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Publication #FSHN12-08

Outbreaks of Foodborne Diseases Associated with Tomatoes1

Angela M. Valadez, Keith R. Schneider, and Michelle D. Danyluk2

Fresh-market tomatoes are a popular commodity in homes and food service around the world. The inherent risks of contamination by foodborne pathogens present a challenge to the produce industry and regulators. Since fresh-market tomatoes are intended to be consumed fresh, there is no “kill-step” in the processing that would eliminate pathogens in the event that tomatoes become contaminated (Maitland et al., 2011). Public health officials often meet numerous challenges when conducting traceback investigations in the event of a produce outbreak, such as tomatoes. It is often difficult for them to isolate organisms from the raw product, when the raw product may have been consumed, discarded, or reached the end of its shelf-life (Lynch et al., 2009). It can be difficult for public health officials to determine where the implicated food was produced. As a consequence, recognizing unusual food vehicles, such as certain items of fresh produce, can delay the foodborne outbreak investigation (Lynch et al., 2009).

A “case” in a foodborne illness outbreak is identified as an infected patient carrying a strain that was isolated from a collected stool sample and documented to be associated with an outbreak. The number of sporadic cases linked to the consumption of contaminated fresh fruits and vegetables is unknown (Heaton and Jones 2008).

Figure 1. 

Tomatoes


Credit:

USDA Photo by Scott Bauer


[Click thumbnail to enlarge.]

This document is intended to serve as a reference for everyone concerned about the safety of fresh-market tomatoes by highlighting tomato-related outbreaks in the United States and Europe and reviewing locations and venues of tomato preparations as well as the severity of outbreaks. Three tables are presented, separated by foodborne outbreaks where tomatoes are confirmed as the food vehicle (Table 1); confirmed as part of complex foods vehicles (Table 2); and suspected, but not specified or confirmed, as the food vehicle (Table 3).

References

ACMSF (Advisory Committee on the Microbiological Safety of Food). 2005. Information Paper ACM/745: Microbiological status of ready to eat fruit and vegetables. Retrieved February 1, 2012, from http://www.food.gov.uk/multimedia/pdfs/acm745amended.pdf.

CDC (Centers for Disease Control and Prevention). 2011. Foodborne Outbreak Online Database (FOOD). Data retrieved February 1, 2012 from http://wwwn.cdc.gov/foodborneoutbreaks/Default.aspx.

FDA (US Food and Drug Administration). 2009. Safe Practices for Food Processes, Chapter IV: Outbreaks Tables, Analysis and Evaluation of Preventive Control Measures for the Control and Reduction/Elimination of Microbial Hazards on Fresh and Fresh-Cut Produce. Retrieved April 1, 2013, from http://www.fda.gov/Food/FoodScienceResearch/SafePracticesforFoodProcesses/ucm090977.htm.

Heaton, J. C., and K. Jones. 2008. Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: A review. Journal of Applied Microbiology 104(3): 613–626.

Hedberg, C. W., F. J. Angulo, K. E. White, C. W. Langkop, W. L. Schell, M. G. Stobierski, A. Schuchat, J. M. Besser, S. Dietrich, L. Helsel, P. M. Griffin, J. W. McFarland, and M. T. Osterholm. 1999. Outbreaks of salmonellosis associated with eating uncooked tomatoes: Implications for public health. Epidemiology and Infection 122: 385–393.

Lynch, M. F., R. V. Tauxe, and C. W. Hedberg. 2009. The growing burden of foodborne outbreaks due to contaminated fresh produce: Risks and opportunities. Epidemiology and Infection 137(3): 307–315.

Maitland, J. E., R. R. Boyer, J. D. Eifert, and R. C. Williams. 2011. High hydrostatic pressure processing reduces Salmonella enterica serovars in diced and whole tomatoes. International Journal of Food Microbiology 149(2): 113–117.

SSI (Statens Serum Institut). 2012. Outbreak of Salmonella Strathcona. Retrieved February 23, 2012, from http://www.ssi.dk/English/News/News/2012/2012_01_EPI-NEWS%204%20-%202012%20-%20Outbreak%20of%20salmonella%20Strathcona.aspx.

Tables

Table 1. 

Outbreaks of foodborne disease associated with tomatoes, 1990–2009

Year

Month

Location

Pathogenb

Location of consumption

Cases (deaths)

Food Vehicle

Reference

1990

NRa

US (multistate)

S. Javiana

Various

176 (0)

Tomato

Hedberg et al., 1999

1993

NR

US (multistate)

S. Montevideo

Various

100 (0)

Tomato

Hedberg et al., 1999

1994

NR

US (AK)

Hepatitis A

Food handler

92 (0)

Diced tomato

FDA, 2009

2002

February

US (CT)

S. Newport

Private home

7 (0)

Grape tomato

CDC, 2011

2004

June

US (multistate)

S. Braenderup

Private home; Restaurant – other or unknown type

137 (0)

Roma tomato

CDC, 2011

2004

July

US (multistate)

S. Anatum; Javiana; Muenchen; Thompson; Typhimurium

Restaurant – other or unknown type

429 (0)

Roma tomato

CDC, 2011

2005

July

US (multistate)

S. Newport

Restaurant – other or unknown type

52 (0)

Tomato

CDC, 2011

2005

November

US (multistate)

S. Braenderup

Restaurant – other or unknown type

84 (0)

Roma tomato

CDC, 2011

2006

September

US (ME)

S. Typhimurium

Unknown

8 (0)

Tomato

CDC, 2011

2006

January

US (PA)

S. Berta

Hospital; Nursing home, assisted living facility, home care; Restaurant – other or unknown type

16 (0)

Tomato

CDC, 2011

2007

June

US (multistate)

S. Newport

Private home; Restaurant – other or unknown type

65 (0)

Tomato

CDC, 2011

2009

May

US (MI)

S. Saintpaul

Private Home; Restaurant – "Fast-food" (drive-up service or pay at counter); Restaurant – Sit-down dining

21(0)

Tomato

CDC, 2011

aNR – Not reported

bPathogens abbreviated and associated with outbreaks include various serotypes of Salmonella (S.).

Table 2. 

Outbreaks of foodborne disease associated with complex foods including tomatoes, 1979–2008

Year

Month

Location

Pathogenb

Location of consumption

Cases (deaths)

Food Vehicle

Reference

1979

NRa

US (MA)

L. monocytogenes

Hospitals

20 (5)

Tomato, lettuce, celery

FDA, 2009

1989

NR

US (multistate)

G. lamblia

Unknown

21 (0)

Lettuce, onion, tomato

FDA, 2009

1992

NR

UK

Norovirus

Hospital

NR

Lettuce, tomato

ACMSF, 2005; Hughes et al., 2007

1995

NR

UK

S. Typhimurium DT104

Hotel

NR

Sandwich of turkey and tomato

ACMSF, 2005; Hughes et al., 2007

1995

NR

UK

E. coli O157

Pub

NR

Lettuce, tomato

ACMSF, 2005; Hughes et al., 2007

1996

NR

UK

Campylobacter

Hotel

NR

Lettuce, tomato

ACMSF, 2005; Hughes et al., 2007

1996

NR

UK

Norovirus

Club

NR

Tomato and cucumber salad

ACMSF, 2005; Hughes et al., 2007

2003

NR

UK

B. cereus

Unknown

NR

Quiche (tomato, lettuce, mushroom)

ACMSF, 2005; Hughes et al., 2007

2008

July

US (CA)

S. Blockley

Private home

9 (0)

Mole (sauce); and, pasta with tomato sauce

CDC, 2011

aNR – Not reported

bPathogens abbreviated and associated with outbreaks include various serotypes of Bacillus (B.), Escherichia (E.), Giardia (G.), Listeria (L.), and Salmonella (S.).

Table 3. 

Outbreaks of foodborne disease where tomatoes are suspected, but not specified or confirmed, 1998–2011

Year

Month

Location

Pathogena

Location of consumption

Cases (deaths)

Food Vehicle

Reference

1998/9

December/January

US (multistate)

S. Baildon

Nursing home, assisted living facility, home care

86 (3)

Tomato, unspecified

CDC, 2011

2000

November

US (multistate)

S. Thompson

Private home

43 (0)

Tomato, unspecified

CDC, 2011

2002

July

US (multistate)

S. Newport

Hospital; Restaurant – other or unknown type; School

510 (0)

Tomato, unspecified

CDC, 2011

2002

June

US (MA)

S. Javiana

Other; Restaurant – other or unknown type

3 (0)

Tomato, unspecified

CDC, 2011

2002

June

US (FL)

S. Javiana

Restaurant – other or unknown type

159 (0)

Tomato, unspecified

CDC, 2011

2003

March

US (CA)

S. Virchow

Other

11 (0)

Tomato, unspecified

CDC, 2011

2003

June

US (CA)

S. Saintpaul

Private home; Restaurant – other or unknown type

17 (0)

Mango, unspecified; Tomato, unspecified

CDC, 2011

2003

November

US (multistate)

S. Saintpaul

Restaurant – other or unknown type

33 (0)

Chicken, unspecified; Iceberg lettuce, unspecified; Tomato, unspecified

CDC, 2011

2005

July

US (NY)

S. Newport

Grocery store; Picnic; Private home; Restaurant – other or unknown type

27 (0)

Onion, unspecified; Tomato, unspecified

CDC, 2011

2005

June

US (WY)

S. Enteritidis

Private home; Restaurant – other or unknown type

20 (0)

Egg, unspecified; Tomato, unspecified

CDC, 2011

2005

June

US (CA)

S. Enteritidis

Picnic; Private home; Restaurant – other or unknown type; Workplace, not cafeteria

85 (0)

Salsa, unspecified

CDC, 2011

2006

June

US (MD)

S. Typhimurium

Private home; Restaurant – other or unknown type

18 (0)

Lettuce, unspecified; Tomato, unspecified

CDC, 2011

2006

September

US (multistate)

S. Typhimurium

Private home; Restaurant – other or unknown type

192 (0)

Tomato, unspecified

CDC, 2011

2006

June

US (multistate)

S. Newport

Restaurant – other or unknown type

115 (0)

Tomato, unspecified

CDC, 2011

2007

June

US

(Washington, DC)

S. Newport

Private home; Restaurant – other or unknown type

46 (0)

Avocado, unspecified; Cilantro; Guacamole, unspecified; Tomato, unspecified

CDC, 2011

2007

June

US (MD)

S. Javiana

Private home; Restaurant – other or unknown type

5 (0)

Cheese, unspecified; Chicken, unspecified; Tomato, unspecified; and, Unspecified fruit

CDC, 2011

2007

July

US (NY)

S. Newport

Unknown or undetermined

10 (1)

Tomato, unspecified

CDC, 2011

2007

October

US (MN)

S. Typhimurium

Restaurant – other or unknown type

23 (0)

Tomato, unspecified

CDC, 2011

2008

July

US (CA)

S. Braenderup

Restaurant – other or unknown type

17 (0)

Salsa, unspecified

CDC, 2011

2008

April

US (IA)

S. Braenderup

Restaurant – other or unknown type

12 (0)

Green salad; Tomato, unspecified

CDC, 2011

2011

October

Denmark

S. Strathcona

Various locations

43 (0)

Tomato, unspecified

SSI, 2012

aPathogens abbreviated and associated with outbreaks include various serotypes of Salmonella (S.).

Footnotes

1.

This document is FSHN12-08, one of a series of the Food Science and Human Nutrition Department, Florida Cooperative Extension Service, Institute of Food and Agricultural Sciences, University of Florida. Published May 2012. Visit the EDIS website at http://edis.ifas.ufl.edu.

2.

Angela M. Valadez, graduate research assistant, CREC (Citrus Research and Education Center, Lake Alfred, FL); Keith R. Schneider, associate professor, FSHN (Food Science and Human Nutrition Department, UF Main Campus); Michelle D. Danyluk (contact author), assistant professor, CREC; Institute of Food and Agricultural Sciences, University of Florida, Gainesville, FL 32611.

This review was supported by the Center for Produce Safety.


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U.S. Department of Agriculture, UF/IFAS Extension Service, University of Florida, IFAS, Florida A & M University Cooperative Extension Program, and Boards of County Commissioners Cooperating. Nick T. Place, dean for UF/IFAS Extension.