the versatile salmonella: contaminating cantaloupes, peanut butter, chocolate and sprouts michael...
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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
National HealthPathogen Year No. of cases/100,000 persons Objective for 2010
Campylobacter 2000 15.72001 13.82002 13.42003 12.62004 12.92005 12.92006 12.7 12.3
Salmonella 2000 14.42001 15.12002 16.12003 14.52004 14.72005 14.6 2006 14.8 6.8
U.S. Centers for Disease Control and Prevention
Risk Factors for Sporadic Salmonella Enteritidis Infections in the United States (2002 – 2003)
Risk Factors Identified Population Attributable Fraction
Eating chicken outside the home 35%
International travel 30%
Eating undercooked eggs inside the home
15%
Lizard in the home 7%
Bird in the home 5%
Eating eggs outside the home 5%
R. Marcus et al. Epidemiol. Infect. 2006
Selected case-control studies demonstrating risk of acquiring salmonellosis from food prepared outside the home
Salmonella Serotype Risk factor Population Attributable Risk
MDR Typhimurium Eating scrambled eggs prepared outside the home
13%
Heidelberg Eating eggs prepared outside the home
39%
Serogroup B or C Eating eggs prepared in a restaurant
9%
T. F. Jones and F. J. Angulo, Clin. Infect. Dis. 43:1324 (2006)
Prevalence of Salmonella in Meat and Poultry Determined by USDA-FSIS Pathogen Reduction/HACCP Verification Testing Program
Calendar Year
Broiler Carcasses
Ground Chicken
Ground Turkey
Steer & Heifer Carcasses
Bull & Cow Carcasses
Ground Beef
Hog Carcasse
s
(% Positive)
Baseline
(Pre-1998) 20 44.6 49.9 1.0 2.7 7.5 8.7
1998 10.8 4.2 36.5 0 1.1 6.4 5.8
1999 11.4 16.2 31.6 0.3 2.2 4.3 9.8
2000 9.1 13.8 25.7 0.4 2.2 3.3 6.2
2001 11.9 19.5 26.2 0.6 2.4 2.8 3.8
2002 11.5 29.1 17.9 0.3 1.7 2.6 3.2
2003 12.8 35.5 25.4 0.4 1.5 1.7 2.5
2004 13.5 25.5 19.9 0.3 0.8 1.6 3.1
2005 16.3 32.4 23.2 0.6 1.3 1.1 3.7
2006 11.4 45.0 20.3 0.3 0.8 2.0 4.0
USDA-FSIS (http://www.fsis.usda.gov/OPHS/haccp/salm6year.htm)
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
Human infectious dose of SalmonellaFood Serovar Infectious Dose (CFU)
Eggnog Meleagridis 104 – 107
Anatum 105 – 107
Imitation Ice Cream Typhimurium 104
Chocolate Eastbourne 102
Hamburger Newport 101 – 102
Cheddar Cheese Heidelberg 102
Chocolate Napoli 101 – 102
Cheddar Cheese Typhimurium 100 – 101
Chocolate Typhimurium ≤ 101
Alfalfa Sprouts Newport < 4.6 X 102
Ice Cream Enteritidis < 2.8 X 101
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
Examples of Major Outbreaks of Salmonellosis Associated with Chocolate-based Products
Year Country Salmonella serovar No. of Cases
1973 Canada and USA Eastbourne 217
1982 England and Wales Napoli 245
1987 Norway and Finland Typhimurium 361
2000-2001 Germany & International Oranienburg >439
2006 United Kingdom Montevideo > 50
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)
Examples of Outbreaks of Salmonellosis Associated with Tomatoes
Date Pathogen Location
No. of Cases
Likely Source of Contamination
1990 S. Javiana Multistate 176 Packinghouse
1993 S. Montevideo Multistate 100 Packinghouse
1998-99 S. Bailden Multistate 85 Field Contamination
2002 S. Newport 24 States 512 Packinghouse
2004 Multiserotypes Salmonella
Multistate 564 Packinghouse
2005 S. Newport Multistate 72 Field Contamination (Irrigation Pond)
2005 S. Braenderup Multistate 82 Field Contamination
2006 S. Newport Multistate 115 Not Determined
2006 S. Typhimurium Multistate 190 Packinghouse
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
Examples of Salmonellosis Outbreaks Associated with Cantaloupes
Year Type of Melon Pathogen Location No. of Cases
1989-90 Cantaloupe S. Chester Multistate 245
1991 Cantaloupe S. Poona Multistate > 400
1997 Cantaloupe S. Saphra California 24
1998 Cantaloupe S. Oranienburg Canada 22
2000 Cantaloupe S. Poona Multistate 47
2001 Cantaloupe S. Poona Multistate 50
2002 Cantaloupe S. Poona Multistate, Canada 58
2006 Fruit salad; cantaloupe; honeydew
S. Oranienburg 10 States, Canada 41
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:
Texas Mexico
– Cantaloupes at melon farm
Field 1/400 (0.2%) 0/75
Before wash 1/150 (0.6%) 0/75
After wash 1/150 (0.6%) 1/75 (1.3%)
In cooler 2/250 (0.8%) 0/75
– Irrigation water (at source) 9/70 (13%) 4/15 (27%)
After filtration 0/5 5/15 (33%)
As delivered to field 2/25 (8%) 1/15 (7%)
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?
Examples of Salmonellosis Outbreaks Associated with Sprout Consumption
Sprout No. of
Date Type Pathogen Location Cases
1988 Bean Salmonella Saint-Paul UK 143
1994 Alfalfa S. Bovismordificans Sweden 282
Finland 210
1995 Alfalfa S. Newport Oregon 58
British Columbia 70
1995 Alfalfa S. Newport Denmark 154
1995 Alfalfa S. Stanley Multistate, Finland 242
1996 Alfalfa S. Montevideo, S. Meleagridis California >500
1997 Alfalfa S. Infantis, S. Anatum Kansas, Missouri 109
1998 Alfalfa S. Havana, S. Cubana, S. Tennessee California 34
1999 Sprouts Salmonella Colorado 79
1999 Alfalfa S. Paratyphi B Canada 51
2000 Mung Bean S. Enteritidis California 45
2001 Mung Bean S. Enteritidis Canada 85
2001 Alfalfa S. Kottbus Washington 23
2003 Alfalfa Salmonella Oregon > 9
2007 Alfalfa S. Weltevreden Norway 10
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
Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007
Country Product
China Shrimp Harvested in India then sent to ChinaChina ChivesChina Whole Black PeppercornsChina Dog Chicken StripsEgypt BasilEgypt FennelIndia Frozen GingerIndia Frozen Fish Chunks in TrayIndia Black PepperIndia Cumin
(Continued)
Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007 (Continued)
Country Product
Indonesia CinnamonIndonesia Frozen Grouper FilletsMalaysia Frozen ShrimpMexico Dry Hard CheesePakistan Coriander PowderPhilippines Frozen OctopusPhilippines Dried Taro LeavesThailand Shrimp & PrawnsVietnam Frozen GrouperVietnam Ground Black Pepper
FDA Import Program (www.fda.gov/ora/import/ora_import_program.html)
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
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