Globalization and Foodborne Disease Outbreaks

Swati Kumar, MBBS; Margaret R. Hammerschlag, MD


The increasing year-round demand for fresh fruits and vegetables by Americans has partly been met by increasing importation of fresh produce. Advances in technology and transportation have allowed a phenomenal globalization of the food market, with the result that products grown in Mexico, Chile, and Brazil, among other countries, are now making their way to US markets within a matter of hours. Such imports, while allowing a perennial and abundant supply of a seasonal product, render the American consumer susceptible to outbreaks by opening the door to foodborne pathogens that may be present because of unregulated and unsafe food practices.

Traditionally, Americans traveling to developing countries were counseled on how to reduce the risk of traveler's diarrhea by selecting food with care. Yet during the winter, up to 70% of certain fresh fruits and vegetables in our food markets now come from developing countries. Thus, you need not travel to a developing country to contract an exotic foodborne disease; the pathogen may come to you.

Fresh fruits and vegetables are increasingly contributing to the American diet, a trend that has been paralleled by an increase in foodborne illnesses. The proportion of adults who consumed fruits and vegetables at least 5 times a day was 19%, 22%, and 23% in 1990, 1994, and 1996, respectively.[1] The average annual number of outbreaks associated with fresh produce, both domestic and imported, more than doubled between 1973-1987 and 1988-1991, from 4 per year to 10 per year.[2] Although more current data are unavailable, a recent salmonellosis outbreak associated with Brazilian mangoes and hepatitis A outbreaks associated with Mexican spring onions (scallions) point to a continuing trend.

Data on foodborne illnesses are incomplete because of underreporting of illnesses by medical professionals and failure to seek medical care by affected persons. It is frequently not possible to authoritatively link an outbreak to a particular source in the case of perishable fruits and vegetables because of lack of physical evidence at the time of the investigation, which often follows weeks to months after the outbreak. Detecting outbreaks associated with fresh produce is a particular challenge, given the wide geographic distribution of the produce, the diffusely scattered cases that are often unimpressive on a local scale, and the association with new and emerging food products that were not previously recognized as sources of outbreaks.

Until 1996, Cyclospora cayetanensis was regarded as a pathogen endemic in developing countries and an occasional agent of traveler's diarrhea. The first reported outbreak of cyclosporiasis in the United States occurred in 1990, affected 21 people, and was thought to have been caused by a breakdown in the water supply.

However, the parasite came into prominence only in 1996, when a large outbreak of cyclosporiasis occurred, affecting 1465 people in North America. This was also the first outbreak involving foodborne transmission, the implicated vehicle being Guatemalan raspberries.[3] Investigations could not determine the mode of contamination of the raspberries, but one hypothesis was that the raspberries got contaminated through spraying with pesticides diluted with contaminated water. Once contaminated, by whatever means, fresh raspberries may remain contaminated until eaten because they are too fragile and replete with crevices to be washed thoroughly. Since the first major outbreak of cyclosporiasis in 1996, several small-scale outbreaks have occurred in association with raspberries, basil, and mesclun lettuce.

C cayetanensis is a sporulating parasitic protozoan that infects the upper small intestine and causes a protracted, relapsing diarrheal illness in humans characterized by cycles of diarrhea associated with anorexia, malaise, nausea, and cramping with or without a low-grade fever. No known animal reservoirs exist. Complications include Guillain-Barré syndrome, reactive arthritis, and acalculous cholecystitis.

The oocysts of C cayetanensis are 8 to 10 µm in diameter and can be identified in stool specimens by the use of modified acid-fast, trichrome, and safranin stains; the examination of wet mounts with phase contrast microscopy; and the demonstration of autofluorescence. Evidence of sporulation of oocysts with the development of 2 internal sporocysts, each with 2 internal sporozoites, definitively establishes the diagnosis. These tests are not a part of routine testing for ova and parasites and thus should be specifically requested when cyclosporiasis is suspected. Trimethoprim-sulfamethoxazole is the drug of choice for treating patients with cyclosporiasis. For patients allergic to sulfa drugs, alternative choices include ciprofloxacin and trimethoprim alone.

In December 1999, an outbreak of infection with Salmonella enterica serotype Newport affected 78 persons dispersed over 13 states from coast to coast. Meticulous investigation revealed the source of this outbreak to be mangoes imported from a single farm in Brazil.[4]

The mangoes at this farm were being treated with hot water and then cooled. The hot water dip is a fruit fly control measure, mandatory for both domestic and foreign growers, that replaced ethylene dibromide fumigation, which was eliminated because of its carcinogenicity. However, if contaminated, the hot water itself can be a source of pathogens that are internalized by the fruit during sequential treatments with hot and cold water. When warm fruit is placed in cold water, gases within the fruit contract and an inward hydrostatic force can draw in pathogens to varying depths; the pathogens then may not be amenable to removal by any amount of washing, peeling, or scrubbing.

The most recent incident of foodborne illness associated with imported produce was an outbreak of hepatitis A, which affected 650 persons who dined at a Chi-Chi's restaurant in Monaca, Pa, in September and October 2003. Seventy-five of those affected were from 6 other states. Investigations traced the source of the virus to green onions grown on a farm in Mexico.[5] The genetic sequence of the outbreak strain was very similar to viral sequences obtained from persons involved in hepatitis A outbreaks in Tennessee, Georgia, and North Carolina during September 2003 that were also linked epidemiologically to green onions. These sequences also were identical or very similar to sequences observed among persons with hepatitis A living along the United States–Mexico border and travelers returning from Mexico, consistent with a source in Mexico.

Hepatitis A virus (HAV) is transmitted by the fecal-oral route. Fecal contamination of food that is not cooked or is inadequately cooked is a potential source of HAV. Green onions require extensive handling during harvesting and preparation for packing. Contamination could occur by contact with HAV-infected workers in the field during harvesting and preparation or by contact with HAV-contaminated water during irrigation, rinsing, processing, cooling, and icing of the product. Green onions and other select produce items (eg, strawberries) might be more vulnerable to contamination because plant surfaces are particularly complex or particularly adhered to by viral or fecal particles. The risk of acquiring hepatitis A can be reduced or eliminated by thorough cooking.

Globalization of the fresh produce market has led to a significant change in the outbreak scenario. Conventionally, foodborne outbreaks occurred on a local scale following a social gathering of some sort and were readily recognizable by the high attack rate. On the other hand, outbreaks secondary to widely distributed produce may come to attention only when there is a chance concentration of cases in one location or when the outbreak strain or organism is unusual.

This new outbreak scenario has important implications for physicians and local health departments. First, what appears to be a local outbreak may in fact be part of a concurrent or emerging national event. Second, the recognition of a national outbreak calls for further investigation of isolated cases at a local level in order to identify more cases for the follow-up epidemiologic investigations that are vital for identification of the source of the outbreak.

Modern surveillance methods that allow strain characterization using standardized molecular subtyping tools help link geographically scattered cases and thus play a critically important role in recognizing the outbreak. One such tool is PulseNet, the CDC's expanding nationwide network of laboratories that perform pulsed-field gel electrophoresis on foodborne bacteria and share information within the network to detect clusters of isolates with indistinguishable patterns. Information about PulseNet is available at

The economic impact of these outbreaks has made clear the need for improved food safety programs, with a special emphasis on the import industry. Although mandatory guidelines for food safety are lacking at this time, the FDA could impose them if deemed appropriate in the future. Timely recognition of outbreaks and epidemiologic investigations are critical in enabling us to identify new infectious agents, vehicles of transmission, and modes of contamination and to institute corrective measures for prevention of further outbreaks.