Outbreak of Multidrug-Resistant Salmonella enterica serotype Newport Infections Associated with Consumption of Unpasteurized Mexican-Style Aged Cheese --- Illinois, March 2006--April 2007

During March 2006--April 2007, an outbreak of Salmonella enterica serotype Newport infections occurred predominantly among Hispanics in northeastern Illinois. Samples from 85 patients, one sample of Mexican-style aged cheese (cotija) from a local Hispanic grocery store (grocery store A), and milk from a bulk tank on a local dairy farm tested positive for S. Newport and had indistinguishable pulsed-field gel electrophoresis (PFGE) patterns. This report summarizes the investigation into S. Newport infections associated with this outbreak. The findings emphasize the need for regulatory authorities to ensure that dairy products, including Mexican-style cheese, are manufactured and distributed by inspected sources and highlight the need for culturally targeted education of consumers and grocery-store operators regarding risks associated with consuming unpasteurized dairy products.

On October 9, 2006, public health officials in Kane County, Illinois, notified the Illinois Department of Public Health (IDPH) of 13 cases of S. Newport infection among Hispanic residents since March 2, 2006. S. Newport is a rare serotype in Kane County; during 2001--2005, five or fewer infections were reported annually. The Kane County Department of Health conducted the initial investigation and contacted IDPH for assistance in determining the source of infection and developing measures to prevent future illness.

By March 1, 2007, local health departments had identified 67 patients who had illnesses compatible with S. Newport infection. Among these, 46 (69%) reported shopping at local Hispanic grocery stores. Three stores with the highest reported shopping frequency (including grocery store A) and the patients' home addresses were mapped using geographic information system software; clustering of cases near the stores was apparent. A hypothesis-generating questionnaire was developed and included questions regarding consumption of various foods, including Mexican-style cheese, unpasteurized milk, and unpasteurized and homemade cheese. The questionnaire was administered beginning March 2, 2007, to patients with onset of illness within the preceding 3 months. Thirteen patients with an onset during December 30, 2006--February 26, 2007, completed the questionnaire. Ten (77%) reported eating Mexican-style cheese; none reported consuming unpasteurized milk, unpasteurized cheese, or homemade cheese 7 days before onset of illness.

Case Definition and Case Finding

A case was defined as diarrheal illness (three or more loose stools within 24 hours) with onset beginning on or after March 2, 2006, and an isolate of S. Newport with a PFGE match by at least one enzyme (xbaI) in an Illinois resident. A memorandum was sent to all local health departments on November 28 to inform them of the outbreak and encourage prompt reporting to IDPH. Additional cases were identified by performing PFGE on all S. Newport isolate cultures reported to IDPH. Local Illinois health departments contacted all identified patients to obtain information regarding demographic characteristics, date of illness onset, clinical presentation, and household contacts. Patients were asked to report food-consumption and grocery-shopping history for the 3 days (one incubation period) before illness onset by use of a standardized Illinois salmonellosis case report form.

Eighty-five culture-confirmed cases were identified among residents of nine counties in northeastern Illinois, with dates of illness onset during March 2, 2006--April 25, 2007 (Figure). Patients ranged in age from 9 days to 85 years (median: 34 years). Forty-five (53%) were male. Seventy-six (96%) of 79 patients who reported ethnicity were Hispanic, and Spanish was the primary language for 40 (78%) of 51 patients who reported a primary language. Among patients who reported clinical symptoms, 53 (72%) of 74 reported fever, and 43 (59%) of 73 reported bloody diarrhea. Thirty-six (44%) of 82 patients were hospitalized. No deaths were reported. Five patient stool isolates were selected randomly and sent to CDC for antibiotic susceptibility testing. All five isolates were resistant to eight antibiotics: amoxicillin/clavulanic acid, ampicillin, cefoxitin, ceftiofur, chloramphenicol, streptomycin, sulfamethoxazole, and tetracycline. This resistance pattern is consistent with S. Newport multidrug-resistant phenotype AmpC (Newport-MDRAmpC) (1).

Case-Control Study

After investigators found improperly labeled cotija cheese in grocery store A, a case-control study was initiated on March 21, 2007. Case-patients with the most recent onset of illness were contacted first. Controls were selected through a reverse telephone directory and matched by age, ethnicity, and city of residence. Twelve case-patients with onset of illness from November 1, 2006--March 2, 2007, and 27 controls were enrolled. The study included questions about consumption of four specific types of Mexican-style cheese and purchase of cheese from 10 local Hispanic grocery stores. Interviews were ended on March 23 because a press release was issued by the Kane County Department of Health to warn the public, specifically members of the Hispanic community, about the risks of consuming Mexican-style cheese from unlicensed producers, an action that might have biased responses. A matched-pair analysis was performed; no statistical association was found between illness and cotija or grocery store A (Tables 1 and 2).

Environmental Investigation

During March 6--April 5, 2007, local and state public health food sanitarians inspected Hispanic grocery stores in Kane County. On March 9, a sanitarian noticed an improperly labeled Mexican-style aged cheese (cotija) in grocery store A. The cheese label did not specify the manufacturer or distributor; inspectors were unable to determine whether the cheese had been obtained from a licensed source. Illinois law requires grocery stores to purchase dairy products from a licensed manufacturer or distributor (2). An embargo was immediately placed on the cheese, preventing sale to the public. Cheese samples were sent to the IDPH laboratory for testing. Cotija from grocery store A had >29,400 mU/L of alkaline phosphatase activity, indicating inadequate pasteurization (3). On March 19, S. Newport was isolated from the cheese and had a PFGE pattern indistinguishable from the outbreak strain.

The cotija cheese manufacturer was not identified, so investigators searched for the source of unpasteurized milk used to make the cheese. In 2005, dairy farm A had been suspected of illegal sale of unpasteurized milk to grocery store A; a subsequent investigation was inconclusive. In Illinois, a dairy producer may sell unpasteurized milk from its farm to an individual for personal consumption but not for commercial resale (2). Investigators visited dairy farm A on March 27, collected samples of unpasteurized milk, and reviewed bulk-milk weight sheets. The data indicated large variations in pounds of milk sold for pasteurization, suggesting possible illegal sales of unpasteurized milk. Unpasteurized milk collected from the bulk tank tested positive for S. Newport, with a PFGE pattern indistinguishable from the outbreak strain. On April 5, IDPH prohibited unpasteurized milk sale by farm A to the public until a negative Salmonella culture was obtained from the bulk milk tank. No additional cases of S. Newport matching the outbreak pattern were identified after April 25.

Public Health Action

After the investigation, review of dairy farms' daily bulk-milk weight sheets was heightened by IDPH inspectors statewide to monitor fluctuations in milk sales that could indicate improper distribution of unpasteurized milk. Local Illinois health departments were encouraged to visit Hispanic grocery stores and restaurants to ensure cheese products sold were from licensed dairy manufacturers. Information on Illinois regulations regarding sale of dairy products was provided to Hispanic grocery stores. Information was provided to the Spanish-language media to alert their audience about the risks associated with consumption of illegally manufactured Mexican-style cheese.

Reported by: C Austin, DVM, L Saathoff-Huber, MPH, M Bordson, Illinois Dept of Public Health; C Dobbins, MS, C Gross, K Marishta, MPH, F Carlson, MPH, G Maurice, Kane County Dept of Health; IC Trevino, DVM, EIS Officer, CDC.

Editorial Note:

Consumption of unpasteurized dairy products in the United States has been associated with foodborne illnesses attributed to multiple pathogens, including Salmonella species, Campylobacter jejuni, Listeria monocytogenes, and Escherichia coli O157:H7 (4--7). During 1998--2005, 45 outbreaks of foodborne illness were reported to CDC in which either unpasteurized milk or cheese made from unpasteurized milk was implicated. Approximately 1,000 persons became ill; 104 were hospitalized, and two died (CDC, unpublished data, 2007). Hispanics have a higher incidence of salmonellosis and are more likely to consume high-risk foods, including unpasteurized milk and cheese, than other ethnic populations (8).

Dairy products made with dairy farm A milk were likely responsible for this outbreak. All 85 patients, an aged Mexican-style cheese (cotija), and raw milk from a local dairy had an isolate of S. Newport with an indistinguishable PFGE pattern. Although no significant association was found between consumption of the Mexican-style aged cheese and illness, no cases of S. Newport matching the outbreak pattern have been identified since April 25, 2007, and cases of S. Newport have returned to preoutbreak levels in Kane County.

Newport-MDRAmpC has become a public health concern because of the increase in reported incidence in the United States during the last 10 years (1). Antibiotics typically used to treat Salmonella infections, especially in children, are ineffective against this strain (9). Outbreaks of Newport-MDRAmpC infection have been associated with an Italian-style soft cheese and ground beef from dairy cattle (9).

This is the first report of Salmonella isolated from an aged, rather than fresh, Mexican-style cheese. Performed correctly, the aging process inhibits pathogenic bacteria such as salmonellae (10). The Food and Drug Administration allows certain cheeses to be manufactured using unpasteurized milk if they are aged for at least 60 days.* Although all U.S. dairy manufacturers and distributors are inspected, requirements for cheese-manufacturing licensure vary among states. In Illinois, manufacturers must be licensed by the state (2). Although outbreaks caused by illegally manufactured Mexican-style cheese have been commonly associated with sales by street vendors, door-to-door salesmen, and flea markets and with gifts from relatives returning from abroad, small Hispanic grocery stores also have been implicated (5--7).

To prevent future outbreaks and reduce sales of illegally manufactured cheese, local and state food regulatory authorities should enforce compliance with unpasteurized milk sale and distribution regulations; dairy farms' bulk-milk weight sheets should be monitored. Food regulatory authorities should be aware that illegally manufactured cheese might be sold at grocery stores, be alert for missing or incomplete labeling, and ensure that dairy products are from an inspected manufacturer or distributor. Finally, food regulatory and public health officials should recognize that aged Mexican-style cheese can be a source of infection.

Acknowledgments

This report is based, in part, on contributions by C Conover, MD, K Kelly-Shannon, P Ward, R Lucht, MBA, D Hennings, Div of Infectious Diseases, Illinois Dept of Public Health; P Dombroski, J Price, MS, Div of Laboratories, Illinois Dept of Public Health; and G Ewald, MSPH, S Greene, MPH, M Lynch, MD, and M Biggerstaff, MPH, National Center for Zoonotic, Vector-Borne, and Enteric Diseases, CDC.

References

1. CDC. National Antimicrobial Resistance Monitoring System for enteric bacteria (NARMS): Human isolates final report, 2004. Atlanta, GA: US Department of Health and Human Services, CDC; 2007.
2. Grade A pasteurized milk and milk products act. 410 Illinois compiled statutes 635. Effective October 1, 2003. Available at http://www.ilga.gov/legislation/ilcs/ilcs2.asp?chapterid=35.
3. Salter RS, Fitchen J. Evaluation of a chemiluminescense method for measuring alkaline phosphatase activity in whole milk of multiple species and bovine dairy drinks: interlaboratory study. J AOAC Int 2006;89:1061--70.
4. D'Aoust JY. Manufacture of dairy products from unpasteurized milk: a safety assessment. J Food Prot 1989;52:906--14.
5. Villar RG, Macek MD, Simons S, et al. Investigation of multidrug-resistant Salmonella serotype typhimurium DT104 infections linked to raw-milk cheese in Washington State. JAMA 1999;281:1811--6.
6. Cody SH, Abbott SL, Marfin AA, et al. Two outbreaks of multidrug-resistant Salmonella serotype Typhimurium DT104 infections linked to raw-milk cheese in Northern California. JAMA 1999;281:1805--10.
7. MacDonald PD, Whitwam RE, Boggs JD, et al. Outbreak of listeriosis among Mexican immigrants as a result of consumption of illicitly produced Mexican-style cheese. Clin Infect Dis 2005;40:677--82.
8. Banerjee A, Frierman M; EIP FoodNet Working Group, et al. Characterization of high risk food consumption practices among the Hispanic population. FoodNet 2000--2001. Chicago, IL: Infectious Diseases Society of America; 2002.
9. Gupta A, Fontana J, Crow C, et al. Emergence of multidrug-resistant Salmonella enterica serotype Newport infections resistant to expanded-spectrum cephalosporins in the United States. J Infect Dis 2003; 188:1707--16.
10. Bachmann HP, Spahr U. The fate of potentially pathogenic bacteria in Swiss hard and semihard cheeses made from raw milk. J Dairy Sci 1995;78:476--83.

* Food and Drug Administration, Center for Food Safety and Applied Nutrition. Grade "A" pasteurized milk ordinance: 2003 revision. Available at http://www.cfsan.fda.gov/~ear/pmo03toc.html.

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Date last reviewed: 4/24/2008