Raw oyster consumption and outbreaks of viral gastroenteritis in New Zealand: evidence for risk to the public's health

OBJECTIVE: To investigate the relationship between consumption of raw Pacific half shell oysters and outbreaks of Norwalk-like virus (NLV) gastroenteritis in Auckland in the last third of 1999. METHOD: Ten outbreaks were investigated as retrospective cohorts using standardised questionnaires relating to food and drink exposures. Trace back of oysters and site inspections of implicated commercial growing areas were performed. Virological analyses compared oysters linked to outbreaks and faecal samples from cases. RESULTS: Eighty-six cases were identified, of whom 32 (37.2%) were confirmed NLV positive on faecal analysis. The summary risk estimate for illness among oyster consumers for all outbreaks was RR 8.23 (95% CI 4.55-14.90; p< 0.001) and in five of seven outbreaks permitting statistical analysis, the risk for those consuming raw oysters was greater than five-fold that of non-consumers. NLVs were identified in two batches of oysters from different growing areas, implicated in four outbreaks. In both the strain (Genogroup II/3 'Mexico-like virus') from cases matched that in the oysters from the same harvest batch. CONCLUSION: The epidemiological and virological evidence implicates oysters as the source of a number of outbreaks of NLV gastroenteritis. This is the first time NLVs have been identified in commercially farmed Pacific oysters in New Zealand. Sewage effluent from recreational boats was the likely source of faecal contamination of growing waters in one site. IMPLICATIONS: Combined use of virological and epidemiological methods have proved invaluable in investigating NLV outbreaks. Further research is needed into enteric viral contamination of commercial oyster farms.     

Snow Mountain agent gastroenteritis from clams

A 1983 investigation of two clambake-related gastroenteritis outbreaks in Rochester, New York, showed that 84 (43%) of 196 persons interviewed had an acute illness characterized by watery diarrhea, vomiting, and abdominal cramps. None of the ill persons were hospitalized or had complications. Illness was associated with eating raw (p = 0.002) or baked (p less than 0.01) hard-shell clams, with the risk of illness increasing with the total number of clams consumed (p less than 0.01). The median incubation period and duration of illness were 36 and 44 hours, respectively. Stool samples obtained 2-4 days after onset of illness were negative for commonly recognized bacterial and viral pathogens. However, of 31 persons whose stools were tested, the stool of only one ill person was positive by enzyme-linked immunosorbent assay for the Snow Mountain agent, one of the Norwalk-like viruses. Paired serum specimens from six (67%) of nine ill and two (29%) of seven well persons showed a fourfold or greater rise in antibody titer to Snow Mountain agent. Persons who ate clams were more likely to seroconvert to Snow Mountain agent (eight of 12) than were those who did not eat clams (zero of four) (p = 0.04). The clams were harvested off the coast of southern Massachusetts in late October, when harvest waters were documented to be contaminated by untreated municipal sewage. This report describes the first documented outbreak of shellfish-associated gastroenteritis attributed to Snow Mountain agent of which we are aware.     

The frequency of a Norwalk-like pattern of illness in outbreaks of acute gastroenteritis.

Records of 642 outbreaks of acute gastroenteritis were reviewed to determine the proportion of outbreaks that were clinically and epidemiologically consistent with Norwalk-like virus infection. Using as our criteria stool cultures negative for bacterial pathogens, mean (or median) duration of illness 12-60 hours, vomiting in greater than or equal to 50 per cent of cases, and, if known, mean (or median) incubation period of 24-48 hours, we found that 23 per cent of waterborne outbreaks, 4 per cent of foodborne outbreaks, and 67 per cent, 60 per cent, and 28 per cent of outbreaks in nursing homes, in summer camps, and on cruise ships, respectively, satisfied the criteria for Norwalk-like pattern. Of 54 outbreaks that satisfied the criteria for Norwalk-like pattern, 14 were investigated for virus etiology. Ten of these (71 per cent) yielded serologic evidence of Norwalk-like virus infection. Norwalk-like viruses are probably an important cause of outbreaks of acute gastroenteritis. Investigation for Norwalk virus antibody in outbreaks that are clinically and epidemiologically consistent with Norwalk-like virus infection is likely to yield diagnostically useful results.     

Outbreaks of Norwalk-like viral gastroenteritis--Alaska and Wisconsin, 1999

Norwalk-like viruses (NLVs) are the most common cause of epidemic gastroenteritis in the United States, resulting in illness in approximately 23 million persons each year . Persons of all ages are affected because previous infection confers only short-term immunity. Most NLV gastroenteritis outbreaks involve foodborne or person-to-person transmission. This report presents investigations of a foodborne NLV outbreak in Alaska and person-to-person transmission in Wisconsin.     

Investigation of an outbreak of gastroenteritis caused by Norwalk-like virus, using solid phase immune electron microscopy

In February 1993, 95 persons (47 patients and 48 staff members) were affected by an hospital outbreak of viral gastroenteritis. Using direct electron microscopy (EM) the causative agent was identified as a small round structured virus. This was confirmed as a Norwalk-like virus using solid phase immune electron microscopy (SPIEM). Of 94 stool samples examined, 12 (13%) samples containing small round structured viruses (SRSV) were SPIEM positive for Norwalk-like virus. A further 25 (27%) samples contained small round featureless virus (SRFV) identified by direct EM and were negative on SPIEM. The illness was characterized by preceding influenza-like symptoms in 76% of cases followed by vomiting (76%), diarrhoea (79%) and abdominal pain (79%). One fatality was recorded. The outbreak lasted for 15 days, with a peak incidence of new cases amongst patients and staff occurring on day 5. It was controlled through a combination of ward closures, patient cohorting, suspension of duties for affected staff and disinfection procedures. Difficulties were encountered in the education of staff and in the implementation of environmental control measures. Screening of hospital catering services and a case control study, carried out among affected staff members, failed to identify a foodborne source. Consumption of tap water in the hospital was commoner among affected staff members than among controls, but this did not reach significance (P = 0.1).     

A large Clostridium perfringens foodborne outbreak with an unusual attack rate pattern

On November 7, 1985, a Clostridium perfringens gastroenteritis outbreak occurred in approximately 44% of the 1,362 employees at a Connecticut factory. Although the same foods were served to all three shifts at an employee banquet on November 6, the attack rate was almost twice as high for those who ate on the day shift (attack rate = 50%) than for those on the evening shift (attack rate = 20%) or night shift (attack rate = 29%). Among employees of the day shift, attack rates were highest for those who ate during the first 30 minutes of the 2.5-hour day shift serving period and decreased throughout the serving period. The one-hour evening shift serving period had a similar trend toward higher attack rates earlier in the serving period. Four main-course foods were significantly associated with illness, and over 95% of the employees had eaten each of them. Stratified analysis indicated that gravy was the responsible food and, furthermore, that the decreasing attack rate pattern within serving periods occurred only for those who ate gravy. The gravy had been prepared 12-24 hours in advance of banquet service. After it was prepared, the gravy was improperly cooled and was reheated shortly before and throughout the serving periods. Persons who ate gravy that had been reheated for the longest period of time had the lowest attack rate, probably because they were exposed to a lower concentration of organisms. This outbreak underscores the need for properly reheating food to prevent C. perfringens gastroenteritis and suggests that analysis of attack rate trends may provide important epidemiologic clues to understanding the causes of foodborne disease outbreaks.     

Outbreak of Norwalk virus in a Caribbean island resort: application of molecular diagnostics to ascertain the vehicle of infection

In 1998, an outbreak of gastroenteritis affected at least 448 persons including 122 staff at a resort hotel in Bermuda. A survey among staff indicated that gastroenteritis was associated with eating or drinking at the hotel (OR = 60, 95% CI = 2.4-15.1). Multiple specimens of drinking water had elevated faecal coliform levels and Escherichia coli present, suggestive of faecal contamination. Stools from 18 of the 19 persons with gastroenteritis that were tested were positive for genogroup-II Norwalk-like viruses (NLVs). RT-PCR analysis of a 31 specimen of water produced a genogroup-II NLV genome with a sequence identical to that of NLVs in the stools of three ill persons. This outbreak shows the value of new molecular diagnostics to link illness with a contaminated source through the use of sequence analysis. The risk of outbreaks such as these could be reduced in tourism dependent regions like Bermuda and the Caribbean by regular evaluation of data from the inspection and monitoring of drinking water supplies and waste water systems, by ensuring the chlorination of supplemental drinking water supplies and by establishing food-safety initiatives.     

Outbreaks of gastroenteritis caused by SRSVs from 1987 to 1992 in Kyushu, Japan: Four outbreaks associated with oyster consumption

From 1987 to 1992, 18 outbreaks of acute non-bacterial gastroenteritis occurred in Kyushu district. The most common symptoms were diarrhea, vomiting, nausea and abdominal cramp. Small round structured viruses (SRSVs) were detected in 52 (44.8%) of 116 stool samples from 17 outbreaks by the electron microscopy (EM) method, and a significant increase in the antibody level was noted in 42 (80.7%) of 52 paired serum samples from 12 outbreaks by the immune electron microscopy (IEM) method and in 18 (51.4%) of 35 samples from 8 outbreaks by the western blot (WB) method. However, according to the WB method, antigen-antibody reaction was not observed to reference antigen strips (SRSV-9/Tokyo 86-510, 63kDa) in three of the 8 outbreaks. The detected virus was regarded as an etiologic agent for these outbreaks. In four of 5 outbreaks which appeared associated with eating raw oysters, there was a close relation between SRSV infection and consumption of raw oysters.     

Outbreaks of Norwalk-like virus-associated gastroenteritis traced to shellfish: coexistence of two genotypes in one specimen.

We determined the nucleotide sequences of Norwalk-like viruses in 10 PCR products from stool or oyster specimens obtained from four outbreaks of gastroenteritis in which shellfish was suspected as the cause in Shizuoka prefecture in Japan between 1987-94. The sequences were determined from nucleotide positions 4561-4852 (292 bp) in the polymerase region. Two types of sequences were detected. One (genotype 1) had 87% sequence homology with the prototype Norwalk virus, and the other (genotype 2) had 59% sequence homology. The sequences from isolates belonging to the same genotype were almost the same regardless of the year of isolation. Because sequences of 2 genotypes were detected in 2 of the 4 outbreaks, nested PCR was performed with genotype-specific primers to detect the presence of 2 genotypes in the same specimen. In 5 of 10 specimens, PCR bands were detected with both genotype-specific primers, indicating the coexistence of 2 genotypes in 1 specimen. We also detected two genotypes of Norwalk-like virus in an oyster from a sample implicated in one of the outbreaks which may provide direct evidence of oysters as the cause of the gastroenteritis.     

A norovirus outbreak associated with consumption of NSW oysters: implications for quality assurance systems

Norovirus is a common cause of gastroenteritis outbreaks associated with raw shellfish consumption. In Australia there have been several reports of norovirus outbreaks associated with oysters despite the application of regulatory measures recommended by Food Standards Australia New Zealand. This study describes an outbreak of norovirus gastroenteritis following the consumption of New South Wales oysters. In September 2007, OzFoodNet conducted a cohort study of a gastroenteritis outbreak amongst people that had dined at a Port Macquarie restaurant. Illness was strongly associated with oyster consumption, with all cases having eaten oysters from the same lease (RR undefined, p < 0.0001). Norovirus was detected in a faecal specimen. Although no pathogen was identified during the environmental investigation, the source oyster lease had been closed just prior to harvesting due to sewage contamination. Australian quality assurance programs do not routinely test oysters for viral contamination that pose a risk to human health. It is recommended that the feasibility of testing oysters for norovirus, particularly after known faecal contamination of oyster leases, be assessed.     

Norovirus outbreak in Majorca (Spain) associated with oyster consumption

We describe investigation into an outbreak of norovirus gastroenteritis associated with oyster consumption. A survey was conducted in 346 exposed persons, 266 of whom were cases. Only 14 feces samples from patients were sent to the National Microbiology Laboratory. Oysters collected at the production site were sent to the National Food Center. The oysters met the microbiological quality standard required before sale, which did not include virus investigation. Epidemiological analysis showed an association between gastroenteritis and consumption of oysters (OR = 60.4; 95% CI: 26.2-139.3) and razor shells (OR = 3.13; 95% CI: 1.4-6.9). Microbiological analysis confirmed norovirus in affected individuals but not in the oysters that had been tested after a longer purification period than those consumed. Food with a special risk of norovirus transmission should be strictly monitored. Investigators should dispose of the necessary laboratory resources to study food-borne norovirus outbreaks.     

A large foodborne outbreak of norovirus in diners at a restaurant in England between January and February 2009

An outbreak of gastroenteritis affected at least 240 persons who had eaten at a gourmet restaurant over a period of 7 weeks in 2009 in England. Epidemiological, microbiological, and environmental studies were conducted. The case-control study demonstrated increased risk of illness in those who ate from a special 'tasting menu' and in particular an oyster, passion fruit jelly and lavender dish (odds ratio 7·0, 95% confidence interval 1·1-45·2). Ten diners and six staff members had laboratory-confirmed norovirus infection. Diners were infected with multiple norovirus strains belonging to genogroups I and II, a pattern characteristic of molluscan shellfish-associated outbreaks. The ongoing risk from dining at the restaurant may have been due to persistent contamination of the oyster supply alone or in combination with further spread via infected food handlers or the restaurant environment. Delayed notification of the outbreak to public health authorities may have contributed to outbreak size and duration.     

Practical lessons from the management of an outbreak of small round structured virus (Norwalk-like virus) gastroenteritis

An outbreak of viral gastroenteritis caused illness in 92 people during October 2000. All the cases had an association with one hotel and 80% of cases identified had attended one of two buffet meals on 18th October 2000. Cohort analysis did not implicate any particular foodstuff in this outbreak. All bacteriological tests on food samples were negative. Small round structured virus (SRSV)/Norwalk-like virus (NLV) particles were seen by electron microscopy in 6 out of 27 stool samples submitted for analysis. This paper describes the outbreak and in particular the lessons learned from the management and control of it. These include practical points with regard to the outbreak control team, liaison with the microbiology laboratory, handling data, agreeing a case definition, and occupational health issues. All can be applied elsewhere by those responsible for managing outbreaks at a local level.     

An outbreak of Norwalk-like gastroenteritis associated with contaminated drinking water at a caravan park

Abstract: During the 1989 Christmas holiday period, a large outbreak of gastroenteritis occurred among persons staying at a caravan park in southern New South Wales. Review of local hospital records found that 77 per cent of patients presenting with infective diarrhoea between 29 December and 3 January had stayed at the caravan park. In a retrospective cohort study we compared rates of illness among caravan park patrons exposed to different water sources. Stools were tested for pathogens and convalescent sera for viral antibodies. Rain and reticulated river water sampled from the caravan park were tested for bacteria and viruses. Of 351 persons interviewed at the caravan park, 305 (87 per cent) reported an illness characterised by diarrhoea, vomiting and abdominal pain. Of 196 persons who used reticulated river water for drinking or ablutions, 175 (89 per cent) became ill compared with 47 of 72 persons (65 per cent) who did not use this water (relative risk 1.4, 95 per cent confidence interval 1.2 to 1.6). The outbreak was probably caused by a 27–28 nm small round structured virus found in the stool from one ill person. High levels of faecal coliforms in the reticulated river water and enterovirus in sediment samples suggest that the outbreak was caused by sewage contaminating the reticulated river water through a break in the pipe directly over the underground water tanks. To prevent such outbreaks, poor water and sewerage system layouts should be avoided and nonpotable water should be clearly labelled. Where feasible, all camping-ground water should stem from town supplies.     

"Norwalk-like viruses". Public health consequences and outbreak management.

"Norwalk-like viruses" (NLVs) cause outbreaks of gastroenteritis and are spread frequently through contaminated food or water. Molecular diagnostics now enables detecting viruses in clinical and environmental specimens, linking of NLV strains causing outbreaks in multiple geographic locations, and tracing them to their sources in contaminated food or water. This report reviews recent advances in NLV detection and provides guidelines and recommendations for investigating NLV-related outbreaks, including specimen collection and disease prevention and control. This report also updates information provided in CDC's previously published, Viral Agents of Gastroenteritis: Public Health Importance and Outbreak Management (MMWR 1990;39 [No. RR-5]: 1-24). These CDC recommendations are intended for public health professionals who investigate outbreaks of acute gastroenteritis but could be useful in academic and research settings as well.