What We Can Learn from
the Role of the Food
Worker in Outbreaks
Ewen C. D. Todd
Advertising, Public Relations and
Retailing
Michigan State University
Train the Trainer Workshop at the International
Food Safety Conference
Dubai, February 2009
What Have We Learned from
Investigation of Outbreaks
Where Food Workers Were
Implicated?
Impact of the Infected Food Worker
• CDC estimates 76 million cases of foodborne
illness each year in the United States
• Estimated that between 18-20% of foodborne
illness associated with an infected food worker
in the US, and 7% of salmonellosis in the UK
• Thus, there may be up to 13-15 million cases
in the US associated with an infected food
worker (18-20% of 76 million)
Definition of Food Worker
The term food worker is used in this
context to describe individuals, who
harvest, process, prepare and serve food
It is broader in context than food handler
although the two terms are used
interchangeably in the literature and
investigative reports
Purpose of Study of Infected Food
Workers Implicated in Outbreaks
• Project of the Committee on Control of Foodborne
Illness (CCFI) of the International Association for Food
Protection (IAFP)
• Goal: to develop an understanding of the dynamics of
transmission of infectious agents to and from the food
worker in a variety of settings
• The CCFI approached the task with the premise that
all foodborne illness is fundamentally preventable and
that by influencing human behavior there will be fewer
opportunities for spread of infectious disease agents
by workers and others
Papers Prepared on Outbreaks Where Food
Workers Have Been Implicated in the
Spread of Foodborne Disease in the Journal
of Food Protection (2007-2009)
• Part 1: Description of the problem, methods and agents
involved
• Part 2: Description of outbreaks by size, severity, and settings
• Part 3: Factors contributing to outbreaks and description of
outbreak categories
• Part 4: Infective doses and pathogen carriage
• Part 5: Sources of contamination and pathogen excretion from
infected persons
• Part 6: Transmission and survival of pathogens in the food
processing and preparation environment
• Part 7: Barriers and sanitizers in reducing contamination
• Part 8: Hand hygiene
Outbreaks by Geographical Region
Geographical
Region
Number of
Outbreaks (%)
Number of Cases
(%)
647 (79.3)
54,888 (68.0)
Europe
63 (7.7)
7,694 (9.5)
Canada
62 (7.6)
3,320 (4.1)
Australia/Asia
27 (3.3)
4,680 (5.8)
Latin
America/Caribbean
6 (0.7)
5,408 (6.7)
Africa
4 (0.5)
2,394 (3.0)
Middle East
3 (0.4)
400 (0.5)
Multiple Countries
2 (0.2)
1,843 (2.3)
Unknown
2 (0.2)
55 (0.1)
816 (100)
80,682 (100)
USA
Totals
Summary of Data on Pathogens
• 816 outbreak reports with 80,682 cases
• Pathogens in order of frequency:
–
–
–
–
–
–
–
norovirus/probable norovirus (338)
Salmonella enterica (151)
hepatitis A virus (84)
Staphylococcus aureus (53)
Shigella spp (33)
Streptococcus pyogenes Group A (17)
Parasites Cyclospora, Giardia, and
Cryptosporidium (23)
Outbreaks by Food Category
Meats
Poultry
Eggs
Dairy
Seafood
Breads and Bakery
Produce
Beverages
Multi-Ingredient Foods
Other
0
100
200
300
400
Number of Outbreaks
500
Foods Associated with Outbreaks Where
Food Workers Were Implicated
Multiple foods and multi-ingredient foods
were noted most frequently
– Salads, including potato, pasta and coleslaw
(92)
– Sandwiches (74)
– Chinese, Mexican type food, and pizza (19)
– Hors d’oeuvres and other RTE cold snacks
with sauces and glazes (8)
Outbreaks by Settings
*
Food Service
Catered Events
Processing Plant & Bakeries
Retail
Settings
Home
Schools
Health Care
Armed Forces & Camps
Commercial Travel
Community Events
Prison
Unknown
* Mainly restaurants
0
100
200
300
400
Number of Outbreaks
500
Most Extreme Outbreaks
• Largest outbreak:
– 6350 cases [1987, North Carolina: S. sonnei]
• Largest number hospitalized:
– 396 [1998, Brazil: S. aureus]
• Largest number of deaths:
– 68 [1990, Mozambican refugees in Malawi: V.
cholerae]
2b
Offsite food worker(s)
infects other workers at
a different location
1
Single worker causes an
outbreak that affects
patrons
2a, 4a, 4b, 5
Multiple workers cause outbreak at the
same location (2a), through contamination
of food (4a), no clear source (4b), or
workers may be the victims (5)
6
Food
contaminated by
offsite workers
3a, 3b
Foods contaminated by infected
worker are temperature abused
leading to outbreak
7
Infected consumers (patrons,
families, institutional
residents, etc) likely source of
infectious agent
Ill Consumers (Patrons,
Families, Institutional
Residents, etc)
8
Worker(s) are infected but
deny illness and outbreaks
not reported as caused by
infected worker(s)
Code
1
2.a
2.b
3.a
3.b
4.a
4.b
5
6
7
8
Outbreaks
238
29
3
171
70
41
162
13
40
15
34
816
%
29.2
3.6
0.4
21.0
8.6
5.0
19.9
1.6
4.9
1.8
4.2
100.0
Cases
21067
1423
194
12867
10093
5722
10696
8783
8306
635
896
80682
%
26.1
1.8
0.2
15.9
12.5
7.1
13.3
10.9
10.3
0.8
1.1
100.0
Social Gathering and
Staphylococcus aureus
• 8,000 people gathered in a community to celebrate a
Catholic priest’s ordination in 1998 in Brazil
• After eating food provided, 4,000 were acutely ill and
2,000 hospitalized, 16 died
• Eight food workers began preparing the chicken, roast
beef, rice, and beans over 48 h on the Friday before the
event, and stored in aluminum containers at room
temperature until Sunday morning
• These food workers had positive fingernail swabs for
Staphylococcus aureus, and five of them had the same
strain isolated from their nasopharynxes
• Leftover food was also found to contain S. aureus at 2.0
x 108 CFU/g, which produced 6 µg of enterotoxin A/g
Social Gathering and
Staphylococcus aureus
• 8,000 people gathered in a community to celebrate a
Catholic priest’s ordination in 1998 in Brazil
• After eating food provided, 4,000 were acutely ill and
2,000 hospitalized, 16 died
• Eight food workers began preparing the chicken, roast
beef, rice, and beans over 48 h on the Friday before the
event, and stored in aluminum containers at room
temperature until Sunday morning
• These food workers had positive fingernail swabs for
Staphylococcus aureus, and five of them had the same
strain isolated from their nasopharynxes
• Leftover food was also found to contain S. aureus at 2.0
x 108 CFU/g, which produced 6 µg of enterotoxin A/g
Examples of S. aureus Outbreaks
• 2 handlers sores on hands, 5 handlers same strain in nose
• S. aureus isolated from infected cut on hand of person who
baked cake
• 11 hospitalized S. aureus isolated from stool, vomitus,
sandwich and infected finger of food handler, sandwiches
stored 8-10 hours without refrigeration
• S. aureus in food and on food handler, inadequate storage
temperature for 5 hours
• S. aureus phage 6 patients and 6 food handlers, infected
cut on hand of one food worker who mixed food ingredients
with bare hands
• Cook handled and cooked ham with open cuts, sores and
finger lesion
• Contamination from hand of a symptomatic food worker,
stored at inappropriate temperature
School Children and Norovirus
• 3,236 (41.5%) of 7,801 schoolchildren and 117
(39.4%) of 297 teachers were ill in Japan in
1989 after eating catered food
• Food had been provided by a catering
company to nine elementary schools
• Workers had bare-hand contact with the food,
and a worker reported symptoms of
gastrointestinal illness on the day the food was
prepared
School Children and Norovirus
• 3,236 (41.5%) of 7,801 schoolchildren and 117
(39.4%) of 297 teachers were ill in Japan in
1989 after eating catered food
• Food had been provided by a catering
company to nine elementary schools
• Workers had bare-hand contact with the food,
and a worker reported symptoms of
gastrointestinal illness on the day the food was
prepared
Frosted Cakes Leading to
Norovirus Infections
• A bakery worker in Minnesota in 1982 prepared
76 litres of frosting using his arm up to the
elbow to break sugar lumps and scrape the
sides of the vat
• There were subsequently 3,000 cases of
norovirus infection
• He had five episodes of diarrhea and two of
vomiting during his 6-h shift when he frosted the
cakes
• Also he had sick children at home
Frosted Cakes Leading to
Norovirus Infections
• A bakery worker in Minnesota in 1982 prepared
76 litres of frosting using his arm up to the
elbow to break sugar lumps and scrape the
sides of the vat
• There were subsequently 3,000 cases of
norovirus infection
• He had five episodes of diarrhea and two of
vomiting during his 6-h shift when he frosted the
cakes
• Also he had sick children at home
Giardiasis from Salad
• In 1990, a food worker in the cafeteria of a large
Connecticut insurance company was infected with
Giardia lamblia and used her bare hands while slicing
raw vegetables, causing 27 cases of giardiasis
• She tested positive and had used gloves for most food
preparation activities but not for salad bar items
• The investigators noted that the outbreak was probably
only detected because the affected individuals were
insurance company employees whose medical care
was administered by a single health management
team
Giardiasis from Salad
• In 1990, a food worker in the cafeteria of a large
Connecticut insurance company was infected with
Giardia lamblia and used her bare hands while slicing
raw vegetables, causing 27 cases of giardiasis
• She tested positive and had used gloves for most food
preparation activities but not for salad bar items
• The investigators noted that the outbreak was probably
only detected because the affected individuals were
insurance company employees whose medical care
was administered by a single health management
team
Hepatitis at a Resort
• In 2004, a large outbreak with 351 hepatitis A cases
occurred involving tourists at a specific hotel in the
Egyptian resort city of Hurghada
• Guests who developed HAV infection after their
vacation were 2.6 times more likely to have ingested
orange juice than were healthy controls
• None of the hotel staff in Egypt was positive
• The juice was not pasteurized and came from a site
where hygiene problems were identified
• Although an infected worker at the juice production
company was the most likely source, none of the
company staff was IgM positive, but staff members
often changed and were not available for testing
Hepatitis at a Resort
• In 2004, a large outbreak with 351 hepatitis A cases
occurred involving tourists at a specific hotel in the
Egyptian resort city of Hurghada
• Guests who developed HAV infection after their
vacation were 2.6 times more likely to have ingested
orange juice than were healthy controls
• None of the hotel staff in Egypt was positive
• The juice was not pasteurized and came from a site
where hygiene problems were identified
• Although an infected worker at the juice production
company was the most likely source, none of the
company staff was IgM positive, but staff members
often changed and were not available for testing
Norovirus in a Restaurant (1)
• In Michigan in 2006, 364 restaurant patrons became ill
with norovirus GI illness after dining at a restaurant where
employees had reported to work while ill
• On Jan 28, a line cook vomited at home before reporting
to work at 11:00 a.m. and then vomited again into a waste
bin beside the frontline workstation at approximately 2:00
p.m. while preparing antipasti platters, pizzas, and salads
• After vomiting, he remained on site (but off the cooking
line) and left work at 4:15 p.m.
• This cook also reported to work on Jan 29 from 11:00 a.m.
to 4:30 p.m. while still experiencing loose stools
• Because of the open physical layout of the restaurant, no
barrier impeded airborne spread of the virus from the
kitchen to the main dining area
Norovirus in a Restaurant (2)
• There was a significant association between the platter and
the ill persons
• Patron attack rates increased after the cook vomited and
among employees, particularly cooks vs. servers, who worked
on Jan 28
• The investigation revealed deficiencies in employee hand
washing practices, cleaning and sanitizing of food and
nonfood contact surfaces, temperature monitoring and
maintenance of potentially hazardous food, and maintenance
of hand-sink stations for easy accessibility and proper use
• A quaternary ammonium based sanitizer normally used to
clean the restaurant was ineffective against the norovirus
• Then, a bleach solution used to disinfect the restrooms and all
surface areas within at least a 25-ft radius of the vomiting site
was effective for preventing further illnesses
Norovirus in a Restaurant (1)
• In Michigan in 2006, 364 restaurant patrons became ill
with norovirus GI illness after dining at a restaurant where
employees had reported to work while ill
• On Jan 28, a line cook vomited at home before reporting
to work at 11:00 a.m. and then vomited again into a waste
bin beside the frontline workstation at approximately 2:00
p.m. while preparing antipasti platters, pizzas, and salads
• After vomiting, he remained on site (but off the cooking
line) and left work at 4:15 p.m.
• This cook also reported to work on Jan 29 from 11:00 a.m.
to 4:30 p.m. while still experiencing loose stools
• Because of the open physical layout of the restaurant, no
barrier impeded airborne spread of the virus from the
kitchen to the main dining area
Norovirus in a Restaurant (2)
• There was a significant association between the platter and
the ill persons
• Patron attack rates increased after the cook vomited and
among employees, particularly cooks vs. servers, who worked
on Jan 28
• The investigation revealed deficiencies in employee hand
washing practices, cleaning and sanitizing of food and
nonfood contact surfaces, temperature monitoring and
maintenance of potentially hazardous food, and maintenance
of hand-sink stations for easy accessibility and proper use
• A quaternary ammonium based sanitizer normally used to
clean the restaurant was ineffective against the norovirus
• Then, a bleach solution used to disinfect the restrooms and all
surface areas within at least a 25-ft radius of the vomiting site
was effective for preventing further illnesses
Norovirus from Salad
• In 2000, a catered meal and distributed to 52 car
dealerships in the US as a reward for high car sales was
responsible for multiple gastroenteritis outbreaks in 13
states, resulting in at least 333 cases
• Pasta salads from one caterer was strongly associated
with illness
• Pasta was placed in large plastic bins, other ingredients
were added, and food workers mixed the salad by
immersing their ungloved arms up to the elbow
• Although the workers denied any history of illness in the
preceding week, 2 of 15 employees had elevated IgA
antibody titres to norovirus
• This caterer had been cited by health inspectors for
multiple sanitary code violations and was temporarily
closed pending sanitary improvements
Norovirus from Salad
• In 2000, a catered meal and distributed to 52 car
dealerships in the US as a reward for high car sales was
responsible for multiple gastroenteritis outbreaks in 13
states, resulting in at least 333 cases
• Pasta salads from one caterer was strongly associated
with illness
• Pasta was placed in large plastic bins, other ingredients
were added, and food workers mixed the salad by
immersing their ungloved arms up to the elbow
• Although the workers denied any history of illness in the
preceding week, 2 of 15 employees had elevated IgA
antibody titres to norovirus
• This caterer had been cited by health inspectors for
multiple sanitary code violations and was temporarily
closed pending sanitary improvements
Characteristics of Pathogens
Infectivity of Pathogens Transmitted by Infected
Food Workers
Agent
Incubation
Period
In Days
(mean)
Carriage
(C)
Rates
Reported
(%)
Presymptomatic
Shedding
Time
(days)
Norovirus
HAV
Sympto
-matic
Period
(Days)
Postsymptomatic
Shedding
(days)
%
Asymptomatic
Overall
Period
of
Infectivity
(days)
Source of
Infectious
Material
Carriage/
Shedding
0.6-3.2
GI : 1.1-1.5
Control 0.2
1.5?
1-11
2 weeks
32
May be
>2 weeks
IT, F, RT,
V
10-50
(28)
0.01 in
population
10-14
7-14
21
(180)
8 (70 in
elderly)
7-10
4-22
weeks
0.23-10
19 for FWs
in DCs
Up to
years
IT, F
Up to
years
IT, F
Salmonella
0.25-10
GI:0-16
Control:
0.1-1.6
X
Shigella
0.5-6
GI :0-0.8
X
4-7
60-150
55 - 75
20-36
C
C
C
20 - 65
GI:0.4-16
X
S. aureus
Giardia
lamblia
2-6 hours
3-25 (7)
7-60
Up to 35
(children)
Up to 8
weeks
Years
Months
F, U
N, S, C
IT, F
IT = Intestinal Tract, RT = Respiratory Tract, F = Feces, N= Nasal Secretions, S = Skin/Skin
Lesions, U = Urine, V = Vomitus
Foodborne Pathogens Transmitted by Infected
Food Worker and Periods of Infectivity
Time After Exposure (Days)
0
50
100
150
200
250
300
Norovirus (SRSV/NLV)
Hepatitis A
Salmonella spp.
S. Typhi/Paratyphi
Shigella spp.
Staphylococcus aureus
Streptococcus pyogenes
Giardia lamblia
Campylobacter jejuni
Cryptosporidium parvum
Vibrio cholerae
E. coli O157:H7
Yersinia enterocolitica
Incubation
Incubation/
Pre-symptomatic
Post-symptomatic Phase
Pre-symptomatic
Shedding Phase
Extended
Post-symptomatic Phase
Symptomatic
Period
Carrier State
Extended
Symptomatic
Levels of Pathogens in Body Excretions
• Salmonella in feces
–
–
–
–
Ill or early convalescence: 105-107 CFU/g
Late excretion (infants excrete longer): 100-103 CFU/g
10-19 days after illness: 100-106 CFU/g
69-102 days after illness: 100-104 CFU/g
• Sneeze with Streptococcus pyogenes
– up to 106 CFU/sneeze
– up to 500 CFU/154 cm2 1.5 – 9.5 feet from sneeze source
• HAV in feces just before hepatitis symptoms begin
– 108 infectious particles/g
• Norovirus in feces while ill
– 105 – 1010 copies/g
• Cryptosporidium in one bowel movement: 108 – 109 oocysts
Fecal Contamination of Hands During
Toilet Use With and Without Toilet Paper
• Mean fecal weight/hand (g) after cleansing
– Without toilet paper 8.5 x 10-6 - 9.8 x 10-7
– With toilet paper 5.0 x 10-9
• Pathogens can be present in feces at levels of from 105 to
1011 per g. A tenth of a milligram of fecal material (10-4 g), an
amount barely perceptible, might contain up to a million
infectious bacterial cells or viral particles
• At 10-7 g fecal matter of contamination per hand and a
pathogen that present at 1011 per g, if hands were washed
and/or sanitized, a 2 to 3 log reduction (99%-99.9%) could still
allow a worker to transmit a few cells
• Add to the fact that those ill may be more careless with fecal
cleanliness (continual cleanup from diarrhea, fecal accidents,
and not focused on the job and hygienic practices), and the
risk increases greatly
Survival of Enteric Pathogens on Hands
and Surfaces
Infective
Agent
Surfaces
Log, % Loss or
Half Life
Salmonella
Hands, inoculated eggs,
formica surface, utensils
Survived well 24 hrs.
Shigella sonnei
Fecally- contaminated hands
Survival for 3 hrs.
S. aureus
Skin and clothing
1 log/5 hrs.
Campylobacter
jejuni
Hands with peptone,
chicken broth, and
50% blood
3-7 log/ 2 min.
6 log/ 15 min.
6 log/ 45 min.
E. coli
Skin
3 log/5 min.
E. coli in milk
Fingertip
94% loss in 45 min.
Entamoeba
histolytica
Hands (nails in feces)
Survival for 45 min.
Enteritidis in egg
white and yolk
Survival of Pathogens
• Norovirus survived in carpets and toilet facilities
for more than one day after an individual vomited
on seats and washroom; infected clean-up crew
and subsequent concert hall attendees infected
by aerosols
• Illnesses from carpet removers in a hospital ward
12 days after vomiting outbreak occurred
• Pathogens tend to survive longer on surfaces
such as ceramic tile, steel, dust, glass and plastic
than on hands
Levels of Pathogens in Raw Meat and
Poultry
Infective
Agent
Product
Log
Campylobacter
jejuni
Chicken juices, ceca
Chicken carcasses
103-109
<101-109
E. coli O157:H7
Ground beef
Cattle/sheep feces
5
103-105
Salmonella
Chicken juices, organ,
carcasses
Chicken fillets
102-106
10
CFU
<10% with up to 103
Transfer of Organisms from Hands
• The transfer efficiency between hands and lettuce
was found to be 0.3% and from hands to spigots
was 1%
• The transfer rate of HAV from fingerpads of adult
volunteers to pieces of fresh lettuce was determined
to be 9% of the infectious load on the fingers
• Lettuce touched by a washed hand may be
contaminated with as many as 3.8 log10 CFU
indicator bacteria
• A 10% transfer rate of bacteria from food to hands
or bare hand to food; and by using gloves, this rate
was reduced to 0.01%
Outbreaks Associated with Lack of Adequate
Hygienic Facilities
• Inadequate toilet facilities (Yersinia, Shigella,Vibrio,
Salmonella)
• Non functional toilet (Shigella)
• Lack of handwashing facilities (Shigella,Vibrio, HAV)
• Inadequate handwash facilities (Shigella, norovirus)
• Difficult to use faucets (HAV)
• Lack of running water (Yersinia, Shigella,Vibrio)
• Lack of fingernail brush (Giardia)
• Lack of soap (Shigella,Vibrio, Giardia)
• No paper towels for hand drying (Shigella, Salmonella,
norovirus)
Handwashing Occasions
• Wash hands thoroughly with disinfectant soap
and water at appropriate times for the job
description
• Also after the following:
• handing raw foods
• after going to the toilet
• after contact with persons suffering from acute GI
symptoms
• after being in contact with infants and incontinent
individuals
Minimize Hand Contact
Evaluate food handling procedures and
modify to reduce or eliminate hand
contact for RTE food:
– Gloves
– Utensils
– Deli papers
Exclusion and Work Restrictions
•
Exclude infected symptomatic persons (GI) from
preparing and serving food during communicable
periods of illness
• Exclude infected persons known to be
asymptomatic carriers based on screening
• Restrict food workers from preparing or serving food
• Infected skin lesions
• Sore throat
• Acute respiratory infections
• Food workers should be kept on sick leave for 48 h
following disease cessation
Hygiene Education, Training and Supervision
• Train food workers and supervisors:
– in proper food handling practices and procedures
– to report personal and family illness
• Provide supervision of workers:
– Surveillance of workers and correction of handling errors
– Screen food workers (nasal and stool):
• at start of employment
• routine testing
• upon return from travel in area having high endemic disease
rates
• Immunize workers when feasible (HAV, etc)
What Have Investigations of
Outbreaks Where Food Workers Were
Implicated Taught Us - Sources?
• There are many sources where food workers
have become infected
– Ill family members, homosexual partners or diapering
a sick child
– Intravenous drug use
– Eating contaminated food
– Environmental sources, e.g., water, animals
– Travel abroad
– Contact with other infected workers
Spread in the Food Worker
Environment
• Once a worker has brought an agent into a food
operation, it can easily be transferred from person to
person, person to food contact surfaces and to food
– Lack of adequate handwashing facilities and improper
handwashing and drying
– Long and artificial nails are too difficult to clean effectively
– Lesions and wounds harboring pathogens are not properly
covered
– Workers continuing to work when infected and ill (diarrhea
and vomiting): management or worker decision
– Transmission between workers in food preparation area
– Lack of use of gloves/bare hand contact
Removal of Contaminants
• Fecal contamination can be extensive even
after washing – use of toilet paper doesn’t
prevent all fecal organisms from going on
finger tips and from there to contact surfaces
• Vomiting can spread viral particles over long
distances despite any clean up afterwards and
particles can persist for days or weeks
• Thorough and frequent handwashing and use
of gloves keeps contamination in food
environment to a minimum
Some Problems To Be Resolved
• Having incentives for workers to stay home when
they are ill or diagnosed with a likely infection
• Identifying workers who are asymptomatic and need
to be away from handling food and any physical
contact with other workers
• Effective communication with low-paid workers, often
speaking other languages than English, may not read
well and will move on for a continual turnover, issues
of trust and motivation
• Putting more resources into effective local
investigation of outbreaks
• More priorities for handwashing in industry/home
Acknowledgements
• Bert Bartelson, Judy Greig, and Barry
Michaels, members of the Committee for
the Control of Foodborne Illness,
International Association for Food
Protection (IAFP), and IAFP Board
QUESTIONS?
Categorization of Outbreaks Where
Food Workers Were Implicated
3. After food worker(s) contaminates food via:
3a) fecal contamination (e.g., by Salmonella,
Shigella, Yersinia) or
3b) through skin, nose and throat
contamination (e.g., Streptococcus
pyogenes, Staphylococus aureus)
– Temperature abuse results in bacterial multiplication
resulting in high enough numbers to cause illness
Categorization of Outbreaks Where Food
Workers Were Implicated
4. Multiple food workers are:
4a) unequivocally the cause of the outbreak
though contamination of food or food
contact surfaces, or
4b) linked to an outbreak but there is no clear
initiating source
5. Food worker(s) becomes infected but
uncertain whether they are victims or causes
of outbreak
Categorization of Outbreaks Where
Food Workers Were Implicated
6. Food contaminated with pathogens by
offsite workers and delivered to the
location where the outbreak occurs by
directly infecting consumers/patrons
– Details of the worker contribution to the
contamination are usually not known
Categorization of Outbreaks Where Food
Workers Were Implicated
7. Patrons (those being served), not
workers, are the probable source of the
infectious agent though contamination of
food or food contact surfaces
8. Outbreaks where workers are implicated
epidemiologically and likely are infected
or colonized but deny illness
Category 1:Single Worker Causes an
Outbreak
37 cases associated with cold salad bar items from the
cafeteria of a Minnesota college, 2000
– Index case a symptomatic food worker
– Called in sick but symptoms resolved later that day
– Returned to work the next day and worked the
remainder of the week in salad bar section, with
extensive bare-hand contact of salad items
– Noroviral agent based on epidemiological
information
– Call-in ill log useful to determine dates that
employees were ill and to ascertain the responsible
employee
Category 2a:Multiple Workers
Cause Outbreak
Multi-state outbreak of Salmonella Thompson: 78
cases at fast food restaurants and catered events
– Full-time employee did not wear gloves and
handled every individual bread item at least twice
– Worked with symptoms for 4 days until overnight
hospitalization
– Resumed work after discharge and continued
working until termination of employment
– She infected brother who also worked with dough
and bread
– No formal training on safe food-handling practices
– Many employees spoke only Spanish but had
English procedure manuals
Category 2b: Offsite Food Worker(s)
Infects Workers at a Different Location
HAV affected 40 university students, 11 employees of two
restaurants, and 11 other residents in Arizona, 1973
– Two distinct epidemic waves at the 2 restaurants
– Index case of first restaurant prepared salads
– Index case of the second restaurant had eaten at
the first restaurant
– Implicated vehicles at the second restaurant included
guacamole, green salad, spaghetti, and hamburger
Category 3a: Foods Fecally Contaminated by
Infected Worker are Temperature Abused
Leading to Outbreak
July 1981 New York: Y. enterocolitica O:8
isolated from 37 persons including head cook
and kitchen staff
– Five hospitalized for appendicitis
– Powdered milk and dispenser contaminated when
food workers cleaned and repaired a broken spigot
– Same strain isolated from chow mein indicating
multiple contamination scenarios
– Reconstituted milk held 24 hours under cool
conditions but allowed growth of Yersinia
Category 3b:Foods Nasally Contaminated by
Infected Worker are Temperature Abused
Leading to Outbreak
Convention in Florida 1979: outbreak of pharyngitis, 72/231
ill, including waiters and cooks
• Streptococcus pyogenes Group G isolated from 10 of
16 with pharyngitis and 1 of 41 who did not
• Illness associated with chicken salad
• Cook prepared chicken salad a day prior to her
symptoms
• Cooked chicken refrigerated overnight in a deep
container
• No indication she wore gloves or washed hands
frequently
• Opportunity for growth of the Streptococcus
Category 3b: Foods Contaminated by Lesion
of Infected Worker and are Temperature
Abused Leading to Outbreak: Commercial
Travel
• Flight attendant and 196 passengers rapidly developed
vomiting and diarrhea following ingestion of ham and
cheese omelets served during a chartered flight for a
tour group from Tokyo to Paris, stopping en route in
Alaska and Denmark
• Cook who prepared ham had infected finger
• Ham left at room temperature for six hours
• S. aureus isolated from food samples
Category 4a: Multiple Food Workers are
Unequivocally the Cause of the Outbreak
2000: multi-state outbreak, 333 cases, catered meal
prepared in Ohio and distributed to 52 car dealerships
nationwide
– Consumption of any of four side salads strongly
associated with illness
– Ingredients were placed in large plastic bins and mixed
by food workers who immersed ungloved arms up to the
elbow
– 2 of 15 employees had elevated norovirus titers
– Three food handlers were symptomatic before outbreak
Category 4b:
Multiple Food Workers are Linked to Outbreak
But There is No Clear Initiating Source
July 1992, 46 patrons at 21 restaurants in Michigan
and one in Ohio infected with Shigella flexneri
– Associated with consumption of pre-prepared
salads from a central commissary
– 15 infected workers ill during the same time
period and four prepared salad during the
outbreak period
– Salad was mixed with bare hands, bagged by
machine, and employees added or subtracted
from the bags to meet the weight standard
– Investigation failed to identify the infected
employees
Category 5: Food Worker(s) Become Infected but
Uncertain Whether They Are Victims or Cause of
Outbreak
Large outbreak of shigellosis associated with a
mass gathering in a national forest area, North
Carolina, 1987
– Over 50% of 12,700 attendees infected
– Transmission assumed to be by food and water,
followed by person-to-person contact
– Food prepared in 47 communal kitchens with limited
sanitation
– Food from at least one kitchen implicated and unboiled
water drunk by attendees
Category 6:Food Contaminated With Pathogens by
Offsite Workers and Delivered to the Location
Where the Outbreak Occurs
Six norovirus outbreaks (1,143 cases) in institutions or
commercial catering settings, June to Sept. 2005 in
Denmark, linked to frozen raspberries imported from
Poland
– Unheated frozen raspberries served one day before
start of each outbreak
– Estimated 400 elderly people affected and at least 23
hospitalized
– Three different norovirus serotypes isolated
– Several independent contamination events likely
occurred
– Infected workers in the harvesting or processing of
the raspberries in Poland were a likely but not proven
source
.
Category 7: Patrons Are the Source of the Infectious
Agent Though Contamination of Food or Food
Contact Surfaces
.
Mediterranean-style restaurant
in Melbourne,
Australia, three successive norovirus outbreaks,
May 1998 - June 1999
• Food served on platters and patrons ate with
fingers, moving from table to table
• Different norovirus strains isolated in the three
outbreaks indicating no reservoir but recurring
contamination of food
• Demonstrates how norovirus can be transmitted
where many people are in close contact and touch
and eat food
Category 8: Outbreaks Where Workers
Are Implicated but They Deny Illness
Minnesota 2004: six relatives complained of GI
illness after dining at a restaurant
– 1 of 6 positive for norovirus
– None of the workers were obviously symptomatic
– Most of the staff were Spanish speaking and the
manager acted as translator
– Conclusion: outbreak could not be adequately
characterized even though the likely source of the
norovirus was one or more employees
Examples of Streptococcus Outbreaks
• Military base: 3 food handlers of boiled egg
salad were asymptomatic carriers of
Streptococcus – hand contamination or
sneezing
• Military base: an egg salad preparer tested
positive, he shelled boiled eggs with bare
hands for the salad
• School: food preparer had open hand lesion
that came in direct contact with the macaroni
and cheese
• Catered event: preparer of egg salad had
extreme cellulitis on hands; he tasted the
salad, workers coughed or sneezed
Examples of Hepatitis A Outbreaks
• Salads
– Restaurant: two asymptomatic pantry workers
contaminating food by hand shredding lettuce and
dipping fingers into dressing to taste them
– Caterer: “Salad boy” with apparent good hygiene handtore moist lettuce and soon developed fever and malaise
• Drinks
– Employee, who was HAV positive but asymptomatic, was a
suspected IV drug user, and had helped prepare
fountain drinks and sandwiches
– Bar tender had chronic diarrhea and contaminated the
glasses when served beverages
– Asymptomatic carrier did not wash his hands after
using the toilet and contaminated the punch at a catered
event
Examples of Hepatitis A Outbreaks
• Fast food restaurant: food worker, who was a drug
user and family described him as having poor hygiene,
had diarrhea and tested positive for HAV
• Caterer: Asymptomatic sandwich maker had prior nausea
and vomiting, most likely contamination through hand
contact with foods
• Caterer: Pastry-cook had jaundice prior to preparing
pastries by bare hand for meals
• Bakery: baker’s assistant with hepatitis was directly
involved in handling and dipping cooked pastries
Examples of Shigella Outbreaks
• University: Shigella infections after eating shrimp
deveined in India – contamination source uncertain but
has to be human fecal
• Restaurant: employees ill with Shigella flexneri prepared
tossed salad by reaching into chopped salad ingredients
with bare hands
• Restaurant: worker infected with Shigella after a trip to
Mexico washed lettuce with bare hands
• Restaurant: worker infected with Shigella flexneri in
restaurant with hygiene violations, including a lack of
hand washing between tasks and inadequate
handwashing facilities
Examples of Salmonella Outbreaks
• Salmonella enteritidis on curly fried potatoes
and ice handled bare-handed by employee
who had onset of illness 1 day prior, no paper
towels
• Prison: Inmate who deboned turkey had
multiple excoriated lesions on both forearms
that had a positive S. aureus culture,
Salmonella infantis isolated from turkey eaters
Examples of Norovirus Oubreaks
• Salad: asymptomatic noroviral shedding by one or more of
the workers who handled lettuce with bare hands
• RTE food: hand preparation by untrained staff and
patients
• Catered function: food worker excreted the virus and
touched RTE foods including melon
• Cruise ship: ice machine did not have proper air-gap device
to prevent sewage backup, and the ice was contaminated
by hands of those scooping it out
• Bakery: A cake decorator, ill with GI, was wearing long
artificial nails with which she contaminated the icing
• Restaurant: bad management forced employee to work,
who was sick and wanted to stay home, used bare hands
on hamburgers
Examples of Outbreaks Associated with Bare
Hand Contact
• Restaurants
– Bare hands serving pineapple slices, not ill at the time, but ill 3
hours after handling
– Asymptomatic worker with no gloves sliced meats, cheese and
vegetables, no adequate washing area
– Symptomatic worker prepared guacamole and salsa with bare
hands, good hand washing facilities
– Employee excreting virus while using bare hands to remove
tissues from steamed bovine heads
• Bakeries
– Soiled hands not washed due to painful skin lesions
– Contaminated baked goods when applying sugar glaze with bare
hands
• Deli shop
– 76 year old grandmother typhoid carrier handled cannelloni
without gloves after they were cooked once a week
Data Sources
Outbreak data from 1927 to 2004 from:
– Michigan (2000-2003): State line listings
– Minnesota (1999-2004): State line listings and
outbreak reports
– New York (1985-2000): State line listings
– Washington (1990-2003): State line listings and
outbreak reports
– Health Canada (1976-1996): Line listings from
annual reports of foodborne and waterborne
disease outbreaks
– Outbreak reports from other countries
– Published peer-reviewed literature including reviews
Large Gathering and
Shigellosis
• For 2 weeks, food was prepared in 47 communal
kitchens in a national forest area for a Rainbow
gathering in North Carolina in 1987
• There were no toilets, hand washing facilities, safe
drinking water sources, or refrigeration
• The outbreak began on July 4 1987, and rapidly
spread throughout the gathering until it was closed on
July 15 with a total of 6350 cases
• Transmission was assumed to be by food, water, and
person-to-person contact.
• Secondary infections occurred after ill persons
returned to home communities in other parts of the US
Cake and Norovirus
• A cake requiring direct hand contact during its
preparation was associated with the majority of illnesses
in an outbreak of 2700 persons in 2002 in
Massachusetts
• At least two bakery employees experienced noroviruscompatible illness during the week preceding the
weddings. Two wedding guests, a wedding hall
employee, and one of the bakery employees were ill;
identical sequence types were detected in the stool
specimens submitted
Shigellosis from Hamburgers in
a Resort
• A butcher who prepared hamburger
patties at a resort in Haiti in 1984 had a
Shigella flexneri infection and continued
working while ill during the 3-week period
in which 1,136 guests reported illness
• Illnesses were linked only to those who
consumed raw or rare hamburger; this
was followed by secondary person-toperson spread between roommates
Categorization of Outbreaks Where Food
Workers Were Implicated
1. Single food worker causes an outbreak
though contamination of food or food
contact surfaces
2. Single food worker infects other workers
(victims) who in turn infect
consumers/patrons though contamination
of food or food contact surfaces:
a) in the same establishment or
b) in a separate location
Transfer of Organisms from Hands
• Study using Nalidixic acid-resistant Enterobacter
aerogenes as a surrogate for an enteric pathogen
to follow cross-contamination demonstrated that
after handling chicken, contaminated hands
transferred 2.4 to 5.7 log10 of bacteria to a spigot
used to wash hands; after washing 1.9 to 6.5 log10
still remained on hands (Chen et al. 2001)
• Perez et al. (2006) showed that there was a high
risk with the use of the same gloves to handle
contaminated chicken meat and then slice ham
compared to the safer use of different gloves to
handle each product
Listeria monocytogenes in Different Cross-
contamination Scenarios (Perez et al., 2006)
• A series of cross contamination scenarios at retail were ranked
according to their risk level
• The highest risk corresponded to the use of the same gloves to
handle contaminated chicken meat and then sliced ham
compared to the safer use of different gloves to handle each
product
• The lowest risk corresponded to use of gloved hands but washed
between handling the chicken and slicing the ham (only
250/100,000 slices would be contaminated)
• All scenarios were capable of ham reaching levels above 108 cfu/g
after storage when growth can occur
• Lack of knowledge of transfer rates provided the model with an
important uncertainty component
Simulated Distribution of L. monocytogenes at the
Time of Consumption (N) for 3 Scenarios Perez et
al., 2006)
Contaminated meat-bare hands-washing-gloved hands -slice
X >-5,07
95%
0.25
Contaminated meat -gloved hands-gloved hands-slice
X >2
3.534%
X >-8,83
95%
0.25
X >2
.088%
M ean = -2,323807
M ean = -6,145167
Frequency
0.2
0.15
0.1
0.05
0
-10
0.15
0.1
0.05
-8
-6
-4
-2
0
2
4
6
8
0
-15
10
-10
L. monocytogenes (log CFU/g)
-5
X >-5,55
95%
0.25
X >2
3.421%
M ean = -2,566866
0.2
0.15
0.1
0.05
0
-10
-8
0
L. monocytogenes (log CFU/g)
Contaminated meat-bare hands-slice
Frequency
Frequency
0.2
-6
-4
-2
0
2
4
L. monocytogenes (log CFU/g)
6
8
10
5
10
Effective Handwashing
Wash, rinse, dry
Fingernail brush
Instant hand sanitizer
Frequent (Task appropriate)
Minimize cross-contamination-use handsfree
devices, e.g., turn on tap/faucet
• Paper towel dispensers/hot air drying/doorless
entry or automatic doors
• Handwash process monitored, documented and
verified (MDV)
•
•
•
•
•
Studies on Handwashing
• Thumbs, palms, spaces between fingers, and fingertips
including the fingernail area, are areas in which
contamination is most likely to remain. Hand drying
may help make up for deficiencies in the washing
process
• E. coli and Pseudomonas fluorescens mixed with ground
beef and rubbed onto hands were 95% removed with a
single handwashing using an E1 soap
– a 75% reduction was subsequently shown with a tap
water wash only
• Giardia was removed form the hands with soap and
handwashing. When 10,000 cysts were placed in the
palm of the hand, handwashing eliminated 99% (100
cysts)
Studies on Handwashing
• Based on laboratory testing using artificial
contaminants, the effectiveness of
handwashing, including washing, rinsing and
drying, ranged from 2 to 3 log10 reduction
(99%-99.9%)
• Compliance rates for handwashing are
estimated at 50% but no surveys have been
done
Food Preparation and Environmental
Control
• Follow proper cooking, hot holding,
chilling and storage procedures
• Environmental controls:
– Disinfect surfaces often
– Clean change of work clothing
Airflight Illnesses
• 1. British Airways flights in 1984 with a total of 866
cases: 631 passengers, 135 aircrew, and 100 catering
personnel and loaders, with 2 passenger deaths
• An ill chef prepared the aspic glaze, which was then
left at ambient temperatures
• Also, it was reported that a party given by a senior
catering manager at the catering center resulted in all
guests becoming ill, with two hospitalized
• 2. Charter flights to and from Canary Islands to Finland
in 1976 resulted in 1,800 salmonellosis cases
• Salmonella Typhimurium phage type 96 was isolated
from passengers, mayonnaise, and one food worker in
the Las Palmas catering establishment
Airflight Illnesses
• 1. British Airways flights in 1984 with a total of 866
cases: 631 passengers, 135 aircrew, and 100 catering
personnel and loaders, with 2 passenger deaths
• An ill chef prepared the aspic glaze, which was then
left at ambient temperatures
• Also, it was reported that a party given by a senior
catering manager at the catering center resulted in all
guests becoming ill, with two hospitalized
• 2. Charter flights to and from Canary Islands to Finland
in 1976 resulted in 1,800 salmonellosis cases
• Salmonella Typhimurium phage type 96 was isolated
from passengers, mayonnaise, and one food worker in
the Las Palmas catering establishment