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Outbreaks of Escherichia coli O157:H7 Infection and Cryptosporidiosis Associated with Drinking Unpasteurized Apple Cider -- Connecticut and New York, October 1996

In October 1996, unpasteurized apple cider or juice was associated with three outbreaks of gastrointestinal illness. In the Western United States, an outbreak of Escherichia coli O157:H7 infections associated with unpasteurized commercial apple juice caused illness in 66 persons and one death (1). In addition, one outbreak of apple cider-related E. coli O157:H7 infections and another of cider-related Cryptosporidium parvum infections occurred in the Northeast. Apple cider is a traditional beverage produced and consumed in the fall. Cider often is manufactured locally at small cider mills where apples are crushed in presses, and the cider frequently is not pasteurized before sale. This report summarizes the clinical and epidemiologic features of the two apple cider-related outbreaks, which suggest that current practices for producing apple cider may not be adequate to prevent microbial contamination. Connecticut

On October 11, the Connecticut Department of Public Health (DPH) was notified by staff of the Connecticut site of CDC's Foodborne Diseases Active Surveillance Network of four reported cases of E. coli O157:H7 infection in residents of New Haven County (1995 population: 794,785). An investigation of this cluster was initiated by DPH. A case was defined as onset of diarrhea (i.e., three or more loose stools per day) during October 1-11 in a Connecticut resident and laboratory-confirmed infection with E. coli O157:H7. Additional case-finding was conducted by notifying all Connecticut clinical laboratories of a possible outbreak of E. coli O157:H7 infection and requesting that cases be reported immediately to DPH. As a result of active case-finding, DPH initially identified eight cases with onset during October 3-11.

Of the eight case-patients, six were female, and ages of all eight ranged from 2 to 73 years (mean: 25 years). Case-patients resided in six towns within New Haven County. Manifestations included bloody diarrhea and abdominal pain (eight patients), vomiting (five), and fever (four). Duration of illness ranged from 3 to 11 days (median: 7 days). Five patients were hospitalized, including one with hemolytic uremic syndrome (HUS) and one with thrombotic thrombocytopenic purpura.

On October 17, DPH conducted a matched case-control study to determine probable sources for the outbreak. Controls were selected from telephone-exchange lists and were matched to cases by sex, town of residence, and age group. Controls reported no diarrhea during the 20-day period beginning 10 days before illness onset in their matched cases. Case-patients were asked about food consumption during the 7 days preceding illness, and controls were asked about consumption during the same 7 days as their matched cases. Based on interviews with the first eight case-patients and 21 controls, increased risk for illness was associated with drinking fresh apple cider during the 7 days preceding onset of illness (matched odds ratio {OR}=12.0; 95% confidence interval {CI}=1.3-111.3; pless than 0.01). Specifically, illness was associated with drinking brand A cider (matched OR=undefined; 95% CI=3.5-infinity; pless than 0.01). No other food item (including ground beef, unpasteurized milk, or lettuce) or common event was significantly associated with increased risk for illness. Of the eight patients, seven reported drinking brand A cider during the 7 days preceding illness.

After completion of the case-control study, six additional patients were identified; of these, four had culture-confirmed infection, and two had been hospitalized with HUS but did not have culture-confirmed E. coli O157:H7 infection. All six had a history of drinking brand A cider. Ten of the 12 outbreak-associated isolates of E. coli O157:H7 were sent to CDC for pulse-field gel electrophoresis typing; all 10 were determined to be closely related.

On October 18, DPH and the Connecticut Department of Consumer Protection (DCP) advised Connecticut residents to discard or boil before drinking all brand A cider purchased since the beginning of the cider season in September. DCP coordinated a recall of brand A cider from all retail outlets. Approximately 9000 gallons of the cider had been distributed throughout Connecticut and three neighboring states. DCP and the regional office of the Food and Drug Administration (FDA) notified regulatory agency and state health department personnel in the three neighboring states of the recall.

Brand A cider was pressed at a mill in a residential area from apples purchased from multiple sources. Some of the apples used were "drop" apples (i.e., apples picked up from the ground). All apples were brushed and washed in potable municipal water in a flow-through wash system before pressing in a wooden press. Potassium sorbate 0.1% was added as a preservative; the cider was not pasteurized. New York

During October 10-15, a local hospital laboratory notified the Cortland County Health Department (CCHD) about 10 cases of laboratory-confirmed cryptosporidiosis with recent onset among county residents (1990 population: 48,963). During the same period in 1995, one case of cryptosporidiosis was reported to CCHD. All case-patients had onset of symptoms during September 28-October 10 and reported drinking apple cider produced at a local cider mill (mill A). CCHD, the New York State Department of Health (NYSDOH), and the New York State Department of Agriculture and Markets (NYS A&M) initiated an investigation of this cluster.

A confirmed case was defined as onset of diarrhea during September 28-October 19 in a Cortland County resident and laboratory evidence of Cryptosporidium in a stool specimen. A suspected case was defined as onset of diarrhea during the outbreak period in a household member of a person with confirmed cryptosporidiosis. CCHD conducted active surveillance for additional cases by contacting area clinicians, hospitals, and laboratories.

A total of 20 confirmed and 11 suspected cases were identified from 19 households. The median age was 27 years (range: 1-62 years), and 17 were female. Symptoms included diarrhea (100%), abdominal cramping (55%), vomiting (39%), fever (36%), and bloody diarrhea (10%). The median duration of symptoms was 6 days (range: 1-21 days).

CCHD and NYSDOH conducted a matched case-control study to assess probable sources of the outbreak. One neighborhood-matched control-household was contacted for each household with a laboratory-confirmed case. In each control-household, an adult (age greater than or equal to 18 years) member was asked about history of illness, whether anyone in the household had drank apple cider since September 28, which brand of cider was consumed, and the date the cider was purchased.

Eighteen case-households were included in the matched case-control study. A history of drinking cider from mill A was reported for at least one member of the 18 households, compared with only one of the 18 control-households (matched OR=undefined, pless than 0.01). Specifically, cider pressed during September 28-29 (i.e., opening weekend) was associated with illness: 15 of 17 case-households in which the purchase date was known compared with none of the control-households reported drinking cider pressed on opening weekend (matched OR=undefined, pless than 0.01).

Mill A purchased all apples for cider pressing from one New York orchard. Local and state health departments and NYS A&M inspected the cider mill and apple orchard. The owner of the orchard reported that only picked apples were sold to the cider mill, and drop apples were sold for use in processed or pasteurized foods. Before pressing, the mill washed and brushed the apples using water from a 45-foot drilled well; preservatives were not added to the cider. Although dairy livestock were not maintained by the orchard, the cider mill was located across the road from a dairy farm. Testing of remaining cider samples from opening weekend, swabs of equipment surfaces, and water obtained on October 21 from the drilled well did not yield Cryptosporidium. However, coliform bacteria were detected in four water samples obtained from the well, and E. coli was detected in one sample.

Reported by: PA Mshar, ZF Dembek, PhD, ML Cartter, MD, JL Hadler, MD, State Epidemiologist, Connecticut Dept of Public Health; TR Fiorentino, MPH, RA Marcus, MPH, School of Medicine, Yale Univ, New Haven; J McGuire, MA Shiffrin, Connecticut Dept of Consumer Protection. A Lewis, J Feuss, J Van Dyke, Cortland County Dept of Health; M Toly, M Cambridge, J Guzewich, J Keithly, PhD, D Dziewulski, PhD, E Braun-Howland, PhD, D Ackman, MD, P Smith, MD, State Epidemiologist, New York State Dept of Health; J Coates, J Ferrara, New York State Dept of Agriculture and Markets. Foodborne and Diarrheal Diseases Br, Div of Bacterial and Mycotic Diseases, and Div of Parasitic Diseases, National Center for Infectious Diseases; State Br, Div of Applied Public Health and Training (proposed), Epidemiology Program Office, CDC.

Editorial Note

Editorial Note: Unpasteurized apple cider and juice have been associated with outbreaks of E. coli O157:H7 infection, cryptosporidiosis, and salmonellosis (1-4). Animals are the primary reservoir for the pathogenic organisms associated with these outbreaks. In particular, cattle, deer, and sheep can asymptomatically carry E. coli O157:H7 and Cryptosporidium, and many animals, including cattle, chickens, and pigs, can asymptomatically carry Salmonella. Although the exact mechanisms of contamination for these previous outbreaks were not clearly determined, in three of the outbreaks, manure was suspected to have contaminated the apples. For example, in an outbreak of cryptosporidiosis in 1993, drop apples were collected from trees adjacent to an area grazed by cattle whose stool contained Cryptosporidium (3), and in a salmonellosis outbreak in 1974, drop apples had been collected from an orchard fertilized with manure (4). The practice of using drop apples for making apple cider is common (2), and apples can become contaminated by resting on ground contaminated with manure. In an outbreak of E. coli O157:H7 infections in 1991 (2), the cider press operator also raised cattle, and cattle grazed in a field adjacent to the mill. The presence of animals near a cider mill can result in manure inadvertently contacting apples, equipment, or workers' hands. In addition, apples can become contaminated if transported or stored in areas that contain manure, or if rinsed with contaminated water.

These previous outbreaks of illness prompted recommendations to reduce the risk for producing contaminated cider, including 1) preventing the introduction of animal manure into orchards, 2) avoiding use of apples that have fallen to the ground, 3) washing and brushing apples before pressing, 4) using a preservative such as sodium benzoate, and 5) routine pasteurization (3,5). In the outbreaks in Connecticut and New York, some of these recommended production practices had been followed. For example, in Connecticut, apples were washed and brushed before pressing; however, drop apples were used. In New York, the mill reportedly did not use drop apples, and apples were washed and brushed before pressing; however, cattle were present near the farm, and the apples were washed with water from a source later determined to contain E. coli -- an indicator of contamination with animal or human feces.

At least two factors complicate efforts to reduce the risk for transmission of enteric pathogens through unpasteurized apple cider and juice. First, a small number of pathogenic organisms can result in infection -- ingestion of as few as 30 Cryptosporidium (6) and less than 1000 E. coli O157:H7 (7) have caused symptomatic infection in humans. Second, although apple cider and juice usually are acidic (pH of 3-4) (5,8), both Cryptosporidium and E. coli O157:H7 are acid-tolerant, and both organisms can survive in apple cider for up to 4 weeks (3,5). The addition of preservatives to apple cider containing E. coli O157:H7 does not consistently kill the organism (5,8), and Cryptosporidium oocysts are resistant to most common disinfectants (e.g., bleach, iodine, and sodium hydroxide) (9). Pasteurization and boiling kill E. coli O157:H7 and Cryptosporidium, and other methods that might increase the safety of cider are under investigation (10). FDA is evaluating information received at a public meeting held December 16-17, 1996, to determine methods to reduce the risk for illness associated with fresh juices. Until alternative effective methods are developed, consumers can reduce their risk for enteric infections by drinking pasteurized or boiled apple cider and juice.


  1. CDC. Outbreak of Escherichia coli O157:H7 infections associated with drinking unpasteurized commercial apple juice -- British Columbia, California, Colorado, and Washington, October 1996. MMWR 1996;45:975.

  2. Besser RE, Lett SM, Weber JT, et al. An outbreak of diarrhea and hemolytic uremic syndrome from Escherischia coli O157:H7 in fresh-pressed apple cider. JAMA 1993;269:2217-20.

  3. Millard PS, Gensheimer KF, Addiss DG, et al. An outbreak of cryptosporidiosis from fresh-pressed apple cider. JAMA 1994;272:1592-6.

  4. CDC. Epidemiologic notes and reports: Salmonella typhimurium outbreak traced to a commercial apple cider -- New Jersey. MMWR 1975;24:87-8.

  5. Zhao T, Doyle MP, Besser RE. Fate of enterohemorrhagic Escherichia coli O157:H7 in apple cider with and without preservatives. Appl Environ Microbiol 1993;59:2526-30.

  6. DuPont HL, Chappell CL, Sterling CR, Okhuysen PC, Rose JB, Jakubowski W. The infectivity of Cryptosporidium parvum in healthy volunteers. N Engl J Med 1995;332:855-9.

  7. Griffin PM, Bell BP, Cieslak PR, et al. Large outbreak of Escherichia coli O157:H7 infections in the western United States: the big picture. In: Karmali MA, Goglio AG, eds. Recent advances in verocytotoxin-producing Escherichia coli infections. Amsterdam: Elsevier Science B.V., 1994;7-12.

  8. Miller LG, Kaspar CW. Escherichia coli O157:H7 acid tolerance and survival in apple cider. J Food Prot 1994;57:460-4.

  9. Campbell I, Tzipori AS, Hutchison G, Angus KW. Effect of disinfectants on survival of Cryptosporidium oocysts. Vet Rec 1982;111:414-5.

  10. Anderson BC. Moist heat inactivation of Cryptosporidium sp. Am J Public Health 1985:75:1433-4.

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