A Foodborne Norovirus Outbreak at a Hospital and an Attached Long-Term Care Facility

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1 Jpn. J. Infect. Dis., 62, , 2009 Original Article A Foodborne Norovirus Outbreak at a Hospital and an Attached Long-Term Care Facility Kazuhiro Ohwaki*, Haruko Nagashima 1, Makoto Aoki 2, Hiroko Aoki 2, and Eiji Yano Department of Hygiene and Public Health, Teikyo University School of Medicine, Tokyo ; 1 Green Garden Seiju, Tokyo ; and 2 Aoki Hospital, Tokyo , Japan (Received April 8, Accepted October 20, 2009) SUMMARY: We investigated a foodborne norovirus outbreak in a hospital and an attached long-term care facility (LTCF). An at-risk group of 698 people was identified, which included staff, hospital patients, LTCF residents, and adult daycare users who shared consumption of food prepared in a central kitchen. Three different diets were prepared in three separate sections: a standard diet, a special diet, and a diet for residents at the LTCF. During the first 3 days of the outbreak, 47 (16%) of 285 staff members and 55 (13%) of 413 patients became symptomatic. Eating the standard diet was significantly associated with a risk of illness for staff members (relative risk [RR], 18.13; 95% confidence interval [CI], ) and patients (RR, 2.12; 95% CI, Some stool samples were positive for norovirus GII/4. The standard diet may have been contaminated while being prepared in the central kitchen. INTRODUCTION Noroviruses are a common cause of acute gastroenteritis. The onset of illness is usually rapid, often with no prodrome. Incubation periods are generally 24 to 48 h, although ranges from 15 to 60 h have been observed (. Norovirus was first recognized in association with point-source outbreaks of acute gastroenteritis (, and such outbreaks remain the most common situation in which norovirus has been implicated as the etiological agent. Noroviruses have been identified as responsible for approximately half of all outbreaks of gastroenteritis worldwide (3). In Japan, foodborne norovirus infection has been noted since 1997, and the proportion of gastroenteritis outbreaks attributed to norovirus increased from 4.2% in 1998 to 35% in 2006 (4,5). Noroviruses are difficult to study because they cannot be cultivated in culture media, and no animal model is yet available for experimental studies. Until recently, a lack of widely available and sensitive diagnostics limited understanding of the epidemiology and disease burden of norovirus. The development of molecular assays such as reverse transcription polymerase chain reaction (RT-PCR) in the early 1990s (6) allowed sequencing of infectious agents and a better appreciation of noroviruses as a major cause of foodborne disease. Most new knowledge regarding the sources of outbreaks must come from investigations of naturally occurring outbreaks, although volunteer studies have also produced valuable information (7). It is well known that individuals in healthcare settings, such as hospital staff and patients and nursing home staff and residents, are at high risk for outbreaks of infectious diseases (8-1. Furthermore, the elderly and chronically ill are particularly vulnerable to complications resulting from gastroenteritis, such as dehydration and aspiration of vomitus (12,13). Norovirus can be transmitted through contaminated food or *Corresponding author: Mailing address: Department of Hygiene and Public Health, Teikyo University School of Medicine, Kaga, Itabashi, Tokyo , Japan. Tel: , Fax: , ns-waki@med.teikyo-u.ac.jp water, directly from person-to-person, and occasionally by airborne vomitus droplets (14-17). Infected food handlers who work despite manifest diarrhea or vomiting are also a common cause of foodborne norovirus outbreaks (1,18-23). Contaminated fomites in the environment have also been suggested as a possible source of infection (24-28). Among hospitalized patients and nursing home residents, fecal incontinence, dementia, and immobility are common and may facilitate the spread of infection by fecal pathogens. Norovirus outbreaks in healthcare institutions spread rapidly, have high attack rates, and are difficult to control (24,29-33). Nevertheless, there is a paucity of detailed descriptions of foodborne outbreaks of norovirus infection in such settings (18). We investigated a foodborne norovirus outbreak in a hospital and an attached long-term care facility (LTCF) during 2007 in Japan using an epidemiological method to identify the likely route of contamination. MATERIALS AND METHODS Outbreak background: On 22 February 2007, an outbreak of gastroenteritis clustered in a hospital was reported to the local public health center by a hospital director. The cluster began on 21 February. The hospital had a 50-bed medical ward (2nd floor) and a 270-bed psychiatric ward (3rd-7th floors) and was located in a suburban setting in Tokyo, Japan. An attached LTCF was located at the same site. Members of the hospital and LTCF staff were also affected, causing considerable organizational difficulty in the affected institutions. Staff members of the hospital and LTCF, hospital patients, LTCF residents, and users of an adult daycare service all consumed food prepared in a central kitchen located at the LTCF. Based on the review of the clinical symptoms and the positive test results for the virus in 23 stool samples, norovirus was suspected as the etiological agent responsible for the outbreak. Epidemiological investigation: A retrospective cohort study was performed to identify the likely source of the outbreak. Self-administered questionnaires were distributed to 450

2 all staff members and patients, including LTCF residents and daycare users, to screen for symptoms of gastroenteritis during the outbreak period, and food intake histories were recorded for the 2 days immediately before the outbreak (19 and 20 February 2007). Information was obtained on the following: demographic data, clinical onset, symptoms (diarrhea, vomiting, and fever), workplace or type of ward, and intake of diet types served by the facility. Laboratory investigation: Stool specimens were collected from nine symptomatic patients (all hospital patients) and 23 kitchen workers, including eight symptomatic workers. All samples sent to the local health authorities were tested for norovirus using RT-PCR methods (34). In addition, samples were tested for Shigella, Salmonella, the O157 strain of Escherichia coli, Vibrio, Clostridium perfringens, Yersinia, Campylobacter, Bacillus cereus, Aeromonas, Plesiomonas, and Staphylococcus aureus. The kitchen underwent on-site inspection on 22 February. Frozen samples of all food items served between 18 and 21 February were available and were examined for norovirus using real time RT-PCR methods (34). Swabs from 20 environmental fomites (e.g., the hands of nine kitchen workers, the inside wall and handle of the refrigerator, the kitchen sink, and the kitchen counter) were also examined. Statistical analysis: Attack rates for the categorical variables were compared using Fisher s exact test, and age data were compared using Wilcoxon s rank sum test. Relative risk (RR) and 95% confidence intervals (CI) were calculated for consumption of each diet type. Data analyses were performed separately for staff members and patients (including LTCF residents and daycare users). Values of P < 0.05 were considered significant, and analyses were conducted using SAS software. RESULTS Epidemiological investigation: The source population consisted of 698 people, including 285 members of the affected hospital and LTCF staff (including 26 kitchen workers). During the outbreak period, there were 287 patients at the hospital, 83 residents at the LTCF, and 43 daycare users. The staff members were 22% male and their ages ranged from 20 to 78 years (median age, 47 years). The patients (including LTCF residents and daycare users) were 51% male and their ages ranged from 22 to 98 years (median age, 63 years). There were 157 individuals with self-reported diarrhea, vomiting, or fever between 20 February and 4 March. Of these, 64 were staff members, including 10 kitchen workers. Figure 1 illustrates the course of the outbreak. The epidemic curve depicts an explosive outbreak with a prolonged period of ongoing incident cases. Of the 157 individuals who showed symptoms, 102 were affected synchronously between 1:30 p.m. on 20 February and 11 p.m. on 22 February (1-59 h after lunch on 20 February). Taking into account the short incubation period of norovirus (24-48 h), 19 February and 20 February were considered the relevant days on which highrisk food exposure would have occurred. Daycare users ate the same lunch as staff and patients/residents and were also affected. These observations suggested that lunch on 20 February was the potential source of the outbreak. As we sought to investigate the cause of the foodborne outbreak, a case was defined as a person with self-reported diarrhea, vomiting, or fever during the first 3 days (20-22 February) of the outbreak in subsequent analyses. Fig. 1. Onset of symptoms among the patient cases and staff cases of a hospital and a long-term care facility (LTCF) during a norovirus outbreak from February to March Table 1. Comparison of cases and non-cases among hospital and longterm care facility staff during a norovirus outbreak from 20 February to 22 February 2007 Case Non-case Attack n = 47 n = 238 rate (%) P Sex, male 13 (28) 51 ( Median age 3), y 47 (29-59) 47 (33-57) (interquartile range) Workplace Hospital 31 (66) 171 (7 15 Long-term care facility 8 (17) 49 (2 14 Food service 8 (17) 18 (8) 31 Diet 4) < Standard 44 (94) 83 (35) 35 None 3 (6) 154 (65) 2 Values are n (%) unless otherwise stated. : Norovirus test (+)/total = 7/8. : Norovirus test (+)/total = 8/15. 3) : Missing = 2. 4) Among 285 staff members, 47 (16%) fell ill during the first 3 days of the outbreak. Staff members symptoms included diarrhea (72%), vomiting (57%), and fever (57%). The first staff case of gastroenteritis occurred at 3 a.m. on 21 February; this staff member worked at the LTCF (#LS. Surveyed characteristics of staff members, including sex, age, and workplace, were not associated with illness (Table. With regard to workplace, attack rates ranged from 14% at the LTCF to 31% of kitchen workers, although the differences were not significant (P = 0.136). The hospital staff had an attack rate of 15%, similar to the LTCF staff (14%). Fifty-five (13%) of the patients and daycare users fell ill during the first 3 days of the outbreak (Table. Their symptoms included diarrhea (56%), vomiting (62%), and fever (71%). Male and younger age were significantly associated with illness (P = and P < , respectively). However, ward type was also a significant factor (P < Attack rates on individual wards ranged from 0% at the LTCF to 30% of daycare users. The residents at the LTCF were 18% male and older (median age, 85 years), while the daycare users were 77% male and younger (median age, 57 years). The significant associations between sex or age and illness were considered to be due to these demographic characteristics. As none of the LTCF residents fell ill during the first 3 451

3 days, the LTCF residents were excluded from the analyses, and we calculated the RR and 95% CI for consumption of the standard diet (Table 3). For both staff and patients, consumption of the standard diet was significantly associated with illness (staff: RR = and 95% CI = ; patients: RR = 2.12 and 95% CI = None of the kitchen workers or daycare users who had not eaten the standard diet fell ill. For example, the lunch menu items on 20 February Table 2. Comparison of cases and non-cases among hospital patients, residents at a long-term care facility, and daycare users during a norovirus outbreak from 20 February to 22 February 2007 Case Non-case Attack n = 55 n = 358 rate (%) P Sex, male 37 (67) 174 (49) Median age, y 56 (45-66) 64 (56-77) < (interquartile range) Ward < nd floor of hospital 3 (5) 34 (10) 8 3rd -7th floors of hospital 39 (7 211 (59) 16 Long-term care facility 0 (0) 83 (23) 0 Daycare users 13 (24) 30 (8) 30 Diet Standard 47 (85) 220 (63) 18 Special 8 (15) 103 (29) 7 Tube feeding 0 (0) 10 (3) 0 None 0 (0) 19 (5) 0 Values are n (%) unless otherwise stated. : Norovirus test (+)/total = 8/9. : Missing = 6. included rice, meatloaf, asparagus sauté, cooked chicken wings, salad, and fruits. Because most of the people who ate the standard diet consumed all of the food items, no individual food item was identified as a potential source of the infection (data not shown). Two individuals became symptomatic on 20 February. We consider the first case, a hospital patient who became symptomatic at 1:30 p.m. on 20 February (#H, as unrelated to the outbreak and not a source of subsequent cases. This patient showed only a single instance of vomiting within his own room and did not have any other symptoms. The other person was a daycare user who became symptomatic at 6:30 p.m. on 20 February (#D; he experienced a severe episode of vomiting (eight times), had diarrhea, and developed fever after leaving the hospital. These symptoms were considered to be compatible with norovirus infection. Laboratory investigation: Among 32 stool samples collected from symptomatic patients and kitchen workers, 23 were confirmed by RT-PCR to be positive for norovirus GII/ 4 (Table 4). Among 15 kitchen workers, eight were asymptomatic. The norovirus genome was not detected in the frozen samples of food and swabs; however, S. aureus was detected in three food samples and two environmental samples (nontoxigenic). Further investigations based on the results: In the kitchen, the same dishes were cooked by the same process. The kitchen workers were divided into three sections (a standard diet, a special diet, and a diet for residents at the LTCF, which included both the standard and special diets) (Figure. The standard diet was prepared in the location closest to the door, which was across the corridor from a bathroom. Table 3. Attack rates for standard diet among staff, hospital patients, and daycare users with onset between 20 and 22 February 2007 Standard diet eaten Standard diet not eaten Relative risk Case/total Attack rate (%) Case/total Attack rate (%) (95% confidence interval) Staff 4) 44/ / ( ) Hospital 5) 29/ / ( ) Long-term care facility 7/ / ( Food service 8 / /1 0 Hospital patients and daycare users 6) 47/ / ( nd floor of hospital 7) 2/ / ( ) 3rd-7th floors of hospital 8) 32 / ) / ( ) Daycare users 13/ /15 0 : Norovirus test (+)/total = 7/8. : Norovirus test (+)/total = 6/6. 3) : Norovirus test (+)/total = 2/3. 4) 5) 6) : Missing = 6. 7) : Missing = 3. 8) : Missing = 3. Table 4. Results of norovirus GII/4 testing with reverse transcription polymerase chain reaction Positive Negative (n = 23) (n = 9) Kitchen worker Hospital patient Kitchen worker Hospital patient Symptom (+) Onset day 21 Feburary Feburary Feburary Feburary Symptom ( )

4 Fig. 2. Floor plans of the kitchen at the long-term care facility (LTCF) including the location of preparing dishes. The door was always open because of poor ventilation in the kitchen. Because the corridor ran from the staff entrance to the hospital, the bathroom could have been used by any staff member. It was not clear whether someone had vomited near the bathroom. The two kitchen workers who prepared the standard diet fell ill on 21 February (#K1 and #K, as did many of the other cases. Their respective family members had not been symptomatic. DISCUSSION We have described an outbreak of acute norovirus gastroenteritis affecting patients and staff members of a hospital and an attached LTCF. The main mode of transmission was considered to be foodborne. Consumption of the standard diet was significantly associated with a higher risk of illness. We considered the central kitchen to be the probable source of the food contamination. For all 102 individuals who became symptomatic during the first 3 days of the outbreak, the mode of transmission was considered to be foodborne. The cohort study results showed an association between illness and the standard diet served on 20 February. These analytic data, combined with the incubation period for norovirus, support the hypothesis of a point source, foodborne outbreak that originated from contamination of the standard diet. Standard diets, special diets, and diets for residents at the LTCF were prepared separately in the same kitchen. Although norovirus was not detected in any of these lunches, the synchronous appearance of symptomatic individuals supports the hypothesis that the incident was foodborne. For the remaining 55 symptomatic patients and staff members, the virus is highly likely to have been spread directly by person-to-person transmission, by contact with various contaminated environmental surfaces or by aerosolization of viral particles. Infected food handlers working despite manifest diarrhea or vomiting are a common cause of foodborne norovirus outbreaks (1,18-23). In this study, however, none of the kitchen workers became ill before the outbreak. The two kitchen workers who prepared standard diets (#K1 and K fell ill on 21 February, as did many other cases. Although presymptomatic shedding of the virus by kitchen staff cannot be excluded and the possibility has been described elsewhere (35,36), spread of the virus from symptomatic cases is much more likely, as excretion is likely to be higher and hygiene is more difficult to maintain when suffering from diarrhea or vomiting. In addition, although it has been established that manually prepared food can be a source of norovirus infection (1,2, the kitchen workers in the present outbreak wore gloves while preparing the food. In this outbreak, we could not directly link norovirus contamination to the standard diet. However, it is possible that norovirus was spread from the area surrounding the doorway of the kitchen. One of the daycare users (#D became symptomatic at 6:30 p.m. on 20 February. Earlier on the same day, a number of daycare users had moved in and out of the kitchen to prepare plates for themselves. The two kitchen workers who prepared the standard diet (#K1 and #K became symptomatic earlier than the other kitchen workers did. The standard diet might have been contaminated at nearly the same time they were infected. Poor kitchen design is a potential source of virus contamination. Figure 2 illustrates the floor plan of the kitchen, including the locations where dishes were prepared. Standard diets were prepared in the area closest to the door, which was always open because of poor ventilation in the kitchen. Although we could not directly link the open door to norovirus contamination, it may be necessary to consider building reconstruction and room rearrangements as possible contributors to foodborne outbreaks. Although we could not identify the source of norovirus contamination, some preventive measures were instituted. After the present outbreak, employees were given a thorough education on strict hand washing and gargling techniques. The food sanitation manual was significantly revised, and stricter hygiene measures such as wearing face masks and gowns in the kitchen were included. Among the LTCF residents, no one fell ill during the first 3 days of the outbreak. A small outbreak of norovirus gastroenteritis affecting 29 residents and two employees at the LTCF had occurred about 2 months earlier. Only one stool sample was collected from a symptomatic LTCF resident, and norovirus was confirmed by enzyme-linked immunosorbent assay (ELISA). Norovirus genotypes were not confirmed by further testing. In this episode, the main mode of transmission was considered to be person-to-person transmission because of the limited extent of infection. Based on the occurrence of this small outbreak, preventive measures were instituted, including disinfection of doorknobs and floors by chlorine and monthly collection of stool samples from kitchen workers. In addition, employees were instructed to stay at home for a week if they were having symptoms. The present foodborne outbreak occurred despite the enforcement of these measures. Our findings suggest that individuals who consumed the standard diet were more likely to contract the disease. The standard diet may have been contaminated while being prepared in the central kitchen; however, the source of contamination was not identified. Identifying the source of a norovirus outbreak is a challenging task. Further studies are needed to define the patterns of contamination. REFERENCES 1. 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