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Escherichia coli 0157:H7 Infections in Children Associated with Raw Milk and Raw Colostrum From Cows --- California, 2006

On September 18, 2006, the California Department of Public Health (CDPH) was notified of two children hospitalized with hemolytic uremic syndrome (HUS). One of the patients had culture-confirmed Escherichia coli O157:H7 infection, and both patients had consumed raw (unpasteurized) cow milk in the week before illness onset. Four additional cases of E. coli O157:H7 infection in children who had consumed raw cow milk or raw cow colostrum produced by the same dairy were identified during the following 3 weeks. In California, intrastate sale of raw milk and raw colostrum is legal and regulated. This report summarizes the investigation of these cases by CDPH, the California Department of Food and Agriculture (CDFA), and four local health departments and subsequent actions to prevent illnesses. As a result of this and other outbreaks, California enacted legislation (AB 1735), which took effect January 1, 2008, setting a limit of 10 coliforms/mL for raw milk sold to consumers. Raw milk in several forms, including colostrum, remains a vehicle of serious enteric infections, even if the sale of raw milk is regulated.

In mid-September 2006, the parent of one of the two children hospitalized with HUS notified CDFA that both children had consumed raw skim milk from dairy A in the days before illness onset. CDFA notified CDPH and the local health departments of the reports. Dairy A, a licensed raw milk dairy, sells raw milk, raw cream, raw butter, raw cheese, raw colostrum,* and kefir throughout California at retail stores and nationwide via Internet sales, all under a single brand (brand A).

On September 21, 2006, based on the reports from CDPH, CDFA issued a recall and quarantine order for all raw milk, raw cream, and raw colostrum produced by dairy A. The order was extended on September 22 to include all raw products from dairy A, except for cheeses aged at least 60 days according to California and Food and Drug Administration (FDA) standards. Dairy A also was placed under a separate restriction by CDFA during September 21--29 that prevented it from bottling fluid milk and cream because of persistent high standard plate counts.

For this investigation, a case was defined as illness with an onset date of August 1, 2006, or later in a California resident with 1) culture-confirmed E. coli O157:H7 infection with the outbreak strain or 2) HUS with or without culture confirmation, and exposure to raw milk. Case finding was conducted by notifying all California local health departments and infection-control practitioners and reviewing molecular subtyping results from the CDPH Microbial Diseases Laboratory. The 61 health jurisdictions in California were notified on September 20, 2006, to be alert for cases of E. coli O157:H7 and other Shiga toxin-producing E. coli associated with consumption of raw milk. They were asked to report immediately to CDPH any enteric illnesses associated with raw milk or colostrum consumption.

Six cases were identified; four persons had culture-confirmed infections, one had a culture-confirmed infection and HUS, and one had HUS only. The median age of patients was 8 years (range: 6--18 years), and four of the patients (67%) were boys. The six cases identified during this investigation were geographically dispersed throughout California. All six patients reported bloody diarrhea; three (50%) were hospitalized. Illness onset occurred during September 6--24, 2006. Isolates from the five patients with culture-confirmed infections had indistinguishable pulsed-field gel electrophoresis (PFGE) patterns. The PFGE pattern was new to the PulseNet (the National Molecular Subtyping Network for Foodborne Disease) database and differed markedly from the pattern of the E. coli O157:H7 strain associated with a concurrent multistate outbreak linked to spinach consumption (1). Four of the five E. coli O157:H7 isolates were subtyped by multiple-locus variable-number tandem repeat analysis (MLVA) according to a protocol used by CDPH laboratory and were found to have closely related MLVA patterns (2).

Five of six patients reported they had consumed brand A raw dairy products in the week before their illness onset; the sixth patient denied drinking brand A raw milk, although his family routinely purchased it. Among the five patients who consumed brand A dairy products, two consumed raw whole milk, two consumed raw skim milk, and one consumed raw chocolate-flavored colostrum. Four of the five patients routinely drank raw milk from dairy A. One patient was exposed to brand A dairy product only once; he was served raw chocolate colostrum as a snack when visiting a friend. No other food item was commonly consumed by all six patients. No other illness was reported among household members who consumed brand A dairy products.

To assess the level of exposure to raw dairy products among patients with E. coli O157:H7 infection, CDPH epidemiologists reviewed exposure histories for the 50 most recent E. coli O157:H7 cases reported to CDPH during 2004--2006. Among patients who had been asked about exposure to raw milk on the case report, only one of 47 (2%) had consumed raw milk in the week before illness onset. Exposure to raw milk was similarly low (3%) among Californians who responded to a population survey (3).

Environmental Investigation

Using purchase information supplied by the patients' families, investigators determined that the patients consumed raw milk from lots produced at dairy A during September 3--13, 2006. Milk samples from these production dates were not available for testing. Fifty-six product samples from several lots with code dates of September 17, 2006, or later were retrieved from retails stores and dairy A and were tested for aerobic microflora, total coliform, fecal coliform, and E. coli O157:H7. The outbreak strain of E. coli O157:H7 was not found in any product samples. However, standard aerobic plate counts and coliform counts of collected samples with code dates of September 17 through October 9, 2006, were indicative of contamination (Table). Colostrum samples had high standard plate counts and total coliform counts, and fecal coliform counts of 210--46,000 MPN/g. California standards limit standard plate counts for raw and pasteurized milk to 15,000 CFU/mL and total coliform counts for pasteurized milk to 10 coliform bacteria/mL. At the time of this outbreak, California did not have a coliform standard for milk sold raw to consumers. California also classifies colostrum as a dietary supplement, for which it has no microbiologic standards, rather than a milk product.

CDFA and CDPH conducted an initial inspection and environmental investigation of the milk plant and dairy on September 26. E. coli O157:H7 was not isolated from any of four environmental samples. Samples from three heifers yielded E. coli O157:H7, but the PFGE and MLVA patterns of these E. coli O157:H7 isolates differed from the outbreak pattern.

Reported by: J Schneider, MPH, J Mohle-Boetani, MD, D Vugia, MD, California Dept of Public Health. M Menon, MD, EIS officer, CDC.

Editorial Note:

Raw cow milk and raw milk products have been implicated in the transmission of multiple bacterial pathogens, including Campylobacter spp., Brucella, Listeria monocytogenes, Salmonella spp., and E. coli. In a recent review of E. coli O157 infections, raw milk products accounted for 4% of outbreaks during a 20-year period (4). E. coli O157:H7 is responsible for an estimated 73,000 cases of illness annually, and serious sequelae, including HUS and death (5). Children, older adults, and persons with low levels of gastric acid are particularly vulnerable (6).

Raw milk products tested from dairy A were not produced during the same time as the products consumed by the patients in this outbreak. Although the outbreak strain of E. coli O157 was not isolated from dairy A products, the tested products did have high standard plate counts, many exceeding California standards for raw milk, and total coliform counts that exceeded California standards for pasteurized milk. Nonoutbreak strains of E. coli O157 also were isolated from samples from dairy A cows, indicating shedding of this pathogen in the herd. Raw milk from dairy A was the likely vehicle of transmission, but the exact mode of milk contamination in this outbreak was not determined. Asymptomatic cows can harbor pathogens and cause human illness by shedding pathogens in untreated milk or milk products. These findings suggest that if raw milk had been subject to the same coliform standard as pasteurized milk in California, milk from dairy A might have been excluded from sale and this outbreak might have been averted.

FDA mandates that all milk and milk products for direct human consumption be pasteurized in final package form if they are to be shipped for interstate sale (7). States regulate milk shipped within their state. Currently, 21 states require pasteurization of all milk products for sale. However, 25 states, including California, allow raw milk to be sold in some form to the public. Those states that permit the sale and consumption of raw milk report more outbreaks of foodborne disease attributed to raw milk than those states that have stricter regulations. During 1973--1992, raw milk was implicated in 46 reported outbreaks. Nearly 90% of these outbreaks (40 out of 46) occurred in states that allow the sale of raw milk, suggesting that even the regulated sale of raw milk might not be adequate to prevent associated illnesses (8).

This is the first outbreak reported to CDC in which colostrum has been an implicated food vehicle. This outbreak represents the first time colostrum has been reported to CDC as a form of raw milk consumed by any patients in raw milk--associated outbreak, although information on the type of raw milk is reported inconsistently in outbreak surveillance. Colostrum is purported to have increased concentrations of nutrients and protective antibodies and is marketed as a dietary supplement in California; consequently, it is regulated by the CDPH Food and Drug Branch. The colostrum products tested in this investigation were nearly as contaminated as other forms of raw milk tested; therefore, in this outbreak, the risk for human illness from consuming either product was probably similar. Exemption of colostrum from state dairy regulations is not supported by the findings in this outbreak investigation.

From 1998 to May 2005, raw milk or raw milk products have been implicated in 45 foodborne illness outbreaks in the United States, accounting for more than 1,000 cases of illness (CDC, unpublished data, 2007). Because illnesses associated with raw milk continue to occur, additional efforts are needed to educate consumers and dairy farmers about illnesses associated with raw milk and raw colostrum. To reduce the risk for E. coli O157 and other infections, consumers should not drink raw milk or raw milk products.

Acknowledgments

This report is based, in part, on data contributed by D Buglino, MPH, K Smith-Sayer, Nevada County Public Health Dept; S Fortino, Riverside County Dept of Public Health; J Van Meter, MPH, County of San Diego Health and Human Svcs Administration; E Frykman, MD, San Bernardino County Dept of Public Health; L Crawford-Miksza, PhD, C Myers, S Himathongkham, DVM, M Palumbo, PhD, J Atwell, T Chang, D Csuti, S Fontanoz, Y Gerbremichael, J Glover, DVM, J O'Connell, B Sun, DVM, C Wheeler, MD, Y Zhao, California Dept of Public Health; California Dept of Food and Agriculture; and M Lynch, MD, Div of Foodborne, Bacterial, and Mycotic Diseases, CDC.

References

  1. CDC. Ongoing multistate outbreak of Escherichia coli serotype O157:H7 infections associated with consumption of fresh spinach---United States, September 2006. MMWR 2006;55:1045--6.
  2. Hyytiä-Trees E, Smole SC, Fields PA, Swaminathan B, Ribot EM. Second generation subtyping: a proposed PulseNet protocol for multiple-locus variable-number tandem repeat analysis of Shiga toxin-producing Escherichia coli O157 (STEC O157). Foodborne Pathog Dis 2006;3:118--31.
  3. CDC. Foodborne diseases active surveillance network (FoodNet): population survey atlas of exposures, 2002. Atlanta, GA: US Department of Health and Human Services, CDC; 2004:205. Available at http://www.cdc.gov/foodnet/surveys/pop/2002/2002atlas.pdf.
  4. Rangel JM, Sparling PH, Crowe C, Griffin PM, Swerdlow DL. Epidemiology of Escherichia coli O157:H7 outbreaks, United States, 1982--2002. Emerg Infect Dis 2005;11:603--9.
  5. Mead PS, Slutsker L, Dietz V, et al. Food-related illness and death in the United States. Emerg Infect Dis 1999;5:607--25.
  6. Dundas S, Todd WT, Stewart AI, et al. The central Scotland Escherichia coli O157:H7 outbreak: risk factors for the hemolytic uremic syndrome and death among hospitalized patients. Clin Infect Dis 2001;33:923--31.
  7. Food and Drug Administration. Grade "A" pasteurized milk ordinance: 2003 revision. Rockville, MD: US Department of Health and Human Services; 2004. Available at http://www.cfsan.fda.gov/~ear/pmo03toc.html.
  8. Headrick ML, Korangy S, Bean NH, et al. The epidemiology of raw milk-associated foodborne disease outbreaks reported in the United States, 1973 through 1992. Am J Public Health 1998;88:1219--21.

* Raw colostrum is secreted during the first few days after giving birth. It contains higher amounts of protein and antibodies than regular raw milk, but is processed in the same way as raw milk.

The 60-day curing process has historically been considered sufficient to eliminate or reduce pathogens that were in the milk; however, its efficacy has been questioned, and FDA is reviewing the safety of raw milk cheeses.

Table

TABLE. Microbial testing results for dairy A raw milk product samples with code dates of September 17 through October 9, 2006  California Standard plate counts Coliform counts
>15,000
>250,000
>10
>1,500
CFU/mL
CFU/mL
coliforms/mL coliforms/mL
Range
Product sample
(n)
(n)
Range (CFU/mL)
(n)
(n)
(coliforms/mL)
Raw skim milk (n = 13)
11
11
2,900 to >10,000,000
12
9
75 to >10,000
Raw whole milk (n = 18)
13
11
1,800 to >9,000,000
15
4
0 to >10,000
Raw colostrum (n = 4)
4
4
2,000,000 to >8,000,000
4
2
110 to >10,000
Raw chocolate colostrum (n = 3)
3
3
263,000 to 1,200,000
3
2
98 to >20,000
Raw cream (n = 11)
9
7
1,800 to 12,000,000
10
6
39 to 6,200
Raw kefir (n = 3)
3
3
320,000 to 9,000,000
3
0
12 to 270
Raw butter (n = 4)
3
2
110,000 to >4,000,000
4
3
110 to >3,300
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Date last reviewed: 6/11/2008

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