Transcript Virulence of Foodborne Pathogens

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
Pathogen
Year
Campylobacter
2000
2001
2002
2003
2004
2005
2006
15.7
13.8
13.4
12.6
12.9
12.9
12.7
12.3
2000
2001
2002
2003
2004
2005
2006
14.4
15.1
16.1
14.5
14.7
14.6
14.8
6.8
Salmonella
No. of cases/100,000 persons
National Health
Objective for 2010
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
T. F. Jones and F. J. Angulo, Clin. Infect. Dis. 43:1324 (2006)
9%
Prevalence of Salmonella in Meat and Poultry Determined by USDAFSIS Pathogen Reduction/HACCP Verification Testing Program
Calendar
Year
Broiler
Carcasses
Ground
Chicken
Ground
Turkey
Steer & Heifer
Carcasses
Bull & Cow
Carcasses
Ground
Beef
Hog
Carcasses
(% 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 Salmonella
Food
Serovar
Infectious Dose (CFU)
Eggnog
Meleagridis
104 – 107
Anatum
105 – 107
Imitation Ice Cream
Typhimurium
104
Chocolate
Eastbourne
102
Hamburger
Newport
Cheddar Cheese
Heidelberg
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
101 – 102
102
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 Chocolatebased Products
Year
Country
Salmonella serovar
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
Montevideo
> 50
United Kingdom
No. of Cases
Contributing factor to Chocolateassociated 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 sucrosecontaining 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 Californiagrown 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
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
Field Contamination
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
9/70 (13%)
4/15 (27%)
After filtration
0/5
5/15 (33%)
As delivered to field
2/25 (8%)
1/15 (7%)
Irrigation water (at source)
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
Date Type
Pathogen
Location
1988 Bean
Salmonella Saint-Paul
UK
1994 Alfalfa
S. Bovismordificans
Sweden
Finland
1995 Alfalfa
S. Newport
Oregon
British Columbia
1995 Alfalfa
S. Newport
Denmark
1995 Alfalfa
S. Stanley
Multistate, Finland
1996 Alfalfa
S. Montevideo, S. Meleagridis
California
1997 Alfalfa
S. Infantis, S. Anatum
Kansas, Missouri
1998 Alfalfa
S. Havana, S. Cubana, S. Tennessee
California
1999 Sprouts
Salmonella
Colorado
1999 Alfalfa
S. Paratyphi B
Canada
2000 Mung Bean S. Enteritidis
California
2001 Mung Bean S. Enteritidis
Canada
2001 Alfalfa
S. Kottbus
Washington
2003 Alfalfa
Salmonella
Oregon
2007 Alfalfa
S. Weltevreden
Norway
No. of
Cases
143
282
210
58
70
154
242
>500
109
34
79
51
45
85
23
> 9
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
China
China
China
Egypt
Egypt
India
India
India
India
Shrimp Harvested in India then sent to China
Chives
Whole Black Peppercorns
Dog Chicken Strips
Basil
Fennel
Frozen Ginger
Frozen Fish Chunks in Tray
Black Pepper
Cumin
(Continued)
Examples of FDA Food Import Refusals for Salmonella Contamination
for August 2007 (Continued)
Country
Product
Indonesia
Indonesia
Malaysia
Mexico
Pakistan
Philippines
Philippines
Thailand
Vietnam
Vietnam
Cinnamon
Frozen Grouper Fillets
Frozen Shrimp
Dry Hard Cheese
Coriander Powder
Frozen Octopus
Dried Taro Leaves
Shrimp & Prawns
Frozen Grouper
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