Evaluating the competence of the primary vector, Culex tritaeniorhynchus, and the invasive mosquito species, Aedes japonicus japonicus, in transmitting three Japanese encephalitis virus genotypes

Japanese encephalitis virus (JEV) is maintained in an enzootic cycle between swine, water birds, and mosquitoes. JEV has circulated indigenously in Asia, with Culex tritaeniorhynchus as the primary vector. In some areas where the primary vector is scarce or absent, sporadic cases of Japanese encepha...

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Published inPLoS neglected tropical diseases Vol. 14; no. 12; p. e0008986
Main Authors Faizah, Astri Nur, Kobayashi, Daisuke, Amoa-Bosompem, Michael, Higa, Yukiko, Tsuda, Yoshio, Itokawa, Kentaro, Miura, Kozue, Hirayama, Kazuhiro, Sawabe, Kyoko, Isawa, Haruhiko
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.12.2020
Public Library of Science (PLoS)
Subjects
Aedes - virology
Aedes japonicus japonicus
Animals
Aquatic insects
Asia - epidemiology
Biology and Life Sciences
Cell culture
Cell Line
Chlorocebus aethiops
Culex - virology
Culex tritaeniorhynchus
Diptera
Disease control
Disease spread
Disease transmission
Distribution
DNA
Ecology and Environmental Sciences
Encephalitis
Encephalitis Virus, Japanese - genetics
Encephalitis Virus, Japanese - growth & development
Encephalitis Virus, Japanese - isolation & purification
Encephalitis, Japanese - epidemiology
Encephalitis, Japanese - transmission
Experiments
Exposure
Genetic aspects
Genotype
Genotypes
Health aspects
Humans
Humidity
Identification and classification
Infections
Introduced species
Invasive insects
Invasive species
Japanese encephalitis
Laboratories
Medicine and Health Sciences
Mosquito Vectors - virology
Mosquitoes
Nucleotide sequence
PCR
People and Places
Polymerase chain reaction
Route selection
Transmission
Tropical diseases
Vector-borne diseases
Vero Cells
Viral Envelope Proteins - genetics
Virus-vector relationships
Viruses
West Nile virus
Asia
Japan
South Korea
Europe
China
East Asia
Russia
Online AccessGet full text

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Abstract Japanese encephalitis virus (JEV) is maintained in an enzootic cycle between swine, water birds, and mosquitoes. JEV has circulated indigenously in Asia, with Culex tritaeniorhynchus as the primary vector. In some areas where the primary vector is scarce or absent, sporadic cases of Japanese encephalitis have been reported, with Aedes japonicus japonicus presumed to have the potential as a secondary vector. As one of the world’s most invasive culicid species, Ae . j . japonicus carries a considerable health risk for spreading diseases to wider areas, including Europe and North America. Thus, evaluation of its competency as a JEV vector, particularly in a native population, will be essential in preventing potential disease spread. In this study, the two mosquito species’ vector competence in transmitting three JEV genotypes (I, III, and V) was assessed, with Cx . tritaeniorhynchus serving as a point of reference. The mosquitoes were virus-fed and the infection rate (IR), dissemination rate (DR), and transmission rate (TR) evaluated individually by either RT-qPCR or focus forming assay. Results showed striking differences between the two species, with IR of 95% (261/274) and 9% (16/177) in Cx . tritaeniorhynchus and Ae . j . japonicus , respectively. Both mosquitoes were susceptible to all three JEV genotypes with significant differences in IR and mean viral titer. Results confirm the primary vector’s competence, but the fact that JEV was able to establish in Ae . j . japonicus is of public health significance, and with 2%–16% transmission rate it has the potential to successfully transmit JEV to the next host. This may explain the human cases and infrequent detection in primary vector-free areas. Importantly, Ae . j . japonicus could be a relevant vector spreading the disease into new areas, indicating the need for security measures in areas where the mosquito is distributed or where it may be introduced.
AbstractList Japanese encephalitis virus (JEV) is maintained in an enzootic cycle between swine, water birds, and mosquitoes. JEV has circulated indigenously in Asia, with Culex tritaeniorhynchus as the primary vector. In some areas where the primary vector is scarce or absent, sporadic cases of Japanese encephalitis have been reported, with Aedes japonicus japonicus presumed to have the potential as a secondary vector. As one of the world's most invasive culicid species, Ae. j. japonicus carries a considerable health risk for spreading diseases to wider areas, including Europe and North America. Thus, evaluation of its competency as a JEV vector, particularly in a native population, will be essential in preventing potential disease spread. In this study, the two mosquito species' vector competence in transmitting three JEV genotypes (I, III, and V) was assessed, with Cx. tritaeniorhynchus serving as a point of reference. The mosquitoes were virus-fed and the infection rate (IR), dissemination rate (DR), and transmission rate (TR) evaluated individually by either RT-qPCR or focus forming assay. Results showed striking differences between the two species, with IR of 95% (261/274) and 9% (16/177) in Cx. tritaeniorhynchus and Ae. j. japonicus, respectively. Both mosquitoes were susceptible to all three JEV genotypes with significant differences in IR and mean viral titer. Results confirm the primary vector's competence, but the fact that JEV was able to establish in Ae. j. japonicus is of public health significance, and with 2%-16% transmission rate it has the potential to successfully transmit JEV to the next host. This may explain the human cases and infrequent detection in primary vector-free areas. Importantly, Ae. j. japonicus could be a relevant vector spreading the disease into new areas, indicating the need for security measures in areas where the mosquito is distributed or where it may be introduced.
[...]as well as the two dominant genotypes (GI and GIII), JEV GV was included in this study because it is considered a rising threat in Japan. Furthermore, the presence of JEV in non-endemic areas such as Europe [30,31] and Africa [32] has emphasized the importance of elucidating the migration route and determining the potential for disease spread by an invasive species. [...]assessing the competency of Ae. j. japonicus as a JEV vector, particularly from a native population in Japan, is crucial in determining their disease transmission potential. In this study, we assessed the competence of Ae. j. japonicus mosquitoes as a JEV vector relative to Cx. tritaeniorhynchus through exposure to three JEV genotypes (GI and GIII as the current and past dominant genotypes, respectively; and GV which has a restricted range and has never been detected in Japan), and we determined infection, dissemination, and transmission rates by either real-time quantitative polymerase chain reaction (RT-qPCR) or focus forming assay (FFA). After viral exposure, the ISV infection status was determined by reverse-transcriptase polymerase chain reaction (RT-PCR).
Japanese encephalitis virus (JEV) is maintained in an enzootic cycle between swine, water birds, and mosquitoes. JEV has circulated indigenously in Asia, with Culex tritaeniorhynchus as the primary vector. In some areas where the primary vector is scarce or absent, sporadic cases of Japanese encephalitis have been reported, with Aedes japonicus japonicus presumed to have the potential as a secondary vector. As one of the world's most invasive culicid species, Ae. j. japonicus carries a considerable health risk for spreading diseases to wider areas, including Europe and North America. Thus, evaluation of its competency as a JEV vector, particularly in a native population, will be essential in preventing potential disease spread. In this study, the two mosquito species' vector competence in transmitting three JEV genotypes (I, III, and V) was assessed, with Cx. tritaeniorhynchus serving as a point of reference. The mosquitoes were virus-fed and the infection rate (IR), dissemination rate (DR), and transmission rate (TR) evaluated individually by either RT-qPCR or focus forming assay. Results showed striking differences between the two species, with IR of 95% (261/274) and 9% (16/177) in Cx. tritaeniorhynchus and Ae. j. japonicus, respectively. Both mosquitoes were susceptible to all three JEV genotypes with significant differences in IR and mean viral titer. Results confirm the primary vector's competence, but the fact that JEV was able to establish in Ae. j. japonicus is of public health significance, and with 2%-16% transmission rate it has the potential to successfully transmit JEV to the next host. This may explain the human cases and infrequent detection in primary vector-free areas. Importantly, Ae. j. japonicus could be a relevant vector spreading the disease into new areas, indicating the need for security measures in areas where the mosquito is distributed or where it may be introduced.Japanese encephalitis virus (JEV) is maintained in an enzootic cycle between swine, water birds, and mosquitoes. JEV has circulated indigenously in Asia, with Culex tritaeniorhynchus as the primary vector. In some areas where the primary vector is scarce or absent, sporadic cases of Japanese encephalitis have been reported, with Aedes japonicus japonicus presumed to have the potential as a secondary vector. As one of the world's most invasive culicid species, Ae. j. japonicus carries a considerable health risk for spreading diseases to wider areas, including Europe and North America. Thus, evaluation of its competency as a JEV vector, particularly in a native population, will be essential in preventing potential disease spread. In this study, the two mosquito species' vector competence in transmitting three JEV genotypes (I, III, and V) was assessed, with Cx. tritaeniorhynchus serving as a point of reference. The mosquitoes were virus-fed and the infection rate (IR), dissemination rate (DR), and transmission rate (TR) evaluated individually by either RT-qPCR or focus forming assay. Results showed striking differences between the two species, with IR of 95% (261/274) and 9% (16/177) in Cx. tritaeniorhynchus and Ae. j. japonicus, respectively. Both mosquitoes were susceptible to all three JEV genotypes with significant differences in IR and mean viral titer. Results confirm the primary vector's competence, but the fact that JEV was able to establish in Ae. j. japonicus is of public health significance, and with 2%-16% transmission rate it has the potential to successfully transmit JEV to the next host. This may explain the human cases and infrequent detection in primary vector-free areas. Importantly, Ae. j. japonicus could be a relevant vector spreading the disease into new areas, indicating the need for security measures in areas where the mosquito is distributed or where it may be introduced.
Japanese encephalitis virus (JEV) is maintained in an enzootic cycle between swine, water birds, and mosquitoes. JEV has circulated indigenously in Asia, with Culex tritaeniorhynchus as the primary vector. In some areas where the primary vector is scarce or absent, sporadic cases of Japanese encephalitis have been reported, with Aedes japonicus japonicus presumed to have the potential as a secondary vector. As one of the world’s most invasive culicid species, Ae . j . japonicus carries a considerable health risk for spreading diseases to wider areas, including Europe and North America. Thus, evaluation of its competency as a JEV vector, particularly in a native population, will be essential in preventing potential disease spread. In this study, the two mosquito species’ vector competence in transmitting three JEV genotypes (I, III, and V) was assessed, with Cx . tritaeniorhynchus serving as a point of reference. The mosquitoes were virus-fed and the infection rate (IR), dissemination rate (DR), and transmission rate (TR) evaluated individually by either RT-qPCR or focus forming assay. Results showed striking differences between the two species, with IR of 95% (261/274) and 9% (16/177) in Cx . tritaeniorhynchus and Ae . j . japonicus , respectively. Both mosquitoes were susceptible to all three JEV genotypes with significant differences in IR and mean viral titer. Results confirm the primary vector’s competence, but the fact that JEV was able to establish in Ae . j . japonicus is of public health significance, and with 2%–16% transmission rate it has the potential to successfully transmit JEV to the next host. This may explain the human cases and infrequent detection in primary vector-free areas. Importantly, Ae . j . japonicus could be a relevant vector spreading the disease into new areas, indicating the need for security measures in areas where the mosquito is distributed or where it may be introduced. It is widely known that not all mosquito species serve as medically-important virus’ vectors. Even among the vectors, there are variations in their ability to transmit one virus or the other. Nonetheless, while the known primary vectors’ transmission efficiency is evident, the importance of confirming the ability of other potential vectors is indispensable when it comes to the threat of disease introduction to new areas. Japanese encephalitis is a mosquito-borne disease mainly circulating in Asia. However, pockets of infection have been detected outside this endemic area, where the primary mosquito vector (a Culex species) is almost nonexistent. One possibility is that the causal virus is carried by the invasive mosquito species (an Aedes species), originating from Asia, confirmed to adapt well in Europe and North America. Thus, a thorough evaluation will be needed to determine the competence of both the Culex and Aedes species to transmit Japanese encephalitis virus (JEV). Here, the authors found that although the difference in the transmission efficiency between the Culex and Aedes was significant, their competence as vector is evident. This research provides evidence of the possible relevance of the Aedes species in the distribution and spread of JE into new areas.
Japanese encephalitis virus (JEV) is maintained in an enzootic cycle between swine, water birds, and mosquitoes. JEV has circulated indigenously in Asia, with Culex tritaeniorhynchus as the primary vector. In some areas where the primary vector is scarce or absent, sporadic cases of Japanese encephalitis have been reported, with Aedes japonicus japonicus presumed to have the potential as a secondary vector. As one of the world’s most invasive culicid species, Ae . j . japonicus carries a considerable health risk for spreading diseases to wider areas, including Europe and North America. Thus, evaluation of its competency as a JEV vector, particularly in a native population, will be essential in preventing potential disease spread. In this study, the two mosquito species’ vector competence in transmitting three JEV genotypes (I, III, and V) was assessed, with Cx . tritaeniorhynchus serving as a point of reference. The mosquitoes were virus-fed and the infection rate (IR), dissemination rate (DR), and transmission rate (TR) evaluated individually by either RT-qPCR or focus forming assay. Results showed striking differences between the two species, with IR of 95% (261/274) and 9% (16/177) in Cx . tritaeniorhynchus and Ae . j . japonicus , respectively. Both mosquitoes were susceptible to all three JEV genotypes with significant differences in IR and mean viral titer. Results confirm the primary vector’s competence, but the fact that JEV was able to establish in Ae . j . japonicus is of public health significance, and with 2%–16% transmission rate it has the potential to successfully transmit JEV to the next host. This may explain the human cases and infrequent detection in primary vector-free areas. Importantly, Ae . j . japonicus could be a relevant vector spreading the disease into new areas, indicating the need for security measures in areas where the mosquito is distributed or where it may be introduced.
[...]as well as the two dominant genotypes (GI and GIII), JEV GV was included in this study because it is considered a rising threat in Japan. Furthermore, the presence of JEV in non-endemic areas such as Europe [30,31] and Africa [32] has emphasized the importance of elucidating the migration route and determining the potential for disease spread by an invasive species. [...]assessing the competency of Ae. j. japonicus as a JEV vector, particularly from a native population in Japan, is crucial in determining their disease transmission potential. In this study, we assessed the competence of Ae. j. japonicus mosquitoes as a JEV vector relative to Cx. tritaeniorhynchus through exposure to three JEV genotypes (GI and GIII as the current and past dominant genotypes, respectively; and GV which has a restricted range and has never been detected in Japan), and we determined infection, dissemination, and transmission rates by either real-time quantitative polymerase chain reaction (RT-qPCR) or focus forming assay (FFA). After viral exposure, the ISV infection status was determined by reverse-transcriptase polymerase chain reaction (RT-PCR).
Audience Academic
Author Miura, Kozue
Faizah, Astri Nur
Tsuda, Yoshio
Amoa-Bosompem, Michael
Higa, Yukiko
Itokawa, Kentaro
Kobayashi, Daisuke
Isawa, Haruhiko
Sawabe, Kyoko
Hirayama, Kazuhiro
AuthorAffiliation Stanford University, UNITED STATES
2 Department of Medical Entomology, National Institute of Infectious Diseases, Shinjuku, Tokyo, Japan
1 Laboratory of Veterinary Public Health, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo, Tokyo, Japan
3 Department of Environmental Parasitology, Tokyo Medical and Dental University, Bunkyo, Tokyo, Japan
4 Pathogen Genomics Center, National Institute of Infectious Diseases, Shinjuku, Tokyo, Japan
AuthorAffiliation_xml – name: 4 Pathogen Genomics Center, National Institute of Infectious Diseases, Shinjuku, Tokyo, Japan
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– name: Stanford University, UNITED STATES
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33370301$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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Snippet Japanese encephalitis virus (JEV) is maintained in an enzootic cycle between swine, water birds, and mosquitoes. JEV has circulated indigenously in Asia, with...
[...]as well as the two dominant genotypes (GI and GIII), JEV GV was included in this study because it is considered a rising threat in Japan. Furthermore, the...
[...]as well as the two dominant genotypes (GI and GIII), JEV GV was included in this study because it is considered a rising threat in Japan. Furthermore, the...
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SubjectTerms Aedes - virology
Aedes japonicus japonicus
Animals
Aquatic insects
Asia - epidemiology
Biology and Life Sciences
Cell culture
Cell Line
Chlorocebus aethiops
Culex - virology
Culex tritaeniorhynchus
Diptera
Disease control
Disease spread
Disease transmission
Distribution
DNA
Ecology and Environmental Sciences
Encephalitis
Encephalitis Virus, Japanese - genetics
Encephalitis Virus, Japanese - growth & development
Encephalitis Virus, Japanese - isolation & purification
Encephalitis, Japanese - epidemiology
Encephalitis, Japanese - transmission
Experiments
Exposure
Genetic aspects
Genotype
Genotypes
Health aspects
Humans
Humidity
Identification and classification
Infections
Introduced species
Invasive insects
Invasive species
Japanese encephalitis
Laboratories
Medicine and Health Sciences
Mosquito Vectors - virology
Mosquitoes
Nucleotide sequence
PCR
People and Places
Polymerase chain reaction
Route selection
Transmission
Tropical diseases
Vector-borne diseases
Vero Cells
Viral Envelope Proteins - genetics
Virus-vector relationships
Viruses
West Nile virus
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Title Evaluating the competence of the primary vector, Culex tritaeniorhynchus, and the invasive mosquito species, Aedes japonicus japonicus, in transmitting three Japanese encephalitis virus genotypes
URI https://www.ncbi.nlm.nih.gov/pubmed/33370301
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http://dx.doi.org/10.1371/journal.pntd.0008986
Volume 14
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