Salmonella Typhimurium Infection Associated with Raw Milk and Cheese Consumption --- Pennsylvania, 2007

In February 2007, the Pennsylvania Department of Health received reports, through routine electronic laboratory disease reporting, of two persons with recent laboratory-confirmed infections with Salmonella enterica serotype Typhimurium. Both persons had reported drinking raw (unpasteurized) milk from the same York County, Pennsylvania, dairy (dairy A). S. Typhimurium isolates from these persons had pulsed-field gel electrophoresis (PFGE) patterns that were indistinguishable by use of the XbaI restriction enzyme. The same month, the Pennsylvania Department of Agriculture (PDA) received reports of illness from raw-milk customers of dairy A. PDA obtained milk samples from the raw-milk bulk tank at dairy A, which yielded S. Typhimurium with a PFGE pattern that was identical to the pattern from patient isolates. On February 26, the Pennsylvania Department of Health and PDA launched an investigation to determine the source and scope of the outbreak. This report summarizes the findings of that investigation, which determined that 29 cases of diarrheal illness caused by S. Typhimurium were associated with consumption of raw milk or raw-milk products from dairy A. The findings underscore the need to inform policymakers and the public of the potential health risks associated with raw-milk consumption.

Epidemiologic and Laboratory Investigation

In Pennsylvania, raw-milk sales are legal at farms that hold a PDA permit, and vendors must display public notices regarding the potential hazards of consuming raw milk (1). Dairy A owned 120 cows and sold raw milk for pasteurization and by PDA permit directly to consumers. In February 2007, PDA estimated that dairy A was selling 200--300 gallons of raw milk weekly to 275 regular customers.

A case of salmonellosis was defined as a diarrheal illness with onset since February 1, 2007, in a Pennsylvania resident who provided a stool specimen that tested positive for S. Typhimurium with a PFGE pattern that matched the outbreak pattern by use of the XbaI restriction enzyme. Nationally notifiable disease reports from Pennsylvania since January 2005 were reviewed for PFGE-matched S. Typhimurium isolates to identify cases and risk factors. To locate additional cases, ill household contacts of persons with confirmed cases were asked to provide food histories and submit stool specimens for testing. Raw milk for testing was obtained from dairy A milk tanks on five dates (February 20, February 28, March 27, May 14, and July 19) and from households of two ill persons on two dates (February 28 and July 20). In addition, PDA conducted multiple dairy A inspections during February--July 2007.

Investigative Findings

A total of 29 cases were identified, with illness onset occurring in three temporal clusters during February 3--July 14, 2007 (Figure). The first cluster consisted of 15 cases with onsets of illness from February 3 to March 5. Raw-milk samples were collected February 20 from a dairy A bulk milk tank and February 28 from the home of an ill person. Both sets of samples yielded the outbreak strain of S. Typhimurium. On March 2, PDA ordered dairy A to stop raw-milk sales and advised the public not to consume raw-milk products from dairy A.

On March 19, PDA allowed dairy A to resume sales of raw milk after PDA conducted inspections and recorded two consecutive negative cultures from milk-tank samples. However, a second cluster of three cases was detected when the outbreak strain of S. Typhimurium was identified in another patient, whose diarrheal illness began on March 21 and who had consumed raw milk from dairy A after sales resumed. The two additional cases were identified in persons with onsets of illness on March 19 and March 22. The first of these occurred in one of six ill persons who primarily spoke Spanish and who told investigators they had not consumed raw milk. However, when reinterviewed in early April, three of these six persons reported consuming queso fresco (a type of soft cheese) they bought at a grocery store serving the local Hispanic community. PDA learned that the queso fresco had been made by an unlicensed producer who purchased approximately 20 gallons of raw milk weekly from dairy A. Sale of raw-milk cheeses aged <60 days is illegal in Pennsylvania. Subsequently, in April, PDA inspectors seized 18 unlabeled retail containers of queso fresco from the grocery store. The cheese tested positive for alkaline phosphatase, indicating the cheese was produced from unpasteurized milk (2). Bacterial cultures were negative for pathogens.

On March 27, PDA again ordered dairy A to halt raw-milk sales and suspended its raw-milk permit. No additional cases were noted until June--July 2007, when a third cluster of 11 PFGE-matched S. Typhimurium cases was detected through routine electronic laboratory reporting. Of these, 10 occurred among residents of three counties near dairy A. On July 19, PDA confirmed that dairy A had been distributing raw milk to the public despite its suspended permit; the date when illegal milk distribution began could not be determined. The outbreak strain of S. Typhimurium was isolated from dairy A raw milk collected from a bulk milk tank on July 19 and from the home of an ill person on July 20. PDA ordered dairy A to halt distribution of raw milk on July 20 and subsequently revoked the raw-milk permit for this dairy.

Among the 29 persons identified with diarrheal illness and PFGE-matched S. Typhimurim, 17 (59%) were male, and the median age was 6 years (range: 5 months--76 years). Fourteen (48%) patients reported drinking raw milk from dairy A, four (14%) consumed unregulated queso fresco (three linked to dairy A raw milk and one from an unknown source), and two (7%) consumed raw milk but did not identify the source. Two (7%) other patients were unrelated infants aged 5 months and 7 months. The parents of these infants acknowledged that raw milk from dairy A was present in their households but told investigators the milk was not consumed by the infants. For seven (24%) patients who did not reside with any of the other patients, no source of exposure to S. Typhimurium could be determined. Two of the 29 patients were hospitalized; no deaths were reported.

Environmental Inspections

Eight PDA inspections of dairy A conducted during January--April 2007 revealed improper cleaning of milking equipment, insufficient supervision of workers, unspecified illness among lactating cows, and bird and rodent infestation. On at least two inspections, the required public notice regarding the potential hazards of drinking raw milk was not visible at the dairy A retail store.

S. Typhimurium matched by PFGE to the outbreak pattern was isolated from dairy A raw-milk tank samples collected on three different dates (February 20, May 14, and July 19); an S. Typhimurium isolate collected from a milk tank February 28 was unavailable for PFGE typing. In addition to Salmonella, dairy A raw-milk tank samples also yielded Listeria monocytogenes (February 28, May 14, and July 19) and Campylobacter jejuni (February 28 and May 14). Although a stool specimen from one patient with February 28 illness onset yielded both S. Typhimurium and C. jejuni, the Campylobacter isolate was unavailable for subtyping. No Listeria infections were associated with dairy A.

Reported by: L Lind, MPH, J Reeser, K Stayman, M Deasy, M Moll, MD, A Weltman, MD, V Urdaneta, MD, S Ostroff, MD, Pennsylvania Dept of Health; W Chirdon, Pennsylvania Dept of Agriculture. E Campagnolo, DVM, Div of State and Local Readiness, Coordinating Office for Terrorism Preparedness and Emergency Response; T Chen, MD, EIS Officer, CDC.

Editorial Note:

Raw milk is a well-documented source of infections from Salmonella, Escherichia coli O157:H7, Campylobacter, Listeria, Mycobacterium bovis, and other pathogens (2--6). In 1938, before widespread adoption of milk pasteurization in the United States, an estimated 25% of all foodborne and waterborne outbreaks of disease were associated with milk (7). By 2001, the percentage of such outbreaks associated with milk was estimated at <1% (7). During 1998--2005, a total of 45 outbreaks of foodborne illness were reported to CDC in which unpasteurized milk (or cheese suspected to have been made from unpasteurized milk) was implicated. These outbreaks accounted for 1,007 illnesses, 104 hospitalizations, and two deaths (CDC, unpublished data, 2007). Because not all cases of foodborne illness are recognized and reported, the actual number of illnesses associated with unpasteurized milk likely is greater.

In the investigations described in this report, the evidence indicating raw milk from dairy A as the source of this outbreak included the 1) high percentage of ill persons who reported consuming either raw milk (48%) or queso fresco traced to raw milk (10%) from dairy A, 2) temporal associations between clusters of illnesses and starts and stops of distribution of raw milk by dairy A, and 3) repeated isolation of the outbreak strain of S. Typhimurium from dairy A raw-milk tanks. The PFGE pattern of the outbreak strain (XbaI JPXX01.0022) is rare, previously identified only 24 times in isolates from 11 states in 3 years, in a national PulseNet database of approximately 43,000 S. Typhimurium isolates.

Consumers have reported consuming raw milk for convenience, taste preference, or perceived health benefits. Although some advocates claim health benefits from raw milk compared with pasteurized milk, including decreased risks for atherosclerosis, arthritis, and lactose intolerance, such claims are not supported by scientific evidence (8). Unsubstantiated claims of health benefits of raw milk for infants and children are particularly concerning for caregivers because infants and children are dependent on their caregivers to make safe dietary decisions for them. Sixteen of the 29 ill persons in this outbreak were aged <7 years.

Pathogens that infect humans are shed in the feces of cows, can be present in or on the udders of cows, and can contaminate their milk. Standard hygiene practices during milking can reduce but not eliminate the risk for milk contamination. In a 2001--2002 survey of Pennsylvania dairy farms, pathogenic bacteria, including Salmonella, were isolated from 13% of samples from raw-milk bulk tanks (9). Pasteurization decreases the number of pathogenic organisms, prevents transmission of pathogens, and has been determined to improve the safety of milk more than other measures, including certification of raw milk (4,5).

Farms in Pennsylvania that hold PDA raw-milk permits undergo twice-monthly milk testing for coliforms and standard plate counts and monthly testing for growth inhibitors and somatic cell counts; annual PDA inspection and culture of raw milk for Salmonella, Campylobacter, E. coli O157, and L. monocytogenes; and annual herd skin testing for Mycobacterium bovis and Brucella (1). Despite these measures, consumers cannot be assured that certified raw milk is free of pathogens.

As of 2004, at least 27 states permitted some form of raw-milk sales to the public, including sales at dairies, farmers' markets, or through purchase of "cow shares." Certain states also allow public sales of raw milk but for pet food only (10). In Pennsylvania, the number of dairies with raw-milk permits increased from 42 in 2005 to 75 in 2007. During 2006--2007, three clusters of illness from Campylobacter were associated with consumption of raw milk from three different Pennsylvania dairies (Pennsylvania Department of Health, unpublished data, 2007). During the same period, PDA announced raw-milk recalls from three other dairies after finding L. monocytogenes in milk samples; no human illness was associated with these findings.

Given the continued interest in raw-milk production, policymakers, parents, and the public need to be informed regarding the potential health risks posed by raw-milk consumption. The only sure way for consumers to prevent raw-milk--associated infection from Salmonella or other pathogens is to refrain from consuming raw milk.

Acknowledgments

This report is based, in part, on data contributed by C Sandt, B Perry, Bur of Laboratories, P Feliciano, Pennsylvania Dept of Health; M Hydock, R Malik, L Sulpizio, Pennsylvania Dept of Agriculture; T Nguyen, T Ayers, G Ewald, M Lynch, Div of Foodborne, Bacterial, and Mycotic Diseases, National Center for Zoonotic, Vector-Borne, and Enteric Diseases; A Patel, A Sheth, EIS officers, CDC.

References

1. Commonwealth of Pennsylvania. Chapter 59: Milk sanitation. Available at http://www.agriculture.state.pa.us/agriculture/lib/agriculture/legalreference/007_0059.pdf.
2. Gillespie IA, Adak GK, O'Brien SJ, Bolton FJ. Milkborne general outbreaks of infectious intestinal disease, England and Wales, 1992--2000. Epidemiol Infect 2003;103:461--8.
3. Leedom JM. Milk of nonhuman origin and infectious disease in humans. Clin Infect Dis 2006;43:610--5.
4. Currier RW. Raw milk and human gastrointestinal disease: problems resulting from legalized sale of "certified raw milk." J Public Health Policy 1981;2:226--34.
5. Potter ME, Blaser MJ, Sikes RK, Kaufmann AF, Wells JG. Human Campylobacter infection associated with certified raw milk. Am J Epidemiol 1983;117:475--83.
6. CDC. Human tuberculosis caused by Mycobacterium bovis---New York City, 2001--2004. MMWR 2005;54:605--8.
7. Center for Food Safety and Applied Nutrition. Grade "A" pasteurized milk ordinance: 2001 revision. US Department of Health and Human Services, Food and Drug Administration, Center for Food Safety and Applied Nutrition; 2002. Available at http://www.cfsan.fda.gov/~ear/pmo01.html.
8. Leonard C. On the safety of raw milk (with a word about pasteurization). Presented at the National Conference on Interstate Milk Shipments, Columbus, Ohio, May 12--17, 2005. Available at http://www.cfsan.fda.gov/~ear/milksafe/milksa1.htm.
9. Jayarao BM, Donaldson SC, Straley BA, Sawant AA, Hegde NV, Brown JL. A survey of foodborne pathogens in bulk tank milk and raw milk consumption among farm families in Pennsylvania. J Dairy Sci 2006;89:2451--8.
10. Dairy Division of National Association of State Departments of Agriculture. Raw milk survey: November 2004. Available at http://www.nasda.org/file.aspx?id=11160.

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Date last reviewed: 11/7/2007