Outbreak of Salmonella Serotype Muenchen Infections Associated with Unpasteurized Orange Juice -- United States and Canada, June 1999

During June 1999, Public Health-Seattle and King County (PHSKC) and the Washington state health department and the Oregon Health Division independently investigated clusters of diarrheal illness attributed to Salmonella serotype Muenchen infections in each state. Both clusters were associated with a commercially distributed unpasteurized orange juice traced to a single processor, which distributes widely in the United States. As of July 13, 207 confirmed cases associated with this outbreak have been reported by 15 states and two Canadian provinces; an additional 91 cases of S. Muenchen infection reported since June 1 are under investigation. This report summarizes the two state-based investigations and presents preliminary information about the outbreak in the other states and Canada.

On June 19, state health officials were notified of three cases of Salmonella serogroup C2 infection, which were confirmed subsequently as S. Muenchen. Interviews of the ill persons revealed one common feature: drinking a fruit smoothie containing unpasteurized orange juice from different outlets of restaurant chain A. PHSKC and the Washington State Department of Health initiated an investigation. A case was defined as illness with onset after June 9, with isolation of S. Muenchen from stool or blood or isolation of Salmonella serogroup C2 with a pulsed-field gel electrophoresis (PFGE) or restriction fragment length polymorphism pattern that was indistinguishable from the outbreak strain.

In a case-control study by PHSKC of nine ill and 29 well restaurant A patrons, illness was significantly associated with drinking smoothies containing orange juice (100% of cases exposed compared with 14% of controls; odds ratio=undefined, pless than 0.001). By July 9, 85 persons with onset of illness during June 10-30 were identified in Washington. Sixty-seven patients reported either drinking unpasteurized orange juice produced by Sun Orchard* of Tempe, Arizona or eating at an establishment where the juice was served. Among 79 patients for whom information was available, the median age was 27 years (range: 9 months-95 years), and 51% were male. The predominant symptoms reported were diarrhea (94%), fever (75%), and bloody diarrhea (43%). Eight (10%) patients were hospitalized, and one man had a stroke coincident with his Salmonella infection. No patients died.

On June 23, the Washington County Department of Health received a report of a case of salmonellosis; the isolate was serotyped subsequently as S. Muenchen. An investigation by the Oregon Health Division identified four ill persons among a group of 13 that had eaten a brunch buffet in Portland. A case was defined as diarrhea (three or more loose stools within 24 hours) or vomiting in a person who attended the buffet. Illness was significantly associated with drinking unpasteurized orange juice produced by Sun Orchard (relative risk=undefined; pless than 0.001).

By July 12, 57 persons with S. Muenchen infection with onset of illness during June 14-29 were identified in Oregon. The median age was 36 years (range: 9 months-95 years), and 54% were female. Forty-four patients were known to have drank unpasteurized orange juice before illness onset. Among the 39 patients for whom information was available, the predominant symptoms were diarrhea (100%), fever (89%), abdominal cramps (85%), chills (82%), and bloody diarrhea (59%). Seven persons were hospitalized; no patients died.

On June 25, on the basis of the epidemiologic information from the investigations in Washington and Oregon and discussions with the Food and Drug Administration (FDA), Sun Orchard voluntarily issued a recall. Unpasteurized orange juice produced by Sun Orchard is distributed to Arizona, California, Colorado, Nevada, New Mexico, Oregon, Texas, Utah, Washington, Wisconsin, and the Canadian provinces of Alberta and British Columbia under the brand names Aloha, Earls and Joeys Tomato's, Markon, Sysco, Trader Joe's, Voila, and Zupan. Other states and provinces received these products through secondary distribution. The juice was distributed to hotels, restaurants, and supermarkets, and was served in individual glasses as "fresh-squeezed" juice in hotels and restaurants. In addition, a frozen form of the unpasteurized juice was sold under the brand name Vareva for use in restaurants and institutions.

On June 28, samples from a previously unopened container of unpasteurized Sun Orchard orange juice analyzed at an FDA laboratory and the Washington State Public Health Laboratory yielded S. Muenchen; samples from the smoothie blender and juice dispenser at an outlet of restaurant A analyzed by the Washington State Public Health Laboratory yielded Salmonella serogroup C2. Isolates from both sources had a PFGE pattern that was indistinguishable from strains isolated from patients. Subsequently, orange juice collected from the Sun Orchard factory, cultured in an FDA laboratory and serotyped by the California State Public Health Laboratory, yielded S. serotype Javiana, S. serotype Gaminara, S. serotype Hidalgo, and S. serotype Alamo in addition to S. Muenchen. Efforts are ongoing to determine the source of all orange juice components, whether they might have been used in other brands, and the source of the Salmonella contamination.

An outbreak-related case was defined as S. Muenchen infection after June 1 in a person who drank unpasteurized orange juice or whose isolate had a PFGE pattern with no more than one band difference from the Washington outbreak strain. In addition to the Washington and Oregon cases, 66 cases were reported in persons in 13 other states: Arizona (four), California (21), Connecticut (one), Florida (one), Illinois (one), Iowa (two), Massachusetts (seven), Michigan (three), Minnesota (six), New Mexico (10), Texas (five), Utah (four), and Wisconsin (one). Cases also were reported from the Canadian provinces of Alberta (four) and British Columbia (eight). Among the 66 patients for whom information was available, the median age was 32 years (range: 6 months-66 years), and 58% were female. Six persons were hospitalized. An additional 78 cases of S. Muenchen infection occurring after June 1 reported by nine other states and the two Canadian provinces are under investigation.

Reported by: J Boase, MSN, S Lipsky, MPH, P Simani, MPH, S Smith, C Skilton, MS, S Greenman, S Harrison, J Duchin, MD, Public Health-Seattle and King County; M Samadpour, PhD, Univ of Washington, Seattle; R Gautom, PhD, S Lankford, T Harris, K Ly, MD, D Green, J Kobyashi, MD, Washington State Dept of Health. E DeBess, DVM, T McGivern, S Mauvais, V Balan, MS, D Fleming, State Epidemiologist, Oregon Health Div, Oregon Dept of Human Resources; K Sanchez, Washington County Dept of Health, Hillsboro, Oregon. PD Vertz, Infectious Disease Epidemiology Section, Arizona Dept of Health Svcs. JC Mohle-Boetani, MD, Disease Investigations and Surveillance Br, Div of Communicable Disease Control, California Dept of Health Svcs. D Seuring, JoDaviess County Health Dept, Golena, Illinois. JH Goddard, Iowa Dept of Public Health. PE Kludt, MPH, Div of Epidemiology and Immunizations, Massachusetts Dept of Public Health. SA Bidol, MPH, Communicable Disease Div, Michigan Dept of Community Health. J Bender, DVM, Acute Disease Epidemiology Section, Minnesota Dept of Health. CM Sewell, DrPH, State Epidemiologist, Office of Epidemiology, IN Vold, MPH, New Mexico Dept of Health. L Marengo, MS, Infectious Disease Epidemiology and Surveillance Div, Texas Dept of Health. J Archer, MS, Communicable Diseases Section, Bur of Public Health, Wisconsin Div of Public Health. British Columbia Center for Disease Control, Alberta Health, Nova Scotia Dept of Health. Bur of Infectious Diseases Laboratory, Center for Disease Control, Health Canada. Center for Food Safety and Applied Nutrition and Office of Regional Operations, Food and Drug Administration. Foodborne and Diarrheal Diseases Br, Div of Bacterial and Mycotic Diseases, National Center for Infectious Diseases; and EIS officers, CDC.

Editorial Note:

S. Muenchen is one of approximately 2400 Salmonella serotypes that can cause illness in humans. Salmonella infection typically causes gastroenteritis characterized by diarrhea, abdominal cramps, fever, and dehydration. Bacteremia, meningitis, osteomyelitis, and abscesses also can occur. Each year in the United States, 800,000-4 million Salmonella infections result in approximately 500 deaths (1 ). S. Muenchen is an infrequently isolated serotype, accounting for approximately 1.6% of human Salmonella isolates reported in 1997 to the Public Health Laboratory Information System (2,3). Oregon typically reports less than 6 isolates per year and Washington less than 10 per year.

Juice has been implicated as the vehicle of transmission in at least 15 outbreaks in the United States in this century involving pathogens, including Escherichia coli O157:H7, Cryptosporidium parvum, and other Salmonella serotypes (e.g., S. Typhi and S. Hartford) (4). In an outbreak of E. coli O157:H7 infections attributed to unpasteurized apple juice, one child died, and 14 children developed hemolytic uremic syndrome (5). The outbreak described in this report is the second and largest Salmonella outbreak associated with unpasteurized orange juice (6). The acidic nature of orange juice (pH of 3.4-4.0) previously was believed to inhibit bacterial growth and protect against foodborne illness; however, recent outbreaks and laboratory investigations have demonstrated otherwise. Salmonella serotypes Gaminara, Hartford, Rubislaw, and Typhimurium have survived in orange juice for up to 27 days at pH 3.5 and 60 days at pH 4.1 (7).

In 1998, FDA proposed Hazard Analysis and Critical Control Point (HACCP) and labeling regulations to improve the safety of juice products (8). The proposed HACCP regulation requires juice to be produced using methods such as pasteurization or an equivalent process to ensure that pathogenic microorganisms are destroyed. In the outbreak described in this report, the implicated company had a HACCP plan. Investigations are under way to determine where these control measures failed and how the juice became contaminated. FDA published a final rule for the labeling of fruit and vegetable juices that includes a warning statement to advise consumers of the risks associated with drinking unprocessed juices (9). However, the labeling requirements do not apply to juice or products containing juice that are not packaged (i.e., sold by the glass) in retail establishments, such as the product implicated in this outbreak. In Washington, some consumers were unaware that they were drinking unpasteurized commercial orange juice in their fruit smoothies.

Because the source of contamination of the orange juice is unknown and to facilitate outbreak investigation, local and state health departments are encouraged to investigate all cases of S. Muenchen infections occurring since June 1 using a questionnaire from CDC's Foodborne and Diarrheal Diseases Branch, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, telephone (404) 639-2206, and to consider referring isolates for PFGE with the standardized PulseNet Salmonella protocol by the Washington State Public Health Laboratory or by another PulseNet laboratory. Health departments also should consider investigating cases of S. Alamo, S. Gaminara, S. Hidalgo, and S. Javiana in which illness onset occurred after June 1.

References

1. Tauxe RV. Salmonella: a postmodern pathogen. Journal of Food Protection 1991;54:563-8.
2. Martin SM, Bean NH. Data management issues for emerging diseases and new tools for managing surveillance and laboratory data. Emerging Infectious Diseases 1995;1:124-8.
3. CDC. Salmonella surveillance: annual tabulation summary, 1997. Atlanta, Georgia: US Department of Health and Human Services, CDC, 1998.
4. Parish ME. Public health and nonpasteurized fruit juices. Crit Rev Microbiol 1997;23:109-19.
5. Cody SH, Glynn MK, Farrar JA, et al. An outbreak of Escherichia coli O157:H7 infection from unpasteurized commercial apple juice. Ann Intern Med 1999;130:202-9.
6. Cook KA, Dobbs TE, Hlady WG, et al. Outbreak of Salmonella serotype Hartford infections associated with unpasteurized orange juice. JAMA 1998;280:1504-9.
7. Parish ME, Narciso, JA, Friedrich LM. Survival of Salmonella in orange juice. Journal of Food Safety 1997;17:273-81.
8. Food and Drug Administration. Hazard Analysis and Critical Control Point (HACCP); procedures for the safe and sanitary processing and importing of juice; food labeling; warning notice statements; labeling of juice products; proposed rules. Federal Register 1998;63:20449-86.
9. Food and Drug Administration. Food labeling: warning and notice statement; labeling of juice products. Federal Register 1998;63:37030-56.

* Use of trade names and commercial sources is for identification only and does not imply endorsement by CDC or the U.S. Department of Health and Human Services.

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