The Versatile Salmonella : Contaminating Cantaloupes, Peanut Butter, Chocolate and Sprouts

1. The Versatile Salmonella: Contaminating Cantaloupes, Peanut Butter, Chocolate and Sprouts Michael Doyle

2. 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

4. Incidence of cases of Campylobacter, Salmonella, and Escherichia coli O157 infections under surveillance in the Foodborne Diseases Active Surveillance Network (Food Net), 2000 - 2006

7. Prevalence of Salmonella in Meat and Poultry Determined by USDA-FSIS Pathogen Reduction/HACCP Verification Testing Program

8. 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)

9. 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

10. 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

11. 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

13. 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

15. Contributing factor to Chocolate-associated outbreaks of salmonellosis • Contamination of chocolate during processing via leaking pipe/contaminated water

16. 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

17. 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

18. 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)

19. 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

20. 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)

22. 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

24. 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)

25. Salmonella Contamination during Cantaloupe Production • Salmonella isolated from:

26. 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

27. What Food Is Considered by Many Food Safety Experts to be the Most Hazardous?

29. 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

30. Microbiological Safety Issues Associated with Imported Foods • Sanitation practices for food production and preparation are not universally equivalent throughout the world

31. 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

33. 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

36. 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

37. Conclusions • Substantial progress has been made in reducing Salmonella contamination of meat products but not ground poultry products

38. 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

39. 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

40. Conclusions • Need for renewed emphasis by food industry to prevent and control Salmonella contamination from farm to plate