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).
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
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.). |
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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.). |
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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.). |
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Footnotes
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.
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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