ZIKA virus isolated from mosquitoes: a field and laboratory investigation in China, 2016

Abstract

A field investigation of arboviruses was conducted in Dejiang, Guizhou Province in the summer of 2016. A total of 8,795 mosquitoes, belonging to four species of three genera, and 1,300 midges were collected. The mosquito samples were identified on site according to their morphology, and the pooled samples were ground and centrifuged in the laboratory. The supernatant was incubated with mosquito tissue culture cells (C6/36) and mammalian cells (BHK-21) for virus isolation. The results indicated that 40% (3,540/8,795) were Anopheles sinensis, 30% (2,700/8,795) were Culex pipiens quinquefasciatus, and 29% (2,530/8,795) were Armigeres subbalbeatus. Furthermore, a total of eight virus isolates were obtained, and genome sequencing revealed two Zika viruses (ZIKVs) isolated from Culex pipiens quinquefasciatus and Armigeres subbalbeatus, respectively; three Japanese encephalitis viruses (JEVs) isolated from Culex pipiens quinquefasciatus; two Banna viruses (BAVs) isolated from Culex pipiens quinquefasciatus and Anopheles sinensis, respectively; and one densovirus (DNV) isolated from Culex pipiens quinquefasciatus. The ZIKVs isolated from the Culex pipiens quinquefasciatus and Armigeres subbalbeatus mosquitoes represent the first ZIKV isolates in mainland China. This discovery presents new challenges for the prevention and control of ZIKV in China, and prompts international cooperation on this global issue.

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References

  1. Attoui, H., Mohd Jaafar, F., de Micco, P., and de Lamballerie, X. (2005). Coltiviruses and seadornaviruses in North America, Europe, and Asia. Emerg Infect Dis 11, 1673–1679.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Cao-Lormeau, V.M., Blake, A., Mons, S., Lastère, S., Roche, C., Vanhomwegen, J., Dub, T., Baudouin, L., Teissier, A., Larre, P., Vial, A.L., Decam, C., Choumet, V., Halstead, S.K., Willison, H.J., Musset, L., Manuguerra, J.C., Despres, P., Fournier, E., Mallet, H.P., Musso, D., Fontanet, A., Neil, J., and Ghawché, F. (2016). Guillain-Barré Syndrome outbreak associated with Zika virus infection in French Polynesia: a case-control study. Lancet 387, 1531–1539.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Diallo, D., Sall, A.A., Diagne, C.T., Faye, O., Faye, O., Ba, Y., Hanley, K.A., Buenemann, M., Weaver, S.C., and Diallo, M. (2014). Zika virus emergence in mosquitoes in southeastern Senegal, 2011. PLoS ONE 9, e109442.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Deng, Y.Q., Zhao, H., Li, X.F., Zhang, N.N., Liu, Z.Y., Jiang, T., Gu, D.Y., Shi, L., He, J.A., Wang, H.J., Sun, Z.Z., Ye, Q., Xie, D.Y., Cao, W.C., and Qin, C.F. (2016). Isolation, identification and genomic characterization of the Asian lineage Zika virus imported to China. Sci China Life Sci 59, 428–430.

    Article  PubMed  Google Scholar 

  5. Enserink, M. (2015). An obscure mosquito-borne disease goes global. Science 350, 1012–1013.

    CAS  Article  PubMed  Google Scholar 

  6. Franca, R.F.O., Neves, M.H.L., Ayres, C.F.J., Melo-Neto, O.P., and Filho, S.P.B. (2016). First International Workshop on Zika Virus Held by Oswaldo Cruz Foundation FIOCRUZ in Northeast Brazil March 2016—A Meeting Report. PLoS Negl Trop Dis 10, e0004760.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Gould, E., Pettersson, J., Higgs, S., Charrel, R., and de Lamballerie, X. (2017). Emerging arboviruses: why today? One Health 4, 1–13.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Gao, X., Nasci, R., and Liang, G. (2010). The neglected arboviral infections in mainland China. PLoS Negl Trop Dis 4, e624.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Guedes, D.R., Paiva, M.H., Donato, M.M., Barbosa, P.P., Krokovsky, L., Rocha, S.W.D.S., Saraiva, K.L., Crespo, M.M., Rezende, T.M., Wallau, G.L., Barbosa, R.M., Oliveira, C.M., Melo-Santos, M.A., Pena, L., Cordeiro, M.T., Franca, R.F.O., Oliveira, A.L., Peixoto, C.A., Leal, W.S., and Ayres, C.F. (2017). Zika virus replication in the mosquito Culex quinquefasciatus in Brazil. Emerg Microbes Infect 6, e69.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Guo, X.X., Li, C.X., Deng, Y.Q., Xing, D., Liu, Q.M., Wu, Q., Sun, A.J., Dong, Y., Cao, W.C., Qin, C.F., and Zhao, T.Y. (2016). Culex pipiens quinquefasciatus: a potential vector to transmit Zika virus. Emerg Microbes Infect 5, e102.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hills, S.L., and Phillips, D.C. (2009). Past, present, and future of Japanese encephalitis. Emerg Infect Dis 15, 1333–1333.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Kumar, S., Stecher, G., and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33, 1870–1874.

    CAS  Article  PubMed  Google Scholar 

  13. Karabatsos, N. (1985). International Catalogue of Arthropod-Borne Viruses. 3rd ed. (San Antonio (TX): American Society for Tropical Medicine and Hygiene).

    Google Scholar 

  14. Li, M.H., Fu, S.H., Feng, Y., Ye, X.F., Zhao, S.Y., Liu, C.T., and Liang, G.D. (2012). Investigation of arboviruses in different regions of Guizhou province, China in 2008 (in Chinese). Chin J Vector Biol Control 23, 417–420.

    Google Scholar 

  15. Li, J., Xiong, Y., Wu, W., Liu, X., Qu, J., Zhao, X., Zhang, S., Li, J., Li, W., Liao, Y., Gong, T., Wang, L., Shi, Y., Xiong, Y., Ni, D., Li, Q., Liang, M., Hu, G., and Li, D. (2016a). Zika virus in a traveler returning to China from Caracas, Venezuela, February 2016. Emerg Infect Dis 22, 1133–1136.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Li, X.F., Han, J.F., Shi, P.Y., and Qin, C.F. (2016b). Zika virus: a new threat from mosquitoes. Sci China Life Sci 59, 440–442.

    Article  PubMed  Google Scholar 

  17. Liu, H., Li, M.H., Zhai, Y.G., Meng, W.S., Sun, X.H., Cao, Y.X., Fu, S.H., Wang, H.Y., Xu, L.H., Tang, Q., and Liang, G.D. (2010). Banna Virus, China, 1987–2007. Emerg Infect Dis 16, 514–517.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Liu, H., Shen, L., Zhang, X.L., Li, X.L., Liang, G.D., and Ji, H.F. (2016a). From discovery to outbreak: the genetic evolution of the emerging Zika virus. Emerg Microbes Infect 5, e111.

    Article  PubMed  PubMed Central  Google Scholar 

  19. Liu, H., Gao, X.Y., Fu, S.H., Li, M.H., Zhai, Y.G., Meng, W.S., Sun, X.H., Lv, Z., Wang, H.Y., Shen, X.X., Cao, Y.X., He, Y., and Liang, G.D. (2016b). Molecular evolution of emerging Banna virus. Infect Genet Evol 45, 250–255.

    CAS  Article  PubMed  Google Scholar 

  20. Liu, Y., Liu, J., Du, S., Shan, C., Nie, K., Zhang, R., Li, X.F., Zhang, R., Wang, T., Qin, C.F., Wang, P., Shi, P.Y., and Cheng, G. (2017a). Evolutionary enhancement of Zika virus infectivity in Aedes aegypti mosquitoes. Nature 545, 482–486.

    CAS  Article  PubMed  Google Scholar 

  21. Liu, Z., Zhou, T., Lai, Z., Zhang, Z., Jia, Z., Zhou, G., Williams, T., Xu, J., Gu, J., Zhou, X., Lin, L., Yan, G., and Chen, X.G. (2017b). Competence of Aedes aegypti, Ae. albopictus, and Culex quinquefasciatus mosquitoes as Zika Virus Vectors, China. Emerg Infect Dis 23, 1085–1091.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Lourenço-de-Oliveira, R., and Failloux, A.B. (2017). Lessons learned on Zika virus vectors. PLoS Negl Trop Dis 11, e0005511.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Liang, G., Gao, X., and Gould, E.A. (2015). Factors responsible for the emergence of arboviruses; strategies, challenges and limitations for their control. Emerg Microbes Infect 4, e18.

    Article  PubMed  PubMed Central  Google Scholar 

  24. Lu, Z., Fu, S.H., Cao, L., Tang, C.J., Zhang, S., Li, Z.X., Tusong, M., Yao, X.H., Zhang, H.L., Wang, P.Y., Wumaier, M., Yuan, X.Y., Li, M.H., Zhu, C.Z., Fu, L.P., and Liang, G.D. (2011). Human infection with West Nile Virus, Xinjiang, China, 2011. Emerg Infect Dis 20, 1421–1423.

    Article  Google Scholar 

  25. Mackenzie, J.S., Gubler, D.J., and Petersen, L.R. (2004). Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med 10, S98–S109.

    CAS  Article  PubMed  Google Scholar 

  26. Mlakar, J., Korva, M., Tul, N., Popović, M., Poljšak-Prijatelj, M., Mraz, J., Kolenc, M., Resman Rus, K., Vesnaver Vipotnik, T., Fabjan Vodušek, V., Vizjak, A., Pižem, J., Petrovec, M., and Avšič Županc, T. (2016). Zika virus associated with microcephaly. N Engl J Med 374, 951–958.

    CAS  Article  PubMed  Google Scholar 

  27. National Health and Family Planning Commission (NHFPC), Notification about the release of national strategy for prevention and control of ZIKV infection in China. (2016). Beijing: National Health and Family Planning Commission.

  28. Ogden, S.C., Hammack, C., and Tang, H. (2016). Zika virus and neural developmental defects: building a case for a cause. Sci China Life Sci 59, 536–538.

    Article  PubMed  Google Scholar 

  29. Pettersson, J.H.O., Eldholm, V., Seligman, S.J., Lundkvist, Å., Falconar, A.K., Gaunt, M.W., Musso, D., Nougairède, A., Charrel, R., Gould, E.A., and de Lamballerie, X. (2016). How did Zika Virus emerge in the Pacific Islands and Latin America? mBio 7, e01239-16–16.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Qin, X.F. (2016). Understanding the pathogenic evolution of Zika virus. Sci China Life Sci 59, 737–739.

    Article  PubMed  Google Scholar 

  31. Rahman, N.A., and Huhtaniemi, I. (2017). Zika virus infection—do they also endanger male fertility? Sci China Life Sci 60, 324–325.

    Article  PubMed  Google Scholar 

  32. Song, S., Li, Y., Fu S., Liu, H., Li, X., Gao, X., Xu, Z., Liu, G., Wang, D., Tian, Z., Zhou, J., He, Y., Lei, W., Wang, H., Wang, B., Lu, X., and Liang, G. (2017). Could Zika virus emerge in mainland China? Virus isolation from nature in Culex quinquefasciatus, 2016. Emerg Microbes Infect 6, e94.

    Article  Google Scholar 

  33. Su, S., Qiu, X., and Zhou, J. (2016). Spread of ZIKV and YFV to China: potential implications. J Infect 73, 289–291.

    Article  PubMed  Google Scholar 

  34. Wang, L., Fu, S., Zhang, H., Ye, X., Yu, D., Deng, Z., Yuan, J., Zhai, Y., Li, M., Lv, Z., Chen, W., Jiang, H., Gao, X., Cao, Y., Wang, H., Tang, Q., and Liang, G. (2010). Identification and isolation of Genotype-I Japanese Encephalitis virus from encephalitis patients. Virol J 7, 345.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Wang, H., Feng, Y., Wang, J., Zhang, H., Liang, G.D., Sun, X., Fu, S., Wang, H., and Tang, Q. (2011). Distribution of mosquitoes and mosquito-borne arboviruses in Yunnan Province near the China-Myanmar-Laos border. Am J Trop Med Hyg 84, 738–746.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Wang, H.Y., Takasaki, T., Fu, S.H., Sun, X.H., Zhang, H.L., Wang, Z.X., Hao, Z.Y., Zhang, J.K., Tang, Q., Kotaki, A., Tajima, S., Liang, X.F., Yang, W.Z., Kurane, I., and Liang, G.D. (2007). Molecular epidemiological analysis of Japanese encephalitis virus in China. J Gen Virol 88, 885–894.

    CAS  Article  PubMed  Google Scholar 

  37. Weaver, S.C., and Reisen, W.K. (2010). Present and future arboviral threats. Antiviral Res 85, 328–345.

    CAS  Article  PubMed  Google Scholar 

  38. WHO Strengthening implementation of the global strategy for dengue fever/dengue haemorrhagic fever prevention and control. Report of the Informal Consultation. Geneva: World Health Organization.

  39. Ye, C., Lan, R., Xia, S., Zhang, J., Sun, Q., Zhang, S., Jing, H., Wang, L., Li, Z., Zhou, Z., Zhao, A., Cui, Z., Cao, J., Jin, D., Huang, L., Wang, Y., Luo, X., Bai, X., Wang, Y., Wang, P., Xu, Q., and Xu, J. (2010). Emergence of a new multidrug-resistant serotype X variant in an epidemic clone of Shigella flexneri. J Clin Microbiol 48, 419–426.

    CAS  Article  PubMed  Google Scholar 

  40. Ye, X., Fu, S., Gao, X., Zhao, S., Liu, C., Wang H., Wu, S., and Liang, G. (2012). Investigation of infection with Barmah Forest virus and Ross River virus in Guizhou province, China (in Chinese). Chin J Vector Biol Control 23, 428–431.

    Google Scholar 

  41. Zhang, J., Wang, J., Wang, L., Fu, S., Li, M., Zhao, G., Zhu, W., Wang, D., and Liang, G. (2014). Molecular characterization and seroprevalence in pigs of SC0806, a cat que virus isolated from mosquitoes in Sichuan province, China. Vector-Borne Zoonotic Dis 15, 423–431.

    CAS  Article  Google Scholar 

  42. Zhai, Y.G., Lv, X.J., Sun, X.H., Fu, S.H., Gong, Z., Fen, Y., Tong, S.X., Wang, Z.X., Tang, Q., Attoui, H., and Liang, G.D. (2008). Isolation and characterization of the full coding sequence of a novel densovirus from the mosquito Culex pipiens pallens. J Gen Virol 89, 195–199.

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

We appreciate the help provided by the staff of Dejiang County CDC during the collection of mosquito samples. This work was supported by the National Natural Science Foundation of China (81290342, 81501757), the Special National Project on Research and Development of Key Biosafety Technologies (2016YFC1201904), the National Key Plan for Scientific Research and Development of China (2016YFD0500300), the Development Grants of State Key Laboratory of Infectious Disease Prevention and Control (2014SKLID103, 2015SKLID505), the National Key Research and Development Program of China (2017YFC1200202) and the Open Research Fund Program of Wuhan National Bio-Safety Level 4 Lab of CAS (2017SPCAS003).

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Correspondence to Xiaoqing Lu or Guodong Liang.

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Fu, S., Song, S., Liu, H. et al. ZIKA virus isolated from mosquitoes: a field and laboratory investigation in China, 2016. Sci. China Life Sci. 60, 1364–1371 (2017). https://doi.org/10.1007/s11427-017-9196-8

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Keywords

  • arbovirus surveillance
  • mosquito-borne arbovirus
  • Japanese encephalitis virus
  • Zika virus