Investigation of Concurrent Outbreaks of Gastroenteritis and Typhoid Fever following a Party on a Floating Restaurant, France, March 1998

Marta Valenciano1,2, Sabine Baron1, Alain Fisch3, Francine Grimont4 and Jean Claude Desenclos1

1 Institut de Veille Sanitaire, Saint-Maurice, France.
2 European Programme for Intervention Epidemiology Training, Saint-Maurice, France.
3 Centre Hospitalier Villeneuve St. Georges, France.
4 Centre National de Référence pour le Typage Moléculaire Entérique, Unité des Entérobactéries, Institut Pasteur, Paris, France.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A retrospective cohort study was carried out to investigate concurrent outbreaks of gastroenteritis and typhoid fever that occurred among guests of a supper on a floating restaurant in France in March 1998. A total of 133 guests (attack rate = 90%) reported gastroenteritis within 12 days of the supper. Twenty-seven guests developed typhoid fever (attack rate = 18%) of whom 15 were confirmed by stool or blood culture. All patients with typhoid fever had had an initial gastroenteritis. The results suggest that the same food items served during the supper, chicken and rice, were the vehicles of both gastroenteritis and typhoid fever, but the authors could not determine the specific source of infection. Initial gastroenteritis has been described as a clinical manifestation of typhoid fever but whether or not these two syndromes (gastroenteritis and typhoid fever) were due to the same etiology remains unclear in this outbreak. Am J Epidemiol 2000;152:934–9.

disease outbreaks; food poisoning; gastroenteritis; typhoid

Abbreviations: CI, confidence interval; RR, relative risk


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In France, as in the rest of the industrialized countries, improvement in hygienic conditions has led to a substantial and important decrease in typhoid fever incidence (from 0.23/100,000 in 1987 to 0.13/100,000 in 1997). Most of the cases (70 percent) reported are sporadic and occur after traveling to an endemic area (1Go). However, in September 1997 an outbreak of typhoid fever with 16 cases in the Alpes-Maritimes region of France following a common meal demonstrated that the potential for food-borne outbreaks still exists in France at the end of the 20th century (2Go).

On April 8, 1998, the Institut de Veille Sanitaire was informed of three French cases of typhoid fever admitted to a hospital in the region of Paris. All three cases had attended a party on a floating restaurant in the river Seine 1 month before. An investigation was carried out to assess the size of the outbreak, to determine the vehicle and source of infection, and to implement control measures.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
A retrospective cohort study was conducted among the guests at the party who had consumed at least one food item or one drink during the party on the floating restaurant. Participants were identified using a list provided by the organizers. The participants were asked the names and addresses of any additional guests, thereby extending the list. Participants were interviewed either by telephone or face-to-face using a standardized questionnaire that gathered information about demographics, onset of illness, type, severity and duration of symptoms, participation in the supper preparation, food and beverage consumption during the supper, and amount consumed. During the interviews participants were informed of basic hygienic measures intended to avoid secondary transmission.

Case definitions
During the interviews we noticed that most of the guests reported having had gastrointestinal symptoms on the days following the supper. Thus, we used two different case definitions: one for gastroenteritis and one for typhoid fever. A case of gastroenteritis was defined as a participant at the supper who had diarrhea (more than three stools per day for at least 1 day) within 12 days of the supper. A case of probable typhoid fever was defined as a participant at the supper who had a fever equal or superior to 38°C for more than 2 days (with no other cause of fever checked by the practitioner) with onset more than 10 days after the supper, and who had either a negative stool or blood culture to Salmonella typhi or did not have a specimen tested. A case of typhoid fever was confirmed if, in addition to the fever, a stool or blood specimen cultured positive for S. typhi.

A secondary case of gastroenteritis was defined as a household contact of a participant at the supper who met the criteria for gastroenteritis following the supper. A secondary case of typhoid fever was defined as a household contact of a participant at the supper who had a positive stool or blood culture to S. typhi following the supper.

Case finding
Through a press release and during the telephone interviews, participants at the supper and their contacts were advised to submit a specimen for stool culture. The National Reference Center for Salmonella and Shigella was asked to inform the Institut de Veille Sanitaire of all the isolates of S. typhi identified since March. The typhoid cases reported through the routine surveillance system were investigated to determine if they could be linked to the supper.

Microbiologic investigation
Stool specimens were cultured in MacConkey medium (Oxoid, Dardilly, France) and Salmonella-Shigella agar. In addition, a MUCAP test (Mascia Brunelli-Biolife S.p.A., Milan, Italy) to detect Salmonella was performed on lactose-negative colonies. A system from Bio-Mérieux (Marcy-L'Etoile, France) was used for blood cultures.

S. typhi isolates from blood and stool specimens were submitted to the National Reference Center. Phage typing was performed using the Craigie and Yen method (3Go) and ribotyping, using the method described by F. Grimont and P. A. Grimont (4Go). No specimens of food served at the supper were available for microbiologic analysis.

Environmental investigation
An environmental investigation was carried out by the District Veterinary Services in collaboration with the District Health Department and consisted of an inspection of the floating restaurant and interviewing the food handlers on delivery of food items and their preparation. In addition, water specimens were collected from the water distribution in the boat and in the Seine and were analyzed to look for fecal contamination.

Statistical analysis
Specific attack rates for each food item served, their relative risks, and 95 percent confidence intervals (Greenland and Robins method) (5Go) were calculated using Epi-Info, version 6.04 (Centers for Disease Control and Prevention, Atlanta, Georgia).


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Of the 199 participants at the party identified, 157 (79 percent) were interviewed; 147 (94 percent) had consumed at least one food item or one beverage during the supper and were therefore included in the retrospective cohort analysis. The mean age of the cohort was 31 years (minimum age, 16 years; maximum age, 60 years), and 77 (52 percent) were women.

Gastroenteritis cases
Gastroenteritis was reported by 133 guests (attack rate = 90.5 percent). Besides diarrhea, the most common symptoms reported were abdominal cramps (109/130; 84 percent), fever of >=38°C (69/130; 53 percent), vomiting (65/130; 50 percent), and headache (58/126; 46 percent). Other symptoms reported were bloody diarrhea (three cases), bleeding nose (two cases), asthenia (two cases), and insomnia (one case). Among the 101 cases for whom information was available, 14 (14 percent) had received antibiotic treatment. The mean duration of symptoms was 8 days. Twenty-seven gastroenteritis cases (20 percent) developed typhoid fever later on. The distribution of onsets of illness suggests a common source of infection with a peak occurrence 2 days after the supper (figure 1).



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FIGURE 1. Cases of gastroenteritis among supper participants (n = 106) by date of onset, Ile de France, March 1998.

 
The attack rate was 88 percent (68/77) for women and 93 percent (65/70) for men (relative risk (RR) = 1.05, 95 percent confidence interval (CI): 0.9, 1.2). The attack rate by age varied between 75 percent and 94 percent (table 1).


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TABLE 1. Attack rate of gastroenteritis and typhoid fever among supper participants, by age group, Ile de France, March 1998

 
Persons who reported having eaten chicken or having eaten rice were more likely to develop gastroenteritis than were those who had not eaten those food items (RR = 2.6, 95 percent CI: 1.2, 5.7 and RR = 2.9, 95 percent CI: 1.4, 6.0, respectively). No other foods or drinks were associated with an increased risk of gastroenteritis (table 2).


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TABLE 2. Food-specific attack rate of gastroenteritis and typhoid fever (probable and confirmed cases) among supper participants, Ile de France, March 1998

 
Cases of typhoid fever
Twenty-seven guests developed typhoid fever (attack rate = 18.4 percent) of whom 15 cases were confirmed. During the course of the typhoid illness, fever was associated with abdominal pain (66 percent), diarrhea (55 percent), typhoid state (22 percent), and jaundice (7 percent). Twenty-one typhoid cases were hospitalized and two had severe complications: one had an acute renal failure requiring a 23-day stay in an intensive care unit and the other presented more serious complications (rhabdomyolysis, acute renal failure, acute hepatic failure, encephalopathy, and peritonitis leading to a 38-day stay in an intensive care unit). All patients with typhoid fever had also had an initial episode of gastroenteritis within 12 days of the supper. The initial gastroenteritis presented by the typhoid fever cases had clinical characteristics (abdominal cramps, 19/26; vomiting, 13/25; fever, 16/27; headache, 13/26) and an incubation period (1.9 days) similar to those of gastroenteritis presented by the 106 cases who did not develop typhoid fever later on.

The median incubation period for typhoid fever was 21 days (range, 10–38 days) (figure 2). The attack rate was 21 percent (16/77) for women and 16 percent (11/70) for men (p = 0.3). The median age was 25 (minimum, 16; maximum, 35) years; participants from the younger age groups were more likely to develop a typhoid fever than were the older ones (table 1) with no cases reported among participants over 40 years.



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FIGURE 2. Cases of typhoid fever among supper participants (n = 27) by date of onset, Ile de France, March 1998.

 
The comparison of food-specific attack rates indicated that eating rice and eating chicken were associated with an increased risk of typhoid fever. Their relative risks were of the same magnitude as those observed for gastroenteritis (RR = 2.3 and RR = 2, respectively), but 95 percent confidence intervals included 1. Twenty-six cases could be explained by having eaten rice or chicken (24 cases had eaten both, and information was not available for one case) (table 2).

A dose-response analysis could not be performed as most of the participants could not state precisely the quantity of food consumed.

Secondary cases
Six cases of gastroenteritis were reported among persons who didn't attend the party but who had contact with participants, and a case of Shigella was isolated in one child whose parents attended the supper. No secondary cases of typhoid fever were identified.

Microbiologic results
Among gastroenteritis cases who didn't develop typhoid fever, 75 had a stool culture, only two of which were taken during the gastroenteritis phase. One cultured positive for a Salmonella group D but was not serotyped, and the second one was negative. Salmonella panama, also belonging to group D, was isolated in one case 3 weeks after the supper. The other 72 stool cultures performed during the investigation (more than 1 month after the supper) were all negative.

Among typhoid fever cases, S. typhi was isolated in six stool cultures and in 14 blood cultures (five cases with both cultures positive) between March 28, 1998, and April 9, 1998.

S. typhi isolates had identical phage-type DVS and ribotype TP7. The strain was sensitive to commonly used antibiotics such as ampicillin, cephalosporins, sulfamethoxazol-trimethoprim, and quinolones.

Environmental results
The environmental investigation was carried out 1 month after the party and revealed major deficiencies in the hygienic conditions of the restaurant, such as the absence of potable water in the kitchen, insufficient hand-washing sinks for employees, and common toilets for food handlers and for guests. Water for the boat distribution system (tap water) was pumped directly from the Seine without any microbiologic treatment.

Seven people, nonprofessional cooks, were involved in food preparation; none of them reported having been sick before or during the preparation of the food. All of them ate during the supper, six developed gastroenteritis (85.7 percent), and two (28.6 percent) developed typhoid fever (confirmed cases) later on; none of them had recently traveled to an endemic typhoid fever area. Five had a negative stool culture at the time of the investigation. The only food handler who was not ill after the supper did not have any stool or blood culture.

The chicken was marinated with oil, vinegar, lemon, and garlic overnight in the home of one of the food handlers and barbecued during the supper on the floating restaurant. Food handlers reported having boiled rice with potable water during the afternoon and having stored it at room temperature until served. A garnish (onions, bacon, tomatoes, and sweetcorn) was separately cooked and added to the rice. The chicken and rice were served together with a sauce prepared the day before with oil, lemon, garlic, onion, chili, and cabbage. Food was served in dishes that had been washed in tap water from the boat.

The analysis of water samples showed evidence of fecal contamination in the water from both the distribution system (1,000 thermotolerant coliforms/100 ml and 600 fecal streptococci/100 ml) and the Seine (2,100 thermotolerant coliforms/100 ml and 120 fecal streptococci/100 ml). No Salmonella species were isolated.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The results of the investigation suggest that the consumption of the rice and chicken at the supper was responsible for the two syndromes, gastroenteritis and typhoid fever. Microbiologic proof of contamination of these dishes could not be obtained because there were no leftovers at the time of the investigation. As the diarrhea outbreak was not reported to the health authority through the routine surveillance system, the investigation began when the typhoid cases were reported (1 month after the meal). We have not been able to identify the source of the contamination, but different possibilities exist. As the profile of the S. typhi isolated in the typhoid cases is common in France, no specific source for this pathogen could be suspected. Chicken not being a reservoir of S. typhi, the dishes could have been contaminated during their preparation by a healthy carrier as in most of the food-borne outbreaks reported in developed countries (6Go, 7Go). Barbecued chicken, if insufficiently cooked, could have been the source of a nontyphoidal Salmonella (as the S. panama isolated from one participant) responsible for the gastroenteritis syndrome. Anyway, we cannot exclude the possibility of food contamination by the tap water used during meal preparation. Fecal contamination was found in the tap water as a result of poor plumbing in the boat. However, the cooks reported using tap water only for the washing up and not for the meal preparation. The poor hygienic conditions and the food preparation for 200 participants by unskilled people would have favored the contamination of the items served.

We could not determine specifically which of the two incriminated food items (chicken or rice) was the vehicle of the outbreak as 86 percent of the participants consumed both. Among rice consumers, 98 percent ate chicken, and among chicken consumers, 94 percent ate rice, reducing the possibility of detecting a significant association. A dose-response analysis couldn't be performed as most of the participants could not remember the quantity of food consumed.

This outbreak was striking because of the occurrence of two syndromes associated with the same supper, an early gastroenteritis characterized by a high attack rate and a typhoid fever. Two hypotheses can be advanced. 1) Two different agents were present: one responsible for the gastroenteritis and another, S. typhi, responsible for the typhoid cases. 2) S. typhi was responsible for both syndromes.

Facts supporting the first hypothesis are as follows:

  1. Another Salmonella species was isolated in one case of gastroenteritis. Unfortunately, few stool cultures were performed during the gastroenteritis episodes so we cannot reach any conclusions about the possible role of S. panama.
  2. The clinical features of the initial gastroenteritis were more compatible with a nontyphoid Salmonella infection (incubation period, diarrhea, fever, and so on) than with typhoid fever. In previous series, diarrhea has been reported in 30–50 percent of patients with typhoid, but it was not as severe and much more variable in onset (8Go).
  3. Combinations of different agents can occur in infectious diarrhea. During an outbreak of typhoid fever in Florida in 1973, among 105 bacteremic cases, 13 were also positive for Shigella (7Go).

The second hypothesis (S. typhi was the only agent causing the two syndromes) is less likely but some arguments could support it:

  1. All the typhoid cases had an initial gastroenteritis.
  2. During the gastroenteritis, some of the cases reported symptoms usually associated with typhoid fever (insomnia, nose bleeding).
  3. Early gastroenteritis within days after contamination has been described as a clinical manifestation of typhoid fever in countries with low endemicity (8Go, 9Go). In France during a food-borne typhoid fever outbreak in 1997, 70 percent of the participants presented with an initial gastroenteritis and were considered possible cases of typhoid fever (2Go).

Although this was a food-borne typhoid fever outbreak, we were not able to identify the specific source. However, the results suggest that the same food items could be the vehicles in both syndromes. Other food-borne outbreaks of typhoid fever have been described in countries with low incidence, most of them the result of food contamination by a carrier (6Go, 7Go, 10Go, 11Go). In developed countries, improved public health measures have led to a low level of exposure to S. typhi and to a lower immunity, especially among young people, as evident in the results of this investigation. The higher attack rates of typhoid fever in participants under 30 years of age could also be explained by behavioral factors, such as greater food consumption, or by other factors, such as antibiotic intake or immunization, but the information gathered on those items was neither complete enough nor sufficiently accurate to be taken into account.

This outbreak emphasizes the importance of good hygiene practices in restaurants and the need to have professional food handlers trained in basic hygiene when food is prepared for a large group. Poor hygiene in food preparation represents a risk for both developing mild illnesses and being exposed to more virulent pathogens such as Escherichia coli O157 or S. typhi.


    ACKNOWLEDGMENTS
 
This investigation was conducted as part of routine activities in the institutions concerned. The Institut de Veille Sanitaire is funded by the Ministry of Social Affairs. The European Programme for Intervention Epidemiology Training is funded by the European Commission Direction Générale V (DGV).

The authors thank the persons and organizations who participated in this investigation: Institut de Veille Sanitaire: E. Delarocque Astagneau, V. Vaillant, H. de Valk, S. Haeghebaert, A. Canestri, V. Cerase, A. Guinard, M. Ledrans; Centre Hospitalier Villeneuve St. Georges: C. Bezelgues, J. Breuil, A. Dublanchet, T. Prazuck, C. Semaille; Centre Hospitalier St. Germain-en-Laye: A. Boisivon, M. Saillour; Centre National de Référence des Salmonella et des Shigella, Unité des Entérobactéries, Institut Pasteur, Paris: P. Bouvet, P. A. D. Grimont; Direction Départementale des Affaires Sanitaires et Sociales, Val de Marne: I. Genot, C. Julien, M. C. Pierre, E. Poulat, S. Ragell; Direction Départementale des Services Vétérinaires, Val de Marne: P. Moyon; Direction Départementale des Affaires Sanitaires et Sociales, Essone: I. Plaud-Diakite, M. Wluczka.


    NOTES
 
Reprint requests to Dr. Sabine Baron, CHU de Tours, Unité d'Information Médicale et d'Economie de la Santé, Hôpital Bretonneau, 2 Bd Tonnelé, 37044 Tours, France (e-mail: s.baron{at}bretonneau.chu-tours.fr).

Presented at EPIET Scientific Seminar, Veyrier du Lac, France, October 1998.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Guigue L, Baron S. Les fièvres typhoïdes et paratyphoïdes en France en 1997. (In French). In: Annual epidemiological report. Infectious diseases epidemiology in France in 1997. Saint-Maurice, France: Réseau National de Santé Publique, 1999. (Institut de Veille Sanitaire publication no. 2).
  2. Pradier C, Keita-Perse O, Vezolles MJ, et al. Epidémie de fièvre typhoïde à Utelle (Alpes-Maritimes, France, 1997). (In French). Bull Epidemiol Hebdomadaire 1998;32:137–9.
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  9. Hoffman TA, Ruiz C, Counts G, et al. Waterborne typhoid fever in Dade County, Florida: clinical and therapeutic evaluation of 105 bacteremic patients. Am J Med 1975;59:481–6.[ISI][Medline]
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Received for publication August 17, 1999. Accepted for publication January 27, 2000.





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