|Year : 2022 | Volume
| Issue : 1 | Page : 37-44
Zika virus vertical transmission in mosquitoes: A less understood mechanism
Nisha Dahiya1, Mahima Yadav1, Ashwani Yadav2, Neelam Sehrawat1
1 Department of Genetics, Maharshi Dayanand University, Rohtak, Haryana, India
2 Department of Biotechnology, Chaudhary Bansi Lal University, Bhiwani, Haryana, India
|Date of Submission||28-Aug-2021|
|Date of Acceptance||06-Oct-2021|
|Date of Web Publication||7-Jun-2022|
Department of Genetics, Maharshi Dayanand University, Rohtak, Haryana
Source of Support: None, Conflict of Interest: None
Zika virus disease is a great concern in different parts of the world, and it has become a Public Health Emergency of International Concern. The global pandemic of ZIKV in 2015 prompted concern among scientific community. Zika is a flavivirus of the family Flaviviridae transmitted by mosquitoes. Natural vertical transmission is an ecological strategy that arboviruses adopt to ensure their survival inside the mosquito vector during harsh conditions or interepidemic periods when horizontal transmission is difficult. ZIKV is vertically transmitted from infected females to its offspring. This review has concluded various studies regarding the vertical transmission ability of different mosquito species for ZIKV. Previously Aedes aegypti was considered to be a major vector, however Aedes albopictus and Culex quinquifasciatus are discovered to have the similar vertical transmission potential. Different studies shown that natural vertical transmission has been detected in mosquito species which are not implicated as possible vectors. It leads to the possibility that many other mosquito species may be potential ZIKV vectors.
Keywords: ZIKA virus; Vertical transmission; Aedes aegypti; Aedes albopictus; Culex quinquifasciatus
|How to cite this article:|
Dahiya N, Yadav M, Yadav A, Sehrawat N. Zika virus vertical transmission in mosquitoes: A less understood mechanism. J Vector Borne Dis 2022;59:37-44
|How to cite this URL:|
Dahiya N, Yadav M, Yadav A, Sehrawat N. Zika virus vertical transmission in mosquitoes: A less understood mechanism. J Vector Borne Dis [serial online] 2022 [cited 2022 Jun 25];59:37-44. Available from: https://www.jvbd.org/text.asp?2022/59/1/37/331411
| Introduction|| |
Vertical transmission is the strategy of virus transmission from infected females to offspring. Vertical transmission is an important strategy to maintain the circulation of arbovirus in the mosquito vector population. It is essential to verify and understand strategy of transmission dynamics of arboviruses worldwide. The arbobiologists are confused about how arbovirus cope with the harsh environmental conditions, cold period in a temperate region, hot, dry season in tropical zones even when adult vectors, such as mosquitoes, are absent/present in low number. Vertical transmission is the popular hypothesis to answer this question. Vertical transmission of a virus from infected female to offspring helps the virus to cope in harsh conditions. It also helps the virus to survive in a specific locality even when most potential vertebrate hosts are immunized by vaccination or natural infection. ZIKA belongs to the family Flaviviridae consisting of dengue virus (DENV), yellow fever virus (YFV), chikungunya (CHIKV), Japanese Encephalitis virus (JCV), St. Louisencephalitis virus (SLEV), west Nile virus (WNV) and tickborne encephalitis virus (TBEV) which are mosquitoborne viruses and also vertically transmitted, proven by both field and laboratory shreds of evidence,,. According to the data available, there are two cycles of ZIKV; one cycle, which involves the non-human primates and forest-dwelling mosquitoes, is known as the sylvan cycle, while the other, which involves the human and locality dwelling mosquitoes is known as urban/suburban cycle,. The other arbovirus ZIKV, DENV, CHIKV and YFV shows a similar sylvan and urban cycle with Aedes aegypti as a primary vector in their urban cycle,,.
The symptoms of Zika include headache, fever, joint pain, although it also leads to the increasing number of microcephaly, Guillain-Barre syndrome, meningoencephalitis and myelitis,,. ZIKV infection leads to many complications like Guillain-Barre Syndrome and prenatal depression and adverse birth outcomes like death of foetus consisting of inherent defects known as congenital Zika syndrome (CZS), including abnormalities of brain, limb and eye, microcephaly, calcium deposition in brain and other neurologic manifestations. Healthcare systems and community-based programs aim to provide long-term care to the affected children and their families.
Epidemiology of Zika
To date, there is limited epidemiological data on ZIKV. In most cases, the ZIKV infection is asymptomatic or the symptoms are either mild or non-specific, which may not be detected. In the absence of large outbreaks, the information is based on the research studies, clinical case reports and traveller cases, because countries have a limited system for routine surveillance, reporting and case detection. Limitations in the present diagnostic test challenged the case detection, surveillance system and laboratory capacity,,. So, areas with low transmission levels shouldn’t be equated with no transmission occurring. World Health Organization (WHO) is strengthening public health systems to detect the disease at an early stage and monitor the emergence, re-emergence, and global spread of ZIKV infection and its complications like congenital Zika Guillain-Barré syndrome.
In 1947, the first Zika virus strain MR766 was isolated from the Rhesus monkey while collecting yellow fever virus (YFV) samples in the Zika forest, Uganda. Later on, in 1948, the virus was isolated from the pool of Aedes africans in the ZIKA forest,. First human infection was reported in Africa in 1950 and later in Asia and remained restricted to these regions till 2007,,. After that, ZIKV spread geographically in North Pacific,,, French Polynesia and South Pacific. In 2015, the first case was reported in America, and it spread across the Pacific Ocean to invade Brazil, Suriname and Columbia. Since 2015, 84 countries reported the incidence of ZIKV either by re-introduction or by new introduction besides taking prevention and control measures. It’s risk of infection is still a reality, mainly in the region where many mosquito vectors are present. In 2016, WHO declared the cases of microcephaly and neurological disorders occurring in the Zika virus prone areas and represent a public health emergency of international concern. In 2017, four cases of ZIKV were reported in India (three in Gujrat state and one in Tamil Nadu state) which were confirmed by realtime reverse transcription-polymerase chain reaction by the Ministry of Health and Family Welfare, Government of India,. After this declaration and three confirmed cases of ZIKV, India shifted from WHO category-4 virus may be present but no notified cases were documented to WHO category-2. There is no travelling record of ZIKV infection; this suggests that infection has occurred due to locally invading viruses. Cases of Zika virus obtained from Ahmedabad, India shows close sequence similarity with Asian strains. In India, ZIKV outbreak was detected in Rajasthan state in 2018. In December 2018, 130 cases from Madhya Pradesh, one case from Gujarat state and 159 active cases of ZIKV from Rajasthan, including 63 pregnant women, were reported by the India National Centre for Disease Control, Ministry of Health and Family. The sequence analysis of five specimens of virus from the Jaipur, India outbreak demonstrated the outbreak potential of the older Asian strain.
Geographical distribution of ZIKV infection
Until July 2019, about 87 countries and territories had incidences of indigenous Zika virus (ZIKV) spread over four of the six WHO Regions, viz., South-East Asia Region, Western Pacific Region, African Region, and Region of the Americas. In America, ZIKV infection incidence had reached the maximum in 2016 and then reduced significantly in 2017 and 2018. The African, South-East Asian, and Western Pacific Regions lacked epidemiological data leading to the accumulation of new scientific evidence and advancing our knowledge for understanding the complications of global ZIKV transmission. Worldwide studies provided information about the pattern of ZIKV transmission and its prevalence e.g., a population-based serosurvey in Indonesia found prior ZIKV infection in 9% of children until five years, while 10% of asymptomatic adults had evidence of previous ZIKV infection,. Recent studies have shown that the American ZIKV strain had spread to Angola, responsible for microcephaly cluster in 2017–2018,. Cases of Zika-associated congenital malformations, microcephaly and foetal death identified in Asia’s countries,,. Globally from WHO regions, 61 countries and territories had no reported case of ZIKV. Still, Aedes aegypti vectors alarm towards the risk of ZIKV spread to these countries or any case may not have been detected or reported yet. Analyzing the ZIKV genetic sequence helped annotate its spread worldwide,,,,. There are two lineages of ZIKV, the Asian and African lineages. The Asian line first spread from Pacific Islands to the Americas and was first identified in Asia. In 2015–16 the Asian strain is referred as the American strain while the strain that continues to circulate in Asia was referred as the “Asia lineage-Asian strain” or the “older” Asian strain. The 2018 Zika outbreak in India demonstrated the epidemic potential of older Asian strain. The epidemic in Americas provided the evidence that complications of ZIKV are not limited to the strains,,. Both the American and Asian strains are providing new evidence that adverse birth outcomes are not limited to the strains that caused the epidemic in the Americas,. The African strain has been circulating in Africa from decades with no reported active case in human. The study carried out on human beings shows increased pathogenesis compared to Asian lineage, leading to the death of the foetus,. [Figure 1] shows the geographical distribution of ZIKV in different regions of the world.
Vertical transmission cases
Mosquitoes remain reproductively inactive in the specific period of the dry season in tropical regions or cold season in temperate areas. Adult mosquito’s absence or low density leads to inhibition of transmission from host to vector, i.e., horizontal transmission. Mosquitoes have adapted various physiological and behavioral mechanisms for survival in the dry and cold seasons. When herd immunity of the host community is at a high level, it may prevent transmission above the minimal level required for sustained horizontal transmission. During unfavorable or high herd immunity condition, arboviruses are maintained by the presence of an alternate host, different mode of transmission or virus re-introduction. Previously it has been reported that Ae. furcifer, Ae. apicocoargenteus, Ae. africanus, Ae. vittatus and, Ae. aegypti, Ae. luteocephalus are the potential vectors for ZIKV,,. Similarly, in South-eastern Senegal, Anopheles coustani, Ae. furcifer, Ae. luteocephalus, Ae. africanus, Ae. dalzieli, Ae. unilineatus, Ae. metallicus, Ae. vittatus, Ae. aegypti, Ae. hirsutus, Culex perfuscus and Ae. taylori proved as probable vectors by isolating viruses and performing their RT-PCR (Reverse transcription-polymerase chain reaction). In Brazil, Aedes aegypti is the possible primary vector for the ZIKV, while Ae. albopictus and Culex quinquefasciatus were negative for ZIKV. In early 2016, researchers from northeastern Brazil and China announced that Culex quinquefasciatus, could transmit the ZIKV based on the detection of ZIKV RNA in field-caught mosquitoes, artificial infection and transmission experiments. These findings led to the conflict among researchers, health personnel and media about the competency of Cx. quinque-fasciatus for ZIKV. Later, various studies carried out and published attempting to detect ZIKV RNA and virus in field mosquitoes.
It is reported that there is a possibility of involvement of yolk granules in vertical transmission of ZIKV as the virus may infect germ cells or matured egg during spawning,. Although the transovarial transmission is under investigation and not clear till now. Nervous system infection is revealed by infection in facet cells. Ferraera de brito et al. 2016 tested mosquitoes and found Aedes aegypti are ZIKV positive, and one male was also ZIKV positive. A similar result of infection of male mosquitoes was reported in field-collected Aedes frucifers from Senegal. It shows the possibility of sexual and vertical transmission in Ae. aegypti as one male found ZIKV positive,. [Table 1] shows the different vertical transmission studies across the world.
|Table 1: Different field and laboratory studies of vertical transmission in different mosquito species across the world.|
Click here to view
In Thailand, a study concluded no role of adult Aedes albopictus in vertical transmission by the laboratory colonies when fed artificially. Similar results were observed in both field and laboratory studies in Thailand. Another laboratory study in Spain reported the inability to vertically transmit the disease when artificially fed and reared at 20°C and 25°C. Against this MIR in New York for Aedes albopictus was found to be 11.8 in the field study. In another study, the IR was 15% for females and 10% for males in Brazil. In Brazil also IR for ZIKV is found to be 7.2, and two pools found ZIKV positive. In China the infection rate in the first gonadotrophic cycle was 40.66% and in second gonadotrophic cycle was 93.75% while in another study the MIR for eggs *4.4/1000 and larvae *53.3/1000 one female salivary gland also tested positive for ZIKV RNA. A survey was carried out in Brazil in which three specimens found ZIKV positive among 18 pools having 615 specimens with a MIR for Ae. albopictus of 2.3 (1/442), suggesting that the transovarial route has transmitted arboviruses.
In Thailand, FIR was found to be 1:290 when tested after feeding the Aedes mosquito intrathoracically. In Argentina and Mexico FIR was slightly higher than Thailand and found after evaluating 104 pools and found 6 to be ZIKV positive with FIR 1:84. Costa evaluated 264 Ae. albopictus and IR calculated for ZIKV as per 1000 mosquitoes found to be 0.45 for MIR and 0.44 for MLE in Brazil. In Brazil, 4490 Aedes aegypti screened for the ZIKV and IR by MLA method was 1.8. In Thailand in field strains of Ae. aegypti found that the ZIKV exposed males and females were able to transmit the ZIKA virus to one subsequent generation only with an infection rate of 3.3%, 3.3% with FIR 1:60, 1:900 respectively, while in the laboratory strain, the infection rate is 1.7% in two pools of female F1 progeny with FIR 1:1,200. No F1 male was detected ZIKV positive. In Mexico only 10.8% (17) pools and 5.7% (9) larvae raised from June collected eggs and 5.1% (8) from larvae raised from November collected eggs were found to be positive. The MIR for June collected eggs found to be 2.5 while for November collected eggs found to be 6.9. In Spain in a laboratory study at 20°C and 25°C, Aedes aegypti showed higher infection rates at 20°C dissemination rate is found as dpi (63%), dpi14 (53%) and at dpi21 no dissemination was detected at temp 20°C while at 25°C the dissemination was dpi7(41%), dpi14(80%) and dpi21(75%). No F1 generation was found to be positive for ZIKA virus suggesting its inability to transmit the virus vertically. Chaves analyzed 600 F1 female mosquitoes in 20 pools per life stage in Brazil, and the result showed that due to vertical transmission ZIKV infection rate was 55% in larvae (11 out of 20 pools), 50% in pupae and 70% in adults. The MFIR was found 1:18 in larvae, 1:20 pupae and 1:14.3 in adults. In China, the MIR for F1 adult progeny of Jiegao strain is found significantly higher than the Mengding strain. The MIR of eggs, larvae and adult is 1:128.57, 1:35.71 and 1:14.29, respectively in Jiegao strain, while the Mengding strain was 1:174, 1:100, 1:200 in eggs, larvae, adults, respectively. In Brazil, the RT-PCR performed for CHIKV, ZIKV and DENV in all pools; Maniero analyzed 18 pools, and results showed that three pools with only larvae were found positive for ZIKV. This study suggests that ZIKV transovarial transmission occurrence is 11.6% (2/173) for Ae. aegypti. The positive pools were from October 2015, containing 38 Ae. Aegypti and December 2015, 3 larvae of Ae. aegypti. According to these results, the cycle thresholds of positive pools, when screened by RT-qPCR, were: in October/2015: 37.34 larvae Ae. aegypti and December/2015: 37.84 larvae Ae. aegypti.
In Thailand a primary vector Cx. quinquefasciatus had highest level for ZIKV infection in F1progeny i.e., 29.2% with FIR 1:66, that varied from 24.2%, 8.3%, 7.5%, 5.8%, 0.83% to 0% from F2 to F7 generations respectively in female mosquitoes, respectively and the ZIKV RNA detected till F6 generations. Although ZIKV RNA was found in male mosquitoes of F2 generation, F1 has 20% infection with FIR 1:150 and F2 with 16.7%, and ZIKV RNA is undetectable in the F3 generation. Still, an investigation is going on the major role of ZIKV vertical transmission. Data suggest that transmission of ZIKV occurred transovarially to progeny in both field and laboratory studies. Guo et al. 2016 unveil that in China Cx. pipiensquinquefasciatus has potential to be ZIKV vector. When Cx. quinquefasciatus laboratory colonies were artificially blood-fed, ZIKV detected in the midgut and salivary glands. In field study Cx. quinquefasciatus tested positive for ZIKV by RT-PCR in Brazil. In Brazil, ZIKV is found in the salivary gland of Cx. quinquefasciatus on 7 and 15 days post-feeding. Besides the number of reports showing no competence of ZIKV in Culex species as determined in United States ZIKV inability to replicate by using plaque assay,,,. Similar results were seen for C. pipiens and other Culex species from Brazil, Germany, Tunisia, Italy and Australia. The variation in the competence of mosquito vectors may occur due to the following reasons (a) Variation of viral competence ability may occur due to different genetic backgrounds as mosquitoes collected from different geographical regions,,. The genetic variation affects the morphological characters of vector mosquito and virus replication, dissemination, immune responses, small RNA-based interferon (RNAi) pathways,, and the midgut and salivary gland barriers, (b) Presence of variable types of microviromes and microbiomes in mosquito vectors interfere with mosquito’s virus replication ability and competency. A variety of microbiomes and microviromes are present in mosquitoes collected from different geographical regions,,. If we consider bacterial presence in mosquito Wolbachia is another contributing factor that influences viral replication in vector. An approach proposed using Wolbachia pipientis (wPip) as a mode of interference reduces arbovirus transmission in mosquitoes,. However, Lourenço-de-Oliveira et al. (2018) showed that no ZIKV was found in Cx. quinquifasciatus lines whether or not they contained Wolbachia (c) The variation in the ZIKV strain used, titer level, genotype of virus and number of passages may have affected the capability of ZIKV to invade mosquito organs and the variation in the rate of replication and dissemination of virus inside mosquito (d) Maybe the techniques like the mode of infection, either orally or intrathoracically, the ZIKV detection assays such as plague assay, molecular techniques, immunological techniques, have different specificities and sensitivities that result in variation in results.
Conflict of interest: None
| Acknowledgements|| |
The authors are grateful to Maharshi Dayanand University for providing University Research Scholarship to Nisha Dahiya and Mahima Yadav.
| Conclusion|| |
The vertical transmission of ZIKV suggests the mechanism of virus survival in adverse conditions. The vertical transmission ability of different mosquito vectors in Thailand, New York, Brazil, Spain, China and Mexico have been studied and confirmed. Aedes aegypti is the primary vector of ZIKV worldwide and studies also confirmed the vectorial ability of Aedes albopictus in New York, Brazil, China, and Culex quinquifasciatus in Thailand. However, only a few studies have been done on the ZIKV. So, further study on vertical transmission in these mosquito species will help to demonstrate the circulation of ZIKV and the identification of new possible vectors for ZIKV transmission. Therefore, to understand the complete ecology and control of the disease, more studies should be carried out in this respect. Alternative maintenance mechanisms must be studied so that the dynamic transmission of the ZIKV virus in endemic countries can be understood in a better way.
| References|| |
Tesh RB, Bolling BG, Beaty BJ. Role of vertical transmission in arbovirus maintenance and evolution. Arboviruses: Molecular Biology, Evolution and Control
Gubler DJ. Human arbovirus infections worldwide. Annals of the New York Academy of Sciences
Pierson TC, Kielian M. Flaviviruses: braking the entering. Current Opinion in Virology
2013; 3(1): 3–12.
Gatherer D, Kohl A. Zika virus: a previously slow pandemic spreads rapidly through the Americas. Journal of General Virology
2016; 97(2): 269–273.
Musso D, Stramer SL, Busch MP. Zika virus: a new challenge for blood transfusion. The Lancet
2016; 387(10032): 1993–1994.
Pacheco O, Beltrán M, Nelson CA, Valencia D, Tolosa N, Farr SL, Padilla AV, Tong VT, Cuevas EL, Espinosa-Bode A, Pardo L. Zika virus disease in Colombia-preliminary report. New England Journal of Medicine
Monath TP. Yellow fever: an update. The Lancet Infectious Diseases
2001; 1(1): 11–20.
Vasilakis N, Weaver SC. The history and evolution of human dengue emergence. Advances in Virus Research
2008; 72: 1–76.
Weaver SC, Reisen WK. Present and future arboviral threats. Antiviral Research
2010; 85(2): 328–45.
Diaz LA, Flores FS, Quaglia A, Contigiani MS. Intertwined arbovirus transmission activity: reassessing the transmission cycle paradigm. Frontiers in Physiology
2013; 3: 1–7.
Samarasekera U, Triunfol M. Concern over Zika virus grips the world. The Lancet
2016; 387(10018): 521–4.
Rasmussen SA, Jamieson DJ, Honein MA, Petersen LR. Zika virus and birth defects-reviewing the evidence for causality. New England Journal of Medicine
World Health Organization, 2019. Countries and territories with current or previous Zika virus transmission. World Health Organization: Geneva, Switzerland
Lanciotti RS, Kosoy OL, Laven JJ, Velez JO, Lambert AJ, Johnson AJ, Stanfield SM, Duffy MR. Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerging Infectious Diseases
2008; 14(8): 1232–1239.
Santiago GA, Vázquez J, Courtney S, Matías KY, Andersen LE, Colón C, Butler AE, Roulo R, Bowzard J, Villanueva JM, Muñoz-Jordan JL. Performance of the Trioplex real-time RT-PCR assay for detection of Zika, dengue, and chikungunya viruses. Nature Communications
2018; 9(1): 1–10.
Stettler K, Beltramello M, Espinosa DA, Graham V, Cassotta A, Bianchi S, Vanzetta F, Minola A, Jaconi S, Mele F, Foglierini M. Specificity, cross-reactivity, and function of antibodies elicited by Zika virus infection. Science
2016; 353(6301): 823–6.
Marano G, Pupella S, Vaglio S, Liumbruno GM, Grazzini G. Zika virus and the never-ending story of emerging pathogens and transfusion medicine. Blood Transfusion
2016; 14(2): 95–100.
Dick GW, Kitchen SF, Haddow AJ. Zika virus (I). Isolations and serological specificity. Transactions of the Royal Society of Tropical Medicine and Hygiene
Dick GW, Kitchen SF, Haddow AJ. Zika virus (II). Pathogenicity and physical properties. Transactions of the Royal Society of Tropical Medicine and Hygiene
1952; 46(5): 521–534.
Simpson DI. Zika virus infection in man. Transactions of the Royal Society of Tropical Medicine and Hygiene
1964; 58(4): 335–8.
Aubry M, Richard V, Green J, Broult J, Musso D. Inactivation of Z ika virus in plasma with amotosalen and ultraviolet a illumination. Transfusion
2016; 56(1): 33–40.
Olson JG, Ksiazek TG. Zika virus, a cause of fever in Central Java, Indonesia. Transactions of the Royal Society of Tropical Medicine and Hygiene
1981; 75(3): 389–93.
Duffy MR, Chen TH, Hancock WT, Powers AM, Kool JL, Lanciotti RS, et al
. Zika virus outbreak on Yap Island, federated states of Micronesia. New England Journal of Medicine
2009; 360(24): 2536–43.
Haddow AD, Schuh AJ, Yasuda CY, Kasper MR, Heang V, Huy R, et al
. Genetic characterization of Zika virus strains: geographic expansion of the Asian lineage. PLoS Neglected Tropical Diseases
2012; 6(2): e1477.
Cao-Lormeau VM, Roche C, Teissier A, Robin E, Berry AL, Mallet HP, et al
. Zika virus, French polynesia, South pacific, 2013. Emerging Infectious Diseases
2014; 20(6): 1085.
Chan JF, Choi GK, Yip CC, Cheng VC, Yuen KY. Zika fever and congenital Zika syndrome: an unexpected emerging arboviral disease. Journal of Infection
2016; 72(5): 507–24.
World Health Organization, 2016. Zika situation report: Zika virus, microcephaly and Guillain-Barré syndrome.
Broutet N, Krauer F, Riesen M, Khalakdina A, Almiron M, Aldighieri S, et al
. Zika virus as a cause of neurologic disorders. New England Journal of Medicine
2016; 374(16): 1506–9.
Darwish MA, Hoogstraal H, Roberts TJ, Ahmed IP, Omar F. A sero-epidemiological survey for certain arboviruses (Togaviridae) in Pakistan. Transactions of the Royal Society of Tropical Medicine and Hygiene
1983; 77(4): 442–5.
Sapkal GN, Yadav PD, Vegad MM, Viswanathan R, Gupta N, Mourya DT. First laboratory confirmation on the existence of Zika virus disease in India. Journal of Infection
2018; 76(3): 314–7.
Bhardwaj S, Gokhale MD, Mourya DT. Zika virus: Current concerns in India. The Indian Journal of Medical Research
2017; 146(5): 572.
World Health Organization. Zika virus infection: India, 2 Nov 2018
Yadav PD, Malhotra B, Sapkal G, Nyayanit DA, Deshpande G, Gupta N, et al
. Zika virus outbreak in Rajasthan, India in 2018 was caused by a virus endemic to Asia. Infection, Genetics and Evolution
2019; 69: 199–202.
Sasmono RT, Rama Dhenni BY, Pronyk P, Hadinegoro SR, Soepardi EJ, Ma’roef CN, et al
. Zika virus seropositivity in 1–4-year-old children, Indonesia, 2014. Emerging Infectious Viseases
2018; 24(9): 1740.
Pastorino B, Sengvilaipaseuth O, Chanthongthip A, Vongsouvath M, Souksakhone C, Mayxay M, et al
. Low Zika Virus Seroprevalence in Vientiane, Laos, 2003–2015. The American Journal of Tropical Medicine and Hygiene
2019; 100(3): 639.
Sassetti M, Zé-Zé L, Franco J, Cunha JD, Gomes A, Tomé A, Alves MJ. First case of confirmed congenital Zika syndrome in continental Africa. Transactions of The Royal Society of Tropical Medicine and Hygiene
2018; 112(10): 458–62.
Hill SC, Vasconcelos J, Neto Z, Jandondo D, Zé-Zé L, Aguiar RS, et al
. Emergence of the Zika virus Asian lineage in Angola. Bio Rxiv
Wongsurawat T, Athipanyasilp N, Jenjaroenpun P, Jun SR, Kaewnapan B, Wassenaar TM, et al
. Case of microcephaly after congenital infection with Asian lineage Zika virus, Thailand. Emerging Infectious Diseases
2018; 24(9): 1758.
Lan PT, Quang LC, Huong VT, Thuong NV, Hung PC, Huong TT, et al
. Fetal Zika virus infection in Vietnam. PLoS Currents
Moi ML, Nguyen TT, Nguyen CT, Vu TB, Tun MM, Pham TD, et al
. Zika virus infection and microcephaly in Vietnam. The Lancet Infectious Diseases
2017; 17(8): 805–6.
Metsky HC, Matranga CB, Wohl S, Schaffner SF, Freije CA, Winnicki SM, et al
. Zika virus evolution and spread in the Americas. Nature
2017; 546(7658): 411–5.
Pettersson JH, Bohlin J, Dupont-Rouzeyrol M, Brynildsrud OB, Alfsnes K, Cao-Lormeau VM, Gaunt MW, Falconar AK, De Lamballerie X, Eldholm V, Musso D. Re-visiting the evolution, dispersal and epidemiology of Zika virus in Asia. Emerging Microbes & Infections
Liu ZY, Shi WF, Qin CF. The evolution of Zika virus from Asia to the Americas. Nature Reviews Microbiology
2019 Mar; 17(3): 131–9.
Hu T, Li J, Carr MJ, Duchêne S, Shi W. The Asian lineage of Zika virus: transmission and evolution in Asia and the Americas. Virologica Sinica
2019; 34(1): 1–8.
Sheridan MA, Balaraman V, Schust DJ, Ezashi T, Roberts RM, Franz AW. African and Asian strains of Zika virus differ in their ability to infect and lyse primitive human placental trophoblast. PLoS One
2018; 13(7): e0200086.
Duggal NK, Ritter JM, McDonald EM, Romo H, Guirakhoo F, Davis BS, Chang GJ, Brault AC. Differential neurovirulence of African and Asian genotype Zika virus isolates in outbred immunocompetent mice. The American Journal of Tropical Medicine and Hygiene
2017; 97(5): 1410.
Reeves WC. Overwintering of arboviruses. Overwintering of Arboviruses
Ferreira-de-Lima VH, Lima-Camara TN. Natural vertical transmission of dengue virus in Aedes aegypti
and Aedes albopictus:
a systematic review. Parasites & Vectors
Haddow AJ, Williams MC, Woodall JP, Simpson DI, Goma LK. Twelve isolations of Zika virus from Aedes (Stegomyia) africanus (Theobald) taken in and above a Uganda forest. Bulletin of the World Health Organization
1964; 31(1): 57.
Fagbami AH. Zika virus infections in Nigeria: virological and seroepidemiological investigations in Oyo State. Epidemiology & Infection
1979; 83(2): 213–9.
McCrae AW, Kirya BG. Yellow fever and Zika virus epizootics and enzootics in Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene
1982; 76(4): 552–62.
Diallo D, Sall AA, Diagne CT, Faye O, Faye O, Ba Y, et al
. Zika virus emergence in mosquitoes in southeastern Senegal, 2011. PloS One
2014; 9(10): e109442.
Ferreira-de-Brito A, Ribeiro IP, Miranda RM, Fernandes RS, Campos SS, Silva KA, et al
. First detection of natural infection of Aedes aegypti
with Zika virus in Brazil and throughout South America. Memórias do Instituto Oswaldo Cruz
. 2016; 111
van den Hurk AF, Hall-Mendelin S, Jansen CC, Higgs S. Zika virus and Culex quinquefasciatus mosquitoes: a tenuous link. The Lancet Infectious Diseases
2017; 17(10) :1014–6.
Lequime S, Lambrechts L. Vertical transmission of arboviruses in mosquitoes: a historical perspective. Infection, Genetics and Evolution
2014; 28: 681–90.
Dodson BL, Rasgon JL. Vector competence of Anopheles and Culex mosquitoes for Zika virus. Peer J
2017 Mar 14; 5: e3096.
Phumee A, Buathong R, Boonserm R, Intayot P, Aungsananta N, Jittmittraphap A, et al
. Molecular epidemiology and genetic diversity of Zika virus from field-caught mosquitoes in various regions of Thailand. Pathogens
2019 Mar; 8(1): 30.
Rosen L. Further observations on the mechanism of vertical transmission of flaviviruses by Aedes mosquitoes. The American Journal of Tropical Medicine and Hygiene1988;
Thangamani S, Huang J, Hart CE, Guzman H, Tesh RB. Vertical transmission of Zika virus in Aedes aegypti mosquitoes. The American Journal of Tropical Medicine and Hygiene
2016; 95(5): 1169.
Phumee A, Chompoosri J, Intayot P, Boonserm R, Boonyasuppayakorn S, Buathong R, et al
. Vertical transmission of Zika virus in Culex quinquefasciatus
Say and Aedes aegypti
(L.) mosquitoes. Scientific Reports
2019; 9(1): 1–9.
Ciota AT, Bialosuknia SM, Ehrbar DJ, Kramer LD. Vertical transmission of Zika virus by Aedes aegypti and Ae. albopictus mosquitoes. Emerging Infectious Diseases
2017 May; 23(5): 880.
Smartt CT, Stenn TM, Chen TY, Teixeira MG, Queiroz EP, Souza Dos Santos L, et al
. Evidence of Zika virus RNA fragments in Aedes albopictus (Diptera: Culicidae) field-collected eggs from Camaçari, Bahia, Brazil. Journal of Medical Entomology
2017; 54(4): 1085–7.
Maia LM, Bezerra MC, Costa MC, Souza EM, Oliveira ME, Ribeiro AL, et al
. Natural vertical infection by dengue virus serotype 4, Zika virus and Mayaro virus in Aedes (Stegomyia) aegypti and Aedes (Stegomyia) albopictus. Medical and Veterinary Entomology
2019; 33(3): 437–42.
Lai Z, Zhou T, Zhou J, Liu S, Xu Y, Gu J, et al
. Vertical transmission of zika virus in Aedes albopictus. PLoS Neglected Tropical Diseases
. 2020; 14(10): e0008776.
Guo X, Li C, Deng Y, Jiang Y, Sun A, Liu Q, et al
. Vector competence and vertical transmission of Zika virus in Aedes albopictus (Diptera: Culicidae). Vector-Borne and Zoonotic Diseases
2020; 20(5): 374–9.
Maniero VC, Rangel PS, Coelho LM, Silva CS, Aguiar RS, Lamas CC, et al
. Identification of Zika virus in immature phases of Aedes aegypti and Aedes albopictus: a surveillance strategy for outbreak anticipation. Brazilian Journal of Medical and Biological Research
Costa CF, Silva AV, Nascimento VA, Souza VC, Monteiro DC, Terrazas WC, et al
. Evidence of vertical transmission of Zika virus in field-collected eggs of Aedes aegypti in the Brazilian Amazon. PLoS Neglected Tropical Diseases
2018; 12(7): e0006594.
Izquierdo-Suzán M, Zárate S, Torres-Flores J, Correa-Morales F, González-Acosta C, Sevilla-Reyes EE, et al
. Natural vertical transmission of Zika virus in larval Aedes aegypti populations, Morelos, Mexico. Emerging Infectious Diseases
2019; 25(8): 1477.
Hernández-Triana, L.M., E. Barrero, S. Delacour-Estrella, I. Ruiz-Arrondo, J. Lucientes, et al
. Evidence for infection but not transmission of Zika virus by Aedes albopictus (Diptera: Culicidae) from Spain. Parasites & vectors
2019; 12(1): 1–6.
Chaves BA, Junior AB, Silveira KR, Paz AD, Vaz EB, Araujo RG, et al
. Vertical transmission of Zika virus (Flaviviridae, Flavivirus) in Amazonian Aedes aegypti (Diptera: Culicidae) delays egg hatching and larval development of progeny. Journal of Medical Entomology
2019; 56(6): 1739–44.
Zhu C, Jiang Y, Zhang Q, Gao J, Gu Z, Lan C, et al
. Vertical Transmission of Zika Virus by Jiegao and Mengding Aedes aegypti (Diptera: Culicidae) Strains in Yunnan Province in China. Vector-Borne and Zoonotic Diseases
2020; 20(9): 664–9.
Guo XX, Li CX, Deng YQ, Xing D, Liu QM, Wu Q, et al
. Culex pipiensquinquefasciatus: a potential vector to transmit Zika virus. Emerging Microbes & Infections
2016; 5(1): 1–5.
Guedes DR, Paiva MH, Donato MM, Barbosa PP, Krokovsky L, Rocha SW, Saraiva KL, Crespo MM, Rezende TM, Wallau GL, Barbosa RM. Zika virus replication in the mosquito Culex quin-quefasciatus in Brazil. Emerging microbes & infections
2017 Jan 1; 6(1): 1–1.
Franca RF, Neves MH, Ayres CF, Melo-Neto OP, Filho SP. First international workshop on zika virus held by oswaldocruz foundation fiocruz in northeast brazil March 2016–a meeting report. PLoS Neglected Tropical Diseases
2016; 10(6): e0004760.
Epelboin Y, Talaga S, Epelboin L, Dusfour I. Zika virus: An updated review of competent or naturally infected mosquitoes. PLoS Neglected Tropical Diseases
Liu Z, Zhou T, Lai Z, Zhang Z, Jia Z, Zhou G, et al
. Competence of Aedes aegypti, Ae. albopictus, and Culex quinquefasciatus mosquitoes as Zika virus vectors, China. Emerging Infectious Diseases
2017; 23(7): 1085.
Aliota MT, Peinado SA, Osorio JE, Bartholomay LC. Culex pipiens and Aedes triseriatus mosquito susceptibility to Zika virus. Emerging Infectious Diseases
2016; 22(10): 1857.
Kenney JL, Romo H, Duggal NK, Tzeng WP, Burkhalter KL, Brault AC, et al
. Transmission incompetence of Culex quinque-fasciatus and Culex pipienspipiens from North America for Zika virus. The American Journal of Tropical Medicine and Hygiene
2017; 96(5): 1235.
Fernandes RS, Campos SS, Ferreira-de-Brito A, Miranda RM, Barbosa da Silva KA, Castro MG, et al
. Culex quinquefasciatus from Rio de Janeiro is not competent to transmit the local Zika virus. PLOS Neglected Tropical Diseases
2016; 10(9): e0004993.
Heitmann A, Jansen S, Lühken R, Leggewie M, Badusche M, Pluskota B, et al
. Experimental transmission of Zika virus by mosquitoes from central Europe. Eurosurveillance
2017; 22(2): 30437.
Amraoui F, Atyame-Nten C, Vega-Rúa A, Lourenço-de-Oliveira R, Vazeille M, Failloux AB. Culex mosquitoes are experimentally unable to transmit Zika virus. Eurosurveillance
2016; 21(35): 30333.
Boccolini D, Toma L, Di Luca M, Severini F, Romi R, Remoli ME, et al
. Experimental investigation of the susceptibility of Italian Culex pipiens mosquitoes to Zika virus infection. Eurosurveillance
2016; 21(35): 30328.
Duchemin JB, Mee PT, Lynch SE, Vedururu R, Trinidad L, Paradkar P. Zika vector transmission risk in temperate Australia: a vector competence study. Virology Journal
Dodson BL, Rasgon JL. Vector competence of Anopheles and Culex mosquitoes for Zika virus. PeerJ
. 2017; 5: e3096.
Lambrechts L. Quantitative genetics of Aedes aegypti vector competence for dengue viruses: towards a new paradigm? Trends in Parasitology
2011; 27(3): 111–4.
Tabachnick WJ. Nature, nurture and evolution of intra-species variation in mosquito arbovirus transmission competence. International Journal of Environmental Research and Public Health
2013; 10(1): 249–77.
Olson KE, Blair CD. Arbovirus–mosquito interactions: RNAi pathway. Current opinion in Virology
2015; 15: 119–26.
Blair CD, Olson KE. The role of RNA interference (RNAi) in arbovirus-vector interactions. Viruses
2015; 7(2): 820–43.
Donald CL, Kohl A, Schnettler E. New insights into control of arbovirus replication and spread by insect RNA interference pathways. Insects
2012; 3(2): 511–31.
Lourenço-de-Oliveira R, Marques JT, Sreenu VB, Nten CA, Aguiar ER, Varjak M et al
. Culex quinquefasciatus mosquitoes do not support replication of Zika virus. The Journal of general virology
2018; 99(2): 258.
Hart CE, Roundy CM, Azar SR, Huang JH, Yun R, Reynolds E, et al
. Zika virus vector competency of mosquitoes, Gulf Coast, United States. Emerging Infectious Diseases
2017; 23(3): 559.
Saldaña MA, Hegde S, Hughes GL. Microbial control of arthropod-borne disease. Memórias do Instituto Oswaldo Cruz
. 2017; 112
Alfonso-Parra C, Avila FW. Molecular responses to the Zika virus in mosquitoes. Pathogens
2018; 7(2): 49.
Mishra N, Shrivastava NK, Nayak A, Singh H. Wolbachia: A prospective solution to mosquito borne diseases. Int. J. Mosq. Res
. 2018; 5: 1–8.
Huang YJ, Higgs S, Vanlandingham DL. Biological control strategies for mosquito vectors of arboviruses. Insects
2017; 8(1): 21.