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The Versatile Salmonella : Contaminating Cantaloupes, Peanut Butter, Chocolate and Sprouts. Michael Doyle. The Versatile Salmonella. Incidence and trends of salmonellosis in United States Risk factors for acquiring salmonellosis Prevalence and trends of Salmonella in meat and poultry
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The Versatile Salmonella: Contaminating Cantaloupes, Peanut Butter, Chocolate and Sprouts Michael Doyle
The Versatile Salmonella • Incidence and trends of salmonellosis in United States • Risk factors for acquiring salmonellosis • Prevalence and trends of Salmonella in meat and poultry • Survival characteristics of Salmonella • Infectious dose • Food-assisted outbreaks of salmonellosis (other than meat or poultry) • Salmonella contamination of imported foods
Incidence of cases of Campylobacter, Salmonella, and Escherichia coli O157 infections under surveillance in the Foodborne Diseases Active Surveillance Network (Food Net), 2000 - 2006
Prevalence of Salmonella in Meat and Poultry Determined by USDA-FSIS Pathogen Reduction/HACCP Verification Testing Program
Some Salmonella strains have unusual resilience to extreme environmental conditions • Preexposure to adverse environmental conditions can precondition salmonellae to tolerate extreme conditions • Preexposure to sodium chloride in acidic environment can increase tolerance of salmonellae to low concentrations of organic acids • Anaerobic conditions can potentiate greater salt tolerance • Brief exposure of S. Typhimurium cells to mild acidic environments (pH 5.5 - 6.0) followed by exposure of adapted cells to pH < 4.5 (acid shock) triggers acid tolerance response • Cells can survive in extreme acidic environments (pH 3 - 4)
Acid stress can trigger enhanced resistance of salmonellae to other adverse environmental conditions • Growth of S. Typhimurium at pH 5.8 engendered: • increased thermal tolerance at 50ºC; • enhanced thermal tolerance to high osmotic stress (2.5 M NaCl) • increased resistance to the antibacterial lactoperoxidase system and surface active agents such as polymyxin B
Salmonella can persist in hostile environments • Heat resistance increases with decreased moisture content/water activity • Acquires greater heat resistance following exposure to sublethal temperatures • Synthesizes heat shock proteins • S. infantis can grow in tomatoes at pH 4.0
Infectious dose of Salmonella • Newborns, infants, the elderly and immunocompromised individuals are more susceptible to Salmonella infections than healthy adults • Incompletely developed immune system in newborns or infants • Weak or delayed immune response in the elderly and debilitated persons • Low gastric acid production in infants and seniors
High fat content of food influences infectious dose • High fat content of chocolate (cocoa butter), cheese (milk fat), and meat (animal fat) is common factor among foods associated with low infectious dose • Suggested that entrapment of salmonellae within hydrophobic lipid micelles affords protection against the bactericidal action of gastric acidity • Rapid emptying of gastric contents could also provide alternate mechanism
Contributing factor to Chocolate-associated outbreaks of salmonellosis • Contamination of chocolate during processing via leaking pipe/contaminated water
Salmonella Survival in a Chocolate Confectionary Product • Thermal inactivation of salmonellae in molten chocolate is not practically possible because the time-temperature conditions required to kill the pathogen in this high sucrose-containing product of low water activity would result in organoleptically unacceptable product • Salmonellae can survive for many years in finished chocolate products when stored at ambient temperature • Effective decontamination of raw cocoa beans and stringent in-plant control measures to prevent cross-contamination of products are critical
Salmonella Tennessee Outbreak Associated with Peanut Butter • From August 2006 – May 2007, 628 persons in 47 states were infected with S. Tennessee • Vehicle was two brands of peanut butter made by same manufacturer at same processing facility • Source of contamination was a leaky roof over area after peanut roasting Centers for Disease Control and Prevention, June 1, 2007
Salmonellosis from Raw Almonds • In 2003 – 2004, 29 cases of Salmonella Enteritidis infections in 12 states and Canada from California-grown raw almonds • 13 million pounds of raw almonds recalled • In 2001, outbreak of S. Enteritidis infections, mostly in Canada, during 6-month period • Traced to 3 CA orchards MMWR 53(22):484-487 (June 11, 2004)
Salmonellosis from Raw Almonds • Almonds are California’s largest agricultural crop ($1.5 billion annually) • 1 billion pounds produced in 2003 • 5% of almonds consumed in US are raw • Harvesting, drying and hulling-shelling practices enable cross contamination • Salmonella isolated for many months from soil of almond orchards; almonds that contact soil can be contaminated • Almonds can be pasteurized with heat, steam or propylene oxide to reduce risk of contamination
Examples of Outbreaks of Salmonellosis Associated with Tomatoes • Two multistate (midwest) outbreaks of salmonellosis identified by laboratory-based surveillance • In 1990, 176 cases of S. Javiana • In 1993, 100 cases of S. Montevideo • Source: Tomatoes from a single South Carolina tomato packer • Contamination likely occurred at packing shed • Field-grown tomatoes dumped into common water bath • Tomatoes placed in water cooler then tomato pulp absorb water and salmonellae into core tissues through stem scar C. W. Hedberg et al. Epidemiol. Infect. 122:385 (1999)
Salmonellosis Outbreak Associated with Cantaloupes • More than 400 cases of Salmonella Poona infection in 23 states and Canada during June-July 1991 • Vehicle – cantaloupe • Likely source of cantaloupe was Rio Grande region of Texas • Implicated cantaloupe associated with fruit salads from salad bars • FDA survey of imported cantaloupes and watermelons at U.S. border in 1990 and 1991 isolated Salmonella spp. from about 1% of rinds Morbid. Mortal. Weekly Rep. 40:549, 1991
Salmonella Contamination during Cantaloupe Production • 6 cantaloupe farms and packing plants in South Texas and 3 farms in Colima State, Mexico were sampled to evaluate Salmonella contamination of cantaloupe during production and processing • Sampled cantaloupe surface and irrigation water • E. coli detected on 3.9% of melons from Texas and 25.7% from Mexico A. Castillo et al. J. Food Protect. 67:713-720 (2004)
Salmonella Contamination during Cantaloupe Production • Salmonella isolated from:
Salmonella Associated with Cantaloupes • Reported outbreaks have been associated both with whole melons contaminated in growing fields and with precut melons • Disinfection of irregular surface of cantaloupes is difficult • Cut fruit can be contaminated when rind is removed and fruit is sliced • Inner flesh of melons contains nutrients that support microbial growth; improper refrigeration of cut melon can cause Salmonella growth
What Food Is Considered by Many Food Safety Experts to be the Most Hazardous?
FDA Warning Regarding Sprout Consumption • July 9, 1999 consumer advisory by U.S. Food and Drug Administration • All consumers (not just those at highest risk of foodborne illness) can reduce the risk of foodborne illness by cooking sprouts or completely avoiding consumption of sprouts • FDA believes that all sprouts (not only alfalfa or clover sprouts) may pose a risk
Microbiological Safety Issues Associated with Imported Foods • Sanitation practices for food production and preparation are not universally equivalent throughout the world
Chicken/Shrimp Farming in Thailand • Chicken/shrimp farming is only means of income for many small stakeholders • Chicken coops (e.g., 20,000 birds/farm) sit in rows suspended over ponds that hold shrimp and fish • Livestock below feeds on waste from above BBC News, January 27, 2004
Food Safety Issues with Imported Fishery/Seafood Products • Salmonella is the most common contaminant of fish and fishery products resulting in detention by FDA • In 2001, of 6,405 violations 28.6% were for adulteration by Salmonella • More than half of violations for Salmonella were for contaminated shrimp and prawns J. Allhouse et al., USDA, ERS, International Trade and Seafood Safety, AER-828, p. 109-124, Nov 2003
Conclusions • Salmonella spp. is the leading cause of foodborne bacterial disease in the United States • There has been minimal progress in reducing the incidence of salmonellosis during the past decade
Conclusions • Substantial progress has been made in reducing Salmonella contamination of meat products but not ground poultry products
Conclusions • Eggs and poultry are major vehicles of Salmonella infections, however, many other foods, including fresh produce and occasionally some RTE products are also important contributors • Many imported foods are vehicles of Salmonella because they are produced or processed under unsanitary conditions
Conclusions • Many strains of Salmonella are unusually resilient to extreme environmental conditions • Preexposure to sodium chloride or acid increase tolerance to acid • Heat resistance increases with decreased moisture content • Salmonella can persist for months to years in soil and in dry locations in food processing facilities
Conclusions • Need for renewed emphasis by food industry to prevent and control Salmonella contamination from farm to plate