In May 2008, a multistate outbreak of Salmonella enterica serotype Saintpaul infections with indistinguishable pulsed-field gel electrophoresis (PFGE) patterns was detected which ultimately became the largest known foodborne outbreak in the United States in over 10 years. Initial investigations identified an association between illness and the consumption of raw tomatoes [6]. On June 7, the US Food and Drug Administration (FDA) issued a national alert to avoid “raw red plum, red Roma, and red round tomatoes” [7].

As cases continued to occur, a specific variety of tomato could not be epidemiologically implicated and the sources of suspected tomatoes were not converging to any specific growing region or to a common distributor. Furthermore, a possible association between infections and eating Mexican-style foods began to emerge. Because tomatoes are a staple ingredient in many cuisines, not just Mexican, this finding suggested there might be something else, besides tomatoes, more unique to Mexican food involved. Collectively, these observations raised concern that an unidentified vehicle of infection might exist.

This outbreak is one in a series of increasingly recognized, large, and widely-dispersed outbreaks caused by contaminated produce [10]–[17]. The proportion of all reported foodborne outbreaks in the United States associated with contaminated produce increased from 0.7% in the 1970s to 6% in the 1990s; this trend appears to be ongoing [2], [3]. Related forces likely driving this shift include increasing consumption of fresh produce, increasing centralization of the produce industry to maintain year-round availability, expansion of growing fields to areas adjacent to animal production areas, and improved detection and investigation of widely dispersed outbreaks [1], [2], [18]. Centralization might foster outbreaks by increasing the number of points at which contamination may occur and the amount of product that could be contaminated in a given event. Centralization could also lead to more widely dispersed outbreaks because contaminated produce may be widely distributed [19].

Routine laboratory-based surveillance, especially molecular subtyping by PulseNet USA, has greatly improved our ability to detect widely dispersed outbreaks [20]. However, investigation of these outbreaks can be challenging when there is little apparent epidemiologic clustering by person, place, or time, and because of time delays inherent with laboratory-based surveillance. When generating hypotheses, investigators must consider an enormous list of possible food, water, animal, and environmental exposures [2]. Furthermore, patients are often interviewed several weeks after becoming ill, when recall of basic foods consumed is limited, and even more diminished for specific details, such as tomato type or ingredients within prepared dishes.

Our investigations highlight how these challenges can be reduced by searching for and investigating clusters of cases associated with specific food establishments or events within a larger outbreak. Investigations of localized clusters simplify hypothesis generation because the suspected sources of infection are usually limited to a finite list of menu items [2]. Likewise, patient recall is enhanced by focusing on a specific, often memorable, meal. Furthermore, investigators can obtain recipes to assess associations between illness and specific ingredients; this is especially helpful in identifying stealthy vehicles, such as jalapeño peppers, that some people might have been unaware they consumed. Additionally, turnover rate of ingredients within restaurants can be evaluated to find those ingredients that best fit the exposure period of patients in the outbreak. For example, at Restaurant A we noted that approximately 25 boxes of tomatoes would have been used during the 4-day period when patients ate there compared with one box of jalapeno peppers; thus contamination present in just one box of peppers could account for the Restaurant A outbreak duration. Finally, food delivery invoices kept by restaurants and caterers contain specific information that can improve the accuracy of traceback investigations; this is particularly important in fresh produce-associated outbreaks because fruits and vegetables sold in stores typically come in many varieties and may have minimal labeling to identify their source. Collectively, these attributes of localized cluster investigations serve to generate more specific exposure information [21].

Detailed exposure information allowed us to document the stealthy nature of jalapeño peppers in this outbreak. Three case-patients in our study of Restaurant Chain B also participated in a multistate case-control study [6]. Our study, aided by restaurant recipes, documented that all three consumed foods containing raw jalapeño peppers at the restaurant, as all reported having consumed salsa; one patient also reported adding raw jalapeño peppers to an entrée. In the multistate study, which asked patients to recall consumption of specific ingredients in restaurants, the two patients, whose only exposure to raw jalapeño peppers at Restaurant Chain B was from salsa, denied exposure to this ingredient, presumably because they were unaware that it was present in the salsa.

Some restaurant-prepared fresh salsas might be prone to amplifying and spreading small amounts of bacterial contamination present on a few individual produce items to a large number of servings because they often are made in large batches containing pooled and diced raw produce ingredients [21]. Salmonella grows better on diced, as compared with intact, tomatoes and jalapeño peppers [22]. Diced tomatoes, and any foods containing them, unless acidified to a pH of <4.2, are included in the 2009 FDA Food Code as a potentially hazardous food, and thus require storage at or below 41°F (5°C) [23]. High Salmonella growth rates have been observed in salsas prepared using the Restaurant A and Restaurant Chain B recipes at temperatures at or above 54°F (12°C) [22]. Growth might be reduced by replacing granulated garlic with fresh garlic and adding lime juice to the recipes [22].

Because so much produce is consumed raw and disinfection methods are not highly effective on fresh produce, the keys to preventing produce-associated outbreaks are preventing the initial contamination and minimizing handling practices that lead to amplification [2]. Water used for irrigation and pesticide application is one possible source of contamination in this outbreak. Keeping water used for these purposes protected from animals and waste run-off is important. Modifying salsa recipes to include growth-inhibitory ingredients might limit amplification of Salmonella [22]; all fresh salsas with a pH ≥4.2 should be stored in adherence with established time and temperature recommendations to minimize growth [24]. Additionally, because Salmonella grows rapidly in diced jalapeño peppers, regulatory consideration is warranted to define foods containing them as potentially hazardous.

During the summer of 2008, 1,500 Salmonella serotype Saintpaul infections with the outbreak PFGE pattern were reported from 43 states and the District of Columbia and Canada. Shortly after jalapeño peppers were identified as the probable source of infections in the two Texas clusters described in this report, an independent investigation of restaurant-acquired serotype Saintpaul infections in Minnesota implicated raw jalapeño peppers [6]. During the outbreak, 33 restaurant clusters were reported nationally; 31 served foods that contained jalapeño or serrano peppers [6].