An Outbreak of Escherichia Coli O157:H7 Infection Linked to Unpasteurized Apple Cider in Oklahoma, 1999 Mamadou O

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An Outbreak of Escherichia coli O157:H7 Infection Linked to Unpasteurized Apple Cider in Oklahoma, 1999 Mamadou O. Diallo1*, Kristy K. Bradley2, James M. Crutcher3, Mike Lytle4, Anthony Lee2 and Ronald L. Moolenaar5 1Epidemic Intelligence Service, Centers for Disease Control and Prevention, Atlanta, GA 30333, USA; 2Communi- cable Disease Division, Oklahoma State Dept. of Health, Oklahoma City, OK 73117, USA; 3State Epidemiologist, Oklahoma State Dept. of Health, Oklahoma City, OK 73117, USA; 4Public Health Laboratory, Oklahoma State Dept. of Health, Oklahoma City, OK 73117, USA; 5Epidemiology Program Office, Center for Disease Control and Prevention, Atlanta, GA 30333, USA

INTRODUCTION ABSTRACT In 1982, Riley et al. (22) investi- During the fall of 1999, an outbreak with 16 cases (11 gated two outbreaks of an unusual gastrointestinal illness that affected 47 or confirmed and five probable) of Escherichia coli O157:H7 more persons. They determined that infections was identified in Oklahoma. Nine persons (82%) the outbreak was caused by a rare E. coli experienced bloody diarrhea, six (54%) required hospitalization, serotype, O157:H7, apparently trans- and three (27%) developed hemolytic uremic syndrome (HUS). mitted by undercooked meat. During Twelve of the sixteen (75%) cases were children from 2 to the following decades, multiple E. coli O157:H7 outbreaks were associated with 13 years old. All nine available E. coli O157:H7 isolates had an consumption of raw or undercooked identical pulsed-field gel electrophoresis pattern. Ten of the 11 ground meat, meat products, and unpas- confirmed patients and none of the 24 control subjects had teurized milk (2, 3, 15, 16, 17). After the drunk unpasteurized apple cider from Orchard A (matched 1990s, an increased number of reported odds ratio undefined;P < 0.00001). All environmental specimen outbreaks were associated with fresh veg- etables (e.g., lettuce, spinach, sprouts) or cultures were negative. Orchard A was in compliance with unpasteurized apple juice (1, 4, 5, 6, 8, U.S. Food and Drug Administration requirements for product 11, 12, 13, 19, 24). warning labels on unpasteurized products, although only one of In 1999, Mead et al. (18), from the eight patients (or surrogates) interviewed recalled having read Centers for Disease Control and Pre- the label. This outbreak raises questions about whether the vention (CDC), estimated that E. coli O157:H7 accounted for 73,480 illnesses current practice of requiring warning labels for unpasteurized annually in the United States, including cider provides sufficient protection for vulnerable populations, 2,000 hospitalizations and 60 deaths, as especially children. a direct result of E. coli O157:H7 infections and its complications. Despite progress in making food safer in the United States, E. coli O157:H7 associ- A peer-reviewed article ated with animal products and fresh pro- *Author for correspondence: +1 347.488.4881; Fax: +1 347.920.4771 duce remains a public health challenge E-mail: [email protected] putting a large number of persons at risk

88 FOOD PROTECTION TRENDS | FEBRUARY 2011 for E. coli O157:H7 infection and its without diarrhea history from October 1 The Oklahoma Dairy, Food, and complications (7, 11, 14, 21). to the date of interview. Water Laboratory and the OSDH Public In Oklahoma, from 1994 through During October 12–25, a total of Health Laboratory tested the environ- 1998, an average of 17 cases of E. coli 16 case-patients (11 confirmed and five mental swabs and samples of the apple O157:H7 infections were reported to the probable) and 24 control subjects were cider collected during the environmen- Oklahoma State Department of Health interviewed by use of a standard ques- tal investigation. They performed total (OSDH) annually. On October 11, tionnaire. If the age of the case-patient and fecal coliform testing and testing for 1999, a hospital laboratory in northeast or control subject was less than 14 years, E. coli O157:H7 antigen, using the visual Oklahoma notified OSDH of four pa- a parent/guardian responded to the ques- immunoprecipitation assay (VIP™: Bio- tient specimens that had tested positive tions. Case-patients were asked questions Control System, Bellevue, WA, USA) for E. coli O157:H7 by a fecal antigen- regarding food consumption within 7 and direct plating of samples from eight screening assay. In response to these re- days of illness onset. Control subjects unopened containers of apple cider (mul- ports, OSDH immediately initiated an were asked to report on foods consumed tiple lot numbers) and one cider sample epidemiologic investigation to (1) de- during the 7-day period before the inter- collected from a case-patient’s household. termine if these represented an outbreak view. Bacterial culture and antigen testing were and if so, the magnitude of the outbreak, also performed on 20 environmental (2) identify risk factors for illness and the swabs collected during the investigation Environmental investigation possible source or vehicle for infection, (unopened jugs of cider, environmental and (3) implement preventive measures. After epidemiologically linking the swabs of cider production equipment, outbreak to consumption of unpasteur- and samples of tap water from the cider MATERIALS AND METHODS ized apple cider from a single orchard mill). Additionally, coliform counts and (defined here as Orchard A), staff from bacterial culture were performed on tap- Case finding the OSDH Consumer Protection Di- water samples collected from the cider After the initial case report, OSDH vision, the Wagoner County Health processing room and packing shed. initiated active surveillance. All hospitals Department, and the OSDH Com- and clinical laboratories in Tulsa and municable Disease Division conducted Statistical analysis neighboring counties in Oklahoma were separate site visits and inspections of the Data were entered into Epi-Info™ contacted by telephone and encouraged suspected orchard. Unopened contain- 6.04b (CDC, Atlanta, Georgia). A de- to report suspected cases of E. coli infec- ers of cider, environmental swabs of the scriptive analysis was performed to calcu- tion or postdiarrheal hemolytic uremic cider production equipment, and sam- late frequency of selected variables. Only syndrome (HUS). A confirmed case ples of tap water from the cider mill were confirmed cases were included in the was defined as diarrheal illness (more collected for laboratory analyses. matched case-control analysis of possible than three loose stools per 24 hours) risk factors to determine matched odds occurring among persons of Northeast- Laboratory investigation ratios (ORs) and their 95% confidence ern Oklahoma (Tulsa and neighboring intervals (95% CIs). counties) during October 1999, and a All available patients’ stools were positive fecal antigen test or culture for cultured at the county laboratory for E. coli O157:H7. A probable case was diarrheal pathogen identification. Test- RESULTS defined as diarrhea (three or more loose ing included direct culture attempts, ® Active surveillance stools per 24 hours) occurring in a fam- Shiga-toxin testing (ImmunoCard STAT ily member of a patient with confirmed EHEC, Meridian Diagnostics, Inc., Cin- Sixteen cases of E. coli O157:H7 in- illness who was ill at approximately the cinnati, Ohio), and E. coli O157:H7 fection (11 confirmed and five probable) same time as that patient, but without isolation attempts by using immuno- were identified during October 12–25, laboratory confirmation. magnetic beads provided by the Food- 1999, with diarrhea onsets during borne Diseases Laboratory, CDC. Posi- October 2–17. Reported clinical symp- tive E. coli O157:H7 tests were referred Case-control study toms of the 11 confirmed cases included to the OSDH Public Health Laboratory abdominal cramping (91%), bloody di- OSDH conducted a matched case- for confirmation. Isolates cultured from arrhea (82%), fever (73%), and vomit- control study to determine possible risk available case-patient stools and con- ing (55%). Duration of diarrheal illness factors and sources for acquiring infect- firmed as E. coli O157:H7 by testing at ranged from 2 days to 13 days (mean = ion with E. coli O157:H7. For each case- the OSDH laboratory were forwarded to 5 days). Six persons (55%) were hospi- patient, two to three acquaintance con- the Texas Department of Health Labo- talized, including three children with trol subjects were selected and matched ratory for pulsed-field gel electrophore- hemolytic uremic syndrome requiring by age and neighborhood. The control sis (PFGE) subtyping. PFGE subtypes dialysis treatment. Twelve (75%) were subjects’ names and contact information were compared among outbreak cases children from 2 to 13 years old. No oth- were provided by the index case-patient. and with previously identified cases that er vulnerable population was identified All case-patients and control subjects had occurred earlier in the year. All Xba- during this outbreak. were asked questions regarding clinical I patterns were forwarded to the PFGE symptoms and risk factors for illness, in- E. coli national database at the national Case-control study cluding animal contact, food exposures, network of public health and food regu- and recreational water exposure. All latory agency laboratories coordinated by All 11 confirmed case-patients and control subjects were asymptomatic and CDC (PulseNet). 24 control subjects were included in the

FEBRUARY 2011 | FOOD PROTECTION TRENDS 89 case-control study. Case-patients and Employees described using public toilet outbreak strain. Testing of all apple control subjects had similar sociode- facilities with hand-washing sinks on the cider and environmental samples col- mographic characteristics. All the case- farm. lected during the environmental inves- patients and controls were residents of The owner reported that no apples tigation of Orchard A failed to detect O157. two counties in northern Oklahoma. were obtained from other orchards, and E. coli no apples retrieved from the ground The median age was 10 years, with a (known as droppers) were used for cider DISCUSSION range of 2–38 years, for the cases vs. 9 production before the outbreak. Employ- years, with a range of 2–42 years for con- ees had picked apples from trees, placed This investigation confirmed that trols. The majority of participants were them in wooden crates, and sent them to a regional E. coli O157:H7 outbreak female; (64% of the cases vs. 62% for the apple washer facility, which used mu- occurred in Oklahoma during October nicipal running water. After washing, the 1999. Sixteen cases (11 confirmed and controls) and all were white. Ten (91%) 5 probable) were identified as outbreak- of the 11 case-patients reported drinking apples were transported in pickup trucks to the cider press approximately 50 me- associated. The investigation provided apple cider within one week before onset epidemiologic evidence that unpasteur- ters away. of diarrheal illness, and only two (8%) ized apple cider produced and bottled at During the cider production pro- a local family orchard and then sold to of 24 control subjects reported drinking cess, potassium polysorbate was added as apple cider before the interview. All case- local grocery outlets was the most likely a preservative, but the juice was unpas- vehicle of the outbreak. Results of the patients with this exposure identified the teurized. Then the cider was stored in a same orchard as the source of the apple PFGE subtyping on patients’ isolates refrigerated main container of about 270 were compatible with a point-source cider they had consumed. The two con- gallons. At the end of the 1-day process, outbreak and consistent with the epide- trol subjects who had consumed apple the juice was dispensed from the main miologic findings. Only one confirmed cider described having obtained their container to half- or one-gallon plastic adult case-patient, whose diarrhea began apple cider from a different orchard. containers identified by using a Julian October 15, 1999, did not report apple Analysis of possible risk factors re- system of dating. All containers of un- cider consumption; this case-patient pasteurized cider were labeled with the lived in the same zip code area as two vealed that consumption of apple cider standard Food and Drug Administra- produced at a single orchard (defined other confirmed case-patients, whose tion (FDA)-required warning label for diarrhea had started October 8 and here as Orchard A) was discovered to be persons at highest risk for experiencing 9, respectively. We did not investigate strongly associated with E. coli O157:H7 foodborne illnesses (i.e., “Warning: This whether contact occurred among these infection (matched OR undefined; un- product has not been pasteurized and, three patients. In prior reported E. coli matched P-value < 0.00001). No associa- therefore, may contain harmful bacteria O157:H7 outbreaks (20, 23), secondary tion with other factors was identified. that can cause serious illness in children, cases have been identified, and the case- On the basis of this epidemiologic the elderly, and persons with weakened patient without apple cider consumption evidence, OSDH ordered Orchard A immune systems.”) (25). might have been a secondary case. Detailed written distribution re- to discontinue unpasteurized apple ci- Similar outbreaks of E. coli O157: cords were not produced, but according H7 infection associated with consump- der production and recalled the apple to verbal reports, distribution of the cider tion of unpasteurized apple cider or cider on October 12, 1999. A press re- was limited to retail grocery outlets. juice have been reported (4, 5, 6, 8, 13). lease was issued advising persons not to After identification of Orchard A That none of these investigations was drink purchased unpasteurized apple unpasteurized apple cider as the possible able to definitively identify the mode cider from local grocery outlets in the vehicle of contamination, eight study of contamination underscores the diffi- outbreak geographic area. The last case participants and/or their parents/guard- culty of doing so. In our investigation, of E. coli O157:H7 illness was reported ians were recontacted and asked if they we likewise were unable to establish how the apple cider became contaminated. on October 17, 1999, a total of 5 days had read the warning label on the apple cider container. Only one out of the However, three explanations are plau- after Orchard A’s unpasteurized apple ci- eight reported having read the warning sible. First, droppers might have been der recall. label, and then only after a portion of the used earlier, although the orchard owner cider had already been consumed. might have been unaware of the fact. Environmental investigation Because the infectious dose of E. coli Laboratory analyses O157:H7 is relatively low, even a small During the environmental investi- number of contaminated droppers could Nine stools (82%) out of the 11 gation, the owner reported that Orchard cause human illness. At the time of the stool specimens collected from con- A, a family-owned farm, had been pro- investigation, the cider producer indicat- firmed cases had positive cultures for ducing apple cider for approximately 20 ed that he had not yet used droppers to E. coli O157:H7, seven (64%) had years before this outbreak. Orchard A make cider, because the apples had just positive fecal O157:H7 antigen comprised approximately 15–20 acres. E. coli begun to fall from the trees. This suggests Cattle were pastured approximately 200 tests and five (45%) had both antigen that the practice of using fallen apples was yards from the orchard. No evidence test and culture positive. PFGE testing acceptable. Second, cross-contamination (tracks or manure) existed to indicate performed on nine available isolates of might have occurred from an infected recent presence of deer or cattle in the E. coli O157:H7 cultured from case- asymptomatic worker, and because of orchard area. Rain water flowed out of patients’ stool specimens exhibited the wide clinical spectrum of E. coli the orchard and toward a pasture adja- Xba-I patterns that were indistinguish- O157:H7 infections, an infected worker cent to the orchard. Before the outbreak, able from each other. This was classi- might have experienced a relatively mild five employees had worked on the farm fied as the outbreak strain. Four E. coli diarrheal illness and continued to work and reported working there during the O157:H7 isolates from sporadic cases in Orchard A. Third, a worker might last 10 years. No new staff were recently reported during the outbreak period have cross-contaminated apples by wear- hired; none reported recent history of from other regions of the state were also ing gloves or other clothing that had gastrointestinal illness or diarrhea, travel, subtyped by PFGE. One of these four been used elsewhere and become con- absenteeism, or contact with animals. displayed a pattern consistent with the taminated with ruminant feces.

90 FOOD PROTECTION TRENDS | FEBRUARY 2011 Because the cider operation used teurized apple cider by persons at highest of diarrhea and hemolytic uremic potable water obtained from a municipal risk for experiencing a foodborne illness. syndrome from Escherichia coli water system in a rural water district, wa- Because of the serious and pos- O157:H7 in fresh-pressed apple ter contamination was unlikely. Further- sibly life-threatening consequences of cider. J. Am. Med. Assn.269(17):2264– more, no cases of E. coli O157:H7 infec- E. coli O157:H7 infection, protection of 2266. tion had been reported in the geographic children can be enhanced by educating 5. Centers for Disease Control and area of the orchard or rural water district schools and other groups that host chil- Prevention. 1996. Outbreak of during that calendar year. dren (e.g. scouts) about the risks that can Escherichia coli O157:H7 infec- Although all laboratory tests be associated with traditional activities tions associated with drinking failed to detect the presence of E. coli such as orchard field trips in the fall. It is unpasteurized commercial apple O157:H7 in sampled lots of the ci- noted that educational efforts also can be juice—British Columbia, California, der and environmental specimens, directed to those institutions that serve Colorado, and Washington. MMWR this is not unusual, compared with children. 45(44):975. results of other investigations (6, 9, 6. Centers for Disease Control and 10, 26). Investigators of a substantial ACKNOWLEDGMENTS Prevention. 1997. Outbreaks of E. coli O157:H7 outbreak linked to un- Escherichia coli O157:H7 infection We recognize and express our grati- and cryptosporidiosis associated pasteurized commercial apple juice in tude to Debbie Chambers and Terry 1996 tested 184 bottles of unopened with drinking unpasteurized apple Wright, Consumer Protection Division, cider—Connecticut and New York, apple juice, yet only one yielded a posi- Tulsa City-County Health Department tive culture and isolation (8). October 1996. MMWR 46(1): 4–8. (TCCHD), for their invaluable assis- 7. Centers for Disease Control and Orchard A’s apple cider operator was tance with case interviewing and data producing and labeling his product so as Prevention. 2005. Outbreaks of collection. We also thank Robert Rock- Escherichia coli O157:H7 associated to meet FDA requirements (25). The man and Paul Early for their hard work with petting zoos—North Carolina, FDA expected that information on the and support with the environmental Florida, and Arizona, 2004 and 2005. warning label would allow consumers to investigation. In kind, we acknowledge MMWR 54(50):1277–1280. make an informed decision on whether and thank Michael McDermott, OSDH 8. Cody, S. H., M. K. Glynn, J. A. Farrar, to purchase and consume unpasteurized Public Health Laboratory, for his dili- K. L. Cairns, P. M. Griffin, J. Kobayashi, juice. Although the cider associated with gence and patient assistance with the M. Fyfe, R. Hoffman, A. S. King, J. H. this outbreak carried a warning label, it microbiologic testing, and Julie Magri, Lewis, B. Swaminathan, R.G. Bryant, was not an effective public health safe- MD, MPH, Epidemic Intelligence Ser- and D. J. Vugia. 1999. An outbreak guard for children. Only one out of the vice Field Assignments Branch, CDC of Escherichia coli O157:H7 infect- eight study participants and/or their par- Atlanta, for editing the manuscript. ion from unpasteurized commer- ents or guardians reported having read Note: The findings and conclusions cial apple juice. Ann. Intern. Med. in this report are those of the authors and the prominent display on the product of 130(3):202–209. do not necessarily represent the official the FDA warning label concerning con- 9. Dingmand, D. W. 2000. Growth of position of the Centers for Disease Con- sumption of unpasteurized apple cider Escherichia coli O157:H7 in bruised trol and Prevention. by persons at highest risk of experiencing apple (Malus domestica) tissue as in- a foodborne illness. fluenced by cultivar, date of harvest, The only vulnerable population REFERENCES and source. Appl. Environ. Microbiol. identified during this outbreak was chil- 1. Ackers, M. L., B. E. Mahon, E. 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The Samuel J. Crumbine Consumer • Providing targeted outreach; Protection Award for Excellence in forming partnerships; and participating Food Protection at the Local Level in forums that foster communication and is seeking submissions for its 2011 information exchange among the regula- program. tors, industry and consumer representa- tives. All local environmental health jurisdictions in the U.S. and Canada are encouraged The award is sponsored by the to apply, if they meet the following basic Conference for Food Protection, in criteria: cooperation with the American Academy of Sanitarians, American Public Health • Sustained excellence over the preceding four to six Association, Association of Food and Drug Of cials, years, as documented by speci c outcomes and Foodservice Packaging Institute, International Association achievements, and evidenced by continual improve- for Food Protection, National Association of County & ments in the basic components of a comprehensive City Health Of cials, National Environmental Health program; Association, National Restaurant Association Solutions, NSF International and Underwriters Laboratories, Inc. • Demonstrated improvements in planning, managing and evaluating a comprehensive program; For more information on the Crumbine Award program and to download the 2011 entry guidelines, please go to • Innovative and effective use of program methods and www.fpi.org (see “Awards” section). Deadline for entries problem solving to identify and reduce risk factors that is March 15, 2011. are known to cause foodborne illness; and

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