Food Protection Trends - April 2009 - (Page 217) lying disease) showed that illness was strongly associated with consumption of pasteurized whole or 2% milk (OR = 9.0, P < 0.01 for neighborhood-matched study; OR = 11.5, P < 0.001 for illnessmatched study) (47). After inspection of the dairy plant with which the outbreak was associated, neither improper pasteurization nor a source of contamination after pasteurization was identified. As the result of further epidemiologic study, it was determined that this vulnerable population had in fact consumed raw milk that was contaminated after processing (47). Y. enterocolitica O:8 infections have the potential of being transmitted through pasteurized milk because the bacterium is capable of growing under refrigeration (62). In 1976, 38 schoolchildren became ill with yersiniosis after becoming infected by way of contaminated chocolate milk. The bacterium had been introduced into the milk through improper handling of chocolate syrup, which was hand-mixed with pasteurized milk. A large multistate outbreak of this disease also occurred in Tennessee, Arkansas, and Mississippi, where three different case-control studies indicated that milk consumption from a specific plant was statistically associated with illness characterized by enteritis involving fever, diarrhea, and abdominal pain (90). Inspection of the plant did not reveal a source or mechanism of contamination. However, an outbreak of yersiniosis in 10 residents of the Upper Valley of Vermont and New Hampshire was linked to consumption of bottled pasteurized milk (1). The contamination likely occurred when milk bottles were rinsed with untreated well water after they had been handled by workers caring for pigs. S. Typhimurium outbreaks have also been linked to poor pasteurization techniques (12). The largest outbreak of salmonellosis in U.S. history was attributed to two brands of pasteurized 2% milk taken from a single dairy plant in Kentucky; at least sixteen cases of gastroenteritis occurred because of improperly pasteurized milk. People who consumed the milk were approximately six times more likely to develop illness (P = 0.01) than those who did not consume it (26). Unpasteurized soft cheeseassociated outbreaks Unpasteurized milk is preferred by cheese makers because pasteurization can decrease flavor and lengthen the ripening time of cheese (23). However, United States Department of Agriculture regulations require that cheeses made from unpasteurized milk be aged for more than 60 days, as stated in the Standards of Identity in the U.S. Code of Federal Regulations CFR, section 7 CFR 58.439. The FDA permits the manufacture and interstate sale of unpasteurized milk cheeses if they are aged for a minimum of 60 days at a temperature greater than 35°F. Soft cheeses tend to be high in moisture. Unpasteurized soft cheeses implicated in disease outbreaks include Brie, Camembert, Vacherin, and homemade, soft, and unripened cheeses (106). A variety of pathogens have been implicated in outbreaks associated with raw soft cheeses (106). During the cheese-making process, some pathogens are inactivated, depending on the temperature and pH during production and ripening, yet many others survive this aging process. Ripened soft cheeses present a greater risk for growth and survival of microorganisms than do aged hard cheeses (43). The raw milk soft cheeses of greatest concern to public health are “queso fresco” style cheeses, which are typically soft and white and which are often imported from Mexico and Central American countries (5). They are typically made at home, sold door-to-door, illegally imported, or sold in local markets and restaurants. In the U.S., a variety of raw milk cheese-associataed outbreaks have occurred (5). In 1983, sixteen cases of Group C Streptococcal infections in New Mexico were linked to “queso blanco,” a homemade white cheese (5). In North Carolina, in an outbreak of listeriosis associated with homemade Mexican-style cheese, infection of 10 pregnant women with L. monocytogenes resulted in five stillbirths, three premature deliveries, and two infected newborns (87). A case-control study showed that cases had a seven times greater odds of having ingested queso fresco compared to controls (OR = 7.3, 95% CI 1.4 – 37.5) (30). In another case-control study, S. Typhimurium DT104 was also shown to have caused queso fresco-associated illness due to raw milk cheese ingestion, when isolates were drawn from seventynine people (37). Lastly, a comparison of patients with neighborhood controls linked S.Typhimurium with eating raw milk queso fresco in an outbreak in Washington state (matched OR = 32.3, 95% CI 3.0 – 874.6) (95). In France, where many of the world’s raw milk soft cheeses are produced, several outbreaks have occurred. Desenclos and colleagues identified an outbreak in 273 people in France who consumed raw goats’ milk cheese in which the organism implicated was Salmonella enterica serovar paratyphi B (42). Brie de Meaux cheese made from raw cows’ milk was the source of L. monocytogenes infection among 20 people in France; “pregnant women were affected, of whom two suffered spontaneous abortions, two had stillbirths, and five gave birth prematurely (49). A case-control study linked acute hemolytic uremic syndrome that occurred in four children in a French village to a cheese made with unpasteurized mixed cows’ and goats’ milk (P = 0.006) (41). All four patients had fever, diarrhea, acute renal failure, anemia, schistocytosis, and thrombocytopenia (41). Interestingly, a risk assessment performed by Sanaa and colleagues revealed that the predicted probability of contracting severe listeriosis after consumption of both Brie de Meaux cheese and Camembert of Normandy made from raw milk is lower than after consumption of soft cheeses made from pasteurized milk (81, 103). The incidence rate of severe listeriosis after consuming one of these two cheeses was 10-3 per year (81). In 1997, a community-wide outbreak of Salmonella enterica serovar Typhimurium infection secondary to raw milk Morbier cheese consumption occurred in thirty-three of forty cases, compared to 23 of 42 controls matched in age and area of residence (OR = 6.5, 95% CI 1.4 – 28.8) (39). All cases suffered from fever and/or diarrhea during the investigation period. Lastly, a cluster of four cases of bloody diarrhea and hemolytic uremic syndrome in 1994 was traced to consumption of fromage frais made from raw cows’ and goats’ milk (7). An outbreak of Q fever caused by C. burnetii occurred in a psychiatric hospital in southern France among support staff and patients who also worked on a dairy farm near the hospital (46). A serologic survey performed among suspected cases (those with exposure to goats and their unpasteurized dairy products) revealed that 66% had elevated C. burnetii titers. Seropositive rates were significantly higher among persons who had worked on the farm and consumed unpasteurized milk products (69%, 22 of 32, P = 0.007), suspected cases who only had worked on the farm (75%, 9 of 12, P = 0.009), APRIL 2009 | FOOD PROTECTION TRENDS 217
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