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Dengue Virus Infection in Aedes albopictus during the 2014 Autochthonous Dengue Outbreak in Tokyo Metropolis, Japan
Daisuke Kobayashi
Daisuke Kobayashi
Department of Environmental Parasitology, Tokyo Medical and Dental University, Tokyo, Japan;
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
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Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
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Katsunori Murota
Katsunori Murota
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
Department of Research Promotion, Japan Agency for Medical Research and Development, Tokyo, Japan;
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Department of Research Promotion, Japan Agency for Medical Research and Development, Tokyo, Japan;
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Ryosuke Fujita
Ryosuke Fujita
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
Department of Research Promotion, Japan Agency for Medical Research and Development, Tokyo, Japan;
Isotope Imaging Laboratory, Creative Research Institution, Hokkaido University, Hokkaido, Japan;
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Department of Research Promotion, Japan Agency for Medical Research and Development, Tokyo, Japan;
Isotope Imaging Laboratory, Creative Research Institution, Hokkaido University, Hokkaido, Japan;
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Kentaro Itokawa
Kentaro Itokawa
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
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Akira Kotaki
Akira Kotaki
Department of Virology I, National Institute of Infectious Diseases, Tokyo, Japan;
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Meng Ling Moi
Meng Ling Moi
Department of Virology I, National Institute of Infectious Diseases, Tokyo, Japan;
Department of Virology, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan;
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Department of Virology, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan;
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Hiroko Ejiri
Hiroko Ejiri
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
Division of Infectious Diseases Epidemiology and Control, National Defense Medical Research Institute, National Defense Medical College, Saitama, Japan;
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Division of Infectious Diseases Epidemiology and Control, National Defense Medical Research Institute, National Defense Medical College, Saitama, Japan;
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Yoshihide Maekawa
Yoshihide Maekawa
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
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Kohei Ogawa
Kohei Ogawa
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
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Yoshio Tsuda
Yoshio Tsuda
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
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Toshinori Sasaki
Toshinori Sasaki
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
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Mutsuo Kobayashi
Mutsuo Kobayashi
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
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Tomohiko Takasaki
Tomohiko Takasaki
Department of Virology I, National Institute of Infectious Diseases, Tokyo, Japan;
Kanagawa Prefectural Institute of Public Health, Kanagawa, Japan;
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Kanagawa Prefectural Institute of Public Health, Kanagawa, Japan;
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Haruhiko Isawa
Haruhiko Isawa
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
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Kyoko Sawabe
Kyoko Sawabe
Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan;
Department of Agricultural and Environmental Biology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan
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Department of Agricultural and Environmental Biology, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan
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In 2014 in Japan, 162 autochthonous dengue cases were reported for the first time in nearly 70 years. Here, we report the results of the detection and isolation of dengue virus (DENV) from mosquitoes collected in Tokyo Metropolis in 2014 and 2015. The phylogenetic relationship among DENV isolates from mosquitoes and from patients based on both the entire envelope gene and whole coding sequences was evaluated. Herein, 2,298 female and 956 male Aedes albopictus mosquitoes were collected at six suspected locations of DENV infection in Tokyo Metropolis from August to October in 2014 and grouped into 124 and 35 pools, respectively, for viral genome detection and DENV isolation. Dengue virus RNA was detected using reverse transcription polymerase chain reaction and TaqMan assays from 49 female pools; 16 isolates were obtained using C6/36 and Vero cells. High minimum infection rates (11.2–66.7) persisted until mid-September. All DENV isolates belonged to the genotype I in serotype 1 (DENV-1), and its sequences demonstrated > 99% homology to the sequence of the DENV isolated from a patient in the vicinity of Tokyo Metropolis in 2014. Therefore, Ae. albopictus was a major DENV vector, and a single DENV-1 strain circulated in Tokyo Metropolis in 2014. Dengue virus was not detected from male mosquitoes in 2014 and wild larvae in April 2015. Thus, the possibility of both vertical transmission and overwintering of DENV was extremely low, even in dengue-epidemic areas. This study reports the first entomological information on a dengue outbreak in a temperate region, where no Aedes aegypti mosquitoes are distributed.
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Author Notes
Financial support: This work was partly supported by grant-in-aids awarded by the Ministry of Health, Labour, and Welfare (H24-Shinko-Ippan-007), Research Program on Emerging and Reemerging Infectious Diseases (2015–2017) from Japan Agency for Medical Research and Development (AMED), and by the Japan Initiative for Global Research network on Infectious Diseases (J-GRID) (2015–2017) from Ministry of Education, Culture, Sport, Science, and Technology in Japan and AMED.
Authors’ addresses: Daisuke Kobayashi, Katsunori Murota, Kentaro Itokawa, Yoshihide Maekawa, Kohei Ogawa, Yoshio Tsuda, Toshinori Sasaki, Mutsuo Kobayashi, Haruhiko Isawa, and Kyoko Sawabe, Department of Medical Entomology, National Institute of Infectious Diseases, Tokyo, Japan, E-mails: dkoba@nih.go.jp, murota@nih.go.jp, Itokawa@nih.go.jp, maekawa@nih.go.jp, kogawa@spring8.or.jp, tsudayso@nih.go.jp, tsasaki@nih.go.jp, mutsuo@nih.go.jp, hisawa@nih.go.jp, and sawabe@nih.go.jp. Ryosuke Fujita, Isotope Imaging Laboratory, Creative Research Institution, Hokkaido University, Hokkaido, Japan, E-mail: r-fujita@cris.hokudai.ac.jp. Akira Kotaki, Department of Virology 1, National Institute of Infectious Diseases, Tokyo, Japan, E-mail: ak@nih.go.jp. Meng Ling Moi, Institute of Tropical Medicine, Nagasaki University, Nagasaki, Japan, E-mail: sherry@nagasaki-u.ac.jp. Hiroko Ejiri, Division of infectious Diseases Epidemiology and Control, National Defense Medical Research Institute, National Defense Medical College, Saitama, Japan, E-mail: ejiri@ndmc.ac.jp. Tomohiko Takasaki, Kanagawa Prefectural Institute of Public Health, Kanagawa, Japan, E-mail: takasaki.jp58@pref.kanagawa.jp.
These authors contributed equally to this work.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Ministry of Health, Labour and Welfare, 2014. Domestic Cases of Dengue Fever (First Report). Available at: http://www.mhlw.go.jp/stf/houdou/0000055605.html. Accessed September 10, 2017.
-
2.
Seki N et al. 2014. An autochthonous outbreak of dengue type 1 in Tokyo, Japan 2014 [in Japanese with English summary]. Nippon Koshu Eisei Zasshi 62: 238–250.
-
3.
Tanikawa T, Yamauchi M, Ishihara S, Tomioka Y, Kimura G, Tanaka K, Suzuki S, Komagata O, Tsuda Y, Sawabe K, 2015. Operation note on dengue vector control against Aedes albopictus in Chiba City, Japan, where an autochthonous dengue case was confirmed in September 2014 [in Japanese with English summary]. Jap J Sanit Zool 66: 31–33.
-
4.
Bhatt S et al. 2013. The global distribution and burden of dengue. Nature 496: 504–507.
-
5.
Infectious Disease Surveillance Center, National Institute of Infectious Diseases, 2016. Local Transmission of Dengue, Japan. Infectious Diseases Weekly Report (IDWR), 2015 and 2016. Available at: http://www.nih.go.jp/niid/ja/data.html. Accessed February 28, 2017.
-
6.
Hotta S, 1998. Dengue vector mosquitoes in Japan: the role of Aedes albopictus and Aedes aegypti in the 1942–1944 dengue epidemics of Japanese main islands [in Japanese with English summary]. Jap J Sanit Zool 49: 267–274.
-
7.
Schmidt-Chanasit J et al. 2014. Autochthonous dengue virus infection in Japan imported into Germany, September 2013. Euro Surveill 19: 20681.
-
8.
Miyiagi I, Toma T, Iha S, 1983. Studies on the mosquitoes in Yaeyama Islands, Japan 9. On the mosquitoes breeding around human dwellings in Ishigakijima and Iriomotejima [in Japanese with English summary]. Jap J Sanit Zool 34: 1–6.
-
9.
Enserink M, 2008. Entomology. A mosquito goes global. Science 320: 864–866.
-
10.
Tsuda Y et al. 2006. Dry-ice trap collection of mosquitoes at urban areas surrounding Tokyo, Japan in 2003 and 2004 [in Japanese with English summary]. Jap J Sanit Zool 57: 75–82.
-
11.
Arima Y et al. 2014. Ongoing local transmission of dengue in Japan, August to September 2014. Western Pac Surveill Response J 5: 27–29.
-
12.
Kutsuna S et al. 2014. Autochthonous dengue fever, Tokyo, Japan. Emerg Infect Dis 21: 517–520.
-
13.
Tsuda Y, Maekawa Y, Ogawa K, Itokawa K, Komagata O, Sasaki T, Isawa H, Tomita T, Sawabe K, 2016. Biting density and distribution of Aedes albopictus during the September 2014 outbreak of dengue fever in Yoyogi Park and the vicinity of Tokyo Metropolis, Japan. Jpn J Infect Dis 69: 1–5.
-
14.
Rosen L, Shroyer DA, Tesh RB, Freier JE, Lien JC, 1983. Transovarial transmission of dengue viruses by mosquitoes: Aedes albopictus and Aedes aegypti. Am J Trop Med Hyg 32: 1108–1119.
-
15.
Mitchell CL, Miller BR, 1990. Vertical transmission of dengue viruses by strains of Aedes albopictus recently introduced into Brazil. J Am Mosq Control Assoc 6: 251–253.
-
16.
Buckner EA, Alto BW, Lounibos LP, 2013. Vertical transmission of Key West dengue-1 virus by Aedes aegypti and Aedes albopictus (Diptera: Culicidae) mosquitoes from Florida. J Med Entomol 50: 1291–1297.
-
17.
Thenmozhi V, Hiriyan JG, Tewari SC, Philip Samuel P, Paramasivan R, Rajendran R, Mani TR, Tyagi BK, 2007. Natural vertical transmission of dengue virus in Aedes albopictus (Diptera: Culicidae) in Kerala, a southern Indian state. Jpn J Infect Dis 60: 245–249.
-
18.
Cecilio AB, Campanelli ES, Souza KP, Figueiredo LB, Resende MC, 2009. Natural vertical transmission by Stegomyia albopicta as dengue vector in Brazil. Braz J Biol 69: 123–127.
-
19.
Martins VEP, Alencar CH, Kamimura MT, de Carvalho Araújo FM, De Simone SG, Dutra RF, Guedes MIF, 2012. Occurrence of natural vertical transmission of dengue-2 and dengue-3 viruses in Aedes aegypti and Aedes albopictus in Fortaleza, Ceará, Brazil. PLoS One 7: e41386.
-
20.
Tanaka K, Mizusawa K, Saugstad ES, 1979. A revision of the adult and larval mosquitoes of Japan (including the Ryukyu Archipelago and the Ogasawara Islands) and Korea (Diptera: Culicidae). Contrib Am Entomol Inst 16: 1–987.
-
21.
Morita K, Tanaka M, Igarashi A, 1991. Rapid identification of dengue virus serotypes by using polymerase chain reaction. J Clin Microbiol 29: 2107–2110.
-
22.
Ito M, Takasaki T, Yamada K, Nerome R, Tajima S, Kurane I, 2004. Development and evaluation of fluorogenic reverse transcriptase PCR (TaqMan RT-PCR) assays for dengue virus types 1–4. J Clin Microbiol 42: 5935–5937.
-
23.
Hoshino K, Isawa H, Tsuda Y, Yano K, Sasaki T, Yuda M, Takasaki T, Kobayashi M, Sawabe K, 2007. Genetic characterization of a new insect flavivirus isolated from Culex pipiens mosquito in Japan. Virology 359: 405–414.
-
24.
Thompson JD, Higgins DG, Gibson TJ, 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680.
-
25.
Felsenstein J, 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17: 368–376.
-
26.
Kumar S, Stecher G, Tamura K, 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870–1874.
-
27.
Nakayama E et al. 2016. Two different dengue virus strains in the Japanese epidemics of 2014. Virus Genes 52: 722–726.
-
28.
Tajima S, Nakayama E, Kotaki A, Moi ML, Ikeda M, Yagasaki K, Saito Y, Shibasaki K, Saijo M, Takasaki T, 2017. Whole genome sequencing-based molecular epidemiologic analysis of autochthonous dengue virus type 1 strains circulating in Japan in 2014. Jpn J Infect Dis 70: 45–49.
-
29.
Quam MB, Sessions O, Kamaraj US, Rocklöv J, Wilder-Smith A, 2016. Dissecting Japan’s dengue outbreak in 2014. Am J Trop Med Hyg 94: 409–412.
-
30.
Tian H, Sun Z, Faria NR, Yang J, Cazelles B, Huang S, Xu B, Yang Q, Pybus OG, Xu B, 2017. Increasing airline travel may facilitate co-circulation of multiple dengue virus serotypes in Asia. PLoS Negl Trop Dis 11: e0005694.
-
31.
Sukehiro N, Kida N, Umezaki M, Murakami T, Arai N, Jinnai T, Inagaki S, Tsuchida H, Murayama H, Tsuda Y, 2013. First report on invasion of yellow fever mosquito, Aedes aegypti, at Narita International Airport, Japan in August 2012. Jpn J Infect Dis 66: 189–194.
-
32.
Chung YK, Pang FY, 2002. Dengue virus infection rate in field populations of female Aedes aegypti and Aedes albopictus in Singapore. Trop Med Int Health 7: 322–330.
-
33.
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