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Commentary: Diversity, Geography, and Host Range of Emerging Mosquito-Associated Viruses — China, 2010–2020

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  • Funding: The Special Foundation of Basic Science and Technology Resources Survey of Ministry of Science and Technology of China (No. 2017FY101200); The Open Project of Key Laboratory of Parasite and Vector Biology, China Ministry of Health (No. WSBKFKT-201804); and The Fifth Round of Three-Year Public Health Action Plan of Shanghai (No. GWV-10.1-XK13)
  • [1] Cuervo-Parra JA, Cortés TR, Ramirez-Lepe M. Mosquito-borne diseases, pesticides used for mosquito control, and development of resistance to insecticides. In: Trdan S, editor. Insecticides resistance. Rijcka: IntechOpen, 2016, 111-34. https://www.intechopen.com/chapters/49257.https://www.intechopen.com/chapters/49257
    [2] Castro MC, Wilson ME, Bloom DE. Disease and economic burdens of dengue. Lancet Infect Dis 2017;17(3):e70-8. http://dx.doi.org/10.1016/S1473-3099(16)30545-XCrossRef
    [3] Puntasecca CJ, King CH, LaBeaud AD. Measuring the global burden of chikungunya and Zika viruses: a systematic review. PLoS Negl Trop Dis 2021;15(3):e0009055. http://dx.doi.org/10.1371/journal.pntd.0009055CrossRef
    [4] Pielnaa P, Al-Saadawe M, Saro A, Dama MF, Zhou M, Huang YX, et al. Zika virus-spread, epidemiology, genome, transmission cycle, clinical manifestation, associated challenges, vaccine and antiviral drug development. Virology 2020;543:34-42. http://dx.doi.org/10.1016/j.virol.2020.01.015CrossRef
    [5] Wilder-Smith A, Chang CR, Leong WY. Zika in travellers 1947–2017: a systematic review. J Travel Med 2018;25(1):1-10. http://dx.doi.org/10.1093/jtm/tay044CrossRef
    [6] Wang J, Xu HB, Song S, Cheng R, Fan N, Fu SH, et al. Emergence of Zika Virus in Culex tritaeniorhynchus and Anopheles sinensis mosquitoes in China. Virol Sin 2021;36(1):33-42. http://dx.doi.org/10.1007/s12250-020-00239-wCrossRef
    [7] Zhou CM, Liu JW, Qi R, Fang LZ, Qin XR, Han HJ, et al. Emergence of Zika virus infection in China. PLoS Negl Trop Dis 2020;4(5):e0008300. http://dx.doi.org/10.1371/journal.pntd.0008300CrossRef
    [8] Su JL, Li S, Hu XD, Yu XL, Wang YY, Liu PP, et al. Duck egg-drop syndrome caused by BYD virus, a new Tembusu-related flavivirus. PLoS One 2011;6(3):e18106. http://dx.doi.org/10.1371/journal.pone.0018106CrossRef
    [9] Yu GL, Lin Y, Tang Y, Diao YX. Evolution of Tembusu virus in ducks, chickens, geese, sparrows, and mosquitoes in Northern China. Viruses 2018;10(9):485. http://dx.doi.org/10.3390/v10090485CrossRef
    [10] Fang Y, Zhang W, Xue JB, Zhang Y. Monitoring mosquito-borne arbovirus in various insect regions in China in 2018. Front Cell Infect Microbiol 2021;11:640993. http://dx.doi.org/10.3389/fcimb.2021.640993CrossRef
    [11] Yang T, Li R, Hu Y, Yang L, Zhao D, Du L, et al. An outbreak of Getah virus infection among pigs in China, 2017. Transbound Emerg Dis 2018;65(3):632-7. http://dx.doi.org/10.1111/tbed.12867CrossRef
    [12] Prow NA, Mah MG, Deerain JM, Warrilow D, Colmant AMG, O'Brien CA, et al. New genotypes of Liao ning virus (LNV) in Australia exhibit an insect-specific phenotype. J Gen Virol 2018;99(4):596-609. http://dx.doi.org/10.1099/jgv.0.001038CrossRef
    [13] Attoui H, Jaafar FM, Belhouchet M, Tao SJ, Chen BQ, Liang GD, et al. Liao ning virus, a new Chinese seadornavirus that replicates in transformed and embryonic mammalian cells. J Gen Virol 2006;87(Pt 1):199-208. http://dx.doi.org/10.1099/vir.0.81294-0CrossRef
    [14] Moureau G, Cook S, Lemey P, Nougairede A, Forrester NL, Khasnatinov M, et al. New insights into flavivirus evolution, taxonomy and biogeographic history, extended by analysis of canonical and alternative coding sequences. PLoS One 2015;10(2):e0117849. http://dx.doi.org/10.1371/journal.pone.0117849CrossRef
    [15] Fang Y, Zhang Y, Zhou ZB, Shi WQ, Xia S, Li YY, et al. Co-circulation of Aedes flavivirus, Culex flavivirus, and Quang Binh virus in Shanghai, China. Infect Dis Poverty 2018;7:75. http://dx.doi.org/10.1186/s40249-018-0457-9CrossRef
    [16] Fang Y, Li XS, Zhang W, Xue JB, Wang JZ, Yin SQ, et al. Molecular epidemiology of mosquito-borne viruses at the China-Myanmar border: discovery of a potential epidemic focus of Japanese encephalitis. Infect Dis Poverty 2021;10(1):57. http://dx.doi.org/10.1186/s40249-021-00838-zCrossRef
    [17] Patterson EI, Villinger J, Muthoni JN, Dobel-Ober L, Hughes GL. Exploiting insect-specific viruses as a novel strategy to control vector-borne disease. Curr Opin Insect Sci 2020;39:50-6. http://dx.doi.org/10.1016/j.cois.2020.02.005CrossRef
    [18] Newman CM, Cerutti F, Anderson TK, Hamer GL, Walker ED, Kitron UD, et al. Culex flavivirus and West Nile virus mosquito coinfection and positive ecological association in Chicago, United States. Vector Borne Zoonotic Dis 2011;11(8):1099-105. http://dx.doi.org/10.1089/vbz.2010.0144CrossRef
    [19] Goenaga S, Kenney JL, Duggal NK, Delorey M, Ebel GD, Zhang B, et al. Potential for Co-infection of a mosquito-specific flavivirus, Nhumirim Virus, to block West Nile virus transmission in mosquitoes. Viruses 2015;7(11):5801-12. http://dx.doi.org/10.3390/v7112911CrossRef
    [20] Romo H, Kenney JL, Blitvich BJ, Brault AC. Restriction of Zika virus infection and transmission in Aedes aegypti mediated by an insect-specific flavivirus. Emerg Microbes Infect 2018;7(1):181. http://dx.doi.org/10.1038/s41426-018-0180-4CrossRef
    [21] Farfan-Ale JA, Loroño-Pino MA, Garcia-Rejon JE, Hovav E, Powers AM, Lin M, et al. Detection of RNA from a novel West Nile-like virus and high prevalence of an insect-specific flavivirus in mosquitoes in the Yucatan Peninsula of Mexico. Am J Trop Med Hyg 2009;80(1):85-95. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2663380/.CrossRef
  • FIGURE 1.  Geographic distribution and diversity of insect specific flaviviruses in China by 2020.

    Abbreviations: AAFV=Anopheles associated flavivirus; AeFV=Aedes flavivirus; CHAOV=Chaoyang virus; CTFV=Culex theileri flavivirus; CxFV=Culex flavivirus; HANKV=Hanko virus; QBV=Quang Binh flavivirus; YDFV=Yamadai flavivirus; YNCxFV=Yunnan Culex flavivirus.

    TABLE 1.  Vectors, hosts, geographic distributions, and collection years of emerging mosquito-associated viruses in China (2010–2020).

    VirusVectorVertebrate hostDistribution (year)
    ZIKVArmigeres subalbatus
    Culex quinquefasciatus
    Cx. tritaeniorhynchus
    Anopheles sinensis
    HumanGuizhou (2016); Jiangxi (2018); Yunnan (2016)
    TMUVCx. pipiens
    Cx. tritaeniorhynchus
    Cx. annulus
    Duck
    Goose
    Chicken
    Sparrow
    Pigeon
    Anhui (2013); Beijing (2010); Chongqing (2013); Fujian (2010); Guangdong (2011–2015); Guangxi (2011); Hebei (2010); Henan (2010); Hubei (2018); Inner Mongolia (2017); Jiangsu (2010, 2012); Jiangxi (2010); Shandong (2010, 2011, 2012, 2016); Shanghai (2010); Zhejiang (2010–2016); Yunnan (2012); Sichuan (2013); Taiwan (2019)
    LNVAedes flavidorsalis
    Ae. caspius
    Cx. pipiens
    Cx. modestus
    Ae. dorsali
    Ae. vexans
    MiceBeijing (2014); Gansu (2011); Jilin (1997); Liaoning (2012); Qinghai (2007); Shanxi (2007); Xinjiang (2005, 2006–2008, 2011)
    GETVCx. tritaeniorhynchus
    Ar. subalbatus
    Cx. pseudovishnui
    Cx. fuscocephala
    Cx. annulus
    An. sinensis
    Cx. pipiens
    Horse
    Swine
    Cattle
    Blue fox
    Anhui (2017); Gansu (2006); Guangdong (2018); Guizhou (2008); Hainan (1964, 2018); Hebei (2002); Henan (2011); Hubei (2010); Hunan (2017); Inner Mongoria (2018); Jilin (2017, 2018); Liaoning (2006); Shandong (2017); Shanghai (2005); Shanxi (2012); Sichuan (2012, 2018); Taiwan (2002); Yunnan (2005, 2007, 2010, 2012)
    CHAOVAe. vexans
    Cx. pipiens
    Liaoning (2008); Inner Mongolia (2018)
    AeFVAe. albopictus
    Hubei (2018); Shanghai (2016); Yunnan (2018)
    CxFVCx. pipiens
    Cx. tritaeniorhynchus
    An. sinensis
    Cx. modestus
    Gansu (2011); Henan (2004); Hubei (2018); Inner Mongolia (2018); Liaoning (2011); Shaanxi (2012); Shandong (2009, 2012, 2018); Shanghai (2016, 2018); Shanxi (2012); Taiwan (2010); Xinjiang (2012)
    QBVCx. tritaeniorhynchus
    Cx. pipiens
    An. sinensis
    Hainan (2018); Hubei (2018); Inner Mongolia (2018); Shandong (2018); Shanghai (2016, 2018)
    Abbreviations: AeFV=Aedes flavivirus; CHAOV=Chaoyang virus; CxFV=Culex flavivirus; GETV=Getah virus; LNV=Liao ning virus; QBV=Quang Binh flavivirus; TMUV=Tembusu virus; ZIKV=Zika virus.
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Diversity, Geography, and Host Range of Emerging Mosquito-Associated Viruses — China, 2010–2020

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  • 1. National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention (Chinese Center for Tropical Diseases Research); NHC Key Laboratory of Parasite and Vector Biology; WHO Collaborating Centre for Tropical Diseases; National Center for International Research on Tropical Diseases, Shanghai, China
  • 2. School of Global Health, Chinese Center for Tropical Diseases Research, Shanghai Jiao Tong University School of Medicine, Shanghai, China
  • 3. School of Publish Health, Weifang Medical University, Weifang, Shandong, China
  • Corresponding author:

    Yi Zhang, zhangyi@nipd.chinacdc.cn

  • Funding: The Special Foundation of Basic Science and Technology Resources Survey of Ministry of Science and Technology of China (No. 2017FY101200); The Open Project of Key Laboratory of Parasite and Vector Biology, China Ministry of Health (No. WSBKFKT-201804); and The Fifth Round of Three-Year Public Health Action Plan of Shanghai (No. GWV-10.1-XK13)
  • Online Date: August 27 2021
    doi: 10.46234/ccdcw2021.184
  • Epidemics of emerging and neglected infectious diseases are severe threats to public health and are largely driven by the promotion of globalization and by international multi-border cooperation. Mosquito-borne viruses are among the most important agents of these diseases, with an associated mortality of over one million people worldwide (1). The well-known mosquito-borne diseases (MBDs) with global scale include malaria, dengue fever, chikungunya, and West Nile fever, which are the largest contributor to the disease burden. However, the morbidity of some MBDs has sharply decreased due to expanded programs on immunization and more efficient control strategies (e.g., for Japanese encephalitis and yellow fever). Nevertheless, the global distribution and burden of dengue fever, chikungunya, and Zika fever are expanding and growing (2-3). Similar to the seemingly interminable coronavirus disease 2019 (COVID-19) pandemic sweeping across the globe since the end of 2020, MBDs could also spread at an unexpected rate (Table 1, Supplementary Table S1) and cause great economic damage.

    VirusVectorVertebrate hostDistribution (year)
    ZIKVArmigeres subalbatus
    Culex quinquefasciatus
    Cx. tritaeniorhynchus
    Anopheles sinensis
    HumanGuizhou (2016); Jiangxi (2018); Yunnan (2016)
    TMUVCx. pipiens
    Cx. tritaeniorhynchus
    Cx. annulus
    Duck
    Goose
    Chicken
    Sparrow
    Pigeon
    Anhui (2013); Beijing (2010); Chongqing (2013); Fujian (2010); Guangdong (2011–2015); Guangxi (2011); Hebei (2010); Henan (2010); Hubei (2018); Inner Mongolia (2017); Jiangsu (2010, 2012); Jiangxi (2010); Shandong (2010, 2011, 2012, 2016); Shanghai (2010); Zhejiang (2010–2016); Yunnan (2012); Sichuan (2013); Taiwan (2019)
    LNVAedes flavidorsalis
    Ae. caspius
    Cx. pipiens
    Cx. modestus
    Ae. dorsali
    Ae. vexans
    MiceBeijing (2014); Gansu (2011); Jilin (1997); Liaoning (2012); Qinghai (2007); Shanxi (2007); Xinjiang (2005, 2006–2008, 2011)
    GETVCx. tritaeniorhynchus
    Ar. subalbatus
    Cx. pseudovishnui
    Cx. fuscocephala
    Cx. annulus
    An. sinensis
    Cx. pipiens
    Horse
    Swine
    Cattle
    Blue fox
    Anhui (2017); Gansu (2006); Guangdong (2018); Guizhou (2008); Hainan (1964, 2018); Hebei (2002); Henan (2011); Hubei (2010); Hunan (2017); Inner Mongoria (2018); Jilin (2017, 2018); Liaoning (2006); Shandong (2017); Shanghai (2005); Shanxi (2012); Sichuan (2012, 2018); Taiwan (2002); Yunnan (2005, 2007, 2010, 2012)
    CHAOVAe. vexans
    Cx. pipiens
    Liaoning (2008); Inner Mongolia (2018)
    AeFVAe. albopictus
    Hubei (2018); Shanghai (2016); Yunnan (2018)
    CxFVCx. pipiens
    Cx. tritaeniorhynchus
    An. sinensis
    Cx. modestus
    Gansu (2011); Henan (2004); Hubei (2018); Inner Mongolia (2018); Liaoning (2011); Shaanxi (2012); Shandong (2009, 2012, 2018); Shanghai (2016, 2018); Shanxi (2012); Taiwan (2010); Xinjiang (2012)
    QBVCx. tritaeniorhynchus
    Cx. pipiens
    An. sinensis
    Hainan (2018); Hubei (2018); Inner Mongolia (2018); Shandong (2018); Shanghai (2016, 2018)
    Abbreviations: AeFV=Aedes flavivirus; CHAOV=Chaoyang virus; CxFV=Culex flavivirus; GETV=Getah virus; LNV=Liao ning virus; QBV=Quang Binh flavivirus; TMUV=Tembusu virus; ZIKV=Zika virus.

    Table 1.  Vectors, hosts, geographic distributions, and collection years of emerging mosquito-associated viruses in China (2010–2020).

  • The Zika virus (ZIKV) causes a traditional mosquito-borne enzootic disease and was first identified in rhesus monkeys in Uganda in 1947, subsequently spreading in Africa, Asia, and the Pacific Islands, and expanding to Brazil in May 2015 (4). China seemed successful in keeping the Zika pandemic at bay with only a few imported cases (5). However, ZIKV was isolated in mosquitoes from Yunnan, Guizhou, and Jiangxi from 2016 to 2018 (6), and 1.8% of healthy individuals in Nanning, China were positive for the ZIKV antibody (7). This suggests the existence of the natural circulation of ZIKV between mosquitoes and humans in China even before the international public health emergency. The sudden outbreak of egg drop syndrome caused by the Tembusu virus (TMUV) quickly swept the coastal provinces and neighboring regions in 2010, resulting in severe economic loss in the poultry industry (8). To date, records of TMUV have covered 18 provinces in China, and are mainly comprised of reports from the last decade (9). Similarly, the Getah virus, which is mainly transmitted between mosquitoes and domestic livestock, has been spreading across China since 2010 (10), with an outbreak on a swine farm in Hunan in 2017 (11). Moreover, despite having a relatively short history (first detected in 1997), the Liao ning virus (LNV) has been recorded in most of Northern China, including Beijing. It was initially thought that the virus was specific to China, until the virus was isolated from 4 genera of mosquitoes collected along coastal regions of Australia during 1988 to 2014, with a characteristic insect-specific phenotype (12). By contrast, the Chinese isolates can be replicated in mammalian cell lines and cause viremia and massive hemorrhage during re-infection of mice (13).

  • Aside from the mosquito-borne zoonotic and potentially pathogenic viruses, the increasing discovery of insect-specific flaviviruses (ISFVs) in the last decade is also worthy of attention (Figure 1). ISFVs, which are specific to insects, have both horizontal and vertical transmission routes, have diverse host relationships, and have a wide geographic distribution. This group can be divided into monophyletic classical ISFVs (cISFVs) and dual-host ISFVs (dISFVs), with the latter being more closely related to mosquito-borne pathogenic flaviviruses (MBPFVs) speculated to have lost their ability to infect vertebrate cells during their evolution (14). There are three common cISFVs hosted by medically important mosquitoes: the Culex flavivirus (CxFV), the Quang Binh virus (QBV), and the Aedes flavivirus (AeFV) (10,15). The distribution and host range of the Hanko virus (Inner Mongolia, 2018), the Yunnan Culex flavivirus (Yunnan, 2009; 2018), the Culex theileri flavivirus (Yunnan, 2018), and the Yamadai flavivirus (Yunnan, 2018) in China are relatively localized (10,16). In some instances, a high prevalence of ISFVs have been observed in the field, such as QBV (21.53/1000) in Cx. pipiens in Jining, CxFV (61.25/1000) in Cx. tritaeniorhynchus in Sanya, and AeFV (33.93/1000) in Aedes albopictus in Songjiang District, Shanghai (10,15). By contrast, the distribution and host range of dISFVs are narrower than that of cISFVs. The two dISFVs recorded in China, the Chaoyang virus (Liaoning, 2008; Inner Mongolia, 2018) and the Donggang virus (Liaoning, 2009, unpublished in China), are transmitted by Ae. vexans and Cx. pipiens and by Aedes mosquitoes, respectively.

    Figure 1.  Geographic distribution and diversity of insect specific flaviviruses in China by 2020. Abbreviations: AAFV=Anopheles associated flavivirus; AeFV=Aedes flavivirus; CHAOV=Chaoyang virus; CTFV=Culex theileri flavivirus; CxFV=Culex flavivirus; HANKV=Hanko virus; QBV=Quang Binh flavivirus; YDFV=Yamadai flavivirus; YNCxFV=Yunnan Culex flavivirus.
  • Since vaccines for the majority of MBVs are unavailable, vector control is the major route for routine control and epidemic disposal. However, the intensive use of insecticides in agriculture and pest management has resulted in the development and increase of insecticide resistance in mosquitoes. Therefore, it is urgent to develop novel control strategies and tools. Biological control is the traditional research hotspot, as it is sustainable and environmentally friendly. Bacteria (Bacillus thuringiensis, Wolbachia) have been wildly used in the field. By contrast, the use of fungi (Metarhizium anisopliae and Beauveria bassiana) and viruses (Densovirus) as alternative mosquito control agents remains at the laboratory or semi-field stages. Further studies on ISFVs have led to the discovery of their natural, physical, and ecological characteristics, as well as their phylogenetic status, and these clues indicate the potential of ISFVs as a novel interventional tool for vector control, most likely based on the mechanism of superinfection exclusion (17). Moreover, because of their phylogenetic similarity, it seems that dISFVs have a greater potential to inhibit the replication of MBPFVs than cISFVs. Superinfection exclusion can occur between closely related viruses; however, more distantly related viruses do not generally interfere with each other (18). In practice, infection with cISFV and CxFV may reportedly increase the West Nile virus (WNV) infection rate, possibly through facilitation of secondary infections with similar agents by the reduction of immune recognition (18), and because prior infection with cell-fusing agent viruses may reduce the dissessmination titer of ZIKV and dengue virus (DENV) both in vitro and in vivo. Other studies have also shown that during instances of prior infection with dISFV, the Nhumirim virus will suppress subsequent replication of mosquito-borne flaviviruses associated with human diseases, including WNV (19), ZIKV, and DENV (20). Nevertheless, further studies are necessary to help us arrive at a consensus regarding whether or not the presence of ISFVs can interfere with infection by MBPFVs, which could also subsequently alter the transmission capacity of certain vector populations for several vector-borne diseases. It is also important to more thoroughly analyze the maintenance cycle of ISFVs and how they escape the host immune system. Furthermore, we should pay more attention to how ISFVs are apparently unable to affect the health of birds, domestic animals, and humans. It is noteworthy that these viruses are carried by medically important mosquitoes and likely to attack vertebrate immune system when vertebrate innate immunity pathways are disabled by known pathogenic flaviviruses (21), which represent a potential threat to both human and animal health.

  • Emerging and preexisting MBVs are spreading globally at an unexpected rate. MBD surveillance may have been constrained by the COVID-19 pandemic, which has drawn the most attention with regards to public health, but hampers the expansion of MBVs because of restrictions in international travel. Routine mosquito surveillance and screening for mosquito-borne pathogens can be early indicators for local disease transmission and outbreaks. These practices also highlight that wide-ranging, systematic, and continuous molecular monitoring of mosquito-borne circulating viruses in vectors is urgently needed. This monitoring would provide a comprehensive understanding of virus diversity, geographic distribution, evolution, shifts in circulating genotypes, and infection rates in China and other neighboring countries and allow accurate and timely estimations of the true disease burden and prevalence of emerging/re-emerging and known mosquito-borne pathogens. This is essential to support the decision-making process regarding appropriate prevention and control strategies in China, neighboring countries, and countries involved in the Belt and Road Initiatives. Moreover, a close watch on the dynamics of mosquito insecticide resistance, alternative insecticides in certain areas, and the proper use of insect growth regulators or biocontrol approaches for integrated vector control programs should also be considered to mitigate and slow the spread and impact of insecticide resistance development in disease vector populations. The biodiversity, widespread presence, and variety of mosquito host species of ISFVs in nature shed light on means of indirect protection against the dissemination of MBVs. Ultimately, there is also an urgent need to develop an MBV vaccine using strains that are prevalent in the field to reduce the increasing health risks posed by MBVs.

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