J Bacteriol Virol.  2008 Dec;38(4):249-257. 10.4167/jbv.2008.38.4.249.

Molecular Epidemiologic Investigation of Norovirus Infections in Incheon City, Korea, from 2005 to 2007

• Gong YW
• Oh BY
• Kim HY
• Lee MY
• Kim YH
• Go JM
• Lee JM
• Jeong HS
• Cheon DS

• KMID: 1483966
• DOI: http://doi.org/10.4167/jbv.2008.38.4.249

Abstract

Noroviruses (NoVs) cause major epidemic gastroenteritis in humans. To obtain the molecular epidemiological information on gastroenteritis sporadic cases in Incheon city, Korea, we analyzed the nucleotide sequences of NoV strains detected during 2005~2007. We performed one step RT-PCR amplifying the open reading frame (ORF) 2 (capsid region) followed by semi-nested PCR from the stool samples from acute gastroenteritis patients from 2005 to 2007. Amplicons of the capsid region of norovirus strains were sequenced and analyzed using MegAlign in DNAstar software. Faecal samples were collected from 6,618 acute gastroenteritis patients during the study period. The incidence of NoV infection was about 10.7% (n=708) among patients with acute gastroenteritis and genotypes of the 320 positive samples were determined by sequence analysis. Sequence comparison of NoV strains revealed that 16 genotypes of GII NoV strains were circulated in Incheon city, from 2005 to 2007. Among norovirus strains, the most prevalent genotype GII/4 was most common 69.7% (223 strains), followed by GII/3 17.2% (55 strains), GII/12 4.4% (14 strains), GII/1 2.2% (7 strains), GII/5 1.6% (5 strains), GII/15 1.3% (4 strains) and 0.6% (2 strains) each of GII/9 and GII/16. The GII-3 strains were most frequently detected in Incheon, 2005. From the phylogenetic analysis of NoV strains, we detected 16 genotypes of GII NoV strains during 2005~2007 in Incheon. Our results suggest that various genotypes of human NoV strains in sporadic case of AGE were circulated in Incheon, Korea.

Keyword

Norovirus; Gastroenteritis; Faecal specimens; RT-PCR; Genotypes

MeSH Terms

Base Sequence
Capsid
Gastroenteritis
Genotype
Humans
Incidence
Korea
Norovirus
Open Reading Frames
Polymerase Chain Reaction
Sequence Analysis

Figure

• 

  Figure 1. Monthly distribution of norovirus-associated gastroenteritis in Incheon, Korea, from January 2005 to December 2007.

• 

  Figure 2. Age group distribution of studied cases tested for norovirus detection in Incheon, Korea, 2005~2007.

• 

  Figure 3. Annual genotypic prevalence of norovirus strains in Incheon, Korea, from 2005 to 2007.

Reference

1). 지영미: 국내 바이러스성 설사질환의 발생현황에 대한역학적 고찰. 소아감염. 10:26–36. 2003.

2). Adler JL., Zickl R. Winter vomiting disease. J Infect Dis. 119:668–673. 1969.

3). Anderson AD., Heryford AG., Sarisky JP., Higgins C., Monroe SS., Beard S., Newport CM., Cashdollar JL., Fout GS., Robbins DE., Seys SA., Musgrave KJ., Medus C., Vinj J., Bresee JS., Mainzer HM., Glass RI. A waterborne outbreak of Norwalk-like virus among snowmobilers-Wyoming, 2001. J Infect Dis. 187:303–306. 2003.

4). Ando T., Mulders MN., Lewis DC., Estes MK., Monroe SS., Glass RI. Comparison of the polymerase region of small round structured virus strains previously classified in three antigenic types by solid-phase immune electron microscopy. Arch Virol. 135:217–226. 1994.

5). Atmar RL., Estes MK. Diagnosis of noncultivatable gastroenteritis viruses, the human caliciviruses. Clin Microbiol Rev. 14:15–37. 2001.

6). Beller M., Ellis A., Lee SH., Drebot MA., Jenkerson SA., Funk E., Sobsey MD., Simmons OD 3rd., Monroe SS., Ando T., Noel J., Petric M., Middaugh JP., Spika JS. Outbreak of viral gastroenteritis due to a contaminated well. International consequences. JAMA. 278:563–568. 1997.

7). Belliot G., Noel JS., Li JF., Seto Y., Humphrey CD., Ando T., Glass RI., Monroe SS. Characterization of capsid genes, expressed in the baculovirus system, of three new genetically distinct strains of “Norwalk-like viruses”. J Clin Microbiol. 39:4288–4295. 2001.

8). Blanton LH., Adams SM., Beard RS., Wei G., Bulens SN., Widdowson MA., Glass RI., Monroe SS. Molecular and epidemiologic trends of caliciviruses associated with outbreaks of acute gastroenteritis in the United States, 2000~2004. J Infect Dis. 193:413–421. 2006.

9). Boccia D., Tozzi AE., Cotter B., Rizzo C., Russo T., Buttinelli G., Caprioli A., Marziano ML., Ruggeri FM. Water-borne outbreak of Norwalk-like virus gastroenteritis at a tourist resort, Italy. Emerg Infect Dis. 8:563–568. 2002.

10). Chikhi-Brachet R., Bon F., Toubiana L., Pothier P., Nicolas JC., Flahault A., Kohli E. Virus Diversity in a Winter Epidemic of Acute Diarrhea in France. J Clin Microbiol. 40:4266–4272. 2002.

11). Cramer EH., Blanton CJ., Blanton LH., Vaughan GH Jr., Bopp CA., Forney DL. Epidemiology of gastroenteritis on cruise ships, 2001~2004. Am J Prev Med. 30:252–257. 2006.

12). Dey SK., Nguyen TA., Phan TG., Nishio O., Salim AF., Rahman M., Yagyu F., Okitsu S., Ushijima H. Molecular and epidemiological trend of norovirus associated gastroenteritis in Dhaka City, Bangladesh. J Clin Virol. 40:218–223. 2007.

13). Fang ZY., Xie HP., Lv HX., Zhang Q., Duan ZJ., Steele D., Jiang B., Jiang X. Investigation of human calicivirus (HuCV) diarrhea among infantile and young children in China, 1999~2005. Bing Du Xue Bao. 23:9–15. 2007.

14). Gallimore CI., Cubitt D., du Plessis ND., Gray JJ. Asymptomatic and symptomatic excretion of noroviruses during a hospital outbreak of gastroenteritis. J Clin Microbiol. 42:2271–2274. 2004.

15). Green J., Wright PA., Gallimore CI., Mitchell O., Morgan-Capner P., Brown DW. The role of environmental contamination with small round structured viruses in a hospital outbreak investigated by reverse-transcriptase polymerase chain reaction assay. J Hosp Infect. 39:39–45. 1998.

16). Green KY., Ando T., Balayan MS., Berke T., Clarke IN., Estes MK., Matson DO., Nakata S., Neill JD., Studert MJ., Thiel HJ. Taxonomy of the caliciviruses. J Infect Dis. 181:S322–S330. 2000.

17). Guntapong R., Hansman GS., Oka T., Ogawa S., Kageyama T., Pongsuwanna Y., Katayama K. Norovirus and sapovirus infections in Thailand. Jpn J Infect Dis. 57:276–278. 2004.

18). Ho EC., Cheng PK., Lau AW., Wong AH., Lim WW. Atypical norovirus epidemic in Hong Kong during summer of 2006 caused by a new genogroup II/4 variant. J Clin Microbiol. 45:2205–2211. 2007.

19). Inouye S., Yamashita K., Yamadera S., Yoshikawa M., Kato N., Okabe N. Surveillance of viral gastroenteritis in Japan: pediatric cases and outbreak incidents. J Infect Dis. 181:S270–S274. 2000.

20). Jee YM. Norovirus food poisoning and laboratory surveillance for viral gastroenteritis in Korea. Health and Welfare Policy Forum. 118:26–34. 2006.

21). Jee Y., Kim KS., Cheon DS., Park JK., Kang YH., Chung YS., Go U., Shin YH., Yoon JD. Sequence analysis of small round structured viruses (SRSV) isolated from a diarrheal patient in Wonju. J Korean Soc Virol. 29:247–259. 1999.

22). Jiang X., Wang M., Wang K., Estes MK. Sequence and genomic organization of Norwalk virus. Virology. 195:51–61. 1993.

23). Johnson PC., Mathewson JJ., DuPont HI., Greenberg HB. Multiple-challenge study of host susceptibility to Norwalk gastroenteritis in US adults. J Infect Dis. 161:18–21. 1990.

24). Kageyama T., Kojima S., Shinohara M., Uchida K., Fukushi S., Hoshino FB., Takeda N., Katayama K. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol. 41:1548–1557. 2003.

25). Kageyama T., Shinohara M., Uchida K., Fukushi S., Hoshino FB., Kojima S., Takai R., Oka T., Takeda N., Katayama K. Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to Norovirus in Japan. J Clin Microbiol. 42:2988–2995. 2004.

26). Kapikian AZ., Wyatt RG., Dolin R., Thornhill TS., Kalica AR,Chanock RM. Visualization by immune electron microscopy of a 27-nm particle associated with acute infectious nonbacterial gasteroenteritis. J Virol. 10:1075–1081. 1972.

27). Karst SM., Wobus CE., Lay M., Davidson J., Virgin HW 4th. STATI-dependent innate immunity to a Norwalk-like virus. Science. 299:1575–1578. 2003.

28). Kim SH., Cheon DS., Kim JH., Lee DH., Jheong WH., Heo YJ., Chung HM., Jee Y., Lee JS. Outbreaks of gastroenteritis that occurred during school excursions in Korea were associated with several waterborne strains of norovirus. J Clin Microbiol. 43:4836–4839. 2005.

29). Lambden PR., Caul EO., Ashley CR., Clarke IN. Sequence and genome organization of a human small round-structured (Norwalk-like) virus. Science. 259:516–519. 1993.

30). Logan C., O'Leary JJ., O'Sullivan N. Real-time reverse transcription PCR detection of norovirus, sapovirus and astrovirus as causative agents of acute viral gastroenteritis. J Virol Methods. 146:36–44. 2007.

31). Lopman BA., Brown DW., Koopmans M. Human calici-viruses in Europe. J Clin Virol. 24:137–160. 2002.

32). Lopman BA., Reacher MH., Vipond IB., Sarangi J., Brown DW. Clinical manifestation of norovirus gastroenteritis in health care settings. Clin Infect Dis. 39:318–324. 2004.

33). Ma SH. Acute infectious diarrhea in pediatric patients. Korean J Pediatr. 48:235–250. 2005.

34). Mayo MA. A summary of taxonomic changes recently approved by ICTV. Arch Virol. 147:1655–1663. 2002.

35). Mounts AW., Ando T., Koopmans M., Bresee JS., Noel J., Glass RI. Cold weather seasonality of gastroenteritis associated with Norwalk-like viruses. J Infect Dis. 181:S284–S287. 2000.

36). Okada M., Ogawa T., Kaiho I., Shinozaki K. Genetic analysis of noroviruses in Chiba Prefecture, Japan, between 1999 and 2004. J Clin Microbiol. 43:4391–4401. 2005.

37). Parashar UD., Dow L., Fankhauser RL., Humphrey CD., Miller J., Ando T., Williams KS., Eddy CR., Noel JS., Ingram T., Bresee JS., Monroe SS., Glass RI. An outbreak of viral gastroenteritis associated with consumption of sandwiches: implications for the control of transmission by food handlers. Epidemiol Infect. 121:615–621. 1998.

38). Parashar U., Quiroz ES., Mounts AW., Monroe SS., Fankhauser RL., Ando T., Noel JS., Bulens SN., Beard SR., Li JF., Bresee JS., Glass RI. “Norwalk-like viruses”. Public health consequences and outbreak management. MMWR Recomm Rep. 50:1–17. 2001.

39). Paraventsis DC., Dove W., Cunliffe NA., Nakagomi O., Combe P., Grosjean P., Hart CA. Norovirus infection in children with acute gastroenteritis, Madagascar, 2004-2005. Emerg Infection Dis. 13:908–911. 2007.

40). Saito H., Saito S., Kamada K., Harata S., Sato H., Morita M., Miyajima Y. Application of RT-PCR designed from the sequence of the local SRSV strain to the screening in viral gastroenteritis outbreaks. Microbiol Immunol. 42:439–446. 1998.

41). Seto Y., Iritani N., Kubo H., Kaida A., Murakami T., Haruki K., Nishio O., Ayata M., Ogura H. Genotyping of Norovirus strains detected in outbreaks between April 2002 and March 2003 in Osaka City, Japan. Microbiol Immunol. 49:275–283. 2005.

42). Shiota T., Okame M., Takanashi S., Khamrin P., Takagi M., Satou K., Masuoka Y., Yagyu F., Shimizu Y., Kohno H., Mizuguchi M., Okitsu S., Ushijima H. Characterization of a broadly reactive monoclonal antibody against norovirus genogroups I and II: recognition of a novel conformational epitope. J Virol. 81:12298–12306. 2007.

43). Svraka S., Duizer E., Vennema H., de Bruin E., van der Veer B., Dorresteijn B., Koopmans M. Etiological role of viruses in outbreaks of acute gastroenteritis in the Netherlands from 1994 through 2005. J Clin Microbiol. 45:1389–1394. 2007.

44). Wang QH., Han MG., Cheetham S., Souza M., Funk JA., Saif LJ. Porcine noroviruses related to human noroviruses. Emerg Infect Dis. 11:1874–1881. 2005.

45). Zheng DP., Ando T. Fankhauser RL., Beard RS., Glass RI., Monroe SS. Norovirus classification and proposed strain nomenclature. Virology. 346:312–323. 2006.