Microbial Contamination of Processed Meat
OA Aiyegoro, Agricultural Research Council, Pretoria, South Africa
r 2014 Elsevier Ltd. All rights reserved.
Glossary
Aerobic It means requiring air (oxygen).
Anaerobic It means without air (oxygen).
Bacilli Taxonomic class of Gram-positive, rod-shape
bacteria; can be obligate aerobes or facultative.
Bacteriocins Proteinaceous toxins produced by bacteria to
inhibit the growth of similar or closely related bacterial
strain(s).
Biocidal Chemical agent, such as a pesticide, that is
capable of destroying living organisms.
Introduction
Processed meat could be defined as any meat preserved by
smoking, curing, or salting, or with the addition of chemical
preservatives; examples include bacon, salami, sausages, hot
dogs or processed deli, or luncheon meats. These meat prod-
ucts maintain at least one-half of their original meat integrity
after processing (i.e., the original meat qualities have reduced
to one-half when a meat is processed into meat products);
meat products are the most popular and one of the most
consumed and highly savored food products worldwide.
Safe food supply is a challenge worldwide due to the
presence of spoilage and pathogenic microorganisms, which
has bewitched food processing and supply industries. ‘Mi-
crobial contamination of food accounts for approximately
2500 cases of illness and approximately US$200 million in
monetary loss in the United States annually.’ In spite of
modern innovations in harvest hygiene and food production
techniques, the safety of commercially processed meat prod-
ucts is a major area of concern.
The absence of centralized harvest facilities and the small
volume of retail business (i.e., the retail venture is usually a
small market), prohibitive capital costs on mechanized infra-
structure, and recurring expenditures have been the hurdles for
hygienic processing of meat.
Reduction of initial bacterial load in meat is of prime im-
portance in an attempt to improve the shelf life of products.
Shelf life of meat products depends on several factors – the
most important of which is the microbiological quality. Sev-
eral studies have indicated that consumption of meat and
meat products has been associated with incidence of outbreaks
of foodborne illnesses. Foodborne pathogens are the leading
causes of illness and death in developing countries costing
billions of dollars in medicare and social costs. Foodborne
disease and microbial spoilage of food results from the failure
or inability to control microorganisms at one or more stages of
the food chain from raw material to consumption of the final
product. The implications of situations that result in food
poisoning outbreaks or food spoilage can be severe for food
producers, retailers, consumers, and regulatory authorities.
Encyclopedia of Meat Sciences, Volume 2 doi:10.1016/B978-0-12-384731-7.00249-X
Cocci Any bacterium that has a spherical shape.
Gram-positive Bacteria that do not retain crystal violet dye
in the Gram staining protocol.
Microbes A microscopic organism.
Pathogenic microorganisms Microorganisms that can
cause disease in other organisms or in humans, animals,
and plants.
Virulence factors Molecules expressed and secreted by
pathogens (bacteria, viruses, fungi, and protozoa) that
enable them to start an infection.
Microbial growth during storage is one of the main factors
affecting the quality of meat products leading to contamin-
ation and spoilage and, hence, economic loss. Microbiological
criteria should take into account any organisms that are likely
to be present in the meat product. The levels of tolerance ap-
plied at the time of manufacture should be such that, even
after allowing for predictable growth of these organisms,
products should remain safe and wholesome till the end of
shelf life, provided they are stored under the appropriate
conditions.
The safety of foods of animal origin for human con-
sumption has become an essential component of public
health debates. Thus, microbiological ecology of meat prod-
ucts will mainly depend on the environment, kind of meat and
raw material, equipment, handling practices, processing,
packaging, and storage temperature.
Traditionally, control of microorganisms in food has been
demonstrated by microbiological testing of samples at various
stages of production, including the final product. The potential
for growth and/or toxin production of residual microbial
population in finished products depends on the type of or-
ganisms present and their ability to grow to a level of concern
under the storage conditions applied during the product shelf
life.
Sources of Microbial Contaminants in Meat Products
Meat products can be contaminated with microorganisms from
meat handlers who carry pathogenic microorganisms during
the processes of manufacturing, packing, and marketing. One
of the major risks of food contamination originates from the
working practices of food handlers and disease-causing micro-
organisms present in or on the food handler's body that
are subsequently transported from the food handler to the
food during the handling process. Personal hygiene is very
important in food processing because a major source of con-
tamination leading to food poisoning caused by Staphylococcus
aureus is human. Poor personal hygiene practices, such as neg-
ligence to wash hands after visiting the bathroom may result in
289
290 Microbial Contamination | Microbial Contamination of Processed Meat
up to 107 CFU (colony-forming units) ml 1 pathogens under
the fingernails of food handlers. Spice, which has an important
role in meat products, can be contaminated with bacteria,
molds, and yeasts. Microbial load of spice depends on its var-
iety, processing method, granule size, and moisture content.
Minced meat and spice mix have been identified as the primary
contamination sources in sausage manufacturing. The most
probable reason for minced meat having high microbial load is
the poor hygienic quality of raw meat. Microbial quality of raw
meat and nonmeat ingredients affects the quality of final
products. The hygienic condition and level of sophistication of
the harvesting and processing equipment are also contributory
sources of contamination in processed meat products. Studies
have revealed that contamination of meat with microbes de-
creased with increased sophistication of harvest facilities. Also,
the incidence of various foodborne pathogens in processed
meat may be different in different parts of carcasses from which
the processed meat is obtained; for instance, studies have
shown that thigh muscles were highly prone to contamination
compared to the breast muscle, irrespective of the processing
conditions.
Some Microbial Contaminants of Processed Meat
Many groups of microorganisms potentially contribute to
meat spoilage under appropriate conditions. This makes the
microbial ecology of spoiled meat products very complex, and
thus the spoilage is very difficult to prevent. Many studies have
determined the presence of foodborne pathogens in meat
products, such as Listeria monocytogenes, S. aureus, Escherichia
coli, Clostridium perfringens, and Samonella spp.
Listeria monocytogenes is a Gram-positive, nonspore form-
ing, highly mobile, rod-type, facultative anaerobic bacterium.
It can grow in a wide range of temperature conditions and pH
range. The organism can tolerate salt and nitrite, and is
widely spread in the environment. The Centers for Disease
Control and Prevention reported that a multistate outbreak
between 1998 and 1999, which caused 101 cases and 21
deaths, was linked to the contamination by L. monocytogenes
in frankfurters and deli meats. In 2000, a multistate outbreak
involving deli turkey meat resulted in 29 cases, 4 deaths, and
3 miscarriages or stillbirths. The recall of 26 million pounds
of meat products in 2002 indicates the economic con-
sequences of contamination with L. monocytogenes. The U.S.
Department of Agriculture (USDA) has thus established a
‘zero tolerance’ policy for L. monocytogenes in meat products.
Therefore, it is important to prevent contamination in meat
products.
Staphylococcus aureus is one of the most common agents in
bacterial food poisoning outbreaks; it is also a major causative
pathogen of clinical or subclinical mastitis of dairy domestic
ruminants. Poultry, meat and egg products as well as milk and
milk products have been reported as common foods that may
cause staphylococcal food poisoning. Staphylococcus aureus is
one of the commonest etiological agents of bacterial diseases
worldwide due to its ability to produce a broad range of
exotoxins and other virulence factors. Among them, the
staphylococcal enterotoxins produced by some S. aureus
strains are the main cause of most widespread foodborne
intoxications. Staphylococcal food poisoning, together with
toxic shock syndrome toxin-1 are responsible for toxic shock
syndrome and staphylococcal scarlet fever. Studies have shown
that augmentation of the additives, onion garlic meal, pepper,
and E vitamin can decrease the microbial agents in meat
products.
Other contamination bacteria in processed meat products
include Salmonella, Bacillus, Clostridium, Escherichia, Campylo-
bacter, Acinetobacter, Aeromonas, Enterococcus, Moraxella, and
Psychrobacter. Some of the pathogenic bacteria, such as Sal-
monella, can be found in fermented meat products because
this organism can tolerate or adapt to a wide variety of en-
vironmental stresses during meat fermentation. Food poi-
soning outbreaks caused by the consumption of fermented
meat products contaminated with Salmonella, such as Sal-
monella typhimurium DT 124 and S. typhimurium PT 193, in
salami have been reported. Although these pathogenic bac-
teria can be destroyed during cooking by heat treatment,
some consumers prefer to consume raw or medium-cooked
products.
Intervention against Microbial Contaminants of
Processed Meat
Most microbial vegetative cells and toxic products are sensitive
to heat treatment and can easily be inactivated by cooking.
Therefore, postcooking recontamination during packaging is
the main concern. Postpackage decontamination methods
such as in-package thermal pasteurization and irradiation, and
formulating meat products with antimicrobial additives are
common approaches to control microbial contaminants in
processed meat. Therefore, it is to the manufacturer's advan-
tage to take measures for reducing contamination in food.
Irradiation
Ionizing radiation is a process in which products are exposed
to radiant energy. Ionizing radiation includes gamma rays,
electron beams, and X-rays. E-beam irradiation was reported
to be more effective than gamma-ray irradiation in decreasing
Bacillus cereus and E. coli O157:H7, but not for L. mono-
cytogenes. In cooked pork chops and hams inoculated with L.
monocytogenes, low-dose (0.75–0.90 kGy) irradiation reduced
L. monocytogenes by 42 log. Irradiation treatments were sig-
nificantly more lethal under aerobic packaging than in either
vacuum or modified atmosphere packaging conditions. One
concern about using modified atmosphere packaging in ir-
radiated meat or poultry is that pathogens may grow and/or
produce toxins because of low competing organisms. This is
of even greater concern if spoilage is suppressed and does not
provide the usual warning signals. Temperature effects must
be carefully considered because reduced irradiation tem-
peratures result in fewer adverse changes in the sensorial
properties of meat and poultry products. However, low
temperature conditions require greater radiation doses to
inactivate the foodborne pathogens. The irradiation dose rate
is another factor because, at low dose rates, microbial en-
zymes may have more time to repair damage to cells,
 Microbial Contamination | Microbial Contamination of Processed Meat
resulting in higher resistance. Generalization of the effects of
irradiation can be misleading because the effectiveness of
irradiation is affected by irradiation conditions and product
compositions.
Food Preservatives
Chemical antimicrobials: The salt of lactate (SL) is frequently
used as an antimicrobial in meat products due to its beneficial
properties to meat quality when applied at appropriate con-
centrations. The addition of lactate to food products with
neutral pH offers good prospects for prolongation of shelf life.
In general, Gram-positive bacteria were more sensitive toward
lactate than Gram-negative bacteria under optimum growth
conditions (pH 6.5, 20 1C). The combined application of
lactate and diacetate resulting in a synergistic inhibitory effect
on the growth of pathogenic organisms in meat products has
been reported to be very effective. A chemically synthesized
short-chain peptide composed of 6 leucine and 8 lysine resi-
dues was shown to be biocidal against several foodborne or-
ganisms, including L. monocytogenes suspended in phosphate
buffer at concentrations 5–50 mg ml 1. Peptide concentrations
of 100 mg ml 1 inhibited aerobic and anaerobic microorgan-
isms present in meat exudate. Sodium hypochlorite, quater-
nary ammonium compound, and peroxyacetic acid used as
sanitizers in meat processing plants were effective in elimin-
ating L. monocytogenes.
Lactobacilli, probiotic bacteria, and bacteriocins: Biopreservation
with various strains of lactic acid bacteria is a suitable alternative
to chemical preservatives. The antimicrobial activity of a bac-
teriocin-producing Lactobacillus plantarum MCS strain against
L. monocytogenes was observed in naturally and artificially con-
taminated salami, all showing strong antimicrobial effects.
Thus, the application of Lactobacillus, Pediococcus, or enterococci
bacteria in starter cultures may provide an additional hurdle
against pathogens in fermented meat products. Lactic acid
bacteria can also be used to inhibit the growth of bacterial
contaminants in nonfermented products. Addition of Lacto-
bacillus sakei Lb 706 prevented the growth of L. monocytogenes
pasteurized minced meat and comminuted cured raw pork
during the first few days after production. The L. sakei strain
applied to cooked products at a concentration of 105–
106 CFU g 1 immediately before slicing and vacuum packaging
inhibited the growth of a cocktail of 3 rifampicin-resistant
mutant L. monocytogenes strains both at 8 1C and 4 1C. Bacter-
iocins are ribosomally synthesized polypeptides produced by
bacteria with an ability to kill or inhibit the growth of similar
bacterial strain(s). Nisin is the most commercially important
bacteriocin due to its relatively long history of safe use. It is
currently recognized as a safe food preservative in approxi-
mately 50 countries.
Plant extracts: Plant extracts, due to their antioxidant and
antimicrobial activities, have a broad spectrum of anti-
microbial activity against many genera of bacteria and fungi. It
has been reported that eugenol (clove extract) and pimento
extract significantly inhibit the growth of Aeromonas hydrophila
and L. monocytogenes inoculated in cooked beef slices. The
numbers of E. coli O157:H7, L. monocytogenes, and S. typhi-
murium in treated raw ground beef declined when 1% pine
291
bark extract was used as an antimicrobial on the ground beef
after 9 days of refrigerated storage. These results suggest that
natural plant extracts have a potential to be used with other
preservation methods to reduce pathogens in processed meat.
In-Package Thermal Pasteurization
Effects of surface pasteurization temperatures on the survival
of L. monocytogenes in low-fat turkey bologna showed that all
the L. monocytogenes cells were destroyed after exposure to an
85 1C water bath for 10 s (46-log reduction), but viable cells
were detected at up to 10 min of heating at 61 1C (o6-log
reduction). The effectiveness of in-package pasteurization in
inactivating pathogenic organisms depended upon package
size and the roughness of the product surface. The strains of
bacteria also influence the effectiveness of thermal pasteur-
ization. Cells grown at 42.8 1C before heat treatment were
more thermotolerant than those grown at 37 1C. Heating at
slowly increasing temperatures (0.7 1C min 1) enhanced the
thermotolerance of L. monocytogenes, and starvation in phos-
phate-buffered saline pH 7 for 6 h at 30 1C increased the heat
resistance of the organism in broth.
High-Pressure Processing
High-pressure processing (HPP) is a novel, nonthermal
method of food processing where food is subjected to elevated
pressures with or without addition of heat. HPP can inactivate
microorganisms without significant changes in texture, color,
or nutritional value of food. HPP is not only a powerful tool to
control pathogenic organisms but also is effective on spores
and viruses. The decontamination efficacy of HPP also de-
pends on many other factors, such as level of pressure, treat-
ment temperature, exposure time, pH, water activity, and food
composition. Many studies have shown that the effectiveness
of HPP was slightly reduced at room temperature compared
with refrigerated temperature. Also, the presence of oil reduced
the effectiveness of high pressure in killing L. monocytogenes
and cell morphology also had an effect on HPP, with bacilli
being more sensitive to pressurization than cocci. When HPP
was combined with antimicrobials, like bacteriocins, death
rate increased because of sublethal injuries to living cells.
Combination Therapy Technology
The concept of combination therapy technology is based on
the application of combined preservative factors to achieve
microbiological safety and stability of foods. The most im-
portant hurdles used in food preservation are temperature,
water activity, acidity, redox potential, antimicrobials, and
competitive microorganisms. A synergistic effect could be
achieved if the hurdles hit at the same time at different targets
that disturb the homeostasis of the microorganisms present in
foods. For meat products, the most frequently applied hurdles
include thermal processing, vacuum packaging, refrigerated
storage, and nitrite. However, these hurdles seem insufficient
for L. monocytogenes due to its ubiquitous nature, ability to
grow at refrigerated temperature and anaerobic condition, and
resistance to salt and nitrite.
292 Microbial Contamination | Microbial Contamination of Processed Meat
Microbial Contamination Intervention and Processed
Meat Quality
Although interventions are very effective in controlling food-
borne pathogens in meat, it generates free radicals that can cause
lipid peroxidation and other chemical changes, which influence
the quality of processed meat. Irradiated meat products can
develop a characteristic odor described as ‘bloody sweet’ or
‘barbecued corn-like.’ Sensory analysis indicated that sulfur odor
increased as irradiation dose increased. In addition to sulfur
compounds, irradiation dramatically increased other volatiles in
the meat products. Irradiation can induce a variety of color
changes depending on irradiation dose, animal species, muscle
type, pH, and reducing potential of meat and packaging type.
The color change induced by irradiation is associated with car-
bon monoxide production during irradiation, which is correl-
ated with increased redness of irradiated meat. They
characterized the pigment that causes pinkness in irradiated
turkey meat as carbon monoxide-myoglobin (CO-Mb). Irradi-
ation is also reported to cause the oxidation of amino acids by
generating high yields of side-chain hydroperoxides that relates
to the oxidation of proteins and lipids.
Injection of SL to cooked, vacuum-packaged beef top rounds
resulted in higher cooking yields and darker, redder color with
less gray surface area. Flavor notes associated with fresh beef
were also enhanced by the addition of SL, and flavor deterior-
ation during storage was minimized. In Chinese-style sausage,
the addition of 3% SL resulted in better quality regarding phy-
sicochemical characteristics. Research reports have shown that SL
added to fresh pork sausage did not affect the internal lean color
but resulted in more rapid surface discoloration, and that 2%
potassium lactate had no effect on quality and sensory properties
of low-fat pork sausage or lean color during refrigerated aerobic
storage. Adding 2% SL to turkey breast rolls resulted in lower
color values, but increased hardness, springiness, cohesiveness,
chewiness, and resilience of turkey breast rolls. Including 3.3%
commercial SL in frankfurter formulation did not affect textural
profile of sausage. Addition of potassium sorbate up to 0.1% or
sodium benzoate up to 0.1% in product formulation had no
effects on the texture of products. These results suggest that the
effect of SL on the quality of products depends on SL level and
product types. A high concentration of sodium diacetate (SDA)
has a negative effect on flavor of ham products. However, at
lower levels (0.1%), SDA does not influence the quality of meat
products. The addition of potassium benzoate greatly increased
the content of benzene in the volatiles of irradiated RTE turkey
ham and breast rolls, suggesting that benzoate salt is not a good
antimicrobial to be used in products for irradiation. HPP causes
minimal changes in ‘fresh’ characteristics of foods because it can
be conducted at ambient or refrigerated temperatures. However,
there is no doubt that HPP causes quality changes of meat. Some
of the changes such as color and lipid oxidation are detrimental,
whereas other changes such as pressure tenderization and pres-
sure-assisted gelation are beneficial.
Conclusion
Microbial contamination can occur and can be reduced at
different stages of processing of meat. Experiments have
confirmed that coliform bacteria, fecal coliform bacteria, E.
coli, total Enterococcus spp. and aerobic plate count are the
most important indicator organisms that are most commonly
used to ensure food safety. In some instances, enumeration of
yeast performed on samples taken during processing in small
businesses to verify good manufacturing practices is also good.
This verification through monitoring was found to be an at-
tractive alternative to the examination of end products.
To ensure the microbiological quality of final products, raw
meat and ingredients must be inspected before entering the
processing plant. Certified suppliers must be selected. Strong
criteria for hygienic quality of raw meat must be set for sup-
pliers. After receiving raw meat and ingredients, they must be
stored in appropriate conditions until use. Effective cleaning
and sanitation programs must be performed in processing
plants. Personnel should follow the standard hygienic pro-
cedures and health conditions of personnel must be moni-
tored regularly, and finally, appropriate time and temperature
settings for meat processing should be selected.
See also: Biofilm Formation. Conversion of Muscle to Meat:
Rigor Mortis, Cold, and Rigor Shortening. Environmental
Contaminants. Foreign Bodies. Growth of Meat Animals:
Muscle. Meat, Animal, Poultry and Fish Production and
Management: Antibiotic Growth Promotants; Disease Control and
Specific Pathogen Free Pig Production; Exotic and other Species;
Meat Production in Organic Farming; Poultry; Red Meat Animals.
Meat-Borne Hazards, Concepts and Methods for Mitigating
Risks Related to. Microbial Contamination: Decontamination of
Fresh Meat; Decontamination of Processed Meat; Microbial
Contamination of Fresh Meat. Microbiological Analysis: DNA
Methods; Indicator Organisms in Meat; Standard Methods.
Microbiological Safety of Meat: Aeromonas spp.; Bacillus
cereus; Clostridium perfringens; Emerging Pathogens; Listeria
monocytogenes; Pathogenic Escherichia coli; Prions; Salmonella
spp.; Staphylococcus aureus; Thermotolerant Campylobacter;
Viruses; Yeasts and Molds; Yersinia enterocolitica.
Microorganisms and Resistance to Antibiotics, the Ubiquity
of: Antibiotic Resistance by Microorganisms. Modeling in Meat
Science: Meat Quality; Microbiology; Refrigeration. Nutrition of
Meat Animals: Pigs; Poultry; Ruminants. Residues in Meat and
Meat Products: Feed and Drug Residues; Residues Associated
with Meat Production. Species of Meat Animals: Cattle; Finfish;
Game and Exotic Animals; Pigs; Poultry; Sheep and Goats; Shellfish
Further Reading
Ahn, D.U., Lee, E.J., 2004. Mechanisms and prevention of off-odor production and
color changes in irradiated meat. American Chemical Society Symposium Series
875, 43–76.
Ahn, J., Grun, I.U., Mustapha, A., 2004. Antimicrobial and antioxidant activities of
natural extracts in vitro and in ground beef. Journal of Food Protection 67,
148–155.
Cegielska-Radziejewska, R., Pikul, J., 2004. Sodium lactate addition on the quality
and shelf life of refrigerated sliced poultry sausage packaged in air or nitrogen
atmosphere. Journal of Food Protection 67, 601–606.
Centers for Disease Control and Prevention (CDC), 2002. Multistate outbreak of
listeriosis − United States. Morbidity and Mortality Weekly Report 51, 950–951.
 Microbial Contamination | Microbial Contamination of Processed Meat
Chen, H., Hoover, D.G., 2003. Bacteriocins and their food applications.
Comprehensive Reviews in Food Science and Food Safety 2, 82–100.
European Food Safety Authority (EFSA), 2006. Opinion of the Scientific Panel on
food additives, flavourings, processing aids and materials in contact with food
(AFC) on a request from the Commission related to 2-isopropyl thioxanthone
(ITX) and 2-ethylhexyl-4-dimethylaminobenzoate (EHDAB) in food contact
materials. European Food Safety Authority Journal 293, 1–15.
Jacobsen, T., Budde, B.B., Koch, A.G., 2003. Application of Leuconostoc carnosum
for bio-preservation of cooked meat products. Journal of Applied Microbiology
95, 242–249.
Jay, J.M., Loessner, M.J., Golden, D.A., 2005. Modern Food Microbiology, fifth ed.
New York, NY: Springer Science and Business Media Inc., p. 790.
Lunden, J.M., Autio, T.J., Sjoberg, A.M., Korkeala, H.J., 2003. Persistent and non-
persistent Listeria monocytogenes contamination in meat and poultry processing
plants. Journal of Food Protection 66, 2062–2069.
Murphy, R.Y., Duncan, L.K., Driscoll, K.H., Marcy, J.A., Beard, B.L., 2003b. Thermal
inactivation of Listeria monocytogenes on ready-to-eat turkey breast meat
products during post-cook in-package pasteurization with hot water. Journal of
Food Protection 66, 1618–1622.
Nam, K.C., Ahn, D.U., 2003b. Effects of irradiation on meat color. Food Science and
Biotechnology 12, 198–205.
293
Ross, A.I., Griffiths, M.W., Mittal, G.S., Deeth, H.C., 2003. Combining non-thermal
technologies to control foodborne microorganisms. International Journal of Food
Microbiology 89, 125–138.
Stekelenburg, F.K., 2003. Enhanced inhibition of Listeria monocytogenes in
Frankfurter sausage by the addition of potassium lactate and sodium diacetate
mixtures. Food Microbiology 20, 133–137.
Zhu, M., Du, M., Cordray, J., Ahn, D.U., 2005. Control of Listeria monocytogenes
contamination in ready-to-eat meat products. Comprehensive Reviews in Food
Science and Food Safety 4, 34–42.
Zhu, M.J., Mendonca, A., Ismail, H.A., et al., 2005. Impact of antimicrobial
ingredients and irradiation on the survival of Listeria monocytogenes and quality
of ready-to-eat turkey ham. Poultry Science 84, 613–620.
Relevant Website
ftp://ftp.cordis.europa.eu/pub/fp7/kbbe/docs/traditional-foods.pdf
European Commission.