This nationwide outbreak of S. Montevideo infections was associated with RTE salami products made with contaminated black and red pepper added after the critical control point for pathogen reduction. This outbreak highlights the importance of preventing raw ingredient contamination and the potential for spices, such as pepper, contaminating RTE products. This outbreak also reveals the importance of manufacturer verification of the safety of ingredients used in RTE foods after the critical control point for pathogen reduction. The implicated pepper had reportedly been treated and tested by suppliers prior to use. However, high standard plate counts and Salmonella were identified from intact containers of treated and untreated pepper. The starting bacterial load for some of these products was extremely high indicating that treatment was insufficient.
Use of membership card information provided critical clues to identify the source in this investigation. State and federal regulatory partners identified production lots of black pepper and red pepper used to produce the contaminated salami products using purchase information gathered from these cards. Membership cards can provide significant information to identify contaminated foods quickly and help verify potential exposures in patients. This technique has been effective in providing additional epidemiological evidence in other outbreak investigations [14
After the source of the outbreak was identified and the case-patients from the wedding and hunting group subclusters were re-interviewed, state and local health departments were able to confirm from shopper card information that the wedding in Arizona was catered with company A Italian-style meats and members of the hunting group reported purchasing an Italian-style delicatessen meat tray. When available, membership card information should be considered for use in future foodborne disease outbreak investigations. Twelve spice-associated Salmonella
outbreaks have been reported in nine countries between 1973 and 2009 with 1783 illnesses, at least 124 hospitalizations, and one death [18
]. European countries reported several Salmonella
outbreaks associated with salami and other fermented sausage products [19
]. However, these outbreaks resulted from insufficient curing time, low water activity, and high pH of the salami, allowing Salmonella
to survive [19
]. The source of this outbreak was contaminated pepper coated on salami products after the lethality step. Although spices are sometimes known to harbour various moulds, fungi, and bacteria, relatively few reports have documented spices as the cause of human illness. This may be because of the difficulty of identifying a source of an ingredient-driven outbreak.
A variety of effective methods exist to decontaminate spices including steam, ethylene oxide, propylene oxide treatments, and irradiation. However, companies are not currently required to treat spices and manufacturers are not required to use treated spices in their products. These treatment methods have increased in importance given the frequent use of spices in RTE foods and the potential for contaminated spices to cause widespread outbreaks. Manufacturer validation of the effectiveness of these treatments along with appropriate post-treatment sampling to verify the process is also critical. The FDA does not have any regulations on aerobic plate counts for spices. Any finding of Salmonella
is a violation of the Federal Food, Drug and Cosmetic Act [24
We detected this outbreak through routine serotype-based surveillance enhanced by PFGE reported to PulseNet. A case-control study identified an exposure significantly associated with illness, but the investigation using warehouse store membership cards revealed specific product and manufacturer information. Many of the case-patients could not remember the exact brand of salami that they had eaten or purchased and the membership card information was critical in identifying this information during the investigation. Information from membership cards should be used in future foodborne outbreak investigations to help identify suspect food items. There are limitations to the use of membership cards. Case-patients may refuse permission to use their information. Each member of the household may have a different membership card number making it difficult to receive all of the purchase records. The cards also may not always reflect the entire consumption of cases. For example, case-patients may purchase foods from different stores that do not have membership cards, many food products are consumed outside the household and not recorded on a card, and the central database of a store does not always contain data on all foods sold such as foods purchased from a salad bar [15
There was a limitation in the case-control study. Cases were interviewed about food exposures before illness onset and controls were asked about the period prior to interview. Without illness to clearly delineate a time period, controls might have more difficulty recalling the timing of exposures. However, when compared to the FoodNet Population Survey Atlas of Exposures, there was not a difference in the amount of salami or prepackaged delicatessen meats by month reported by healthy people [25
As a result of this investigation, the FDA has increased sampling and surveillance of imported pepper spices and continued previously initiated discussions with the American Spice Trade Association regarding preventive controls to safeguard against contaminated spices entering commerce. Manufacturers should implement supplier verification and preventive control programmes in an effort to eliminate contamination of their products.
This investigation demonstrates the challenges of ingredient-driven outbreaks. Foodborne disease outbreak investigations should seek to identify a root cause to help prevent future outbreaks. Without ingredient testing and a root cause investigation in this investigation, a recall would not have occurred, the plant would have gone back into production using contaminated pepper, and illnesses could have continued.