Citation: Han Xia, Yujuan Wang, Evans Atoni, Bo Zhang, Zhiming Yuan. Mosquito-Associated Viruses in China .VIROLOGICA SINICA, 2018, 33(1) : 5-20.  http://dx.doi.org/10.1007/s12250-018-0002-9

Mosquito-Associated Viruses in China

  • Corresponding author: Zhiming Yuan, yzm@wh.iov.cn, ORCID: 0000-0002-3234-9616
  • Received Date: 07 June 2017
    Accepted Date: 05 December 2017
    Available online: 01 February 2018
  • Mosquitoes are classified into approximately 3500 species and further grouped into 41 genera. Epidemiologically, they are considered to be among the most important disease vectors in the world and they can harbor a wide variety of viruses. Several mosquito viruses are considered to be of significant medical importance and can cause serious public health issues throughout the world. Such viruses are Japanese encephalitis virus (JEV), dengue virus (DENV), chikungunya virus (CHIKV), and Zika virus (ZIKV). Others are the newly recognized mosquito viruses such as Banna virus (BAV) and Yunnan orbivirus (YNOV) with unclear medical significance. The remaining mosquito viruses are those that naturally infect mosquitoes but do not appear to infect humans or other vertebrates. With the continuous development and improvement of mosquito and mosquito-associated virus surveillance systems in China, many novel mosquito-associated viruses have been discovered in recent years. This review aims to systematically outline the history, characteristics, distribution, and/or current epidemic status of mosquito-associated viruses in China.

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    1. Adouchief S, Smura T, Sane J, Vapalahti O, Kurkela S (2016) Sindbis virus as a human pathogen—epidemiology, clinical picture and pathogenesis. Rev Med 26:221–241

    2. Attoui H, Billoir F, Biagini P, de Micco P, de Lamballerie X (2000) Complete sequence determination and genetic analysis of Banna virus and Kadipiro virus: proposal for assignment to a new genus (Seadornavirus) within the family Reoviridae. J Gen Virol 81:1507–1515
        doi: 10.1099/0022-1317-81-6-1507

    3. Attoui H, Mohd Jaafar F, Belhouchet M, Aldrovandi N, Tao S, Chen B, Liang G, Tesh RB, de Micco P, de Lamballerie X (2005a) Yunnan orbivirus, a new orbivirus species isolated from Culex tritaeniorhynchus mosquitoes in China. J Gen Virol 86:3409–3417
        doi: 10.1099/vir.0.81258-0

    4. Attoui H, Mohd Jaafar F, de Micco P, de Lamballerie X (2005b) Coltiviruses and seadornaviruses in North America, Europe, and Asia. Emerg Infect Dis 11:1673–1679
        doi: 10.3201/eid1111.050868

    5. Attoui H, Jaafar FM, Belhouchet M, Tao S, Chen B, Liang G, Tesh RB, de Micco P, de Lamballerie X (2006) Liao ning virus, a new Chinese Seadornavirus that replicates in transformed and embryonic mammalian cells. J Gen Virol 87:199–208
        doi: 10.1099/vir.0.81294-0

    6. Attoui H, Mendez-lopez MR, Rao S, Hurtado-Alendes A, LizarasoCaparo F, Jaafar FM, Samuel AR, Belhouchet M, Pritchard LI, Melville L, Weir RP, Hyatt AD, Davis SS, Lunt R, Calisher CH, Tesh RB, Fujita R, Mertens PPC (2009) Peruvian horse sickness virus and Yunnan orbivirus, isolated from vertebrates and mosquitoes in Peru and Australia. Virology 394:298–310
        doi: 10.1016/j.virol.2009.08.032

    7. Bialonski A, Günther S, Jöst H, Schmidt-Chanasit J, Schmetz C, Becker N (2011) Isolation and phylogenetic analysis of Batai Virus, Germany. Am J Trop Med Hyg 84:241–243
        doi: 10.4269/ajtmh.2011.10-0483

    8. Bogoch II, Brady OJ, Kraemer MUG, German M, Creatore MI, Kulkarni MA, Brownstein JS, Mekaru SR, Hay SI, Groot E, Watts A, Khan K (2016) Anticipating the international spread of Zika virus from Brazil. Lancet 387:335–336
        doi: 10.1016/S0140-6736(16)00080-5

    9. Bolling B, Weaver S, Tesh R, Vasilakis N (2015) Insect-specific virus discovery: significance for the arbovirus community. Viruses 7:4911–4928
        doi: 10.3390/v7092851

    10. Bowen RA, Bosco-Lauth AM, Nemeth NM, Kohler DJ (2016) Viremia in North American mammals and birds after experimental infection with chikungunya viruses. Am J Trop Med Hyg 94:504–506
        doi: 10.4269/ajtmh.15-0696

    11. Briese T, Bird B, Kapoor V, Nichol ST, Lipkin WI (2006) Batai and Ngari viruses: m segment reassortment and association with severe febrile disease outbreaks in East Africa. J Virol 80:5627–5630
        doi: 10.1128/JVI.02448-05

    12. Brown CM, Timoney PJ (1998) Getah virus infection of Indian horses. Trop Anim Health Prod 30:241–252
        doi: 10.1023/A:1005079229232

    13. Butt AM, Nasrullah I, Tong YG (2014) Genome-wide analysis of codon usage and influencing factors in chikungunya viruses. PLoS ONE 9:e90905
        doi: 10.1371/journal.pone.0090905

    14. Cao YX, Fu SH, Tian ZF, Lu Z, He Y, Wang HY, Wang JL, Guo WD, Tao B, Liang GD (2011) Distribution of mosquitoes and mosquito-borne arboviruses in Inner Mongolia, China. Vector Borne Zoonotic Dis 11:1577–1581
        doi: 10.1089/vbz.2010.0262

    15. Cao ZZ, Zhang C, Liu YH, Ye WC, Han JW, Ma GM, Zhang DD, Xu F, Gao XH, Tang Y, Shi SH, Wan CH, Zhang C, He B, Yang MJ, Lu XH, Huang Y, Diao YX, Ma XJ, Zhang DB (2011) Tembusu virus in ducks, China. Emerg Infect Dis 17:1873–1875
        doi: 10.3201/eid1710.101890

    16. Chancey C, Grinev A, Volkova E, Rios M (2015) The global ecology and epidemiology of West Nile virus. Biomed Res Int 2015:376230

    17. Chen J, Lu HZ (2016) Yellow fever in China is still an imported disease. Biosci Trends 10:158–162
        doi: 10.5582/bst.2016.01051

    18. Chen ZH, Liu L, Lv YN, Zhang W, Li JD, Zhang Y, Di T, Zhang S, Liu JY, Li J, Qu J, Hua WH, Li C, Wang P, Zhang QF, Xu YL, Jiang RM, Wang Q, Chen LJ, Wang SW, Pang XH, Liang MF, Ma XJ, Li XW, Wang QY, Zhang FJ, Li DX (2016) A fatal yellow fever virus infection in China: description and lessons. Emerg Microbes Infect 5:e69
        doi: 10.1038/emi.2016.89

    19. Cook S, Moureau G, Harbach RE, Mukwaya L, Goodger K, Ssenfuka F, Gould E, Holmes EC, de Lamballerie X (2009) Isolation of a novel species of flavivirus and a new strain of Culex flavivirus (Flaviviridae) from a natural mosquito population in Uganda. J Gen Virol 90:2669–2678
        doi: 10.1099/vir.0.014183-0

    20. Deng YQ, Zhao H, Li XF, Zhang NN, Liu ZY, Jiang T, Gu DY, Shi L, He JA, Wang HJ, Sun ZZ, Ye Q, Xie DY, Cao WC, Qin CF (2016) Isolation, identification and genomic characterization of the Asian lineage Zika virus imported to China. Sci China Life Sci 59:428–430

    21. Deng C, Liu S, Zhang Q, Xu M, Zhang H, Gu D, Shi L, He J, Xiao G, Zhang B (2016) Isolation and characterization of Zika virus imported to China using C6/36 mosquito cells. Virol Sin 31:176–179
        doi: 10.1007/s12250-016-3778-5

    22. Doherty RL, Standfast HA, Wetters EJ, Whitehead RH, Barrow GJ, Gorman BM (1968) Virus isolation and serological studies of arthropod-borne virus infections in a high rainfall area of North Queensland. Trans R Soc Trop Med Hyg 62:862–867
        doi: 10.1016/0035-9203(68)90014-X

    23. Feng Y, Zhang HL, Fu SH, Yang WH, Zhang YZ, Wang PY, Yang J, Liu YH, Dong CL, Li S, Zhang BS, Yin ZL, Dong XQ, Wang HY, Liang GD (2014) Investigation on mosquitoes and mosquito-borne viruses in Dehong prefecture, Yunnan province, 2007 and 2010. Zhonghua Liu Xing Bing Xue Za Zhi 35:528–532 (In Chinese)

    24. Filipe AR, Pinto MR (1969) Survey for antibodies to arboviruses in serum of animals from southern Portugal. Am J Trop Med Hyg 18:423–426
        doi: 10.4269/ajtmh.1969.18.423

    25. Fu X, Wang L, Fang B, Ma R, Zheng Y, Huang S, Zhou P, Cao Z, Tian J, Li S, Zhang G (2016) Import of Rift Valley fever to China: a potential new threat? Virol Sin 31:454–456
        doi: 10.1007/s12250-016-3876-4

    26. Fu S, Song S, Liu H, Li Y, Li X, Gao X, Xu Z, Liu G, Wang D, Tian Z, Zhou J, He Y, Lei W, Wang H, Wang B, Lu X, Liang G (2017) ZIKA virus isolated from mosquitoes: a field and laboratory investigation in China, 2016. Sci China Life Sci 60:1364–1371
        doi: 10.1007/s11427-017-9196-8

    27. Gao XY, Nasci R, Liang GD (2010) The neglected arboviral infections in mainland China. PLoS Negl Trop Dis 4:e624
        doi: 10.1371/journal.pntd.0000624

    28. Gao XY, Liu H, Li MH, Fu SH, Liang GD (2015) Insights into the evolutionary history of Japanese encephalitis virus (JEV) based on whole-genome sequences comprising the five genotypes. Virol J 12:43
        doi: 10.1186/s12985-015-0270-z

    29. Gu W, Jin C, Zhang S, Zhang QF, Li JD, Hang XT, Wang Q, Li C, Liang MF, Li DX (2012) Biological characteristics of dengue virus type 3 isolated from Yiwu, China. Chin J Zoonoses 28:695–699

    30. Harley D, Sleigh A, Ritchie S (2001) Ross river virus transmission, infection, and disease: a cross-disciplinary review. Clin Microbiol Rev 14:909–932
        doi: 10.1128/CMR.14.4.909-932.2001

    31. Heilman JM, De Wolff J, Beards GM, Basden BJ (2014) Dengue fever: a Wikipedia clinical review. Open Med 8:e105–e115

    32. Hoshino K, Isawa H, Tsuda Y, Yano K, Sasaki T, Yuda M, Takasaki T, Kobayashi M, Sawabe K (2007) Genetic characterization of a new insect flavivirus isolated from Culex pipiens mosquito in Japan. Virology 359:405–414
        doi: 10.1016/j.virol.2006.09.039

    33. Huang WL, Zhang HL, Mi ZQ, Shi HF, Bao MH, Qian XY (1998) Some animals' susceptibility to Yunnan CHIK virus. J Dali Med Coll 7:12–15

    34. Huang WL, Zhang HL, Hou ZL, Mi ZQ, Zi DY (2001) Investigation on Arboviruses Antibodies of Patients with Fever in Xishuangbanna, Yunnan Province. Endem Dis Bull 16:39–42

    35. Huang XY, Ma HX, Wang HF, Du YH, Su J, Li XL, Tang XY, Ma HP, Zu BC, Zhang QH, Chen HM, Xu BL (2014) Outbreak of dengue fever in central China, 2013. Biomed Environ Sci 27:894–897

    36. Hubálek Z (2008) Mosquito-borne viruses in Europe. Parasitol Res 103:S29–S43

    37. Huhtamo E, Lambert AJ, Costantino S, Servino L, Krizmancic L, Boldorini R, Allegrini S, Grasso I, Korhonen EM, Vapalahti O, Lanciotti RS, Ravanini P (2013) Isolation and full genomic characterization of Batai virus from mosquitoes, Italy 2009. J Gen Virol 94:1242–1248
        doi: 10.1099/vir.0.051359-0

    38. Jentes ES, Poumerol G, Gershman MD, Hill DR, Lemarchand J, Lewis RF, Staples JE, Tomori O, Wilder-Smith A, Monath TP (2011) The revised global yellow fever risk map and recommendations for vaccination, 2010: consensus of the informal WHO Working Group on Geographic Risk for yellow fever. Lancet Infect Dis 11:622–632
        doi: 10.1016/S1473-3099(11)70147-5

    39. Jiang SF, Zhang YM, Guo XX, Dong YD, Xing D, Xue RD, Zhao TY (2010) Experimental studies on comparison of the potential vector competence of four species of Culex mosquitoes in China to transmit West Nile virus. J Med Entomol 47:788–790

    40. Jiang S, Wang Z, Guo X, Zhang Y, Li C, Dong Y, Xing D, Zhao T (2014) Infection and dissemination of West Nile virus in China by the potential vector, Culex pipiens pallens. J Vector Ecol 39:78–82
        doi: 10.1111/jvec.2014.39.issue-1

    41. Jing QL, Yang ZC, Luo L, Xiao XC, Di B, He P, Fu CX, Wang M, Lu JH (2012) Emergence of dengue virus 4 genotype Ⅱ in Guangzhou, China, 2010: survey and molecular epidemiology of one community outbreak. BMC Infect Dis 12:87
        doi: 10.1186/1471-2334-12-87

    42. Karabatsos N (1978) Supplement to international catalogue of Arboviruses including certain other viruses of vertebrates. Am J Trop Med Hyg 27:372–440
        doi: 10.4269/ajtmh.1978.27.372

    43. Kim DY, Guzman H, Bueno R, Dennett JA, Auguste AJ, Carrington CVF, Popov VL, Weaver SC, Beasley DWC, Tesh RB (2009) Characterization of Culex Flavivirus (Flaviviridae) strains isolated from mosquitoes in the United States and Trinidad. Virology 386:154–159
        doi: 10.1016/j.virol.2008.12.034

    44. Klapsing P, MacLean JD, Glaze S, McClean KL, Drebot MA, Lanciotti RS, Campbell GL (2005) Ross River virus disease reemergence, Fiji, 2003–2004. Emerg Infect Dis 11:613–615
        doi: 10.3201/eid1104.041070

    45. Kono Y, Tsukamoto K, Hamid MA, Darus A, Lian TC, Sam LS, Yok CN, Di KB, Lim KT, Yamaguchi S, Narita M (2000) Encephalitis and retarded growth of chicks caused by Sitiawan virus, a new isolate belonging to the genus Flavivirus. Am J Trop Med Hyg 63:94–101
        doi: 10.4269/ajtmh.2000.63.94

    46. Kurkela S, Rätti O, Huhtamo E, Uzcátegui NY, Nuorti JP, Laakkonen J, Manni T, Helle P, Vaheri A, Vapalahti O (2008) Sindbis virus infection in resident birds, migratory birds, and humans, Finland. Emerg Infect Dis 14:41–47
        doi: 10.3201/eid1401.070510

    47. Lai S, Huang Z, Zhou H, Anders KL, Perkins TA, Yin W, Li Y, Mu D, Chen Q, Zhang Z, Qiu Y, Wang L, Zhang H, Zeng L, Ren X, Geng M, Li Z, Tatem AJ, Hay SI, Yu H (2015) The changing epidemiology of dengue in China, 1990–2014: a descriptive analysis of 25 years of nationwide surveillance data. BMC Med 13:100
        doi: 10.1186/s12916-015-0336-1

    48. Laine M, Luukkainen R, Toivanen A (2004) Sindbis viruses and other Alphaviruses as cause of human arthritic disease. J Intern Med 256:457–471
        doi: 10.1111/jim.2004.256.issue-6

    49. Lan D, Ji W, Yu D, Chu J, Wang C, Yang Z, Hua X (2011) Serological evidence of West Nile virus in dogs and cats in China. Arch Virol 156:893–895
        doi: 10.1007/s00705-010-0913-8

    50. Lauber C, Ziebuhr J, Junglen S, Drosten C, Zirkel F, Nga PT, Morita K, Snijder EJ, Gorbalenya AE (2012) Mesoniviridae: a proposed new family in the order Nidovirales formed by a single species of mosquito-borne viruses. Arch Virol 157:1623–1628
        doi: 10.1007/s00705-012-1295-x

    51. Lee JS, Grubaugh ND, Kondig JP, Turell MJ, Kim HC, Klein TA, O'Guinn ML (2013) Isolation and genomic characterization of Chaoyang virus strain ROK144 from Aedes vexans nipponii from the Republic of Korea. Virology 435:220–224
        doi: 10.1016/j.virol.2012.10.020

    52. Lei W, Guo X, Fu S, Feng Y, Nie K, Song J, Li Y, Ma X, Liang G, Zhou H (2015) Isolation of Tibet orbivirus, TIBOV, from Culicoides Collected in Yunnan, China. PLoS ONE 10:e0136257

    53. Lei W, Guo X, Fu S, Feng Y, Tao X, Gao X, Song J, Yang Z, Zhou H, Liang G (2017) The genetic characteristics and evolution of Tembusu virus. Vet Microbiol 201:32–41
        doi: 10.1016/j.vetmic.2017.01.003

    54. Li XD, Qiu FX, Yang H, Rao YN, Calisher CH (1992) Isolation of Getah virus from mosquitos collected on Hainan Island, China, and results of a serosurvey. Southeast Asian J Trop Med Public Health 23:730–734

    55. Li WJ, Wang JL, Li MH, Fu SH, Wang HY, Wang ZY, Jiang SY, Wang XW, Guo P, Zhao SC, Shi Y, Lu NN, Nasci RS, Tang Q, Liang GD (2010) Mosquitoes and mosquito-borne Arboviruses in the Qinghai–Tibet Plateau—focused on the Qinghai area, China. Am J Trop Med Hyg 82:705–711
        doi: 10.4269/ajtmh.2010.09-0649

    56. Li MH, Fu SH, Chen WX, Wang HY, Guo YH, Liu QY, Li YX, Luo HM, Da W, Ji DZ, Ye XM, Liang GD (2011) Genotype V Japanese encephalitis virus is emerging. PLoS Negl Trop Dis 5:e1231
        doi: 10.1371/journal.pntd.0001231

    57. Li XF, Jiang T, Deng YQ, Zhao H, Yu XD, Ye Q, Wang HJ, Zhu SY, Zhang FC, Qin ED, Qin CF (2012) Complete genome sequence of a chikungunya virus isolated in Guangdong, China. J Virol 86:8904–8905
        doi: 10.1128/JVI.01289-12

    58. Li XL, Fu SH, Liu WB, Wang HY, Lu Z, Tong SX, Li ZX, Nasci RS, Kosoy O, Cui Y, Liang GD (2013) West Nile virus infection in Xinjiang, China. Vector Borne Zoonotic Dis 13:131–133
        doi: 10.1089/vbz.2012.0995

    59. Li W, Cao Y, Fu S, Wang J, Li M, Jiang S, Wang X, Xing S, Feng L, Wang Z, Shi Y, Zhao S, Wang H, Wang Z, Liang G (2014) Tahyna virus infection, a neglected arboviral disease in the Qinghai–Tibet Plateau of China. Vector-Borne Zoonotic Dis 14:353–357
        doi: 10.1089/vbz.2013.1351

    60. Li M, Zheng Y, Zhao G, Fu S, Wang D, Wang Z, Liang G (2014) Tibet orbivirus, a novel Orbivirus species isolated from Anopheles maculatus mosquitoes in Tibet, China. PLoS ONE 9:e88738
        doi: 10.1371/journal.pone.0088738

    61. Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, Qin XC, Xu J, Holmes EC, Zhang YZ (2015) Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negativesense RNA viruses. Elife. https://doi.org/10.7554/eLife.05378
        doi: 10.7554/eLife.05378

    62. Li YY, Fu SH, Guo XF, Lei WW, Li XL, Song JD, Cao L, Gao XY, Lyu Z, He Y, Wang HY, Ren XJ, Zhou HN, Wang GQ, Liang GD (2017) Identification of a newly isolated Getah virus in the China-Laos Border, China. Biomed Environ Sci 30:210–214

    63. Liang GD, Li L, Zhou GL, Fu SH, Li QP, Li FS, He HH, Jin Q, He Y, Chen BQ, Hou YD (2000) Isolation and complete nucleotide sequence of a Chinese Sindbis-like virus. J Gen Virol 81:1347–1351
        doi: 10.1099/0022-1317-81-5-1347

    64. Liang W, He X, Liu G, Zhang S, Fu S, Wang M, Chen W, He Y, Tao X, Jiang H, Lin X, Gao X, Hu W, Liu Y, Feng L, Cao Y, Yang G, Jing C, Liang G, Wang H (2015) Distribution and phylogenetic analysis of Culex flavivirus in mosquitoes in China. Arch Virol 160:2259–2268
        doi: 10.1007/s00705-015-2492-1

    65. Ling Y, Chen J, Huang Q, Hu Y, Zhu A, Ye S, Xu L, Lu H (2016) Yellow fever in a worker returning to China from Angola, March 2016. Emerg Infect Dis J 22:1317
        doi: 10.3201/eid2207.160469

    66. Liu H, Li MH, Zhai YG, Meng WS, Sun XH, Cao YX, Fu SH, Wang HY, Xu LH, Tang Q, Liang GD (2010) Banna virus, China, 1987–2007. Emerg Infect Dis 16:514–517
        doi: 10.3201/eid1603.091160

    67. Liu H, Gao XY, Liang GD (2011) Newly recognized mosquitoassociated viruses in mainland China, in the last two decades. Virol J 8:68
        doi: 10.1186/1743-422X-8-68

    68. Liu H, Shao X, Hu B, Zhao J, Zhang L, Zhang H, Bai X, Zhang R, Niu D, Sun Y, Yan X (2014) Isolation and complete nucleotide sequence of a Batai virus strain in Inner Mongolia, China. Virol J 11:138
        doi: 10.1186/1743-422X-11-138

    69. Liu H, Gao XY, Fu SH, Li MH, Zhai YG, Meng WS, Sun XX, Wang HY, Lyu Z, Shen XX, Cao YX, He Y, Liang GD (2016) Analysis on molecular genetic evolution of Banna virus based on the 12(th) segment. Zhonghua Liu Xing Bing Xue Za Zhi 37:1277–1282 (in Chinese)

    70. Liu J, Sun Y, Shi W, Tan S, Pan Y, Cui S, Zhang Q, Dou X, Lv Y, Li X, Li X, Chen L, Quan C, Wang Q, Zhao Y, Lv Q, Hua W, Zeng H, Chen Z, Xiong H, Jiang C, Pang X, Zhang F, Liang M, Wu G, Gao GF, Liu WJ, Li A, Wang Q (2017) The first imported case of Rift Valley fever in China reveals a genetic reassortment of different viral lineages. Emerg Microbes Infect 6:e4
        doi: 10.1038/emi.2016.136

    71. Lu Z, Lu XJ, Fu SH, Zhang S, Li ZX, Yao XH, Feng YP, Lambert AJ, Ni DX, Wang FT, Tong SX, Nasci RS, Feng Y, Dong Q, Zhai YG, Gao XY, Wang HY, Tang Q, Liang GD (2009) Tahyna virus and human infection, China. Emerg Infect Dis 15:306–309
        doi: 10.3201/eid1502.080722

    72. Lu Z, Fu SH, Wang FT, Nasci RS, Tang Q, Liang GD (2011a) Circulation of diverse genotypes of Tahyna virus in Xinjiang, People's Republic of China. Am J Trop Med Hyg 85:442–445
        doi: 10.4269/ajtmh.2011.10-0368

    73. Lu Z, Liu H, Fu S, Lu X, Dong Q, Zhang S, Tong S, Li M, Li W, Tang Q, Liang G (2011b) Liao ning virus in China. Virol J 8:282
        doi: 10.1186/1743-422X-8-282

    74. Lu X, Li X, Mo Z, Jin F, Wang B, Huang J, Huang J, Zhao H, Shi L (2014) Chikungunya emergency in China: microevolution and genetic analysis for a local outbreak. Virus Genes 48:15–22
        doi: 10.1007/s11262-013-0991-2

    75. Lu Z, Fu SH, Cao L, Tang CJ, Zhang S, Li ZX, Tusong M, Yao XH, Zhang HL, Wang PY, Wumaier M, Yuan XY, Li MH, Zhu CZ, Fu LP, Liang GD (2014) Human infection with West Nile virus, Xinjiang, China, 2011. Emerg Infect Dis J 20:1421–1423
        doi: 10.3201/eid2008.131433

    76. Lv Z, Fu S, Wang F, Kosoy OL, Nasci RS, Liang G (2011) Investigation of Tahyna virus infection among unknown fever cases in Xinjiang, China. Chin J Virol 27:71–74

    77. Lv X, Jaafar FM, Sun X, Belhouchet M, Fu S, Zhang S, Tong S, Lv Z, Mertens PPC, Liang G, Attoui H (2012) Isolates of Liao Ning virus from wild-caught mosquitoes in the Xinjiang Province of China in 2005. PLoS ONE 7:e37732
        doi: 10.1371/journal.pone.0037732

    78. Machado DC, Mondini A, dos Santos SantanaV, Yonamine PTK, Chiaravalloti Neto F, Zanotto PM, Nogueira ML (2012) First identification of Culex flavivirus (Flaviviridae) in Brazil. Intervirology 55:475–483
        doi: 10.1159/000337166

    79. McIntosh BM, Paterson HE, McGillivray G, De Sousa J (1964) Further studies on the chikungunya outbreak in Southern Rhodesia in 1962. Ann Trop Med Parasitol 58:45–51
        doi: 10.1080/00034983.1964.11686213

    80. Messina JP, Brady OJ, Scott TW, Zou C, Pigott DM, Duda KA, Bhatt S, Katzelnick L, Howes RE, Battle KE, Simmons CP, Hay SI (2014) Global spread of dengue virus types: mapping the 70 year history. Trends Microbiol 22:138–146
        doi: 10.1016/j.tim.2013.12.011

    81. Misra UK, Kalita J (2010) Overview: Japanese encephalitis. Prog Neurobiol 91:108–120
        doi: 10.1016/j.pneurobio.2010.01.008

    82. Monath TP, Vasconcelos PFC (2015) Yellow fever. J Clin Virol 64:160–173
        doi: 10.1016/j.jcv.2014.08.030

    83. Nabeshima T, Nga PT, Guillermo P, del Carnen Parquet M, Yu F, Thuy NT, Trang BM, Hien NT, Nam VS, Inoue S, Hasebe F, Morita K (2008) Isolation and molecular characterization of Banna virus from mosquitoes, Vietnam. Emerg Infect Dis 14:1276–1279
        doi: 10.3201/eid1408.080100

    84. Nemoto M, Bannai H, Tsujimura K, Yamanaka T, Kondo T (2016) Genomic, pathogenic, and antigenic comparisons of Getah virus strains isolated in 1978 and 2014 in Japan. Arch Virol 161:1691–1695
        doi: 10.1007/s00705-016-2840-9

    85. O'Guinn ML, Turell MJ, Kengluecha A, Jaichapor B, Kankaew P, Miller RS, Endy TP, Jones JW, Coleman RE, Lee JS (2013) Field detection of Tembusu virus in western Thailand by RTPCR and vector competence determination of select Culex mosquitoes for transmission of the virus. Am J Trop Med Hyg 89:1023–1028
        doi: 10.4269/ajtmh.13-0160

    86. Pepin M, Bouloy M, Bird BH, Kemp A, Paweska J (2010) Rift Valley fever virus (Bunyaviridae: Phlebovirus): an update on pathogenesis, molecular epidemiology, vectors, diagnostics and prevention. Vet Res 41:61
        doi: 10.1051/vetres/2010033

    87. Pialoux G, Gaüzère BA, Jauréguiberry S, Strobel M (2007) Chikungunya, an epidemic arbovirosis. Lancet Infect Dis 7:319–327
        doi: 10.1016/S1473-3099(07)70107-X

    88. Rasmussen SA, Jamieson DJ, Honein MA, Petersen LR (2016) Zika virus and birth defects—reviewing the evidence for causality. N Engl J Med 374:1981–1987
        doi: 10.1056/NEJMsr1604338

    89. Rosen L, Gubler DJ, Bennett PH (1981) Epidemic polyarthritis (Ross River) virus infection in the Cook Islands. Am J Trop Med Hyg 30:1294–1302
        doi: 10.4269/ajtmh.1981.30.1294

    90. Rossi SL, Ross TM, Evans JD (2010) West Nile virus. Clin Lab Med 30:47–65
        doi: 10.1016/j.cll.2009.10.006

    91. Russell RC (2002) Ross River virus: ecology and distribution. Annu Rev Entomol 47:1–31
        doi: 10.1146/annurev.ento.47.091201.145100

    92. Sam IC, Chua CL, Rovie-Ryan JJ, Fu JYL, Tong C, Sitam FT, Chan YF (2015) Chikungunya virus in Macaques, Malaysia. Emerg Infect Dis 21:1683–1685
        doi: 10.3201/eid2109.150439

    93. Scrimgeour EM, Aaskov JG, Matz LR (1987) Ross River virus arthritis in Papua New Guinea. Trans R Soc Trop Med Hyg 81:833–834
        doi: 10.1016/0035-9203(87)90045-9

    94. Seo HJ, Kim HC, Klein TA, Park JY, Cho YS, Cho IS, Kyung SG, Yeh JY (2012) Characterization of recent Getah virus isolates from South Korea. Acta Virol 56:265–267
        doi: 10.4149/av_2012_03_265

    95. Shi C, Liu Y, Hu X, Xiong J, Zhang B, Yuan Z (2015) A metagenomic survey of viral abundance and diversity in mosquitoes from Hubei province. PLoS ONE 10:e0129845
        doi: 10.1371/journal.pone.0129845

    96. Shi M, Lin XD, Tian JH, Chen LJ, Chen X, Li CX, Qin XC, Li J, Cao JP, Eden JS, Buchmann J, Wang W, Xu J, Holmes EC, Zhang YZ (2016) Redefining the invertebrate RNA virosphere. Nature 540:539–543
        doi: 10.1038/nature20167

    97. Shi Y, Zheng K, Li X, Li L, Li S, Ma J, Dai J, Ji J, Yuan S, Lu H, Li J, Sun F, Xu X, Huang J (2017) Isolation and phylogenetic study of Rift Valley fever virus from the first imported case to China. Virol Sin 32(3):253–256
        doi: 10.1007/s12250-017-3949-z

    98. Solomon T, Ni H (2003) Origin and evolution of Japanese encephalitis virus in southeast Asia. J Virol 77:3091–3098
        doi: 10.1128/JVI.77.5.3091-3098.2003

    99. Solomon T, Dung NM, Kneen R, Gainsborough M, Vaughn DW, Khanh VT (2000) Japanese encephalitis. J Neurol Neurosurg Psychiatry 68:405–415
        doi: 10.1136/jnnp.68.4.405

    100. Song S, Li Y, Fu S, Liu H, Li X, Gao X, Xu Z, Liu G, Wang D, Tian Z, Zhou J (2017) Could Zika virus emerge in Mainland China? Virus isolation from nature in Culex quinquefasciatus, 2016. Emerg Microbes Infect 6:e93
        doi: 10.1038/emi.2017.80

    101. Su S, Qiu X, Zhou J (2016) Spread of ZIKV and YFV to China: potential implications. J Infect 73:289–291
        doi: 10.1016/j.jinf.2016.06.004

    102. Sun XH, Fu SH, Gong Z, Ge J, Meng W, Feng Y, Wang J, Zhai Y, Wang HH, Nasci RS, Tang Q, Liang GD (2009a) Distribution of arboviruses and mosquitoes in Northwestern Yunnan Province, China. Vector-Borne Zoonotic Dis 9:623–630
        doi: 10.1089/vbz.2008.0145

    103. Sun XH, Meng WS, Fu SH, Feng Y, Zhai YG, Wang JL, Wang HQ, Lv XJ, Liang GD (2009b) The first report of Kadipiro virus isolation in China. Chin J Virol 25:173–177

    104. Sun JM, Lin JF, Yan JY, Fan WZ, Lu L, Lv HK, Hou J, Ling F, Fu T, Chen ZP, Cong LM, Liu QY, Zhang YJ, Chai CL (2011) Dengue virus serotype 3 subtype Ⅲ, Zhejiang Province, China. Emerg Infect Dis 17:321–323
        doi: 10.3201/eid1702.100396

    105. Sun Y, Yan J, Mao H, Zhang L, Lyu Q, Wu Z, Zheng W, Feng C, Zhang Y (2013) Characterization of the complete genome of chikungunya in Zhejiang, China, using a modified virus discovery method based on cDNA-AFLP. PLoS ONE 8:e83014
        doi: 10.1371/journal.pone.0083014

    106. Takhampunya R, Kim HC, Tippayachai B, Lee DK, Lee WJ, Chong ST, Kim MS, Lee JS, Klein TA (2014) Distribution and mosquito hosts of Chaoyang virus, a newly reported flavivirus from the Republic of Korea, 2008–2011. J Med Entomol 51:464–474
        doi: 10.1603/ME13033

    107. Tang Y, Gao X, Diao Y, Feng Q, Chen H, Liu X, Ge P, Yu C (2013) Tembusu virus in Human, China. Transbound Emerg Dis 60:193–196
        doi: 10.1111/tbed.2013.60.issue-3

    108. Tang Y, Diao Y, Chen H, Ou Q, Liu X, Gao X, Yu C, Wang L (2015) Isolation and genetic characterization of a Tembusu virus strain isolated from mosquitoes in Shandong, China. Transbound Emerg Dis 62:209–216
        doi: 10.1111/tbed.2015.62.issue-2

    109. Tao S, Chen B (2005) Studies of Coltivirus in China. Chin Med J 118:581–586

    110. Taylor RM, Hurlbut HS, Work TH, Kingston JR, Frothingham TE (1955) Sindbis virus: a newly recognized arthropodtransmitted virus. Am J Trop Med Hyg 4:844–862
        doi: 10.4269/ajtmh.1955.4.844

    111. Thuy NT, Huy TQ, Nga PT, Morita K, Dunia I, Benedetti L (2013) A new nidovirus (NamDinh virus NDiV): its ultrastructural characterization in the C6/36 mosquito cell line. Virology 444:337–342
        doi: 10.1016/j.virol.2013.06.030

    112. Wang HY, Takasaki T, Fu SH, Sun XH, Zhang HL, Wang ZX, Hao ZY, Zhang JK, Tang Q, Kotaki A, Tajima S, Liang XF, Yang WZ, Kurane I, Liang GD (2007) Molecular epidemiological analysis of Japanese encephalitis virus in China. J Gen Virol 88:885–894
        doi: 10.1099/vir.0.82185-0

    113. Wang JL, Zhang HL, Che YC, Wang LC, Ma SH, Liu LD, Liao Y, Li QH (2008) Isolation and complete genomic sequence analysis of a new Sindbis-like virus. Virol Sin 23:31–36
        doi: 10.1007/s12250-008-2891-5

    114. Wang FT, Lv Z, Wang JL, Fu SH, Zhang HL, Wang ZY, Liang GD (2009) Sequencing and analysis of the full coding sequence of Batai virus isolated in China. Chin J Virol 25:83–87

    115. Wang HY, Li YX, Liang XF, Liang GD (2009) Japanese encephalitis in mainland China. Jpn J Infect Dis 62:331–336

    116. Wang ZS, An SY, Wang Y, Han Y, Guo JQ (2009) A new virus of flavivirus: Chaoyang virus isolated in Liaoning Province. Chin Pub Heal 25:769–772

    117. Wang JL, Zhang HL, Sun XH, Fu SH, Wang HQ, Feng Y, Wang HY, Tang Q, Liang GD (2011) Distribution of mosquitoes and mosquito-borne arboviruses in Yunnan Province near the ChinaMyanmar-Laos border. Am J Trop Med Hyg 84:738–746
        doi: 10.4269/ajtmh.2011.10-0294

    118. Wang HY, Fu SH, Liu GF, Liu H, Gao XY, Song LZ, Simon R, Xu AQ, Liang GD (2012) Isolation and identification of a distinct strain of Culex Flavivirus from mosquitoes collected in Mainland China. Virol J 9:73
        doi: 10.1186/1743-422X-9-73

    119. Wang J, Li H, He Y, Zhou Y, Meng J, Zhu W, Chen H, Liao D, Man Y (2015) Isolation and genetic characterization of Mangshi virus: a newly discovered Seadornavirus of the Reoviridae family found in Yunnan Province, China. PLoS ONE 10:e0143601
        doi: 10.1371/journal.pone.0143601

    120. Wang W, Yu B, Lin XD, Kong DG, Wang J, Tian JH, Li MH, Holmes EC, Zhang YZ (2015) Reemergence and autochthonous transmission of Dengue virus, Eastern China, 2014. Emerg Infect Dis J 21:1670–1673
        doi: 10.3201/eid2109.150622

    121. Wang YJ, Xia H, Zhang B, Liu XY, Yuan ZM (2017) Isolation and characterization of a novel mesonivirus from Culex mosquitoes in China. Virus Res 240:130–139
        doi: 10.1016/j.virusres.2017.08.001

    122. Wasserman S, Tambyah PA, Lim PL (2016) Yellow fever cases in Asia: primed for an epidemic. Int J Infect Dis 48:98–103
        doi: 10.1016/j.ijid.2016.04.025

    123. Wu JY, Lun ZR, James A, Chen XG (2010) Dengue fever in mainland China. Am J Trop Med Hyg 83:664–671
        doi: 10.4269/ajtmh.2010.09-0755

    124. Wu D, Wu J, Zhang Q, Zhong H, Ke C, Deng X, Guan D, Li H, Zhang Y, Zhou H, He J, Li L, Yang X (2012) Chikungunya outbreak in Guangdong Province, China, 2010. Emerg Infect Dis J 18:493–495
        doi: 10.3201/eid1803.110034

    125. Xing S, Guo X, Zhang X, Zhao Q, Li L, Zuo S, An X, Pei G, Sun Q, Cheng S, Wang Y, Fan H, Mi Z, Huang Y, Zhang Z, Zhou H, Zhang J, Tong Y (2017) A novel mosquito-borne reassortant orbivirus isolated from Xishuangbanna, China. Virol Sin 32:159–162
        doi: 10.1007/s12250-016-3886-2

    126. Xiong YQ, Chen Q (2014) Epidemiology of dengue fever in China since 1978. J South Med Univ 34:1822–1825 (In Chinese)

    127. Xu PT, Wang YM, Zuo JM, Lin JW, Xu PM (1990) New Orbiviruses isolated from patients with unknown fever and encephalitis in Yunnan province. Chin J Virol 6:27–33

    128. Yan JY, Zhang YJ, Mao HY, Lin JF, Chen JH, Ling F, Wang XY, Lu YY (2010) Diagnosis of a dengue fever outbreak in Yiwu city, Zhejiang province in 2009 and its molecular tracing of the pathogen. Zhonghua Yu Fang Yi Xue Za Zhi 44:1091–1096

    129. Yan P, Zhao Y, Zhang X, Xu D, Dai X, Teng Q, Yan L, Zhou J, Ji X, Zhang S, Liu G, Zhou Y, Kawaoka Y, Tong G, Li Z (2011) An infectious disease of ducks caused by a newly emerged Tembusu virus strain in mainland China. Virology 417:1–8
        doi: 10.1016/j.virol.2011.06.003

    130. Yang M, Jiang J, Guo X, Wu C, Zhou H (2015) Epidemiological analysis and investigation of dengue fever in Yunnan province from 2009 to 2014. J Pathog Biol 10:738–742

    131. Ye X, Fu S, Gao X, Zhao S, Liu C, Wang H, Wu S, Liang G (2012) Investigation of infection with Barmah Forest virus and Ross River virus in Guizhou province, China. Chin J Vect Bio Co 23:428–431

    132. Yu W, Mengersen K, Dale P, Mackenzie JS, Toloo GS, Wang X, Tong S (2014) Epidemiologic patterns of Ross River virus disease in Queensland, Australia, 2001–2011. Am J Trop Med Hyg 91:109–118
        doi: 10.4269/ajtmh.13-0455

    133. Zanluca C, Duarte CN, Santos D (2016) Zika virus—an overview. Microbes Infect 18:295–301
        doi: 10.1016/j.micinf.2016.03.003

    134. Zhai YG, Wang HY, Sun XH, Fu SH, Wang HQ, Attoui H, Tang Q, Liang GD (2008a) Complete sequence characterization of isolates of Getah virus (genus alphavirus, family Togaviridae) from China. J Gen Virol 89:1446–1456
        doi: 10.1099/vir.0.83607-0

    135. Zhai YG, Lv XJ, Sun XH, Fu SH, Gong ZD, Fen Y, Tong SX, Wang ZX, Tang Q, Attoui H, Liang GD (2008b) Isolation and characterization of the full coding sequence of a novel densovirus from the mosquito Culex pipiens pallens. J Gen Virol 89:195–199
        doi: 10.1099/vir.0.83221-0

    136. Zhang HL, Liang GD (2012) Arboviruses and arboviral diseases in China. Chin J Vector Biol Control 23:377–380

    137. Zhang QL, He JF, Wu D, Wang ZJ, Zhong XG, Zhong HJ, Ding F, Liu ZQ, Wang SW, Huang ZY, Zhang YH, Ke CW, Yuan DK, Liang WJ, Li DQ, Chen PH (2012) Maiden outbreak of chikungunya in Dongguan city, Guangdong province, China: epidemiological characteristics. PLoS ONE 7:e42830
        doi: 10.1371/journal.pone.0042830

    138. Zhang FC, Zhao H, Li LH, Jiang T, Hong WX, Wang J, Zhao LZ, Yang HQ, Ma DH, Bai CH, Shan XY, Deng YQ, Qin CF (2014) Severe dengue outbreak in Yunnan, China, 2013. Int J Infect Dis 27:4–6
        doi: 10.1016/j.ijid.2014.03.1392

    139. Zhang Y, Chen W, Wong G, Bi Y, Yan J, Sun Y, Chen E, Yan H, Lou X, Mao H, Xia S, Gao GF, Shi W, Chen Z (2016) Highly diversified Zika viruses imported to China, 2016. Protein Cell 7:461–464
        doi: 10.1007/s13238-016-0274-5

    140. Zhang W, Chen S, Mahalingam S, Wang M, Cheng A (2017) An updated review of avian-origin Tembusu virus: a newly emerging avian Flavivirus. J Gen Virol 98:2413–2420
        doi: 10.1099/jgv.0.000908

    141. Zhao C, Jiang L, Yu X, Chen W (1997) Isolation of Ross River virus and its antibody Prevalence in Hainan Province. Chin J Vet Sci 17:241–243

    142. Zhao Y, Li L, Ma D, Luo J, Ma Z, Wang X, Pan Y, Chen J, Xi J, Yang J, Qiu L, Bai C, Jiang L, Shan X, Sun Q (2016) Molecular characterization and viral origin of the 2015 dengue outbreak in Xishuangbanna, Yunnan, China. Sci Rep 6:34444
        doi: 10.1038/srep34444

    143. Zheng K, Li J, Zhang Q, Liang M, Li C, Lin M, Huang J, Li H, Xiang D, Wang N, Hong Y, Huang L, Li X, Pan D, Song W, Dai J, Guo B, Li D (2010) Genetic analysis of chikungunya viruses imported to mainland China in 2008. Virol J 7:8
        doi: 10.1186/1743-422X-7-8

    144. Zheng Y, Cao Y, Fu S, Cheng J, Zhao J, Dai P, Kong X, Liang G (2015) Isolation and identification of mosquito-borne Arboviruses in Yuncheng city, Shanxi province, 2012. Zhonghua Liu Xing Bing Xue Za Zhi 36:368–373

    145. Zhou G, Liang G, Li L (1999) Complete nucleotide sequence of the nonstructural gene of alphavirus YN87448 strain isolated in China and its relationship to other Sindbis viruses. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 13:314–320

    146. Zhou J, Jin Y, Chen Y, Li J, Zhang Q, Xie X, Gan L, Liu Q (2017) Complete genomic and ultrastructural analysis of a Nam Dinh virus isolated from Culex pipiens quinquefasciatus in China. Sci Rep 7:271
        doi: 10.1038/s41598-017-00340-3

    147. Zuo S, Zhao Q, Guo X, Zhou H, Cao W, Zhang J (2014) Detection of Quang Binh virus from mosquitoes in China. Virus Res 180:31–38
        doi: 10.1016/j.virusres.2013.12.005

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    Mosquito-Associated Viruses in China

      Corresponding author: Zhiming Yuan, yzm@wh.iov.cn
    • 1. Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan 430071, China
    • 2. University of Chinese Academy of Sciences, Beijing 100049, China

    Abstract: Mosquitoes are classified into approximately 3500 species and further grouped into 41 genera. Epidemiologically, they are considered to be among the most important disease vectors in the world and they can harbor a wide variety of viruses. Several mosquito viruses are considered to be of significant medical importance and can cause serious public health issues throughout the world. Such viruses are Japanese encephalitis virus (JEV), dengue virus (DENV), chikungunya virus (CHIKV), and Zika virus (ZIKV). Others are the newly recognized mosquito viruses such as Banna virus (BAV) and Yunnan orbivirus (YNOV) with unclear medical significance. The remaining mosquito viruses are those that naturally infect mosquitoes but do not appear to infect humans or other vertebrates. With the continuous development and improvement of mosquito and mosquito-associated virus surveillance systems in China, many novel mosquito-associated viruses have been discovered in recent years. This review aims to systematically outline the history, characteristics, distribution, and/or current epidemic status of mosquito-associated viruses in China.