Multistate Outbreaks of Salmonella Infections Associated with Raw Tomatoes Eaten in Restaurants --- United States, 2005--2006
During 2005--2006, four large multistate outbreaks of Salmonella infections associated with eating raw tomatoes at restaurants occurred in the United States. The four outbreaks resulted in 459 culture-confirmed cases of salmonellosis in 21 states (Figure). This report describes the epidemiologic, environmental, and laboratory investigations into these four outbreaks by state and local health departments, national food safety agencies, and CDC. The results of these investigations determined that the tomatoes had been supplied to restaurants either whole or precut from tomato fields in Florida, Ohio, and Virginia. These recurrent, large, multistate outbreaks emphasize the need to prevent Salmonella contamination of tomatoes early in the production and packing process. Current knowledge of mechanisms for tomato contamination and methods of eradication of Salmonella in tomatoes is incomplete; the agricultural industry, food safety agencies, and public health agencies should make tomato-safety research a priority.
Salmonella Newport: Multiple States, July--November 2005
A total of 72 culture-confirmed S. Newport isolates with indistinguishable pulsed-field gel electrophoresis (PFGE) patterns (PulseNet XbaI pattern JJPX01.0061 [/ BlnI pattern JJPX01.0021]) were identified from stool specimens collected during July--November 2005 in 16 states (Delaware, Illinois, Maine, Maryland, Massachusetts, Missouri, New Hampshire, New Jersey, New York, North Carolina, Ohio, Pennsylvania, Tennessee, Vermont, Virginia, and Wisconsin) (1). Median patient age was 29 years (range: <1--75 years); 42 (58%) patients were female. Eight (11%) patients were hospitalized, and no deaths were reported.
A case-control study of persons aged 18 --70 years was conducted; 29 case-patients were matched geographically with 140 well community controls in nine states. Illness was associated with eating raw, large, red, round tomatoes at restaurants; 19 (70%) of 27 case-patients ate such tomatoes compared with 26 (20%) of 128 controls (matched odds ratio [mOR]: 9.7; 95% confidence interval [CI] = 3.3--34.9). Implicated tomatoes had been purchased whole and sliced at restaurants. No single restaurant or restaurant chain was associated with the outbreak.
Investigators determined that the implicated tomatoes were grown on two farms on the eastern shore of Virginia. The outbreak strain of S. Newport was isolated from irrigation pond water near tomato fields in this region in October 2005. This region also had been the source of tomatoes for a multistate outbreak of S. Newport infections in 2002 (1); strains from both outbreaks had the same PFGE pattern.
Salmonella Braenderup: Multiple States, November--December 2005
A total of 82 culture-confirmed S. Braenderup isolates with indistinguishable PFGE patterns (PulseNet XbaI pattern JBPX01.0050 [/ BlnI pattern JBPA26.0004]) were identified in eight states (Illinois, Indiana, Kentucky, Massachusetts, Michigan, Ohio, Pennsylvania, and West Virginia) during November--December 2005. Median patient age was 34 years (range: 6--78 years); 51 (67%) patients were female. Eighteen (35%) patients were hospitalized, and no deaths were reported.
A case-control study of persons aged 18--60 years was conducted; 38 case-patients were geographically matched to 108 well community controls in two states. Twenty (52%) of 38 patients had eaten at chain restaurant A compared with 13 (12%) of 108 controls (mOR: 19.9; CI = 4.6--86.6). Among chain restaurant A patrons, illness was associated with eating items containing raw, prediced Roma (i.e., plum) tomatoes (OR: 11.3; CI = 2.0--62.2).
The implicated tomatoes had been grown in one of two tomato fields in Florida and were prediced and packaged at a firm in Kentucky before being shipped to chain restaurant A. The environmental investigation revealed that multiple potential animal reservoirs of Salmonella (e.g., cattle, wild pigs, wild birds, amphibians, and reptiles) were present in and adjacent to the drainage ditches. Environmental samples from the farm, including drainage ditch water and animal feces from around the tomato fields, yielded Salmonella of different serotypes than the outbreak strain.
Salmonella Newport: Multiple States, July--November 2006
A total of 115 culture-confirmed S. Newport isolates with indistinguishable PFGE patterns (PulseNet XbaI pattern JJPX01.0061 [/ BlnI pattern JJPX01.0021]) were identified from stool specimens provided during July--November 2006 in 19 states (Colorado, Connecticut, Delaware, Georgia, Illinois, Kentucky, Maine, Massachusetts, Maryland, Michigan, New Jersey, New York, North Carolina, Ohio, Pennsylvania, Rhode Island, Tennessee, Virginia, and Washington). The PFGE pattern was identical to the pattern observed during the 2005 S. Newport outbreak. Median patient age was 28 years (range: <1 month--86 years); 54 (50%) patients were female. Eight (32%) patients were hospitalized, and no deaths were reported.
A case-control study of persons aged 18--75 years was conducted; 25 case-patients were geographically matched with 41 well community controls in nine states. Illness was associated with eating raw tomatoes in restaurants; 14 (67%) of 21 matched case-patients ate raw tomatoes in restaurants compared with nine (28%) of 32 controls (mOR: 4.9; CI = 1.03--23.3). No single restaurant or restaurant chain was associated with the outbreak. The source of the implicated tomatoes was not determined. An assessment of tomato-growing practices in the suspected region was conducted by the Food and Drug Administration (FDA) during the July 2007 growing season.
Salmonella Typhimurium: Multiple States and Canada, September--October 2006
A total of 190 culture-confirmed S. Typhimurium isolates with indistinguishable PFGE patterns (PulseNet XbaI pattern JPXX01.0604 [/ BlnI pattern JPXA26.0174]) were identified during September--October 2006 in 21 states (Arkansas, Connecticut, Georgia, Indiana, Kentucky, Maine, Massachusetts, Michigan, Minnesota, Nebraska, New Hampshire, New York, North Carolina, Ohio, Pennsylvania, Rhode Island, Tennessee, Vermont, Virginia, Washington, and Wisconsin). The median age of patients was 34 years (range: 2--88 years); 112 (58%) patients were female. Twenty-four (22%) patients were hospitalized, and no deaths were reported.
A case-control study of persons aged 18--70 years was conducted; 59 case-patients were geographically matched with 59 well community controls in nine states. Illness was associated with eating raw, large, red, round tomatoes at a restaurant; 26 (52%) of 50 case-patients ate such tomatoes compared with 12 (24%) of 50 controls (mOR: 3.1; CI = 1.3--7.3).
Implicated tomatoes were traced to a single packinghouse in Ohio supplied by three tomato growers from 25 fields in three counties. Tomato production had ended by the time the packinghouse was implicated. As a result, FDA deferred the investigation until the next growing season and completed the investigation in August 2007.
Reported by: SA Bidol, MPH, Michigan Dept of Community Health. ER Daly, MPH, New Hampshire Dept of Health and Human Svcs. RE Rickert, MPH, Pennsylvania Dept of Health. S. Newport Investigation Team 2005, S. Braenderup Investigation Team 2005, S. Newport Investigation Team 2006, S. Typhimurium Investigation Team 2006, PulseNet. TA Hill, MPH, S Al Khaldi, PhD, Food and Drug Admin. TH Taylor Jr, MS, Div of Bacterial Diseases, National Center for Immunization and Respiratory Diseases; MF Lynch, MD, JA Painter, DVM, CR Braden, MD, PA Yu, MPH, L Demma, PhD, Div of Foodborne, Bacterial, and Mycotic Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases; C Barton Behravesh, DVM, CK Olson, MD, SK Greene, PhD, AM Schmitz, DVM, DD Blaney, MD, M Gershman, MD, EIS officers, CDC.
Salmonella infections can be transmitted through various foods and cause an estimated 1.4 million illnesses and 400 deaths annually in the United States (2). The first large multistate outbreak of Salmonella infections was linked to contaminated tomatoes in 1990, when Salmonella Javiana caused 176 illnesses in four Midwestern states (3). Since 1990, at least 12 multistate outbreaks of salmonellosis traced to various types of tomatoes (e.g., red, round; Roma; and grape) have been reported to the CDC Electronic Foodborne Outbreak Reporting System (eFORS) by state public health departments. These 12 outbreaks accounted for approximately 1,990 culture-confirmed infections. However, because an estimated 97.5% of Salmonella infections are not confirmed by culture, these outbreaks might have resulted in as many as 79,600 illnesses (2).
Approximately 5 billion pounds of fresh tomatoes are eaten annually in the United States. The data in this report demonstrate the potential for large outbreaks of Salmonella infections caused by contaminated tomatoes. The outbreaks described were widely dispersed, indicating that contamination occurred early in the distribution chain, such as at the farm or packinghouse, rather than in restaurants. Illness in the four multistate outbreaks was associated with eating tomatoes that originated from growing regions in Florida, Ohio, and Virginia. Clusters of infections with S. Newport PFGE pattern JJPX01.0061 have been detected every year since 2002 and were traced to tomatoes grown in Virginia in 2002 and 2005. These recurrent multistate outbreaks indicate that the tomato-growing environment is an ongoing source of contamination of tomatoes.
Possible sources for environmental Salmonella contamination of tomatoes include feces from domestic or wild animals (e.g., reptiles, amphibians, or birds) or contaminated habitats, such as ponds or drainage ditches. Although the mechanism by which tomatoes become contaminated is not known, certain possibilities are suggested by experimental evidence. Tomatoes can internalize Salmonella when they are immersed in water with a temperature less than the temperature of the tomato (4). Tomatoes also can become internally contaminated when tomato stems and flowers are inoculated with Salmonella (5), which can occur during growth if contaminated water is applied directly to plants. Contamination on the tomato surface also can be transferred to the interior of a tomato when it is cut. Once contaminated, cut tomatoes provide an efficient medium for bacterial amplification (6).
Tomatoes served in restaurants pose a particular concern because restaurants often store and handle tomatoes in ways that allow for amplification of bacteria. In response to these recurrent outbreaks and experimental evidence that Salmonella can replicate on the surface of a cut tomato, the 2007 FDA Federal Food Code has been amended so that cut tomatoes (because they have a pH >4.2 and water activity >0.99*) are defined as a "time/temperature control for safety" food, which requires refrigeration of cut, sliced, or processed tomatoes (7). In addition, growers, harvesters, repackers, retailers, and food service employees should follow guidelines for good manufacturing practices and good agricultural practices when handling tomatoes (8,9).
Consumers should avoid purchasing bruised or damaged tomatoes. All tomatoes, including those grown conventionally or organically at home or purchased from a grocery store or farmer's market, should be thoroughly washed under running water just before eating. Tomatoes that appear spoiled should be discarded. Cut, peeled, or cooked tomatoes should be refrigerated within 2 hours or discarded. Refrigeration of cut tomatoes at 40°F (4.4°C) is needed to maintain both quality and safety. Cut tomatoes should be separated from raw, unwashed produce items, raw meats, and raw seafood.
To prevent future tomato-associated outbreaks of Salmonella infections, further environmental and laboratory research is necessary to determine the source and routes of contamination, mechanisms by which pathogens contact tomatoes and become internalized, the stages of development at which plants are most susceptible to contamination that persists, and procedures by which contamination can be reduced or eliminated. Toward this end, the North American Tomato Trade Work Group published Commodity Specific Food Safety Guidelines for the Fresh Tomato Supply Chain in May 2006 to promote adoption of good agricultural practices throughout the fresh tomato supply chain. Traceback investigations in future outbreaks should consider all levels of tomato production, including the field and packinghouse. Studies focused on these areas should be a priority for the agricultural industry, food safety agencies, and the public health community.
This report is based, in part, on data contributed by state and local public health departments in Arkansas, Connecticut, Delaware, Georgia, Illinois, Indiana, Kentucky, Maine, Maryland, Massachusetts, Michigan, Minnesota, Missouri, Nebraska, New Hampshire, New Jersey, New York, North Carolina, Ohio, Pennsylvania, Rhode Island, Tennessee, Vermont, Virginia, Washington, West Virginia, and Wisconsin; Food and Drug Administration; and RM Hoekstra, PhD, A Wilkinson, DVM, Div of Foodborne, Bacterial, and Mycotic Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases, CDC.
- Greene SK, Daly ER, Talbot EA, et al. Recurrent multistate outbreak of Salmonella Newport associated with tomatoes from contaminated fields, 2005. Epidemiol Infect 2007;May3:1--9 [Epub ahead of print].
- Voetsch AC, Van Gilder TJ, Angulo FJ, et al. FoodNet estimate of the burden of illness caused by nontyphoidal Salmonella infections in the United States. Clin Infect Dis 2004;38(Suppl 3):S127--34.
- Hedberg CW, Angulo FJ, White KE, et al. Outbreaks of salmonellosis associated with eating uncooked tomatoes: implications for public health. Epidemiol Infect 1999;122:385--93.
- Zhuang, RY, Beuchat, LR, Angulo, FJ. Fate of Salmonella Montevideo on and in raw tomatoes as affected by temperature and treatment with chlorine. Appl Environ Microbiol 1995;61:2127--31
- Guo X, Chen J, Brackett RE, Beuchat LR. Survival of salmonellae on and in tomato plants from the time of inoculation at flowering and early stages of fruit development through fruit ripening. Appl Environ Microbiol 2001;67:4760--4.
- Lin C, Wei C. Transfer of Salmonella Montevideo onto the interior surfaces of tomatoes by cutting. J Food Prot 1997;60:858--62.
- Food and Drug Administration. 2005 food code. College Park, MD: US Department of Health and Human Services, Food and Drug Administration; 2005. Available at http://www.cfsan.fda.gov/~dms/fc05-toc.html.
- Food and Drug Administration. Guidance for industry: guide to minimize microbial food safety hazards of fresh-cut fruits and vegetables. College Park, MD: US Department of Health and Human Services, Food and Drug Administration; 2007. Available at http://www.cfsan.fda.gov/~dms/prodgui3.html.
- North American Tomato Trade Work Group to Further Adoption of Good Agricultural Practices throughout the Fresh Tomato Supply Chain, 2006. Commodity specific food guidelines for the fresh tomato supply chain. Available at http://www.tomato.org/contentassets/fdaguidefinal.pdf.
* A measure of the free moisture in a food. Pure water has a water activity of 1.0 and potentially hazardous foods have a water activity of 0.85 and higher.
All MMWR HTML versions of articles are electronic conversions from typeset documents.
This conversion might result in character translation or format errors in the HTML version.
Users are referred to the electronic PDF version (http://www.cdc.gov/mmwr)
and/or the original MMWR paper copy for printable versions of official text, figures, and tables.
An original paper copy of this issue can be obtained from the Superintendent of Documents, U.S.
Government Printing Office (GPO), Washington, DC 20402-9371;
telephone: (202) 512-1800. Contact GPO for current prices.
**Questions or messages regarding errors in formatting should be addressed to firstname.lastname@example.org.