Low vector competence in sylvatic mosquitoes limits Zika virus to initiate an enzootic cycle in South America

AbstractZika virus (ZIKV) has spread in the Americas since 2015 and the potential establishment of a sylvatic transmission cycle in the continent has been hypothesized. We evaluated vector competence of five sylvatic Neotropical mosquito species to two ZIKV isolates. Distinct batches of Haemagogus leucoceleanus, Sabethes albiprivus, Sabethes identicus, Aedes terrens and Aedes scapularis females were respectively orally challenged and inoculated intrathoracically with ZIKV. Orally challenged mosquitoes were refractory or exhibited low infection rates. Viral dissemination was detected only in Hg. leucocelaenus, but with very low rates. Virus was not detected in saliva of any mosquito orally challenged with ZIKV, regardless of viral isolate and incubation time. When intrathoracically injected, ZIKV disseminated in high rates in Hg. leucocelaenus, Sa. identicus and Sa. albpiprivus, but low transmission was detected in these species; very low dissemination and no transmission was detected in Ae. terrens and Ae. scapularis. Together these results suggest that genetically determined tissue barriers, especially in the midgut, play a vital role in inhibiting ZIKV for transmission in the tested sylvatic mosquito species. Thus, an independent enzootic transmission cycle for ZIKV in South America is very unlikely.

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Transmission Potential of Zika Virus by Aedes aegypti (Diptera: Culicidae) and Ae. mediovittatus (Diptera: Culicidae) Populations From Puerto Rico

Journal of Medical Entomology ◽

10.1093/jme/tjaa286 ◽

2021 ◽

Author(s):

Rebecca A Zimler ◽

Donald A Yee ◽

Barry W Alto

Keyword(s):

Puerto Rico ◽

Aedes Aegypti ◽

Zika Virus ◽

Mosquito Species ◽

The United States ◽

Infection Rates ◽

Transmission Potential ◽

Transmission Rates ◽

Higher Doses ◽

Local Transmission

Abstract Recurrence of local transmission of Zika virus in Puerto Rico is a major public health risk to the United States, where mosquitoes Aedes aegypti (Linnaeus) and Aedes mediovittatus (Coquillett) are abundant. To determine the extent to which Ae. mediovittatus are capable of transmitting Zika virus and the influence of viremia, we evaluated infection and transmission in Ae. mediovittatus and Ae. aegypti from Puerto Rico using serial dilutions of infectious blood. Higher doses of infectious blood resulted in greater infection rates in both mosquitoes. Aedes aegypti females were up to twice as susceptible to infection than Ae. mediovittatus, indicating a more effective midgut infection barrier in the latter mosquito species. Aedes aegypti exhibited higher disseminated infection (40–95%) than Ae. mediovittatus (<5%), suggesting a substantial midgut escape barrier in Ae. mediovittatus. For Ae. aegypti, transmission rates were low over a range of doses of Zika virus ingested, suggesting substantial salivary gland barriers.

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A Survey of Aedes (Diptera: Culicidae) Mosquitoes in Tunisia and the Potential Role of Aedes detritus and Aedes caspius in the Transmission of Zika Virus

Journal of Medical Entomology ◽

10.1093/jme/tjz067 ◽

2019 ◽

Vol 56 (5) ◽

pp. 1377-1383

Author(s):

Wiem Ben Ayed ◽

Fadila Amraoui ◽

Youmna M’ghirbi ◽

Francis Schaffner ◽

Adel Rhaim ◽

...

Keyword(s):

Zika Virus ◽

New Caledonia ◽

Vector Competence ◽

Mosquito Species ◽

Breeding Site ◽

Widespread Species ◽

Larval Habitats ◽

Aedes Caspius ◽

Aedes Detritus

Abstract The present study aimed to update the list of Aedes mosquito species occurring in Tunisia and to test the vector competence of Aedes (Ochlerotatus) caspius (Pallas) and Ae. (Ochlerotatus) detritus (Haliday), the locally most abundant and widespread species, to transmit Zika virus (ZIKV). In 2017–2018, mosquito larvae were collected from 39 different larval habitats in seven bioclimatic zones of Tunisia. The salinity and pH of each breeding site were measured. The survey revealed the presence of 10 Aedes species in Tunisia: Ae. (Stegomyia) albopictus (Skuse), Ae. (Ochlerotatus) berlandi (Séguy), Ae. caspius, Ae. detritus, Ae. (Finlaya) echinus (Edwards), Ae. (Finlaya) geniculatus (Olivier), Ae. (Acartomyia) mariae (Sergent and Sergent), Ae. (Ochlerotatus) pulcritarsis (Rondani), Ae. (Aedimorphus) vexans (Meigen), and Ae. (Fredwardsius) vittatus (Bigot). Of these 10 species, Ae. caspius and Ae. detritus were the most abundant in Tunisia. Aedes detritus and Ae. caspius larvae were reared until the imago stage under insectary conditions to test autogeny. The study showed that Ae. detritus is autogenous and stenogamous and Ae. caspius, anautogenous and eurygamous. Finally, the collected strains of these two species were experimentally infected with the Asian genotype of ZIKV, originally isolated from a patient in April 2014 in New Caledonia, to test their vector competence. Neither of these species was able to transmit ZIKV at 7 and 14 d postexposure. Further investigations are needed to test the competence of other Tunisian mosquito species that may be associated with ZIKV transmission.

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Colonized Sabethes cyaneus, a Sylvatic New World Mosquito Species, Shows a Low Vector Competence for Zika Virus Relative to Aedes aegypti

Viruses ◽

10.3390/v10080434 ◽

2018 ◽

Vol 10 (8) ◽

pp. 434 ◽

Cited By ~ 12

Author(s):

Ajit K. Karna ◽

Sasha R. Azar ◽

Jessica A. Plante ◽

Rumei Yun ◽

Nikos Vasilakis ◽

...

Keyword(s):

Aedes Aegypti ◽

Yellow Fever ◽

Zika Virus ◽

New World ◽

Yellow Fever Virus ◽

Vector Competence ◽

Mosquito Species ◽

Sylvatic Cycle ◽

Post Feeding ◽

Body Compartments

The introduction of Zika virus (ZIKV) to the Americas raised concern that the virus would spill back from human transmission, perpetuated by Aedes aegypti, into a sylvatic cycle maintained in wildlife and forest-living mosquitoes. In the Americas, Sabethes species are vectors of sylvatic yellow fever virus (YFV) and are therefore candidate vectors of a sylvatic ZIKV cycle. To test the potential of Sabethes cyaneus to transmit ZIKV, Sa. cyaneus and Ae. aegypti were fed on A129 mice one or two days post-infection (dpi) with a ZIKV isolate from Mexico. Sa. cyaneus were sampled at 3, 4, 5, 7, 14, and 21 days post-feeding (dpf) and Ae. aegypti were sampled at 14 and 21 dpf. ZIKV was quantified in mosquito bodies, legs, and saliva to measure infection, dissemination, and potential transmission, respectively. Of 69 Sa. cyaneus that fed, ZIKV was detected in only one, in all body compartments, at 21 dpf. In contrast, at 14 dpf 100% of 20 Ae. aegypti that fed on mice at 2 dpi were infected and 70% had virus in saliva. These data demonstrate that Sa. cyaneus is a competent vector for ZIKV, albeit much less competent than Ae. aegypti.

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Anopheles Mosquitoes May Drive Invasion and Transmission of Mayaro Virus across Geographically Diverse Regions

10.1101/359349 ◽

2018 ◽

Author(s):

Marco Brustolin ◽

Sujit Pujhari ◽

Cory A. Henderson ◽

Jason L. Rasgon

Keyword(s):

South America ◽

Aedes Aegypti ◽

Culex Quinquefasciatus ◽

Vector Competence ◽

Mosquito Species ◽

Anopheles Mosquitoes ◽

The World ◽

The Caribbean ◽

Geographic Regions ◽

Mayaro Virus

AbstractThe Togavirus (Alphavirus) Mayaro virus (MAYV) was initially described in 1954 from Mayaro County (Trinidad) and has been responsible for outbreaks in South America and the Caribbean. Imported MAYV cases are on the rise, leading to invasion concerns similar to Chikungunya and Zika viruses. Little is known about the range of mosquito species that are competent MAYV vectors. We tested vector competence of 2 MAYV genotypes for six mosquito species (Aedes aegypti, Anopheles gambiae, An. stephensi, An. quadrimaculatus, An. freeborni, Culex quinquefasciatus). Ae. aegypti and Cx. quinquefasciatus were poor MAYV vectors, and either were poorly infected or poorly transmitted. In contrast, all Anopheles species were able to transmit MAYV, and 3 of the 4 species transmitted both genotypes. The Anopheles species tested are divergent and native to widely separated geographic regions, suggesting that Anopheles may be important in the invasion and spread of MAYV across diverse regions of the world.

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Vector competence experiments with Rocio virus and three mosquito species from the epidemic zone in Brazil

Revista de Saúde Pública ◽

10.1590/s0034-89101986000300001 ◽

1986 ◽

Vol 20 (3) ◽

pp. 171-177 ◽

Cited By ~ 33

Author(s):

Carl J. Mitchell ◽

Oswaldo Paulo Forattini ◽

Barry R. Miller

Keyword(s):

First Generation ◽

Vector Competence ◽

Mosquito Species ◽

Virus Transmission ◽

Infection Rates ◽

Feeding Technique ◽

Generation Progeny ◽

In Vitro Feeding ◽

Vector Competency

First-generation progeny of field-collected Psorophora ferox, Aedes scapularis, and Aedes serratus from the Rocio encephalitis epidemic zone in S.Paulo State, Brazil, were tested for vector competency in the laboratory. Psorophora ferox and Ae. scapularis are susceptible to per os infection with Rocio virus and can transmit the virus by bite following a suitable incubation period. Oral ID50S for the two species (10(4.1) and 10(4.3) Vero cell plaque forming units, respectively) did not differ significantly. Infection rates in Ae. serratus never exceeded 36%, and, consequently, an ID50 could not be calculated for this species. It is unlikely that Ae. serratus is an epidemiologically important vector of Rocio virus. The utility of an in vitro feeding technique for demonstrating virus transmission by infected mosquitoes and difficulties encountered in working with uncolonized progeny of field-collected mosquitoes are discussed.

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Author Correction: Low vector competence in sylvatic mosquitoes limits Zika virus to initiate an enzootic cycle in South America

Scientific Reports ◽

10.1038/s41598-021-91676-4 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Rosilainy S. Fernandes ◽

Maria I. Bersot ◽

Marcia G. Castro ◽

Erich Loza Telleria ◽

Anielly Ferreira-de-Brito ◽

...

Keyword(s):

South America ◽

Zika Virus ◽

Vector Competence ◽

Enzootic Cycle

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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Vector competence ofAnophelesandCulexmosquitoes for Zika virus

PeerJ ◽

10.7717/peerj.3096 ◽

2017 ◽

Vol 5 ◽

pp. e3096 ◽

Cited By ~ 28

Author(s):

Brittany L. Dodson ◽

Jason L. Rasgon

Keyword(s):

Anopheles Gambiae ◽

Culex Quinquefasciatus ◽

Zika Virus ◽

Anopheles Stephensi ◽

Vector Competence ◽

Mosquito Species ◽

Plaque Assay ◽

Virus Transmission ◽

Serious Disease ◽

Blood Meals

Zika virus is a newly emergent mosquito-borne flavivirus that has caused recent large outbreaks in the new world, leading to dramatic increases in serious disease pathology including Guillain-Barre syndrome, newborn microcephaly, and infant brain damage. AlthoughAedesmosquitoes are thought to be the primary mosquito species driving infection, the virus has been isolated from dozens of mosquito species, includingCulexandAnophelesspecies, and we lack a thorough understanding of which mosquito species to target for vector control. We exposedAnopheles gambiae,Anopheles stephensi, andCulex quinquefasciatusmosquitoes to blood meals supplemented with two Zika virus strains. Mosquito bodies, legs, and saliva were collected five, seven, and 14 days post blood meal and tested for infectious virus by plaque assay. Regardless of titer, virus strain, or timepoint,Anopheles gambiae,Anopheles stephensi, andCulex quinquefasciatusmosquitoes were refractory to Zika virus infection. We conclude thatAnopheles gambiae,Anopheles stephensi, andCulex quinquefasciatusmosquitoes likely do not contribute significantly to Zika virus transmission to humans. However, future studies should continue to explore the potential for other novel potential vectors to transmit the virus.

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Arbovirus Vectors of Epidemiological Concern in the Americas: A Scoping Review of Entomological Studies on Zika, Dengue and Chikungunya Virus Vectors

10.1101/713693 ◽

2019 ◽

Author(s):

Reilly Jones ◽

Manisha A. Kulkarni ◽

Thomas M. V. Davidson ◽

Benoit Talbot ◽

Keyword(s):

Low Socioeconomic Status ◽

Scoping Review ◽

Zika Virus ◽

English Language ◽

Vector Competence ◽

Mosquito Species ◽

Transmission Dynamics ◽

Health Concern ◽

Future Research ◽

Related Factors

AbstractBackgroundThree arthorpod-borne viruses (arboviruses) causing human disease have been the focus of a large number of studies in the Americas since 2013 due to their global spread and epidemiological impacts: Zika, dengue, and chikungunya viruses. A large proportion of infections by these viruses are asymptomatic. However, all three viruses are associated with moderate to severe health consequences in a small proportion of cases. Two mosquito species, Aedes aegypti and Aedes albopictus, are among the world’s most prominent arboviral vectors, and are known primary vectors for all three viruses in the Americas.ObjectivesThis review summarizes the state of the entomological literature surrounding the biology and ecology of vectors of Zika, dengue and chikungunya viruses and factors affecting virus transmission. The rationale of the review was to elucidate consensus and discord between studies, and guide future research based on identified knowledge gaps.ResultsA total of 196 studies were included in the scoping review after initial screening and subsequent exclusion of out-of-scope studies, secondary data publications, duplicate records, and studies unavailable in English language.Key findingsTemperature and humidity have the strongest impact on mosquito distribution and dynamics, development of immatures and arborviral infection rates. Low socioeconomic status and related factors, including poor infrastructure, inconsistent access to water, and high household resident density, have been consistently associated with arbovirus vector occurrence. Effects of interspecific competition on arboviral vector species is currently poorly understood. Vector competence for Zika virus is well established for Ae. aegypti and Ae. albopictus. Information on Zika virus vector transmission dynamics is sparse in contrast to the wealth of research available for dengue and chikungunya viruses.ConclusionsBased on the internationally recognized urgency of Zika virus infection as a public health concern, further research on arbovirus vectors and transmission dynamics is of pressing need.

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Zika Virus Potential Vectors among Aedes Mosquitoes from Hokkaido, Northern Japan: Implications for Potential Emergence of Zika Disease

Pathogens ◽

10.3390/pathogens10080938 ◽

2021 ◽

Vol 10 (8) ◽

pp. 938

Author(s):

Leo Uchida ◽

Miki Shibuya ◽

Ronald Enrique Morales-Vargas ◽

Katsuro Hagiwara ◽

Yasukazu Muramatsu

Keyword(s):

Virus Infection ◽

Zika Virus ◽

Vector Competence ◽

Febrile Illness ◽

Infection Rates ◽

Potential Vector ◽

Aedes Mosquitoes ◽

Ad Libitum ◽

Main City ◽

Northern Japan

The Zika virus (ZIKV) is a rapidly expanding mosquito-borne virus that causes febrile illness in humans. Aedes aegypti and Ae. albopictus are the primary ZIKV vectors; however, the potential vector competence of other Aedes mosquitoes distributed in northern Japan (Palearctic ecozone) are not yet known. In this study, the susceptibility to Zika virus infection of three Aedes mosquitoes distributed in the main city of the northern Japan and their capacities as vectors for ZIKV were evaluated. Field-collected mosquitoes were fed ad libitum an infectious blood meal containing the ZIKV PRVABC59. The Zika virus was detected in the abdomen of Ae. galloisi and Ae. japonicus at 2–10 days post infection (PI), and from the thorax and head of Ae. galloisi at 10 days PI, resulting in 17.6% and 5.9% infection rates, respectively. The Zika virus was not detected from Ae. punctor at any time. Some northern Japanese Aedes could be suspected as vectors of ZIKV but the risk may be low when compared with major ZIKV vectors.

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Replication Variance of African and Asian Lineage Zika Virus Strains in Different Cell Lines, Mosquitoes and Mice

Microorganisms ◽

10.3390/microorganisms9061250 ◽

2021 ◽

Vol 9 (6) ◽

pp. 1250

Author(s):

Tey Putita Ou ◽

Heidi Auerswald ◽

Saraden In ◽

Borin Peng ◽

Senglong Pang ◽

...

Keyword(s):

Zika Virus ◽

Mammalian Cells ◽

Vector Competence ◽

Mosquito Species ◽

Survival Rates ◽

Transmission Efficiency ◽

Phenotypic Differences ◽

Local Risk

Since the epidemic in 2007, studies on vector competence for Zika virus (ZIKV) have intensified, showing that the transmission efficiency varies depending on the vector population, ZIKV strain, and dose of the infectious blood meal. In this study, we aimed to investigate the replication of African and Asian ZIKV strains in vitro and in vivo in order to reveal their phenotypic differences. In addition, we investigated the vector competence of Cambodian Aedes aegypti (Ae. aegypti) mosquitoes (urban and rural) for these ZIKV strains. We observed a significantly higher pathogenicity of the African ZIKV strain in vitro (in mosquito and mammalian cells), and in vivo in both Ae. aegypti and mice. Both mosquito populations were competent to transmit ZIKV as early as 7 days p.i., depending on the population and the ZIKV strain. Ae. aegypti from rural habitats showed significant higher transmission and survival rates than those from urban. We observed the highest transmission efficiency for the African ZIKV isolate (93.3% 14 days p.i.) and for the Cambodian ZIKV isolate (80% 14 days p.i.). Overall, our results highlight the phenotypic differences of the ZIKV lineages and the potential risk of ZIKV transmission by Ae. aegypti mosquitoes. Further investigations of Cambodian mosquito species and ZIKV specific surveillance in humans is necessary in order to improve the local risk assessment.

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