In the period 1992–2000, the Public Health Laboratory Service Communicable Disease Surveillance Centre collected standardized epidemiologic data on 1,877 general outbreaks of
Recent population-based studies have shown that Noroviruses ([NVs] formal name:
Three factors contribute to the considerable impact of disease caused by NV: a large human reservoir of infection (
Gastroenteritis caused by NV is mild and self-limiting in the absence of other factors. Kaplan et al. and others have proposed that NV outbreaks can be recognized on clinical symptoms (short duration and incubation) and epidemiology (high attack rates and high frequency of vomiting) alone (
We describe the epidemiology of NVs in different outbreak settings. The data we present were collected by routine surveillance of general outbreaks of infectious intestinal diseases in England and Wales from 1992 to 2000 (
Since January 1992, the Public Health Laboratory Service Communicable Disease Surveillance Centre has operated a standardized comprehensive surveillance system for general outbreaks of infectious intestinal diseases (see Appendix). The details of how this system operates are described elsewhere (
We used the statistical software package STATA 6.0 for these analyses (
Completed outbreak questionnaires were returned for 5,241 general outbreaks occurring from January 1, 1992, to December 31, 2000 (response rate 73%). Laboratory confirmation of NV was recorded for 1,877 (36%) outbreaks (
Seasonality of all outbreaks and confirmed
Information on setting was available for every NV outbreak (n=1,877). The most common settings were health-care institutions: 754 (40%) outbreaks occurred in hospitals and 724 (39%) in residential-care facilities. Information on the type of unit affected was available for 648 (86%) of 754 hospital outbreaks and 190 (26%) of the 724 in residential-care facilities. NV infection was centered on elderly care and geriatric units in 251 (39%) of 648 hospital outbreaks and 169 (89%) of 190 residential home outbreaks. A total of 147 (7.8%) outbreaks occurred in hotels, 73 (4%) occurred in schools, and 105 (6%) were linked to food outlets (Appendix). Seventy-four outbreaks (3.9%) occurred in other settings such as private homes, holiday camps, and military bases.
A total of 57,060 people were affected in the 1,877 NV outbreaks. After excluding hospital outbreaks (n=711), we recorded 128 hospitalizations (case-hospitalization rate = 33/10,000 cases) from 52 outbreaks (mean hospitalizations per outbreak 0.19; range 0–38). Forty-three deaths (case-fatality rate 7.5/10,000 cases) occurred in 38 outbreaks (mean deaths per outbreak 0.07; range 0–2); all were associated with outbreaks in hospitals (24 deaths) and residential-care facilities (19 deaths).
Reports of NV outbreaks peaked in 1995 (367 outbreaks) (
Seasonality of
The reported modes of transmission were as follows (
| etting of outbreak | Foodbornea | Person to persona | Other/unknowna | Total |
|---|---|---|---|---|
| Hospital | 10 (1.3) | 716 (95.0) | 28 (3.7) | 754 |
| Residential facilities | 33 (4.5) | 658 (91.0) | 32 (4.4) | 723 |
| School | 4 (5.5) | 65 (89.0) | 4 (5.5) | 73 |
| Food outlet | 70 (66.7) | 23 (21.9) | 12 (11.4) | 105 |
| Hotel | 42 (28.6) | 94 (63.9) | 11 (7.5) | 147 |
| Other | 25 (33.8) | 43 (58.1) | 6 (8.1) | 75 |
| Total | 184 (9.9) | 1,599 (85.2) | 93 (5.0) | 1,877 |
aNo. of outbreaks (% of all outbreaks in setting).
Person-to-person spread was reported in 716 (95%) of the 754 hospital outbreaks. This figure was a significantly higher proportion than observed in food outlets (22%; 23/105 [χ2 551.3; p<0.0001], hotels (64%; 94/147 [χ2 175.9; p<0.0001], schools (89%; 65/73 [χ2 27.6; p<0.0001]), or residential facilities (91.0%; 658/723 [χ2 13.9; p=0.0002]). Food outlets were the only setting where foodborne transmission predominated (67%; 70/105).
Person-to-person outbreaks occurred more commonly from November to April than in the rest of the year (1,020/514; ratio 1.98). Foodborne outbreaks showed a significantly weaker seasonality (105/73; ratio 1.43) than person-to-person outbreaks (χ2 3.99; p=0.05).
Specific vehicles were implicated in 72 (39.1%) of the 184 NV outbreaks reported to be transmitted by food. In 12 of these outbreaks, multiple food vehicles were reported, for a total of 86 implicated items. A wide range of food types were reported as vehicles of infection, including oysters, salad vegetables, poultry, red meat, fruit, soups, desserts, and savory snacks. The evidence implicating these food vehicles included cohort studies (55%; 47/86), case-control studies (8%; 7/86), and microbiologic studies (6%; 5/86) (
| Implicated food | Microbiologic evidence | Cohort study | Case-control study | Any evidence | Total no. of outbreaks in which food vehicle implicated |
|---|---|---|---|---|---|
| Oysters | 5 (25%)a | 9 (45%) | 0 | 14(70%) | 20 |
| Poultry | 0 | 6 (67%) | 0 | 6 (67%) | 9 |
| Meat | 0 | 3 (60%) | 0 | 3 (60%) | 5 |
| Fish | 0 | 3 (50%) | 1 (16%) | 4 (67%) | 6 |
| Salads and vegetables | 0 | 10 (59%) | 3 (18%) | 13 (76%) | 17 |
| Other items | 0 | 16 (55%) | 3 (10%) | 19 (65%) | 29 |
| Total | 5 (6%) | 47 (55%) | 7 (8%) | 59 (68%) | 86 |
aPercentages represent outbreaks with evidence per total outbreaks where food vehicle was implicated
Contributory factors were reported in 113 (61%) of the 184 foodborne outbreaks. Infected food handlers were more commonly identified in food-related NV outbreaks (32%; 58/184) than in those caused by other pathogens (9%; 164/1750) (χ2 80.39; p<0.0001). Contamination by an infected food handler was reported less frequently in outbreaks involving oysters than other foods (oysters 0%, other foods 47%; χ2 14.69; p<0.0001). Cross-contamination was also reported less frequently in outbreaks involving oysters than other foods (oysters 5%, other foods 17%; χ2 3.35; p=0.07).
The median duration of outbreaks was 8 days (range 1–139 days). By setting, data on the duration of outbreaks were right-skewed since some outbreaks persisted for exceptionally long periods. The following results are therefore presented as geometric means. The duration of hospital outbreaks (8.8 days; 95% confidence intervals [CI] 8.4 to 9.3) was greater than those in food outlets (3.3 days; 95% CI 2.8 to 3.8; t = –12.699; p<0.0001) and hotels (4.3 days; 95% CI 3.6 to 5.1; t = –7.025; p<0.0001). However, the duration of hospital outbreaks and those in residential facilities did not differ significantly (8.7 days; 95% CI 8.1 to 9.4; t = –0.321; p=0.7) or schools (8.1 days; 95% CI 6.8 to 9.7; t = –0.879; p=0.4) (
| Setting | Median (days) | N | Geometric mean of duration (days)(95% CI)a | t test | p value |
|---|---|---|---|---|---|
| Duration of outbreaks | |||||
| Hospital | 8 | 679 | 8.8 (8.4 to 9.3) | ||
| Residential facilities | 9 | 664 | 8.7 (8.1 to 9.4) | –0.321 | 0.73 |
| School | 8 | 63 | 8.1 (6.8 to 9.7) | –0.879 | 0.40 |
| Food outlet | 3 | 94 | 3.3 (2.8 to 3.8) | –12.699 | <0.0001 |
| Hotel | 5 | 133 | 4.3 (3.6 to 5.1) | –7.025 | <0.0001 |
| Other | 4 | 69 | 4.3 (3.6 to 5.1) | –8.043 | <0.0001 |
| All settings | 8 | 1,702 | 7.7 (7.5 to 8.0) | ||
| Numbers affected per outbreak | |||||
| Hospital | 17 | 751 | 17.5 (16.4 to 18.5) | ||
| Residential facilities | 23 | 723 | 21.5 (19.8 to 23.3) | 4.895 | <0.0001 |
| School | 24 | 73 | 24.9 (20.5 to 30.3) | 3.594 | <0.0001 |
| Food outlet | 23 | 104 | 23.4 (19.8 to 27.6) | 3.444 | 0.001 |
| Hotel | 29 | 147 | 26.5 (23.0 to 30.6) | 5.729 | <0.0001 |
| Other | 29 | 74 | 24.5 (20.2 to 29.7) | 3.432 | 0.001 |
| All settings | 21 | 1,872 | 20.3 (19.7 to 21.1) |
aCI, confidence interval.
The median number of persons affected per outbreak was 21 (range 2–1,200).
Data on the number of people affected in outbreaks were right-skewed since a number of outbreaks were exceptionally large. The following results are therefore presented as geometric means. The number affected in hospital outbreaks (17.5; 95% CI 16.4 to 18.5) was significantly lower than for other settings (geometric means 21.5 to 26.5;
Examination of the features of NV outbreaks by setting reveals that outbreaks in health-care facilities have a distinctive epidemiologic profile. When compared with outbreaks in other settings, those in health-care institutions were unique in exhibiting a winter peak; they were also associated with higher death rates and prolonged duration but were smaller in size and were less likely to be foodborne. School outbreaks shared some but not all of the features that characterize outbreaks in health-care institutions.
Several epidemiologic and biologic reasons may contribute to the divergent seasonality. The respiratory infections season, which increases activity in health-care institutions, occurs concurrently with the peak in NV outbreaks in these facilities. Greater admission of patients in hospitals increases both the population at risk and the opportunities for NV to be introduced. An increase in transfers of people between residential-care facilities and hospitals also facilitates the movement of viruses between institutions. Populations in health-care facilities differ from the rest of the population in that they require nursing care. Health-care settings are semi-closed environments where patients and residents are subject to person-to-person spread and potentially contaminated environments.
Biologic differences between strains may also result in different clinical patterns. NVs from outbreaks in health-care institutions have less genetic diversity compared with those from other settings (
The observation that a hospitalization was associated with 1 in every 40 outbreaks and a death with 1 in every 50 outbreaks calls into question the belief that NV gastroenteritis is a trivial disease. Although we have no information about the other health conditions of patients who were hospitalized or died, these figures are generated from laboratory-confirmed outbreaks. Previous estimates generated by Mead et al. (which were derived from Mounts et al.) were based on the assumption that NV causes a certain proportion of gastroenteritis hospitalizations and deaths (11%), an assumption that was not based on diagnostic results (
Deaths were only reported from outbreaks in health-care institutions. The populations in these institutions differ from those found in other settings by virtue of their greater age or presence of other underlying diseases. While NV infection is not likely the principal cause of death in most cases, this infection might constitute an additional burden on patients already weakened by other conditions and thus become an important contributory factor. In hospital outbreaks, attack rates among staff are similar to those among patients (
The only settings in which foodborne transmission predominated were food outlets. That setting was the only category in which the purchase or consumption of food was the main factor linking at-risk populations. In other settings, living, working, or recreational areas were shared by at-risk populations for varying lengths of time, thus increasing the opportunities for person-to-person spread. Even in those instances where foodborne transmission initiated an outbreak within a health-care institution, high levels of person-to-person spread usually followed. Therefore, prolonged levels of contact between persons in semi-closed institutions such as hospitals, residential-care facilities, and schools facilitate person-to-person spread to an extent not seen in other settings, which in turn leads to more prolonged outbreaks. However, schools differ from health-care institutions in terms of the seasonality and duration of NV outbreaks. In this respect, schools are more like hotels, food outlets, and other settings.
The number of affected persons was smaller in hospital outbreaks than in all other settings. This finding may reflect the lack of a universally employed definition of the spatial boundaries of an outbreak. In some hospitals, each unit affected was reported as a separate outbreak, resulting in smaller but more numerous outbreaks. In addition, cases that occur in institutions are more easily recognized as part of an outbreak than cases in open settings or the community. Thus, smaller outbreaks occurring in open settings might not be recognized or reported to investigating agencies.
The peak in recorded outbreaks seen in the winter of 1995–1996 can largely be seen as a consequence of enhanced surveillance through the development of the Public Health Laboratory Service electron microscopy network. However, there are anecdotal reports of an increase in workload in these laboratories, and other countries also recorded an increase in NV activity during the same period (
Biases in different surveillance systems partly explain the wide variation in estimates of the levels of foodborne transmission in NV outbreaks. The data presented in this report suggest foodborne transmission in 10% of outbreaks in England and Wales. Estimates in Sweden (16%) (
The data sources that contribute to a surveillance system are a key factor affecting the estimate of the importance of foodborne transmission. In England and Wales, surveillance is broad-based and collects reports on outbreaks spread by all modes of transmission from a range of public health professionals such as physicians, environmental health officers, and diagnostic laboratories. By contrast, FoodNet, a U.S. network, is designed to detect foodborne infections (
The importance of NV as a cause of gastroenteritis outbreaks in U.S. nursing homes has been demonstrated by Green et al. (
The link between oysters and NV infection is well described (
These data, which show NV as the causative agent in 36% of outbreaks, support previous reports that NVs are the most common cause of infectious intestinal diseases in industrialized nations (
These analyses demonstrate the value of maintaining standardized outbreak surveillance over an extended period. By examining the epidemiologic characteristics of general outbreaks of NV by setting, we demonstrated that this pathogen is not merely an extremely common cause of infectious intestinal diseases but that its effects vary widely according to the population at risk. Within health-care institutions, NV contributes to substantial illness and is associated with substantial numbers of deaths. The elucidation of a distinct outbreak pattern that is characteristic of health-care institutions suggests that a combination of host, virologic, and environmental factors mediate these divergent epidemiologic patterns. Focused research studies need to be developed to investigate the population as well as the microbiologic and behavioral processes that might explain these observations. In addition, population-based studies incorporating virus typing are required to gain a deeper understanding of the epidemiology of sporadic NV infection in the wider population. Such studies are a prerequisite to the development of firm evidence-based and targeted control strategies.
We thank André Charlett for reviewing the statistical methods of this report and Sue LeBaigue and Sally Long for their assistance with the gastrointestinal diseases outbreak database. We thank the environmental health officers, consultants in communicable disease control, infection control officers, and virologists who conducted the outbreak investigations presented here.
Mr. Lopman works as an epidemiologist at the Gastrointestinal Diseases Division of the Public Health Laboratory Service Communicable Disease Surveillance Centre. His work focuses on the epidemiology of viral gastroenteritis in health-care settings and coordination of epidemiologic surveillance for the Foodborne Viruses in Europe Consortium.