Nationwide and long-term molecular epidemiologic studies of mumps viruses that circulated in Japan between 1986 and 2017

Minoru Kidokoro; Teiichiro Shiino; Tomohiro Yamaguchi; Eri Nariai; Hiroe Kodama; Keiko Nakata; Takako Sano; Keiko Gotou; Tomoko Kisu; Tomomi Maruyama; Yumani Kuba; Wakako Sakata; Teruaki Higashi; Naoko Kiyota; Takashi Sakai; Shunsuke Yahiro; Akira Nagita; Kaori Watanabe; Chika Hirokawa; Hirotsune Hamabata; Yoshiki Fujii; Miwako Yamamoto; Hajime Yokoi; Misako Sakamoto; Hiroyuki Saito; Chihiro Shibata; Machi Inada; Misako Fujitani; Hiroko Minagawa; Miyabi Ito; Akari Shima; Keiko Murano; Hiroshi Katoh; Fumihiro Kato; Makoto Takeda; Shigeru Suga; Surveillance Team for Mumps Virus in Japan

doi:10.3389/fmicb.2022.728831

Nationwide and long-term molecular epidemiologic studies of mumps viruses that circulated in Japan between 1986 and 2017

Front Microbiol. 2022 Oct 28:13:728831. doi: 10.3389/fmicb.2022.728831. eCollection 2022.

Authors

Minoru Kidokoro¹, Teiichiro Shiino², Tomohiro Yamaguchi³, Eri Nariai⁴, Hiroe Kodama⁴, Keiko Nakata⁵, Takako Sano⁶, Keiko Gotou⁷, Tomoko Kisu⁸, Tomomi Maruyama⁹, Yumani Kuba¹⁰, Wakako Sakata¹¹, Teruaki Higashi¹¹, Naoko Kiyota¹², Takashi Sakai¹², Shunsuke Yahiro¹², Akira Nagita¹³, Kaori Watanabe¹⁴, Chika Hirokawa¹⁴, Hirotsune Hamabata¹⁵, Yoshiki Fujii¹⁶, Miwako Yamamoto¹⁶, Hajime Yokoi¹⁷, Misako Sakamoto¹⁷, Hiroyuki Saito¹⁸, Chihiro Shibata¹⁸, Machi Inada¹⁹, Misako Fujitani¹⁹, Hiroko Minagawa²⁰, Miyabi Ito²⁰, Akari Shima²¹, Keiko Murano²², Hiroshi Katoh²², Fumihiro Kato²², Makoto Takeda²², Shigeru Suga²³; Surveillance Team for Mumps Virus in Japan

Affiliations

¹ Department of Quality Assurance, Radiation Safety, and Information Management, National Institute of Infectious Diseases, Tokyo, Japan.
² Center for Clinical Sciences, National Center for Global Health and Medicine, Tokyo, Japan.
³ Public Hygiene Division, Gifu Prefectural Tono Region Public Health Center, Tajimi, Japan.
⁴ Department of Health and Food Safety, Ishikawa Prefectural Institute of Public Health and Environmental Science, Kanazawa, Japan.
⁵ Division of Virology, Osaka Institute of Public Health, Osaka, Japan.
⁶ Division of Microbiology, Kanagawa Prefectural Institute of Public Health, Chigasaki, Japan.
⁷ Division of Virology, Ibaraki Prefectural Institute of Public Health, Mito, Ibaraki, Japan.
⁸ Virus Research Center, Clinical Research Division, Sendai National Hospital, Sendai, Japan.
⁹ Department of Infectious Diseases, Gifu Prefectural Research Institute for Health and Environmental Sciences, Kakamigahara, Japan.
¹⁰ Department of Medical Microbiology and zoology, Okinawa Prefectural Institute of Health and Environment, Uruma, Japan.
¹¹ Kitakyushu City Institute of Health and Environmental Sciences, Kitakyushu, Japan.
¹² Department of Microbiology, Kumamoto Prefectural Institute of Public-Health and Environmental Science, Uto, Japan.
¹³ Department of Pediatrics, Mizushima Central Hospital, Kurashiki, Japan.
¹⁴ Virology Section, Niigata Prefectural Institute of Public Health and Environmental Sciences, Niigata, Japan.
¹⁵ Awase Daiichi Clinic, Okinawa, Japan.
¹⁶ Division of Biological Science, Hiroshima City Institute of Public Health, Hiroshima, Japan.
¹⁷ Health Science Division, Chiba City Institute of Health and Environment, Chiba, Japan.
¹⁸ Department of Microbiology, Akita Prefectural Research Center for Public Health and Environment, Akita, Japan.
¹⁹ Virology and Epidemiology Division, Nara Prefecture Institute of Health, Sakurai, Japan.
²⁰ Laboratory of Virology, Aichi Prefectural Institute of Public Health, Nagoya, Japan.
²¹ Microbiology Division, Saga Prefectural Institute of Public Health and Pharmaceutical Research, Saga, Japan.
²² Department of Virology III, National Institute of Infectious Diseases, Tokyo, Japan.
²³ Department of Pediatrics, National Hospital Organization Mie National Hospital, Tsu, Japan.

Abstract

In Japan, major mumps outbreaks still occur every 4-5 years because of low mumps vaccine coverage (30-40%) owing to the voluntary immunization program. Herein, to prepare for a regular immunization program, we aimed to reveal the nationwide and long-term molecular epidemiological trends of the mumps virus (MuV) in Japan. Additionally, we performed whole-genome sequencing (WGS) using next-generation sequencing to assess results from conventional genotyping using MuV sequences of the small-hydrophobic (SH) gene. We analyzed 1,064 SH gene sequences from mumps clinical samples and MuV isolates collected from 25 prefectures from 1986 to 2017. The results showed that six genotypes, namely B (110), F (1), G (900), H (3), J (41), and L (9) were identified, and the dominant genotypes changed every decade in Japan since the 1980s. Genotype G has been exclusively circulating since the early 2000s. Seven clades were identified for genotype G using SH sequence-based classification. To verify the results, we performed WGS on 77 representative isolates of genotype G using NGS and phylogenetically analyzed them. Five clades were identified with high bootstrap values and designated as Japanese clade (JPC)-1, -2, -3, -4, -5. JPC-1 and -3 accounted for over 80% of the total genotype G isolates (68.3 and 13.8%, respectively). Of these, JPC-2 and -5, were newly identified clades in Japan through this study. This is the first report describing the nationwide and long-term molecular epidemiology of MuV in Japan. The results provide information about Japanese domestic genotypes, which is essential for evaluating the mumps elimination progress in Japan after the forthcoming introduction of the mumps vaccine into Japan's regular immunization program. Furthermore, the study shows that WGS analysis using NGS is more accurate than results obtained from conventional SH sequence-based classification and is a powerful tool for accurate molecular epidemiology studies.

Keywords: Japan; genotype; molecular epidemiology; mumps virus; next-generation sequencing; phylogenetic analyses; whole-genome sequencing.

Copyright © 2022 Kidokoro, Shiino, Yamaguchi, Nariai, Kodama, Nakata, Sano, Gotou, Kisu, Maruyama, Kuba, Sakata, Higashi, Kiyota, Sakai, Yahiro, Nagita, Watanabe, Hirokawa, Hamabata, Fujii, Yamamoto, Yokoi, Sakamoto, Saito, Shibata, Inada, Fujitani, Minagawa, Ito, Shima, Murano, Katoh, Kato, Takeda, Suga and The Surveillance Team for Mumps Virus in Japan.