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

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

• Michael Doyle

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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

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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 Health
Pathogen Year No. of cases/100,000 persons Objective for 2010

Campylobacter 2000 15.7
2001 13.8
2002 13.4
2003 12.6
2004 12.9
2005 12.9
2006 12.7 12.3

Salmonella 2000 14.4
2001 15.1
2002 16.1
2003 14.5
2004 14.7
2005 14.6
2006 14.8 6.8

U.S. Centers for Disease Control and Prevention U.S. Centers for Disease Control and Prevention U.S. Centers for Disease Control and Prevention U.S. Centers for Disease Control and Prevention
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Risk Factors for Sporadic Salmonella Enteritidis Infections in the United States (2002 2003) Risk Factors for Sporadic Salmonella Enteritidis Infections in the United States (2002 2003) Risk Factors for Sporadic Salmonella Enteritidis Infections in the United States (2002 2003)

Risk Factors Identified Population Attributable Fraction Population Attributable Fraction

Eating chicken outside the home Eating chicken outside the home 35
International travel International travel 30
Eating undercooked eggs inside the home Eating undercooked eggs inside the home 15
Lizard in the home Lizard in the home 7
Bird in the home Bird in the home 5
Eating eggs outside the home Eating eggs outside the home 5

R. Marcus et al. Epidemiol. Infect. 2006 R. Marcus et al. Epidemiol. Infect. 2006 R. Marcus et al. Epidemiol. Infect. 2006

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Selected case-control studies demonstrating risk of acquiring salmonellosis from food prepared outside the home Selected case-control studies demonstrating risk of acquiring salmonellosis from food prepared outside the home 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. 431324 (2006) T. F. Jones and F. J. Angulo, Clin. Infect. Dis. 431324 (2006) T. F. Jones and F. J. Angulo, Clin. Infect. Dis. 431324 (2006)
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Prevalence of Salmonella in Meat and Poultry
Determined by USDA-FSIS Pathogen Reduction/HACCP
Verification Testing Program
Calendar Year Broiler Carcasses Broiler Carcasses Ground Chicken Ground Turkey Steer Heifer Carcasses Bull Cow Carcasses Ground Beef Hog Carcasses
( Positive) ( Positive) ( Positive) ( Positive) ( Positive) ( Positive) ( Positive)
Baseline Baseline
(Pre-1998) (Pre-1998) 20 44.6 49.9 1.0 2.7 7.5 8.7
1998 1998 10.8 4.2 36.5 0 1.1 6.4 5.8
1999 1999 11.4 16.2 31.6 0.3 2.2 4.3 9.8
2000 2000 9.1 13.8 25.7 0.4 2.2 3.3 6.2
2001 2001 11.9 19.5 26.2 0.6 2.4 2.8 3.8
2002 2002 11.5 29.1 17.9 0.3 1.7 2.6 3.2
2003 2003 12.8 35.5 25.4 0.4 1.5 1.7 2.5
2004 2004 13.5 25.5 19.9 0.3 0.8 1.6 3.1
2005 2005 16.3 32.4 23.2 0.6 1.3 1.1 3.7
2006 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) USDA-FSIS (http//www.fsis.usda.gov/OPHS/haccp/salm6year.htm) USDA-FSIS (http//www.fsis.usda.gov/OPHS/haccp/salm6year.htm) USDA-FSIS (http//www.fsis.usda.gov/OPHS/haccp/salm6year.htm) USDA-FSIS (http//www.fsis.usda.gov/OPHS/haccp/salm6year.htm) USDA-FSIS (http//www.fsis.usda.gov/OPHS/haccp/salm6year.htm) USDA-FSIS (http//www.fsis.usda.gov/OPHS/haccp/salm6year.htm) USDA-FSIS (http//www.fsis.usda.gov/OPHS/haccp/salm6year.htm) USDA-FSIS (http//www.fsis.usda.gov/OPHS/haccp/salm6year.htm)
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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 lt 4.5 (acid
  shock) triggers acid tolerance response
• Cells can survive in extreme acidic environments
  (pH 3 - 4)

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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

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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

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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

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Human infectious dose of Salmonella Human infectious dose of Salmonella Human infectious dose of Salmonella
Food 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 lt 4.6 X 102
Ice Cream Enteritidis lt 2.8 X 101
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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

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Examples of Major Outbreaks of Salmonellosis Associated with Chocolate-based Products Examples of Major Outbreaks of Salmonellosis Associated with Chocolate-based Products Examples of Major Outbreaks of Salmonellosis Associated with Chocolate-based Products 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 gt439
2006 United Kingdom Montevideo gt 50
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Contributing factor to Chocolate-associated
outbreaks of salmonellosis

• Contamination of chocolate during processing via
  leaking pipe/contaminated water

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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

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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

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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)

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Salmonellosis from Raw Almonds

• Almonds are Californias 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

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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. 122385
  (1999)

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Examples of Outbreaks of Salmonellosis Associated with Tomatoes Examples of Outbreaks of Salmonellosis Associated with Tomatoes Examples of Outbreaks of Salmonellosis Associated with Tomatoes Examples of Outbreaks of Salmonellosis Associated with Tomatoes 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
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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. 40549, 1991

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Examples of Salmonellosis Outbreaks Associated with Cantaloupes Examples of Salmonellosis Outbreaks Associated with Cantaloupes Examples of Salmonellosis Outbreaks Associated with Cantaloupes Examples of Salmonellosis Outbreaks Associated with Cantaloupes 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 gt 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
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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. 67713-720
  (2004)

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Salmonella Contamination during Cantaloupe
Production

• Salmonella isolated from

Texas Mexico
Cantaloupes at melon farm Cantaloupes at melon farm Cantaloupes at melon farm
Field Field 1/400 (0.2) 1/400 (0.2) 0/75
Before wash Before wash 1/150 (0.6) 1/150 (0.6) 0/75
After wash After wash 1/150 (0.6) 1/150 (0.6) 1/75 (1.3)
In cooler In cooler 2/250 (0.8) 2/250 (0.8) 0/75

Irrigation water (at source) Irrigation water (at source) Irrigation water (at source) 9/70 (13) 9/70 (13) 4/15 (27)
After filtration After filtration 0/5 0/5 5/15 (33)
As delivered to field As delivered to field 2/25 (8) 2/25 (8) 1/15 (7)
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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

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

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Examples of Salmonellosis Outbreaks Associated with Sprout Consumption Examples of Salmonellosis Outbreaks Associated with Sprout Consumption Examples of Salmonellosis Outbreaks Associated with Sprout Consumption Examples of Salmonellosis Outbreaks Associated with Sprout Consumption 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 gt500
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 gt 9
2007 Alfalfa S. Weltevreden Norway 10
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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

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Microbiological Safety Issues Associated with
Imported Foods

• Sanitation practices for food production and
  preparation are not universally equivalent
  throughout the world

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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

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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

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Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007 Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007 Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007 Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007 Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007


Country Country Product Product


China China Shrimp Harvested in India then sent to China Shrimp Harvested in India then sent to China
China China Chives Chives
China China Whole Black Peppercorns Whole Black Peppercorns
China China Dog Chicken Strips Dog Chicken Strips
Egypt Egypt Basil Basil
Egypt Egypt Fennel Fennel
India India Frozen Ginger Frozen Ginger
India India Frozen Fish Chunks in Tray Frozen Fish Chunks in Tray
India India Black Pepper Black Pepper
India India Cumin Cumin

(Continued) (Continued)
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Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007 (Continued) Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007 (Continued) Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007 (Continued) Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007 (Continued) Examples of FDA Food Import Refusals for Salmonella Contamination for August 2007 (Continued)


Country Country Product Product


Indonesia Indonesia Cinnamon Cinnamon
Indonesia Indonesia Frozen Grouper Fillets Frozen Grouper Fillets
Malaysia Malaysia Frozen Shrimp Frozen Shrimp
Mexico Mexico Dry Hard Cheese Dry Hard Cheese
Pakistan Pakistan Coriander Powder Coriander Powder
Philippines Philippines Frozen Octopus Frozen Octopus
Philippines Philippines Dried Taro Leaves Dried Taro Leaves
Thailand Thailand Shrimp Prawns Shrimp Prawns
Vietnam Vietnam Frozen Grouper Frozen Grouper
Vietnam Vietnam Ground Black Pepper Ground Black Pepper


FDA Import Program (www.fda.gov/ora/import/ora_import_program.html) FDA Import Program (www.fda.gov/ora/import/ora_import_program.html) FDA Import Program (www.fda.gov/ora/import/ora_import_program.html) FDA Import Program (www.fda.gov/ora/import/ora_import_program.html) FDA Import Program (www.fda.gov/ora/import/ora_import_program.html)
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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

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Conclusions

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

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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

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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

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Conclusions

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