We conclude that an inherently contaminated alfalfa sprout seed lot was distributed to 33 sprouters in 10 states and resulted in at least 157 Salmonella
serovar Muenchen outbreak-related illnesses in 7 states. The likely range in number of cases associated with this outbreak was probably 3,500 to 16,200 based on rates of underreporting defined in other Salmonella
). Evidence for a contaminated seed lot as opposed to individual sprouter-associated contamination is supported by temporal and geographic clustering of cases associated with multiple sprouting facilities in multiple states receiving the implicated lot and by indistinguishable PFGE patterns of Salmonella
serovar Muenchen among human isolates from residents of seven states, product isolates from retail sprout packages traced back to lot COA98, and isolates from the irrigation water of the implicated seed lot during sprouting. Distribution of a contaminated seed lot to multiple growers geographically corresponding to the distribution of cases in a nationwide outbreak has been reported (13
Previously reported sprout-related outbreaks did not provide conclusive documentation that the sprouters had consistently followed recommended presprouting disinfection methods. This is the first reported outbreak with specific documentation (signed FDA affidavit) that an outbreak occurred despite sprout growers (in Wisconsin) having soaked alfalfa seed in 20,000-ppm chlorine solution for 15 min prior to sprouting. It reinforces the fact that currently recommended disinfection methods alone will not prevent continuing sprout outbreaks and reinforces the need for testing of irrigation water as described in the guideline.
Growing, harvesting, processing, mixing, and shipping of seed, followed by sprouting and distribution of finished product provide multiple points where pathogens can be introduced or amplified before reaching the consumer. Viable pathogens can persist not only on the surface but also in the inner tissue and stomata of cotyledons of sprouts experimentally contaminated with bacteria (11
). Low numbers of culturable Salmonella
may not be detected in seed even with methods that provide the greatest potential for detection and recovery (10
). While several chemical treatments can reduce Salmonella
populations up to 3.2 log10
CFU/g on alfalfa seeds, as analyzed by direct plating, no chemical treatment will eliminate the pathogen, as evidenced by detection in enrichment samples (21
). Treatment of seeds with a concentration of calcium hypochlorite as high as 2% does not prevent outgrowth of Salmonella
from naturally contaminated seeds (18
). Once present, high humidity and temperatures in the 21 to 25°C range favor amplification of bacteria in or on the seed during germination and sprouting (19
). Previous sprout-related outbreaks have established that pathogens can exceed 107
CFU per g of sprouts without adversely affecting the appearance of sprouts and that treating seeds and sprouts with chlorinated water or other disinfectants fails to eliminate pathogens (3
). Testing for pathogens following sprouting of seed has been suggested.
An FDA guidance document to improve the safety of raw sprouts was published in the Federal Register on 27 October 1999 (7
). In addition to good agricultural practices, the document also recommends that seed disinfection treatments be combined with microbial testing of spent irrigation water from each batch of sprouts for both Salmonella
and E. coli
O157:H7. Because testing for pathogens can be done at 48 h into what is generally a 3- to 10-day growing period, producers can obtain results before shipping the product without losing product shelf life and before sprouts enter the food supply.
Until routine testing of spent irrigation water from each batch of sprouts is universally implemented, sprouts, when served raw, remain a potential public health risk, especially to those with a compromised immune system. The only effective way to eliminate risk of food-borne illness from raw sprouts is to avoid eating them. In particular, persons at high risk for severe complications of infection with Salmonella
and E. coli
O157:H7, such as the elderly, children, and those with compromised immune systems, have been cautioned not to eat raw sprouts (19
A disturbing finding of this investigation is that people may not be aware that they are consuming sprouts in their food. Even if individuals are trying to reduce their risk by avoiding consumption of sprouts, foods may be served with sprouts without the knowledge of the consumer. Only 48% (30 of 62) of Wisconsin's laboratory-confirmed outbreak-related case patients knowingly chose to eat sprouts during the week before illness. Among the other 32 Wisconsin outbreak case patients, who did not knowingly consume sprouts in the week before illness onset, 38% (12 of 32) would not have eaten sprouts if given the choice. While it is possible that cross contamination of other foods with Salmonella-infected sprouts or poor hygienic practices at some restaurants may have been responsible for exposure of individuals who had no recall of sprout consumption, it is also possible that many of these individuals may have unknowingly eaten contaminated sprouts in sandwiches or in salads that they ordered. Restaurants and sandwich shops that routinely include sprouts in salads and sandwiches should ensure that sprouts are prominently listed as components of that food item or allow the customer to specifically choose this ingredient if they order that food item. Because individuals must make informed decisions about food choices, given what we know about the potential public health risk of consuming raw sprouts, food establishments have a shared responsibility to inform consumers that a food item contains sprouts.
A press release warning Wisconsin residents not to sell, serve, or eat sprouts until the specific sprout type associated with the outbreak was identified had a significant impact in preventing additional Wisconsin cases. At the time of the press release, the complex traceback had just begun and alfalfa sprouts from contaminated seeds had not yet been pulled from the shelves and were still available in retail establishments. The traceback investigation took about 1 month to complete and resulted in 32,900 lb of remaining alfalfa seed lot COA98 being recalled nationwide. Outbreak traceback investigations are labor-intensive and need to be timely to have an impact on reducing disease morbidity. However, once a specific seed lot is identified as contaminated and recalled, the risk of other outbreaks is not necessarily eliminated. Because seed lots routinely consist of a mixture of seeds from many seed-supplying farms, traceback and testing of “library” samples of all individual components of an implicated seed lot are essential if the individual farm contributing contaminated seeds is to be identified and appropriate measures taken to eliminate or minimize risk of contamination of future seed lots.