Outbreak of Salmonella Enteritidis Phage Type 913 Gastroenteritis Associated with Mung Bean Sprouts

Outbreak of Salmonella Enteritidis Phage Type 913 Gastroenteritis Associated with Mung Bean Sprouts – Edmonton, 2001
Canada Communicable Disease Report
Volume 27-18
15 September 2001


During February and March 2001, 84 cases of Salmonella enteritidis phage type 913 (SE PT 913) were reported in Alberta, British Columbia and Saskatchewan. Of these, 73 (87%) resided in the Capital Health region (greater Edmonton, Alberta) at the time of diagnosis. The ensuing outbreak investigation conducted by Capital Health-Environmental Health, summarized below, epidemiologically linked consumption of mung bean sprouts distributed in the Edmonton area with onset of SE PT 913 infection.



Case Series Data

Laboratory confirmation ofS. enteritidis cases was provided by the Provincial Laboratory of Northern Alberta (PLNA), and phage typing of these cases was conducted by the National Laboratory for Enteric Pathogens, National Microbiology Laboratory, Winnipeg, Manitoba. Cases of SE PT 913 captured through notifiable disease surveillance in the Capital Health region were contacted by telephone and administered a standard questionnaire, from which demographic data, symptoms experienced and environmental exposures during the incubation period were obtained. Capital Health was provided analogous information for confirmed SE PT 913 cases outside of the Capital Health region by Alberta Health and Wellness, which obtained these data from the health regions in which the cases resided at time of diagnosis.


Investigation of Implicated Mung Bean Sprout Producer

When case series data revealed a link to a local producer of mung bean sprouts (see below), Capital Health and the Canadian Food Inspection Agency (CFIA) conducted an onsite evaluation of mung bean sprout manufacturing practices at this facility, and collected 40 food and other environmental samples. Mung bean husks, wash water, sprouting seeds and food and non-food contact environmental samples were obtained from the facility, as well as ready-to-eat sprouts from both the plant and from restaurants that received product from the implicated grower. Mung bean sprouting seed samples were analyzed both dry and following germination in the laboratory. Clinical (stool) samples were also obtained from employees at the implicated sprout grower. The environmental and clinical samples were submitted to PLNA or the CFIA Calgary Laboratory for microbiologic analysis.


Case-Control Study

A case-control study was conducted to test the association between the suspected exposure elucidated from case series data and subsequent onset of SE PT 913 infection. A detailed overview of the study design appears later in this report.


Case Definition/Follow-up

The outbreak case definition was restricted to laboratory-confirmed cases of SE PT 913 reported to Capital Health on or between 1 February and 31 March 2001; a total of 84 cases met this definition. During the investigation, 81 of these cases were contacted by Capital Health or by the health region in which cases resided at the time of diagnosis. As a result of failed attempts to contact three cases by telephone or mail, these individuals were lost to follow-up.


Causative Agent

The S. enteritidis isolates from outbreak cases were of a phage type not previously identified (R Ahmed, F Rodgers. National Laboratory for Enteric Pathogens, National Microbiology Laboratory, Winnipeg: personal communication, 2001). As such, this outbreak represents the first known occurrence of SE PT 913 infection in humans.


Disease Presentation

Most cases contacted (78, 96%) reported onset of gastroenteritis between 3 and 20 February 2001 (Figure 1). Reported symptoms included diarrhea (100%), abdominal cramps (74%), fever (55%), vomiting (45%), chills (39%), headache (29%), nausea (29%), body ache (23%) and malaise (7%). Approximately 6% of cases were hospitalized; no resultant deaths occurred. An incubation period was calculated (mean 50 hours, median 48 hours) when investigators were able to hypothesize a probable time of exposure. The mean and median age of cases was 32 years, with a range of 1 to 68; 51% of cases were male.

Figure 1 : Epidemic curve – Salmonella enteritidis phage type 913 outbreak

Exposure History Data

Without exception, all cases of SE PT 913 that were contacted (including those who reside outside of Alberta) reported being in the greater Edmonton area during the incubation period. Food exposures were investigated as a possible source of infection, and 62% (50/81) of cases recalled consumption of food at one of 13 Vietnamese, Chinese or Japanese-style restaurants in the Edmonton area during the incubation period. The number of cases linked to each restaurant ranged from one to 17 (Figure 2), and the dates of implicated meal consumption at these restaurants occurred on or between 3 and 17 February 2001. It was learned that all implicated restaurants received mung bean sprouts from one Edmonton supplier during February 2001. Of those that recalled a meal at one of the 13 implicated restaurants, 42 (84%) recalled mung bean sprouts as being an ingredient of that meal. No other exposures were reported with significant frequency in the case series data, and no other links were found among the implicated restaurants.

Figure 2 : Distribution of Salmonella enteritidis phage type 913 cases

Evaluation of Sprout Production and Distribution Practices

The implicated bean sprout producer had been in operation since 1995, and during inspections of the production facility by Capital Health, Environmental Health prior to the outbreak, concerns pertaining to plant sanitation, employee hand washing practice and quality control/assurance were observed. Bean sprout samples from this facility analyzed prior to the outbreak were free of common enteric pathogens (including Salmonella), but did show elevated levels of fecal coliforms. There was no gastrointestinal illness among plant employees during February 2001, as reported by plant management.

The seeds used for mung bean sprout production by the implicated grower originated in China, and were obtained through a distributor in the United States. The implicated sprout grower had reportedly been using seed from the same shipment between November 2000 and the time of the outbreak. The label on each bag of mung bean sprout seeds included a statement indicating that the product could contain pathogens including but not limited to Salmonella and Escherichia coli, as well as recommended seed disinfection procedures. However, it was discovered that plant employees were not disinfecting the mung sprouting seeds as per label instructions.


A comprehensive list of mung bean sprout recipients of this supplier was not available; however, the producer reportedly distributed mung bean sprouts almost exclusively to restaurants. At the time of the outbreak, the producer was providing mung bean sprouts to at least 40 restaurants in the Edmonton area. Recipients of bean sprouts from the implicated producer typically received fresh sprout shipments every few days, and in some instances on a daily basis. Several of the implicated restaurants served the bean sprouts raw, while others added sprouts to cooked foods late in the heating process, to ensure the desired texture was preserved.


Sample Results

All food and environmental samples submitted as part of this investigation were negative for Salmonella bacteria, including the dry and laboratory-germinated mung bean sprouting seeds. Stool samples were obtained from five of the seven employees at the implicated sprout grower, which were all negative for Salmonella. Clinical samples were not obtained from two employees lost to follow-up, as they reportedly left the province following the voluntary closure of the plant.


Public Health Intervention

The implicated sprout grower voluntarily ceased production of sprouts on 16 February 2001, under the supervision of Capital Health, and on that same day, mung bean sprouts in distribution were recalled under the supervision of CFIA. On 21 February 2001 Capital Health issued a news release in the greater Edmonton area advising of the outbreak and associated mung bean sprout recall, and advised those experiencing gastroenteritis that may have consumed mung bean sprouts to seek medical attention.


Case-control Study

Study Design

A case-control study was conducted within the Capital Health region to test the association between consumption of mung bean sprouts from the grower implicated through case series data, and subsequent onset of SE PT 913 infection. A total of 59 cases and 62 controls were entered into the study. Case and exposure criteria for the study are outlined below:


Case definition:Adult (>= 18 years of age) residents of the Capital Health region with onset of laboratory-confirmed infection with SE PT 913 in February 2001. Cases were obtained through notifiable disease surveillance, and the exposure data was obtained from cases by telephone between 5 February and 12 March 2001. Note: 11 laboratory-confirmed cases < 18 years of age were restricted from the study; those < 18 years of age were excluded from the study to better assure accuracy of exposure information.


Control definition:Adult (>= 18 years of age) residents of the Capital Health region with no self-report of diarrhea, travel or ingestion of antibiotics during February 2001. Controls were obtained through random digit dialing between 9 and 16 March 2001, at which time exposure information was obtained.

Exposure criteria:Self-report of consumption of food at a restaurant on the distribution list of the implicated mung bean sprout grower, between 1 and 15 February 2001 inclusive. To aid study participant recall, self-report of food at restaurants, rather than consumption of mung bean sprouts specifically, was used for exposure criteria.


Non-exposure criteria:No self-report of consumption of food at a restaurant on the distribution list of the implicated mung bean sprout grower, between 1 and 15 February 2001 inclusive, or no self-report of consumption of food at any restaurant between 1-15 February 2001 inclusive.


Results/Limitations of Case-Control Study

A statistically significant association was found (odds ratio = 24.4, 95% confidence interval = 7.8 to 76.4, p < 0.001) between self-report of consumption of food at a restaurant on the distribution list of the implicated sprout grower and subsequent onset of SE PT 913 infection. However, there are several potential sources of bias in this study.


Matching: Matching was not carried out for age or sex. Controls were statistically older and more likely to be female than cases.


Recall bias: Exposure data for most controls were obtained, on average, approximately 4 weeks after analogous data from cases. It is possible that cases were better able to recall exposure information than controls.


Misclassification of exposed/non exposed: The restaurant distribution list provided by the implicated sprout grower was reportedly incomplete. This likely resulted in misclassification of some study subjects (both cases and controls) as non-exposed, when they may have in reality eaten at a restaurant that did receive mung bean sprouts from the implicated grower. However, this misclassification likely occurred more frequently among cases than controls, as verified through contact of restaurants reported by cases and controls to confirm source of mung bean sprouts, and may in fact have resulted in an underestimation of the true odds ratio. As well, 1 to 15 February 2001 was used as the exposure time frame, as this was the exposure window observed from case series data at the time the study began. One case was later found to have been exposed to the implicated sprouts outside of this time window on 17 February 2001, and was classified as not being exposed.



Outbreaks of Salmonella infection associated with mung bean sprouts have been reported previously(1,2). Contaminated sprout seed is likely responsible for most sprout-associated outbreaks, however, as was observed in this outbreak, pathogens frequently fail to be isolated from implicated seed, which may indicate that pathogenic contamination of seed may be low, intermittent or unequally distributed within seed lots(3). However, the sprouting process, which involves soaking of seeds for several days to allow for germination, provides excellent conditions for bacterial growth, meaning that even low levels of seed contamination may result in proliferation of pathogens to hazardous levels(4). It is therefore not surprising that approximately 9% of mung bean sprouts analyzed as part of a microbiologic survey in Thailand were contaminated with Salmonella(5). Because of the likelihood of pathogenic contamination, disinfection treatments for sprouting seeds are often recommended. However, this does not guarantee a pathogen-free product – no single disinfection procedure has been shown to reliably result in more than a three-log reduction of bacterial pathogens on seeds intended for sprout production(6).

If the transmission vehicle in this outbreak was in fact mung bean sprouts, the source of the contamination could not be confirmed. Possible sources include contaminated seed, cross-contamination within the sprout production facility, or Salmonella-infected plant workers. It is unknown whether failure by the implicated sprout grower to chlorinate mung bean seeds as per label instructions is significant, but it remains a possible contributing factor in this outbreak.


This outbreak has again demonstrated that sprouts are a potential source of foodborne illness. As there currently appears to be no reliable process to ensure adequate removal of pathogenic contamination from mung bean sprouts, and because of apparent consumer preference for raw or lightly cooked sprouts, protection of the public from this identified hazard will remain a challenge. Until contamination of this food product can be further minimized, those with compromised immune systems should refrain from consuming raw or lightly cooked mung bean sprouts (similar recommendations have been made previously for alfalfa sprouts(7)), and consumers should continue to be advised of the potential risks associated with sprouts.



The authors would like to acknowledge the contributions of the following Capital Health staff to this investigation: Ingrid Zazulak, Jody Tom, Diane Luka and, Nyall Hislop.


  1. Mohle-Boetani J. CA EPI 00-09 – Salmonella enteritidis (SE) infection outbreak in Sacramento and Placer counties, March/April, 2000. State of California, Department of Health Services, Berkeley, California, 2000.
  2. O’Mahony M, Cowden J, Smyth B et al. An outbreak of Salmonella saint-paulinfection associated with beansprouts. Epidemiol Infect 1990;104:229-35.
  3. National Advisory Committee on Microbiological Criteria for Foods. Current topics in food microbiology: microbiological safety evaluations and recommendations on sprouted seeds. Int J Food Microbiol 1999;52:123-53.
  4. Feng P. A summary of background information and foodborne illness associated with the consumption of sprouts. U.S. Food and Drug Administration, Center for Food Safety and Applied Nutrition, Washington DC, 1997.
  5. Jerngklinchan J, Saitanu K. The occurrence of Salmonellae in bean sprouts in Thailand. Southeast Asian J Trop Med Public Health 1993;24:114-18.
  6. Taormina PJ, Beuchat LR, Slutsker L. Infections associated with eating seed sprouts: an international concern. Emerg Infect Dis 1999;5:626-34.
  7. Barrett E, Linn M, Woolard D et al. Outbreaks of Escherichia coli O157:H7 infection associated with eating alfalfa sprouts – Michigan and Virginia, June-July 1997. MMWR 1997;46:741-44.

Source:Lance Honish, BSc, CPHI(C), Environmental Health Epidemiologist; Quan Nguyen, MD, CPHI(C), Environmental Health Officer, Capital Health-Regional Public Health, Edmonton, Alberta.


Other SproutNet articles related to Salmonella PT913 outbreaks in bean sprout outbreaks:

“Outbreak of Salmonella Enteritidis Phage Type 913  Maine – January 2002” The EpiGram March 2002, Maine Bureau of Health’s Division of Disease Control.

“A Multi-County and Multi-State Outbreak of Salmonella Enteriditis (group D) Among Oriental Restaurant and Market Patrons” Bill L. Toth, MPH, Donna Walsh, RN, BSN, Zuber Mulla, PhD, MSPH, Dean Bodager, RS, MPA, Roberta Hammond, PhD.

“Trace Back, Maine 2002 Salmonella Enteritidis PT913 Bean Sprout Outbreak” Personal Communication, Anthony Yartel, MPH Infectious Disease Epidemiologist, Division of Disease Control, Maine Bureau of Health.