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Escherichia coli O157:H7 Infections Associated with Ground Beef from a U.S. Military Installation --- Okinawa, Japan, February 2004

In February 2004, the Okinawa Prefectural Chubu Health Center (OCHC) and the Okinawa Prefectural Institute of Health and Environment (OIHE), Japan, investigated three cases of Escherichia coli O157:H7 infection in a Japanese family associated with eating ground beef. Public health officials from multiple agencies in Japan and the United States collaborated on this investigation, which resulted in a voluntary recall of approximately 90,000 pounds of frozen ground beef in the United States and at U.S. military bases in the Far East. This was the first reported instance in which Japanese public health officials identified contaminated, commercially distributed ground beef that was produced in the United States. This report summarizes epidemiologic and laboratory investigations conducted by OCHC and OIHE. The results underscore the importance of using standardized molecular subtyping methods throughout the world to facilitate international public health communication and intervention.

Cases were ascertained through surveillance for laboratory-confirmed E. coli O157:H7 infection. Laboratory investigation of implicated food items was conducted using methods recommended by the Japanese Ministry of Health, including culture of food samples, immunomagnetic separation, and polymerase chain reaction to characterize isolates. Pulsed-field gel electrophoresis (PFGE) of the genomic DNA fragments of E. coli O157:H7 isolates was performed after restriction with XbaI enzyme in accordance with the PulseNet protocol by the National Institute of Infectious Diseases, Japan. PFGE patterns were analyzed and transmitted electronically to PulseNet USA* at CDC for comparison with U.S. isolates.

On February 17, 2004, OCHC was notified of laboratory-confirmed E. coli O157:H7 infection in a hospitalized child in Okinawa. The child had been hospitalized with bloody diarrhea and, 6 days previous, had other symptoms, including abdominal pain and fever. Interviews with the child's family revealed that a sibling appeared to have some of the same symptoms. Family members were also questioned about food history; all family members had eaten hamburgers on February 6. In addition to the hospitalized child, E. coli O157:H7 was isolated from the symptomatic sibling and one asymptomatic family member.

The frozen ground beef patties eaten by the family were purchased from a U.S. military commissary in Okinawa. OCHC obtained the remaining frozen ground beef patties from the family and sent a sample to OIHE for laboratory evaluation; E. coli O157:H7 was isolated from the ground beef patties. Epidemiologic and laboratory findings were reported by the Okinawa Prefecture to the U.S. Naval Hospital in Okinawa. To exclude the possibility that the patties were contaminated after opening, the U.S. Naval Hospital obtained unopened frozen ground beef patties with the same lot number from the base commissary for microbiologic analysis; E. coli O157:H7 was isolated from these previously unopened ground beef patties. Isolates from the unopened package, leftover ground beef patties, and the three human isolates had indistinguishable PFGE patterns. The pattern had not been previously observed in Japan or in the PulseNet USA database.

Results of the investigations indicated that the source of infections was contaminated ground beef patties obtained from the U.S. military base in Okinawa. Traceback of the lot number indicated that the frozen patties were produced on August 11, 2003, by a U.S. company. Fresh and frozen ground beef products produced on that day were distributed to U.S. military installations in the Far East and to institutional and retail outlets in California, Idaho, Oregon, and Washington.

As a result of this investigation, the Food Safety Inspection Service of the U.S. Department of Agriculture announced a voluntary recall by the company of approximately 90,000 pounds of frozen ground beef and other ground beef products (1). Identification of the contaminated lot and the subsequent recall likely prevented additional infections.

Reported by: J Kudaka, R Asato, K Itokazu, M Nakamura, DVM, K Taira, DVM, Okinawa Prefectural Institute of Health and Environment; H Kuniyosi, MD, Y Kinjo, Okinawa Prefectural Chubu Health Center, Okinawa; J Terajima, DVM, H Watanabe, MD, J Kobayashi, MD, Field Epidemiology Training Program, National Institute of Infectious Diseases, Tokyo, Japan. B Swaminathan, PhD, CR Braden, MD, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases; JR Dunn, DVM, EIS Officer, CDC.

Editorial Note:

E. coli O157:H7 infection is a major cause of foodborne illness in many countries, including the United States and Japan (2). In 1996, Japanese public health officials investigated the largest outbreak of E. coli O157:H7 infection, which was associated with consumption of radish sprouts, with approximately 6,000 persons becoming ill (3). The outbreak described in this report demonstrates the need to eliminate E. coli O157:H7 contamination of ground beef and the need for consumers to follow guidelines for safe food preparation (4). Moreover, this outbreak demonstrates the potential for multinational foodborne outbreaks and the benefits of international public health communication and use of standardized methods of molecular subtyping for detection and prevention of foodborne diseases.

During the weeks after this investigation, three additional E. coli O157:H7 infections were identified as potentially associated with this outbreak, one in Japan and two in the United States. On February 27, a child aged 11 years of a U.S. military family in Okinawa was hospitalized with E. coli O157:H7 infection; the PFGE pattern was indistinguishable from that of the three infected persons described in this report. The family had purchased the same brand of frozen ground beef patties from the U.S. military commissary in Okinawa. The hamburgers were prepared and eaten on February 22, 2 days before the recall notice. Although the company name was the same, the lot number could not be confirmed because the family discarded the package after learning of the recall.

In the United States, two clinical E. coli O157:H7 isolates with the outbreak PFGE pattern were identified in a woman aged 40 years and a child aged 10 years in Orange County, California; both patients were hospitalized. Both patients had eaten beef during the week preceding their illness. Specimen collection dates were August 26, 2003, and September 8, 2003. No association with the recalled product was made, although the PFGE pattern was unique to California, and the cases were temporally related with respect to distribution of the recalled products to institutional and retail establishments in California. The 6-month lag between production in the United States and sale in Japan, with intervening cases in the United States, demonstrates the long life of products such as frozen ground meat and the prolonged survival of foodborne pathogens in frozen foods. This investigation also highlights the ability of PulseNet USA to identify small clusters of indistinguishable isolates and the potential for prevention, particularly if epidemiologic links can be made between ill persons and food items in a timely and coordinated manner.

The use of standardized protocols for molecular subtyping during international outbreaks of foodborne disease and the ability to communicate with international public health authorities have been important in previous outbreaks (5,6). The development of PulseNet USA has had an important impact on the investigation of foodborne outbreaks and public health in the United States. PFGE was used to characterize food and clinical isolates after a large outbreak of E. coli O157:H7 infections in 1993 (7). Subsequently, CDC standardized PFGE protocols, disseminated them to state and local public health partners, and began building the PulseNet USA network (8).

Use of the PulseNet USA protocols during the public health investigation by Japan led to an international recall of contaminated ground beef and enabled international comparison of isolates facilitating detection of presumptively associated E. coli O157:H7 infections in the United States. In collaboration with many partners, CDC has facilitated establishment of PulseNet International, which has launched networks in several regions of the world (9). The continued development of PulseNet International will enhance international collaboration in the investigation of foodborne diseases and outbreaks.

Acknowledgments

The findings in this report are based, in part, on contributions from M Irei, MD, Okinawa Prefectural Chubu Health Center; M Iwanaga, MD, Dept of Microbiology, Graduate School of Medicine, Univ of the Ryukyus; D Baker, M Sekine, U.S. Naval Hospital, Okinawa; Japan District Veterinary Office, Camp Zama, Japan. Food Safety Inspection Svc, U.S. Dept of Agriculture.

References

  1. US Department of Agriculture, Food Safety Inspection Service. California firm recalls ground beef products for possible E. coli O157:H7. Available at http://www.fsis.usda.gov/frame/frameredirect.asp?main=http://www.fsis.usda.gov/oa/recalls/prelease/pr007-2004.htm.
  2. O'Brien AD, Kaper JB. Escherichia coli O157:H7 and other Shiga toxin-producing E. coli strains. Washington, DC: ASM Press; 1998.
  3. Michino H, Araki K, Minami S, et al. Massive outbreak of Escherichia coli O157:H7 infection in schoolchildren in Sakai City, Japan, associated with consumption of white radish sprouts. Am J Epidemiol 1999;150:787--96.
  4. US Department of Agriculture, Food Safety Inspection Service. FSIS issues alert on the importance of cooking and handling ground beef. Available at http://www.fsis.usda.gov/oa/news/2004/alert012904.htm.
  5. Lindsay EA, Lawson AJ, Walker RA, et al. Role of electronic data exchange in an international outbreak caused by Salmonella enterica serotype Typhimurium DT204b. Emerg Infect Dis 2002;8:732--4.
  6. Mahon BE, Ponka A, Hall WN, et al. An international outbreak of Salmonella infections caused by alfalfa sprouts grown from contaminated seeds. J Infect Dis 1997;175:876--82.
  7. Barrett TJ, Lior H, Green JH, et al. Laboratory investigation of a multi-state food-borne outbreak of Escherichia coli O157:H7 by using pulsed-field gel electrophoresis and phage typing. J Clin Microbiol 1994;32:3013--7.
  8. Swaminathan B, Barrett TJ, Hunter SB, Tauxe RV, CDC PulseNet Task Force. PulseNet: the molecular subtyping network for foodborne bacterial disease surveillance, United States. Emerg Infect Dis 2001;7:382--9.
  9. CDC. PulseNet International. Available at http://www.cdc.gov/pulsenet/pulsenet_international.htm.

* The national molecular subtyping network for foodborne surveillance, available at http://www.cdc.gov/pulsenet.

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