Viral gastroenteritis outbreaks caused by caliciviruses (i.e., Norwalk-like viruses or small round-structured viruses) have been associated with eating contaminated shellfish, particularly oysters (Crassostrea virginica) (1-3). This report describes the findings of the investigation of an outbreak of oyster-associated viral gastroenteritis in Louisiana during the 1996-97 winter season and implicates sewage from oyster harvesting vessels as the probable cause of contaminated oysters.

On December 30, 1996, the Louisiana Office of Public Health (LOPH) was notified about a cluster of six persons who had onset of gastroenteritis after eating raw oysters on December 25. During December 30, 1996-January 3, 1997, three additional clusters were identified. In all four clusters, ill persons had eaten oysters harvested from Louisiana waterways. LOPH notified all state epidemiologists in the United States about the apparent association of gastroenteritis with eating oysters and requested reports of suspected cases.

A case of gastroenteritis was defined as three or more watery stools or vomiting within a 24-hour period, with onset during December 15-January 9. A cluster of oyster-related cases was defined as a group of three or more persons who had shared a common meal, at least one of whom had eaten oysters and at least one of whom developed gastroenteritis. Sixty clusters comprising 493 persons were reported from Alabama, Florida, Georgia, Louisiana, and Mississippi, and all were included in the subsequent traceback investigation. Of the 60 clusters, data were included in the descriptive analysis of the illness only for those 34 clusters for whom all persons in a cluster could be interviewed. The 34 clusters comprised 290 persons who completed interviews and were included in the descriptive analysis; 271 of 290 persons supplied information on oyster consumption.

Onsets of illness occurred during December 21-January 7 (Figure_1). Of the 290 persons interviewed, 179 (62%) had symptoms that met the case definition. The most common symptoms were diarrhea (83%), abdominal cramps (78%), vomiting (58%), headache (50%), and fever (50%). The median incubation period was 38 hours (range: 8-90 hours), and the median duration of illness was 2 days (range: 1-14 days). The median age of case-patients was 42 years (range: 14-83 years), and 111 (62%) were male. The number of reported cases peaked during December 31-January 5 (Figure_1); the harvest dates of subsequently implicated oysters ranged from December 15 to January 1. Of 201 persons who ate raw oysters, 153 (76%) became ill, compared with 13 (19%) of 70 persons who did not eat raw oysters (risk ratio=4.0). Small round-structured viruses were found by direct electron microscopy in fecal specimens from eight of 11 ill persons. Sequence analysis of nucleic acid from eight specimens representing six clusters demonstrated three unique genetic sequences that corresponded with oysters harvested from three separate harvest sites. Small round-structured viruses were detected in oysters, but genetic sequencing could not be conducted.

The LOPH traced oysters eaten by ill persons to retailers, wholesalers, and harvesters. Restaurants and seafood markets were inspected to observe handling and storage of shellfish, and tags that identified the date and site of harvesting and the harvester's identification number were obtained from purchasers and retailers of sacks that were definitely or possibly implicated. Retailer records were cross- referenced with records from wholesalers and harvesters to establish the accuracy of information about harvester and site of harvest. Oysters associated with the 60 clusters were traced to 26 retailers, 11 wholesalers, and 20 harvesters. Records from several wholesalers did not agree with the information on the oyster sack tag.

As of February 15 (6 weeks after notification of the outbreak), LOPH, despite repeated attempts, had been successful in completing interviews with only three of 20 harvesters about the date and specific location of harvesting of potentially contaminated oysters. However, with the assistance of Louisiana Department of Wildlife and Fisheries, 12 additional harvesters were interviewed. Of eight oyster harvesting boats inspected, seven had inadequate sewage collection and disposal systems.

Testing by the LOPH Molluscan Shellfish Program determined that a toxic algal bloom, which causes paralytic shellfish poisoning, was present in Louisiana's northeastern waterways beginning November 13, 1996; these findings prompted LOPH to close these waterways that day and required harvesters to move to southeastern harvest sites. In addition, on November 15, a freshwater diversion was opened to decrease the salinity and eliminate the algal bloom in the northeastern waters; the diversion also decreased the salinity in the southeastern waters.

On January 3, 1997, LOPH mandated an emergency closure of eight waterways with suspected contamination southeast of the Mississippi River, and on January 6, LOPH recalled oysters harvested from these sites after December 22, 1996. On January 23, 1997, harvesting was permitted to resume, and no additional cases of oyster-associated gastroenteritis were reported.

Reported by: TA Farley, MD, L McFarland, PhD, Epidemiology Section, Louisiana Dept of Health and Hospitals. M Estes, K Schwab, Baylor Univ, Dept of Virology, Houston, Texas. Viral Gastroenteritis Section, Respiratory and Enteric Viruses Br, Div of Viral and Rickettsial Diseases, National Center for Infectious Diseases; Div of Applied Public Health Training (proposed), Epidemiology Program Office, CDC.

Editorial Note

Editorial Note: Caliciviruses are small single-stranded RNA viruses that cause acute gastroenteritis characterized by vomiting and/or diarrhea (4). The viruses are difficult to detect, requiring relatively sophisticated molecular methods to identify the virus in fecal specimens and in oysters. There is no reliable marker for indicating presence of the virus in oyster harvesting waters.

This report represents the third oyster-related gastroenteritis outbreak attributed to calicivirus in Louisiana since 1993. An outbreak in 1993 accounted for cases of illness in 73 persons in Louisiana and approximately 130 persons in other states (5) who had consumed oysters from Louisiana. In that outbreak, a harvester with a high level of immunoglobulin A to Norwalk virus reported having been ill before the outbreak and admitted to dumping sewage directly into harvest waters. The findings of the investigation of that outbreak suggested that one ill harvester could contaminate large quantities of oysters in a relatively large oyster bed (6). An oyster-associated outbreak in 1996 was attributed to a malfunctioning sewage disposal system on an oil rig on which some workers had been ill with Norwalk-like gastroenteritis (LOPH, unpublished data, 1997). However, harvesters dumping feces overboard could not be excluded as an additional source of oyster contamination. In both outbreaks, recommendations focused on proper sewage disposal and its regulation.

In this outbreak, the link to the large number of wholesalers and retailers suggests that the oyster contamination preceded distribution and probably occurred in the oyster beds. In addition, harvest sites were 12-15 miles from the nearest community sewage outlet, recreational boating was infrequent in December, commercial boating traffic was infrequent because of the shallow depth of the water, and all oil rigs were considered to have had adequate sewage facilities. The only known source of caliciviruses, such as that implicated in this outbreak, is feces from ill persons. Therefore, based on these considerations, the probable source of human sewage found in the implicated waterways was oyster harvesters, who admitted to routinely discharging their sewage overboard, despite recent recommendations in Louisiana for proper sewage collection and disposal (6; LOPH, unpublished data, 1997).

In previous outbreak investigations, molecular tracebacks generally identified a single strain from a single source. A distinguishing feature of this outbreak was its protracted duration and involvement of three geographically separate harvest sites, each associated with a unique strain of calicivirus. These characteristics suggest a contributory role for different oyster harvesters who were concurrently infected with genetically distinct strains of calicivirus, and each of whom dumped their sewage in different waterways, possibly when environmental conditions (e.g., low water temperatures and decreased salinity) facilitated contamination of oysters with calici- viruses.

Findings in this investigation underscore some of the inadequacies in both the current sewage-disposal practices of oyster harvesting vessels and the oyster tagging system designed to reduce the risk for and magnitude of oyster-associated gastroenteritis outbreaks. Oyster-related outbreaks of viral gastroenteritis probably will continue unless seafood regulators and the oyster industry develop, adopt, and enforce standards for the proper disposal of human sewage from oyster harvesting vessels. Traceback investigations of oysters in outbreaks such as this are difficult because of the prevalence of mislabeling in wholesalers' records and on oyster tags and because harvest identification numbers cannot be consistently traced to harvesters. In this investigation, the inability to accurately trace many of the contaminated oysters hampered efforts to contain the outbreak and prevent recurrences and caused a recall of more products than may have been necessary.

Prevention of oyster-related outbreaks of gastroenteritis requires intensified efforts to 1) develop and enforce laws for appropriate sewage containers on oyster harvesting boats with dump-pumpout stations at docks, 2) educate workers in the oyster industry about the consequences of improper sewage disposal, 3) improve record- keeping by oyster harvesters, wholesalers, and retailers to enhance the reliability of traceback investigations, and 4) further assess the relation between environmental conditions and contamination of oysters.

References

1. Murphy AM, Grohmann GS, Christopher PJ, Lopez WA, Davey GR, Millsom RH. An Australia-wide outbreak of gastroenteritis from oysters caused by Norwalk virus. Med J Aust 1979;2:329-33.

2. Gill ON, Cubitt WD, McSwiggan DA, Watney BM, Bartlett CL. Epidemic of gastroenteritis caused by oysters contaminated with small round structured viruses. Br Med J {Clin Res} 1983;287:1532-4.

3. Gunn RA, Janowski HT, Lieb S, Prather EC, Greenberg HB. Norwalk virus gastroenteritis following raw oyster consumption. Am J Epidemiol 1982;115:348-51.

4. Estes MK, Atmar RL, Hardy ME. Norwalk and related diarrhea viruses in clinical virology. New York, New York: Churchill Livingstone, 1997:1073-95.

5. Dowell SF, Groves C, Kirkland KB, et al. A multistate outbreak of oyster-associated gastroenteritis: implications for interstate tracing of contaminated shellfish. J Infect Dis 1995;171: 1497-503.

6. Kohn MA, Farley TA, Ando T, et al. An outbreak of Norwalk virus gastroenteritis associated with eating raw oysters: implications for maintaining safe oyster beds. JAMA 1995;273:466-71.

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