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Journal of Clinical Microbiology, September 2005, p. 4836-4839, Vol. 43, No. 9
0095-1137/05/$08.00+0     doi:10.1128/JCM.43.9.4836-4839.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Outbreaks of Gastroenteritis That Occurred during School Excursions in Korea Were Associated with Several Waterborne Strains of Norovirus

Sung-Han Kim,¹ Doo-Sung Cheon,¹ Jin-Hyeun Kim,² Dong-Han Lee,² Won-hwa Jheong,³ Young-Joo Heo,² Hyen-Mi Chung,³ Youngmee Jee,^1* and Joo-Shil Lee¹

Division of Enteric and Hepatitis Viruses, Department of Virology, National Institute of Health, Seoul, Republic of Korea,¹ Division of Epidemiologic Investigation, Department of Infectious Disease Control, Center for Disease Control and Prevention, Seoul, Republic of Korea,² Division of Water Microbiology, Department of Water Environment Research, National Institute of Environmental Research, Incheon, Republic of Korea³

Received 28 January 2005/ Returned for modification 30 March 2005/ Accepted 6 May 2005

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In May 2004, 97 of 309 (31%) and 97 of 207 (47%) school students from geographically distant areas were affected by acute gastroenteritis during excursions to neighboring hotels. The two hotels were 300 m apart, on Jeju Island, South Korea. Several strains of norovirus, including both genogroup I and genogroup II viruses, were identified in stool samples from the students and food handlers and in groundwater from the hotels. Of these several strains of norovirus, the nucleotide sequences for one strain were identical for samples from the students, food handlers, and groundwater.

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Noroviruses are the most common cause of epidemic food- and waterborne viral gastroenteritis (5). The presence of noroviruses in water sources is a particular public health concern due to the potential for widespread outbreaks (10). Several large outbreaks due to contaminated water have been described (1-4, 7, 9, 10). However, there are few reports in which epidemiological and environmental data have been supported by molecular data on the waterborne norovirus (1, 2, 7, 10). This report describes an investigation of two outbreaks of gastroenteritis caused by several strains of norovirus during school excursions to Jeju Island, South Korea, which were traced to contaminated groundwater, the supplemental water supply to the hotels.

In May 2004, the Korea Center for Disease Control and Prevention received reports of two outbreaks of acute gastroenteritis during school excursions from two geographically different areas of Jeju Island (Fig. 1). One school visited hotel A from 17 to 20 May, and the other visited hotel B from 18 to 20 May. The two hotels were located just 300 m apart. Both epidemiological and virological investigations were conducted to determine the etiological agent of the outbreaks and the mode of transmission.

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FIG. 1. Map of Korea showing the locations of the two schools that experienced the outbreaks caused by noroviruses and the hotels in Jeju Island where the students stayed during the excursions. (Copyright Picture Map International Co., Ltd. Reproduced with permission.)

We conducted a retrospective cohort study of the 309 and 213 students from the two schools, using structured questionnaires. A case was defined as illness for any student who stayed at hotel A or B and showed gastrointestinal manifestations such as vomiting or diarrhea (three or more loose stools within a 24-h period) during the 3 days after arriving on Jeju Island. Five food handlers (three for hotel A and two for hotel B) were questioned about cooking procedures, water sources, and symptoms of gastrointestinal illness. We also surveyed the environments of the hotel restaurants and water supply systems. Water sampling and concentration procedures were carried out by the National Institute of Environmental Research, Incheon, Republic of Korea. Briefly, all samples were collected with a filter apparatus containing 1-MDS filters (ZetaPor Virosorp, Cuno) according to standard procedures (6, 10). Samples of 570 to 1,400 liters were collected depending on the turbidity of the water, which ranged from 2.3 to 5.5 nephelometric turbidity units and was thus unexpectedly high. The samples were eluted and further concentrated for norovirus assay. The identification of noroviruses was performed by the National Institute of Health, Seoul, Republic of Korea, using reverse transcription-PCR (RT-PCR) as previously described (8). The seminested PCR was performed with primers based on the 314-bp sequence of the capsid region. NV-G1F1 (5' CTG CCC GAA TTY GTA AAT GAT GAT 3') and NV-G1R1 (5' CCA ACC CAR CCA TTR TAC ATY TG 3') were used for RT and outer PCR for genogroup I (GI). NV-GIIF1 (5' GGG AGG GCG ATC GCA ATC T 3') and NV-GIIR1 (5' CCR CCI GCA TRI CCR TTR TAC AT 3') were used for RT and outer PCR for GII. For the seminested PCR, NV-GIF2 (5' ATG ATG ATG GCG TCT AAG GAC GC 3') and NV-GIIF2 (5' TTG TGA ATG AAG ATG GCG TCG ART 3') were added to the type-specific sense primers (NV-G1F1 and NV-GIIF1) in the PCR mixture. The PCR products were further characterized by sequencing. Stool specimens were also tested for the presence of Salmonella, Shigella, Campylobacter, and Yersinia.

Thirty-one percent (97) of 309 students who stayed at hotel A from 17 May to 20 May and 47% (97) of 207 students who stayed at hotel B from 18 May to 20 May developed acute gastroenteritis during the school excursion or within 3 days of their stay at the hotel (Table 1). The symptoms most commonly reported by case patients were diarrhea (92%), nausea (85%), and vomiting (59%). The duration of illness ranged from 1 to 7 days (median, 3 days). No food items were associated with illness (data not shown). Among the students who occupied hotel B, illness was significantly associated with water consumption (chi-square test for linear trend; P = 0.02); the number of ill students among the total students who drank less than one glass of water supplied by the hotel was 5/19 (26%), among those who drank one to three glasses of water supplied by the hotel was 31/70 (44%), among those who drank four to six glasses of water supplied by the hotel was 29/64 (45%), and among those who drank more than six glasses of water supplied by the hotel was 32/54 (59%).

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TABLE 1. Comparison of two outbreaks of acute gastroenteritis during school excursions to neighboring hotels

Of the 88 stool specimens collected from case students, 32 (36%) were positive by norovirus RT-PCR; 4 of 8 stool specimens from case students who stayed at hotel A and 28 of 80 specimens from students who stayed at hotel B were positive (Table 1). The amplified PCR products of the 32 positive specimens were sequenced. Twenty-eight specimens contained genogroup I strains (24 Desertshield [GI.3] strains and 4 Chiba [GI.4] strains), while 11 specimens contained genogroup II strains (8 Fayetteville-US [GII.14] strains, 2 Wortley-UK [GII.8] strains, and 1 Hillingdon-UK6 [GII.5] strain). All 11 genogroup II-positive stool specimens also contained genogroup I strains. Five distinct clusters were detected in the two outbreaks (Fig. 2). No bacterial pathogens were identified in the stool samples.

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FIG. 2. Phylogenetic tree analysis of the two outbreaks during school excursions to Jeju Island. The norovirus capsid region (314 nucleotides) was amplified by seminested RT-PCR. "A school" denotes the school group that visited hotel A, and "B school" denotes the one that visited hotel B. The phylogenetic tree was constructed by the unweighted-pair group method using arithmetic averages (DNASTAR Inc., Madison, WI). Parentheses provide GenBank accession numbers.

Of five food handlers, three from hotel A and two from hotel B, none developed gastrointestinal symptoms from April to May 2004. However, genogroup I norovirus strains were detected in 2 specimens (one Desertshield [GI.3] strain and one Sindlesham [GI.6] strain) and a genogroup II norovirus strain was detected in 1 specimen (1 Grimsby [GII.4] strain) of 10 stool specimens from the five food handlers (Table 1). One genogroup I sequence was identical to a sequence from one of the case students (Fig. 2).

Noroviruses were detected in the concentrates of two groundwater samples collected on 9 June 2004 from hotel A and hotel B (Table 1) (one Desertshield [GI.3] strain, two Norwalk [GI.1] strains, one Toronto [GII.3] strain, and one Seacroft [GII.6] strain). Phylogenetic analysis showed that the strains in the water samples had 99% sequence homology to the corresponding strains from the case patients (Fig. 2). Both groundwater samples, collected simultaneously with the virus samples, were positive for fecal coliforms.

We conclude that the two outbreaks of gastroenteritis caused by several strains of norovirus can be traced to simultaneous exposures to noroviruses that may have come from contaminated groundwater in the two neighboring hotels. Although norovirus outbreaks have been identified before, few studies have linked the outbreaks with food handlers or environmental constituents by molecular analysis (1, 2, 7, 10). Furthermore, the identification of several norovirus strains in the outbreak (4, 7, 9), the presence of fecal bacteria in the water samples (3, 7), and epidemiological evidence such as dose-response relationships (1) support the inference that contaminated groundwater was the source of these outbreaks.

Jeju Island came into existence when lava spewed from a subsea volcano, forming vesicular volcanic rocks with a high hydrologic conductivity. Groundwater is the major source of water on the island, unlike on the main Korean peninsula. The two hotels are located in the oldest town, Jeju City, where the borehole was constructed long before adequate controls were introduced. We suspect, because of the unusually high turbidity of the groundwater, that the facilities were not operated or maintained properly. It is possible that cracks had formed in the borehole, permitting the introduction of external contamination.

It is not certain whether the hotels in this area share the same groundwater reservoir, although the altitudes of the groundwater reservoirs are similar, i.e., 55 m (hotel A) and 47 m (hotel B). Considering the fact that one genogroup I norovirus strain infecting patients from the school group staying in hotel A was identical to one infecting those from the other school group, we believe that several strains of norovirus may have been circulating in this area and that the groundwater reservoirs may have been exposed to virus contamination. Although we did not confirm any breakdown in the hotel groundwater system, the presence of fecal indicators in the groundwater strongly suggests the existence of an external source of contamination.

In conclusion, we have described two related outbreaks of gastroenteritis caused by several strains of noroviruses which were closely related with the contaminated groundwater.

 
This study was supported by the Korea Center for Disease Control and Prevention (intramural grants 6111-217-207 and 6111-211-207), Seoul, Republic of Korea.

 
* Corresponding author. Mailing address: Division of Enteric and Hepatitis Viruses, Department of Virology, National Institute of Health, 5 Nokbun-dong, Eunpyung-gu, Seoul 122-701, Republic of Korea. Phone: 82-2-380-1494. Fax: 82-2-382-6542. E-mail: ymeejee{at}nih.go.kr.

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1
1. Anderson, A. D., A. G. Heryford, J. P. Sarisky, C. Higgins, S. S. Monroe, S. Beard, C. M. Newport, J. L. Cashdollar, G. S. Fout, D. E. Robbins, S. A. Seys, K. J. Musgrave, C. Medus, J. Vinj, J. S. Bresee, H. M. Mainzer, and R. I. Glass. 2003. A waterborne outbreak of Norwalk-like virus among snowmobilers—Wyoming, 2001. J. Infect. Dis. 187:303-306.[CrossRef][Medline]
2
2. Beller, M., A. Ellis, S. H. Lee, M. A. Drebot, S. A. Jenkerson, E. Funk, M. D. Sobsey, O. D. Simmons, S. S. Monroe, T. Ando, J. Noel, M. Petric, J. P. Middaugh, and J. S. Spika. 1997. Outbreak of viral gastroenteritis due to a contaminated well. JAMA 278:563-568.[Abstract/Free Full Text]
3
3. Boccia, D., A. E. Tozzi, B. Cotter, C. Rizzo, T. Russo, G. Buttinelli, A. Caprioli, M. L. Marziano, and F. M. Ruggeri. 2002. Water-borne outbreak of Norwalk-like virus gastroenteritis at a tourist resort, Italy. Emerg. Infect. Dis. 8:563-568.[Medline]
4
4. Brugha, R., I. B. Vipond, M. R. Evans, Q. D. Sandifer, R. J. Roberts, R. L. Salmon, E. O. Caul, and A. K. Mukerjee. 1999. A community outbreak of food-borne small round-structured virus gastroenteritis caused by a contaminated water supply. Epidemiol. Infect. 122:145-154.[CrossRef][Medline]
5
5. Centers for Disease Control and Prevention. 2001. "Norwalk-like viruses": public health consequences and outbreak management. Morb. Mortal. Wkly. Rep. 50(RR-9):1-17.[Medline]
6
6. Fout, G. S., B. C. Martinson, M. Moyer, D. R. Dahling, and R. E. Stetler. 1996. ICR microbial laboratory manual. U.S. Environmental Protection Agency, Washington, D.C.
7
7. Häfliger, D., P. Hübner, and J. Lüthy. 2000. Outbreak of viral gastroenteritis due to sewage-contaminated drinking water. Int. J. Food Microbiol. 54:123-126.[CrossRef][Medline]
8
8. Kojima, S., T. Kageyama, S. Fukushi, F. B. Hoshino, K. Uchida, K. Natori, N. Takeda, and K. Katayama. 2002. Genogroup-specific PCR primers for detection of Norwalk-like viruses. J. Virol. Methods 100:107-114.[CrossRef][Medline]
9
9. Kukkula, M., L. Maunula, E. Silvennoinen, and C. H. von Bonsdorff. 1999. Outbreak of viral gastroenteritis due to drinking water contaminated by Norwalk-like viruses. J. Infect. Dis. 180:1771-1776.[CrossRef][Medline]
10
10. Parshionikar, S. U., S. Willian-True, G. S. Fout, D. E. Robbins, S. A. Seys, J. D. Cassady, and R. Harris. 2003. Waterborne outbreak of gastroenteritis associated with a norovirus. Appl. Environ. Microbiol. 69:5263-5268.[Abstract/Free Full Text]

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Journal of Clinical Microbiology, September 2005, p. 4836-4839, Vol. 43, No. 9
0095-1137/05/$08.00+0     doi:10.1128/JCM.43.9.4836-4839.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

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