795
Journal of Food Protection, Vol. 53, No. 9, Pages 795-803 (September 1990)
Copyright© International Association of Milk, Food and Environmental Sanitarians
The Use of HACCP in the Production of
Meat and Poultry Products1
R. B. TOMPKIN
Swift-Eckrich, Inc., 2001 Butterfield Road, Downers Grove, IL 60515
(Received for publication January 26, 1990)
ABSTRACT
Meat and poultry products frequently have been implicated
in outbreaks of foodborne illness. The risk of foodborne illness
can be reduced through implementation of the hazard analysis
critical control point (HACCP) concept. The basic principles of
HACCP described by the International Commission on Micro-
biological Specifications for Foods are briefly reviewed. Ex-
amples are presented to describe how these principles can be
used to manufacture meat and poultry products with improved
microbiological safety and quality. The future acceptance of HACCP
will depend on the resolution of certain issues.
Meat and poultry products are significant factors in
foodborne illness. Foods containing meat and poultry were
implicated in 54% of all the reported outbreaks of food-
borne illness in the U.S. between 1968 and 1977 (4). This
was later reported to be 33% of all reported outbreaks
between 1977 and 1984 (5). Improvements in the prepa-
ration and handling of meat and poultry products could
result in significant reductions in foodborne illness. The
hazard analysis critical control point (HACCP) concept
provides a systematic approach to achieve this end.
If the goal of reduced foodborne illness is to be achieved,
it is necessary to identify the errors which are involved in
food preparation. Table 1 summarizes the major errors in
food preparation as reported from three regions of the
world: England and Wales, United States, and New South
Wales, Australia (3,6,8). It should be noted that the most
common errors in each region involved some aspect of
time-temperature control. Usually a combination of fac-
tors was involved. For example, preparing foods too far in
advance was a factor in 21-61% of the outbreaks in the
three regions. While preparing foods too early does not, in
'Portions of this material were presented at earlier symposia: Applica-
tions of the Hazard Analysis Critical Control Point (HACCP) Approach to
Food Safety, Union of Microbiological Societies of Yugoslavia and Micro-
biological Society of Serbia, Dubrovnik, Yugoslavia, October 17, 1988;
Applications of the Hazard Analysis Critical Control Point (HACCP)
Concept for Food Operations, Italian Society for Applied Microbiology,
Milan, Italy, September 15, 1989; and Refrigerated Foods and Emerging
Pathogens, Western New York Section of the Institute of Food Technolo-
gists and the Department of Food Science and Technology, Cornell
University, Rochester, NY, November 16, 1989.
JOURNAL OF FOOD PROTECTION, VOL. 53, SEPTEMBER 1990
itself, cause foodborne illness; if the food is recontami-
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nated or if spores survive and the food is held at an improper
temperature, then the growth of foodborne pathogens can
occur and illness can result. The information in Table 1
consists of data for outbreaks from all foods in each region;
however, the same errors do occur in outbreaks in which
meat and poultry are implicated. This information should
be used to direct educational and regulatory efforts to prevent
future outbreaks. Certainly, HACCP systems for meat and
poultry products must consider time and temperature as
the two major factors that must be controlled. The purpose
of this paper is to describe the use of HACCP to improve
the microbiological safety and quality of meat and poultry
products.
PRINCIPLES OF HACCP
There has been considerable evolution in the defini-
tions and principles since HACCP was proposed at the
National Conference on Food Protection (2); however, to
minimize confusion, one reference source on HACCP will
be used to introduce the concept. Some of the basic
components of HACCP which were recently described by
the International Commission on Microbiological Specifi-
cations for Foods (ICMSF) are summarized in Table 2 (7).
Developing the HACCP plan
Each process and the conditions of processing are unique
to each establishment. Although it is possible to general-
ize, as will be done later in the examples with flow dia-
grams, HACCP plans must be customized to the unique
conditions existing within each establishment. Furthermore,
the plans must be updated as future changes are made in
the process or the establishment.
The HACCP plan should be developed by a team of
individuals representing certain disciplines (e.g., engineer-
ing, quality assurance, production, microbiology, sanita-
tion). The team should include local personnel from the
establishment because they will be the most knowledge-
able about the actual conditions which occur during proc-
essing (e.g., variability and limitations of the process).
Other reasons for involving local personnel include: a) the
796 TOMPK1N

TABLE 1. Major errors contributing to foodborne disease in Hazard analysis

three regions of the world. The first step toward establishing a HACCP plan in a
Percentages meat or poultry plant is for the team to conduct a hazard
England, United New South analysis. Hazard has been defined as "the unacceptable
Wales States Wales
1970-1972 1961-1976 1977-1984 contamination, unacceptable growth and/or unacceptable
Improper reheating 29 12
survival by microorganisms of concern to safety or spoil-
10
Inadequate cooking 15 20 5 age and/or the unacceptable production or persistence in
Preparation too far in foods of products of microbial metabolism (e. g., toxins,
advance of serving 61 21 40 enzymes, biogenic amines)" (7).
Improper warm holding 6 16 15 The purpose of the hazard analysis is to identify potential
Storage at ambient problems which could occur in an operation. More than
temperature 40 46 43 one hazard may be associated with a step in an operation.
Improper cooling 32 46 18 Each hazard must be considered and controls established
The number of outbreaks in each region was 1044 in England to minimize or prevent its occurrence. Examples of poten-
and Wales, 1152 in the United States, and 44 in New South tial hazards which might be identified in a meat or poultry
Wales, Australia. There were multiple errors in most of the plant include: raw materials with a history of causing
outbreaks.
microbiological problems; sites of contamination in the

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TABLE 2. Some basic components of a HACCP system as outlined
by ICMSF.
• A hazard analysis is performed and potential hazards are
identified and prioritized according to severity and risk.
• Critical points in the operation which permit control of the
hazards are identified.
• Criteria (e.g., time, temperature, pH) are specified that in-
dicate whether an operation is under control at a particular
CCP.
• Rapid tests are used to monitor whether the CCPs are under
control. The sampling frequency is determined by the severity
and risk of the hazard.
• Corrective action is taken when monitoring results indicate the
operation is not under control.
• Verification tests are used to check that the overall HACCP
system is working and that all hazards have been identified.
• Records are maintained and reviewed. Records include action
taken when criteria have not been met.
process of developing a HACCP plan is educational and
this opportunity for educating local personnel in food safety
should not be overlooked; b) there will be a sense of local
ownership for the plan if plant personnel participate; c) the
plan must be understood and implemented by local per-
sonnel after the "experts" leave; and d) someone, most
likely a local person, should be responsible for assuring
that the HACCP plan is properly updated. A HACCP plan
which is mandated by outside sources will likely be poorly
conceived, erroneous, and/or incomplete, regardless of the
expertise involved.
One individual should be assigned the responsibility
that the completed HACCP plan will achieve its stated
objectives. To be successful, it is essential that the team
be provided with adequate resources and all pertinent
information. There must be an open free exchange of
information by all members of the team. It may be desir-
able or, perhaps, even necessary to obtain outside advice
during the development of the plan or for a final review
of the plan. The qualifications of an "expert" is a signifi-
cant issue but will not be addressed in this paper.
process; and the potential for microorganisms to survive
or multiply during production, storage, distribution, or use.
As a minimum, the hazard analysis should question
the effect of the following upon the safety and quality of
the product: (a) raw materials; (2) characteristics of the
food during and after processing; (c) the procedures used
for processing; (d) packaging, (e) conditions of distribu-
tion; and (f) how the product is used. The analysis of
hazards must be quantitative if it is to be meaningful. This
requires two assessments for each potential hazard, namely,
severity (e.g., spoilage of a food vs. botulism) and risk
(e.g., one chance in a million vs. every time).
Critical control point
After the hazards have been identified, then proce-
dures must be established for their control. The definition
for critical control point (CCP) is of practical importance
to the meat and poultry processor and regulator because it
defines the limits of what should be achieved when a HACCP
program is established. Experience indicates that there can
be considerable debate over which steps in a process are
CCPs, how and how well the CCPs can be controlled, and
the level of confidence that the hazards can be prevented
when the CCPs are under control.
Since the introduction of HACCP, the definition for
CCP has changed markedly. As originally stated, "the critical
control point is a concept adopted by the panel to describe
the location(s) or point(s) in a food processing operation
at which failure to prevent contamination can be detected
by laboratory tests with maximum assurance and efficiency"
(2). This narrow definition focused upon preventing con-
tamination, such as from salmonellae, and the use of
laboratory tests to detect failures if they occur. This origi-
nal definition for CCP was modified by ICMSF in 1980 to
"a location or a process which, if not correctly controlled,
could lead to contamination with unacceptable growth"
(14). Attempts to apply this definition to the control of
salmonellae in a wide variety of products and processes
led to a revised definition (9).
The current ICMSF definition for a critical control
point is "a location, practice, procedure or process at which

JOURNAL OF FOOD PROTECTION, VOL. 53, SEPTEMBER 1990

 USE OF HACCP FOR MEAT AND POULTRY PRODUCTS
control can be exercised over one or more factors which,
if controlled, could minimize or prevent a hazard" (7).
This new definition states in positive terms the value of a
CCP and limits CCPs only to those steps in a process
where some degree of control is possible. This definition
is particularly suitable for fresh meat and poultry as well
as ready-to-eat products. In particular, the definition al-
lows for and encourages the adoption of CCPs to mini-
mize contamination with enteropathogens during the slaugh-
tering processes and the subsequent handling of raw meat
and poultry. The definition is realistic in its recognition
that there is a gradient in the ability to control a hazard.
The gradient ranges from partial control to absolute con-
trol of a hazard. This led ICMSF to propose two general
classifications of CCP based upon the level of confidence
that hazards can be prevented.
A CCP1 will assure control while a CCP2 will mini-
mize but cannot assure the control of a hazard. Both types
of CCP are important and both must be controlled. The net
result of the effort applied to controlling a CCP1 should
be a high level of confidence that the hazard has been
prevented. In the case of a CCP2, the risk of the hazard
can be minimized, but elimination of the hazard cannot be
assured. Conversely, at a CCP2 the risk of the hazard can
be significantly higher if no attempt is made to control the
hazard. Thus, every reasonable effort must be made to
exercise control. Of course, the degree of effort applied
will be influenced by the severity of the potential hazard
and the risk of its occurrence. In situations where the severity
of the hazard is high (e.g., botulism) and the ability to
control the hazard cannot be assured (i.e., CCP2), the
conditions of the process either must be modified so that
control can be assured or the process should not be used.
Tables 3 and 4 provide examples of CCP1 and CCP2,
respectively, in the preparation of meat and poultry prod-
ucts.
A definition for the term, control, as applied to HACCP
has not been suggested to date. In this text and as used in
ICMSF Book 4, control means managing the conditions of
an operation to maintain compliance with established criteria.
Thus, an operation is under control when the established
criteria are being met. Within the context of HACCP, the
net result of control at a CCP is to minimize or prevent
the risk of one or more hazards.
Criteria
Table 3 provides examples of criteria which are used
for monitoring CCPs. If the criteria are met, the hazards
will be prevented or eliminated. For example, the USDA
has established minimum criteria for time and temperature
when cooking roast beef (13). These criteria are based
upon achieving a 7-log destruction of salmonellae in the
coldest area of the roast. This does not include the addi-
tional thermal destruction associated with the rather long
heating and cooling periods during the cooking process.
Thus, the criteria for time and temperatures are very
conservative, and there should be no risk of salmonellae
survival if the criteria are met. Similarly, the USDA has
JOURNAL OF FOOD PROTECTION, VOL. 53, SEPTEMBER 1990
797
TABLE 3. Examples of CCP I in meat and poultry operations.
• Cooking to 63°C, or its equivalent at a lower temperature for
a specified time, assures the destruction of salmonellae in raw
meat.
• Controlled fermentation prevents the formation of S. aureus
enterotoxin during the production of dry sausage.
• Controlled time-temperature at freezing temperatures will assure
the destruction of Trichinella in raw pork.
• Storage at less than 10°C prevents the growth of proteolytic
C. botulinum in meat and poultry.
• Acidifying to pH <4.6 prevents pathogen growth in shelf stable
pickled sausages.
• Drying to Aw <0.86 prevents bacterial pathogen growth in
snack meats.
TABLE 4. Examples of CCP2 in meat and poultry operations.
• Proper care in eviscerating reduces the incidence of Salmon-
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ella and Campylobacter on fresh meat and poultry.
• Separating raw meat from cooked meat processing reduces the
risk of pathogen contamination on cooked products.
• Following correct personal hygiene practices reduces the risk
of product contamination.
• Cleaning, sanitizing, and drying the environment reduces the
risk of Listeria contamination on cooked products.
• Refrigerating cooked products reduces the risk of pathogen
growth between cooking and serving.
established specific time-temperature criteria for holding
raw pork to assure trichinae destruction (12). The risk of
enterotoxin production during the fermentation step for
dry sausage production can be prevented if recommended
criteria for time, temperature, and pH are met (J).
All the criteria suggested in Table 3 permit timely
measurements for determining whether each of the proc-
esses is under control. The examples suggest that the criteria
associated with a CCP1 tend to be specific, quantifiable,
supported by research or the technical literature, and provide
a yes/no response. There is usually an established history
that the criteria can be met reliably with existing technol-
ogy and the hazards can be prevented. One test of the
level of confidence might be that, if requested by a cus-
tomer, a signed letter of guarantee that a certain hazard
does not exist could be issued.
The criteria for CCP2 can be of the same nature as
described for CCP1 above. However, the CCP may be
designated a CCP2 because the procedures available can
minimize but not prevent the hazard, or there may be an
unreliable history of compliance with the established cri-
teria. An example of the latter is whether perishable meat
or poultry products will be maintained below 4.4 or 7.2°C
during storage, distribution, display, and in the home.
The criteria for CCP2 can also be based upon whether
certain established practices are being followed correctly.
In most of the examples in Table 4, compliance is meas-
ured visually by a person knowledgeable in the established
procedures. There may be a human element involved which
798
raises questions of consistency and the training and per-
formance of new employees. Criteria which are based upon
following certain procedures tend to be less specific, less
quantifiable, dependent upon human judgment for meas-
urement, based upon experience as opposed to research,
and provide a yes/no response, but with some reservation.
Experience normally indicates a very high level of com-
pliance. Caution should prevail when signing a letter of
guarantee that a potential hazard does not exist or will not
occur.
Monitoring and verification
A key element of the HACCP system is the use of
rapid measurements to monitor whether established crite-
ria are being met at each CCP. Examples of rapid meas-
urements used in the meat and poultry industry include
visual observations and measurements for fat, moisture,
pH, time, temperature, humidity, and air pressure or vacuum.
These and other measurements can be used to assess whether
established criteria are being met at each CCP. Since the
results become quickly available, the data can be used to
make adjustments during processing and, thereby, main-
tain continuous control of the operation. Measurements
which require too much time to allow adjustments while
an operation is in process are not suitable for monitoring.
Such measurements, however, can be useful for verifica-
tion.
Verification has been defined as the use of supple-
mentary information to check whether the HACCP system
is working (7). Examples of measurements used for veri-
fication include microbiological assays; official methods
for fat, moisture, protein; and tests to check the final internal
temperature of cooked products (e.g., coagulation test,
catalase test).
The use of monitoring and verification will be de-
scribed in the following example. Recontamination of cooked
meat and poultry products is a potential hazard that must
be controlled. Control of the cooked product environment
is a CCP which depends on many factors including plant
layout, equipment design, employee practices, procedures
used for handling product between cooking and final
packaging, and cleaning and sanitizing the equipment and
environment. Although each of these factors is important,
in this example the focus will be limited to equipment
sanitation as a factor influencing product shelf life.
Table 5 lists examples of measurements that are
applicable for monitoring and verifying that equipment is
acceptably clean for handling cooked meat and poultry
products. The three rapid measurements most commonly
used to assess whether equipment is satisfactorily clean
rely upon the human senses for visual appearance, aroma,
and touch. These observations give a rapid assessment but
provide only limited confidence that the equipment is, in
fact, microbiologically acceptable. Thus, it is common in
commercial processing facilities to conduct further analy-
ses for verification purposes.
Several procedures are commonly used in the meat
and poultry industry to verify that equipment has been
JOURNAL OF FOOD PROTECTION, VOL. 53, SEPTEMBER 1990
TOMPKIN
TABLE 5. Measurements for evaluating whether equipment is
hygienically acceptable.
Monitoring measurements:
• visual
• aroma
• touch
Verification measurements:
• Microbiological assays
• samples from equipment (e.g., swabs)
• flow sheet samples
• analysis of finished product
• shelf life tests
• Records and reports
• records which document the results of monitor-
ing and, in the event of deviations, action taken
to correct the problem
• reports from regulatory agency and corporate
staff inspections
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• information from the field on product shelf life
properly cleaned and sanitized. The procedures include
microbiological assays of samples from equipment (e.g.,
swabs), product from various stages of processing (i.e.,
flow sheet samples), finished product, and testing the keeping
quality of the finished product (i.e., does the product meet
the expected shelf life). Other sources of information which
are useful for verification include reports of inspections by
regulatory agencies and others, such as representatives from
the corporate staff and information from the field on product
shelf life. All of these procedures and sources of informa-
tion provide useful data to verify that the monitoring results
have been providing a valid measure of equipment sani-
tation.
Records
A HACCP program is not complete without adequate
documentation. Records of results obtained during the
monitoring of CCPs must be retained for some appropriate
length of time. The results must include action taken when
the established criteria have been exceeded. For example,
it may have been necessary to reprocess product, destroy
product, or alter the manner in which the product is la-
beled, distributed, and used (e.g., reduce the sell-by-date
on the package, distribute frozen instead of refrigerated,
ship to a processor who can use the product in a manner
where the defect does not pose a hazard). The results obtained
from verification tests also must be retained. Ideally, data
obtained during monitoring and verification should be
summarized and used to follow trends so that problems
can be anticipated.
Regulatory agencies will play a significant role in the
use of HACCP in meat and poultry plants. It will be necessary
that certain records be made available to regulatory offi-
cials for their review. Agencies also should have some
responsibility for reviewing HACCP plans to assess whether
there are flaws in the plan relative to the consideration of
hazards, CCPs, criteria, monitoring, verification, and rec-
 USE OF HACCP FOR MEAT AND POULTRY PRODUCTS
ord keeping. Numerous issues must and will be resolved
as the industry and the U.S. Department of Agriculture
move toward adoption and implementation of HACCP.
EXAMPLES OF THE USE OF HACCP IN THE MEAT
AND POULTRY INDUSTRY
Flow diagrams can be very useful when developing a
HACCP program to describe a process, identify sites of
contamination, identify steps in the process where control
can be exercised, and provide an estimate of the degree of
control which can be expected. This helps management
understand the process, including where the potential
problems exist, and, depending upon their severity and
risk, how to allocate resources to control the hazards. This
information also can be used to help document a HACCP
plan and facilitate inspections and the review of processes
by regulatory personnel.
A few examples of the use of flow diagrams and
application of HACCP to meat and poultry processing appear
in Fig. 1-4. A detailed discussion for three of the flow
diagrams (Fig. 1, 2, 4) appears in chapters 10 and 11 of
ICMSF Book 4 (7). The discussion for Fig. 3 appears in
a WHO-ICMSF report (9). Continuing with its desire to
place HACCP on a more quantitative basis, ICMSF pro-
posed two general categories according to the risk that
contamination can occur. The terms, major and minor,
were selected for this purpose and are used throughout
Fig. 1-4.
Slaughtering process
In the first example, the slaughtering process for cattle,
sheep, goats, and horses is described from the point of
holding the live animals through chilling of the carcasses.
The slaughtering process in Fig. 1 lists three CCPs, only
one of which is a CCP1. The skinning and eviscerating
steps are major sites of contamination and if these proce-
dures are conducted in a correct manner, the degree of
contamination can be reduced. The chilling process was
assigned a CCP1 because this step is effective in restrict-
ing the growth of pathogens. At the time ICMSF Book 4
(7) was being developed, the significance of Listeria
monocytogenes was uncertain. The risk for growth of L.
monocytogenes during the chilling step remains unclear.
Roast beef
In Fig. 2, an example of a process for manufacturing
roast beef is outlined. Five CCPs are listed where the
control of hazards can be exercised. The cooking step is
listed as a CCP1 because meeting certain minimum time-
temperature requirements can assure the destruction of
enteropathogens (e.g. salmonellae). In this example, chill-
ing prevents the growth of surviving sporeformers, but the
method of chilling in the example cited involves immers-
ing the bags of cooked roast beef in cold water. This can
result in contamination through openings where defective
seals occur. The major site of contamination to the cooked
JOURNAL OF FOOD PROTFCTION, VOL. 53, SEPTEMBER 1990
799
Holding
Slaughtering
Skinning CCP2
Eviscerating • CCP2
Washing
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Chilling CCP1
o indicates a site of minor contamination
• indicates a site of major contamination
CCP1 effective CCP
CCP2 not absolute
Figure 1. Flow diagram for the slaughtering process for cattle,
sheep, goats, and horses.
product occurs when the bags are opened to drain away
excessive meat juices and the bags are resealed or a new
bag is applied. The general process outlined in Fig. 2 also
is applicable to certain poultry products.
Dry sausage
In Fig. 3, an example of a process for producing
fermented dry sausage is outlined. This example was
developed to discuss the control of salmonellae in a WHO-
ICMSF document (9). In that report, the destruction of
salmonellae was reviewed in terms of the wide variety of
products and processes used throughout the world. Within
this context, the fermentation step was considered a CCP2
for the control of salmonellae. The technology currently
exists for producing these products with a very high level
of confidence that salmonellae will be destroyed. This
technology includes applying appropriate controls over the
formulation, fermentation, and drying steps in the process.
In the course of applying this technology, traditional
characteristics of some varieties of dry sausage might change.
As mentioned in the criteria section, multiplication
and enterotoxin by Staphylococcus aureus can occur in
uncontrolled fermentations for dry and semi-dry sausage
production. This problem has been reported only in the
United States where higher fermentation temperatures have
been used more widely. Since this potential hazard can be
prevented with a high level of confidence, a CCP1 can be
800 TOMPKIN
Raw material
selecting o CCP2
Seasoning
Bagging
Cooking CCP1
Chilling CCP2
Rebagging CCP2
Storing and
distributing CCP2
o indicates a site of minor contamination
• indicates a site of major contamination
CCP1 effective CCP
CCP2 not absolute
• indicates a site of major contamination
Figure 2. Flow diagram for production of roast beef.
CCP2 not absolute
assigned to the fermentation step with regard to entero-
toxin production.
Canned hams for slicing
Figure 4 is an example of a process for producing
canned hams which are subsequently sliced and packaged
as sliced ham. In this example, the cooking process was
identified as the only CCP1. The time-temperature of heating
assures the destruction of nonsporeforming pathogens and
spoilage organisms. The degree of contamination occur-
ring during the slicing and packaging steps strongly influ-
ences the ultimate rate of spoilage of the packaged prod-
uct. The temperatures encountered during storing and
distribution also influence the shelf life. Slicing, packag-
ing, and storing/distributing are CCP2s because control
can be exercised, but absolute control cannot be assured.
Experience indicates that some contamination with spoil-
age flora will occur, and some degree of subsequent
temperature abuse is likely. The rate of spoilage of the
packaged product will be influenced by the degree of
contamination and the temperatures that will be encoun-
tered. The process outlined in Fig. 4 is generally followed
for producing many cooked, cured, and noncured poultry
JOURNAL OF FOOD PROTECTION, VOL. 53, SEPTEMBER 1990
Raw Meat •,
Salt, Dextrose/
Sucrose, Spices,
Nitrite and/or
Nitr_ate
Starter Culture
Blending
Stuffing
Fermentation
18-44°C CCP2
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Drying
Ageing
Packaging
Delivery
Figure 3. Flow diagram for production of fermented sausage.
products. One difference is that poultry products are normally
cooked in a casing or pouch rather than a metal container.
Adjusting conditions to reduce the risk of hazards
When manufacturers of ready-to-eat meat and poultry
products perform a hazard analysis, five factors within
their control should be considered for reducing the risk of
microbiological hazards (Table 6). First, the processing
procedure must be designed and controlled to eliminate
hazards whenever possible. Second, the characteristics of
a product should be modified to improve its microbial
stability during processing and during subsequent storage,
distribution, and use. Third, contamination must be pre-
vented between the time when products are processed (e.g.,
cooked) and when they are packaged. Fourth, appropriate
packaging design and labeling information should be used
to instruct consumers in proper handling of the product
(e.g., keep refrigerated). Fifth, a combination of as many
factors as possible should be used (10). Examples of product
characteristics (the second factor above) which can be
modified to reduce the risk of microbiological hazards are
listed in Table 7 (11).
 USE OF HACCP FOR MEAT AND POULTRY PRODUCTS 801

TABLE 7. Examples of product characteristics influencing the

Raw material microbial stability of ready-to-eat meat and poultry products.
selecting o CCP2 • Brine content or Aw
1 • Carbohydrate content
Injecting, • Acid content, pH
tumbling, o • Smoke (liquid or natural)
f illincr • Phosphate content
1 • Metal ion content (e.g., iron, manganese)
Cooking • Nitrite content
CCP1
• Microbial content of ingredients
1 • Browning of the product's surface (hot oil, flame)
• Seasonings added after processing
Chilling o CCP2 • Sodium lactate, potassium sorbate

1
1 Slicing, TABLE 8. Ten factors which help prevent the occurrence ofL.
packaging • CCP2 monocytogenes in cooked meat and poultry products.
1 • Obtain commitment from management.
Storing, • Use processes which destroy Listeria.

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distributing CCP2
o indicates a site of minor contamination
• indicates a site of major contamination
CCP1 effective CCP
CCP2 not absolute
Figure 4. Flow diagram for production of packaged sliced ham
from canned ham.
TABLE 6. Five steps to reduce the risk of microbiological hazards
in ready-to-eat meat and poultry products.
• Use a controlled process to destroy the vegetative cells of
pathogens and limit the growth of surviving sporeformers.
• Build safety into the product through changes in formulation
or processing.
• Prevent contamination between the time of processing and
packaging.
• Use appropriate packaging design and labeling information.
• Combine two or more of the above.
The use of HACCP for Listeria control
At the present time, no greater microbiological issue
faces the meat and poultry industry than that of the poten-
tial pathogen, L. monocytogenes. Table 8 summarizes ten
factors which can help prevent contamination of cooked
meat and poultry products with L. monocytogenes. HACCP
can be an effective system to control Listeria, but inade-
quate technology and the prevalence and characteristics of
L. monocytogenes combine to make it difficult to elimi-
nate this potential pathogen from the cooked product
environment of meat and poultry processing establishments.
For the present, a realistic assessment is that the control
of L. monocytogenes in the cooked product environment is
a CCP2. This assessment and recognition of the potential
severity of the hazard (i.e., listeriosis with a high rate of
fatality among certain segments of the population) means
• Separate raw meats from cooked products.
• Use cleaning and disinfection procedures designed for Listeria
control.
• Package cooked products in a clean, dry environment.
• Isolate and control wet processes involving cooked products
(e.g., peeling casings from linked product, removing cooked
product from metal molds).
• Properly design equipment to facilitate cleaning and minimize
areas for growth. Maintain equipment to minimize breakdowns
and risk of contamination during repair.
• Establish effective personal hygiene practices with the control
of Listeria as a major objective.
• Identify and implement procedures to control high risk situ-
ations (e.g., installation of new equipment on a packaging line,
new employee on sanitation staff).
• Establish a meaningful sampling program to verify control.
that greater effort must be applied to minimize the risk of
post-process contamination than has ever been applied,
heretofore, in this industry.
Additional information for the control of Listeria during
the production of ready-to-eat meat and poultry products
is available through the American Meat Institute (P.O.
Box 3556, Washington, DC 20007). The available infor-
mation includes a written guideline for Listeria control, a
video on equipment design, and a video for training
employees in proper hygiene practices.
THE FUTURE ACCEPTANCE OF HACCP
The concept of HACCP is applicable to a wide vari-
ety of problems which we face in our daily lives. It is,
after all, a common sense approach to preventing prob-
lems. In the case of food operations, technical knowledge
is required to anticipate and prevent problems. The HACCP
system requires the involvement of experts who must reduce
technical information to a form that nontechnical persons
can apply to their operation.
HACCP is the best system currently available for
improving the microbiological safety of food. It is not

JOURNAL OF FOOD PROTECTION, VOL. 53, SEPTEMBER 1990

802 TOMPKIN
unexpected that HACCP is being embraced by various
groups as a means to prevent foodbome illness. Will there
be long term acceptance of HACCP or will HACCP be
viewed as a fad and be rejected in the future? The follow-
ing are some issues that must be considered.
• There continues to be a nonuniform understanding of
HACCP both domestically and internationally. The intent
of ICMSF Book 4 is to describe the HACCP concept
and encourage its use to improve the microbiological
safety and quality of foods. The definitions and prin-
ciples evolved from extensive debate over a period of
several years. Whether future efforts by others will result
in documents which are in agreement with ICMSF Book
4 (7) remains to be seen.
• There is a misunderstanding or an unrealistic expecta-
tion that the application of HACCP will prevent all
problems. This is, in part, due to a failure to recognize
or accept the reality that only partial control of a hazard
is possible at certain CCPs (i.e., CCP2). The current,
revised ICMSF definition for CCP reflects this concern.
• The "expert" can be a weak link in the system. The fact
that several experts will often provide different opin-
ions raises questions of credibility and confidence in
the overall system.
• Most outbreaks of foodbome illness are due to errors in
homes and food service establishments. Can the HACCP
concept be effectively incorporated into the educational
process for food handlers in these situations?
• Will the acceptance of HACCP result in decreased foo-
dbome illness? If not, will the failure be assigned to
inadequacies of HACCP as a system for prevention or
to improper implementation of HACCP.
• How much time will be required to train inspectors and
industry personnel with one common understanding of
HACCP? How long will it take to convert to a HACCP
based control system, including the adoption of new
HACCP based regulations? Will HACCP survive this
transition period? Perhaps, the educational process and
procedures for implementation should be subjected to
HACCP to assure a smooth, timely transition.
• Can HACCP be incorporated into state and federal regu-
lations? HACCP deals with the uniqueness of each op-
eration, whereas, regulations tend to be generic in scope.
• Will HACCP be accepted by food inspectors and the
public? Under a HACCP based control system, the focus
and method of inspection will change from traditional
methods. Inspections might be limited to certain as-
pects of a food process. Without a certain amount of
freedom to inspect other areas, this can lead to a per-
ception that HACCP results in reduced inspection and
loss of regulatory control even though the intent of
HACCP is just the opposite.
• The acceptance of HACCP requires some degree of
mutual trust between the regulator and the regulated.
Can this be resolved to the satisfaction of both parties
and the public?
• HACCP requires that processors assume greater respon-
sibility for assuring control, thus leaving regulators with
JOURNAL OF FOOD PROTECTION, VOL. 53, SEPTEMBER 1990
a greater emphasis on verification. The impact of this
change would be greatest in USDA inspected facilities.
• Verification is one aspect of HACCP. Thus, end-prod-
uct testing is performed when appropriate. Producer-
buyer and producer-regulator disagreements over end-
product testing will not disappear with the adoption of
HACCP. Differences of opinion will exist over the degree
to which HACCP can replace the need for end-product
testing. This will be an issue for foods in both domestic
and international commerce.
• Even with the acceptance of HACCP, it is predicted
that the historical debate over microbial criteria (num-
bers and types of microorganisms) will continue. The
debate, however, will expand to include hazards, risks,
CCPs, monitoring, and the ability to control at certain
CCPs. Will this encourage or hinder the adoption of
microbiological criteria?
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• The application of HACCP to numerous nonsafety issues
(e.g., net weight) can result in a complex system in
which the focus on safety is lost. This dilutes the value
of HACCP as a system for assuring the control of hazards
that are of the greatest severity. This lack of focus
increases the likelihood that limited resources will be
diverted from controlling CCPs of greatest concern to
safety. For this reason, some have proposed that HACCP
be limited to safety issues. For example, a formal
"HACCP Plan" might need to be developed as a regu-
latory requirement for assuring safety. Yet, the HACCP
concept remains the best approach to assuring consis-
tency and preventing major problems of all kinds (e.g.,
spoilage). HACCP is a powerful tool which should be
used for preventing all problems where the potential
hazards have a high degree of severity.
• Control systems continue to evolve. While HACCP is
now being considered for adoption on a fairly wide
scale, will a newer, better system be developed in the
future? Is HACCP the system for beyond the year 2000?
REFERENCES
1. American Meat Institute. 1989. Good manufacturing practices. Fer-
mented dry and semi-dry sausage. American Meat Institute, Arling-
ton, VA.
2. American Public Health Association. 1972. Proceedings of the 1971
National Conference on Food Protection. U.S. Government Printing
Office, Washington, DC.
3. Bryan, F. L. 1978. Factors that contribute to outbreaks of foodbome
disease. J. Food Prot. 41:816-827.
4. Bryan, F. L. 1980. Foodbome diseases in the United States associated
with meat and poultry. J. Food Prot. 43:140-150.
5. Bryan, F. L. 1988. Risks associated with vehicles of foodbome patho-
gens and toxins. J. Food Prot. 51:498-508.
6. Davey, G. R. 1985. Food poisoning in New South Wales: 1977-84.
Food Technol. Australia. 37:453-456.
7. International Commission on Microbiological Specifications for
Foods. 1988. Microorganisms in foods. 4. Application of the hazard
analysis critical control point (HACCP) system to ensure microbio-
logical safety and quality. Blackwell Scientific Publications, London.
8. Roberts, D. 1982. Factors contributing to outbreaks of food poisoning
in England and Wales 1970-1979. J. Hygiene 89:491-498.
9. Simonsen, B., F. L. Bryan, J. H. B. Christian, T. A. Roberts, R. B.
Tompkin, and J. H. Silliker. 1987. Prevention and control of food-
 USE OF HACCP FOR MEAT AND POULTRY PRODUCTS gfj3

borne salmonellosis through application of Hazard Analysis Critical
Control Point (HACCP). Int. J. Food Microbiol. 4:227-247.
10. Tompkin, R. B. 1986. Microbiological safety of processed meat: new
products and processes - new problems and solutions. Food Technol.
40(4):172-176.
11 Tompkin, R. B. 1986. Microbiology of ready-to-eat meat and poultry
products, p. 89. In A. M. Pearson and T. R. Dutson (ed.s) Advances
in meat research, volume 2. Meat and poultry microbiology. The AVI
Publishing Co., Westport, CT..
12. United States Department of Agriculture. 1987. Meat and Poultry In-
spection Regulations, Part 318.10. Prescribed treatment of pork and
pork products to destroy trichinae. U.S. Department of Agriculture,
Washington, DC.
13 United States Department of Agriculture. 1987. Meat and Poultry In-
spection Regulations, Part 318.17. Requirements for the production of
cooked beef, roast beef and cooked corned beef. U.S. Department of
Agriculture, Washington, DC.
14. World Health Organization/International Commission on Microbio-
logical Specifications for Foods. 1982. Report of the WHO/1CMSF
meeting on hazard analysis: critical control point in food hygiene.
Document VPH/82.37. World Health Organization, Geneva.

Korkeala et al., con't. from p. 794

Downloaded from http://jfoodprotection.org/doi/pdf/10.4315/0362-028X-53.9.795 by guest on 06 March 2020

whose thermoresistant isolate was able to grow at a
temperature 4.2°C higher than the parent strain.
According to the present results, the maximum growth
temperature of lactobacilli seems not to be a stable char-
acter. The same was also found by Stahl and Olsson (8),
who have reported facultatively and obligatively thermo-
philic variants in mesophilic Bacillus megaterium strains.
However, the significance of this interesting phenomenon
is not known and needs further study.

ACKNOWLEDGMENTS

We wish to thank Ms. Mirja Eerikainen and Ms. Johanna Seppala for
their excellent technical assistance. This study was supported by the
Academy of Finland and the Technology Development Centre of Finland.

REFERENCES

Junttila, J. R., S. I. Niemela, and J. Hirn. 1988. Minimum growth tem-

Figure 1. The boundary of the maximum growth (38.4° C) of the
Lactobacillus strain A210 (A) and the respective boundary (39.3°C)
of its thermoresistant isolate (B). The thermoresistant isolate
was obtained from the colony at 39.3°C marked by the arrow
(A). The temperature gradient in both runs was the same.
strains except for strain Al. Strain Al may be earlier selected
to tolerate a higher temperature. The greatest increase in
maximum growth temperature was found for strain CI,
peratures of Listeria monocytogenes and nonhaemolytic listeria. J.
Appl. Bacteriol. 65:321-327.
Korkeala, H., and P. Makela. 1988. Tyhjiopakattujen lihavalmisteiden
limaantuminen sailytyksen aikana. (Ropy slime formation in vacuum-
packed meat products during storage). Suom. Elainlaakaril. 94:292-
294.
Korkeala, H., T. Suortti, and P. Makela. 1988. Ropy slime formation in
vacuum-packed cooked meat products caused by homofermentative
lactobacilli and a Leuconostoc species. Int. J. Food Microbiol. 7:339-
347.
Niemela, S. 1. 1987. Temperature-gradient incubator, GradiplateR W10.
User's guide. Biodata Oy, Helsinki.
Reuter, G. 1970. Laktobazillen und eng verwandte Mikroorganismen
in Flcisch und Fleischerzeugnissen. 2. Mitteilung: Die Charaktcrisi-
erung der isolierten Laktobazillenstamme. (Lactobacilli and closely
related micro-organisms in meat and meat products. 2. Characterisation
of isolated lactobacilli strains). Fleischwirtschaft 50:954-962.
Reuter, G. 1975. Classification problems, ecology, and some biochemi-
cal activities of lactobacilli of meat products, pp. 221 -229. In J. C. Can,
C. V. Cutting, and G. C. Whiting (eds.), Lactic Acid bacteria in bev-
erages and food. Academic Press, London and New York.
Reuter, G. 1982. Psychrotrophic lactobacilli in meat products, pp. 254-
258. In T. A. Roberts, E. Hobbs, J. H. B. Christian, and N. Skovgaard
(eds.), Psychrotrophic microorganisms in spoilage and pathogenicity.
Academic Press, London.
Stahl, S., and O. Olsson. 1977. Temperature range variants of Bacillus
megaterium. Arch. Microbiol. 113:221-229.

JOURNAL OF FOOD PROTECTION, VOL. 53, SEPTEMBER 1990