rabies from the taken in past decades (including dog vaccination and post- 1990s to 2013 in mainland China. Additionally, the genetic exposure prophylaxis following human exposure), rabies remains diversity and phylogeny of available wildlife-originated RABVs 4–7 a significant public health problem in mainland China. were analyzed. Currently, China is second only to India in the number of people killed by rabies worldwide, and the epidemic area has expanded to 2. Species of wildlife carrying rabies in mainland China almost the entire country. Many provinces are beginning to report 5–8 their first cases in more than 10 years. Any warm-blooded animal can catch rabies and pass rabies to 3 human beings. Dogs are the main vectors of rabies and have 5–9 played a pivotal role in human rabies in mainland China. * Corresponding author. Tel.: +86 10 58900896; fax: +86 10 58900840. E-mail address: [email protected] (L. Wang). However rabies has also been reported in wildlife and livestock http://dx.doi.org/10.1016/j.ijid.2014.04.016 1201-9712/ß 2014 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/). L. Wang et al. / International Journal of Infectious Diseases 25 (2014) 122–129 123 Figure 1. Distribution of wildlife and livestock rabies reported in mainland China from the 1990s to 2013. Species of wildlife and livestock reported to carry rabies are indicated next to the name of each province. Provinces: AH, Anhui; BJ, Beijing; CQ, Chongqing; FJ, Fujian; HA, Henan; HB, Hebei; HI, Hainan; HLJ, Heilongjiang; HuB, Hubei; HuN, Hunan; GD, Guangdong; GS, Gansu; GX, Guangxi; GZ, Guizhou; JL, Jilin; JS, Jiangsu; JX, Jiangxi; LN, Liaoning; NM, Inner Mongolia; NX, Ningxia; QH, Qinghai; SC, Sichuan; SD, Shandong; SH, Shanghai; SN, Shaanxi; SX, Shanxi; TJ, Tianjin; XJ, Xingjiang; XZ, Tibet; YN, Yunnan; ZJ, Zhejiang. CFB, Chinese ferret badger; RD, raccoon dog. including the Chinese ferret badger, raccoon dog, bat, Apodemus, 2.2. Raccoon dog deer, vole, fox, wolf, cat, pig, yellow bull, goat, sheep, cattle, buffalo, and donkey. Cases of wildlife rabies have occurred in both rabies In mainland China, raccoon dogs are distributed widely in the endemic areas (southeast) and sporadic areas (northeast) of northeastern and southwestern regions of rabies-endemic 14,21 mainland China (Figure 1, Table 1). areas. Two outbreaks of raccoon dog rabies have been recorded in mainland China. One occurred in the county of Qingyuan of 2.1. Chinese ferret badger Liaoning Province in 1982, causing more than 30 raccoon dog 13 14 deaths. The other occurred in Inner Mongolia in 2007. The As one of the most popular wildlife animals, Chinese ferret latter outbreak was caused by one wild raccoon dog, and 15 badgers (Melogale moschata) are distributed mostly in the domestic raccoon dogs died. The rabid animals had typical clinical 5,11 southeast region of China. Since 1995, Chinese ferret badger signs of rabies, and samples tested positive by direct fluorescence rabies outbreaks have occurred periodically in the southeast of assay (DFA), reverse transcription polymerase chain reaction mainland China, including the provinces of Anhui, Jiangxi, and (RT-PCR), and mouse inoculation test (MIT). Genetic analysis of 20 Zhejiang. RABVs were first detected in Chinese ferret badgers the isolated virus showed that the outbreak was caused by an 14 collected in Zhejiang Province in 2008, and have since been arctic-like RABV. This was the first report of arctic-like RABV in detected continuously in Chinese ferret badgers (alive and China. dead) collected in Anhui, Jiangxi, and Zhejiang provinces 12,19,20 (Figure 1, Table 1). Nucleotide sequencing revealed 2.3. Bat 99.4–99.8% homology within the Chinese ferret badger isolates, and 83–89% homology to the dog RABV isolates in the Other than carnivores, the bat is the most important natural 22 nucleoprotein and glycoprotein genes in the same rabies- reservoir host of RABVs known today. In recent years, several 12,19,20 endemic regions. In addition, one study showed appar- research groups have conducted long-term studies to investigate ently healthy Chinese ferret badgers with a high percentage of whether bats carry rabies in mainland China; RABV antibodies rabies seroconversion (69.6%). Although the titration of virus were detected in the serum of collected bats. Of the bat serum neutralizing antibodies (VNA) was very low, ranging from 0 to samples collected from four southern provinces (Yunnan, Guangxi, 2.6 IU/ml, the high percentage of rabies seroconversion in Guangdong, and Hainan) of China in 2010, 2.2% (15/685) were 23 Chinese ferret badgers is an interesting discovery, and could be positive for RABV antibodies. However, no bat-originated due to abortive rabies infections in the Chinese ferret badger lyssavirus was isolated until 2012: the first bat-originated 20 population. lyssavirus (Irkut virus, IRKV-THChina12; in Murina leucogaster) 124 L. Wang et al. / International Journal of Infectious Diseases 25 (2014) 122–129 Table 1 Summary of reported wildlife rabies and wildlife-associated human rabies in mainland China, 1990–2013 a b Provinces Counties Period Rabies cases Number Confirmation method Ref. tested Chinese ferret ZJ Lishui 2008 1 23 DFA/RT-PCR 19 badger rabies JX Fuzhou 2009 1 23 DFA/MIT/RT-PCR 12 c ZJ, AH, JX / 2010 9 265 FAT/MIT 20 Bat rabies
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