Perspective

Coming to Grips with Foodborne Infection — Peanut Butter, Peppers, and Nationwide Salmonella Outbreaks

Dennis G. Maki, M.D.

N Engl J Med 2009; 360:949-953March 5, 2009

Article

Two years ago, a nationwide outbreak of Shiga toxin–producing Escherichia coli O157:H7 enteritis linked to consumption of contaminated spinach from one California supplier captured the attention of the national media for weeks. It was at least the 26th reported U.S. outbreak of E. coli infection that had been traced to contaminated leafy green vegetables since 1993. Each year, approximately 110,000 persons acquire endemic toxigenic E. coli infection, and 50 of them die,1 despite greatly intensified efforts during the past decade on the part of our federal food-safety agencies — the U.S. Department of Agriculture (USDA), the Food and Drug Administration (FDA), and the Centers for Disease Control and Prevention (CDC) — to prevent the spread of such infections.

Now we are confronted by two large nationwide outbreaks of salmonella infection (see graphsSalmonella Infections in Two Nationwide Outbreaks in 2008–2009.). Between April and August 2008, Salmonella serotype Saintpaul enteritis was diagnosed in 1407 persons in 43 states, the District of Columbia, and Canada. Ultimately, 282 patients were hospitalized, and 2 elderly patients died.2 Initial epidemiologic investigations by state health departments and the CDC suggested that contamination of tomatoes grown in the southwestern United States was the cause, although this was never proved microbiologically. Predictably, tomato consumption plummeted, and the industry lost an estimated $200 million. After several months of investigation, the outbreak strain was isolated from jalapeño and serrano peppers that had been grown on one Mexican farm, and the CDC concluded that the outbreak derived from contamination of peppers that were eaten raw — probably in many cases with tomatoes, which might explain the misleading results from the initial case–control studies.

In a second outbreak, which began on September 1 and is ongoing, S. Typhimurium enteritis had been diagnosed in 600 persons in 44 states and Canada by February 8, 2009 (see mapCases of Infection with the Outbreak Strain of S. Typhimurium in the United States, September 1, 2008, through February 8, 2009. and imageClustered Gram-Negative Salmonella Typhimurium Bacteria.).3 The CDC quickly traced the outbreak to contamination of one Georgia producer's peanut butter and the processed foods of other manufacturers that contained the company's peanut butter or paste. More than half the cases have occurred in children, hundreds of patients have been hospitalized, and at least eight have died. Beyond a recall of all peanut products produced by the company since January 1, 2008, more than 400 food products (including cookies, crackers, cereal, candy, ice cream, and pet foods) have been recalled. Investigations have revealed that salmonella had been isolated from the implicated company's peanut butter or peanut paste in its internal quality-control sampling program on at least 12 occasions during the past year, but no action was taken to investigate the source of contamination, review sterilization procedures, or reclean the production machinery. The company is now under criminal investigation.

It has been estimated that in large salmonella outbreaks, for every case identified by clinical culture, there are approximately 38 additional undetected cases — meaning that these two outbreaks may each have affected more than 20,000 persons. And these are not rare outbreaks. In 2006 and 2007, peanut butter contaminated by S. Tennessee sickened tens of thousands of persons in 46 states, and there have been at least 12 other multistate salmonella outbreaks traced to contaminated tomatoes since 1990.

Once again, we must ask ourselves how foodborne disease can develop in 76 million residents of one of the world's most technically advanced countries each year, causing 350,000 hospitalizations and 5000 deaths and adding $7 billion to our health care costs, despite intensive regulation of food production and distribution.

Enormous shifts in food production during the past half century underlie the increased risk and complexity of foodborne disease caused by bacterial enteropathogens originating in food animals in North America.4 Today, virtually all food consumed domestically is grown and processed on a vast industrial scale or, increasingly, is imported: milk and complex dairy products, eggs and egg products, fresh vegetables and fruits, and the processed snacks and condiments incorporating these foodstuffs. Relatively little of the fresh food we eat is now grown or produced locally. Moreover, Americans like to eat out, and the risk of foodborne disease is considerably higher with food prepared in restaurants than with meals made at home.

Although U.S. farmers and companies that process and distribute our food have made considerable progress in reducing the risk of microbial contamination of their products, raw meats and poultry, raw milk, and most vegetables still commonly harbor microorganisms of food-animal origin that are often enteropathogens, such as campylobacter, salmonella, Shiga toxin–producing E. coli, and listeria. With centralized production and transcontinental distribution of commercially produced foods, unusually heavy contamination of a basic foodstuff or a failure to remove contaminants in a single production step can result in the shipment of contaminated food to millions of consumers, as these two recent salmonella outbreaks have illustrated.

To those who believe that the solution is a return to a pastoral, early-20th-century model with millions of small farms producing more “natural” food, I would point out that even if the millions of farm workers who would be required were available to produce food on a quasi-boutique scale, the costs would be enormous; it would be impossible to feed 300 million Americans, let alone the rest of the world. Efficient, industrialized production of huge quantities of food is an inescapable necessity to avoid food shortages and global famine. The challenge is to enhance the quality and safety of industrially produced food.

Meeting this challenge will mean building on the success of the USDA's Pathogen Reduction, Hazard Analysis, and Critical Control Point (HACCP) program, which was launched in 1996, the same year as FoodNet, a program of more intensive surveillance of foodborne infections in 10 states, and PulseNet, a system for pulsed-field gel electrophoresis DNA subtyping of enteric pathogens identified in U.S. clinical laboratories. The HACCP program needs to be scientifically validated and applied more consistently at all stages of food production — actions that might have prevented the current salmonella outbreak. A nationwide expansion of FoodNet could improve the surveillance of documented foodborne disease, but more timely, electronic central reporting (which as done now requires nearly 2 weeks) and expansion of our national program to an international scale are required to permit more effective investigation of disease clusters. PulseNet's pathogen subtyping should be accelerated, and the program should be integrated with similar efforts in other countries.

We need more effective programs for monitoring the production and processing of food (including imported food) and assessing its safety. Inspections of food producers and processors by state agencies, the FDA, and the USDA have been limited by insufficient personnel and inadequate budgetary support. Safer food will come only when the federal government commits the resources needed to achieve it. We also need to develop rapid and more sensitive molecular methods for detecting enteropathogens in food, both during processing and in random sampling of final products, and programs applying these technologies need to be developed and implemented for high-risk foods.

Requiring bar codes indicating the provenance of all commercial foods would permit immediate tracing of a food item to a specific farm, processing plant, or distribution center. Such a system could have greatly accelerated the resolution of the salmonella outbreak traced to Mexican peppers. Consumers have the right to know the origin of their food, which should be stated on the label of every fresh, perishable food item.

But there are further steps that I believe are necessary. We should vigorously pursue promising new approaches to the feeding of poultry, swine, and cattle that can reduce colonization by campylobacter, salmonella, and E. coli. This effort should include an international moratorium on the incorporation into animal feeds of growth-promoting antibiotics, which have been linked to greatly increased antimicrobial resistance in bacterial enteropathogens recovered from human infections and may weaken animals' resistance to colonization by enteropathogens. Similarly, we should aim to eliminate all unnecessary use of antimicrobial agents in both human and veterinary medicine.

Hygienic food-preparation practices in restaurants, hospitals, nursing homes, and private homes should be improved. We should greatly strengthen the capacities of local and regional health departments to monitor the food-handling practices of grocery stores, restaurants, and caterers, to pursue suspected problems more vigorously, and to more effectively integrate their activities with the national surveillance and control programs of the CDC, the FDA, and the USDA.

Finally, we already have the capacity to improve food safety by adopting a technology that can protect against safety breakdowns during production, preparation, or cooking: routine irradiation of the final commercial product in the case of poultry and hamburger, processed foods containing eggs or milk, and selected leafy and other vegetables eaten raw could greatly reduce the incidence of bacterial foodborne disease. Research has shown that irradiation kills pathogens or markedly reduces pathogen counts without impairing the nutritional value of food or making it toxic, carcinogenic, or radioactive.5 Food irradiation has been endorsed by the World Health Organization, the CDC, the FDA, the USDA, the American Medical Association, and the European Commission's Scientific Committee on Food and is already used in many other countries. In the United States, irradiation of fresh meat has been allowed since 1997; last August, the FDA approved the irradiation of iceberg lettuce and spinach. The CDC has estimated that irradiation of high-risk foods could prevent up to a million cases of bacterial foodborne disease each year in North America. I believe it is time to launch a major effort to gain public acceptance of irradiation of high-risk foods. It is time to stop reliving history.

No potential conflict of interest relevant to this article was reported.

This article (10.1056/NEJMp0806575) was published at NEJM.org on February 11, 2009.

Source Information

Dr. Maki is a professor of medicine at the University of Wisconsin School of Medicine and Public Health and a hospital epidemiologist at the University of Wisconsin Hospital and Clinics — both in Madison.

References

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