Most molds are considered to be a spoilage problem.
Examples of mold spoilage include: mold on cheese, fruits
and vegetables, and bread. The mold growth alters the flavor
and texture of the food products. If the mold growth is not
extensive, the moldy part of the food can be trimmed and the
food can be consumed.
CHAPTER 4
FOOD MICROBIOLOGY
FOOD MICROORGANISMS
Parasites
Molds
Trichina spp., Anisakis, beef tapeworm, Toxoplasma gondii
Live within animals and fish (in muscle, intestinal tract).
1 to 10 will cause illness.
Killed by freezing according to government-specified temperatures and times.
Killed by cooking to 145ºF, 15 seconds.
Some types of mold are beneficial and are used to produce
characteristic flavor in cheeses (e.g., Roquefort cheese) or
produce soy sauce. Some types of mold are harmful and
produce aflatoxins (carcinogenic compounds) when they grow
in cereals and grains. The government tests for mold toxins in
food and controls this hazard.
Aspergillus spp., Fusarium, penicillin on wholesale, stored grain and peanuts
Most molds are spoilage. Cut off.
Molds on grains and nuts can form toxins. Keep grains and nuts dry.
Throw out.
Viruses
Noroviruses, hepatitis A, rotavirus
From human feces and vomit.
Double wash fingertips.
Bacteria
Vegetative bacteria: Salmonella, E. coli, Vibrio, Shigella, Streptococcus, etc.
100,000-to-1 kill; 145F, 3 minutes; 150F, 1 minute; 155F, 15 seconds.
Double wash fruits and vegetables (100-to-1 reduction).
Spores: Clostridium perfringens, Bacillus cereus, Clostridium botulinum,
hot food
Survive pasteurization. Hold 135F.
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Food Microorganisms
Introduction
In order to develop sound safety standards and operating
procedures, a basic understanding of microbiology is
necessary. Microbiology is the study of small living systems
(i.e., microorganisms), which include bacteria, yeasts, molds,
viruses, and parasites. Some of these microorganisms are
beneficial in food production and food processing. However,
some microorganisms are pathogenic (cause disease and
illness) and must be controlled or destroyed in food processing
and preparation.
Parasites
Parasites are organisms that live at the expense of the hosts
(humans, animals, fish, and birds). In this text, parasites refer
to protozoa (microscopic, single-celled animals with a defined
nucleus) and helminths (small worms and their larvae).
Protozoa of common concern are Giardia lamblia and
Entamoeba histolytica. Both of these protozoa cause diarrheal
illness and intestinal discomfort of varying severity. They are
often found in untreated or in inadequately chlorinated water
supplies. They can become foodborne if water containing
these protozoa is used to irrigate plants or wash food prior to
service. Infected people and animals can also pass these
protozoa in their feces to infect others, as with Toxoplasma
gondii, a parasite whose original hosts are cats.
Helminths are parasitic worms. These worms are usually
large enough to be seen without the aid of a microscope.
However, a microscope is needed to detect their cysts and
eggs. The parasitic worms of most concern in food are
Trichinella spiralis, Taenia (tapeworms), and Anisakis spp.
Viruses
Viruses are not true living cells. They are acellular and have
no cytoplasm, nucleus, cell wall, or cell membrane. Viruses
are much smaller than bacteria and are composed of a protein
coating around genetic material (DNA or RNA). Viruses are
not able to reproduce unless inside a living cell (e.g., the
Hepatitis A virus multiplies within human liver cells).
Diseases and illnesses caused by viruses include colds, flu,
and norovirus gastroenteritis.
Bacteria
There are three basic forms of bacteria. These include: bacilli
or rods, cocci, and spirilla. Cocci are round in shape and can
be found as single cells, as chains (streptococci), in clusters
(staphylococci, and in pairs (diplococci), or tetrads (sarcinae).
Bacterial cells are very small and measure approximately
0.05-2.0 x 2.0-10.0 microns or micrometers. One micron is
1/1,000 millimeter or 1/1,000,000 meter (10-6 m). A micron
is also 1/25,400 inch. This means the length of 25,000
bacteria aligned end to end would be approximately one inch.
The human eye can only resolve or see objects that are
approximately 75 microns. Bacteria are 75 times smaller than
the eye can see. Microscopes are needed to magnify bacteria
so that they can be seen by the eye.
When millions of bacteria are present in a solution of clear
broth, the broth becomes cloudy. In the same way, when
bacteria multiply to numbers of 10,000,000 per gram of food,
the food becomes slimy and is considered to be spoiled. Food
with 10,000,000 spoilage bacteria per gram usually has offflavor and odor and people judge it to be spoiled.
Yeasts
Yeasts are much larger than bacteria. With a couple of rare
exceptions, yeasts are not pathogenic (do not cause foodborne
disease or illness).
Yeasts are used in food processing to produce bread, beer, and
wine. When yeast grow in foods where their growth is not
desired they cause changes in flavor, odor, and texture (e.g.,
yeast growth in fresh fruit juices and in ketchup).
Parasites are unique in that they can be destroyed by freezing
according to government-specified temperatures and times.
For example, Anisakis spp. in fish will be destroyed if the fish
is held at -4ºF (-20ºC) for 7 days.
Pathogenic vs. Non-pathogenic Microorganisms
Pathogenic microorganisms cause disease or illness. The
multiplication of pathogenic bacteria in foods does not usually
change the odor or flavor of food.
Molds
Molds are larger than bacteria. Their presence can be seen as
a cottony, powdery, or fuzzy patch on the surface of food and
may be white or gray or highly colored.
Non-pathogenic microorganisms do not cause disease or
illness and can be used to produce desirable changes in food
(e.g. production of cheese and wine). The growth of nonpathogenic microorganisms causes food to spoil when they
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4a-1
grow in food products where their growth is not desired. Nonpathogenic microorganisms produce acid, carbon dioxide, and
other by-products that alter the texture, flavor and odor of
food.
Primary Sources of Food Pathogens
The intestinal tract of colonized humans and animals is a
source of many pathogenic bacteria, which include:
Escherichia coli, Salmonella spp. Shigella spp.,
Campylobacter spp., Staphylococcus aureus, Streptococcus,
and Clostridia. Humans and animals also transmit viruses
(e.g., hepatitis A virus and norovirus) through fecal
contamination of foods. Parasitic infections are also spread
through the fecal contamination of food products and water
supplies. These include giardiasis and amoebic dysentery.
Soil and water are sources of molds, viruses, bacteria, and
parasites. The following bacteria are commonly found in soil:
Listeria monocytogenes, Clostridium botulinum, Clostridium
perfringens, and Bacillus cereus. Water is a source of Vibrios,
viruses, (e.g., hepatitis A virus and norovirus), and parasites
(e.g., Giardia). Mold. can be found in both water and soil and
they include Aspergillus, Penicillium, Fusarium, and others.
Foods grown in soil and watered with river or lake sources
will contain these pathogens, depending upon the
contamination level of the water. Fish and seafood taken from
rivers, lakes, and oceans may contain varying amounts of
pathogenic microorganisms due to sewage treatment plant
effluent as well as marine life contaminants.
Plants and plant products (e.g., fruits, vegetables, grains,
and cereals) carry most of the same pathogens that are found
in soil and water. Plants and plant products are also sources of
molds and parasites.
Food utensils such as serving utensils, knives, cutting boards,
slicing and chopping equipment will contain various kinds of
microorganisms, depending on the food handled, the food
handler, and the sanitization and storage of this equipment.
For example, if a chicken containing Salmonella spp. is cut on
a cutting board, the knife, cutting board, and hands of the food
handler will all carry or become contaminated with this
bacterium. These utensils (and the food handler's hands) must
be thoroughly washed and sanitized to prevent the spread of
this pathogen. Utensils that are stored in the open should be
expected to contain airborne bacteria and molds.
Other sources of human contamination include the
microflora on the hands, nasal cavities, and mouth of food
handlers. Staphylococcus aureus is found in the nasal cavity
(nose) and in infected cuts and wounds. Food handlers should
never work with food if they have an open infected cut or boil.
Animal feeds may contain any one of a number of pathogenic
microorganisms that include bacteria, molds, and viruses. It is
well documented that animal feeds have been a source of
Salmonella spp. in animals and poultry. The meat from these
animals and poultry was then a source of Salmonella
contamination and foodborne illness. Rodents and birds
transmit microorganisms through their fecal contamination of
grains and animal feed.
Air can carry many types of bacteria, viruses, and molds.
Bacillus spp. and Micrococcus are able to endure dryness and
can be carried in the air for many miles.
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4a-2
Control of Pathogens
Table 4-1 (next page) lists some of the potential microbial
pathogens in food. Note that all foods are a potential source of
pathogens. There will never be a zero pathogen level in
raw foods. However, they can, and must, be reduced to a safe
level by the cook. Managers and food handlers must know the
different types of pathogenic microorganisms of concern in
food and food production. They must know their sources,
conditions for optimal multiplication, and ways of preventing
or inhibiting the presence and multiplication of these
pathogens in foods to prevent foodborne illness outbreaks
from occurring.
References:
Frazier, W.C. and Westhoff, D.C. 1988. Food Microbiology.
3rd edition. McGraw-Hill, New York, NY.
Jay, J. M. 2000. Modern Food Microbiology. 6th ed.
Chapman & Hall. New York, N.Y.
Mossel, D.A.A., Corry, J. E. L., Struijk, C. B., and Baird, R.
M. 1995. Essentials of the Microbiology of Foods.
John Wiley & Sons. New York, NY.
Table 4-1
Potential Pathogens in Food
PATHOGENS
FOOD
Meat, Poultry, and Eggs
Infective
Salmonella spp.
Campylobacter jejuni
Escherichia coli
Yersinia enterocolitica
Salmonella spp
Vibrio spp.
Yersinia enterocolitica
Listeria monocytogenes
Hepatitis A virus
Trichinella spiralis
Tapeworms
Hepatitis A virus
Anisakis
Tapeworms
Shellfish
Salmonella spp
Vibrio spp.
Shigella spp.
Yersinia enterocolitica
Norovirus
Hepatitis A virus
Fruits and Vegetables
Hepatitis A virus
Norovirus
Giardia lamblia
Cereals, Grains,
Legumes, and Nuts
Salmonella spp.
Listeria monocytogenes
Shigella spp.
Escherichia coli
Salmonella spp.
Aflatoxins (mold)
Spices
Salmonella spp.
Milk and Dairy Products
Salmonella spp.
Yersinia enterocolitica
Listeria monocytogenes
Escherichia coli
Fin Fish
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Campylobacter jejuni
Shigella spp.
Hepatitis A virus
Norovirus
4a-3
Toxin and/or Spore
Producers
Staphylococcus aureus
Clostridium perfringens
Clostridium botulinum
Bacillus cereus
Staphylococcus aureus
Clostridium botulinum
Microbial by-products
(Histamine poisoning)
Staphylococcus aureus
Clostridium botulinum
Microbial by-products
(Paralytic shellfish
poisoning)
Staphylococcus aureus
Clostridium botulinum
Bacillus cereus
Staphylococcus aureus
Clostridium botulinum
Bacillus cereus
Staphylococcus aureus
Clostridium botulinum
Bacillus cereus
Clostridium perfringens
Staphylococcus aureus
Clostridium perfringens
Bacillus cereus
especially rapidly at 85 to 120°F (29.4 to 48.9°C). These
temperatures allow rapid bacterial multiplication. The spores,
which have turned into vegetative cells, multiply rapidly,
possibly producing toxic by-products (e.g., Clostridium
botulinum, Bacillus cereus). When people eat the food
containing the vegetative cells or toxin of these pathogens,
they become ill with diarrhea, vomiting, or neurological
symptoms and death, depending on the specific pathogen or
toxin consumed. The vegetative cells and/or spores are
eliminated in fecal material and return to the environment
through waste disposal and sludge, to cycle again.
THE SPORE CYCLE (CLOSTRIDIA AND BACILLUS)
Food receiving
Cook 130 to 212°F
Hold-serve-leftovers
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The Spore Cycle
Spores
Some rod-shaped pathogenic bacterial cells, such as
Clostridium perfringens, Clostridium botulinum, and Bacillus
cereus, have the ability to form spores. The spore state is a
period of no growth, similar to hibernation, in which the
vegetative cell dries up. The reproductive system becomes
encapsulated in a tough shell or membrane and the outer part
of the old vegetative cell sloughs off. Spore capsules are very
resistant to heat, chemicals, etc. The tough outside coat or
membrane of spores is a survival mechanism brought on by
some environmental stress or removal of nutrients necessary
for multiplication. Spores have survived thousands of years in
the tombs of Egypt and in the Antarctica.
Spores can change into vegetative bacterial cells when
environmental conditions are present to support bacterial
multiplication. When conditions are less than optimum, the
vegetative cells again form spores, which are dormant until
conditions are conducive to cell multiplication.
The Spore Cycle
Both vegetative cells and spores are present in raw foods (e.g.,
fresh meat, fish, poultry, vegetables). Vegetables that have
any contact with the ground will have Clostridium botulinum.
These include onions, garlic, beans, tomatoes, cabbage,
mushrooms, and potatoes. Meat can become contaminated
during slaughter by the dirt on the hide. Fish found near
shores or in bays consume sludge and have Clostridium
botulinum in their intestinal contents. Rice and grain may be
contaminated with Bacillus cereus. Meat and poultry are
often contaminated with Clostridium perfringens because it is
part of the normal intestinal flora of most warm- blooded
animals.
During slow heating of food [i.e., taking longer than 6 hours to
reach a temperature of 130°F (54.4°C)] vegetative cells can
multiply. Cooking food to over 130°F (54.4°C) supplies
sufficient heat, given adequate time, to pasteurize (i.e.,
inactivate to safe numbers) the vegetative cells of pathogenic
bacteria and viruses. Vegetative cells are inactivated by most
cooking processes, but spores survive and are actually
activated by the heating process.
The activated spores germinate into vegetative cells and
multiply during cooling or improper holding of food
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4a-4
References:
Frazier, W.C., and Westhoff, D.C. 1988. Food Microbiology,
3rd ed. McGraw Hill Inc., New York, NY.
International Commission of Microbiological Specifications
for Foods. 1996. Microbial Ecology of Foods. Vol.5.
Microorganisms in Food. Microbiological Specifications
of Food Pathogens. Blackie Academic & Professional,
New York, NY.
Jay, J. M. 2000. Modern Food Microbiology. 6th ed.
Chapman & Hall. New York, N.Y.
Mossel, D.A.A., Corry, J. E. L., Struijk, C. B., and Baird, R.
M. 1995. Essentials of the Microbiology of Foods.
John Wiley & Sons. New York, NY.
Examples of foods produced by process microorganisms
include: pickles, sauerkraut, yogurt, vinegar, cottage cheese,
beer, wine, and bread. See Table 4-2 (next page).
HOW DO YOU KNOW
IF FOOD IS HAZARDOUS OR SAFE?
You control the process.
Note: Histamine may also be produced during the
multiplication of some process microorganisms. The presence
of substantial amounts of histamine in food can cause adverse
reactions in both sensitized and healthy individuals.
Food Spoilers
Do not cause illness.
Change the flavor, odor, and appearance of food.
Inhibit growth of pathogens.
Food Process "Spoilers"?
Used in the production of food products
(e.g., vinegar, bread, sauerkraut, cheese).
They "spoil" the food.
Pathogens
Pathogenic microorganisms cause illness and disease. In
many instances, they have no effect on the odor, taste, or
appearance of the food. Many people even claim that the roast
beef, cake icing, tuna salad, or other food that made them ill
was the best they ever tasted.
Food Pathogens
Cause illness.
Often do not change the flavor, odor, and appearance
of food to indicate that the food is hazardous.
If in doubt about how food was handled after cooking,
throw it out.
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References
Frazier, W.C., and Westhoff, D.C. 1988. Food Microbiology.
4th ed. McGraw-Hill, Inc., New York, NY.
Jay, J. M. 2000. Modern Food Microbiology. 6th ed.
Chapman & Hall. New York, N.Y.
Mossel, D.A.A., Corry, J. E. L., Struijk, C. B., and Baird, R.
M. 1995. Essentials of the Microbiology of Foods.
John Wiley & Sons. New York, NY.
Food Microorganisms - Spoilers, Process
Organisms, and Pathogens
Microorganisms in Food
There are useful as well as harmful microorganisms in food.
Useful microorganisms are used to produce food products
such as bread, cheese, wine, and soy sauce. Harmful
microorganisms are those that cause spoilage in food products
and pathogenic microorganisms that cause illness and disease.
Spoilers
Food spoilage microorganisms do not cause illness. Spoilage
organisms do, however, produce changes in the flavor, odor,
color, and texture of food and food products. For thousands of
years, spices have been used to mask the effects of spoilage
microorganisms in order to make the food edible.
In raw food, spoilage microorganisms are usually present in
much higher numbers than pathogens. Spoilage bacteria are
able to grow more rapidly than pathogenic bacteria at
temperatures below 80°F (26.7°C). Spoilage bacteria are also
able to stop or inhibit the growth of many pathogens by
competitive inhibition. Spoilage bacteria compete with
pathogenic bacteria for nutrients and excrete by-products that
discourage the growth of pathogens.
Spoilage microorganisms are a critical safety factor, especially
in cooked food. When food is cooked, particularly for a long
period of time or to the well-done condition, most of the
spoilage microorganisms are destroyed. If a few pathogens
remain in the food or if the food is recontaminated from
utensils or hands, pathogens will be able to multiply to levels
that make people ill, if given enough time at a favorable
temperature.
Food Process Organisms
Food process organisms are purposely cultured in food to
produce desired flavors and textures. They are used to
produce many food products such as: beer, wine, bread,
cheese, soy sauce, and salami. The multiplication of food
process microorganisms produces by-products such as acids,
carbon dioxide, and alcohol, which help to preserve the food.
If these same microorganisms are allowed to grow in foods
where their presence is not desired, they are called spoilage
microorganisms. Refrigeration and processing are often not
required for these foods because the acidity or alcohol content
of the products prevents the multiplication of pathogens.
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4a-5
Table 4-2
Examples of Microorganisms Used In Processing Food
Organisms
Lactic acid bacteria, species of
Leuconostock, Lactobacillus,
Pediococcus, and /or Streptococcus.
Substrates
Products
Cabbage
Sauerkraut
Cucumber
Pickles
Olives
Olives (green and ripe)
Vanilla beans
Vanilla
Red Meat
Sausages, (salami, Thuringer. Lebanon bologna,
Cervelat, summer sausage, pepperoni)
Milk and cream
Sour cream, cultured butter, ghee
Milk
Cultured milk, acidophilus, yogurt
Milk
Cheese-unripened (cottage, pot, cream)
Milk
Cheese-ripened (Cheddar, American, Edam,
Cheshire
Penicillium roqueforti
Unripened cheese
Cheese (Roquefort, blue, Stilton, Gorgonzola
P. camemberti
Unripened cheese
Camembert cheese
Lactic acid bacteria
Flour (dough)
Sour dough bread and sour dough pancakes
Yeasts
Malt
Beer, ale, stout, lager, bock, porter, Pilsner
Fruit
Wine, vermouth
Molasses
Rum
Grain mash
Whiskey
Flour (dough
Bread
Yeast with Acetobacter or
Gluconobacter
Sugar, fruit, potatoes, honey,
malt, grain alcohol
Vinegar
Halophilic bacteria
Fish
Nuoc-mam-ngapi
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4a-6
hydrophila, and Clostridium botulinum Type E) can multiply.
Foodservice owners/managers who are concerned about both
food safety and spoilage set their refrigeration systems to
operate at 32 to 35°F (0 to 1.7°C), in order to slow bacterial
spoilage and prevent multiplication of all pathogenic bacteria.
Food spoils three to five times faster at 45°F (7.2°C) than at
32°F (0°C).
SPOILAGE MICROOGRANISMS
The quality problem
In order to maintain high quality and product safety, fresh
seafood, poultry products, and fresh meat must be stored at
30°F (-1.1°C) in packaging material or closed containers to
prevent surface drying and cross-contamination. If this
temperature cannot be maintained during shipping and
refrigerated storage, these products must be iced.
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Enzyme Activity
Enzymes are organic catalysts that increase the rate of
chemical reactions. Enzymatic activity is slower as
temperatures are decreased. However, they are still active at
freezing temperatures over long periods of freezer storage.
Spoilage Microorganisms – The Real
Problem
Spoilage Microorganisms
There are many spoilage bacteria. Spoilage bacteria present
an economic problem to the foodservice industry because of
food losses.
Below 25°F (-3.9°C), food quality deteriorates due to
enzymatic action. Food is not considered stable unless stored
below -40°F (-40°C). Between 25 to -40°F (-3.9 to -40°C),
natural enzymes are capable of causing nutrient losses (e.g.,
oxidation of ascorbic acid), changes in flavor and odor due to
the oxidation of fat in food, and changes in protein
components of food.
As bacteria multiply and utilize protein, they break down its
components, frequently producing unstable, volatile byproducts. These compounds contribute to off-flavors and offodors in food. Common by-products are ammonia and sulfur
compounds.
When meat is frozen at 28.5°F (-3.9°C), there are still tiny
pockets of water in the food that gradually freeze as the
temperature is reduced to -40°F (-40°C). Enzymatic reactions
occur within these tiny pockets over a period of months to
produce adverse effects in meat quality, primarily flavor.
Yeasts produce carbon dioxide, alcohol, and acids from
fermentable sugars. If catsup is stored at room temperature
after it is opened, it may become contaminated with yeast.
When yeasts grow in catsup, the flavor changes due to the
production of alcohol. Visible gas bubbles of carbon dioxide
may appear in the catsup.
Some raw foods are heated prior to freezing in order to
inactivate enzymes, maintain quality, and extend the shelf life
of the products. For example, most frozen vegetables are
blanched (i.e., heated in steam or water just long enough to
inactivate enzymes) prior to freezing. If vegetables are frozen
unblanched, their quality decreases rapidly.
Mold growth causes spoilage of many foods, which include
fruits, vegetables, meats, cheese, and cereals. The color,
texture, flavor, and odor of foods are changed as a result.
Some spoilage bacteria, notably Proteus morganii, produce
chemicals such as histamines that can cause a rapid onset of
foodborne illness. Histamine is a bacterial breakdown product
of proteins, particularly in fish and shellfish.
Multiplication Requirements
Some spoilage bacteria begin to multiply at approximately 23
to 25°F (-5 to -3.9°C). Meat thaws at about 28.5°F (-2°C).
The significance of this is that spoilage microorganisms begin
to multiply when the food is still frozen and some multiply
actively at 32°F (0°C). Optimum multiplication occurs at 85 to
90°F (29.4 to 32.2°C). Multiplication of most bacteria stops at
about 115°F (46.1°C), and bacterial cells are slowly
inactivated as temperatures rise above this point.
Some pathogenic bacteria can begin to multiply at 29.3°F
(-1.5°C), (Hudson et al., 1994). The USDA recommends that
food storage refrigerators be maintained at 40°F (4.4°C) or
below. The FDA recommends a temperature of 41°F (5°C) or
below to prevent pathogenic bacterial multiplication. When
refrigerators or coolers are set at 40 to 45°F (4.4 to 7.2°C),
spoilage bacteria and bacterial pathogens (e.g., Listeria
monocytogenes, Yersinia enterocolitica, Aeromonas
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4a-7
Freezer Temperature
The quality retention of frozen products is maintained for
longer periods of time if freezer units are set at -10°F
(-23.3°C) or below. Freezer storage units should maintain
stable temperatures. Fluctuations of temperature ±5°F
(±2.8°C) are detrimental to the food quality due to the
formation of large ice crystals that form when small ice
crystals thaw and recrystalize during refreezing.
References:
Hudson, J.A., Mott, S.J., and Penney, N. 1994. Growth of
Listeria monocytogenes, Aeromonas hydrophila,
Yersinia enterocolitica on vacuum and saturated carbon
dioxide controlled atmosphere-packaged sliced roast
beef. J. Food Protect. 57 (3): 204-208.
International Commission of Microbiological Specifications
for Foods. 1998. Microbial Ecology of Foods. Vol. 6.
Microbial Ecology of Food Commodities. Blackie
Academic & Professional, New York, NY.
Jay, J. M. 2000. Modern Food Microbiology. 6th ed.
Chapman & Hall. New York, N.Y.
Mossel, D.A.A., Corry, J. E. L., Struijk, C. B., and Baird, R.
M. 1995. Essentials of the Microbiology of Foods.
John Wiley & Sons. New York, NY
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4a-8
highly heat-resistant Salmonella senftenberg 775 W, which is
very difficult to inactivate, is not included as a test organism.
S. senftenberg has only been implicated in one foodborne
illness, as far as is known, and is therefore not considered to
be a threat on which food process standards should be based.
FOOD SAFETY MICROBIOLOGY
HACCP process control vs. finished product sampling
•
•
•
•
•
•
•
•
•
Commercial sterilization: destruction of Clostridium botulinum spores
Foodservice pasteurization: reduce infective microorganisms to a safe
level
Raw or rare food must have supplier certification
Refrigeration holding: 41ºF, 7 days (or 10 multiplications equivalent
Heating: 41 to 130ºF in <6 hours
Salmonella 5D pasteurization: 130ºF, 86.45 minutes; 140ºF, 8.65 minutes;
150ºF, 51.9 seconds; 160ºF, 5.19 seconds
Hot holding: 130ºF (safety); 135ºF (FDA)
Cooling:
USDA - 120 to 55°F, <6 hours; continue to 40°F to prevent spore
outgrowth and multiplication of Clostridium perfringens;
FDA - 135 to 70°F within 2 hours, followed by cooling to 41°F, 6 total
hours
Thermally resistant microorganisms
The USDA has also identified that the process should be able
to reduce the population of Listeria monocytogenes by 10,000
to 1. Listeria monocytogenes is slightly more heat resistant
than Salmonella. However, the required 105 Salmonella cell
reduction process will inactivate 104 cells of Listeria
monocytogenes. It is therefore possible for processing
operations to continue using existing processing standards
based on Salmonella spp. reduction.
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Food Safety Microbiology
Microbiological Foundations for HACCP-Based
Process Control
When food is purchased, raw, unprocessed food must be
assumed to be contaminated with low levels of infective and
spore-forming pathogens. Periodically, there may be levels of
pathogen contamination that can cause an immediate hazard.
Most foodservice cooking processes do not heat food long
enough to reduce spore contamination, but do provide
sufficient thermal energy to inactivate the vegetative cell
forms of pathogens to a safe level.
Process Control vs. Finished Product
Microbiological Control
In the past, the food microbiologist has relied on finished
product sampling procedures to assure the safety of the food.
HACCP principles require that the pathogen level in the
finished product should be below normal microbiological
detectable limits. To assure the safety of a product (i.e., an
infective pathogen level of 1 microorganism per 100 grams of
food) through microbiological testing, the total output of the
process would need to be evaluated. This is impractical. The
commercial canning industry has determined times necessary
for thermal destruction of spores of Clostridium botulinum in
cans of food. (Processing times and temperatures are based on
reducing the number of spores of C. botulinum from 1012 to 1.)
When commercial canning processes operate according to
these recognized safety guidelines, the safety of unopened
cans of foods stored at room temperature is assured.
Pasteurization in Foodservice vs. Processing
D-value is the time at a specific temperature for the reduction
of the microbiological population by 1 log or a factor of 10 to
1. In designing a HACCP-based safety-assured process, the
object is to identify the approximate incoming load of
pathogens and then apply sufficient heat to reduce this
population of pathogens by a specified amount. In chilled
food processing plants, the USDA has identified D-values
(i.e., times at specified temperatures) required for preparing
meat and meat products. Salmonella spp. has been used as the
test or control organism; times and temperatures for
processing are based on reducing a population of 100,000
Salmonella cells to 1.
It is important not to set processing standards that force foods
to be over-processed without really reducing the risk. The
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4a-9
Foodservice Food Pasteurization
Food used or prepared in foodservice units usually has very
low levels of pathogens and is not subjected to the same
degree of mishandling that occurs when commercial
processors of food release their products for distribution and
sale in the retail marketing system. In foodservice, it is very
unlikely for processed food to have more than 1,000
Salmonella spp. Under most conditions, healthy people can
eat 1,000 Salmonella and not become ill. If cooking/heat
processing times for destruction of 100,000:1 Salmonella are
used, pasteurization should be adequate. Temperatures and
times necessary for this 100,000:1 Salmonella reduction are:
130°F (54.4°C) for 86.43 min.; 140°F (60.0°C) for 8.64 min.;
150°F (65.6°C) for 0.864 min.; and 160°F (71.1°C) for 0.0864
min. The reason that food must be cooked at the retail level is
basically a result of HACCP failures by persons who grow,
harvest, and process raw ingredients.
Serving Rare or Raw Food
When raw food, such as fruits and vegetables, are washed,
there is some reduction in the microbial population. If water
alone is used, the population can be reduced 10 to 1 or more.
If the products are washed in a 200-ppm chlorine solution or
5% acetic acid at a temperature of 130 to 140°F (54.4 to
60°C), there will be a 100 to 1 reduction. While chemical
disinfectants are used in the food processing industry, they
should not be used in the retail sector. If these foods have an
unacceptable microbial population, the source of supply
should be changed.
If rare and raw food is served in foodservice establishments,
suppliers must be required to provide microbiological
certification that indicates the pathogen level of the products is
below that which is hazardous to the health of people.
Other Process Controls
In addition to thermal inactivation, there are other controls that
must be in place. These include the following:
1. The sanitizing process must reduce the pathogen
population to a low enough level to avoid a crosscontamination problem. The sanitation process provided
by reputable chemical supplies must meet the
government requirement of 100,000-to-1 microorganism
reduction (99.999% reduction).
2. The multiplication rate of microorganisms at
refrigeration and elevated temperatures must be
understood so that the food will not be held too long at
hazardous temperatures. It is not possible to totally halt
3.
4.
5.
6.
pathogen multiplication unless food is stored below 29°F
(-1.5°C). It is reasonable to limit multiplication to no
more than 10 generations.
Prevent multiplication of Clostridium perfringens during
heating by cooking food from 41 to 130°F (5 to 54.4°C)
in less than 6 hours.
Provide adequate pasteurization for the number of
microorganisms present in the food (as mentioned
above).
Hold hot food above 130°F (54.4°C) to prevent the
multiplication of pathogens. [The FDA Food Code
recommends holding food at or above 135°F (57.2°C).]
Cool food continuously from 120 to 55°F (48.9 to
12.8°C) in less than 6 hours, then continue to cool food
to 40°F (4.4°C) to prevent spore outgrowth and
multiplication of Clostridium perfringens (according to
USDA Guidelines). [The FDA Food Code recommends
cooling potentially hazardous food from 135 to 70°F (57
to 21°C) within 2 hours; followed by cooling to 41°F
(5°C) or below within with in a total time of 6 hours or
less.]
Infective and Spore Control Process Design
It is not necessary to check a process for all the pathogenic
microorganisms. The following organisms represent the
control standards at various temperatures at which to base
process design:
1. Growth at refrigeration temperature: Listeria
monocytogenes is the organism of choice because it is
very common in the environment and will multiply under
all types of environments beginning at a temperature of
29°F (-1.5°C). Clostridium botulinum Type E, which
begins to multiply at 38°F (3.3°C), is also a potential
hazard if food, particularly vacuum packaged fish, is
kept for a long time (over 21 days at above 38°F (3.3°C)
after it has been cooked.
2. Control of growth at 60 to 127.5°F (15.6 to 53.1°C):
Clostridium perfringens is the microorganism of choice
for control in this temperature range. The reason for this
is that it multiplies faster than any other microorganism
in this range.
3. The organism of choice for destruction in a
temperature range of 130 to 160°F (54.4 to 71.1°C) is
Salmonella, because if Salmonella is reduced 100,000 to
1, all of the parasitic and vegetative cells will also be
controlled. There is some speculation that viruses may
be more thermally resistant than Salmonella. However,
it appears that viruses can be partially controlled by
correct hand washing and prevention of crosscontamination of the food.
Thermally Resistant Organisms
Staphylococcus aureus and Streptococcus spp. are more
resistant than Salmonella spp. to thermal inactivation. It can
be expected that low levels will survive the cooking process, if
there are more than 100 cells per gram in the raw product.
If food is properly refrigerated below 41°F (5°C), then neither
of these organisms can multiply, and low numbers of these
microorganisms can be tolerated in the final product without
becoming a hazard to the health of consumers.
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4a-10
Summary
1. Any food can become hazardous.
2. The sources of the hazard(s) must be assessed.
3. It is important that suppliers have HACCP programs and
pathogen certification so that only very low levels of
pathogens are present in incoming food products.
4. Critical process controls must be used to prevent hazards
from causing a foodborne illness.
5. Measurement of processing time and temperature must
be used to assure that processing and preparation
procedures are sufficient to ensure safety.
Toxin-Producing Bacteria
Some bacteria produce toxins as a waste product when they
multiply. The toxins may be excreted into the surrounding
medium or food (exotoxins), or retained within the cell
(intracellular toxins). They are released when the cells
disintegrate in the human intestine after contaminated food is
eaten. Exotoxins produced by Staphylococcus aureus and
Bacillus cereus are heat resistant and require temperatures
above 212°F (100°C) for many minutes for their destruction or
inactivation. Fortunately, the toxins of Clostridium botulinum,
which are extremely lethal, are relatively easily destroyed by
heat. If these toxins are heated to 185°F (85°C) for 5 minutes,
they are inactivated. When foods are cooked, toxins may not
be destroyed and their production in food must be prevented.
BACTERIA
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6
Bacteria
Bacterial Structure, Identification, and Classification
Bacteria are so small that they can be seen only by using a
microscope. They measure 0.05-2.0 by 2.0-10.0 micrometers.
Bacteria are structurally simple cells that contain a nuclear
region in place of a true nucleus. The shape and size of a
bacterial cell is one of the first clues to its identification.
Bacteria can have the shape of a rod, a sphere, a comma
(Vibrio), or a spiral. Some bacteria are pleomorphic and can
assume more than one shape. Some types of bacterial cells
contain flagella or tail-like structures, which give the cells
mobility. When viewed through a microscope, the shape of
bacteria and their cellular association in chains, clusters, and
tetrads is important for their identification and classification.
Most bacteria multiply by a process called binary fission, a
division process that results in two equal cells forming when
one bacterial cell divides. Some bacteria divide by budding.
Budding results in cells of unequal size.
Spore-Forming Bacteria
The Clostridium and Bacillus, which are members of the
family Bacillaceae, are capable of forming spores
(endospores) when subjected to adverse conditions. The
process is called sporogenesis. Spores have no detectable
metabolic activity, and are able to survive for thousands of
years as a resting form of the cell. Bacterial spores are more
resistant to heat, drying, and chemicals than their viable cell
forms.
Growth Requirements
All bacteria have relatively specific requirements for growth.
These include food or nutritional requirements, temperature,
moisture, atmosphere (i.e., ability to multiply with or without
oxygen), and acidity. Requirements for growth vary with the
kind of bacteria and within strains of a species of bacteria.
Methods of Control
Bacteria can be killed with heat, chemicals, or ionizing
radiation. High temperatures denature proteins and nucleic
acids by breaking their hydrogen bonds. When this happens,
the proteins unfold and the double stranded nucleic acids
(DNA) separate. The bacterial cells are no longer capable of
reproduction. Ionizing radiation inactivates vegetative cells
by causing chemical changes within the nitrogenous bases
(units) of nucleic acids.
Groups of Bacteria Important in Food Microbiology
Bacteria are often grouped according to temperatures of
growth. Table 4-3 tabulates these different growth
temperatures.
Table 4-3
Groupings of Microorganisms Based on Temperatures of
Growth *
Spores in food become activated when food is cooked. For
example, the standard laboratory procedure for activating
spores of Clostridium perfringens is to heat the spore culture
in a beef broth media to 176°F (80°C) and hold the culture at
this temperature for 20 minutes. Activated spores then
undergo a process of germination to form viable (living) cells
when cooled to suitable growth temperatures of 80 to 120°F
(26.7 to 48.9°C).
Type
Psychrophiles
Psychrotrophs
Mesophiles
Thermotrophs
Thermophiles
In order to destroy the thermally resistant forms of
Clostridium botulinum Types A and B, the standard
inactivation procedure for spores, used by the canning
industry, is to heat can contents of low-acid food to a
temperature of 250°F (121.1°C) for 3 minutes at the coldest
spot within the can.
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Toxins are also classified as to their physiological effect (i.e.,
effect on humans or animals if consumed). For example,
toxins that cause gastroenteritis or inflammation of the lining
of the stomach and intestines, such as the toxin produced by
Staphylococcus aureus, are called enterotoxins. Toxins that
affect the central nervous system, such as those produced by
Clostridium botulinum, are termed neurotoxins.
Minimum
Temp.
°F
32
41
1-50
59
104
Optimum
Temp.
°F
50
77
36-99
107-115
113-131
Maximum
Temp.
°F
68
95
113
122
140-176
* Adapted from Essentials of Microbiology of Foods by
D.A.A. Mossel.
Bacteria are sometimes grouped according to their metabolic
by-products and other conditions that either support or allow
their growth. Many bacteria possess more than one of these
4a-11
common characteristics, as is indicated by the following types
or groups.
of psychrotrophic bacteria include Pseudomonas spp. which
cause spoilage in meat and poultry.
Acid-forming bacteria are capable of metabolizing sugars, other
carbohydrates, and alcohol to form organic acids. Acid-forming
bacteria include: lactic acid-forming bacteria (e.g., Lactobacillus
acidophilus, Streptococcus lactis), acetic acid-forming bacteria
(e.g., Acetobacter, Gluconobacter), butyric acid-forming bacteria
(e.g., Clostridium), and proprionic acid-forming bacteria (e.g.,
Proprionibacterium).
Halophilic bacteria or halophiles require certain minimal
concentrations of dissolved salt (sodium chloride) for growth.
Salt requirements vary from as low as 2% to as high as 30%
salt. Halobacterium require salt for growth.
Proteolytic bacteria produce enzymes that are capable of
decomposing proteins into foul-smelling compounds such as
hydrogen sulfide, amines, indole, and amino acids. Clostridium
putrefaciens and Clostridium botulinum Type A are examples of
proteolytic bacteria.
Lipolytic bacteria produce enzymes that are capable of
splitting fats into fatty acids and glycerol. Pseudomonas fragi
and Staphylococcus aureus, if present in raw milk, produce
heat-resistant lipases, which may survive pasteurization
[161°F 72.2°C)] and cause development of off-flavors in milk
during distribution.
Saccharolytic bacteria produce enzymes that split complex
sugars and starches into simple sugars or smaller
carbohydrates. Examples of saccharolytic bacteria are Bacillus
subtilis and Clostridium butyricum.
Pectolytic bacteria produce enzymes that cause pectin to
hydrolyze or split into smaller molecules. As a result there is
softening of plant tissues and loss of gelling capability of fruit
juices. Erwinia carotovora causes raw fruits and vegetables to
have a water-soaked appearance, a soft, mushy consistency,
and often, bad odor.
Thermophilic bacteria, or thermophiles (i.e., hightemperature-loving bacteria), have an optimum temperature
for growth of 113°F (45°C), but can grow at 132°F (55.6°C)
and above. Bacillus stearothermophilus is an example of a
thermophilic bacteria that causes flat sour spoilage of canned
foods stored at high temperatures. These spoilage bacteria
will multiply in food held at hot holding temperatures [135 to
150°F (57.2 to 65.5°C)].
Thermotrophic bacteria, or facultative thermophiles, are
bacteria that are tolerant of high temperatures. An example of
a thermotrophic bacteria is Bacillus coagulans, which causes
flat sour spoilage of acid foods such as tomatoes and tomato
juice. The spore forms of both thermophilic and
thermotrophic bacteria can survive ordinary cooking and cause
food to spoil, even if held at 140°F (60°C)
Mesophilic bacteria are bacteria that grow in the middle
temperature range. Their optimal temperature for growth is 86
to 99°F (30 to 37°C). Most foodborne pathogens (e.g.,
Shigella spp., Staphylococcus aureus, Salmonella spp.) grow
rapidly in this temperature range.
Psychrophilic bacteria are those bacteria whose optimum
temperature for growth is 50°F (10°C) or lower. Vibrio
parahaemolyticus, Vibrio cholerae, and Vibrio vulnificus are
examples of psychrophilic bacteria that may be found on fish
and seafood.
Psychrotrophs have an optimal temperature for growth of
77°F (25°C) but can grow at 41°F (5°C) or lower. Examples
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4a-12
Halotolerant bacteria are salt tolerant and can grow with or
without salt. Staphylococcus aureus can grow well without
salt, but it can grow well in 7 to 10% concentrations of salt.
Some strains grow in 20% salt concentrations.
Osmophilic and saccharophilic bacteria are bacteria that
grow in high concentrations of sugar. Most bacteria that are
called osmophilic are merely sugar tolerant (e.g., some
Leuconostoc spp.).
Pigmented bacteria produce various colors on or in foods as
a result of their growth in foods. An example of a pigmented
bacteria is the rust-colored Lactobacillus plantarum, which
discolors cheese.
Slime- and rope-forming bacteria cause ropiness in milk and
beer and produce a slimy surface growth on various foods.
Enterobacter aerogenes causes ropiness in milk. Bacillus
mesentericus causes rope in bread, and the bread smells like
ripe cantaloupe.
Gas-forming bacteria produce carbon dioxide or both carbon
dioxide and hydrogen. Some genera of Leuconostoc,
Lactobacillus, Escherichia, Enterobacter, Proteus, Bacillus,
and Clostridium are gas-forming bacteria.
References:
Frazier, W.C. and Westhoff, D.C. 1988. Food Microbiology.
Fourth edition. McGraw-Hill, New York, NY.
Jay, J.M. 2000. Modern Food Microbiology. 6th edition.
Chapman & Hall Inc., New York, NY.
Prescott, L. M., Harley, J. P., and Klein, D. A. 1996.
Microbiology. W. C. Brown. Dubuque, IA.
Mossel, D.A.A., Corry, J. E., Struijk, C. B., and Baird, R.
1995. Essentials of the Microbiology of Foods. John
Wiley and Sons, New York, NY.
end of the mother cells, it is called polar budding. If the bud
forms at both ends, it is bipolar budding. When buds appear
any place on the mother cell this is called multilateral budding.
YEASTS
Yeasts can change in their physiological characteristics,
especially the true yeasts, which have the sexual method of
reproduction. These types of yeast can mutate or be bred to
new forms. Most yeast can adapt to conditions, which
previously would not have supported their multiplication. For
example, there are a large number of strains of Saccharomyces
cerevisae that are best suited for different uses (e.g., bread
strains, beer strains, wine strains and high-alcohol-producing
strains).
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Yeasts
General Characteristics
Yeasts have been defined as fungi with a unicellular form.
There are over 350 species of yeast, which are classified into
39 genera. Yeasts are microscopic organisms that are
differentiated from bacteria by their larger cell size, and by
their production of buds during the process of division. Yeast
cells may be oval, elongated, elliptical, or spherical in shape.
Their size varies from 5 to 8 millimicrons in diameter. Some
yeasts may be as large as 100 millimicrons in length. Older
yeast cells tend to be smaller than young multiplying cells.
Most yeasts are not pathogenic. They are important in food
manufacturing (e.g., bread, beer) but can cause foods to spoil
when their multiplication is not desired (e.g., fermentation of
catsup and fresh fruit juices).
Multiplication Requirements
Yeasts multiply over a wide range of pH, alcohol, and sugar
concentrations. In general, yeasts require sugar as a source of
energy. As a result of this metabolism by-products of carbon
dioxide and alcohol are produced. This process is called
fermentation. Other yeasts, such as film yeasts, oxidize
organic acids and alcohol. Yeasts also have nutritional
requirements for a source of nitrogenous compounds and
minerals. This requirement varies with the type and strain of
yeasts.
Most yeasts multiply best with a plentiful supply of water or
moisture. Some yeasts are capable of multiplying in high
concentrations of salt and sugar. Yeasts are classified as
ordinary yeasts if they do not multiply in high concentrations
of sugar and salt and as osmophilic yeasts if they are capable
of multiplication in these conditions. The lower limits of
water activity (aw) range from 0.88 to 0.94 for ordinary yeasts.
Osmophilic yeasts can multiply in media such as syrups with
an aw as low as 0.62 to 0.65. Each type of yeast has its own
characteristic optimal aw and range of aw for multiplication.
Candida albicans is a pathogenic yeast. It can invade the
epidermis (skin) and mucous membranes of the body,
particularly those of the mouth, intestinal, urinary and
reproductive tract. It is of concern for infants (a cause of
thrush) and for immune-compromised individuals.
The range for optimal temperature for multiplication of most
yeasts is 77 to 86°F (25 to 30°C). The maximum
multiplication temperature ranges from 95 to 117°F (35 to
47°C). Some kinds of yeast multiply at 32°F (0°C) or less.
Some yeasts are pigmented or colored. When these pigmented
yeast multiply in food, streaks of color provide evidence of
their presence (e.g., red, pink, black, or yellow streaks of
color) in food products.
The pH for optimum multiplication of most yeasts is in the
acid range of 4 to 4.5 pH. Yeasts do not multiply well in
alkaline conditions, unless they adapt to these conditions.
Most yeasts multiply best under aerobic conditions, but some
types can multiply slowly, anaerobically.
Reproduction
On the basis of reproduction, yeasts can be separated into four
groups. Only two of these groups contain yeasts involved
with foods. One group of yeasts found in food is called
Ascomycetes, or true yeasts. True yeasts reproduce by sexual
reproduction. True yeasts produce asexual spores and
chlamydospores. Chlamydospores are very durable and are
produced when yeasts find environmental conditions
unfavorable for multiplication.
The other group of yeasts found in food is asporogenes yeasts
(i.e., false, or wild yeasts) because they do not display sexual
reproduction and form no spores. Vegetative reproduction
refers to asexual reproduction. All yeasts can reproduce
asexually, and this is the only method for asporogenes yeasts.
The usual vegetative (asexual) reproduction is by budding.
Some yeasts reproduce by fission or by an intermediate system
called bud fission. If a new cell or bud appears at the short
1901-04: ch4a rev 6/16/05 print 3/7/16
4a-13
Methods of Control
Yeasts are destroyed when heated to temperatures of 131 to
149°F (55 to 65°C) for a few minutes. Most cooking
procedures and pasteurization procedures reach temperatures
and times that are sufficiently high enough and long enough to
inactivate yeasts. However, yeasts can recontaminate food
products. Care must be taken to prevent this from occurring.
After products have received these treatments, they should be
covered and sealed in containers to prevent recontamination,
and stored at refrigerator or freezing temperatures.
Yeasts in Food Products
Yeasts are associated with nearly all types of food products.
Yeasts cause spoilage of various food products, particularly
those containing sugars, brined foods, and fruits. Yeasts are
also important in processing of foods: in the fermentation of
alcoholic beverages, the baking industry (i.e., bread
production), and as a single-cell protein source.
Fresh vegetables, meat, poultry, and cheese often contain
yeasts, but usually bacteria in these foods out-number and outmultiply the yeasts. If bacteria are destroyed or their
multiplication is inhibited, yeasts can dominate. For instance,
products with high concentrations of sugar such as honey and
molasses will not support the multiplication of most bacteria,
but will support the multiplication of some yeasts such as
Saccharomyces rouxii, which is known to cause spoilage in
these products.
Trichosporon multiply best at low temperatures. These yeasts
are found on various foods such as fresh shrimp, crab, beef,
butter, cheese, fruit, fruit juice and rice. T. pullulans is a
common species.
Rhodotorula multiply on foods to produce red, pink, or yellow
spots (e.g., colored spots on meats or pink areas in sauerkraut).
Groups of Yeast Important in Food Microbiology
True Yeasts
Saccharomyces reproduce by budding and ascospore
formation. The most important species of this group is
Saccharomyces cerevisiae has many uses in food production.
Special strains are used to leaven bread, to produce wine and
beer, and for the production of alcohol and glycerol (i.e.,
glycerine). Other species of Saccharomyces include: S.
carlbergensis, which is used to make beer; S. fragilis and S.
lactis, which ferment lactose in milk; and S. rouxii and S.
mellis, which are osmophilic and multiply in high sugar
solutions such as maple syrup and honey.
References:
Chin, J. ed. 2000. Control of Communicable Diseases in
Man. 17th edition. American Public Health Assoc.
Washington, D.C.
Frazier, W.C. and Westhoff, D.C. 1988. Food Microbiology.
Third edition. McGraw-Hill, New York, NY.
Jay, J.M. 2000. Modern Food Microbiology. 6th edition.
Chapman & Hall Inc., New York, NY.
Mossel, D.A.A., Corry, J. E., Struijk, C. B., and Baird, R.
1995. Essentials of the Microbiology of Foods. John
Wiley and Sons, New York, NY.
Schizosaccharomyces reproduce by fission and ascospore
formation. This group of yeast has been found in tropical
fruits, molasses, soil, and honey.
Zygosaccharomyces are capable of multiplication in high
concentrations of sugar, and cause spoilage of honey, syrups,
and molasses. Strains of this group are also used in the
production of soy sauce and some wines.
Pichia oxidize alcohol to form films on wine and beer (e.g, P.
membranaefaciens).
Hansenula oxidize alcohol and organic acids and form films
on beer, sauerkraut, and other brined products.
Debaryomyces are very salt tolerant and form films on meat
brines. D. kloeckeri causes spoilage when it multiplies on
cheese and sausage.
Hanseniaspora are lemon-shaped yeasts that multiply in fruit
juices and wine to produce compounds, which give these
products off-flavors. Nadsonia is one of these species.
False Yeasts
Torulopsis are round or oval, fermentative yeasts that
reproduce by budding. T. sphaeric causes spoilage in milk
and dairy products due to its ability to ferment lactose. Other
species cause spoilage of sweetened condensed milk, fruitjuice concentrates, and acid foods.
Candida form films and are capable of causing spoilage in
foods high in acid and salt. C. lipolytica can spoil margarine
and butter. Some strains have benefit in food production. For
instance, C. utilis is grown for food and feed, and C.krusei is
sometimes grown with dairy starter cultures to maintain
activity and increase longevity of lactic acid bacteria.
C. albicans is pathogenic and has the potential of being spread
by foodservice personnel who are carriers and who use poor
personal hygiene. A typical mode of transmission would be
failure to wash hands after using the toilet and then touching
food items that receive no heat treatment prior to consumption
(e.g., salads and cold hors d'oeuvres).
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Brettanomyces produce high amounts of acid and are used in
the late fermentation of some beers and wines in order to
produce characteristic flavor. B. bruxellansis and B. lambicus
are typical of this species.
4a-14
Table 4-4
Approximate Minimum Water Activity (aw) Values for the
Growth of Microorganisms in Foods *
MOLD
Organism
aw
Most spoilage bacteria
Most spoilage yeasts
Most spoilage molds
Halophilic bacteria
Xerophilic molds
Osmophilic yeasts
0.90
0.88
0.80
0.75
0.61
0.61
* Adapted from Jay, J.M. 2000. Modern Food Microbiology.
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Mold
General Characteristics
Mold is a term that is applied to certain multicellular,
filamentous fungi whose growth on food is readily recognized
by its fuzzy or cottony appearance. Molds grow rapidly and
can cover several inches of area in a few days. Mold growth
commonly appears white but may be colored or smoky grey.
Reproduction
The total mass of the mold or any large single portion is called
the mycelium. The mycelium is composed of branches or
filaments called hyphae. The hyphae may be submerged (i.e.,
growing within the food), or aerial (i.e., growing into the air
above the food). Molds are divided into two groups on the
characteristics of their hyphae. Septate molds have cross
walls that divide the hypha into cells. Nonseptate molds have
hyphae that consist of cylinders without cross walls. The
nonseptate hyphae have nuclei scattered throughout their
length and are considered multicellular.
Reproduction of molds is chiefly by means of asexual
reproduction. At the time of asexual reproduction,
sporangiophores or conidophores are formed, which produce
sporangiaspores or conidia at their tips. Molds also produce
other asexual spores. Chlamydospores are formed when a
thick wall develops around any cell of the mycelium.
Arthrospores are formed by some molds that produce septate
mycelium. (Septate mycelium are capable of separating into
units or segments.) Chlamydospores and arthrospores are
more resistant to changes in environmental conditions. Molds
also reproduce by sexual means when they form either
ascospores, oospores, or zygospores.
Growth Requirements
Most molds require less available moisture than most yeasts
and bacteria. (See Table 4-4.) A total moisture content below
14-15% in foods such as flour or dried fruits prevents mold
growth.
Most molds grow well at ordinary temperatures. The optimal
temperature for growth is 77 to 86°F (25 to 30°C). A number
of molds are psychrotrophic and grow well at refrigeration
temperatures. Some molds grow at temperatures below
freezing [i.e., at 14 to 23°F (-10 to -5°C)]. A few molds are
thermophilic and have a high optimal temperature.
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Molds are aerobic. They require oxygen for growth. Molds
grow over a wide pH range (i.e., pH 2 to 8.5). Molds grow on
many foods. Molds grow on moist and dry foods, acid and
non-acid foods, and in foods that are high or low in sugar and
salt.
Mycotoxins
Although most molds are not considered to be pathogenic,
some produce mycotoxins that are very toxic and are a health
hazard. Mycotoxins produced by molds generally have an
effect on liver and kidney functions. Some mycotoxins can
have an effect on the central nervous system. A mycotoxin of
current concern is aflatoxin. Aflatoxin is produced when
Aspergillus flavus grows in grains, nuts, and legumes that
contain higher levels of moisture. Aflatoxin is a liver
carcinogenic compound. Aflatoxins are destroyed in grains
and cereals by heat processing products at high temperatures
above 250°F (121.1°C).
Methods of Control
Certain chemical compounds are mycostatic (i.e., inhibit mold
growth). Sorbic, proprionic, and acetic acids are used in food
products for this purpose. Initiation of mold growth is slow
when compared to bacteria or yeasts, and the growth of these
microorganisms competitively inhibit mold growth. If
cooked, pasteurized, or other heat-processed foods are
contaminated by molds, their growth in foods will be quite
rapid. Care must be taken to prevent moldy food products
from contaminating fresh foods.
Equipment surfaces, refrigeration units, and freezers must be
cleaned and sanitized regularly to prevent mold growth and
contamination.
Vegetative molds are destroyed during cooking and heat
processing, but some mold spores can survive heat processing.
Food that is excessively moldy should be discarded. If there is
any doubt about the safety of molded food, it should be
discarded.
The FDA has specified that if there is mold on cheese, the
mold on the cheese must be cut off. An additional 1/2 inch of
cheese beneath the mold should also be cut off and discarded.
Molds in Food Products
Molds are considered to be spoilage organisms in food
products where their growth is not desired. The appearance of
mold on products is an indication of spoilage, but molds can
degrade food products before growth is evident.
4a-15
Molds are also useful in the processing of many foods such as
cheese and soy sauce. Their enzyme systems have been
isolated and used for food processing (e.g., isolation and
extraction of amylases, pectinases, proteinases, and lipases).
Some molds are used to convert waste products into usable
animal food products. Some molds are a source of vitamins.
Some molds are a source of antibiotics such as penicillin.
Groups of Molds in Food Products
This is a partial list of molds of importance in food products.
Aspergillus appear yellow to green to black on a large number
of foods. They have septated mycelia and produce conidia
(i.e., free spores). The growth of Aspergillus flavus in cereals,
grains, legumes, and nuts produces aflatoxin. Other species of
Aspergillus are used to produce citric acid and proteases.
Aspergilli are found on cakes, fruits, vegetables, meats, and
other products. Aspergillus glaucus is a common cause of
mold on hams and sausage.
Cladosporium are composed of septated mycelium and
produce conidia. One species, C. herbarum, grows on
connective tissue or fat covering of meat when refrigerated for
several days, producing black spots on meat.
Fusarium (Gibberella) The mycelium produced by the
growth of these molds produces a cottony growth that has
tinges of pink, purple, and yellow. They cause spoilage of
many fruits and vegetables, including "neck rot" of bananas.
Some Fusarium produce T-2 toxin (a neurotoxin) and
vomitoxin.
Geotrichum are yeastlike fungi that are usually white. They
have septated mycelium and reproduction occurs by
fragmentation of the mycelium into arthrospores. They are
sometimes referred to as "dairy mold" since they produce
flavor and odor in many types of cheese. They are also
referred to as "machinery molds" since they build up on foodcontact equipment in food-processing plants. The mold is
killed during thermal processing of the food, but the hyphae
can be determined by microscopic examination. The presence
of mold in canned foods is considered to be an adulterant and
indicates inadequate sanitation during processing.
Geotrichum also infect ripe fruits.
Penicillium produce septate mycelia and form conidia. The
growth of this species of mold produces blue to blue-green
colors on food. P. digitatum causes green mold rot, and P.
italicum causes blue mold rot of citrus fruits. Penicillium
expansum causes soft, blue mold rot of apples, peaches, and
pears. Species of Penicillium are found growing on the fat
and connective tissue of meat stored in the refrigerator and in
moldy bread. Other species of Penicillium are used to produce
Camembert and Brie cheese. P. Roqueforti is used to produce
Roquefort, Gorganzola, and other blue-veined cheeses. Some
species of Penicillium are used to produce antibiotics such as
penicillin. Some people are allergic to this mold.
Rhizopus have nonseptated mycelia and produce spores. They
are very widespread in nature and can be found growing on
bread, cakes, preserves, and fruits. Rhizopus stolonifer is
often called bread mold. Some species of Rhizopus are used
to convert starch to alcohol.
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4a-16
Thamnidium have nonseptated mycelia and produce spores.
They are sometimes found on refrigerated meats, especially
hind quarters that have been refrigerated for a long period of
time, where they cause "whiskering" of the meat. They are
also found in decaying eggs.
Byssochlamys produce ascospores. The ascospores of these
molds are heat resistant and produce spoilage in high-acid
canned foods as this organism can grow at low oxygen levels.
They exist in soils and can be recovered from ripening fruits,
especially grapes. They are the most heat resistant of all
spoilage molds.
References:
Frazier, W.C. and Westhoff, D.C. 1988. Food Microbiology.
Third edition. McGraw-Hill, New York, NY.
Jay, J.M. 2000. Modern Food Microbiology. 6th edition.
Chapman & Hall Inc., New York, NY.
Mossel, D.A.A., Corry, J. E., Struijk, C. B., and Baird, R.
1995. Essentials of the Microbiology of Foods. John
Wiley and Sons, New York, NY.
that cause enteric illnesses because it is yet impossible to
culture them in a laboratory.
VIRUSES
Methods of Control
Foodservice workers must wash their hands, using a fingernail
brush by the double hand wash method in order to assure that
all fecal pathogens, which include viruses, are removed from
their hands and fingernails. Only a safety-assured source of
water should be used in food preparation and foodservice
facilities.
Foodborne viruses can be inactivated by heat. Thorough
cooking of food destroys viruses. The pasteurization of milk
[161°F (72C) for 15 seconds) is sufficient to destroy high
levels of viruses. Ultraviolet light and hypochlorite (bleach)
are effective against viruses on exposed surfaces, but do not
reach viruses below the surface.
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9
Viruses
General Characteristics
Viruses are much smaller than bacteria. They are too small to
be seen with a light microscope but can been seen with an
electron microscope. They vary in size from 0.01 to 0.45
micrometers. Virus particles contain a nucleic acid (either
DNA or RNA, which are genetic information), and a protein
coat. Viruses are not capable of multiplying outside a host
cell. If not present in a host cell, viruses will retain or lose
their infectious potential.
When a virus particle attaches to and invades a susceptible
host cell, the nucleic acid core and the protein coat separate.
The nucleic acid from the virus then directs the host cell's
"machinery" to make hundreds to thousands of virus particles.
In this way, viruses multiply and are able to destroy host cells.
If a significant number of cells stop or cease their special
functions for any length of time as a result of the virus
infection, illness may result. If enough cells in a vital organ
cease to function, as with hepatitis A virus and liver cells,
death results.
Immunity
Most viruses transmitted in foods seldom kill their hosts.
Instead, the host throws off the infection by means of
nonspecific immunity and antiviral antibodies. Antibodies are
slow to develop and often do not take effect until after the
viral infection has run its course. The biggest effect of the
antiviral antibody is to usually prevent recurrences of infection
by the same virus. This is called immunity.
Methods of Transfer
Viruses that cause foodborne illness can be transferred on
food, usually by fecal contamination caused by foodservice
workers who do not wash their hands properly after using the
toilet, and by water polluted with raw sewage. Rotavirus,
Norwalk agent, echo- and coxsackieviruses have all been
shown to cause gastroenteritis. As few as 1 to 5 virus
organisms can cause foodborne illness.
Methods of Isolation
It is much easier to isolate viruses from fecal and vomit
material than from foods. Hepatitis A virus and poliovirus
have been studied extensively. However, it has been difficult
to study the norovirus, snow mountain agent and other viruses
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4a-17
Seafood from contaminated waters often harbors fecal viruses.
Seafood should be cooked well or it should be obtained from
sources that certify safety of their seafood products. Any food
can contain viruses.
It is important to remember that viruses do not grow on or in
food, but can be transferred to another host (human or animal)
by food or water. Viruses can survive refrigeration and
freezing temperatures for months. They can be fairly resistant
to heat. Peterson et al., (1978) reported that hepatitis A virus
was not inactivated after thermal treatment of oysters at 140°F
(60°C) for 19 minutes.
Foodborne Viruses of Significance
Table 4-5 lists some of the enteric viruses of man that can be
transmitted by food and water.
Table 4-5
Enteric Viruses of Man*
Virus
Poliovirus
Hepatitis Type A
Norovirus
Snow mountain agent
Disease caused
Meningitis, paralysis, fever
Infectious hepatitis
Diarrhea, vomiting, fever
Gastroenteritis
* Adapted from Gerba, 1988.
Poliovirus has been transmitted in contaminated water and
milk that was inadequately pasteurized. This virus is easily
inactivated by heat. Poliovirus affects the central nervous
system and can cause paralysis. A vaccine has been
developed for this virus and the incidence of this disease has
declined since the 1950s. However, when people are not
immunized with the vaccine, the virus can cause a debilitating
illness (e.g., when unvaccinated people drink raw milk from
an infected cow).
Rotaviruses can cause life-threatening gastroenteritis in
humans and animals. They can cause severe diarrhea and
vomiting in children and adults. Rotaviruses are excreted in
large numbers in the feces from infected persons, and have
been isolated from water contaminated with sewage. Crops
that are irrigated with raw or treated wastewater can transmit
rotaviruses to humans, since rotaviruses can survive
conventional sewage treatment. When vegetables such as
radishes and lettuce are produced in this manner, they can
carry rotaviruses.
Noroviruses (Norwalk virus) (caliciviruses) are small, round
virus (.027 micrometers in diameter). Symptoms of the illness
are nausea, vomiting, diarrhea, and abdominal cramps, which
may last 2 to 3 days. Outbreaks of the illness have occurred in
recreational camps, on cruise ships, in schools, and in nursing
homes. Sources of these viruses have been attributed to
contaminated water, ingestion of raw shellfish and other
uncooked foods, and cake frosting handled in an unsanitary
manner. Noroviruses are transmitted by the fecal-oral route
and can be transferred by person to person contact. These
viruses are resistant to the amount of chlorine (3.75 ppm) used
in most water treatment facilities but can be inactivated by
sanitizing solutions containing an adequate amount of
chlorine.
Hepatitis A virus has been responsible for many documented
foodborne illness outbreaks. Illness occurs when people eat
contaminated food or drink contaminated water. The onset of
symptoms is 10 to 50 days. Symptoms include jaundice, loss
of appetite, and gastrointestinal disturbances. A lifetime
immunity is developed as a result. However, hepatitis A virus
affects the liver and serious long-term complications may
result in some people. The virus is transmitted by human
carriers, in contaminated food and water, and by shellfish
taken from contaminated waters.
Other viruses. Snow mountain agent, a small round virus
similar to norovirus, has been demonstrated to be the cause of
both food and waterborne disease outbreaks. Astroviruses,
calciviruses, and rotaviruses have been recognized as causing
human gastroenteristis, and are undergoing study at this time.
References:
Badawy, A.S., Gerba, C.P., and Kelley, L.M. 1985.
Development of a method for recovery of rotavirus from
the surface of vegetables. J. Food Prot. 48(3): 261-264.
Cliver, D.O. 1988. Virus transmission via Foods. Food
Technol. 42(4): 241-248.
Cliver, D.O. 1990. Foodborne Diseases. Academic Press,
Inc. San Diego, CA.
Frazier, W.C. and Westhoff, D.C. 1988. Food Microbiology.
Third edition. McGraw-Hill, New York, NY.
Gerba, C. P. 1988. Viral disease transmission by seafoods.
Food Technol. 42(4): 99-103.
Jay, J.M. 2000. Modern Food Microbiology. 6th edition.
Chapman & Hall Inc., New York, NY.
Mossel, D.A.A., Corry, J. E., Struijk, C. B., and Baird, R.
1995. Essentials of the Microbiology of Foods. John
Wiley and Sons, New York, NY.
Peterson, D.A., Wolfe, L.G., Larkin, E.P., and Deinhardt,
F.W. 1978. Thermal treatment and infectivity of hepatitis
A virus in human feces. J. Med. Virology 2:201.
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4a-18
Giardia are thermally resistant. Suspect food and water
should be heated thoroughly to boiling temperature [212°F
(100°)]. As long as people carry this organism in their
intestines, they can transmit this disease.
PARASITES
Protozoa (single-celled animals with a nucleus)
• Giardia lamblia
Control with filter or boiling
• Toxoplasma gondii
Control with hand washing, food contact
surface sanitizing, heat >145ºF, 15 seconds
• Entamoeba histolytica
Control with heat >122ºF
Toxoplasma gondii is a protozoan parasite that can be
transmitted by fecal-oral contamination. Cats are the original
hosts for these protozoa. The cats excrete oocysts
(microscopic inactive forms of this protozoa) in their feces.
Infectious sporozoites form within the oocysts 1 to 5 days
after excretion. The oocysts containing the sporozoites are
then transmitted to other animals in food (feeds) and water.
When these oocysts reach the intestine, they break open,
releasing 8 sporozoites. The sporozoites form active forms
(tachyzoites and trophozoites) which multiply rapidly and
spread to the rest of the body by way of blood and lymph.
Eventually, these forms encyst themselves in the brain, heart
muscle, other skeletal muscle, and liver. (These cysts are
microscopic and can survive as long as the host lives.)
Helminths
• Trichinella spiralis
• Taenia
• Anisakis spp.
• Control with:
Freezing according to government-specified
temperatures and times
Heat >145ºF, 15 seconds
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10
Parasites
Parasites in Foods
Humans may consume infective forms of foodborne parasites
when they eat raw or inadequately cooked food that contains
these parasites, or drink water from an unsafe source. In this
text, parasites of concern in food and water include protozoa
and helminths (worms).
Protozoa
Protozoa are single-celled animals that have a defined nucleus.
They are larger than bacteria and can be seen with a
microscope. Protozoa often feed on bacteria. Protozoa differ
in size, shape, and their mobility by means of flagella, cilia,
and pseudopodia.
There are many types of protozoa. They all have defined
needs for growth, which include temperature, nutrients,
atmosphere, and a supply of moisture. Some types of
protozoa are beneficial, some are of no harm, and some can
cause a wide variety of diseases. The protozoa that will be
discussed in this text are those that can cause foodborne
illnesses when these organisms are ingested in food and water.
Giardia lamblia is a flagellated protozoan. Giardia causes
giardiasis in humans when it is ingested as a cyst (i.e., resting
form of the living protozoa). Cysts form active forms of this
protozoa (trophozoites) in the upper small intestine, which
then attach to the intestinal lining. Here they consume mucous
secretions and replicate by binary fission.
After an incubation period of about 15 days, infected persons
experience a sudden onset of diarrhea, abdominal distension,
gas, nausea, and loss of appetite. The acute stage lasts 3 to 4
days. During this time, Giardia can be passed in the feces.
Recent outbreaks of this illness have occurred as a result of
drinking or using contaminated water. Foods can carry this
organism if they become contaminated by a food handler, if
they are irrigated with water that contains the organism, and if
they are contaminated with an unsafe water supply during
their preparation. Hikers in remote Rocky Mountain areas
may contract this disease by drinking water from streams that
have been contaminated with Giardia from wild animals such
as beavers. Domesticated animals such as dogs, cats, and
cattle may also be a source of this infection.
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4a-19
Farm animals (notably sheep, and pigs) can become infected
by consuming feed and water contaminated by barn cats.
When they are slaughtered to provide meat, the raw meat
contains the cysts, which can then infect humans if eaten raw
or not heated sufficiently to inactivate the various forms of
this parasite. Fresh pork is the main meat source of
Toxoplasma gondii in the United States. If cutting and
grinding equipment is not thoroughly washed and sanitized,
other raw meats such as ground beef can become
contaminated. Cysts of this protozoa are also found in wild
game meats such as elk, moose, and venison.
Clinical symptoms of the disease in humans are fever, muscle
aches, headaches, loss of appetite and sore throat. (Other
symptoms will appear depending upon the internal organ(s)
involved.)
In pregnant women, these parasites can be carried by way of
the placenta to fetal tissues. If fetuses are infected,
miscarriages may occur.
If a woman acquires Toxoplasma gondii during pregnancy,
there is a 20-to-50% probability that her fetus will be infected.
Most infected infants show no obvious symptoms at birth, but
will show signs of eye damage and mental retardation later in
life. It is estimated that there are over 3,300 cases of
congenital toxoplasmosis each year, resulting in 450 infant
deaths. Other surviving infected children are mentally
retarded as a result of this parasitic infection. Each year, it is
estimated that over 2,000,000 people (excluding infants) in the
U. S. are also affected by this parasite, resulting in 2 to 3
deaths.
This is a very serious infection. To prevent the spread of this
disease, food handlers must wash their hands thoroughly with
soap and water after handling meat. All cutting boards,
utensils, and knives must be washed and sanitized thoroughly
after coming in contact with raw meat, particularly raw pork.
To insure the destruction of this parasite, meat of any type
should be cooked until all parts of the meat reach a
temperature of 145°F (62.8°C) for 15 seconds before it is
consumed by humans or animals. Tasting raw meat should be
avoided. Pregnant women should avoid contact with cats,
soil, and raw meat. Vegetables should be washed thoroughly,
because they may be contaminated with fecal material from
cats.
and swelling of eyelids, face, and hands. Death can occur
with severe infections.
Entamoeba histolytica causes amebiasis or amebic dysentery.
Entamoeba histolytica is a large protozoan (50 micrometers).
It exists in both an active form (trophozoite) and in an inactive
form (cyst). Amebic dysentery occurs when food or water
containing cysts of this protozoa are ingested. The cysts are
not affected by the acidity and enzymes in the stomach and
pass through the stomach to the intestine. Once in the
intestine, the nuclei of cysts divide to form 8 new trophozoites
(active forms). These active forms of this protozoa produce
enzymes that enable it to invade the intestinal wall and
produce lesions (sores). Infected persons experience severe
abdominal pains and diarrhea, which may contain mucous and
blood. This disease is sometimes confused with cancer of the
colon and hemorrhagic colitis. These protozoa can penetrate
the blood vessels of the bowel and be transported to the liver
and lungs. Death may result due to the effect on these vital
organs. Individuals are carriers as long as they pass cysts.
People can be carriers for years.
To prevent this disease in humans, methods of preventing the
disease in hogs and using treatments that insure the destruction
of this parasite in meat must be used. Hogs must be raised
under the most sanitary conditions possible and should not be
fed raw garbage. In order to insure the destruction of
Trichinella spiralis, pork and game meat should be:
Entamoeba histolytica is often responsible for traveler's
diarrhea when visitors to tropical countries are exposed to
communities with poor sanitation, poor personal hygiene, and
a high incidence of carriers in the population. Amebiasis also
occurs in northern climates and is epidemic among some
native people living in the Arctic region.
To prevent the spread of this illness, there must be sanitary
disposal of fecal material. Safe water supplies should be used
to wash food during food preparation. Food should be grown
under adequate sanitary conditions and should not be fertilized
with animal or human fecal material. Food handlers must be
taught to use proper hand washing procedures. This protozoa
and its cysts are destroyed when food and water are heated
above 122°F (50°C). Health organizations recommend boiling
temperatures for suspect foods and water.
Helminths
Helminths are parasitic worms that live at the expense of their
hosts (humans, animals, fish, and birds). These worms are
large enough to be seen without the aid of a microscope.
However, a microscope is needed to detect their eggs or cysts.
The parasitic worms of most concern in food include
Trichinella spiralis, Taenia (tapeworms), and Anisakis spp.
Trichinella spiralis is a nematode (worm) that causes the
illness or disease Trichinosis. Trichinosis develops when
people consume raw or insufficiently cooked pork or other
meat containing encysted larvae. The larvae are released into
the intestinal tract during digestion and invade the mucous
membranes of the intestine, where they develop into adults.
Fertilized females produce numerous larvae, which travel
through the circulatory system (blood and lymph) to skeletal
muscle tissue where they again form cysts.
The incubation period for the first symptoms to develop varies
from a day or two to as long as several weeks. Symptoms
include nausea, vomiting, diarrhea, sweating, abdominal
cramps, and loss of appetite. These symptoms may continue
for days and are often confused with other foodborne illnesses.
Later symptoms, which result from encystment of larvae in
muscle include muscle soreness, spastic paralysis of muscles,
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4a-20


Cooked until every part of the meat reaches a temperature
of 155°F (68°C) for 15 seconds; or 150°F (66°C) for 1
minute; or 145°F (63°C) for 3 minutes
Quick frozen or stored at government-specified
temperatures and times [e.g., -20°F (-28.9°C) for 6 to 12
days].
People should not consume raw or insufficiently heated game
meats or pork, unless there is certification by the supplier that
it is trichinella free.
Taenia are tapeworms and can cause disease in humans when
larvae infested meat is eaten. People can be a host for both
beef and hog tapeworms. The adult worm is a parasite in
humans, while the larvae infest animal tissues. A cycle occurs
when humans pass eggs or proglottids (segments of the
tapeworm) in their feces. When people defecate or spread raw
sewage in a crop area used to raise feed, the eggs and
proglottids are passed on to the livestock. The eggs hatch
within the animal host and develop larvae, which settle in the
muscle. This encystment stage in livestock is called
cysticercosis. When people consume raw or undercooked
larva-infested meat, the larvae develop in the human intestinal
tract into adulthood. Infestation of the human intestine with
tapeworms is called taeniasis. The tapeworms produce eggs
that are then passed in the feces, enabling the cycle to begin
again, unless there is proper disposal of human fecal material.
Symptoms of the illness include: abdominal pain, nausea,
weakness, weight loss, increased or decreased appetite, hunger
pain, change in bowel habits, and nervousness. Humans are
often unaware they carry this parasite until it is passed in fecal
material. If these parasites become encysted in vital organs
such as the liver, heart, lungs, eyes, and brain, their presence
becomes life threatening.
The incidence of taeniasis has declined since the 1930s.
However, there is still an estimated incidence of 1,000 cases in
the U. S. each year, resulting in 10 deaths.
The USDA inspects carcasses for signs of cycticercosis and
condemns carcasses that have extensive signs of tapeworm
cysts. Carcasses with a very few number of lesions or cysts
can be marketed, if the cysts are removed and the carcasses
are exposed to freezing temperatures of 15°F (-9.4°C) or lower
for 10 to 20 days. Carcasses with high infestations are
condemned. Heating every part of the muscle to an end
temperature of 140°F (60°C) is sufficient to destroy the larvae
in meat.
Anisakis spp. are nematodes (worms) in fish. Consumption of
raw or insufficiently processed fish may cause anisakiasis in
humans. Natural hosts for adult worms are marine mammals
such as dolphins, whales, and seals. Eggs excreted by these
marine mammals are eaten by crustaceans. The crustaceans
are eaten by fish or squid and the life cycle is completed when
these are in turn eaten by sea mammals. People become
infected by eating raw or undercooked seafood such as sushi.
Anisakiasis is common in countries like Japan, the
Netherlands and Scandinavia where people eat raw and
underprocessed fish.
Signs and symptoms of the illness include irritation of the
digestive tract and throat. Anisakine larvae can either remain
free or become attached to the human digestive tract to cause
irritation, inflammation, or ulceration. The larvae do not
mature in people. They can be expelled by coughing or
vomiting. Often, they must be removed surgically.
The larvae are destroyed if fish are heated to 140°F (60°C) or
are frozen and stored at government-specified freezing
temperatures and times. Cleaning (evisceration) of fish soon
after catching them prevents the larvae from migrating from
the intestinal tract to the muscle of the fish.
References:
American Veterinary Medical Assoc. 1995. Zoonosis
Updates. 2nd edition. Am. Vet. Med. Assoc.,
Schaumberg, IL.
Anon. 1989. A case of Anisakiasis - Alberta. Canadian
Weekly Report. Vol. 15(44): 221-224.
Chin, J., 2000. Control of Communicable Diseases in Man.
17th edition. The American Public Health Assoc.,
Washington, D.C.
Dubey, J.P. 1986. Toxoplasmosis. J. Am. Vet. Med. Assoc.
189 (2): 166-170.
Jay, J.M. 2000. Modern Food Microbiology. 6th edition.
Chapman & Hall Inc., New York, NY.
Mossel, D.A.A., Corry, J. E., Struijk, C. B., and Baird, R.
1995. Essentials of the Microbiology of Foods. John
Wiley and Sons, New York, NY.
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4a-21
evisceration for off-odors and other evidence of mishandling
that could result in histamine formation. Routine examination
for histamine is common even though decomposition is not
evident.
FISH AND SHELLFISH TOXINS AND POISONS
Histamine poisoning
• Scombroid fish (tuna, snapper, grouper, amberjack,
mahi mahi)
• Spoilage bacteria change histidine to histamine
• Not heat denatured
Paralytic shellfish poisoning
• Shellfish ingest small dinoflagellates that provide toxins
• Toxins are not inactivated by heat
Ciguatera poisoning
• Dinoflagellates provide toxin that accumulates in fish
tissue
• Toxin is not inactivated by heat
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Fish and Shellfish Toxins
Types of Poisoning
Marine fishery products may contain some of the most potent
toxins known. These toxins are unaffected by cooking, and no
antidotes or antitoxins exist to reduce their toxicity of some of
these toxins. Poisonings through eating toxic fish and
shellfish are significant causes of human illness. Outbreaks
are usually due to three types of poisoning: histamine
poisoning, paralytic shellfish poisoning, and ciguatera
poisoning.
Histamine Poisoning
Histamine poisoning is the second most frequently reported
fishborne illness in the United States. Illness results from
eating fish that have become toxic after undergoing some
microbial decomposition, although signs of spoilage may not
be evident. The fish belong to the Scombridae family and
include tuna, snapper, grouper, amberjack, and mahi mahi.
Scombroid fish have high concentrations of the amino acid
histidine in their tissues. When histidine is decarboxylated,
the COO- group is removed from the molecule and histamine,
the toxic agent, is formed. Fresh tuna has a histamine level of
less than 20 mg per 100 grams. An excess of 100 milligrams
per 100 grams histamine is reported in tuna that has undergone
microbial decomposition. Morganella morganii and
Klebsiella pneumoniae are the two types of bacteria most
often associated with histamine formation in various
scombroid fish.
The onset of symptoms is short, ranging from a few minutes to
a few hours. Symptoms of scombroid (histamine) poisoning
include: tingling and burning sensations around the mouth,
flushing, a rash with itching, hypertension, rapid pulse,
headache, dizziness, nausea, and diarrhea. If the condition is
recognized quickly, the use of antihistamine therapy can be
useful. With the exception of cheese, foods other than fish are
rarely involved.
There is no immunity. The poisoning occurs throughout the
world and is thought to be vastly under-reported.
An assay method for histamine is available and is applicable
for routine use in a well-equipped laboratory. It is common
commercial practice within the fisheries industry to inspect
scombroid-type fish at point of receipt and in-plant at time of
1901-04: ch4a rev 6/16/05 print 3/7/16
4a-22
After canning, the muscle tissue of some affected fish have a
honeycombed decomposition pattern even when no visible
changes are present in raw fish. Imported scombroid fish,
usually tuna, are frequently inspected for evidence of
deterioration and are analyzed for histamine content by the
FDA. Canned albacore, skipjack, and yellow fin tuna with
histamine levels of 20 mg or more per 100 grams are subject
to regulatory action by FDA as being suspect of deterioration.
The agency will consider regulatory action against any tuna
found to contain between 10 and 20 mg of histamine per 100
grams when a second indication of decomposition is present.
The FDA has established, on an interim basis, a level of 50 mg
of histamine per 100 grams of tuna as the level of histamine in
tuna that it considers a health hazard. Accordingly, this
microbiological criteria with histamine as the designated
contaminant is useful when applied, as indicated above, to
prevent deteriorated fish as well as toxic fish from reaching
the processor or consumer.
Paralytic Shellfish Poisoning
Paralytic shellfish poisoning (PSP) is one of the most toxic
forms of food poisoning. Certain species of dinoflagellates
(flagellated protozoa), most notably Gonyaulax catenella and
Gonyaulax tamarensis, produce saxitoxin, which is known to
cause PSP. Ingestion of toxic shellfish causes acute toxicity in
humans. Shellfish involved most frequently include mussels,
clams, soft-shelled clams, butter clams, and occasionally,
scallops.
Toxic shellfish may contain multiple toxins. Saxitoxin may
represent only a part of the total toxicity. These newly
discovered toxins are related to saxitoxin and their
pharmacological action seems to be similar to that of
saxitoxin.
In addition to gastrointestinal symptoms, PSP produces
neurological symptoms including tingling lips within 15
minutes, profuse paralysis, and death in 2 to 24 hours. There
is no antidote. Respiratory arrest causes death if the patient is
not put on a respirator immediately. Major cardiac damage
usually occurs if there is a heavy dose of toxin, even if the
patient is given appropriate treatment. A field test for PSP is
desperately needed.
There are medical records of over 1,650 cases of PSP
(worldwide) that have resulted in at least 300 fatalities.
Outbreaks, although infrequent, occur sporadically along the
Atlantic and Pacific coasts of the United States.
Routine sampling and testing for toxins in shellfish obtained
from wholesale or retail markets is not practiced, nor is it
necessary. A microbiological criterion for PSP is applied
when state authorities regularly assay representative samples
of shellfish from growing areas. If toxin content reaches 80
micrograms per 100 grams of edible portion of raw shellfish
meat, the area is closed to harvesting of the species involved.
These actions and other preventive measures are undertaken in
accordance with the National Shellfish Sanitation Program
(NSSP), a federal-state-industry cooperative program. Cases
of PSP have resulted from shellfish taken from closed fishing
areas where fishing was prohibited.
Note, The NSSP is not funded by the national government, but
by state governments. Sometimes state governments do not
fund these control programs in their states. Therefore, a
seafood buyer must get the supplier to certify PSP safety.
Ciguatera Poisoning
Ciguatera poisoning is one of the largest public health
problems related to poisoning from ingestion of fish.
Ciguatoxin has been known since the time of the
Conquistadors in the 1600s when affected sailors continued to
have asthenia (loss of body strength) and arthralgia (pain in
the joints along the nerves) for years after consumption.
Ciguatoxin poisoning occurs throughout the Caribbean and
tropical Pacific regions, where outbreaks have been reported
by both residents and tourists. From 1983 to 1992 in the
United States, 129 outbreaks of ciguatera poisoning involving
508 persons were reported to the CDC. No ciguatera-related
deaths were reported. Most outbreaks were reported from
Hawaii and Florida, although outbreaks and sporadic cases
occurred in California, New York, and Illinois. (The case in
Illinois was due to imported fish.)
The toxin is synthesized by the dinoflagellate Gambierdiscus
toxicus, and possibly by certain other dinoflagellate species.
Fish may feed on these organisms and accumulate the toxin in
their tissues. As the toxin passes through the fish food chain,
it increases (i.e., large carnivores tend to be more toxic than
herbivores and small carnivores). The fish are seemingly
unaffected toxin accumulation. Large, old barracuda carry
great quantities of toxin in their flesh. Fish found in the
Pacific Ocean and throughout the Caribbean are often sources
of ciguatoxin.
Four to eight hours may elapse between ingestion of the
poison and the onset of symptoms, which include weakness
and abnormal sensory phenomena. Beyond the
gastrointestinal upset, the involvement of the cardiovascular
and neurological systems is even more serious. Blood
pressure drops and tachycardia (rapid heartbeat) develops;
numbness and the reversal of hot and cold sensations occur.
The infective dose is less than l mg of toxin. More than
10,000 cases occur annually, worldwide.
The factors that trigger the buildup of toxic concentrations of
the toxin of G. toxicus and possibly those of other
dinoflagellate species are not clear. Fish toxins, other than
ciguatoxin, are not well defined and assay methods for them
are neither precise nor specific. Because of the lack of
sufficient knowledge in these areas, there are no federal or
state surveillance programs for preventing the occurrence of
ciguatoxin poisoning. Supplier certification is the only safety
control available. The toxin is heat stable and remains in fish
after it is cooked.
As the domestic and imported fish industry expands its
market, the diagnosis of this "tropical" disease must be
considered even in areas to which coral-reef fish are not
native. Ciguatera fish poisoning can be diagnosed by the
characteristic combination of gastrointestinal and neurologic
symptoms in a person who ate a suspect fish. The diagnosis
can be supported by detection of ciguatoxin in the implicated
fish.
Hawaii now uses a "stick test" immunoassay to detect
ciguatoxin in fish. The test is sensitive, specific, inexpensive,
and easy to use in the field. In Hawaii, if an outbreak-related
fish tests positive for ciguatoxin, the reef area of catch is
closed to discourage further fishing in that area. In Miami,
Florida, because barracuda have been frequently associated
with ciguatera poisoning, a city ordinance bans the sale of
barracuda.
OUTBREAK EXAMPLE. The following outbreak example
appeared in MMWR 47(33) 692, 1998.
Ciguatera Fish Poisoning – Texas. On October 21, 1997, the
Southeast Texas Poison Center was contacted by a local
physician requesting information about treatment for crew
members of a Norwegian cargo ship docked in Freeport,
Texas, who were ill with nausea, vomiting, diarrhea, and
muscle weakness.
Gastrointestinal illness developed after the crew members ate
fish on October 12. Of 23 crew members interviewed, 17
(74%) reported the following symptoms: diarrhea (17
[100%]), abdominal cramps (14 [82%]), nausea (13 [76%]),
and vomiting (13 [76%]). Symptoms occurred within 2 to 16
hours after eating fish. All ill crew members also experienced
neurologic symptoms characteristic of ciguatera poisoning.
These symptoms included: muscle weakness and pain,
numbness or itching of the mouth, itching of the hands and
feet, temperature sensation reversal, dizziness, and aching or
loose feeling teeth. Seventeen crew members ate the
barrocuda and all became ill. Although crew members also
ate red snapper and grouper at the same meal, neither of these
fish were linked epidemiologically with illness.
Investigators found samples of the leftover barracuda that was
eaten, in cold storage on the ship. These samples tested
positive for ciguatoxin.
Human ciguatera poisoning can occur after consumption of a
wide variety of coral reef fish, such as barracuda, grouper, red
snapper, amberjack, surgeonfish, and sea bass. Ciguatoxin
and related toxins are derived from dinoflagellates, which
herbivorous fish consume while foraging through the macroalgae. Humans ingest the toxin by consuming either
herbivorous fish or carnivorous fish that have eaten the
1901-04: ch4a rev 6/16/05 print 3/7/16
contaminated herbivores. Larger, more predacious reef fish
are more likely to be toxic. Since the toxin is heat-stable,
cooking does not make the fish safe to eat.
4a-23
References:
Ahmed, F. 1991. Seafood Safety. National Academy Press.
Washington, D.C.
CDC 1998. Ciguatera fish poisoning - Texas 1997. MMWR
47 (23) 692-694.
Jay, J.M. 2000. Modern Food Microbiology. 6th edition.
Chapman & Hall Inc., New York, NY.
Mossel, D.A.A., Corry, J. E., Struijk, C. B., and Baird, R.
1995. Essentials of the Microbiology of Foods. John
Wiley and Sons, New York, NY.
Taylor, S.L. 1988. Marine toxins of microbial origin. Food
Technol. 42(3):94-98.
reach a population of 105 to 106 microorganisms per gram of
food. A 10-generation multiplication is probably safe.
GROWTH OF BACTERIA IN FOOD
BASED ON FDA FOOD CODE HOLDING / STORAGE RECOMMENDATIONS
The population of pathogens in food should be low enough to
allow time for refrigerated storage before the number of
pathogenic bacteria in the product becomes hazardous.
Refrigerator storage does not inhibit the multiplication of all
pathogenic bacteria. Some pathogenic bacteria are capable of
multiplying at refrigeration temperatures between 30 to 40°F
(-1.1 to 4.4°C) (Hauschild, 1989; Hudson et al., 1994; van
Netten et al., 1990).
Eventually, when a bacterial population is around 10,000,000
to 50,000,000 / gram or slightly higher, waste concentration
becomes high and the growth nutrients are so scarce that the
microorganisms stop multiplying and enter the stationary
phase. A critical question is: "What type of pathogen
multiplied?" If it is a pathogen whose waste products are
toxic, then further processing such as reheating to 165°F
(73.9°C) will not make the food safe. Staphylococcus aureus,
C. botulinum, and B. cereus can all produce this type of toxin.
Therefore, pathogenic growth must be limited to levels that
are not harmful (less than 10 multiplications). The stationary
phase is followed by the death phase when vegetative cells
decrease in numbers and internal bacterial enzymes dissolve
the non-multiplying cells. However, if toxins have been
produced, they will remain in the surrounding media or food.
1382
4/12/2005
1901(4a&b)
12
The Multiplication of Pathogenic Bacteria
and Factors Controlling Multiplication
Bacterial Multiplication Controls
If favorable environmental conditions exist, bacterial
multiplication occurs. When dormant bacteria are transferred
to a nutritious medium such as warm turkey broth, there is a
short period of adjustment known as the "lag phase," before
they begin to multiply. The lower the temperature, the more
unfavorable the chemistry of the food, the longer the lag
period. At optimum temperatures [e.g., 95°F (35°C) the lag
phase is quite short, 2 hours. During the lag phase, the
dormant cells warm up and soak up nutrients. The metabolic
cycle inside the cells begins to function at an optimum rate.
For multiplication, bacteria need the proper amount of oxygen
or lack of oxygen depending on whether they are aerobic
(require oxygen) or anaerobic (do not require oxygen). They
also require proper temperature, adequate nutrients, free water,
time, and a favorable acid or base pH. Any imbalance of these
factors can reduce or stop bacterial multiplication.
After some hours or days, depending on temperature,
atmosphere, water, and pH, the vegetative cells begin to
multiply logarithmically: 2 become 4, then 8, then 16, etc.
Table 4-6 shows that 5 generations of bacteria only permit a
multiplication of 1 to 32.
Bacteria reproduce by cell division. That is, they multiply by
increasing in number, not by growing in size. They can
double in approximately 8 to 30 minutes at optimum
temperatures of 95 to 115°F (35.0 to 46.1°C). This
multiplication occurs during inadequate hot holding, or slow
cooling in a refrigerator. To be safe, food must be held at
temperatures greater than 130°F (54.4°C) or less than 30°F
(-1.1°C).
Table 4-6
Logarithmic Bacterial Population Multiplication
Generation
1
2
3
4
5
6
7
8
9
10
Number of
Bacteria
2
4
8
16
32
64
128
256
512
1,024
Allowing the first 5 generations of microorganisms to be
produced usually does not create a hazard in the food or food
product. Allowing most of the vegetative infective pathogens
to reach a population of greater than 1,000 must always be
considered hazardous. Note that this is not true for
Staphylococcus aureus, Bacillus cereus, Clostridium
perfringens and Clostridium botulinum type E, which must
1901-04: ch4a rev 6/16/05 print 3/7/16
4a-24
Snyder (1997) has compiled a recommended set of times and
temperatures for holding food. The recommended times for
holding food are shown in Table 4-7. The numbers are based
on the FDA Food Code, which allows 7 days at 41°F (5°C), 4
days at 45°F (7.2°C), and 4 hours if food is held between 46 to
139°F (7.8 to 59.4°C). The temperature for most rapid growth
during the 4 hours is about 112°F (44.4°C). Ratkowsky et al.
(1983), have developed an equation that can be used to predict
growth at temperatures in between given anchor points. By
using the FDA Food Code values and anchoring the ends of
the growth line at about 30°F (-1.1°C) and 126°F (52.2°C)
values for Table 4-7 can be predicted. These data can then be
used to calculate the time for 1 generation to multiply to 10
generations over the entire growth range.
How can this be used? The Microbiological Multiplication
Calculator, on the following page, is a work sheet that allows
one to analyze a process with fluctuating temperatures and to
use this information to judge if the process reached the 10generation safety limit derived from FDA-recommended
holding times of 7 days at 41°F (5°C), 4 days at 45°F (7.2°C),
or 4 hours at 112°F (44.4°C). The Quality Assurance person
simply logs the food handling times and temperatures. Once
the process data is logged, the equivalent growth can be
calculated for each process step by multiplying the time at
each temperature by the multiplication rate and entering it on
the column titled, Accumulated Multiplication. The food
should be cooked or eaten before there have been 10
multiplications.
The values of 41°F (5°C), 4 days at 45°F (7.2°C), and 4 hours
at 112°F (44.4°C) derived from FDA Food Code
recommendations are all very conservative. At temperatures
below about 70°F (21.1°C), spoilage microorganisms multiply
more rapidly than pathogens.
Cooling
The lag is also important during cooling. Spores of B. cereus,
C. botulinum, and C. perfringens are activated above 140°F
(60°C). (Normal activation is 180°F (82.2°C) for 15 minutes.)
When food cools to below 127.5°F (53°C), the spores begin to
germinate and grow out as vegetative cells that begin to
metabolize and multiply. The FDA Food Code recommends
cooling potentially hazardous food to 41°F (5°C) within 6
hours [§3-501.14: from 135 to 70°F (57.2 to 21°C) within 2
hours followed by cooling to 41°F (5°C) or below within a
total time of 6 hours]. To accomplish this a $20,000 blast chill
refrigerator must be used for cooling food. USDA Guidelines
recommend cooling food, within 90 minutes after cooking,
from 120 to 55°F (48.9 to 12.8ºC) within 6 hours, followed by
further cooling to 40°F (4.4ºC) (no time limit) before boxing.
References:
Hauschild, A.H.W. 1989. Clostridium botulinum. In
Foodborne Bacterial Pathogens. Doyle, M.P., ed., Marcel
Dekker, Inc., New York, NY.
Jay, J. M. 2000. Modern Food Microbiology. 6th ed.
Chapman & Hall. New York, N.Y.
Hudson, J. A., S. J. Mott , and N. Penney. 1994. Growth of
Listeria monocytogenes, Aeromonas hydrophila,
Yersinia enterocolitica on vacuum and saturated carbon
dioxide controlled atmosphere-packaged sliced roast
beef. J. Food Prot. 57 (3) 204-208.
Ratkowsky, D. A., R. K. Lowry, T. A. McMeekin, A. N.
Stokes, and R. E. Chandler. 1983. Model for bacterial
culture growth rate throughout the entire biokinetic
temperature range. J. Bacteriol. 154(3):1222-1226.
Snyder, O. P. 1997. Updated Guidelines for Use of Time and
Temperature Specifications for Holding and Storing
Food in Retail Food Operations. Dairy Food Environ.
Sanitation. 18: 574-579.
van Netten, P., van de Moosdijk, A., van Hoensel, P., Mossel,
D.A.A., and Perales, I. 1990. Psychrotrophic strains of
Bacillus cereus producing enterotoxin. J. Appl.
Microbiol. 69: 73-79.
1901-04: ch4a rev 6/16/05 print 3/7/16
4a-25
Table 4-7
Maximum Holding Times at Specified Temperatures
°F
°C
<30
30
35
40
41
45
50
55
60
65
70
75
80
85
90
95
100
105
110
115
120
125
<-1.1
-1.1
1.7
4.4
5.0
7.2
10.0
12.8
15.6
18.3
21.1
23.9
26.7
29.4
32.2
35.0
37.8
40.6
43.3
46.1
48.9
51.7
1
Multiplication
of Pathogens
Safe
297.14 hours
46.34 hours
17.99 hours
15.55 hours
9.49 hours
5.85 hours
3.96 hours
2.86 hours
2.16 hours
1.69 hours
1.36 hours
1.12 hours
0.93 hours
0.79 hours
0.68 hours
0.59 hours
0.52 hours
0.47 hours
0.46 hours
0.56 hours
3.10 hours
SAFETY
LIMIT*
10
Multiplications
of Pathogens
Safe
123.8 days
19.3 days
7.5 days
6.5 days
4.0 days
2.4 days
1.7 days
1.2 days
21.6 hours
16.9 hours
13.6 hours
11.2 hours
9.3 hours
7.9 hours
6.8 hours
5.9 hours
5.2 hours
4.7 hours
4.6 hours
5.6 hours
31.0 hours
* Food should be cooked, eaten or discarded before there
have been 10 multiplications.
MICROBIOLOGICAL MULTIPLICATION CALCULATOR
By_________________________________________________________________ Date _________________
Process ______________________________________________ Task _______________________________
Description
Temp. Time
(oF) (hr.)
Multiplication
rate / hr.
Accumulated
Multiplimultiplication
cation
Table of Calculated Rates
at Specified Temperatures
Temp.
(oF)
<30
30
35
40
41
42
43
44
45
46
47
48
49
50
51
52
53
54
55
56
57
58
59
60
61
62
63
64
65
66
67
68
69
70
71
72
73
74
75
76
77
78
79
80
81
1901-04: ch4a rev 6/16/05 print 3/7/16
4a-26
Multiplic.
rate / hr.
Temp.
(oF)
Safe
0.003
0.022
0.056
0.064
0.074
0.084
0.094
0.105
0.117
0.130
0.143
0.157
0.171
0.186
0.202
0.218
0.235
0.252
0.271
0.289
0.309
0.329
0.350
0.371
0.393
0.416
0.439
0.463
0.487
0.512
0.538
0.565
0.592
0.619
0.648
0.676
0.706
0.736
0.767
0.798
0.831
0.863
0.897
0.931
82
83
84
85
86
87
88
89
90
91
92
93
94
95
96
97
98
99
100
101
102
103
104
105
105
107
108
109
110
111
112
113
114
115
116
117
118
119
120
121
122
123
124
125
126
>127.5
Multiplic.
rate / hr.
0.965
1.000
1.036
1.073
1.110
1.148
1.186
1.225
1.265
1.305
1.346
1.387
1.429
1.472
1.515
1.558
1.602
1.647
1.692
1.737
1.782
1.827
1.872
1.917
1.961
2.004
2.045
2.083
2.119
2.149
2.174
2.190
2.196
2.188
2.163
2.115
2.038
1.927
1.775
1.573
1.319
1.013
0.668
0.323
0.058
Safe
center temperature. The food temperature will tend to coast
up, so it will be more than 1 minute to 150ºF before the grilled
item starts to cool, and a 5D (100,000-to-1) kill will have been
achieved. If the hamburger is ground from fresh product, not
aged beef, and if there are no additives such as soy, the color
will be a pleasing, medium pink at 150ºF center temperature.
When meat is heated to 160ºF center temperature, there will
be little red color left in fresh beef, pork, lamb, chicken, etc.,
and these items, which are medium well, are overly safe.
Cooks have been taught to cook meat until the red color is
gone, or above 160ºF, not because of safety, but rather, it was
assumed that no one had a proper thermometer to measure
temperature, and color was an adequate control. The USDA
now says that one will never cook by color, because color
cannot be trusted to indicate food temperature. One must cook
with a tip-sensitive, electronic thermometer.
DESTRUCTION OF SALMONELLA IN FOOD
DEATH CONTROLS
Time and temperature
Nutrients and acids
Water activity
DESTRUCTION OF
SALMONELLA SPP. IN FOOD
Temp.
ºF (ºC)
5D
Hamburger
(100,000:1)
6.5D
Roast beef
(3,160,000:1)
130 (54.4)
86 min.
112 min.
135 (57.2)
27 min.
35 min.
140 (60.0)
8.7 min.
11.2 min.
145 (62.8)
2.7 min.
3.5 min.
150 (65.6)
52 sec.
67.sec.
155 (68.3)
16 sec.
21 sec.
160 (71.1)
5.2 sec.
6.7 sec.
1326
4/12/2005
1901(4a&b)
13
Destruction of Foodborne Disease Bacteria
Destruction of Bacteria
Favorable environmental conditions of temperature, nutrient,
pH, aw and oxidation-reduction conditions over a period of
time promote the multiplication of microorganisms. By
altering these conditions, the multiplication of microorganisms
can be controlled and/or their destruction can be achieved.
Time and Temperature
Time and temperature can be manipulated in order to destroy
bacteria. Just as growth is logarithmic, destruction is also
logarithmic. The higher the temperature, the shorter the time
required to accomplish destruction of bacterial cells and
spores. The figure shows data that are typical of Salmonella
spp. Salmonella spp. is a common foodborne illnessproducing organism and hence, is suitable to use to develop
safety standards. One thousand Salmonella spp. per gram can
be reduced to 1 per 100 grams of food (a 5D or 5 log
reduction) in 8.7 minutes at 140°F. (A 1D reduction is 1 log
reduction.) At a temperature of 150°F, the process would take
52 seconds. Only 5.2 seconds would be needed to accomplish
the same reduction at 160°F. Note that for each 10°F increase
in temperature, the salmonellae die 10 times faster. Time and
temperature control is far more important in pasteurization of
food than in cold holding and refrigeration; 3ºF error in
measuring the coldest spot in a food item can mean the
survival of twice as many organisms. Precise cooking is
essential if there is to be safety without overcooking. A tipsensitive, electronic thermometer must be used. Note that the
food code calls for a 6.5D reduction of Salmonella for roast
beef. Of course, hamburger is more contaminated than roast
beef, but the roast beef requirement, which was established in
1978, simply has not been changed by the government.
At 140ºF food center temperature, which is a rare hamburger,
it is virtually impossible to hold food for 8.7 minutes to get a
5D pasteurization on a fast-cooking device such as a grill,
broiler, or griddle without the temperature increasing. Note,
the FDA code allows pasteurization at 145ºF, 3 minutes;
150ºF, 1 minute; and 155ºF, 15 seconds. The conclusion is
that rare meat, unless the supplier certifies it as vegetativepathogen free, cannot be made safe except in slow cooking,
such as oven roasting of beef, pork, lamb, etc. In ordinary
grill / griddle cooking, the outside of the food is well above
150ºF, by the time the food is taken off the grill at 150ºF
1901-04: ch4a rev 6/16/05 print 3/7/16
The addition of acids such as lemon juice, vinegar, and wine
to food products not only adds flavor to the product but also
lowers the pH of the food, which slows down or inhibit
bacterial growth and aid in destruction of bacteria when
combined with heat. It will also turn meat brown at lower
cooking temperature. If it is aged and acidic, meat is brown at
150ºF. Meat with 15% textured vegetable protein is brown at
140ºF. On the other hand, if meat is cooked with onions and
celery, high in nitrate, the color of meat becomes the color of
cured meat (e.g., ham) and does not turn completely brown,
even when a temperature of 180ºF is reached.
Nutrients and Acids (pH)
When the supply of nutrients is low or not optimum, the
multiplication of microorganisms is slow and decline in
numbers occurs.
The incorporation of food components that lower the pH of
food products contributes to the destruction of
microorganisms. The pH of some foods (e.g., lemon juice,
wine, vinegar) is quite acid. The presence of organic acids
and alcohol in these foods make heat destruction more
effective. When the pH of food is low (quite acid), bacterial
destruction at a specific temperature is much faster.
Water Activity
Microorganisms require moisture to multiply. Multiplication
is restricted in an environment where water is not available or
bound by other food components such as salt, sugar, and
glycerol. Foods high in moisture, such as fresh fruits and
vegetables, meat, fish, poultry, etc., permit rapid
multiplication of microorganisms. The water in the structural
system of these foods is available for the metabolic functions
of microorganisms. When water is removed to a sufficiently
low level (e.g., cereals, dried fruits and vegetables), the
multiplication of microorganisms is suppressed. Hence, these
foods are shelf stable at room temperature until they absorb
sufficient amounts of water from the atmosphere, at which
time the multiplication of microorganisms will begin.
Although the multiplication of microorganisms is suppressed
as the aw of a food system is lowered, some microorganisms
survive. It is much harder to inactivate these surviving
microorganisms in low water activity foods. Higher
temperatures for longer periods of time are required to ensure
destruction. A practical application of this knowledge is to
add sugar or salt, which lowers water activity to a food
4a-27
product such as egg custard only after it has reached the
pasteurization temperature of 165°F (73.9°C), and the milk,
eggs, meat, etc. are pasteurized.
Survival: Vegetative Cells vs. Spores
Vegetative cells are quite susceptible to thermal destruction
and are reduced to a safe level at the times and temperatures
shown in the slide at the beginning of this section (#1326).
Spores, which are inactive forms of some microorganisms,
require much higher temperatures for inactivation. For
example, a temperature of 250°F (121°C) for 15 seconds in
the middle of the product is required to produce a 1 log
population reduction of Clostridium botulinum type A spores.
The minimum sterilization standard for canned food is to
reduce C. botulinum spores by 12D, or 1,000,000,000,000 to
1. Spores of some spoilage microorganisms are even more
heat resistant, so, canned food is often processed at 250ºF
(121.1ºC) for 9 to 12 minutes.
Spores are present in food, and they can survive most cooking
processes. An exception is the spores of C. botulinum Type E,
commonly found in fish. At 180°F (82.2°C), 0.8 minutes was
required for a 1 log cycle reduction of C. botulinum Type E
spores in evaporated milk, while 6.6 minutes was required to
reduce the number of spores in tuna packed in oil (Simunovic
et. al., 1985). The longer time required for the destruction of
spores in oil is an illustration of the protective effect of fat in
food products.
Freezing
While freezing is not a reliable method for destroying bacteria,
viruses, yeasts, and molds, it is reliable for the inactivation of
parasites. The FDA and USDA have specified temperatures at
specific times, depending on the type of parasite and the size
of the product. The colder the temperature, the more rapid the
destruction.
References:
Frazier, W.C., and Westhoff, D.C. 1988. Food Microbiology,
4th ed. McGraw-Hill, New York, NY.
International Commission of Microbiological Specifications
for Foods. 1996. Microbial Ecology of Foods. V ol.5.
Microorganisms in Food. Microbiological Specifications
of Food Pathogens. Blackie Academic & Professional,
New York, NY.
Jay, J. M. 2000. Modern Food Microbiology. 6th ed.
Chapman & Hall. New York, N.Y.
Mossel, D.A.A., Corry, J. E. L., Struijk, C. B., and Baird, R.
M. 1995. Essentials of the Microbiology of Foods.
John Wiley & Sons. New York, NY.
Simunovic, J., Oblinger, J.L. and Adams, J.P. 1985. Potential
for growth of nonproteolytic types of Clostridium
botulinum in pasteurized restructured meat products: A
review. J. Food Prot. 48 (3): 265-276.
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4a-28
either precedes or follows clinical signs or symptoms, as well
as during the clinical stages of the illness. Both hepatitis A
virus and Salmonella spp. can be transmitted by carriers.
TYPES OF ILLNESS
Food Infection: Illness occurs as a result of consuming food
containing living pathogenic microorganisms that then
multiply in the body [e.g., Salmonella spp., hepatitis A virus,
trichinae].
Control of Infective Microorganisms
Those pathogens that cause infection are inactivated by heat
and are normally destroyed, if food is properly cooked.
However, they are dangerous when levels causing illness in
unheated food or recontaminated cooked food are consumed.
Adequate heating of foods, cleanliness and sanitation of
facilities, appropriate personal hygiene by all foodservice
workers, and progressive batch cooking of food are methods
of controlling multiplication of these pathogens in food.
Careful hand washing is extremely important. Human feces
can contain 108 pathogens per gram. If they are not reduced to
a very low number (1 to 10 per gram), through sufficient hand
washing, they can introduce enough infective microorganisms
into a bowl of food, punch, or salad to cause illness in
hundreds of people.
Food Intoxication: Illness caused by consuming food
containing toxins produced by bacteria when they multiply in
food [e.g., Staphylococcus aureus, Clostridium botulinum,
Bacillus cereus].
Food Poisoning: Illness resulting from eating substance or
compound that the body cannot detoxify [e.g., some
mushrooms, cleaning and sanitizing chemicals, MSG,
sulfites, metal (lead) poisoning]. Normal cooking has no
effect on poisons and will not make poisonous food safe.
1283
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Types of Foodborne Illness – Infection,
Intoxication, and Poisoning
Types of Illness
Foodborne diseases or illnesses are reactions of the body to
consumption of foods containing sufficient quantities of
pathogenic bacteria and/or their by-products or poisonous
substances. The diseases (illnesses) are classified either as
infections, intoxications, or poisonings. When foodborne
illnesses are classified according to these three causes, control
procedures can be applied for each cause.
Infection
A food infection occurs when living pathogenic bacteria are
consumed in sufficient numbers, survive digestion, and
multiply or sporulate in the body.
Two types of foodborne infections are known. One type
results when the intestinal mucosa is penetrated and the
infecting organism multiplies therein or passes to other tissues
where it multiplies or lodges. For example, hepatitis A virus,
is absorbed through the intestinal wall, assimilated in the
blood stream, and carried to the liver. It lodges in liver cells
and multiplies. The second type of infection results when
enterotoxins are released as the infecting organism multiplies,
sporulates, or lyses (fragments or breaks apart) in the intestinal
tract.
Infections in humans and animals result in varied symptoms,
and their manifestations differ in severity. Organisms can
colonize on the skin of the body, the intestinal tract, the
mucosa, and the body tissues without producing identifiable
evidence of a host reaction. An example of this is
Staphylococcus aureus, which is a common resident in the
noses of healthy people. Individuals with no symptoms nor
gross signs of infection can have infecting microorganisms in
their feces and urine and on their skin. When infections
develop, symptoms can range from mild to severe, and are
identified as clinical diseases or illnesses.
Disease or illness is the host response to the pathogenicity and
virulence of an organism. Pathogenicity is the capacity of an
agent to cause disease in an infected host and to produce
severe illness, depending on virulence. Infected persons or
animals are potential sources of infections. Carriers are
persons who are infected and show no signs or symptoms of
illness. A person can be a carrier in a stage of infection that
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4a-29
Pathogens that cause illness through infection and that can
be inactivated by heat include:
Bacteria
Brucella
Listeria monocytogenes
Salmonella spp.
Yersinia enterocolitica
Shigella spp.
Campylobacter jejuni
Vibrio spp.
Escherichia coli
Viruses
Hepatitis A virus
Noroviruses
Parasites
Taenia saginata
Entamoeba histolytica
Trichinella spiralis
Toxoplasma gondii
Giarda lamblia
Fish tapeworms, round worms, and flukes
Intoxication
Bacterial toxins. An intoxication is caused by the ingestion
of metabolic by-products, or toxins, which are formed and
excreted by certain microorganisms when they multiply in
foods. The onset of symptoms usually occurs within a short
period of time (often less than 2 hours) after eating food
containing the toxin.
A fairly high bacterial population (i.e., 105 to 106 per gram) is
required to produce toxin at illness-causing levels. The time
required for toxin producing microorganisms to multiply and
produce toxin in foods is usually more than 8 hours, even at
temperatures above 70°F (21.1°C). Some toxins are altered by
heat, and if products containing these toxins are heated for
sufficient periods of time, the toxin is inactivated. (Toxins
produced by Clostridium botulinum are destroyed when
products are heated to 185°F (85°C) for 5 minutes.) Some
toxins are quite resistant to heat. (Type A toxin produced by
Staphylococcus aureus retains its toxigenicity at boiling
temperatures for more than 25 minutes.)
Some pathogens form toxins within the intestinal tract. For
example, Clostridium perfringens, a spore-forming pathogen,
produces a toxin when vegetative cells form spores in the
intestine.
Some toxin-producing pathogens are also spore-formers (e.g.,
C. botulinum and B. cereus). These pathogens are dangerous
because the heat-resistant spores are difficult to destroy.
Control of Toxin-Producing Microorganisms
The most effective control for toxin-producing
microorganisms is preparing, storing, holding, and serving
food at temperatures and conditions that prevent their growth
in foods.
Pathogens that produce toxic by-products in foods include:
Non-spore forming: Staphylococcus aureus
Poisons that may be present in food as a result of intentional
or unintentional contamination include:
Spore forming: Clostridium botulinum, Bacillus cereus
Mold toxins. Mycotoxins (toxic substances produced by
molds) represent a human health hazard. The full extent of
this hazard is not known at this time. Some mycotoxins have
an effect on liver and kidney function and some affect the
central nervous system. Aflatoxin is a mycotoxin produced by
the growth of Aspergillus flavus in grains, nuts, and legumes
of high moisture content. Aflatoxin is known to cause cancer
of the liver in animals.
Mycotoxin control. To understand the effect of mycotoxins
on public health, methods have been developed to quantify
their concentration in human diets. Methods of detecting the
presence of mycotoxins in food have been developed and
acceptable limits have been established for grains, nuts (e.g.,
peanut butter) and legumes. Harvesting, processing, and
storage conditions influencing mycotoxin production have
been examined. Better methods are being developed to reduce
the incidence of this hazard.
Molds that produce mycotoxins in food include:
Aspergillus flavus
Byssochlamys nivea
Fusarium spp.






An excess amount of monosodium glutamate in food.
Accidental addition of cleaning and sanitizing chemicals
to food.
Consumption of poisonous mushrooms.
Heavy metal poisoning resulting from acid foods (e.g.,
salad dressing, fruit juices, and wine) leaching out
cadmium, copper, and lead from some pottery and metal
containers.
Copper leached from copper water lines by carbon
dioxide backflow valves on carbonated beverage vending
machines.
Scombroid and ciguatera fish poisoning.
Mistaken use of nitrates for salt in salt shakers.
Solanine formed when potatoes are exposed to sunlight.
In 1981, some 25 people suffered mushroom poisoning
resulting in 3 fatalities. Four cases of MSG poisoning were
reported that year. From 1983 to 1987 an average of 250
documented food poisoning cases per year were attributed to
mushrooms, heavy metals, and other chemicals, scrombotoxin,
and ciguatoxin.
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Cleaning compounds
Nitrates, nitrites
Heavy metals
Sulfites
Histamines
Sanitizers
Mushrooms
Monosodium glutamate
Ciguatoxin
Paralytic shellfish toxin
Summary
Bacterial pathogens that can cause illness by infection or by
production of toxins must always be assumed to be present in
food. Spores of Clostridium botulinum, Bacillus cereus, and
Clostridium perfringens survive most cooking procedures.
Other pathogens such as Salmonella and Staphylococcus
aureus may enter food through cross-contamination after it is
cooked.
Cooking or reheating food will destroy vegetative cells of
pathogenic bacteria but probably will not inactivate spores
and toxins produced by some pathogenic microorganisms.
Cooking or reheating foods cannot be relied upon to make
foods safe.
References:
Frazier, W.C., and Westhoff, D.C. 1988. Food Microbiology,
4th ed. McGraw-Hill, New York, NY.
Jay, J. M. 2000. Modern Food Microbiology. 6th ed.
Chapman & Hall. New York, N.Y.
Mossel, D.A.A., Corry, J. E. L., Struijk, C. B., and Baird, R.
M. 1995. Essentials of the Microbiology of Foods.
John Wiley & Sons. New York, NY.
Poisoning
Food poisoning. Food poisoning is intoxication that results
from the consumption of a substance that the liver and other
organs cannot detoxify or eliminate from the body. Usually,
but not always, there is a rapid onset of unfavorable
symptoms. Examples include:


Control. Once there is a toxic compound or poison in a food,
there is nothing a foodservice operator can do. The only
control is to purchase foods that the supplier certifies are safe,
teach employees the importance of using the proper amount of
food chemicals, and separate concentrated chemicals such as
sanitizers, insecticides, and rodenticides in locked storage
areas.
4a-30
The cause of death is a paralysis of the respiratory muscles.
Botulism has a high death rate in the United States.
Approximately 65% of afflicted persons die. This high death
rate is the reason botulism is much feared in spite of the fact
that it does not occur often. Complete recovery of the nonfatal
cases is very slow and may extend over several months.
FOODBORNE ILLNESS SITES IN THE BODY
Clinical diagnosis of botulism is confirmed by detection of the
toxin in the incriminated foodstuff or in patient's specimens
(i.e., serum, vomit, feces). Toxin in the blood serum can
usually be detected for a few days following ingestion of
botulinum toxin and sometimes for up to 25 days.
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15
Human Foodborne Illness – Sites,
Incubation, and Symptoms
Foodborne Illness Symptoms
Symptoms of foodborne illness can affect many different sites
in the body. These include vital organs such as the liver,
kidney, heart, and lungs; the vascular system; the central
nervous system; the skeletal system; and excretory system.
Important symptoms and causes of foodborne illnesses are
listed in Table 4-8. Most people think of foodborne illnesses
as having only short-term (i.e., a few hours to a few days)
effects. This is not always true. Some foodborne illnesses can
be life threatening and can have long-term effects.
Botulism
Onset. Symptoms of botulism usually develop within 12 to
36 hours after ingestion of food containing botulinum toxin.
In extreme cases, symptoms occur within 2 hours or after 14
days.
The severity of the illness is dependent upon amount of toxin
ingested. The toxin of Clostridium botulinum is extremely
lethal and only small amounts are necessary to cause illness
and death if undiagnosed and untreated. The toxin is absorbed
into the bloodstream through the small intestine. It then
circulates throughout the body and is responsible for
neurological impairment when it binds to the neuromuscular
nerve junctures. The result is blockage of neurotransmitters,
as a result vital organs (heart, lungs, intestinal tract) stop
functioning.
Symptoms. Before neurological symptoms appear,
gastrointestinal symptoms such as nausea, vomiting, and
diarrhea may often develop, particularly in Type E botulism.
Weakness, lassitude, dizziness, and vertigo often develop
early. Blurred vision, diplopia, dilated and fixed pupils, and
impaired reflection of light appear very frequently. Difficulty
in speech and in swallowing, severe dryness of the mouth,
tongue, and throat are also noted. Abdominal fullness and
pain are often seen, particularly in Type E cases. Constipation
is severe. Muscle weakness occurs in the soft palate, tongue,
diaphragm, neck, and extremities causing difficulty in walking
and decreased grip. The respiratory muscles and diaphragm
may become paralyzed.
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4a-31
The illness may be treated by administering an antitoxin
specific for the particular type of toxin involved. Despite the
availability of antitoxins, botulism therapy is still not
satisfactory due to the lag times between the ingestion of the
food, the appearance of symptoms, the diagnosis, and the
procurement of the specific antitoxin. The general availability
of the specific antitoxins is limited. Many hospitals do not
stock the antitoxins because of the rarity of botulism incidents.
Toxic dose. As few as 10 spores, if allowed to out-grow and
form vegetative cells in improperly processed, packaged, and
stored food products having low oxygen availability, can
produce sufficient toxin to cause a serious, even fatal, case of
botulism. An inoculum of 104 to 105 cells per gram of food
has been shown to be sufficient to produce sufficient amount
of toxin to cause illness and possible death.
Staphylococcus aureus
General characteristics. Staphylococcal foodborne illness
(intoxication) is caused by ingestion of one or more of six
heat-stable enterotoxins produced by certain strains of this
species.
Small numbers of S. aureus are usually found in foods that
have been exposed to or handled by food handlers. Detection
of a small number S. aureus does not, however, assure the
safety of the food because the organism can be killed after
producing toxin. The toxins are quite stable to heat and can
remain in foods to cause illness, even after being subjected to
high temperatures during commercial canning procedures.
The ingestion of toxin-containing food causes illness. The
toxins accumulate in food when the S. aureus cells are allowed
to multiply profusely. When the toxin-containing food is
ingested, it passes through the stomach and is absorbed in the
intestine. The absorbed toxin triggers the vomiting center in
the brain by way of the vagus and sympathetic nerve. This
effect produces the feeling of nausea, salivation, and vomiting.
Other effects on the central nervous system produce sweating,
headache, and shallow respiration. The toxin also causes
secretion of fluids from intestinal mucosa (lining of the
intestine), resulting in diarrhea. Enteritis (inflammation of the
intestine) develops due to mucosal cell disintegration which
leads to ulceration of the mucosa and destruction of the
surface lining of the intestine.
Symptoms. The symptoms usually appear within 2 to 4 hours
after ingestion of food containing the toxin, but the times vary
from 30 minutes to 8 hours. The symptoms include vomiting,
salivation, nausea, abdominal cramps, diarrhea, headache,
muscular cramps, sweating, chills, prostration, weak pulse,
and shallow respiration. The severity of the symptoms varies
with the susceptibility of the individual, the concentration of
the toxin in the food, and the amount of toxin consumed.
for 6 to 12 hours. Vomiting, fever or headache is rare. The
illness is seldom fatal.
The duration of the illness is less than 24 hours to 2 days.
Mortality is extremely low. In severe cases, headache,
muscular cramping and marked prostration may occur. Body
temperature may be elevated or depressed and lowered blood
pressure can be quite harmful in the elderly. In these severe
cases, saline solutions are administered.
Infective or toxic dose. Sufficient toxin to cause illness is
released during sporulation of a cell population of about 10 6
per gram.
Toxic dose. The number of S. aureus required to produce
enough toxin to cause illness is 106 organisms per gram in the
food. The toxins cause inflammation of the lining of the
intestinal tract of the victim, resulting in gastroenteritis.
Immunity. Considerable variation in susceptibility to this
type of intoxication has been noted in tests performed with
human volunteers and animals.
In outbreaks of staphylococcal food intoxication it is unusual
if all individuals who consume the incriminated food become
ill. The variation in amounts of food eaten and uneven
distribution of the toxin in the food may be responsible. Some
individuals do not seem to be affected by food containing the
toxin and experience few if any symptoms of illness. This
variation between people may be due to prior exposure to the
specific enterotoxin and thus the development of a resistance
or immunity.
Hepatitis A Virus
Characteristics. This virus may be present in sewagepolluted waters and in seafood taken from these waters.
People may also be the source of this virus.
The virus does not multiply in food but can remain viable in
food at refrigeration or freezing temperatures.
Infective dose and symptoms. The exact number of virus
particles required to cause illness is not known at this time, but
is probably less than 100.
The virus is absorbed in the intestine and carried by the blood
to the liver. Hepatitis A virus particles replicate within liver
cells causing the characteristic symptoms listed below.
Symptoms of illness may appear in as soon as 10 days or up to
40 days after consumption. These include jaundice,
abdominal pain, loss of appetite, and general malaise.
Complete recovery occurs within a few months in the majority
of cases, although permanent liver damage can occur.
Clostridium perfringens
The illness occurs when toxin is released from cells of C.
perfringens during sporulation (spore formation) in the small
intestine. The toxin is absorbed into the intestinal mucosa.
This causes an increased release of fluid, sodium, and
chloride. Mucosal cellular function is altered and resultant
symptoms occur.
It is also thought that under some conditions vegetative cells
may form toxins when they sporulate in foods. The toxin is
little affected by freezing or refrigerated storage of foods.
Symptoms. The symptoms of C. perfringens are similar to
those of staphylococcal intoxication but are somewhat milder.
Symptoms of nausea, intestinal cramps and diarrhea begin 8 to
22 hours after ingestion of the contaminated food and continue
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4a-32
Salmonellosis
Characteristics. Salmonellosis results when a sufficient
number of organisms reach the small intestine and multiply in
the lumen. Salmonella spp invade cells in the intestinal
epithelium and multiply. As a result, the function of these
cells is altered and there is a release of fluid, producing
diarrhea. When Salmonella invades cells beyond the intestinal
epithelium it can be absorbed in the bloodstream and carried
by the blood (septicemia) to other organs and tissues of the
body.
The outcome of ingesting viable Salmonella depends upon the
virulence of the strain and the quantity ingested plus host
factors which include age and state of health.
Reduced bactericidal activity from increased pH of gastric
juice, more rapid passage of Salmonella through the stomach,
or altered intestinal flora cause persons to be more susceptible
to salmonellosis. Malnutrition, gastrectomy,
gastroenterostomy, vagotomy, and oral administration of
antibiotics influence susceptibility. General depression of
resistance caused by other concomitant illnesses (e.g., cancer,
nephritis, diabetes, anemia, alcoholism, sickle cell anemia,
AIDS) influence susceptibility, particularly to bacteremia
(carriage of bacteria in the blood stream). Apparently,
previous infection with serotypes other than S. typhi does not
produce acquired immunity.
Infective dose. The dose is the amount of microorganisms
ingested in the food. The number of organisms that actually
cause the infection depend on the age and health of the
individual. For healthy adults the level of contamination must
be fairly high (104 to 1010 organisms per gram of food). The
number necessary to cause illness is much lower in young
children, the elderly, and those whose health is otherwise
compromised. The level may be as low as 1 to 10 organisms
per 100 grams of food.
Age is an important determinant of susceptibility. Infants
under 4 months of age have the highest incidence of
salmonellosis. The incidence drops until age five, cases
reported for individuals after this age reaches a level
approximating that recorded for adults. In the elderly,
incidence rises again, and mortality sometimes occurs.
Symptoms. Illness occurs when people eat foods containing
vegetative Salmonella cells, which survive passage through
the stomach to grow and multiply in the intestine. Symptoms
such as abdominal cramps, diarrhea, fever, and vomiting
develop within 8 to 72 hours, usually between 20 and 48
hours. (Longer incubation periods usually are associated with
water-borne outbreaks.) Abdominal cramps, nausea and
vomiting are common for approximately 24 hours. Headache
and chills are possible Fevers are usually mild [below 100°F
(37.8°C)]. Symptoms usually subside in 2 to 5 days.
Severe symptoms include: water diarrhea containing mucous
and blood, severe cramping, dehydration, and convulsions.
Complications of arthritis, myocarditis, meningitis, and
pneumonia can occur. Death can result.
During the acute phase of diarrhea, 106 to 109 Salmonella per
gram of feces may be excreted. These bacteria may continue
to be excreted for months, rarely more than 3 months.
Chronic carriers are possible. Contamination of food by a
carrier is extremely likely. Salmonella from an ill person or a
carrier transmitted to food as the result of poor hand washing.
Even as few as 100 cells on the hands can seriously
contaminate any food or food product if hand washing is not
thorough.
Trichinosis
Incubation and onset. The incubation period, the time
between consuming infective Trichinella spiralis larvae and
onset of clinical symptoms, can be from 2 days to nearly 28
days depending on the life cycle of the parasite and the
number of larvae ingested. After ingestion of infected meat,
the larvae are released from encysted muscle during digestion.
The larvae mature into adults in the small intestine and
produce new larvae. These parasites migrate through the body
via the blood, invade the muscles and become fully developed,
infective, encysted larvae about 17 to 21 days after initial
infection.
Symptoms. Initial symptoms include: diarrhea, abdominal
discomfort, rapid and sharp intestinal pain, fever, fluid buildup
around the eyes. Later in the course of this infection (after
larvae become encysted in muscle), tenderness, pain, or
inflammation of the muscles develops. If muscle involvement
is extensive and heart muscle is affected, death results.
Treatment is directed toward the relief of symptoms. There is
no satisfactory treatment for trichinosis. Treatment with
thiabendazole may be effective if administered within 24
hours of trichina ingestion. Corticosteroids are given to those
critically ill, but the benefit of their use is in doubt.
Although ground beef is generally considered to be pure beef,
it may be adulterated either by contamination from an
uncleaned, common meat grinder that was previously used to
grind pork or by the intentional mixing of beef and pork. If
this contaminated ground beef is cooked to a rare state of
doneness, infective Trichinella are not destroyed.
References:
CAST (Council for Agricultural Science and Technology)
1994. Foodborne pathogens: Risks and consequences.
Task Force Report No. 122. CAST, 4420 West Lincoln
Way, Ames, Iowa.
Doyle, M. P., ed. 1989. Foodborne Bacterial Pathogens
Marcel Dekker, Inc. New York, NY.
Doyle, M. P., Beuchat, L. R., and Montville, T. J. eds. Food
Microbiology. Fundamentals and Frontiers. 2001
American Society of Microbiology. Washington, D. C.
FDA. 1993. HACCP. Regulatory Food Applications in
Retail Food Establishments. Dept. of Health and Human
Services. Division of Human Resource Development,
HFC-60: Rockville, MD.
Frazier, W.C. and Westhoff, D.C. 1988. Food Microbiology.
3rd ed. McGraw-Hill, New York, NY.
1901-04: ch4a rev 6/16/05 print 3/7/16
4a-33
Jay, J.M. 2000. Modern Food Microbiology. 6fth edition.
Chapman & Hall Inc., New York, NY.
Mims, C.A. 1987. The Pathogenesis of Infectious Disease.
Academic Press. London.
Mossel, D.A.A., Corry, J. E., Struijk, C. B., and Baird, R.
1995. Essentials of the Microbiology of Foods. John
Wiley and Sons, New York, NY.
Table 4-8
ILLNESSES ATTRIBUTED TO FOODS; A CLASSIFICATION BY SYMPTOMS, INCUBATING PERIODS, AND TYPES OF AGENTS
Illness or Disease
Agent
Time for Onset of
Illness
Signs, Symptoms and Severity
Duration/Prognosis
Sources
Factors that Contribute to
Foodborne Outbreaks
Foods most commonly implicated in
producing an allergic or adverse
response in sensitive individuals
include: cows milk, eggs, peanuts,
seafood (fish, oysters, scallops etc.),
all types of wheat products, tree nuts
(walnuts, pecans, pistachios, etc.,)
and corn and corn products.
Food allergies or adverse
reactions to food involve a very
small portion (1%) of the
population. However, retailers
and food producers and preparers
must provide an accurate account
of any ingredients in prepared
products to these individuals
Allergic or Adverse Reaction to Food
Food or component of
food that can cause an
abnormal response in
certain (sensitized)
individuals.
Minutes to hours
Any or a number of the following
symptoms:
Headache, tingling sensations
Pulmonary and cardiovascular
symptoms
Nausea, vomiting, retching,
diarrhea, abdominal cramps
Eczema and hives
Mental confusion
Duration and severity
depend on type and
amount of offending food
that was ingested and
degree of sensitivity of
individuals. Anaphylatic
shock after ingestion of
an offending food can
result in death. Severe
allergic reactions may be
treated with epinephrine.
Incubation (Latency) Period Usually Less than 1 Hour
Gastrointestinal
irritating group
mushroom poisoning
Upper Gastrointestinal Tract Signs and Symptoms (Nausea, Vomiting) Occur First or Predominate
Fungal Agents
30 minutes to 2 hours Nausea, vomiting, retching,
Duration depends on type Mushrooms. Possible resin-like
Purchasing mushrooms from
diarrhea, abdominal cramps
of mushroom ingested;
substance in some mushrooms
persons who mistake toxic
with treat-ment, recovery
mushrooms for edible varieties
period can last from 24
hours to several weeks.
As many as 100 deaths
may result annually
Copper poisoning
Few minutes to few
hours
Metallic taste, nausea, vomiting
(green vomitus), abdominal pain,
diarrhea
Lead poisoning
30 minutes or longer
Metallic taste, burning of mouth,
abdominal pain, milky vomitus,
bloody or black stools, foul
breath, shock, blue gum line
Tin poisoning
30 minutes to 2 hours
Zinc poisoning
Few minutes to a few
hours
Bloating, nausea, vomiting,
abdominal cramps, diarrhea,
headache
Pain in mouth and abdomen,
nausea, vomiting, dizziness
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4a-34
Chemical Agents
Mild cases usually
recover within six hours.
Severe poisoning can
result in death
Copper in pipes and utensils
combines with high-acid foods and
beverages
Processing or storing high-acid
food in contact with copper;
faulty backflow preventer valves
in vending machines that allow
carbonic acid to contact copper
pipes
Processing or storing high-acid
foods in lead-containing vessels
or containers with lead leachable
glazes; storing pesticides in same
area as foods
Acute symptoms subside
within 48 to 72 hours
after treatment is begun.
Therapy in mild cases
lasts 3 to 5 days. Some
symptoms can last for
months
Mild cases generally
recover within 6 hours
Lead in earthenware vessels,
pesticides, paint, plaster, putty
combines with high-acid foods and
beverages
Tin in tinned cans combines with
high-acid foods and beverages
Using uncoated tin containers for
storing high-acid foods
Mild poisonings usually
recover within 6 hours;
severe poisoning can
result in death
Zinc in galvanized containers
combines with high-acid foods and
beverages
Storing high-acid foods in
galvanized containers
Illness or Disease
Agent
Time for Onset of
Illness
Signs, Symptoms and Severity
Duration/Prognosis
Sources
Factors that Contribute to
Foodborne Outbreaks
Nitrite poisoning
1 to 2 hours
Nausea, vomiting, cyanosis,
headache, dizziness, weakness,
loss of consciousness, chocolatebrown colored blood
If amount consumed is
low, symptoms will pass;
if large amount is
consumed, death can
result
Excessive amounts of nitrites or
nitrates used as curing compound or
ground water from shallow well,
fertilizer
Using excessive amounts of
nitrites or nitrates in foods for
curing or for covering up
spoilage; mistaking nitrites for
common salt and other
condiments; improper
refrigeration of fresh produce;
excessive nitrification of
fertilized fields
Sodium hydroxide
poisoning
Few minutes
Burning of lips, mouth and
May be weeks to months,
throat; vomiting, abdominal pain, depending on amount
diarrhea
consumed and severity of
injury.
Sodium hydroxide in bottle washing
compounds, detergents, or drain
cleaners contaminating or remaining
in bottled beverages, pretzels,
seasonings
Inadequate rinsing of bottles
cleaned with caustic soda;
inadequate baking of pretzels;
accidental addition of cleaning
compound to food seasoning
dispenser
Monosodium
glutamate
Few minutes to 1 hour Burning sensation in back of
neck, forearms, chest; feeling of
tightness; tingling; flushing;
dizziness; headache; nausea
Excessive amounts monosodium
glutamate (MSG) or free glutamic
acid in foods.
Using excessive amounts of
MSG as flavor intensifier
Generally less than 24
hours
Neurologic Symptoms and Signs (Visual Disturbances, Tingling, and/or Paralysis) Occur
Fish Toxins
Paralytic shellfish
toxin (PSP). Saxitoxin and similar
toxins from dinoflagellates; Protogonaulax and
Gymnodinium species,
which are consumed
by shell fish.
(Intoxication)
Diarrhetic shellfish
poison.
(Intoxication)
Minutes to 2 hours
Dose = 100 g
Ciguatoxins
(Intoxication)
Minutes to
24 hours
Dose = 40 - 70 ng.
30 minutes to
2 to 3 hours
Dose = 32 - 77 g
1901-04: ch4a rev 6/16/05 print 3/7/16
Tingling, burning, numbness
around lips and fingertips,
giddiness, incoherent speech,
difficulty to stand, respiratory
paralysis. Symptoms persist as
long as toxin remains and is
absorbed by host; fatalities may
occur, depending upon amount
ingested.
(Mild to severe)
Nausea, vomiting, diarrhea, and
abdominal pain accompanied by
chills, head-ache and fever.
(Mild)
Several days
Shell fish only from NE or NW
coasts in U.S. and North America.
[Harvesting shellfish from waters
with high concentration of
Protogonaulax or Gymnodinium.]
Also in Central America and Asia.
2 to 3 days
Consumption of mussels, oysters, and Consumption of shellfish from
unsafe waters.
scallops taken from contaminated
waters
Gastrointestinal symptoms,
tingling and numbness of mouth
and limbs, muscular and joint
pain, dizziness, cold-hot
sensations, rash, weakness,
slowness of heart beat,
prostration, paralysis.
(Mild to severe)
Gastroenteritis disappears
in a few days;
neurological problems
may last several days;
deaths occur.
Eating liver, intestines, roe, gonads,
Consumption of fish from unsafe
waters.
or flesh of tropical reef fishes (e.g.,
barracuda, grouper, red snapper,
amberjack, goat fish, skip jack, parrot
fish). Usually large reef fish are
more commonly toxic.
4a-35
Harvesting shellfish from
contaminated waters.
Illness or Disease
Agent
Time for Onset of
Illness
Signs, Symptoms and Severity
Duration/Prognosis
Sources
Factors that Contribute to
Foodborne Outbreaks
Domoic acid
(Amnesic Shell- fish
Poisoning)
(Intoxication)
Within 24 hours.
Dose = 60 g
Gastrointestinal symptoms
(nausea, vomiting, diarrhea, and
abdominal pain) accompanied by
neurological problems
(confusion, memory loss,
disorientation, seizure, coma.
(Mild to severe)
Hours to permanent
Consumption of mussels and clams
taken from contaminated waters.
Neurotoxic shellfish
poison (brevetoxins)
(Intoxication)
Minutes to hours
Dose = >80 g
Gastrointestinal symptoms
(nausea, vomiting, diarrhea, and
abdominal pain) accompanied by
neurological problems (tingling
and numbness of lips, tongue,
and throat; muscular aches,
dizziness, reversal of sensations
of hot and cold).
(Mild to moderate)
Headache, dizziness, nausea,
vomiting, peppery taste, burning
throat, facial swelling and
flushing, stomach pain, itching of
skin.
(Mild to severe)
A few hours to several
days.
Consumption of shellfish taken along Consumption of shellfish from
unsafe waters.
the Southern coast of the United
States (Florida and the Gulf Coast).
May be associated with the Red Tide.
 1 day to
2 days
[Histamine-like substance produced
by Proteus spp. or other bacteria
from histidine in fish flesh].
Fishery products: tuna (yellow fin
and skipjack), mackerel, mahi-mahi,
blue fish, abalone. Has also been
found in Swiss cheese.
Consumption of products
containing high amounts of
histamine. Toxin forms in a food
when certain bacteria are present
and time and temperature permit
their growth. Cooking, canning
and freezing do not reduce toxic
effect.
Major neurological problems:
numbness in face and hands,
headache, paralysis, respiratory
distress, speech is affected,
dyspnea, cyanosis, hypotension,
cardiac arrhythmia, mental
impairment, and convulsions.
May also be gastrointestinal
involvement (nausea, diarrhea,
and/or vomiting).
(Moderate to severe)
Hours
50% of cases are fatal.
Consumption of Puffer fish only,.
Most cases occur in Japan and in
other regions of the Indo-Pacific.
No recent cases in U.S.
Scombroid (Histamine Minutes to 6 hours
or histamine-like)
Dose = 50 mg
histamine
(Intoxication)
Tetrodoxin
[Puffer fish poisoning
(Intoxication)
Minutes to
3 hours
Dose = 100 g
1901-04: ch4a rev 6/16/05 print 3/7/16
4a-36
Consumption of shellfish from
unsafe waters.
Illness or Disease
Agent
Botulism
Clostridium
botulinum
(Toxicoinfection)
(Infant botulism)
Time for Onset of
Illness
Signs, Symptoms and Severity
2 hours to 8 days;
mean = 18 to 36 hours
Inf. dose = Up to
about 109 LD50 * toxin
in mice.
Intoxication
(Adults)
Duration/Prognosis
Sources
Factors that Contribute to
Foodborne Outbreaks
Bacterial Agent
Neurologic Symptoms and Signs (Visual Disturbances, Tingling, and/or Paralysis) Occur
Toxicoinfection for infants only.
In those who survive the Found in soil, fresh-water mud, and
Gastrointestinal symptoms may
animals. Types A, B, E, and F
Has been traced to giving
precede neurological symptoms; respiratory paralysis,
produce lethal neurotoxins for
babies honey.
vertigo, double or blurred vision, symptoms may last for
humans.
dryness of mouth, difficulty in
weeks to months.
Most adult incidents due to
swallowing, speaking and
7.5% fatality case ratio.
Canned low-acid foods (usually
home-canned or fermented
breathing; descending muscular
home canned), smoked fish, cooked
foods; occasionally
weakness, constipation, pupils
potatoes, garlic in oil, coleslaw,
mishandling in foodservice.
dilated or fixed, respiratory
onions, meat loaf, stew left in
Most due to improper holding
paralysis.
ovens without heat overnight,
and/or preservation of
In severest cases, death results
fermented fish eggs, fish, marine
vegetables (peppers, pimentos)
within 24 hours.
mammals.
meat, fish.
(Severe)
Incubation (Latency) Period 1 to 6 Hours
Upper Gastrointestinal Tract Signs and Symptoms (Nausea, Vomiting) Occur First or Predominate
Bacterial Agents
Bacillus cereus
gastroenteritis
(emetic) Exoenterotoxin of B.
cereus; (strains differ
from those cited later)
(Intoxication)
1/2 to 5 hours.
Usually less than 12
hours.
Inf. dose = 105 to 1011
Nausea, vomiting, occasional
diarrhea
Usually 6 to 24 hours
Staphylococcal
intoxication
Exo-enterotoxins A,
B, C, D, E, or F of
Staphylococcus
aureus;
1 to 8 hours; mean 2
to 4 hours.
Toxin produced by
growth of Growth of
106 CFU/ gram of
food or consumption
of <1g enterotoxin
Nausea, vomiting, retching,
abdominal pain, diarrhea, prostration
24 to 48 hours; deaths are Staphylococcus aureus is found in the
rare but have been
nose and throat and skin of people
recorded among the aged and animals. Incidents occur when
the organism contaminates and grows
in food to high levels and produces a
heat resistant enterotoxin. Can grow
in salty foods.
LD50 = Lethal dose for 50% of the population
1901-04: ch4a rev 6/16/05 print 3/7/16
4a-37
Found in soil. Contaminant of
cereals, spices, grains, sprouts.
Common incidents involve boiled or
fried rice
Holding cooked foods at room
temperature or in a hot holding
device at less than 122°F (50°C);
too slow cooling of food to less
than 41°F (5°C).
Improper handling and storage
of fermented sausages, ham,
meat, and poultry products;
cream-filled pastries; whipped
butter; cheese; dry milk; food
mixtures; high-protein leftover
foods; food handlers with
infected cuts and poor hygiene
practices.
Illness or Disease
Agent
Time for Onset of
Illness
Signs, Symptoms and Severity
Duration/Prognosis
Sources
Factors that Contribute to
Foodborne Outbreaks
Incubation (Latency) Period Usually 7 to 12 Hours
Aeromonas
hydrophila
Lower Gastrointestinal Tract Signs and Symptoms (Abdominal Cramps, Diarrhea) Occur First or Predominate
Bacterial Agents
Onset time = ?
Nausea, vomiting, diarrhea,
Days to weeks
Has been found in fish and shellfish, Cases have been noted in clinical
Inf. dose = unknown
and stomach cramps. Immuneas well as red meats (beef, lamb,
centers, however, there has not
compromised most susceptible.
pork) and poultry.
been a fully confirmed outbreak
(Mild, self-limiting)
in the U.S.
Bacillus cereus
enteritis
(diarrheal)
Enterotoxin of B.
cereus; organism in
soil (strains differ
from those cited
earlier)
(Toxicoinfection)
8 to 16 hours
mean = 12 hours
Nausea, abdominal pain, watery
diarrhea
(Mild, self-limiting)
6 to 24 hours
Found in soil.
Incidents traced to cereal products,
soups, custards and sauces, meat loaf,
sausage, reconstituted dried potatoes,
refried beans. (Spore out-growth in
food. Viable cells proliferate in food
and in GI tract after consumption to
cause illness.)
Holding cooked foods at kitchen
temperatures or in a hot holding
device at less than 122°F (50°C);
cooling food too slowly to less
than 41°F (5°C); inadequate
pasteurization during cooking or
reheating; inadequate reheating
of leftovers
Clostridium
perfringens
gastroenteritis
(Toxicoinfection)
8 to 22 hours
mean = 10 hours
Inf. dose = 106 to
1010 CFU
Endo-enterotoxin formed during
sporulation of C. perfringens in
intestines.
Abdominal pain, diarrhea.
Rarely vomiting or nausea.
Fatalities are rare.
(Mild)
12 to 24 hours
Spores and organisms are found in
feces of infected humans, other
animals, and in soil. Endoenterotoxin forms during sporulation
of C. perfringens in intestines.
Incidents involve cooked meat,
poultry, gravy, sauces, soups, refried
beans.
Holding cooked foods at kitchen
temperatures or in a hot holding
device at less than 127°F
(52.8°C); cooling food too slowly
to less than 41°F (5°C);
inadequate pasteurization during
cooking or reheating
Campylobacter jejuni
enterocolitis
(Infection)
2 to 7 days
Diarrhea (often times bloody),
mean = 3 to 5 days
severe abdominal pain, fever,
Inf. dose =  500 CFU loss of appetite, general feeling
of ill health, headache, vomiting
(Mild to moderate)
1 to 4 days; no longer
than 10 days
Raw milk, poultry, beef liver, raw
clams, water
Escherichia coli
0157:H7 (enterohemorrhagic)
(Toxicoinfection)
3 to 7 days
Inf. dose estimated to
be 101 to 103 CFU
Inadequate pasteurization during
cooking or reheating; crosscontamination on food contact
surface; use of unpasteurized
dairy products; inadequate hand
washing.
Most outbreaks are associated
with insufficiently cooked ground
beef patties in food service
establishments and in nursing
homes; also associated with
consumption of raw milk and
unpasteurized cider.
1901-04: ch4a rev 6/16/05 print 3/7/16
Severe abdominal pain, watery
Days to weeks
diarrhea that may become grossly
bloody. Occasionally vomiting
occurs. May or may not be fever.
May lead to severe complications
in young children, elderly and
immune-compromised persons.
2 % fatality case ratio.
(Moderate to severe)
4a-38
Found in fecal material from animals
and humans
Illness or Disease
Agent
Time for Onset of
Illness
Signs, Symptoms and Severity
E. coli (enteropathogenic)
(Infection ?)
1 to 6 days
Inf. dose estimated to
be 106 to 1010 CFU for
adults
Watery or bloody diarrhea. Seen
in infants and young children of
third world countries. Produces
verotoxin or shiga-like toxin.
(Mild to moderate)
Days to weeks
Fecal organism from animals and
humans.
Unlikely to be a significant cause
of foodborne illness in the U.S.,
Canada, or W. Europe. Most
cases in young children in
tropical areas with poor hygienic
standards.
E. coli (enteroinvasive)
(Infection)
1 to 3 days
Diarrhea or mild dysentery.
May be blood or mucous in
stools. Sometimes mistaken for
shigellosis.
(Mild to moderate)
Days to weeks
Fecal organism from animals and
humans.
E. coli (enterotoxigenic)
(Toxicoinfection)
1 to 3 days
Watery diarrhea, abdominal
cramps, low-grade fever, nausea,
and malaise.
(Mild to moderate)
Days to weeks
Fecal organism from animals and
humans.
Salmonellosis
(Infection)
6 to 72 hours; mean 18
to 36 hours
Inf. dose = 1 to about
109 CFU
Abdominal pain, diarrhea, chills,
fever, nausea, vomiting, general
feeling of ill health
(Mild to severe)
Typically 2 to 5 days,
although protracted cases
may last 10 to 14 days;
stool cultures may be
positive for Salmonella
for up to 4 weeks after
illness
Various serotypes of Salmonella
from feces of infected humans and
animals Foodborne incidents have
commonly implicated meat, poultry,
raw milk, and eggs. However,
numerous other foods are involved,
e.g., peanuts. cantaloupe, chocolate,
water melon, tomatoes
Unlikely to be a significant cause
of foodborne illness in the U.S.,
Canada, or W. Europe. Most
cases in young children in
tropical areas with poor hygienic
standards.
Most cases in tropical countries
with poor hygienic standards.
Cases in U.S. are rare; most are
associated with foreign travel.
Most common cause of traveler's
diarrhea. Highest incidence in
children < 2 years in developing
countries.
Holding cooked foods at
temperatures for periods of time
that allow microorganism to
multiply; cooling food too
slowly; inadequate pasteurization
during cooking or reheating;
cross-contamination between
food products, particularly
between raw and cooked food
products; inadequate hand
washing.
Shigellosis
Shigella flexneri,
S. dysenteriae,
S. sonnei, and S.
boydii
(Infection)
1 to 7 days
Abdominal pain, diarrhea, bloody Generally less than 7
and mucoid stools, fever
days; untreated patients
(Moderate to severe)
may shed Shigella in
feces for 2 weeks or more
after recovery
Fecal contamination from infected
individuals, poor sewage disposal,
contaminated water source. Any food
can be affected through crosscontamination by infected food
handler
Vibrio Cholerae (01)
Cholera
(Toxicoinfection)
1 to 3 days
Profuse watery diarrhea (rice
water stools), vomiting,
abdominal pain, dehydration,
thirst, collapse, reduced skin
turgor, wrinkled finger, sunken
eyes.
(May be mild, usually severe)
Feces of infected humans. Outbreaks Poor sewage disposal,
frequently associated with seafood,
contaminated water source. Rare
contaminated water supply, and foods in U.S.
washed or prepared with
contaminated water.
Inf. dose = 108 CFU
for adults with no
underlying illness
Inf. dose = 106 to 108
CFU for adults with
no underlying illness
Inf. dose = 101 to
106 CFU
Inf. dose = 106 CFU
1901-04: ch4a rev 6/16/05 print 3/7/16
4a-39
Duration/Prognosis
Can last 2 to 7 days with
appropriate therapy; left
untreated, cholera can
cause death
Sources
Factors that Contribute to
Foodborne Outbreaks
Poor personal hygiene of infected
food handlers responsible for
most cases, e.g., inadequate hand
washing. Reported in salads
(lettuce) and water supplies.
Illness or Disease
Agent
Time for Onset of
Illness
Vibrio Cholerae
(non-01)
(Infection,
toxicoinfection)
1 to 3 days
Vibrio parahaemolyticus
(Infection)
2 to 5 days
Inf. dose = 105 to 108
CFU
Vibrio vulnificus
(Infection)
Median time = 16
hours.
Inf. dose = Estimate 1
CFU for persons with
elevated serum iron
concentration.
Inf. dose = 106 to 108
CFU
Yersinia enterocolitica 1 to 3 days
(Infection)
Inf. dose =
3.9 x 109 CFU
1901-04: ch4a rev 6/16/05 print 3/7/16
Signs, Symptoms and Severity
Duration/Prognosis
Sources
Factors that Contribute to
Foodborne Outbreaks
Diarrhea, (may have bloody
stools) abdominal cramps, and
fever; sometimes nausea and
vomiting.
(Mild to moderate)
Abdominal pain, diarrhea,
nausea, vomiting, fever, chills,
headache
(Mild, self-limiting)
Days
Outbreaks associated with seafood
taken from contaminated waters,
mainly in shellfish from southern
waters.
Harvesting shellfish from
contaminated waters.
2 to 5 days
Most cases are associated with sea
food [marine fish, shellfish, crustacea
(raw or recontaminated)].
Contaminated sea water.
Organism enters blood stream to
cause septic shock and death
(50% fatality ratio). Individuals
develop bulbous skin lesions.
Amputations may be required.
(Severe complications)
Days to weeks
All known cases associated with
seafood, especially raw oysters taken
from contaminated waters.
Susceptible individuals are those with
underlying chronic disease
(particularly liver disease). Most
victims are male and have chronic
liver or blood related disorders.
Inadequate cooking; improper
refrigeration; crosscontamination; improper cleaning
of equipment; using sea water in
food preparation or to cool
cooked foods; using suppliers
who do not have effective
HACCP programs
Consumption of raw oysters,
inadequate cooking of oysters
and other shellfish.
Gastroenteritis with diarrhea,
Days to weeks
and/or vomiting; fever and
abdominal pain are common
symptoms. Sometimes mimics
appendicitis. Longer term effects
are linked to reactive arthritis and
Reiter's syndrome.
(Mild to moderate, self-limiting
to chronic)
4a-40
Carried by swine. Associated with
pork, raw milk, or milk products,
carried by swine.
Cross-contamination of products,
failure to heat products to
pasteurization temperatures,
improper storage, poor sanitation
techniques by food handlers.
Illness or Disease
Agent
Time for Onset of
Illness
Signs, Symptoms and Severity
Duration/Prognosis
Sources
Incubation (Latency) Period Usually Greater than 72 Hours
Generalized Infection Symptoms And Signs (Fever, Chills, Malaise, and/or Aches) Occur
Bacterial Agents
Fever, headache, nausea,
4 to 21 days
Found in the soil and fecal material
vomiting, diarrhea precede
of infected humans and animals.
complications of stillbirths,
Foods implicated in outbreaks
meningitis, encephalitis, sepsis.
include coleslaw, lettuce, milk,
In healthy adults, "flu-like"
cheese, animal products, frankfurters.
symptoms may pass within a
week; the pathogen is a great
hazard to pregnant women and
their unborn fetuses; L.
monocytogenes is a cause of
stillbirths and abortions; this
pathogen also causes death in
immune-compromised
individuals.
(Mild to severe)
Factors that Contribute to
Foodborne Outbreaks
Listeriosis
(Listeria
monocytogenes)
(Infection)
4 to 21 days
Salmonella typhi and
paratyphi
[Typhoid or
Paratyphoid Fevers]
(Infection)
7 to 28 days
Inf. dose = <103 to
109 CFU
Malaise, headache, fever, cough, Weeks to months.
nausea, vomiting, constipation,
Possible relapses.
abdominal pain, chills, rose spots,
bloody stools.
10% fatalities
(Severe)
Fecal material from animals and
humans. Virulent form of
Salmonella. Usually traced water or
infected carriers; poor sewage
disposal.
Mycobacterium bovis,
avium, and
tuberculosis
(Infection)
Weeks to months
Inf. dose = 106 CFU
for adults
Cause of tuberculosis. Not
Weeks to months.
highly infectious, however only a
few organisms are needed to
cause disease. First stage is
silent, may or may not have
fever. Second stage: reinfection,
lesions develop in lungs and
possibly other tissues.
Degenerative disease
(Severe)
Fever, profuse sweating, chills,
Weeks
weakness, malaise, body aches,
chest and joint pains, weight loss,
and anorexia.
(Moderate to severe)
Mycobacterium spp. are found in soil, Consumption of raw milk,
water, and animals. Can be
contaminated water, and
transmitted in unpasteurized milk,
inadequately pasteurized meat,
meat, poultry or fish.
fish, and poultry products.
Currently, not thought to be
foodborne in the U.S.
Brucillosis
(Brucela abortus)
(Infection)
Inf. dose = >103 to
>105 CFU
Onset = ?
Inf. dose = ?
1901-04: ch4a rev 6/16/05 print 3/7/16
4a-41
Found in animals (cows, sheep,
goats, etc.) and humans.
Inadequate pasteurization during
cooking or reheating, failure to
properly pasteurize milk,
prolonged refrigeration above
32°F (0°C)
Outbreaks frequently waterborne;
contaminated shellfish or foods
handled by carriers and not
subsequently heated. Rare in
U.S.
Foodborne incidents have
included unpasteurized goat milk
and cheese.
Illness or Disease
Agent
Coxiella burnetii
(Q Fever)
(Infection)
Time for Onset of
Illness
2 to 4 weeks
Inf. dose = ?
Signs, Symptoms and Severity
Duration/Prognosis
Initial fever, followed by malaise, Days to weeks
anorexia, muscular pain, and
intense headache. (may be
misdiagnosed as influenza).
(Mild to severe)
Sources
Factors that Contribute to
Foodborne Outbreaks
Found in wild and domestic animals.
Most incidents have involved
drinking raw milk.
Consumption of raw milk.
Controlled by drinking or using
only pasteurized milk.
Incubation (Latency) Period 13 to 72 Hours
Streptococcal
1 to 3 days
infections. (Strepto
coccus Group A)
Inf. dose = Less than
Streptococcus
103 CFU
pyogenes from throat
and lesions of infected
humans
Sore Throat and Respiratory Signs and Symptoms
Sore throat, fever, nausea,
Generally 5 to 7 days;
Found in the nose, throat and skin of
vomiting, rhinorrhea, sometimes fever may persist up to 9 infected individuals. Infected persons
a rash.
days in children. Tonsils transmit bacteria to food (particularly
may remain swollen up to cooked foods held at growth
6 months
temperatures), milk, salads, custard,
rice, etc.
Persons with skin infections
touching or coughing into cooked
foods; inadequate pasteurization
during cooking or reheating;
inadequate hand washing; poor
food handling practices; crosscontamination.
Viral Agents
Norwalk agent
gastroenteritis
(norovirus)
16 to 48 hours
Inf. dose = unknown
Nausea, vomiting, abdominal
pain, diarrhea, low grade fever,
chills, general feeling of ill
health, loss of appetite, headache
(Mild to moderate)
48 hours; infected
persons may spread
disease 2 to 3 days after
recovery
The virus can be transmitted by
humans, water, seafood (clams,
oysters, cockles), green salads,
pastry, frostings (any food prepared
by infected workers.)
Sewage pollution of shellfish
growing waters; inadequate hand
washing
Hepatitis A (Infectious 10 to 50 days
hepatitis)
mean 25 days
Inf. dose = unknown
Fever, general feeling of ill
health, loss of appetite, tiredness,
nausea, abdominal pain, jaundice
(Moderate to severe)
Typically jaundice lasts 6
to 8 weeks; full recovery
is usually seen after 3 to
4 months
Hepatitis A virus from feces, urine,
blood of infected humans and other
primates.
Can be transmitted in food, especially
raw shellfish, salads, cold cuts; food
handlers; water
Inadequate hand washing;
inadequate pasteurization during
cooking or reheating; using
suppliers without effective
HACCP programs; harvesting
shellfish from sewagecontaminated waters; improper
sewage disposal
Giardia lamblia
(Infection)
5 to 25 days
Inf. dose = 1 or more
viable cysts
Abdominal pain, mucoid
diarrhea, fatty stools
(Mild to moderate)
Weeks to years
Contaminated water supply.
Contaminated vegetables, problem
for day-care centers.
Use of unsafe water.. Crosscontamination. Poor personal
hygiene and inadequate hand
washing by infected food
handler.
Cryptosporidium
parvum
(Infection)
1 to 2 weeks
Inf. dose = < 30 cysts
May be asymptomatic.
Frequently is characterized by
severe watery diarrhea.
Pulmonary or tracheal
cryptosporidiosis is associated
with coughing and low grade
fever accompanied by severe
intestinal distress.
(Moderate to severe)
4 days to 3 weeks
Contaminated water supply, marine
fish, possibly associated with raw
milk and raw vegetables, infected
food handler, problem for day-care
centers.
Use of unsafe water or raw milk.
Cross-contamination. Inadequate
hand washing by infected food
handler.
Parasitic Agents
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4a-42
Illness or Disease
Agent
Time for Onset of
Illness
Signs, Symptoms and Severity
Duration/Prognosis
Sources
Factors that Contribute to
Foodborne Outbreaks
Amebic dysentery
Entamoeba histolytica
(Amebiasis)
2 to 4 weeks
Inf. dose = 1 viable
cyst
May be asymtomatic, or may
produce vague gastrointestinal
distress, dysentery with blood
and mucus. May produce
intestinal blockage
(Mild to severe)
Usually weeks to months, Contaminated drinking water,
but may continue for
contaminated raw vegetables. Large
years
outbreak did occur at U.S. World's
Fair in Chicago in 1933. Was due to
defective plumbing (sewage)
contaminating potable water.
May be acquired when traveling in
third-world countries. Occurs in
crowded situations where there is
poor personal hygiene. Rare in the
U.S..
Toxoplasma gondii
(Infection)
10 to 13 days
Inf. dose = 1 or more
viable cysts
Fever, headache, aching muscles,
rash. Severe complications in
pregnant women; can cause birth
defects and mental retardation of
infants; fatalities occur in infants
and adults.
(Mild to severe)
Weeks to years
Failure to cook pork, beef, veal, and
lamb sufficiently, or consumption of
these same raw meats.
Anisakiasis
(Anisakid nematodes
Anisakis, Phocanema,
Porrocaecum)
(Infection)
Taeniasis (Beef
Tapeworm infection,
Taenia saginata from
flesh of infected
cattle)
(Infection)
Taeniasis (Pork
Tapeworm, Taenia
solium from flesh of
infected swine)
(Infection)
4 to 6 hours
Inf. dose = 1 larva
Stomach pain, nausea, vomiting,
abdominal pain, diarrhea, fever
(Mild to severe)
Symptoms persist as long Marine fish, rock fish, herring, cod,
as parasite survives
squid that carry anisakid
within host
nemitodes.
Consumption of inadequately cooked
or raw fish that contain the anisakid
nemitodes.
8 to 14 weeks
Inf. dose = 1 cyst
Vague discomfort, hunger pain,
loss of weight, abdominal pain
(Mild to severe)
Symptoms persist as long Raw insufficiently cooked beef
as worms and eggs
remain in the intestine; as
long as 30 years
8 to 14 weeks
Inf. dose = 1 cyst
Vague discomfort, hunger pains,
loss of weight
(Mild to severe)
Symptoms persist as long Raw or insufficiently cooked pork
as parasite is present in
host; may affect eyes
causing blindness;
fatalities occur when
heart muscle and central
nervous system are
affected
As long as parasites reMay be found in fresh water fish,
main in host
tuna, salmon, red snapper.
Using suppliers without effective
HACCP programs; inadequate
pasteurization during cooking and
reheating; inadequate sewage
disposal; sewage contaminated
pastures
Using suppliers without effective
HACCP programs; inadequate
pasteurization during cooking and
reheating; improper sewage disposal;
contaminated pastures
Found in pork, beef, veal, and lamb.
May be carried by rats, cats, and
dogs.
Other Parasites
Diphyllobothrium spp. About 10 days after
(Fish tapeworms)
consumption.
(Infection)
Inf. dose = 1 larva
Anemia
(Mild to severe)
Trichinella spiralis
(Infection)
Gastroenteritis, fever, swelling
about eyes, muscular pain, chills,
prostration, labored breathing.
Fatalities occur if vital organs are
invaded.
(Moderate to severe)
4 to 28 days
(mean = 9 days)
Inf. dose = 1 larva
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4a-43
Severe symptoms may
last up to 6 weeks; muscle
pain may persist
indefinitely
May be present in raw pork, game
meat, bear meat, and walrus meat.
Transmitted when fresh water fish,
tuna, salmon, red snapper are under
cooked or eaten raw.
Inadequate pasteurization during
cooking and reheating; eating raw or
inadequately cooked pork or bear
meat, inadequate cooking or heat
processing; feeding uncooked or
inadequately heat-processed garbage
to swine; rats in swine-producing
areas.
References:
Archer, F.E., and Young, F.E., 1988. Contemporary issues: Diseases with a food vector. Clin. Microbiol. Rev. 1:377-398.
Benenson, A.S., 1990. Control of Communicable Diseases in Man, 15th Edition, American Public Health Assoc., Washington, D.C.
CAST (Council for Agricultural Science and Technology) 1994. Foodborne pathogens: Risks and consequences. Task Force Report No. 122. CAST, 4420 West Lincoln Way,
Ames, Iowa.
Doyle, M.P., ed., 1989. Foodborne Bacterial Pathogens. Marcel Dekker, Inc., New York, NY.
FDA, 1993. HACCP. Regulatory Food Applications in Retail Food Establishments. Dept. of Health and Human Services. Division of Human Resource Development, HFC-60;
Rockville, MD.
IAMFES. 1987. Procedures to Investigate Foodborne Illness, 3rd Edition, Ames, IA.
Mossel, D.A.A. 1988. Impact of foodborne pathogens on today's world, and prospects for management. Animal and Human Health. Vol. 1 (1):13-23/
Murray, P.R., Baron, E.J., Pfaller, M.A., Tenover, F.C., and Yolken, R.H., 1995. Manual of Clinical Microbiology. 6th edition. American Society for Microbiology,
Washington, D.C.
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4a-44
source of the original viral cells are causes for placement in
this category.
GROUPING PATHOGENS
BY SEVERITY OF THE HAZARD
PSP (paralytic shellfish poisoning) intoxication frequently
results in respiratory failure and death. Ciguatera toxins
which accumulate in fish flesh cause gastrointestinal and
neurological symptoms with disabilities lasting several days to
many months, even years.
Severe Hazard
• The organism is critical in determining the safety
of the food. Illness is sometimes fatal.
Moderate Hazard, Special Risk
• The organism is widely distributed in nature.
• There is likely to be a secondary spread from an
infected person. Illness is not fatal.
Moderate Hazards
Considering the etiological, clinical, and epidemiological
manifestations of the organisms, moderately hazardous
pathogens may be subdivided into those that present special
epidemiological risks and those that do not. The first group is
termed moderate hazard with potentially extensive spread.
The others are listed as moderate hazards with limited spread.
Moderate Hazard, No Special Risk
• The organism is widely distributed in nature.
Secondary transmission is unlikely. Illness is not
fatal.
1314
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Grouping Pathogens by Severity of the
Hazard
Grouping Microorganisms
Pathogens can be grouped into three categories according to
the severity of the hazard each presents. Although there are
many diseases caused by microorganisms, only a couple dozen
are transmitted by foods. Each year the Centers for Disease
Control (CDC) reports investigations of disease outbreaks
directly related to food. There are about 15 organisms
implicated in these various outbreaks. The severity of each
case and the frequency of outbreaks related to each organism
varies. The grouping outlined here parallels that of the
International Commission on Microbiological Specifications
for Foods (ICMSF) and agrees generally with the program
outlined by the Subcommittee on Microbiological Criteria for
Foods and Food Ingredients of the National Research Council
(NRC).
Severe Hazards
Certain organisms are critical in determining the safety of
foods. Some bacteria are very virulent and not only survive
and multiply in humans but seriously damage health and
threaten life. Those regarded as severe hazards include:







Clostridium botulinum
Listeria monocytogenes
Vibrio cholerae
Salmonella typhi and Salmonella paratyphi
Hepatitis A virus
Fish and shellfish toxins including ciguatera and paralytic
shellfish poisoning (PSP)
Enterohemorrhagic Escherichia coli
Botulism frequently results in death. Cholera may be fatal.
Mild cholera infections do occur and often are not even
recognized as being a foodborne illness. Although most
Salmonella spp. cause only gastroenteritis, the severity of
typhoid and paratyphoid fevers, the need for prolonged
medical care, and the low infective dose cause these species to
labeled as severe hazards.
Likewise, hepatitis A viral infections may range from
asymptomatic to acute liver disease. The severe debilitation
and death which may result plus the difficulty in tracing the
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4a-45
Moderate hazards with potentially extensive spread.
Salmonella, pathogenic Escherichia coli, Streptococcus
pyogenes, and Vibrio parahaemolyticus are classified in this
category. All are hazardous, widely distributed, but resultant
illnesses are usually not fatal. They are initially spread by
specific foods but there may be secondary spread due
environmental contamination and cross-contamination within
processing plants and food preparation areas. The illness dose
may be low, depending on strain and nutritional and health
status of affected individuals.
Moderate hazards with limited spread. Organisms that do
not present special epidemiological risks include: Bacillus
cereus, Clostridium perfringens, Yersinia enterocolitica,
Campylobacter jejuni, Trichinella spiralis, Staphylococcus
aureus and histamine from scombroid and other fishes. These
infection- or toxin-producing microorganisms are usually
found in small numbers in many foods. Generally, illnesses
are only caused when there are large numbers of the pathogens
or when enough time elapses to produce sufficient toxin to
cause illness. Outbreaks are usually restricted to consumers of
a particular meal or a particular kind of food.
Clear delineation between pathogens in these two moderate
hazard categories does not exist. The full importance of
Yersinia, Campylobacter, and Vibrio parahaemolyticus are yet
to be determined. All are being seen more frequently. The
risk of secondary spread is not known.
Primary pathogens, those most frequently seen and those
commonly endured without report, are not significantly
hazardous. The hazard will depend on the health of the
consumer.
Foodservice units in hospitals and extended care units should
avoid contamination at all levels. Food obtained and prepared
for most households, restaurants, and other commercial food
dispensing units usually is expected to contain contamination
by organisms in the moderate hazard category.
Summary
Table 4-9 shows infection and toxin-producing organisms,
grouped by hazards.
Table 4-9
Infection and Toxin-Producing Organisms, Grouped by
Hazards*
Severe Hazards – Death, severe debilitation, respiratory
failure, or neurological disability often result.
Clostridium botulinum
Salmonella cholerae-suis
Vibrio cholerae
Listeria monocytogenes
Vibrio vulnificus
Shigella spp.
Salmonella typhi
Brucella abortus
Salmonella paratyphi A, B, C Brucella melitensis
Mycobacterium bovis
Brucella suis
Hepatitis A virus
Enterohemorrhagic Escherichia coli (E. coli O157:H7)
Fish and shellfish toxins (Ciguatera, Paralytic shellfish
poisoning)
Mycotoxins (Possibly cancer inducing)
Moderate Hazards with Extensive Spread - Illness is
serious, but not usually fatal. Secondary spread through
processing is quite likely.
Salmonella spp.
Streptococcus pyogenes
Pathogenic Escherichia coli
Moderate Hazards with Limited Spread - Much milder
illness results. Illness usually only occurs when foods contain
large numbers of pathogens, or when toxins have been
produced in foods by large numbers of pathogens.
Staphylococcus aureus
Clostridium perfringens
Bacillus cereus
Yersinia enterocolitica
Histamine poisoning
Trichinella spiralis
Campylobacter jejuni
Vibrio parahaemolyticus
Coxiella burnetii
* Adapted from NRC 1985. An Evaluation of the Role of
Microbiological Criteria for Foods and Food Ingredients.
pp. 77-78. National Academy Press, Washington, D.C.
References:
International Commission on Microbiological Specifications
for Foods. International Association of Microbiological
Societies. 1986. Microorganisms in Foods. 2.
Sampling for Microbiological Analysis: Principles and
Specific Applications. 2nd edition. University of
Toronto Press, Toronto, Ontario, Canada.
National Research Council. Food Protection Committee.
Subcommittee on Microbiological Criteria. 1985. An
Evaluation of the Role of Microbiological Criteria for
Foods and Food Ingredients. National Academy Press,
Washington, D.C.
Wekell, M.M. 1986. Seafood poisoning. Presented to
International Association of Milk, Food and
Environmental Sanitarians, Inc. 73rd Annual Meeting,
Minneapolis, MN.
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4a-46
For example, inadequately processed eggs were used to make
ice cream. Over 14 outbreaks of salmonellosis (9,000 cases)
occurred in 4 eastern states within a period of 13 days. The
vehicle of transmission was the contaminated ice cream.
CHARACTERISTICS OF SALMONELLA
•
•
•
Grows with or without air
•
Source is infected animals, birds,
reptiles, and people
•
Common contaminant of raw foods of animal origin
(poultry, eggs, beef, pork)
•
•
•
Vegetative cells multiply in intestinal tract to cause illness
Survives freezing temperatures
The ecological habitat of Salmonella is the intestinal tract of
both warm- and cold-blooded animals. Salmonellae can
develop a resistance to antibiotics in the animal or human host.
The organism exists throughout the world and spreads through
fecal contamination of food, usually during slaughtering. The
food at this stage is not yet adequately pasteurized. One
laboratory-confirmed outbreak of foodborne salmonellosis
involved 57 people who, after eating beef, developed acute
gastroenteritis. One person died. Salmonella organisms were
isolated from the meat and from organs of the person who
died.
Grows between 41 and 115ºF,
in or on most foods
Infective dose = 10 to >10,000 cells in a portion of food
Vegetative cells killed by pasteurization
803
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1901(4a&b)
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Salmonella spp. – Characteristics
Bacterial Characteristics
Salmonella spp. are gram negative, facultative aerobic rods
that ferment glucose to form gas, and do not form spores.
There are over 2,000 serotypes of Salmonella. All species and
strains are pathogenic to humans.
Sources
Salmonella spp. are found in the intestinal tract of infected
animals and people. They have been isolated from many
species of animals such as chickens, ducks, turkeys, cows,
swine, turtles, cats, dogs, hamsters, doves, pigeons, parrots,
sheep, seals, donkeys and others.
A variety of raw and processed foods have been found to carry
Salmonella. Raw meat and poultry, shellfish, grade A shell
eggs, cracked shell eggs, and eggs removed from the shell;
processed meat, poultry, and egg products; dried milk; and
cheese made from unpasteurized milk have been major
sources. Some other foods that have been incriminated
occasionally are dried coconut, dried cereal, smoked fish,
spices, nuts, vegetable gum, and others.
The list of prepared menu items frequently implicated is
headed by protein menu items such as meat and poultry;
mixtures containing meat, poultry, eggs and seafood; dressings
and gravy; salads made with meat, poultry, egg, and seafood;
puddings, cream-filled pastries, custards, cream-filled cakes,
meringue pies; and many others.
The appearance, odor, and flavor of food items containing
hazardous levels of Salmonella are usually not noticeably
altered.
Potential or actual problems that influence transmission of
Salmonella emerge when new kinds of foods are processed by
customary or new methods, or when traditional foods are
processed by modified or new methods. These problems are
intensified when these products are marketed in increased
quantity. Some examples of foods that have led to outbreaks
of salmonellosis are cake mixes containing unpasteurized
dried eggs, turkey rolls, roast beef cooked in meat processing
plants, instantized dry milk, and food supplements containing
yeast and cottonseed protein.
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People are the only source of Salmonella typhi, which causes
typhoid fever. Food handlers with no symptoms who are
carriers of this disease can spread this pathogen by
contaminating foods and beverages they touch. In 1908, a
classic example of an asymptomatic carrier, Typhoid Mary
from Brooklyn, New York, was reported. Water contaminated
with raw sewage is also a source of Salmonella typhi.
Salmonellosis is one of the most important food-transmitted
illnesses in the country. More outbreaks occur in the summer
and autumn than in other seasons of the year. The incidence
of salmonellosis has risen more than 20-fold since 1946. One
reason may lie in the expansion of centralized processing and
bulk distribution of processed food items. An example is an
outbreak of salmonellosis from eating contaminated shrimp,
involving 9,000 persons attending 190 parties, all served by a
single catering service. Raw shrimp had been purchased at
one unsanitary outlet and was then transported to another
place for boiling. The boiled shrimp, still warm, were
returned to the containers in which the raw shrimp had arrived.
They were then transported in an unrefrigerated truck to the
places of service and finally were served. By then, 7 or 8
hours had elapsed. Obviously, the cooked shrimp were
recontaminated when they were placed in the containers in
which the raw shrimp had been packed and the Salmonella
had multiplied to an infective dose level. This incident
emphasizes the critical control procedure of never placing
cooked, pasteurized food back into a container that has been
used for raw food, unless that container has been washed and
sanitized.
Multiplication (Growth)* in Foods
Salmonella spp. have simple nutritional requirements, and will
grow in media containing only salt and glucose. Salmonella
require only simple sugars and inorganic nitrogen to grow.
The rate of growth is greater, however, in foods that contain
many nutrients.
Salmonella spp. do not compete effectively with many of the
naturally occurring food spoilage microorganisms in food and
high spoilage plate counts are a safety factor.
* Note: The words "multiply" and multiplication" will
frequently be replaced by "grow" and "growth," since
they are often used interchangeably.
Salmonella grows in the presence or absence of air. The
temperature range for growth is reported to be 41 to 115F (5
to 41C). It can survive in frozen food at freezing
temperatures. It grows well on or in food with a neutral pH.
Optimal pH for growth is near 7.0 (6.6 to 7.5 depending on the
medium). There is no growth below 4.1 (except in the special
case of Salmonella newport, which may grow in apple juice
and cider at pH 3.68). In most operating situations a pH
below 4.05 will not support growth. An aw below 0.945 also
prevents growth unless the medium is very rich in nutrients.
Symptoms
Vegetative cells cause illness by multiplying in the small
intestine. Because it is an infection, the presence of only a
few cells can cause illness. There are approximately 3 million
cases of salmonellosis in the U.S. each year, which may result
in as many as 2,000 deaths per year.
Symptoms such as abdominal cramps, diarrhea, fever, and
vomiting develop in 8 to 72 hours, usually between 20 and 48
hours. Persons most susceptible to Salmonella include the
elderly, children under age 5, people recovering from a severe
bout with the flu or otherwise physically weakened, and
people who have been ingesting antibiotics for any length of
time. An outbreak in April 1985 of milk-borne salmonellosis
in Illinois illustrated this problem; the fatalities were children.
The gastroenteritis syndrome presents a wide range of signs
and symptoms. Stools may be few but watery. There may be
bloody, mucoid diarrhea and tenesmus. Massive diarrhea with
dehydration, convulsions, and death can result. Abdominal
cramps, nausea, and vomiting are common for approximately
24 hours. Headache and chills are possible but any fever is
usually mild [below 100°F (37.8°C)]. Typically the symptoms
subside in 2 to 5 days. However, chronic arthritic symptoms
may follow 3 to 4 weeks after onset of acute symptoms.
During the acute phase of diarrhea, 106 to 109 Salmonella per
gram of feces may be excreted. If 0.01 g of the feces remains
on the fingertips after using the toilet, the fingertips could
contain 107 Salmonella. This number is more than enough to
cause a foodborne illness. Organisms may continue to be
excreted for 2 to 3 months. In general, carriers are over 30,
female, and have had typhoid. Contamination of food by a
carrier is extremely likely. Salmonella from an ill person or a
carrier may remain on the carrier's hands after poor hand
washing. Even as few as 100 cells on a foodservice worker's
hands can seriously contaminate a wet food such as lettuce if
hand washing is not thorough. This can eventually lead to
foodborne illness, especially in an immune-compromised
individual.
Infective Dose
The dosage required to cause illness and the type of illness
varies with the invading species and serotype. D'Aoast (1985)
in his review article states that a single Salmonella bacterium
can be infective. This statement followed the report of
incidents in which fewer than 50 cells of S. napoli or fewer
than 100 cells of S. eastborne in chocolate bars, and of 100 to
500 cells of S. heidelberg or 1 to 6 cells of S. typhimurium in
cheddar cheese caused illness. The FDA HACCP manual
(1993) states that the infective dose is few as 15 to 20 cells.
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4a-48
In the spring and summer of 1989, the Minnesota Department
of Health reported that 4.7 cells S. javiana per 100 grams of
mozzarella, string, or processed cheese contained sufficient
numbers to cause illness. It appears that the fat content in
these foods coats the surface of the microorganisms and
enables them to survive passage through the acidity of the
stomach (pH 2.0). The salmonellae are then able to multiply
in the intestinal tract and cause illness.
In human volunteer studies, 1.25 x 10 5 S. bareilly produced
illness in one volunteer and as many as 1010 S. pullorum were
required to produce illness in other volunteers. The larger the
dose of Salmonella spp., the more obvious the signs and
severe the symptoms. A high number (105 or more) typically
occurs in foodborne salmonellosis because Salmonella spp.
multiply and reach these numbers in contaminated foods
during periods of improper food handling.
Doses of S. typhi required to cause illness in human adults
have also been investigated. When 1,000 cells were ingested,
no illness resulted. When a group of 116 volunteers each
ingested 105 cells, 28% of the volunteers became ill. The
median incubation period of the disease for those who
ingested 105 cells was 9 days; for those who ingested 109 cells,
3 days. Salmonella typhi was recovered from the stools of the
infected volunteers for periods ranging from 1 to 34 days
(mean, 11 days) after digestion.
A chiffonade-type dessert, which was a vehicle for a large
outbreak of salmonellosis, contained 113 Salmonella per 75gram serving. Interestingly, the initial level in the product
when freshly prepared was more than 10,000 per 75-gram
serving. Freezer storage at -4°F (-20°C) for 1 month caused a
2-log reduction in the initial Salmonella population
(Armstrong et al., 1970).
The outcome of the infection that follows ingestion of viable
Salmonella is determined by the virulence or invasiveness of
the serotype and strain; the number of cells ingested; and host
resistance factors such as age, nature of the alimentary tract,
and state of health. Most Salmonella produce an enteric
infection manifested by diarrhea, but some serotypes such as
S. typhi, S. paratyphi A, B, and C, and S. cholerae-suis, tend
to produce bacteremia (presence of viable microorganisms in
the blood) which leads to septicemia.
All age groups are susceptible, but symptoms are most severe
in the elderly, infants and the infirm. AIDS patients suffer
salmonellosis frequently (estimated 20-fold more than the
general population) and suffer recurrent episodes.
Incidence
It is estimated that there is an annual incidence of about 1.3
million cases of salmonellosis in the United States which may
result in as many as 15,000 hospitalizations and 550 deaths per
year (Mead et al., 1999).
Food Analysis
Conventional culture methods require 5 days for presumptive
results. However, several rapid methods of analysis have been
developed which require 2 days or less.
Epidemic Salmonella enteritidis Due to Eggs
Epidemics of salmonellosis caused by Salmonella enteritidis
in Europe and the United States in the late 1980s and early
1990s were traced to hen's eggs. It was determined that S.
enteritidis is transferred from the infected ovaries of laying
hens to the egg yolk before the shells are formed.
Consequently, intact Grade A eggs have been the source of
this bacterial infection. In 1988, whole flocks of chickens and
crates of eggs were destroyed in England. In 1988 that over
2,000 people on the Northeast coast of the United States
became ill and 11 of them died due to consumption of S.
enteritidis contaminated eggs.
In October 1989, 11 outbreaks of Salmonella enteritidis in
Pennsylvania involved over 300 cases. In one nursing home
incident, 6 elderly patients died as a result of the illness.
Another episode was reported about a man in his 40s who was
reported to be in good health before consuming pie that had
been highly contaminated with S. enteritidis. He became very
ill and died a few days later. Several kinds of pies (cream,
custard, meringue) all with shell egg ingredients were baked in
a restaurant bakery and stored for 2 1/2 hours in a walk-in
cooler. The pies were then picked up and carried in the trunk
of a car to the site of a company party where they were
consumed 3 to 6 hours later. Leftover pie was consumed that
evening and the following day after having been kept
unrefrigerated for as long as 21 hours. All together 14 people
became ill because of this incident and several were
hospitalized. The man who died delayed seeking medical
treatment for his illness, and his cause of death was listed as
being due to extreme dehydration as a result of Salmonella
enteritidis gastroenteritis. This incident illustrates poor
storage practices that allowed the population of
microorganisms to grow to a level that produced severe illness
in otherwise healthy individuals.
Illness incidents due to S. enteritidis emphasize the importance
of: (1) not eating raw or undercooked eggs [especially young
children, the elderly, and immune-compromised persons], (2)
using pasteurized egg products (liquid or in-shell) in hospitals,
nursing homes, foodservice establishments, day care centers,
elementary schools, and commercial kitchens, (3) storing eggs
at 41°F (5°C) or less, and (4) cooking shell eggs until all parts
of the egg reach a temperature of 145°F (63°C) for 15
seconds. Casseroles and other dishes containing eggs should
be cooked to 160°F (71°C).
Culture-confirmed cases of Salmonella enteritidis in the U.S.
peaked in 1989 and the numbers of people affected with this
illness since that time has been declining. The U.S.
Department of Agriculture published regulations in February
of 1990 establishing a mandatory testing program for eggproducing breeder flocks. This type of testing, along with
other measures, has lead to a reduction in the number of cases
of salmonellosis caused by the consumption of Grade A whole
shell eggs.
OUTBREAK EXAMPLE I. MMWR 2000. 49 (4): 73-79.
Salmonella enteritidis Girl Scouts, Los Angeles County,
California. In August 1997, the Los Angeles County
Department of Health Services (LACDHS) received reports of
gastrointestinal illness in members of a Girl Scout troop and
some of their parents. The ill persons had eaten food prepared
in a private residence by the scouts. Stool cultures were taken
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4a-49
from 12 ill persons yielded Salmonella enteritidis. Stool
cultures taken from 12 ill persons yielded S. enteritidis.
An investigation by the health department found that of 17
persons at the dinner, 13 had gastrointestinal illness consistent
with salmonellosis. Cheesecake served at the dinner was
associated with illness; all 13 ill persons and two well persons
ate the cheesecake. The cheese cake contained raw egg whites
and egg yolks that were cooked in a double boiler until
slightly thickened. The California Department of Health
Services and the Department of Food and Agriculture
investigated the farm that supplied the eggs and found S.
enteritidis contamination. Of 476 environmental cultures
taken from manure, feed, and water, 21 yielded S. enteritidis.
All positive cultures were from manure. S. enteritidis was
also isolated from one of 200 pooled egg samples obtained at
the farm. On the basis of these findings, the layer flack was
depopulated to prevent further S. enteritidis cases.
This outbreak illustrates transmission of S. enteritidis to eggs
from a diseased flock of laying hens. It also illustrates the
consequences of consuming raw eggs or undercooked eggs.
OUTBREAK EXAMPLE II. MMWR 1999 48 (27): 582-585.
Outbreak of Salmonella Serotype Muenchen Infections
Associated with Unpasteurized Orange Juice -- United
State and Canada, June 1999. During June 1999, health
departments in Oregon and Washington investigated clusters
of diarrheal illness attributed to Salmonella Serotype
Muenchen infections in each state. Both clusters were
associated with a commercially distributed unpasteurized
orange juice traced to a single processor, which distributes
widely in the United States. By July 13 of 1999 there were
207 confirmed cases associated with this outbreak having been
reported from 15 states and two Canadian provinces. An
additional 91 cases were being investigated.
In a case control study in Seattle, Washington of nine ill and
29 well restaurant A patrons, illness was significantly
associated with drinking smoothies containing orange juice.
Further collection of epidemiological data in the State of
Washington of 85 persons with illness indicated that sixtyseven (67) patients reported drinking unpasteurized orange
juice produced by a company in Tempe, Arizona, or eating at
an establishment where the juice was served. The
predominant symptoms reported were diarrhea (94%), fever
(75%), and bloody diarrhea (43%). Ten (10%) of the patients
were hospitalized. No patients died.
On the basis of epidemiologic information from investigations
of health departments from the states of Washington and
Oregon, and the Food and Drug Administration (FDA), the
company producing the orange juice issued a recall. The
unpasteurized orange juice was distributed in Arizona,
California, Colorado, Nevada, New Mexico, Oregon, Texas,
Utah, Washington, Wisconsin, and the Canadian provinces of
Alberta and British Columbia under 7 different brand names.
The juice was distributed to hotels, restaurants, and
supermarkets, and was served in individual glasses as "fresh
squeezed" juice in hotels and restaurants. In addition, a frozen
form of the unpasteurized juice was sold for use in restaurants
and institutions.
Samples of juice from a previously unopened container of
suspect orange juice analyzed by an FDA laboratory and a
Washington State Public Health laboratory yielded S.
Muenchen. Isolates from a smoothie blender and juice
dispenser at a restaurant yielded Salmonella serogroup C2.
Juice samples obtained from the juice processing facility
yielded S. Hildalgo, S. Javianna, S. Gaminara, and S. Alamo,
in addition to S. Muenchen.
Center for Disease Control. 1999. Outbreak of Salmonella
serotype Muenchen infections associated with
unpasteurized orange juice -- United States and Canada,
June 1999. MMWR 48 (27):582-585.
Center for Disease Control. 2000. Outbreaks of Salmonella
serotype enteritidis infection associated with eating raw
or undercooked shell eggs. United States, 1996-1998.
MMWR 49 (4): 73-79.
D'Aoust, J.Y. 1985. Infective Dose of Salmonella
typhimurium in cheddar cheese. Am. J. Epidemiol. 122
(4) 717-720.
FDA. 1998: Food labeling: warning and notice statement;
labeling of juice products; proposed rules. Federal
Register 63: 20449-86.
Goverd, K.A., Beech, F.W., Hobbs, R.P., and Shannon, R.
1979. The occurrence and survival of coliforms and
salmonellas in apple juice and cider. J. Appl. Bacteriol.,
46: 521-530.
International Commission on Microbiological Specifications
for Foods. 1996. Microorganisms in Foods. Chap. 14
Salmonellae pp. 217-264.
Mead, P. S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee,
J.S., Shapiro, C., Griffin, P. M., and Tauxe, R. V. 1999.
Food-related illness and death in the United States.
Emerg. Inf. Dis. 5 (5): 606-625.
Shapiro, R, Ackers, M., Lance, S, Rabbani, M., Schaefer, L.,
Daughter, J.,Thelen, C., and Swerdlow, D. 1999.
Salmonella Thompson associated with improper
handling of roast beef at a restaurant in Sioux Falls,
South Dakota. J. Food Prot. 62 (2): 118-122.
The FDA published a final rule for the labeling of fruit and
vegetable juices that includes a warning statement to advise
consumers of the risks associated with drinking unprocessed
juices. However the labeling requirements do not apply to
juice or products containing juice that are not packaged (i.e.,
sold by the glass) in retail establishments. In Washington,
some consumers were unaware that they were drinking
unpasteurized commercial orange juice in their fruit
smoothies.
OUTBREAK EXAMPLE III. J. Food Prot. 1999 62 (2): 118122.
Salmonella Thompson associated with improper handling
of roast beef at a restaurant in Sioux Falls, South Dakota.
In October 1996, an outbreak of 52 Salmonella serotype
Thompson infections were associated with a restaurant in
Sioux Falls, South Dakota. The infections were identified
among employees and patrons at the restaurant and at three
luncheons catered by the restaurant. Epidemiologic
investigation documented that the outbreak was caused
primarily by roast beef.
Several facts suggest that a single contaminated roast beef
could explain all the Salmonella Thompson infections among
the restaurant patrons and among those who attended the
catered luncheons the following week. First, three patients
became ill after consuming contaminated roast beef served at
brunch on September 29. Leftover roast beef was probably
used on Greek salads served on October 5 and then again on
October 7.
Salmonella can be cultured from 1 to 5% of raw beef and
Salmonella Thompson is among commonly isolated serotypes
from bovine sources. An inadequate internal cooking
temperature might have allowed the contaminating organisms
to survive. Puncturing raw meat with a temperature gage or a
knife could have also caused internal contamination that might
have survived the cooking process. Subsequently, inadequate
refrigeration temperature could have allowed Salmonella to
multiply. (The walk-in refrigerator had a temperature of
50F).
This outbreak was probably preventable. The roast beef
should have been cooked to temperatures and times that are
sufficient to achieve a 5-log kill of Salmonella. The cooked
roast beef should have been cooled properly and stored at
refrigeration temperatures below 41F.
References:
Armstrong, R.W., Fodor, T., Curlin, G.T., Cohen, A.B.,
Morris, G.K., Martin, W.T., and Feldman, J. 1970.
Epidemic Salmonella gastroenteritis due to contaminated
imitation ice cream. Am. J. Edpidemiol. 91(3): 300-307.
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4a-50
Recent processing methods have been developed for
pasteurizing shell eggs, which assure the destruction of
Salmoella enteritidis in the intact egg (Hou et al., 1996). Only
pasteurized egg products should be used to prepare eggs and
egg products for people at risk (e.g., rest homes and hospitals).
SALMONELLA HACCP
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18
Salmonella spp. – Process Hazard Analysis
The Animal Source
Animals become infected with Salmonella by consuming
contaminated feed and by environmental contact when they lie
in fecal material. Rodents and birds defecate on animal and
poultry feed and can be an initial source of Salmonella.
Salmonella HACCP, then, really begins with the feed. Ideally,
animal feed should be pasteurized so that the animals will not
be infected. However, the cost of this process with no
apparent return on investments has meant minimal and only
academic interest by feed manufacturers.
Animals spread infection to other animals while in transit or in
pens. In fact, during transit when the animals are in stress,
Salmonella can increase 10- to 100-fold in the animals'
intestines. Chickens and turkeys that are infected with
Salmonella bring these organisms into poultry processing
plants. A contaminated carcass or fecal material then
contaminates equipment and/or workers' hands. Salmonella
can be transferred from equipment surfaces and workers'
hands to other carcasses or to processed foods. As plants
process even greater volumes of animals and poultry, the
likelihood becomes greater that an infected carcass will crosscontaminate other finished products. Once introduced into a
plant, Salmonella can survive on equipment or in the plant
environment, and can subsequently contaminate other
products until adequate cleaning and sanitizing measures
(normally, only every 4 hours) are applied.
Salmonella enteritidis has been found to be present within the
yolks of intact Grade A shell eggs. Laying hens infected with
S. enteritidis can transmit the microorganism to the yolk
before the shell of the egg is formed in the ovaries. The U.S.
government standards now recommend that shell eggs be kept
below 45°F (7.2°C). If contaminated Grade A shell eggs are
held at 60° (15.6°C) for 2 weeks, they can become very
hazardous.
In order to control this problem, flocks of chickens must be
raised under conditions which prevent S. enteritidis infection
and hence can be certified Salmonella-free.
Foods prepared by delicatessens and retail markets (e.g.,
salads, sandwiches, roast meats, barbecued poultry) may
become cross-contaminated from knives and cutting boards
with Salmonella from raw food products. Inadequate cooking,
cross-contamination, and storage in warmers at hazardous
temperatures of 80 to 114°F (26.7 to 45.6°C) that allow rapid
growth of Salmonella spp. for more than 2 hours have led to
outbreaks of salmonellosis.
Foods prepared in foodservice establishments are sometimes
prepared a day or more before serving. This practice is labor
efficient, but it decreases the food's quality and safety. If the
food is allowed to be in the temperature range of 80 to 114°F
(26.7 to 45.6°C) for more than an hour, a hazard that permits
the rapid multiplication of Salmonella spp. will develop.
Improper sanitation practices, inadequate cooling and
reheating, and unsafe cooking practices aggravate these
problems.
Salmonella spp. enters foodservice establishments on raw
animal products or in the feces and on the fingers of infected
employees. Salmonella spp. grow when foods are mishandled,
undercooked, or recontaminated after cooking and then
allowed to remain at dangerous temperatures.
Importance of Hand Washing
Persons with Salmonella on their fingers from fecal
contamination can spread these bacterial cells onto salads or
cold garnishes and cause illness. Salmonella can be isolated
from fingertips 3 hours after contamination with 500 to 2,000
cells. One study showed that ham and corned beef became
contaminated after being touched by persons whose hands had
just 100 cells 15 minutes earlier, and had not been washed
adequately. The study shows the potential for crosscontamination and emphasizes the need for vigorous hand
washing using hand soap/detergent and flowing warm water
after touching items that might be contaminated with
Salmonella.
Food Distribution Problems
With modern food distribution systems, widespread disease
outbreaks can result before any attempt to recall a
contaminated lot of food can be made. Contamination that
results from an error in storage of a food that is later
distributed can result in human illness thousands of miles from
The FDA Food Code recommends cooking shell eggs until a
temperature of 145°F (63°C) for 15 seconds is reached
throughout the egg.
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Means of Contamination
The transmission of Salmonella and the occurrence of
outbreaks are influenced by food processing, food distribution,
and foodservice operations. Animal feeds contain rendered
animal by-products that are often contaminated with
Salmonella. This feed then contaminates the intestine of
animals that eat it. When the animal is slaughtered, there is a
high risk of contamination of raw meat. Salmonella can also
survive in litter, soil, animal feces, trough water, and other
substances in a farm environment. Operations where large
numbers of animals are kept in confined areas contribute to
the problem of animal-to-animal transmission.
4a-51
the contamination source and months after the contamination
occurred.
References:
Hou, H., Singh, R.K., Muriana, P.M., and Stadelman, W.J.
1996. Pasteurization of intact shell eggs. Food
Microbiology. 13: 93-101.
International Commission on Microbiological Specifications
for Foods. 1996. Microorganisms in Foods. Chap. 14
Salmonellae pp. 217-264.
Mossel, D.A.A., Corry, J. E. L., Struijk, C. B., and Baird, R.
M. 1995. Essentials of the Microbiology of Foods.
John Wiley & Sons. New York, NY.
Tauxe, R.V. 1991. Salmonella: a postmodern pathogen. J.
Food Prot. 54: 563-568.
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4a-52
freezing and freezer storage. The strains, which have a
tendency to be more susceptible to the cold and dry
environment, are also low-incidence strains. The ability of
certain serotypes to survive may be a factor in their higher
incidence of causing salmonellosis.
SALMONELLA CONTROL -- TEMPERATURE
Heat Resistance
The cells are not heat resistant and at 120°F (48.9°C) they are
inactivated very slowly. Neither spores nor toxins are formed,
so heating food to a center temperature of 165°F (73.9°C) for
3 minutes will reduce any population of Salmonella at a high
water activity to an undetectable level.
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Salmonella spp. – Process Critical Controls
Salmonella Control
The rate of growth of Salmonella is dependent on temperature,
pH, salinity, water activity (aw), and nutrient content of the
surrounding medium. By manipulating any one or a
combination of these factors, the growth of these bacteria in
food can be controlled.
Generation Time
Although some strains of salmonellae may grow at lower
temperatures, it is generally accepted that the growth of most
Salmonella spp is between 41 and 115°F (5 and 46°C).
Table 4-10
Predicted Average Generation Times for Salmonella in
Foods*
Time
little or no growth
23.0 hours
11.5 hours
4.5 hours
2.5 hours
1.5 hours
1.0 hours
50.0 minutes
45.0 minutes
no growth
Temperature
°F (°C)
Chicken a la king
(min.)
Custard
(min.)
130 (54.4)
135 (57.2)
140 (60)
145 (62.8)
150 (65.5)
36
10.5
3.0
0.9
0.3
100
44
19
8.1
3.5
*Adapted from data of Angeloti et al. (1961).
Growth in ideal conditions without competition from other
organisms can begin with cross-contamination from
Salmonella spp. on a cutting board that was used to cut raw
chicken. If cooked meat or hard cooked eggs are subsequently
cut on that board, these products will become contaminated.
When the contaminated meat and eggs are used to prepare a
salad or sandwiches, the population can be large enough to
cause a foodborne illness.
* Adapted from data of Snyder, O.P. (1998).
For example, four (4) hours at 100°F (37.8°C) with a
generation time of 45 minutes allows Salmonella to multiply
about 5 times. If there were 10 Salmonella in a portion of
food at time zero, there will be approximately 320, 4 hours
later. This is a hazardous level for a few people. If the same
food is held at 60°F (15.6°C) (with 4.5-hour generation times)
for 12 hours, there will be a 3-generation increase in
salmonellae which is a very low risk. The upper temperature
limit for growth is approximately 114°F (45.6°C) (Angelotti et
al., 1961). Salmonella spp. have been shown to survive
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Tables 4-11 and 4-12 indicate the times necessary to cause a
107 Salmonella reduction in chicken ala king, custard, and
beef roasts. Products such as dried egg powder, chocolate
candy, and custards because of their lower water activity,
require temperatures at least 10°F (5.5°C) higher or times that
are 10 times longer at a specified temperature in order to
destroy Salmonella.
Table 4-11
Time Required for a 107 Destruction of Salmonella
manhattan in Chicken a la King and Custard*
Table 4-10 lists predicted average generation times (times
necessary for doubling of Salmonella in foods).
Temperature
°F (°C)
41 (5)
45 (7.2)
50 (10)
60 (15.6)
70 (21.1)
80 (26.7)
90 (32.2)
95 (35)
100 (37.8)
115 (46.1)
Heat processes have been designed to destroy Salmonella in
various products. Pasteurization of eggs is an example.
Regulations differ among countries and for each egg product,
but they usually require heating liquid eggs to a temperature of
140°F (60°C) or higher and holding them at these
temperatures for 2 to 4 minutes. Present standards for
pasteurization of milk are: 145°F (62.8°C) for 30 minutes or
161°F (71.7°C) for 15 seconds inactivate more than 1010
Salmonella per gram of milk.
4a-53
Precooked roast beef was a source of salmonellosis in many
states until the USDA instituted regulations in 1977. These
regulations required that raw beef be cooked to a uniform
temperature that provides a 107 reduction (see Table 4-12).
USDA guidelines now recommend a 106.5 reduction.. Since
these regulations/guidelines were adopted by food processors,
the number of outbreaks of salmonellosis due to contaminated
precooked beef has decreased.
Table 4-12
Time Required for a 107 Salmonella Serotypes in 10-lb. or
Larger Cuts of Beef* Compared with a 10 6.5 Destruction of
Salmonella**
Temperature
ºF (ºC)
130 (54.4)
135 (57.2)
140 (60)
144 (62.2)
150 (65.5)
160 (71.1)
Time, 107
121.1 min.
37.0 min.
12.1 min.
5
1.21 min
(72.6 sec.)
0.121 min.
(7.26 sec.)
Time, 106.5
112 min
11.2 min
1.1min.
(67 sec.)
0.11 min.
(6.7 sec.)
*Adapted from data of Goodfellow and Brown (1978).
** USDA FSIS. 2001.
Control
It is essential to prevent the multiplication of Salmonella spp.
in food products. It is even more critical to prevent the
presence of Salmonella spp. in foods that are high in fat.
These foods (e.g., cheese, chocolate) provide a protective
coating for the organism from the stomach acids. Therefore,
fewer organisms are needed to cause illness. After foods are
processed and prepared:



The FDA Food Code recommends cooling potentially
hazardous food to 41°F (5°C) within 6 hours [§3-501.14:
from 135 to 70°F (57.2 to 21°C) within 2 hours followed
by cooling to 41°F (5°C) or below within a total time of 6
hours]. USDA Guidelines recommend cooling food,
within 90 minutes after cooking, from 120 to 55°F within
6 hours, followed by further cooling to 40°F (no time
limit) before boxing.
Holding food at a temperature above 114°F (45.6°C)
exceeds the upper limit for Salmonella growth. [FDA
Food Code recommends holding hot foods above 135°F
(57.2°C)].
Post-process contamination of food must be prevented.
This can be achieved by:
1. Training personnel to use frequent and correct hand
washing and food handling practices.
2. Using sanitary food handling procedures that prevent
cross-contamination. This includes preparation of raw
foods, particularly meat and poultry in separate areas or
with separate sanitized equipment in order to prevent
transfer of this bacteria to cold or pre-cooked food
products that will receive no further heating.
3. Monitoring the environment, the product during
processing, and the finished product for Salmonella.
References:
Angelotti, R., Foter, M.J., and Lewis, K.H. 1961. Time
Temperature effects on Salmonella and Staphylococci in
foods. lll. Thermal death time studies. Appl. Microbiol.
9: 308-315.
Angelotti, R. 1977. Minimum cooking requirements for
cooked beef roasts. Fed. Reg. 42: 44217-44218.
1901-04: ch4a rev 2/25/05 print 3/7/16
4a-54
Bailey, J. S., and Maurer, J. J. 2001. Chapter 8. Salmonella
Species. In Food Microbiology. Fundamentals and
Frontiers. Doyle, M. P., Beuchat, L. R., and Montville,
T. J. eds. pp, 141-178. American Society of
Microbiology. Washington, D. C.
Goodfellow, S.J. and Brown, W.L. 1978. Fate of Salmonella
inoculated into beef for cooking. J. Food Prot. 41: 598605.
Mossel, D.A.A., Corry, J. E., Struijk, C. B., and Baird, R.
1995. Essentials of the Microbiology of Foods. John
Wiley and Sons, New York, NY.
Snyder, O. P. 1998. Updated guidelines for use of time and
temperature specifications for holding and storing food
in retail food operations. Dairy Food Environ. Sanit. 18
(9): 574-579.
USDA FSIS. 2001. Draft compliance guidelines for ready-toeat meat and poultry products.
http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/RTEGui
de.pdf.
minimum water activity (aw) for growth of C. jejuni in foods is
0.987
CHARACTERISTICS
OF CAMPYLOBACTER JEJUNI
Salt tolerance. At 107.6°F (42°C) C. jejuni will grow in
1.5% table salt (sodium chloride, NaCl) and 0.5% NaCl, but
not in 2% NaCl.
•
Grows best in small amount of air
(oxygen)
•
•
Grows between 86 and 113ºF
•
Source is infected animals, birds,
reptiles, and people
•
Common contaminant of raw foods of animal origin
(poultry, pork, raw milk)
•
•
•
Vegetative cells multiply in intestinal tract to cause illness
Survives chilling and freezing
temperatures
Survival. The organism does not grow in milk, but will
survive 22 days at refrigeration temperatures of 39.2°F (4°C).
If milk is held at 77°F (25°C), destruction of the
microorganism occurs within 3 days. C. jejuni can survive on
raw chicken held at -4°F (-20°C) for more than 64 days
(Oosterom et al., 1983).
Infective dose = 400 to 500 cells in a portion of food
Vegetative cells killed by cooking
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Campylobacter jejuni – Characteristics
Bacterial Characteristics
Campylobacter jejuni is a gram-negative, slender, curved to
spiral rod that is motile by means of a single polar flagellum.
It is relatively fragile and sensitive to environmental stresses
of more than 21% oxygen, drying, heating, sanitizers, and
acidic conditions. These bacteria can survive refrigeration and
freezing temperatures for a limited period of time.
Source
Campylobacter jejuni is now recognized as a common cause
of gastroenteritis in humans. It is commonly found as a
pathogen in cattle, sheep, fowl, swine, and rodents. Incidents
in which C. jejuni has been isolated as causing illness have
resulted from the consumption of raw milk, undercooked
poultry and pork. Campylobacter spp. can be spread by a
contaminated water supply, and is carried by common
household pets (particularly cats and dogs in poor health).
Symptoms
The symptoms of illness caused by C. jejuni
(Campylobacteriosis) are similar to those caused by other
enteric pathogens such as Salmonella spp., Shigella spp., and
Escherichia coli. Stool cultures are used to provide positive
identification.
Symptoms may be mild to quite severe and appear 2 to 5 days
after ingestion of contaminated food or water. In severe cases,
ingestion of C. jejuni produces severe, even bloody, diarrhea
with fever, nausea, and severe abdominal pain. Blood in
stools may continue for 2 to 3 days after the symptoms are
first observed.
Interestingly, children seem less seriously affected than adults
who may appear to have ulcerative colitis. The illness may
linger 1 to 2 weeks in all ages. Occasionally there may be a
relapse characterized by a recurrence of abdominal pain and
mild to severe gastroenteritis and bloody diarrhea which may
last for several weeks.
The presence of C. jejuni is high in fresh meat and may be as
high as 100% in fresh poultry. The numbers of CFU (colony
forming units) may vary from 10,000 CFU on a chicken wing
to less than 1 CFU/cm2 in raw pork and 1 to 10 CFU/cm2 in
raw beef (Genigeorgis, 1986).
Growth Conditions
Temperature. In 1981, Doyle et al. reported the temperature
range for growth of C. fetus subsp. jejuni as 90 to 113°F (32 to
45°C). The optimum range for growth seems to be 107.6 to
113°F (42 to 45°C). Doyle (1988) stated that C. jejuni will not
grow below 86°F (30°C).
Ordinary cooking, which destroys Salmonella spp., also
destroys Campylobacter spp. Doyle (1984) reported that
heating meat to 140°F (60°C) and holding it at this
temperature is sufficient to destroy any Campylobacter
present.
pH. The pH range for growth is 5.0 to 8.0.
Atmosphere. The organism is microaerophilic and requires
an atmosphere of reduced oxygen for growth. Optimal growth
conditions require 5 to 10% oxygen and 2 to 10% carbon
dioxide. Because of its sensitivity to air and the relatively high
temperature required for growth, growth of C. jejuni in foods
is unlikely under ordinary conditions of food handling. The
1901-04: ch4a rev 2/25/05 print 3/7/16
Infective Dose
A pathogenic dose is usually given as ranging from 10 6 to as
few as 400 to 500 organisms (Walker et al., 1986; FDA,
1993). Host susceptibility seems to dictate infectious dose.
The pathogenic mechanisms of C. jejuni are still not
completely understood. It does produce a heat-labile toxin
that may cause diarrhea. It may also be an invasive organism
(FDA, 1993).
4a-55
Complications of infection by C. jejuni may include
abdominal pain resulting in unnecessary appendectomies,
reactive arthritis, Reiter's syndrome, and Guillain-Barré
syndrome.
Incidence
Campylobacter jejuni is the most common bacterial cause of
diarrheal illness in the U.S. Mead et al. (1999), estimated an
annual incidence of 1,900,000 cases of Campylobacter illness
in the U.S. resulting in 10,500 hospitalizations and 100 deaths.
The annual incidence as estimated by the FDA (1993) is 2 to
4 million cases a year. Roberts and van Ravenswaay, 1989
estimated the annual cost of campylobacteriosis at about 1
billion dollars.
OUTBREAK EXAMPLE I. The following example appeared in
MMWR 35(19):311-312, 1986.
Campylobacter Associated with Raw Milk Provided on a
Dairy Tour - California. On October 3, 1985, students and
teachers from northern California and some of their family
members made a field trip to a San Joaquin County dairy. Of
the 50 attendees from whom information was available, 23
(46%) became ill with Campylobacter jejuni infection.
Twenty-three (59%) of the 39 attendees who drank raw milk,
and none of the 11 who did not drink it, became ill. Included
among the cases was an infant who had been almost
exclusively breast-fed and became ill after drinking a bottle
filled with raw milk at the dairy. In addition, secondary cases
occurred in 2 women who had not visited the dairy but who
tended an infant who drank raw milk and developed
Campylobacter gastroenteritis. Stool cultures from 1
asymptomatic and 8 ill persons grew C. jejuni.
Of the 23 ill field-trip attendants, 96% reported diarrhea; 35%,
abdominal cramps; 35%, fever; 26%, vomiting; and 22%,
bloody diarrhea. Incubation periods ranged from 1 day to 10
days, but were 3 or 4 days in most cases. Symptoms most
commonly lasted 5 days.
Numerous outbreaks of enteric diseases have occurred among
school children given raw milk while on field trips to dairies
in the United States. As a result, in January 1985, the U.S.
Food and Drug Administration (FDA) issued a "milk
advisory" to all state school officers recommending that
children not be permitted to sample raw milk on such visits.
Healthy lactating cows can carry C. jejuni in the intestinal
tract, providing an extrinsic source of contamination. Since
culture of diarrheal stools for C. jejuni became common, many
raw milk-associated Campylobacter outbreaks involving
thousands of cases have been reported.
Milk is an excellent vehicle for infection, because its fat
content protects pathogens from gastric acid and because,
being fluid, it has a relatively short gastric transit time.
Present technology cannot produce raw milk that can be
assured to be free of pathogens. Milk must be pasteurized to
insure the destruction of Campylobacter jejuni. In Scotland,
the incidence of illness due to C. jejuni has decreased
markedly since 1983 when the sale of raw milk was banned.
OUTBREAK EXAMPLE II. The following example appeared in
a Minnesota Department of Health 1998 Gastroenteritis
Outbreak Summary.
Campylobacteriosis Associated with Eating Lettuce in a
Restaurant. An investigation was taken of a foodborne
illness outbreak involving 152 people that occurred when
three separate groups of individuals developed gastrointestinal
illness days after eating at a restaurant in June 1998. All 152
cases reported diarrheal illness that lasted from 2 to 20 days.
One hundred-nineteen (78%) reported fever, 37 (24%)
reported vomiting, and 22 (14%) reported bloody stools. The
median incubation period was 52.5 hours. The median
duration of illness was 6 days. Forty-two (69%) of the 61
stool specimens tested positive for Campylobacter jejuni.
Salads and sandwiches containing lettuce were significantly
associated with illness. The investigation identified several
possible ways for the cross-contamination of raw chicken and
produce items in various preparation procedures. These
deficiencies included poor handling and storage of fresh
vegetables, raw meat, and poultry products.
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4a-56
References:
Adams, M. R. and Moss, M. O. 1995. Food Microbiology.
The Royal Society of Chemistry. Cambridge, U.K.
Altekruse, S.F., Stern, N.J., Fields, P. L., and Swerdlow, D. L.
1999. Campylobacter jejuni - An emerging foodborne
pathogen. Emerg. Infect. Dis. 5 (1):28-35.
Chin, J. ed. 2000. Control of Communicable Diseases in Man.
American Public Health Assoc., Washington, D.C.
Doyle, M.P. 1984 Campylobacter in foods. Chapt. 14 in
Campylobacter Infections in Man and Animals. Butzler,
J.P. ed. CRC Press, Boca Raton, FL.
Doyle, M.P. 1988. Campylobacter jejuni. Food Technol.
42(4): 187.
Doyle, M.P. and Roman, D.J. 1981 Growth and survival of
Campylobacter fetus subsp. jejuni as a function of
temperature and pH. J. Food Protect. 44(8): 596-601.
FDA, 1993. HACCP. Regulatory Food Applications in Retail
Food Establishments. Dept. of Health and Human
Services. Division of Human Resource Development,
HFC-60; Rockville, MD.
Mead, P. S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee,
J.S., Shapiro, C., Griffin, P. M., and Tauxe, R. V. 1999.
Food-related illness and death in the United States.
Emerg. Inf. Dis. 5 (5): 606-625.
Namchamkin, I. 2001. Campylobacter jejuni. In Food
Microbiology. Fundamentals and Frontiers, 2nd edition.
Doyle, M. P., Beuchat, L. R., and Montville, T. J. eds.
American Society of Microbiology. Washington, D. C.
pp.159-161.
National Advisory Committee on Microbiological Criteria for
Foods. 1995. Campylobacter jejuni/coli. Dairy, Food
and Environmental Sanitation 15 (3): 133-153.
Oosterom, J., DeWilde, G.J.A., DeBoer,E., DeBlaauw, L.H.,
and Karman, H. 1983. Survival of Campylobacter jejuni
during poultry processing and pig slaughtering. J. Food
Protect. 46(8): 702-706.
Roberts, T and van Ravenswaay, E. 1989. The economics of
safe guarding the U.S. Food Supply. USDA Ag. Info.
Bulletin No. 566: 1-6.
Stern, N. J. and Kazmi, S.U. 1989. Campylobacter jejuni. In
Foodborne Bacterial Pathogens. Doyle, M.P., ed.
Marcel Dekker, Inc., New York, NY.
Walker, R.I., Caldwell, M.B., Lee, E.C., Guerry, P., Trust,
T.J., and Ruiz-Palacios, G.M. 1986. Pathophysiology of
campylobacter enteritis. Microbiol. Rev. 50 81-94.
41°F (5°C) or below within a total time of 6 hours or
less.]
5. USDA Guidelines recommend continuously cooling
food, within 90 minutes after cooking, from 120 to 55°F
(48.9 to 12.8ºC) within 6 hours, followed by further
cooling to 40°F (4.4ºC) (no time limit) before boxing.
6. Avoid consumption of unpasteurized milk and dairy
products.
CAMPYLOBACTER JEJUNI HACCP
While microbiological criteria may not be applicable, surveys
to ascertain the incidence of this organism in the general food
supply should be encouraged. Investigations of foodborne
gastroenteritis outbreaks should include examination of
suspect food for the presence of C. jejuni. Methods for
detecting C. jejuni in foods are now available.
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Campylobacter jejuni – Process Hazard
Analysis and Critical Controls
Transmission
Infected humans and animals excrete the organisms in their
feces. High numbers of this pathogen (10 6 per gram) are
passed in the diarrheal stools of infected individuals. The
transmission to humans may be by direct contact with infected
people, animals or poultry; through contaminated carcasses
and contaminated food and water. This means that crosscontamination on a cutting board or from a contaminated knife
can create an instant hazard in another food that is prepared on
that same cutting board or knife if that food is not heated
sufficiently.
Foods most often implicated are poultry products,
unpasteurized milk, meat and eggs, and uncooked foods such
as salads and sandwiches that have been contaminated by meat
or poultry products, by an infected food handler, or by
untreated sewage.
Poultry is a common source of Campylobacter jejuni. Heavily
infected flocks of chickens can contaminate an entire
slaughtering operation. The microorganism can be isolated
from the scalding water, pickers, and chilling tanks.
Contaminated raw products may then cross-contaminate
utensils, work surfaces, and cutting boards in any area where
food is prepared.
Control
Methods to control the transmission of this microorganism
include:
1. Good personal hygiene by food handlers with emphasis
on frequent hand washing.
2. Sanitary food handling procedures that prevent crosscontamination. This includes preparation of raw foods,
particularly meat and poultry in separate areas or with
separate sanitized equipment in order to prevent transfer
of this bacteria to cold or pre-cooked food products that
will receive no further heating.
3. Adequate cooking/pasteurization of meat and poultry to
ensure the destruction of the microorganism.
4. The FDA recommends cooling potentially hazardous
food to 41°F in less than 6 hours (e.g., from 135 to 70°F
(57.2 to 21°C) within 2 hours; followed by cooling to
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References:
Archer, D.L. and Young, F. L. 1988. Contemporary Issues:
Diseases with a food vector. Clin. Microbiol. Rev. 1(4):
377-398.
Franco, D.A. 1989. Campylobacteriosis. J. Environ. Health
52(2): 88-91.
National Advisory Committee on Microbiological Criteria for
Foods. 1995. Campylobacter jejuni/coli. Dairy, Food
and Environmental Sanitation 15 (3): 133-153.
Stern, N. J. and Kazmi, S.U. 1989. Campylobacter jejuni. In
Foodborne Bacterial Pathogens. Doyle, M.P., ed.
Marcel Dekker, Inc., New York, NY.
USDA FSIS. 2001. Draft compliance guidelines for ready-toeat meat and poultry products.
http://www.fsis.usda.gov/OPPDE/rdad/FRPubs/RTEGui
de.pdf
Table 4-13
Predicted Generation Times for Yersinia enterocolitica in
Foods*
CHARACTERISTICS
OF YERSINIA ENTEROCOLITICA
•
•
•
•
Grows with and without air
•
•
Found in raw milk, pork, water
•
•
3.9x109 cells in a portion of food can cause illness
Temperature
F (C)
32 (0)
41 (5)
45 (7.2)
50 (10.0)
60 (15.6)
70 (21.1)
80 (26.7)
90 (32.2)
95 (35.0)
111 (43.9)
Grows between 29.3 and 111ºF
Survives freezing temperatures
Source is infected animals,
shellfish, and people
Vegetative cells multiply in intestinal tract to cause illness
that may simulate appendicitis
Vegetative cells killed by cooking / pasteurization
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Yersinia enterocolitica –
Characteristics
2.5 days
13.5 hours
8.9 hours
5.8 hours
3.0 hours
1.9 hours
1.2 hours
50 minutes
45 minutes
no growth
* Adapted from data of Snyder, O.P. (1998).
Yersinia enterocolitica is destroyed by standard pasteurization
times and temperatures. There have been incidents when it
has been found in pasteurized milk, but this is thought to be
due to cross-contamination after pasteurization.
Bacterial Characteristics
Yersinia enterocolitica is a gram-negative rod that may
arrange itself singly or in short chains or heaps. Cultures
grown at 77°F (25°C) show flagella and are motile, while
those grown at 98°F (37°C) show no flagella and are not
motile. It is aerobic and may be facultatively anaerobic.
Pathogenic Y. enterocolitica is not often encountered. Most
virulent forms of Y. enterocolitica are of the O serotype (O3;
O5,27; O8; and O9). However, serotype alone does not
determine the virulence of the microorganism. The factor that
causes the virulence of Y. enterocolitica is thought to be
mediated by plasmids (self-replicating, extrachromosomal,
circular DNA molecules).
Sources
Yersinia enterocolitica is ubiquitous throughout the animal
world. Yersinia enterocolitica is found in meat, especially
pork, in oysters and mussels, and in milk and drinking water.
Pathogenic strains are principally carried by pigs (Stern and
Pierson, 1979).
Growth Conditions
Growth temperatures range from 29.3 to 111°F (-1.5 to 44°C)
but best growth occurs at 90 to 94°F (32 to 34°C). The
organism is able to multiply at low temperatures under
refrigeration. It is capable of multiplying in vacuum packaged
roast beef at 29.3°F (-1.5°C) (Hudson et al., 1994). Table 413 lists the average generation times for Y. enterocolitica in
foods.
The organism grows at pH 4.6-9.0. A pH of 7.0-8.0 is optimal
for growth. A pH of less than 4.4 or above 9.6 is
bacteriocidal. At 37°F and 77°F (3°C and 25°C), 7% table salt
(sodium chloride, NaCl) is inhibitory, but at 37°F (3°C) in 5%
NaCl, growth is observed.
Extensive reductions of the Y. enterocolitica occur during
frozen storage, but there will still be survivors. Hanna et al.
(1977) found that there was a 2.9 to 4.0 log reduction in the
counts when beef sirloin tip roasts were experimentally
inoculated with 106 to 107 cells per gram and stored at 0 to 4°F (-18 to -20°C) for 28 days.
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Generation Time
Symptoms
Yersinia enterocolitica is the cause of yersiniosis, a foodborne
infection. The incubation time is 24 to 36 hours and longer.
The symptoms of the illness are abdominal pain, fever,
headache, malaise, nausea, vomiting, and diarrhea. The severe
abdominal pain caused by this illness has led to a misdiagnosis
of appendicitis. Several cases have resulted in unnecessary
appendectomies, especially in children.
Complications from yersiniosis sometimes occur. These
include: arthritis, mesenteric lymphadenitis, terminal ileitis,
erythema nodosom, endocarditis, septicemia, and meningitis.
It has sometimes been misdiagnosed as Crohn's disease. The
major complication is unnecessary appendectomies, since one
of the main symptoms is abdominal pain of the lower right
side.
Infective Dose
The infective dose as defined by Moustafa et al. (1983) is 3.9
x 109 organisms or 2 x 107 in 200 grams of cheese. This is
based on a single volunteer study and the infective dose may
be much lower.
Methods of Recovery
Methods of recovering Y. enterocolitica from foods have
improved in recent years. However, no single method is
suitable for recovery of all types of this species from various
foods. Since not all strains are pathogenic, isolates must be
tested for pathogenicity. Primary and secondary or selective
enrichment procedures, followed by determination of
biochemical and serological characteristics of cultural isolates,
are required. Isolation and confirmation may require 2 to 3
weeks.
Incidence
The illness has been more prevalent in Japan and Europe than
in the United States and Canada. The first outbreak reported
to CDC in which foodborne yersiniosis transmission was
documented in the United States occurred in 1976 among
school children in Oneida County, New York. Chocolate milk
4a-58
was the indicted food. Yersinia had been suspected of causing
previous similar foodborne illness outbreaks but this could not
be clearly documented.
In the above-mentioned outbreak of yersiniosis due to
chocolate milk, neither the chocolate syrup nor the milk
(pasteurized) could be implicated, but the mixture was. In the
dairy plant, the chocolate syrup was manually added to a large
open vat of pasteurized milk, and the mixture was not
repasteurized before being placed in cardboard (1/2-pint)
cartons. The milk was distributed to the schools in an
unrefrigerated truck.
Water can be a source of Y. enterocolitica. Water used in the
preparation of tofu was identified as the source of the
microorganism in an outbreak. Another episode of yersiniosis
occurred when skiers in Montana consumed water from a
mountain stream.
An outbreak of yersiniosis occurred in Arkansas, Mississippi,
and Tennessee in 1982. (172 people ill from pasteurized
milk). In this incident, milk crates had been contaminated
with pig feces from a farm that was receiving returned milk
from a local dairy plant.
Another incident occurred the same year in the state of
Washington. It was determined that yersiniosis was due to
consumption of tofu (soybean curd) which had been produced
in a processing facility using non-chlorinated water.
The concern at this time is post-pasteurization contamination
of milk with pathogenic or virulent strains of Yersinia. Raw
or inadequately cooked seafood, vacuum-packaged meat, and
processed products handled by infected workers can be a
potential source of Y. enterocolitica.
The estimated annual incidence of Y. enterocolitica in the U.S.
is over 86,000 cases, resulting in 2 to 3 fatalities (Mead et al.,
1999).
References:
Adams, M. R. and Moss, M. O. 1995. Food Microbiology.
The Royal Society of Chemistry. Cambridge, U.K.
Doyle, M.P. 1988. Yersinia enterocolitica. Food Technol.
42(4):188.
Hanna, M.O., Stewart, J.C., Zink, D.L., Carpenter, Z.L., and
Vanderzant, C. 1977. Development of Yersinia
entercolitica on raw and cooked beef or pork at different
temperatures. J. Food Sci. 42(5): 1180-1184.
Hanna, M.O., Stewart, J.C., Carpenter, Z.I., and Vanderzant,
C. 1977b. Effect of heating, freezing, and pH on
Yersinia enterocolitica-like organisms from meat. J. of
Food Protect. 40: 689-692.
Hudson, J.A., Mott, S.J., and Penney, N. 1994. Growth of
Listeria monocytogenes, Aeromonas hydrophila,
Yersinia enterocolitica on vacuum and saturated carbon
dioxide controlled atmosphere-packaged sliced roast
beef. J. Food Protect. 57 (3): 204-208.
Mead, P. S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee,
J.S., Shapiro, C., Griffin, P. M., and Tauxe, R. V. 1999.
Food-related illness and death in the United States.
Emerg. Inf. Dis. 5 (5): 606-625.
Moustafa, M.K., Ahmad, A. A-H., and Marth, E. 1983.
Behavior of virulent Yersinia enterolitica during
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4a-59
manufacture and storage of colby-like cheese. J. Food
Protect. 46:318-320. In
Robins-Browne, R.M. 2001. Yersinia enterocolitica In Food
Microbiology. Fundamentals and Frontiers, 2nd edition.
Doyle, M. P., Beuchat, L. R., and Montville, T. J. eds.
American Society of Microbiology. Washington, D. C.
pp. 215-246.
Schiemann, D.A. 1989. Yersinia enterocolitica and Yersinia
pseudotuberculosis. In Foodborne Bacterial Pathogens.
Doyle, M.P., editor. Marcel Dekker, Inc., New York,
NY.
Snyder, O. P. 1998. Updated guidelines for use of time and
temperature specifications for holding and storing food
in retail food operations. Dairy Food Environ. Sanitation
18 (9): 574-579.
Stern, N.J. and Pierson, M.D. 1979. Yersinia enterocolitica:
A review of the psychrotrophic water and foodborne
pathogen. J. Food Sci. (44) 1736-1741.
Sutherland, J.P. and Varnham, A.H. 1977. Methods of
isolation and potential importance of Yersinia
enterocolitica in foods stored at low temperatures. J.
Appl. Bacteriol. 43:13-14.
Swaminathan, B., Harmon, M.C., and Mehlman, I.J. 1982. A
review - Yersinia enterocolitica. J. Appl. Bacteriol.
52:151-183.
References:
Adams, M. R. and Moss, M. O. 1995. Food Microbiology.
The Royal Society of Chemistry. Cambridge, U.K.
Doyle, M.P. 1988. Yersinia enterocolitica. Food Technol.
42(4):188.
Mossel, D.A.A., Corry, J. E., Struijk, C. B., and Baird, R.
1995. Essentials of the Microbiology of Foods. John
Wiley and Sons, New York, NY.
Schiemann, D.A. 1989. Yersinia enterocolitica and Yersinia
pseudotuberculosis. In Foodborne Bacterial Pathogens.
Doyle, M.P., editor. Marcel Dekker, Inc., New York,
NY
Snyder, O.P. 1989. Hazard Analysis and Critical Control
Points Manual. Hospitality Institute of Technology and
Management. St. Paul, MN.
Swaminathan, B., Harmon, M.C., and Mehlman, I.J. 1982. A
review - Yersinia enterocolitica. J. Appl. Bacteriol.
52:151-183.
YERSINIA ENTEROCOLITICA HACCP
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Yersinia enterocolitica – Process Hazard
Analysis and Critical Controls
Transmission
Although frequently found in swine and other food animals
and often reported as causing illness in humans in other
countries, relatively few documented outbreaks of foodborne
illness due to Yersinia enterocolitica have been reported in the
United States. The low incidence of this foodborne illness
may be due to the relatively high number of microorganisms
of a virulent strain needed for an infective dose. Incidents of
yersiniosis have been due to contaminated chocolate milk, tofu
(soybean curd) packed in contaminated water, contaminated
pasteurized milk, and drinking water from an unsafe source.
The major mode of transmission is food and water
contaminated with animal feces (particularly swine) and urine.
Control
Yersinia enterocolitica presents a special problem because it is
psychrotrophic (can grow at refrigerator temperatures.) The
introduction of Y. enterocolitica into refrigerated foods, by
cross-contamination and food handlers is very possible. Not
all types of Yersinia are virulent and accurate methods of
detecting virulent strains have yet to be determined.
In order to prevent an outbreak of yersiniosis, food service
establishments should:
1. Use only pasteurized milk.
2. Buy food products from suppliers who certify the
microbiological quality of their products and use safety
assured manufacturing practices.
3. Use care to prevent cross-contamination between raw
products (particularly pork products) and prepared,
ready-to-eat foods.
4. Use water and ice supplied from a safe water supply.
5. Mandate employee hand washing procedures after raw
products are handled (particularly raw meats).
6. Use cold, ready-to-eat food stored at or below 41°F
(5°C) within 7 days.
7. Clean and sanitize all utensils before starting a food task
in order to prevent cross-contamination.
8. Cook food according to the Salmonella pasteurization
standard that will destroy Y. enterocolitica.
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