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The Produce Contamination Problem: Causes and Solutions
Academic PressCopyright © 2009 Elsevier Inc.
All right reserved.
Chapter OneScope of the Produce Contamination Problem
Gerald M. Sapers, Ph.D. (Emeritus) Eastern Regional Research Center, Agricultural Research Service, US Department of Agriculture, Wyndmoor, PA
Michael P. Doyle, Ph.D. Regents Professor and Director, Center for Food Safety, University of Georgia, Griffin, GA
Introduction 3 Produce-Associated Outbreaks—a New Problem? 3 Consequences of Produce-Associated Outbreaks 4 Key Aspects of the Produce Contamination Problem 5 Characteristics of Produce-Associated Outbreaks 5 Prevalence of Produce Contamination with Human Pathogens 7 Microbial Attachment and Survival on Produce Surfaces 8 Potential Sources of Produce Contamination 9 Preharvest Sources 9 Contamination During Packing 10 Contamination During Fresh-Cut Processing 11 Gaps in Our Understanding of Produce Contamination 12 Current State of Knowledge 12 What We Don't Know 12 Developing Effective Interventions 13
Produce-Associated Outbreaks—a New Problem?
For decades, concerns regarding the microbiological safety of foods have focused largely on animal products that were responsible for outbreaks of E. coli O157:H7 from ground beef; salmonellosis from poultry, eggs, and dairy products; and listeriosis from soft cheeses and processed meats. Outbreaks of botulism were associated with canned vegetables, but fresh fruits and vegetables generally were considered to be safe, except in countries where the combination of endemic gastrointestinal diseases, unsafe agricultural practices, and poor sanitation resulted in traveler's diarrhea and other illnesses acquired by consumption of locally grown fresh produce. US produce packers and the fresh-cut industry have long believed that their products were made safe by the use of a triple-wash technology using chlorinated water or other approved sanitizing agents.
In recent years, however, this picture has changed dramatically due to an increase in the number of outbreaks of foodborne illnesses associated with fresh and fresh-cut fruits and vegetables. Many large outbreaks involving widely consumed commodities such as apple cider, cantaloupe, raspberries, bagged lettuce and spinach, tomatoes, green onions, and sprouts have been reported during the past decade (Brackett, 1999; Beuchat, 2002). This increase may be due in part to greater consumption of fresh produce in response to the recommendations of health and nutrition professionals. Increased consumption has translated into increased production and distribution of fresh produce, but the growth of produce packing and fresh-cut processing facilities with regional or national distribution capabilities has exposed more consumers to products that may have been contaminated on a single processing line or at a single farm. Additionally, to meet increased demand for out-of-season items, sourcing of fresh produce became a global endeavor, including growing locations where the potential of human pathogen contamination of fruits and vegetables is high. Furthermore, with better methods for identifying and tracking foodborne outbreaks, the local and state health departments and CDC have become in the past decade much better at detecting produce-associated outbreaks, many of which previously would not have been recognized, or the source not identified.
Consequences of Produce-Associated Outbreaks
Pathogen contamination of fresh produce has important public health consequences. Not only are there more cases of illness from produce-associated outbreaks, highly vulnerable population groups—the very young, the old, and the immunocompromised—are often affected. For these individuals, the severity of foodborne illnesses can be much greater, if not life-threatening, and there may be serious long-term consequences to health. An indirect health-related consequence is the reduced intake of beneficial nutrients from fruits and vegetables by individuals concerned about acquiring a foodborne illness.
The economic consequences of produce-associated outbreaks are substantial, including the medical costs and lost income of patients, the costs of damage control (disposal of unmarketable products, cost of product recalls, cleanups, and retrofitting) for the affected produce packer/processor, and lost production time. In addition, there are the costs associated with litigation, awards from successful lawsuits, and long-term damage to the company's reputation, reflected by reduced sales of fresh produce items. A history of outbreaks can be damaging to an entire segment of the produce industry (e.g., spinach, green onions, and tomatoes) or to a production area (e.g., the Salinas Valley of California), resulting in increased costs for government-mandated changes in production and processing practices and in reduced sales of products nationwide. The estimated cost to tomato growers from the 2008 multistate Salmonella Saintpaul outbreak (over 1400 cases reported) was approximately $200 million (Anon., 2008). This outbreak was originally attributed to contaminated tomatoes, but subsequent investigation implicated jalapeño peppers as the major vehicle, serrano peppers also as a vehicle, and tomatoes possibly as a vehicle (CDC, 2008a). The overall economic cost to the industry could be a generalized reduction in sales and consumption of fresh produce resulting from reduced confidence in their safety.
KEY ASPECTS OF THE PRODUCE CONTAMINATION PROBLEM
Characteristics of Produce-Associated Outbreaks
Data compiled by the Centers for Disease Control and Prevention (CDC) provides insight into trends in the prevalence, size, and causes of produce-related outbreaks. Between 1993 and 1997, the prevalence of outbreaks associated with fresh fruits and vegetables, as reported by the CDC in summary tables for each year (CDC, 2000), was erratic with no upward trend (Table 1.1). However, there was an abrupt increase in the prevalence of produce-associated outbreaks between 1998 and 2002, perhaps in part because of a change in surveillance and/or reporting methodology (CDC, 2006).
The number of outbreaks associated with specific human pathogens during 2003–2006 is shown in Table 1.2. E. coli O157:H7, Salmonella, and norovirus were responsible for most outbreaks; however, the number of outbreaks and cases for each agent varied from year to year, and each year, large single outbreaks were associated with other pathogens (hepatitis A in 2003, Cryptosporidium in 2004, and Cyclospora in 2005). Interestingly, no produce-associated outbreaks were attributed to Listeria monocytogenes during this period or in 2000–2002 (CDC, 2008b).
CDC data reported for 1998–2002 reveal that the incidence of outbreaks is greater for vegetables than for fruits (CDC, 2006). An in-depth examination of outbreak data for 2003–2006 (Table 1.3) reveals that the principal problem commodities were green salads and lettuce, other leafy vegetables or herbs, sprouts, tomatoes, melons, and fruit salad. Many of these commodities are vulnerable to contamination because they grow on or close to soil where contamination can occur. The number of cases and their distribution among commodities varies from year to year. In recent years, major produce-related outbreaks have been caused by Salmonella contamination of tomatoes (FDA, 2004, 2006a) and orange juice (FDA, 2005a), E. coli O157:H7 contamination of fresh-cut lettuce (FDA, 2006b, 2007) and bagged spinach (FDA, 2006c), Cyclospora contamination of basil (FDA, 2005b), and hepatitis A contamination of green scallions from Mexico (FDA, 2003b). Several of the outbreaks associated with leafy greens were traced to farms in the Central Valley and Salinas Valley regions of California.
Prevalence of Produce Contamination with Human Pathogens
The sporadic nature of produce-related outbreaks is suggestive of localized contamination events, which makes systematic study of contamination sources difficult. One approach to assessing the magnitude of the problem is to obtain data on the prevalence of produce contamination for different commodities and growing locations. Both the FDA and USDA have conducted large-scale studies of selected commodities to determine the prevalence of contamination. The FDA's testing of imported produce (FDA, 2001b) revealed a relatively high prevalence of Salmonella and Shigella contamination on culantro (50%), cilantro (9%), cantaloupe (7.3%), celery (3.6), parsley (2.4%), lettuce (1.7%), and scallions (1.7%), all of which are grown on or close to soil. Testing of domestic produce (FDA, 2003a) revealed a lower prevalence of contamination (total 1.1%) than was found with imported produce (total 4.4%). Domestically grown scallions (3.2%) and cantaloupe (3.1%) had the highest prevalence of contamination, whereas the contamination of cilantro, parsley, and lettuce was each about 1%.
A USDA survey of selected produce commodities sampled at wholesale and distribution centers (USDA, 2004) revealed a much lower prevalence of contamination. Salmonella spp. were detected only on lettuce (0.14%), and E. coli with a virulence factor was detected on Romaine lettuce (1.34%), leaf lettuce (1.25%), and on cantaloupe, celery, and tomatoes at prevalences less than 0.2%.
Other studies of fresh and fresh-cut produce, grown either organically or conventionally, revealed a very low or no prevalence of human pathogen contamination (Riordan et al., 2001; Sagoo et al., 2001; Anon., 2002; Phillips and Harrison, 2005; Johnston et al., 2006; Mukherjee, 2006; Dallaire et al., 2006; Danyluk et al., 2007; Bobe et al., 2007). However, Heisick et al. (1989) reported a high prevalence of L. monocytogenes contamination (26–30%) on potatoes and radishes at retail. Castillo et al. (2006) reported high prevalences of Salmonella (14–20%) and Shigella (6–17%) in freshly squeezed orange juice and on fresh oranges collected at public street markets and street booths in Guadalajara, Mexico.
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