Top

Published in:

01-04-2014 | Original Article

Epidemiological and genetic analysis of human group C rotaviruses isolated from outbreaks of acute gastroenteritis in Yokohama, Japan, between 2006 and 2012

Authors: Makoto Kumazaki, Shuzo Usuku

Published in: Archives of Virology | Issue 4/2014

Abstract

Group C rotavirus (GCRV) infection has been described in several parts of the world, predominantly as sporadic cases of acute gastroenteritis. Little is known about the yearly changes in the GCRV strains from diarrheal outbreaks. Stool samples collected from outbreaks of acute gastroenteritis in Yokohama, Japan, between 2006 and 2012 that were negative for norovirus, sapovirus, and group A rotavirus, were screened for GCRV using a reverse passive hemagglutination method. The GCRV strains were characterized by nucleotide sequence and phylogenetic analysis of their VP6, VP7, VP4, and NSP4 genes. Samples from nine of 735 outbreaks in Yokohama (1 %) contained GCRV, and eight of these outbreaks occurred in primary schools. The nucleotide sequences of the strains detected in this study were more closely related to Asian strains than to those from other regions of the world. The nucleotide sequences of the VP7 gene in these nine strains differed, and yearly changes were observed in the amino acid sequences of the VP4 genes. Phylogenetic trees constructed using the nucleotide sequences of the VP6, VP7, VP4, and NSP4 genes showed that sublineage S1 has divided into S1-1 and S1-2 in the VP4 gene only. Our results confirm that the prevalent strains of GCRV change yearly in Yokohama. This is the first study to demonstrate GCRV-associated gastroenteritis outbreaks in Yokohama, Japan.

Abid I, Guix S, Aouni M, Pintó R, Bosch A (2007) Detection and characterization of human group C rotavirus in the pediatric population of Barcelona, Spain. J Clin Virol 38:78–82PubMedCrossRef

Adah MI, Wade A, Oseto M, Kuzuya M, Taniguchi K (2002) Detection of human group C rotaviruses in Nigeria and sequence analysis of their genes encoding VP4, VP6, and VP7 proteins. J Med Virol 56:259–275

Bányai K, Jiang B, Bogdán A, Horváth B, Jakab F, Meleg E, Martella V, Magyari L, Melegh B, Szucs G (2006) Prevalence and molecular characterization of human group C rotaviruses in Hungary. J Clin Virol 37:317–322PubMedCrossRef

Baek IH, Than VT, Kim H, Lim I, Kim W (2013) Full genomic characterization of a group C rotavirus isolated from a child in south Korea. J Med Virol 85:1478–1484PubMedCrossRef

Bridger JC, Pedley S, McCrae MA (1986) Group C rotaviruses in humans. J Clin Microbiol 23:760–763PubMedCentralPubMed

Castello AA, Argüelles MH, Rota RP, Humphrey CD, Olthoff A, Gentsch JR, Glass RI, Glikmann G, Jiang B (2009) Detection and characterization of group C rotavirus in Buenos Aires, Argentina, 1997–2003. J Med Virol 81:1109–1116PubMedCrossRef

Dormitzer PR, Sun ZY, Wagner G, Harrison SC (2002) The rhesus rotavirus VP4 sialic acid binding domain has a galectin fold with a novel carbohydrate binding site. EMBO J 21:885–897PubMedCentralPubMedCrossRef

Estes MK, Kapikian AZ (2007) Rotaviruses. In: Knipe DM, Howley PM, Griffin DE, Martin MA, Lamb RA, Roizman B, Straus SE (eds) Fields virology, 5th edn. Lippincott, Williams & Wilkins, Philadelphia, pp 1917–1974

Freeman MM, Kerin T, Hull J, McCaustland K, Gentsch J (2008) Enhancement of detection and quantification of rotavirus in stool using a modified real-time RT-PCR assay. J Med Virol 80:1489–1496PubMedCrossRef

10.

Gabbay YB, Borges AA, Oliveira DS, Linhares AC, Mascarenhas JD, Barardi CR, Simões CM, Wang Y, Glass RI, Jiang B (2008) Evidence for zoonotic transmission of group C rotaviruses among children in Belém, Brazil. J Med Virol 80:1666–1674PubMedCrossRef

11.

Gabbay YB, Jiang B, Oliveira CS, Mascarenhas JD, Leite JP, Glass RI, Linhares AC (1999) An outbreak of group C rotavirus gastroenteritis among children attending a day-care centre in Belém, Brazil. J Diarrhoeal Dis Res 17:69–74PubMed

12.

Gurgel RQ, Correia JB, Cuevas LE (2008) Effect of rotavirus vaccination on circulating virus strains. Lancet 371:301–302PubMedCrossRef

13.

Hoehne M, Schreier E (2006) Detection of Norovirus genogroup I and II by multiplex real-time RT- PCR using a 3’-minor groove binder-DNA probe. BMC Infect Dis 6:69PubMedCentralPubMedCrossRef

14.

Hung T, Chen GM, Wang CG, Yao HL, Fang ZY, Chao TX, Ye W, Chang XJ, Den SS (1984) Waterborne outbreak of rotavirus diarrhoea in adults in China caused by a novel rotavirus. Lancet 1:1139–1142PubMed

15.

Jeong YJ, Park SI, Hosmillo M, Shin DJ, Chun YH, Kim HJ, Kwon HJ, Kang SY, Woo SK, Park SJ, Kim GY, Kang MI, Cho KO (2009) Detection and molecular characterization of porcine group C rotaviruses in South Korea. Vet Microbiol 138:217–224PubMedCrossRef

16.

Jiang B, Dennehy PH, Spangenberger S, Gentsch JR, Glass RI (1995) First Detection of Group C Rotavirus in Fecal Specimens of Children with Diarrhea in the United States. J Infect Dis 172:45–50PubMedCrossRef

17.

Jothikumar N, Lowther JA, Henshilwood K, Henshilwood K, Lees DN, Hill VR, Vinjé J (2005) Rapid and sensitive detection of noroviruses by using taqman-based one-step reverse transcription-pcr assays and application to naturally contaminated shellfish samples. Appl Environ Microbiol 71:1870–1875PubMedCentralPubMedCrossRef

18.

Khamrin P, Peerakome S, Malasao R, Mizuguchi M, Okitsu S, Ushijima H, Maneekarn N (2008) Genetic characterization of group C rotavirus isolated from a child hospitalized with acute gastroenteritis in Chiang Mai, Thailand. Virus Genes 37:314–321PubMedCrossRef

19.

Kumazaki M, Usuku S, Noguchi Y (2007) New variant of norovirus GII/4 strains prevalent in Yokohama City, October 2006-March 2007. Jpn J Infect Dis 60:323–324PubMed

20.

Kuzuya M, Fujii R, Hamano M, Nagabayashi T, Tsunemitsu H, Yamada M, Nii S, Mori T (1993) Rapid detection of human group C rotaviruses by reverse passive hemagglutination and latex agglutination tests using monoclonal antibodies. J Clin Microbiol 31:1308–1311PubMedCentralPubMed

21.

Kuzuya M, Fujii R, Hamano M, Nishijima M, Ogura H (2007) Detection and molecular characterization of human group C rotaviruses in Okayama Prefecture, Japan, between 1986 and 2005. J Med Virol 79:1219–1228PubMedCrossRef

22.

Logan C, O’Leary JJ, O’Sullivan N (2006) Real-time reverse transcription-PCR for detection of rotavirus and adenovirus as causative agents of acute viral gastroenteritis in children. J Clin Microbiol 44:3189–3195PubMedCentralPubMedCrossRef

23.

Luchs A, Morillo SG, de Oliveira CM, Timenetsky Mdo C (2011) Monitoring of group C rotavirus in children with acute gastroenteritis in Brazil: an emergent epidemiological issue after rotavirus vaccine? J Med Virol 83:1631–1636PubMedCrossRef

24.

Matsumoto K, Hatano M, Kobayashi K, Hasegawa A, Yamazaki S, Nakata S, Chiba S, Kimura Y (1989) An outbreak of gastroenteritis associated with acute rotaviral infection in schoolchildren. J Infect Dis 160:611–615PubMedCrossRef

25.

McDonald SM, Matthijnssens J, McAllen JK, Hine E, Overton L, Wang S, Lemey P, Zeller M, Van Ranst M, Spiro DJ, Patton JT (2009) Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLoS Pathog 5:e1000634PubMedCentralPubMedCrossRef

26.

Medici MC, Abelli LA, Martinelli M, Martella V, Dettori G, Chezzi C (2009) Molecular characterization of group C rotaviruses detected in children in Italy. J Clin Virol 44:62–65PubMedCrossRef

27.

Mitui MT, Bozdayi G, Dalgic B, Bostanci I, Nishizono A, Ahmed K (2009) Molecular characterization of a human group C rotavirus detected first in Turkey. Virus Genes 39:157–164PubMedCrossRef

28.

Monnier N, Higo-Moriguchi K, Sun ZY, Prasad BV, Taniguchi K, Dormitzer PR (2006) High-resolution molecular and antigen structure of the VP8* core of a sialic acid-independent human rotavirus strain. J Virol 80:1513–1523PubMedCentralPubMedCrossRef

29.

Moon S, Humphrey CD, Kim JS, Baek LJ, Song JW, Song KJ, Jiang B (2011) First detection of group C rotavirus in children with acute gastroenteritis in South Korea. Clin Microbiol Infect 17:244–247PubMedCrossRef

30.

Nilsson M, Svenungsson B, Hedlund KO, Uhnoo I, Lagergren A, Akre T, Svensson L (2000) Incidence and genetic diversity of group C rotavirus among adults. J Infect Dis 182:578–584CrossRef

31.

Oishi I, Yamazaki K, Minekawa Y (1993) An occurrence of diarrheal cases associated with group C rotavirus in adults. Microbiol Immunol 37:505–509PubMedCrossRef

32.

Oka T, Katayama K, Hansman GS, Kageyama T, Ogawa S, Wu FT, White PA, Takeda N (2006) Detection of human sapovirus by real-time reverse transcription-polymerase chain reaction. J Med Virol 78:1347–1353PubMedCrossRef

33.

Oseto M, Yamashita Y, Okuyama M, Kuwabara H, Inoue H (1986) Detection of atypical rotaviruses by polyacrylamide gel electrophoresis [in Japanese]. J Clin Exp Med 136:223–224

34.

Parashar UD, Hummelman EG, Bresee JS, Miller MA, Glass RI (2003) Global illness and deaths caused by rotavirus disease in children. Emerg Infect Dis 9:565–572PubMedCentralPubMedCrossRef

35.

Phan TG, Nishimura S, Okame M, Nguyen TA, Khamrin P, Okitsu S, Maneekarn N, Ushijima H (2004) Virus diversity and an outbreak of group C rotavirus among infants and children with diarrhea in Maizuru city, Japan during 2002-2003. J Med Virol 74:173–179PubMedCrossRef

36.

Rahman M, Banik S, Faruque AS, Taniguchi K, Sack DA, Van Ranst M, Azim T (2005) Detection and characterization of human group C rotaviruses in Bangladesh. J Clin Microbiol 43:4460–4465PubMedCentralPubMedCrossRef

37.

Rodger SM, Bishop RF, Holmes IH (1982) Detection of a rotavirus-like agent associated with diarrhea in an infant. J Clin Microbiol 16:724–726PubMedCentralPubMed

38.

Saif LJ, Bohl EH, Theil KW, Cross RF, House JA (1980) Rotavirus-like, calicivirus-like, and 23-nm virus-like particles associated with diarrhea in young pigs. J Clin Microbiol 12:105–111PubMedCentralPubMed

39.

Sánchez-Fauquier A, Roman E, Colomina J, Wilhelmi I, Glass RI, Jiang B (2003) First detection of group C rotavirus in children with acute diarrhea in Spain. Arch Virol 148:399–404PubMedCrossRef

40.

Sanekata T, Ahmed MU, Kader A, Taniguchi K, Kobayashi N (2003) Human group B rotavirus infections cause severe diarrhea in children and adults in Bangladesh. J Clin Microbiol 41:2187–2190PubMedCentralPubMedCrossRef

41.

Schnagl RD, Boniface K, Cardwell P, McCarthy D, Ondracek C, Coulson B, Erlich J, Morey F (2004) Incidence of group C human rotavirus in central Australia and sequence variation of the VP7 and VP4 genes. J Clin Microbiol 42:2127–2133PubMedCentralPubMedCrossRef

42.

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 22:4673–4680PubMedCentralPubMedCrossRef

43.

Tian P, Hu Y, Schilling WP, Lindsay DA, Eiden J, Estes MK (1994) The nonstructural glycoprotein of rotavirus affects intracellular calcium levels. J Virol 68:251–257PubMedCentralPubMed

44.

Ushijima H, Honma H, Mukoyama A, Shinozaki T, Fujita Y, Kobayashi M, Ohseto M, Morikawa S, Kitamura T (1989) Detection of group C rotaviruses in Tokyo. J Med Virol 27:299–303PubMedCrossRef

45.

Usuku S, Kumazaki M, Kitamura K, Tochikubo O, Noguchi Y (2008) An outbreak of food-borne gastroenteritis due to sapovirus among junior high school students. Jpn J Infect Dis 61:438–441PubMed

46.

Yamamoto D, Ghosh S, Kuzuya M, Wang YH, Zhou X, Chawla-Sarkar M, Paul SK, Ishino M, Kobayashi N (2011) Whole-genome characterization of human group C rotaviruses: identification of two lineages in the VP3 gene. J Gen Virol 92:361–369PubMedCrossRef

Title: Epidemiological and genetic analysis of human group C rotaviruses isolated from outbreaks of acute gastroenteritis in Yokohama, Japan, between 2006 and 2012
Authors: Makoto Kumazaki
Shuzo Usuku
Publication date: 01-04-2014
Publisher: Springer Vienna
Published in: Archives of Virology / Issue 4/2014
Print ISSN: 0304-8608
Electronic ISSN: 1432-8798
DOI: https://doi.org/10.1007/s00705-013-1894-1

Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Reserve your place

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin

Prof. Florian Limbourg

Prof. Anoop Chauhan

Developed by: Springer Medicine

Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2014

Inhibitory effect of doxycycline against dengue virus replication in vitro

Discovery of a new sesquiterpenoid from Phellinus ignarius with antiviral activity against influenza virus

Selection and characterization of an acid-resistant mutant of serotype O foot-and-mouth disease virus

Genomic analysis of pandemic and post-pandemic influenza A pH1N1 viruses isolated in Rio Grande do Sul, Brazil

A new endornavirus species infecting Malabar spinach (Basella alba L.)

Engineered retroviral virus-like particles for receptor targeting

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

At a glance: The STEP trials