On November 13, 2000, health-care providers at a hospital in Winston-Salem, North Carolina, contacted the local health department about three cases of listeriosis within a 2-week period in recent Mexican immigrants. The North Carolina General Communicable Disease Control Branch, in collaboration with the Forsyth County Health Department, the North Carolina Departments of Agriculture and Consumer Services (NCDA&CS) and Environment and Natural Resources, the Food and Drug Administration (FDA), and CDC investigated this outbreak of Listeria monocytogenes infections. This report summarizes the results of the investigation, which implicated noncommercial, homemade, Mexican-style fresh soft cheese produced from contaminated raw milk sold by a local dairy farm as the causative agent. Culturally appropriate education efforts are important to reduce the risk for L. monocytogenes transmission through Mexican-style fresh soft cheese.
A case was defined as L. monocytogenes (isolated from a normally sterile site or with placental tissue staining positive using immunohistochemical techniques) in a mother of a stillborn or premature infant (<37 weeks' gestation), or a mother with a febrile illness, who was a Winston-Salem resident during October 24, 2000–January 1, 2001. Through active case finding, 12 cases were identified. On initial interview, most patients reported eating unlabeled Mexican-style fresh soft cheese bought at local markets or from door-to-door vendors. A case-control study was conducted to determine risk factors for illness; the questionnaire addressed symptoms, diet, and grocery-shopping histories during the month preceding illness. L. monocytogenes isolates from patients, raw milk, and cheese were tested using pulsed-field gel electrophoresis (PFGE). Environmental inspections of homes, local markets, and dairy farms were conducted.
All 12 patients were Hispanic; 11 were women with a median age of 21 years (range: 18-38 years), and one was a 70-year-old immunocompromised man. All but one infection were laboratory confirmed. The 11 women did not speak English, were born in Mexico, and had resided in the United States for a median of 2 years (range: 0-5 years). One had traveled outside Forsyth County during the month preceding illness. Ten women were pregnant, and infection with L. monocytogenes resulted in five stillbirths, three premature deliveries, and two infected newborns. The 11th woman was 5 months postpartum when she presented to a local hospital with meningitis caused by L. monocytogenes. She had no preexisting medical conditions. The male patient, who presented with a brain abscess, was receiving corticosteroid therapy after brain tumor surgery. On hospital admission, the 11 women reported symptoms that included fever (nine), chills (nine), headache (nine), abdominal cramps (five), stiff neck (five), vomiting (three), and photophobia (two).
The male patient was excluded from the case-control study because of difficulty finding suitable controls. In the case-control study, a mother and her fetus or newborn were counted as one case-patient. Controls were identified at a Women, Infants, and Children program office and through the county's record of women enrolled in the state's Baby Love Program, which provides outreach and prenatal-care home visits. A median of four controls (range: three to six controls) per case was selected. Controls were restricted to female Hispanic Winston-Salem residents and matched to patients by age and pregnancy status.
Patients were more likely than controls to have eaten any cheese purchased from door-to-door vendors (matched odds ratio [MOR] = 17.5; 95% confidence interval [CI] = 2.0-152.5); queso fresco, a Mexican-style fresh soft cheese (MOR = 7.3; 95% CI = 1.4-37.5); and hotdogs (MOR = 4.6; 95% CI = 1.1-19.4). Illness was not associated with purchases at specific markets or supermarkets, eating raw fruits or vegetables, deli products, other cheeses (e.g., American, cheddar, mozzarella, and blue/Gorgonzola), or other dairy products.
Various members of the Hispanic immigrant community made the Mexican-style fresh soft cheese from raw milk in their homes. Inspectors found unlabeled homemade cheese in all three of the small local Latino grocery stores they visited in Winston-Salem. In addition, many persons regularly sold the cheese in parking lots and by going door-to-door. Owners of two local dairies reported selling raw milk. Milk samples were obtained from these two Forsyth County dairies and from three dairies in neighboring counties. L. monocytogenes isolates were obtained from nine patients, three cheese samples from two stores, one cheese sample from the home of a patient, and one raw milk sample from a manufacturing grade dairy. All 14 isolates had indistinguishable PFGE patterns, indicating a common link.
NCDA&CS conducted an investigation at a manufacturing grade dairy farm to determine the potential source of L. monocytogenes contamination. NCDA&CS collected milk samples from all 49 cows in the herd and samples from the bulk milk storage tanks. Milk from each cow was tested for somatic cell count to identify mastitic cows. Milk from each cow also was tested for presence of L. monocytogenes. Repeated testing did not identify any cow with milk confirmed positive for L. monocytogenes, suggesting that the cows were not infected and that L. monocytogenes may have originated from environmental contamination.
As a result of this outbreak, North Carolina health authorities stopped the sale of raw milk by the dairy farm to noncommercial processors and educated store owners that it is illegal to sell unregulated dairy products. Officials cited the outbreak as sufficient reason to strengthen laws prohibiting the sale of raw milk except to regulated processors. Using already established programs (e.g., Baby Love Program), North Carolina officials recommended reinforcing and expanding the community awareness of the hazards of eating unpasteurized fresh cheese while pregnant. Finally, steps were taken to add listeriosis to the list of reportable diseases in North Carolina.
JD Boggs, RE Whitwam, LM Hale, MD, RP Briscoe, SE Kahn, MD, Forsyth County Health Dept, Winston-Salem, North Carolina; JN MacCormack, MD, J-M Maillard, MD, General Communicable Disease Control Br, Section of Human Ecology and Epidemiology, Div of Public Health; SC Grayson, KS Sigmon, North Carolina Dept of Environment and Natural Resources; JW Reardon, JR Saah, MS, North Carolina Dept of Agriculture and Consumer Svcs, Raleigh, North Carolina. Foodborne and Diarrheal Diseases Br, National Center for Infectious Diseases; and EIS officers, CDC.
The investigation of this outbreak implicated Mexican-style fresh soft cheese made from unpasteurized milk and hotdogs, two vehicles commonly identified as causes of L. monocytogenes outbreaks. The laboratory investigation resulted in isolation of L. monocytogenes from patients, cheese, and raw milk at a dairy farm. Molecular subtyping identified indistinguishable PFGE patterns, establishing the link between human disease, the cheese, and the source of the raw milk used to make the cheese.
Because of the health risks associated with the consumption of raw milk and raw milk products, FDA requires pasteurization of all dairy products sold across state lines except cheese made from raw milk that has to be aged a minimum of 60 days.1,2 Despite North Carolina laws prohibiting the sale and consumption of raw milk and raw milk products, such practices persist in some communities as a result of consumers' taste preferences and for cultural reasons. The popularity of queso fresco, a Mexican-style fresh soft cheese made from unpasteurized milk, has resulted in several outbreaks in Hispanic communities since the 1980s. In 1985, an outbreak of septic abortions attributed to L. monocytogenes occurred among Hispanics in Los Angeles and Orange counties, California.3 In 1997, three outbreaks of multidrug resistant Salmonella serotype Typhimurium DT104 complex strains occurred in Hispanic communities in northern California and Washington.4,5
Because queso fresco in these communities is produced in private homes, food safety regulations are difficult to enforce. Education of milk and cheese producers and consumers about the increased risk for acquiring infections, particularly L. monocytogenes, from consuming unpasteurized milk or fresh soft cheese made from unpasteurized milk, complemented by regulatory action, are the keys to making cheese safe. Successful communication of public health messages to the Hispanic community about the risk for eating Mexican-style fresh soft cheese made from raw milk can be challenging because of language and other social barriers.
The findings in this report are subject to at least four limitations. First, interviewers were not blinded to the status of the persons they were interviewing. Second, efforts were made to select controls from the same population as case-patients; however, controls were selected on the basis of use of public health service programs. Most controls were selected from a county registry for a free prenatal care program that does not require documentation to obtain service. Third, during the study, rumors spread in the community that the suspected vehicle of infection was homemade Mexican-style fresh soft cheese. Finally, patients may have had better recall of potential exposures than controls.
Following a listeriosis outbreak in Yakima County, Washington, an education program to train grandmothers, the primary cheese producers in that community, in the safe production of soft cheeses was introduced and was well received. A licensing requirement for commercial cheese makers and appropriate regulatory action also may curtail the sale of fresh soft cheese made from unpasteurized milk. Twenty-eight states permit the sale of raw milk directly from farmers to consumers.6 Until all states prohibit such sales, outbreaks associated with eating queso fresco and other unpasteurized dairy products may continue despite efforts to educate consumers, especially those who do not speak or read English and whose cultural dietary habits favor such products.
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