ARCHIVED - Salmonella Enteritidis Outbreak Linked to a Local Bakery, British Columbia, Canada

 

Volume 31-07  1 April 2005

Introduction

The association between Salmonella Enteritidis (S. Enteritidis) contaminated raw shell eggs and human illness is well established(1-8). In the United States, S. Enteritidis contaminated shell eggs were a major contributor to foodborne illness starting in the late 1970's(9-11). Although S. Enteritidis related foodborne illness declined with the introduction of S. Enteritidis control programs, periodic outbreaks and sporadic cases continue to occur. In the past, numerous outbreaks have been linked to the use of raw or undercooked eggs in foods(12-14) and to cross-contamination of other foods from improper food handling practices(2,15). In Canada and provincially, in British Columbia (B.C.), S. Enteritidis is the second most common Salmonella serovar isolated, second only to S. Typhimurium;(16) however, large outbreaks specifically linked to raw shell eggs are uncommon in Canada.

During the first 2 weeks of August, 2000, 15 S. Enteritidis clinical isolates received by Laboratory Services, British Columbia Centre for Disease Control (BCCDC) were found to have indistinguishable pulse field gel electrophoresis (PFGE) patterns. Interviews with four subsequent cases found that they had eaten baked products from the same bakery, Bakery X. Bakery X had a main central commissary that produced products for final preparation, and a number of outlet bakeries. An investigation was initiated to confirm the outbreak source and contributing factors, and to determine the extent of the outbreak.

Methods

Case Definition

A case was defined as an individual with laboratory confirmed S. Enteritidis isolated from their stool between 15 July, 2000 and 15 September, 2000 with a PFGE pattern indistinguishable from the outbreak strain. Cases residing in the same household with symptom onset greater than 24 hours after the initial household case were treated as secondary cases.

Case-Control Study

A case-control study included 11 cases and controls. Controls were randomly selected from case notifications of campylo- bacteriosis from 1999(17) and matched on sex, age and ethnicity. Case and control subjects were interviewed on consumption of specific food and baked products by telephone using a standard questionnaire.

Enhanced Surveillance

Enhanced surveillance was conducted on all laboratory-confirmed cases of S. Enteritidis infection occurring between 15 July, 2000 and 15 September, 2000. Cases were interviewed by telephone using a questionnaire that asked about onset date, symptoms, demographics, consumption of baked products from Bakery X and purchase, preparation, and consumption of shell eggs.

Environmental Health Investigation

An environmental health investigation was conducted at both the main commissary and the implicated bakery outlet. Production and distribution information on baked products was obtained. Both premises were inspected for adequate food storage facilities, appropriate food preparation areas and sanitation practices. Food samples, both raw ingredients and baked product, were obtained from both sites. Stool samples were collected from all food handling staff employed at the bakery and analysed for bacterial pathogens.

Microbiological Investigation

Food samples were processed using pre-enrichment (non-selective) and selective procedures for the detection of Salmonella in foods according to the United States Food and Drug Administration Bacteriological Analytical Manual(18). The enrichment cultures were sub-cultured onto selective plates and suspect colonies were tested biochemically.

Stool specimens were cultured for Salmonella by direct plating and enrichment. Suspicious colonies were biochemically confirmed and Salmonella isolates were serotyped using the standard international scheme for Salmonella(19). Confirmed S. Enteritidis were then analysed by PFGE using the standardized protocol PulseNet and the National Molecular Subtyping Network for Foodborne Disease Surveillance by BCCDC Laboratory Services(20). The interpretation was carried out according to the criteria specified by Tenover et al.(21) Phage typing of the isolates was performed by the National Laboratory for Enteric Pathogens, Health Canada(22).

Traceback

An egg traceback was done by the Canadian Food Inspection Agency (CFIA) to identify the producer of eggs supplied to the central commissary and to determine the distribution of the implicated eggs.

Statistical Analysis

Descriptive statistics (means and percents) were used to describe age, sex, geographic distribution, gastrointestinal symptoms, and hospitalization. Mantel-Haenszel matched odds ratios and 95% exact confidence limits were calculated for each food product using Epi Info, version 6.04b. In the case of an undefined odds ratio, the p-value of the Mantel-Haenszel summary chi-square was reported.

Results

Case Control Study

All 11 cases had eaten a baked product from Bakery X compared to zero controls (odds ratio (OR) undefined, p = 0.004) (Table 1). Individuals who consumed the coconut cream bun were significantly more likely to become ill (OR undefined, p = 0.04). The small number of cases precluded finding significant associations for products less frequently consumed although egg custard tarts and ham and egg buns were also consumed by cases.

Table 1. Matched odds ratios for implicated baked goods from Bakery X

Food

Discordant matched pairs

 

Case exposed
(n = 11)

Control exposed
(n = 11)

Odds ratio

Confidence interval

P-value

Baked Products

9

0

undefined

-

0.008

Products from Bakery X*

10

0

undefined

-

0.004

Coconut buns*

6

0

undefined

-

0.04

Egg tarts

2

0

2.00

0.10 - 117.99

0.48

Pineapple buns*

2

9

undefined

-

0.48

* Missing data for one matched pair


Enhanced Surveillance

Sixty-two laboratory-confirmed primary cases of S. Enteritidis accrued over an 8-week period and met the case definition. Phage typing further characterized the isolates as phage type (PT) 8. Of the 55 cases in which exposure data related to Bakery X were available, 48 (87%) reported consuming a baked product from the bakery. The median case age was 10 years and 38% were female (Figure 1). Fifteen cases (27%) reported bloody diarrhea; five cases (10%) were hospitalized an average of 2 days. The epidemic curve by symptom onset depicted a bimodal distribution, peaking at week 32 and week 35 (Figure 2).


Figure 1. S. Enteritidis cases associated with Bakery X, by age and sex

Figure 1. S. Enteritidis cases associated with Bakery X, by age and sex

Figure 2. Epidemic curve of S. Enteritidis cases by date of illness onset

Figure 2. Epidemic curve of S. Enteritidis cases by date of illness onset

Environmental Health Investigation

Only the one bakery outlet, Bakery X was linked to cases. Both the main commissary that pre-prepares the frozen dough and fillings and Bakery X, the processor of the final baked product, were inspected. Pooling of large quantities of raw shell eggs occurred at the main commissary. The pooled eggs were used for the egg tart filling. Whole raw shell eggs, of which 75% were grade B eggs, were distributed by the commissary to the bakery outlets for preparation of the egg wash which was brushed on the dough before baking and for preparing the filling for the ham and egg bun.

Inspection of bakery operations at the Bakery X outlet revealed poor hand-washing practices and questionable food preparation and handling practices. Food preparation counters were not separated from the finished product and inspection of the oven revealed inadequate and uneven cooking temperatures. The internal temperature of an egg tart measured post-baking was < 60°C.

Microbiologic Investigation

All food samples taken from the commissary (whole shell eggs, coconut cream filling, egg tart filling) were negative for S. Enteritidis. Both the egg wash and the coconut sample (used as a topping post-baking) from Bakery X were positive for S. Enteritidis. The PFGE pattern was indistinguishable from the outbreak pattern and phage typing was identical to the human isolates.

Stool samples from a single bakery employee, a baker, were positive for S. Enteritidis PT 8 with a PFGE pattern indistinguishable from the outbreak pattern. Employees frequently consumed baked products from the bakery. The baker's symptom onset corresponds with the second peak in the epidemic curve (Figure 1).

Traceback / Public Health Action

A traceback of eggs used at Bakery X was conducted by the CFIA. Eggs were traced to a single farm. S. Enteritidis PT 8 and the outbreak PFGE pattern were isolated from environmental samples from the producer's barn. All shell eggs from the barn were diverted for pasteurization and an egg recall including commercial and public sector sales was carried out.

Bakery X was subsequently closed, implicated baked products containing egg were discarded and a product advisory issued. A food safety plan was devised and implemented which included the use of pasteurized liquid egg at all locations including the commissary. The baker was excluded from work until two consecutive stool cultures, taken at least 24 hours apart, were negative.

Discussion

This outbreak was linked to the consumption of S. Enteritidis contaminated baked goods. In addition to the raw shell eggs, three key factors likely contributed to the initiation and propagation of this outbreak: poor food handling practices, inadequate baking temperatures, and an ill baker.

First, poor food handling practices allowed finished baked products to become contaminated. Cross-contamination from the S. Enteritidis contaminated egg wash used as a glaze and subsequent contamination of the coconut, which was spread by an ungloved hand on the finished product, played a key role in this outbreak. S. Enteritidis contaminated shell eggs have been implicated in numerous baked/dessert product outbreaks worldwide(7,8,15,23-25), with recent outbreaks being linked to cross-contamination(26-27). Separation between raw and finished product work surfaces and utensils is essential to prevent cross-contamination.

Second, the oven temperature was inadequate, an essential critical control point. Adequate heat treatment of egg-containing products

eliminates Salmonella provided recontamination doesn't occur. Product temperature post-baking should be monitored periodically to ensure the appropriate temperature has been reached. The use of pasteurized eggs would also provide a safer alternative to shell eggs given the practice of pooling large quantities of raw shell eggs by the commissary.

Third, the baker himself was a contributing factor in this outbreak. The baker was likely the victim of his own practices, whether it was from poor hand washing or from consuming the product himself. He became ill midway through the outbreak and likely propagated the second wave of the outbreak. Numerous outbreaks have been associated with ill food handlers/servers who continue to work throughout their illness and either initiate or perpetuate an outbreak(2,6,28-35).The importance of hand washing and abstaining from work during an illness for food handlers cannot be over-emphasized. Certification of all food handlers, repeat educational opportunities to emphasize appropriate hand- washing technique and abstinence from work during episodes of gastrointestinal illness, as well as a sick leave policy that accommodates ill employees(36) would help to prevent food handler- related outbreaks.

In B.C., mandatory food safe programs based on the Hazard Analysis Critical Control Points (HACCP) framework were implemented in April 2001. This regulation requires every operator of a food establishment to hold a valid certificate issued by a health professional for completion of a food handler program. When the operator is absent, only one employee must be certified in food safety. In this outbreak, multiple critical control points were bypassed in the preparation of the baked goods. Food safe programs should be mandatory and reviewed periodically, not only for the operator of the food establishment but also for all individuals involved in food handling.

Seventy-five percent of the raw shell eggs used by the commissary were grade B eggs. Grade B eggs may be covered with dirt (including faeces) and are generally only sold to commercial (restaurant/bakery) establishments. Although a causal association between illness and grade B eggs cannot be proven, eggs that are soiled with feces impose an undue risk and should not be used. As a result of this outbreak, the egg-grading station no longer distributes shell eggs covered with visible contaminants.

More aggressive campaigns to reduce S. Enteritidis associated illness have been implemented in both Britain and the United States. Britain introduced a S. Enteritidis vaccination program for its layers in the year 2000 and has reported a provisional 50% reduction in human illness since its introduction(37). In 2001, the United States introduced safe handling labels on egg cartons to reduce S. Enteritidis associated illness(38). In B.C., the number of reported S. Enteritidis case notifications has remained stable over the past 4 years after nearly a decade of decline. Although outbreaks associated with S. Enteritidis contaminated eggs have been rare in B.C., the actual number of sporadic S. Enteritidis cases associated with egg consumption is unknown. Several studies have demonstrated that individuals infected with S. Enteritidis were more likely to consume eggs 3 days prior to becoming ill(14,39); hence, follow-up of future S. Enteritidis cases is needed to establish morbidity related to raw shell egg consumption and the need for further prevention strategies.

In response to this outbreak, a committee was formed to review farm-to-table practices in B.C. to prevent future outbreaks and illness related to raw shell egg consumption. Recommendations include: testing layer feed for Salmonella and monitoring these results, enhancing surveillance of subtypes of environmental Salmonella isolates obtained from producers and comparison with human isolate subtypes; removing grade B eggs covered in feces from the market; and repeatedly distributing information for the public and the food industry on averting high-risk practices.

Conclusion

Foodborne outbreaks linked to commercial bakeries have the potential to affect a large proportion of the population and result in substantial morbidity. Poor sanitary and food handling practices can result in the spread of S. Enteritidis from contaminated shell eggs to finished product. Food safety training programs should be mandatory for all individuals involved in food preparation/handling. Laboratory surveillance of human and environmental isolates of S. Enteritidis should be integrated in order to evaluate the effectiveness of current policies and programs aimed at reducing S. Enteritidis associated illness in B.C.

Acknowledgements

We thank the Richmond/Vancouver Health Board, South Fraser Health Region and Simon Fraser Health Region for their assistance in this outbreak investigation, especially Dalton Cross CPHI(C) for his contribution to the investigation.

References

  1. Ejidokun OO, Killalea D, Cooper M et al. Four linked outbreaks of Salmonella enteritidis phage type 4 infection - the continuing egg threat. Commun Dis Public Health 2000;3:95-100.

  2. McNeil MM, Sweat LB, Carter JR SL et al. A Mexican restaurant-associated outbreak of Salmonella enteritidis type 34 infections traced to a contaminated egg farm. Epidemiol Infect 1999;122:209-15.

  3. Dodhia H, Kearney J, Warburton F. A birthday party, home-made ice cream, and an outbreak of Salmonella enteritidis phage type 6 infection. Commun Dis Public Health 1998;1:31-34.

  4. Mackenzie AR, Laing RBS, Cadwgan TMS et al. Raw egg ingestion and salmonellosis in body builders. Scot Med J 1998;43:146-47.

  5. Pilon PA, Laurin M. Outbreak of Salmonella enteritidis phage type 8 in a Montreal hotel. CCDR 1997;23:148-50.

  6. Doherty L, McCartney M, Mitchell E et al. An outbreak of Salmonella enteritidis phage type 4 infection in a rural community in Northern Ireland. Commun Dis Rep CDR Rev 1997;7:R73-76.

  7. Harrison C, Quigley C, Kaczmarski E et al. An outbreak of gasto-intestinal illness caused by eggs containing Salmonella enteritidis phage type 4. J Infect 1992;24:207-10.

  8. Barnes GH, Edwards AT. An investigation into an outbreak of Salmonella enteritidis phage-type 4 infection and the consumption of custard slices and trifles. Epidemiol Infect 1992;109:397-403.

  9. Mason J. Salmonella enteritidis control programs in the United States. Int J Food Microbiol 1994;21:155-69.

  10. Rodrigue DC, Tauxe RV, Rowe B. International increase in Salmonella enteritidis: a new pandemic? Epidemiol Infect 1990;105:21-27.

  11. Hogue A, White P, Guard-Petter J et al. Epidemiology and control of egg-associated Salmonella enteritidis in the United States of America. Rev Sci Tech 1997;16:542-53.

  12. Angulo FJ, Swerdlow DL. Salmonella enteritidis infections in the United States. J Am Vet Med Assoc 1998;213:1729-31.

  13. Wilson D, Patterson WJ, Hollyoak V et al. Common source outbreak of salmonellosis in a food factory. Commun Dis Public Health 1999;2:32-34.

  14. Hayes S, Nylen G, Smith R et al. Undercooked hens eggs remain a risk factor for sporadic Salmonella enteritidis infection. Commun Dis Public Health 1999;2:66-67.

  15. Wight JP, Cornell J, Rhodes P et al. Four outbreaks of Salmonella enteritidis phage type 4 food poisoning linked to a single baker. Commun Dis Rep CDR Rev 1996;6:R112-15.

  16. Cuff WR, Ahmed R, Woodward DL et al. Enteric pathogens identified in Canada. Annual Summary, 1998. Winnipeg: Minister of Public Works and Government Services Canada, 2000.

  17. McCarthy N, Giesecke J. Case-case comparisons to study causation of common infectious diseases. Int J Epidemiol 1999;28:764-68.

  18. Andrews WH, June GA, Sherrod PS et al. Salmonella. In: U.S. Food and Drug Administration Bacteriological Analytical Manual, 8th ed., 1998, AOAC International, Gaithersburg, MD.

  19. Popoff MY, LeMinor L. Antigenic formulas of the Salmonella serovars, 6th ed. 1992. World Health Organization Collaborating Centre for Reference and Research on Salmonella. Pasteur Institute, Paris, France.

  20. Centers for Disease Control and Prevention. 1998. Standardized molecular subtyping of foodborne bacterial pathogens by pulsed-field gel electrophoresis. The National Molecular Subtyping Network for Foodborne Disease Surveillance, Centers for Disease Control and Prevention, Atlanta, GA.

  21. Tenover FC, Arbeit RD, Goering RV et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: Criteria for bacterial strain typing. J Clin Microbiol. 1995;33:2233-39.

  22. Ward LR, de Sa JD, Rowe B. A phage-typing scheme for Salmonella enteritidis. Epidemiol Infect 1987;99:291-94.

  23. Evans MR, Tromans JP, Dexter ELS et al. Consecutive salmonella outbreaks traced to the same bakery. Epidemiol Infect 1996;116:161-67.

  24. Reporter R, Mascola L, Kilman L et al. Outbreaks of Salmonella serotype Enteritidis infection associated with eating raw or undercooked shell eggs United States, 1996-1998. MMWR 2000:73-79.

  25. Tsuji H, Shimada K, Hamada K. Outbreak of Salmonella enteritidis caused by contaminated buns peddled by a producer using traveling cars in hyogo and neighboring prefectures in 1999: An epidemiological study using pulsed-field gel electrophoresis. Jpn J Infect Dis 2000;53(1):23-4.

  26. Humphrey TJ. Contamination of egg shell and contents with Salmonella enteritidis: A review. Int J Food Microbiol 1994;21(1-2):31-40. Review.

  27. Humphrey TJ, Martin KW, Whitehead A. Contamination of hands and work surfaces with Salmonella enteritidis PT4 during the preparation of egg dishes. Epidemiol Infect 1994;113:403-09.

  28. Hedberg CW, White KE, Johnson JA et al. An outbreak of Salmonella enteritidis infection at a fast-food restaurant: Implications for foodhandler-associated transmission. J Infect Dis 1991;164:1135-40.

  29. Patterson T, Hutchings P, Palmer S. Outbreak of SRSV gastroenteritis at an international conference traced to food handled by a post-symptomatic caterer. Epidemiol Infect 1993;111:157-62.

  30. Dunn RA, Hall WN, Altamirano JV et al. Outbreak of Shigella flexneri linked to salad prepared at a central commissary in Michigan. Public Health Rep 1995;110:580-96.

  31. Quiroz ES, Bern C, MacArthur JR et al. An outbreak of cryptosporidiosis linked to a foodhandler. J Infect Dis 2000;2:695-700.

  32. Olsen SJ, Hansen GR, Bartlett L et al. An outbreak of Campylobacter jejuni infections associated with food handler contamination: the use of pulsed-field gel electrophoresis. J Infect Dis 2001;184:242-44.

  33. Maguire H, Pharoah P, Walsh B et al. Hospital outbreak of Salmonella virchow possibly associated with a food handler. J Hosp Infect 2000;48:324-25.

  34. Honish L, Bergstrom K. Hepatitis A infected food handler at an Edmonton, Alberta retail food facility: Public health protection strategies. CCDR 2001;27:177-80.

  35. Olsen SJ, Hansen GR, Bartlett L et al. An outbreak of Campylobacter jejuni infections associated with food handler contamination: The use of pulsed-field gel electrophoresis. J Infect Dis 2001;183:164-67.

  36. Altekruse SF, Cohen ML, Swerdlow DL. Emerging foodborne diseases. Emerg Infect Dis 1997;3:285-93.

  37. Press Release 9 February 2001. Salmonella infections at lowest level since 1985. http://www.phls.org.uk/press_media/ press_releases/archive/01pr/010209pr.htm

  38. Department of Health and Human Services, Food and Drug Administration. Food labelling, safe handling statements, labelling of shell eggs; refrigeration of shell eggs held for retail distribution. Federal Register vol. 65, No 234, December 5, 2000 Rules and Regulations.

  39. Hedberg CW, David MJ, White KE et al. Role of egg consumption in sporadic Salmonella enteritidis and Salmonella typhimurium infections in Minnesota. J Infect Dis 1993;167(1):107-11.

Source: B Strauss, RN, MSc, Field Epidemiology Training Program, British Columbia Centre for Disease Control (BC CDC), Vancouver, British Columbia (BC); M Fyfe, MD, MSc, FRCPC, BC CDC, Vancouver, BC; K Higo, CPHI(C), Vancouver/Richmond Health Board, BC; M Sisler, CPHI(C), Vancouver/Richmond Health Board, BC; A Paccagnella, BSc, BC CDC, Vancouver, BC; A Trinidad, ART, BScPH, BC CDC, Vancouver, BC; K Louie, CPHI(C), South Fraser Health Region, BC; C Kurzac, CPHI(C), Vancouver/ Richmond Health Board, BC; B Zaharia, CPHI(C) Vancouver/ Richmond Health Board, BC.


Page details

Date modified: