Meat Science 66 (2003) 33–43

www.elsevier.com/locate/meatsci

Microbiological safety standards and public health goals

to reduce foodborne disease
Ewen C.D. Todd*
National Food Safety & Toxicology Center, Michigan State University, East Lansing, Michigan, USA

Received 10 November 2002; accepted 22 December 2002

Abstract
Even though microbiological standards have been promulgated for many decades, their utility has sometimes been questioned,
and this is one reason that performance standards associated with programs like HACCP in processing plants and now in other
food industries have been espoused. The public has an increasing concern over food safety and perceives a zero tolerance policy (i.e.
no pathogens in a sample of food) and strict enforcement with punitive consequences for failure to comply is the answer to making
food safer. At present, there is no clear connection between government policy and a reduction in foodborne illness. Although
national disease statistics may show gradual declines over long periods for some pathogens associated with food, other problems,
including new pathogens, tend to emerge. International bodies and some governments, however, are increasingly considering
adopting a risk-based approach to managing a food supply, with the potential for introducing the Acceptable Level of Protection
(ALOP) and Food Safety Objectives (FSOs) concepts. These make it possible to see a connection between a goal for disease reduction
and what industry must do to accomplish this with specific objectives through performance standards and microbiological testing.
However, it may not be easy to apply this approach for all types of industries and pathogens and in developing countries.
# 2003 Elsevier Ltd. All rights reserved.

1. Introduction much better job on enforcement, and they need better

Microbiological food safety standards have been
around for a long time but reasons for their develop-
ment and the differences between countries and jur-
isdictions lead to ambivalence to them by industry and
trading countries. There is an underlying assumption
that these need to protect the public by reducing the
contamination level of pathogens in raw meats and
poultry even if they are not completely eliminated. But
there is little apparent connection between public health
goals (if they exist) and standards or guidelines except in
a general way of reducing or limiting contamination.
Opinions vary from having more standards, testing and
enforcement on the one hand, to letting the industry
control itself. Since some standards have been around
for decades, is it simply a matter of poor oversight by
government and industry? Senator Tom Harkin’s com-
ment reflects this viewpoint. ‘‘Report after report gives
us the same result—our food safety laws are not being
effectively enforced. USDA and FDA need to do a
enforcement tools’’ (Anon, 2002b). Harkin has also sup-
ported a bill for Safe and Fair Enhancement and Recall
for Meat, Poultry, and Food Act (SAFER Meat, Poul-
try, and Food Act) (Kernellu, 2002b). The bill would:
1. Require any person, other than the consumer, to
report to the federal government any food that
the person has reason to believe is adulterated or
misbranded.
2. Authorize the federal government to order
mandatory recall of any violative food upon
receipt of such notice or by other means, if there
is a reasonable probability that consumption of
the food would present a threat to public health.
3. Authorize huge civil money penalties for viola-
tion of any federal rules; and
4. Authorize withdrawal of inspection from meat
and poultry establishments upon more than one
willful violation of even minor rules under the
meat or poultry inspection acts.

* Fax: +1-517-432-2310. William D. Marler, a trial lawyer who specializes in

E-mail address: toddewen@cvm.msu.edu (E.C.D. Todd). winning large settlements for E. coil 0157:H7 victims
0309-1740/03/$ - see front matter # 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0309-1740(03)00023-8
34 E.C.D. Todd / Meat Science 66 (2003) 33–43
also focuses on enforcement to reduce meat-borne dis-
ease (Marler, 2002):
1. Hire more inspectors and give them real
authority to sample meat and stop its distribu-
tion as soon as a pathogen is detected;
2. Implement a scientific sampling system that
provides a reasonable chance of preventing out-
breaks;
3. Have a clear line of responsibility whenever a
food product needs to be promptly recalled;
4. Establish a trace-back program to document
where specific lots of food are sold, so they can be
recalled quickly if a pathogen is detected;
5. Merge the two federal agencies responsible for
food safety—USDA’ s Food Safety Inspection
Service (FSIS) and the inspection arm of the
FDA.
These comments probably typify the public’s attitude
to food safety—enforce the regulations and make the
industries comply to producing food with no dangerous
organisms present. However, is enforcement the most
effective solution? Or even more importantly, are there
direct relationships between enforceable standards and
reduction of illness? In one specific issue, is mandatory
HACCP for pathogen reduction in poultry plants effec-
tive or not in reducing human salmonellosis? There have
been standards for years and outbreaks still occur.
Routine testing does not guarantee absence of patho-
gens, and governments have limited resources to do
these effectively, but at least the results are available to
the public, as well as to industry and government policy
makers to observe trends. In this paper, I will show that
there can be a relationship established between reduc-
tion of human illness and achievable objectives or tar-
gets in processes or products, even if it is still in the
formative stages.
2. Current public attitudes to food safety and stan-
dards
Attitudes to food safety and enforceable standards
change over time and differ from country to country
and even within a country. In a recent survey in Europe
1000 consumers in France, Germany, the UK, Italy and
the Netherlands were interviewed by telephone and
asked which factor had the greatest adverse effect on
health (Harris, 2002c). Smoking, drinking, stress and
environmental pollution were identified as the most
important. Only 11% considered food safety as a major
factor (from 17% in Italy to 5% in the Netherlands). It
was argued by the Dutch Meat Board that the low
concern by the Dutch consumers reflected the con-
fidence they had in the Dutch food safety standards. In
contrast, in May 2002, a survey of 10 countries (only
two were European) showed that most were somewhat
or very concerned about food safety (Anon., 2002a).
This level of concern ranged from 99% in India to 76%
in Germany. Over 90% of respondents in China, Brazil,
Japan, Mexico, USA and Canada were concerned. For
all 10 countries together, the most important food issue
was food safety (43%), followed by nutrition (25%),
prices (13%), taste/appearance (9%), and food shorta-
ges (8%). Specific issues included agricultural inputs
(animal disease, pesticides, air, water and soil pollution,
antibiotics and hormones and genetically modified
foods), food processing, sources of contamination and
irradiation. From a USDA annual food survey, 80% of
American households now report cooking their home-
made burgers until they are brown or well done, an
increase from 76% in 1991; it was indicated that cook-
ing habits changed upon hearing about meat recalls and
associated illnesses, and not so much from safe handling
labels on meat (Gay, 2002; Harris, 2002b).
Clearly, there are divergent views on the importance
of food safety but this may depend on the way the
questions are put and perceived. From the above infor-
mation, for most consumers there appears to be a lack
of trust in the producers and controlling agencies to
have safer food, and only some of the issues relate to
pathogens. Perhaps one of the reasons for this is that
the public does not see a clear connection between gov-
ernment policy and a reduction in foodborne illness,
although there have been several initiatives in making
food safer for consumers over the last decade or more.
Specifically, microbiological standards are rarely dis-
cussed at the public level unless there is a zero tolerance
policy for particular pathogens, which fits well with the
public’s general perception that producers should pro-
vide food at minimal risk (CSPI, 2002; S.T.O.P., 2002)
even if the consumer may abuse it afterwards.
3. Current microbiological standards
A microbiological criterion is designed to find a food
product acceptable, based on the absence or presence, or
the number of microorganisms, and/or the quantity of
their toxins/metabolites, per unit of mass, volume, area or
food lot (Codex definition, FAO, 2001). A micro-
biological criterion should state the reason for having a
standard for the microorganism of concern, list the meth-
od(s) for detection or quantification of the microorgan-
ism, indicate the number of samples, method of sampling,
and size of analytical unit, identify the microbiological
limits considered appropriate at specified points in the
food chain, and the number of analytical units to conform
to these limits (Codex Definition). Any actions when a
criterion is not met should also be stated. Criteria can be
established for several reasons (ICMSF, 2002).
 E.C.D. Todd / Meat Science 66 (2003) 33–43
1. Utility (economic, aesthetic): general con-
tamination, incipient spoilage, reduced shelf-life;
2. Indicator: indirect indicators of pathogens, e.g.
generic E. coil; indicative of good cleaning pro-
cedures, e.g. Listeria innocua for L. mono-
cytogenes; sporeformers in low acid canned foods
for underprocessing; coliforms after processing
for recontamination; S. aureus in processed foods
indicative of human skin contact; verification of
GHP/HACCP;
3. Pathogen: conformity to standards; investigation
of outbreaks; routine testing; verification of
GHP/HACCP.
All three types are found in national standards but
those involving pathogen detection or enumeration have
the greatest impact for trade and potential for recalls.
ELISA, PCR, biosensor methods are being considered
more as screening tools and for industry applications,
but government policy usually requires isolates for tak-
ing any regulatory action. This is unlikely to change
soon, since governments typically require isolates for
such reasons as legal purposes. A lot of food can be
tested for a number of reasons as well as meeting a
specific microbiological standard, such as involvement
of a food in an outbreak or similar foods to the one
implicated; foods intended for specific high risk popu-
lations, e.g. homes for the aged, AIDS patients, astro-
nauts; food lots with a record of previous
contaminations; exporting companies and countries
with inadequate inspection programs; and base-line sur-
veys for setting guidelines or standards by government
agencies. The media or public health interest groups
may commission surveys to demonstrate a concern.
Industry testing for contractual agreements is probably
where most analysis is done, but these results are con-
fidential; occasionally an industry association will poll
its members or conduct a specific study to respond to
government or public concerns and release the results.
4. Examples of microbiological standards
The number of standards varies considerably between
countries and no one country has microbiological stan-
dards for all commercial foods. The following are some
examples that demonstrate utility, indicator and patho-
gen criteria in some meat products.
4.1. Safely standards
In South Africa (1997) standards for gelatin and
cooked poultry are as follows.
Edible gelatin: Total bacterial count < 1000/g, E. coil
and Clostridium spp. absent in 0.1 g, Salmonella absent
in 1 g.
35
Cooked poultry: no antimicrobials that exceed gov-
ernment maximum limits, total bacterial count
< 10 000/g, absence of Salmonella, Shigeila, C. perfrin-
gens, S. aureus and E. coli in 20 g.
In Japan, there are standards for dry meat products
(aw < 0.87), unheated meat products (smoked or salted
and dried), heat pasteurized meat products, specified
meat products (pasteurized by other than 63
C for 30
min): no Salmonella, E. coli negative to not more than
100 cfu/g, S. aureus and Clostridium spp. not more than
1000 cfu/g (Japan, 1959).
In Iceland, standards for both raw and cooked meat
products have different minimum and maximum levels
of plate count, coliforms, faecal coliforms, S. aureus,
suiphite-reducing clostridia, Bacillus cereus, and absence
of Salmonella and Shigella (Environmental and Food
Administration, Director General Hermann Sveinb-
jornsson, PO Box 8080, IS-128 Reykjavik, Iceland, per-
sonal communication).
In the United Kingdom and Ireland 17 RTE meat
products have to satisfy aerobic plate count criteria, as
well as absence of Salmonella, Campylobacter spp., E.
coli O157:H7 and other VTEC in 25 g, and low numbers
of Listeria monocyto genes, S. aureus and C. perfringens.
The action levels are 4 fold: satisfactory, borderline
limit of acceptability. unsatisfactory, unacceptable
potentially hazardous (Gilbert et al., 2000).
In Argentina, 274 samples of a wide variety of foods
including meats from 19 different shops were analyzed.
From data recorded in the good quality shops (GMP
Class I) it was proposed that maximum aerobic colony
counts for cooked ready-to-eat foods should be 105cfu/g
(De Sousa, Tamagnini, Olmos, & Gonzalez, 2002).
EU standards for minced meat and meat preparations
(Anon., 2001) use the 2- and 3-class attribute plan sys-
tem developed by the International Commission for
Microbiological Specifications for Foods (ICMSF,
2002), where no 10- or 1-g sample in the 5 taken (n) can
contain Salmonella, but some samples are allowed to
contain generic E. coli and S. aureus as well as sub-
stantial numbers of aerobic mesophilic bacteria. For
example, for meat preparations 2 (c) of 5 (n) samples
can contain up 500 E. coli/g (m) but no more than 5000
Table 1
EU microbiological meat standards
Meat products n c m M
Minced meat
Salmonella absent in 10 g 5 0 – –
E. coli 5 2 50 per g 500 per g
S. aureus 5 2 100 per g 1000 per g
Aerobic mesophilic bacteria 5 2 500000 per g 5000000 per g
Meat preparations
Salmonella absent in 1 g 5 0 – –
E. coil 5 2 500 per g 5000 per g
S. aureus 5 1 500 per g 5000 per g
36 E.C.D. Todd / Meat Science 66 (2003) 33–43
Table 2
Australian and New Zealand microbiological prepared meat standards
Meat products
Packaged cooked cured/salted meat
Salmonella and Listeria monocytogenes absent in 25 g
S. aureus
Packaged heat treated meat paste and packaged heat treated pate
Salmonella and Listeria monocyto genes absent in 25 g
Fermented, comminuted meat which has not been cooked
Salmonella absent in 25 g
E.coli
S. aureus
E. coli/g (M) (Table 1). The Australian and New Zeal-
and standards are similar but not identical (Table 2).
4.2. Microbiological criteria as HACCP verification
checks
In the EU there was a decision (EU microbiological
criteria, 2001) requiring operators of abattoirs and meat
cutting establishments to apply the HACCP (hazard
analysis critical control point) principles and to carry
out microbiological checks for more effective risk man-
agement using a 3-class plan approach (Table 3). These
are a measure of hygiene (total viable counts and
Enterobacteriaceae counts) rather than specific patho-
gen detection. The Enterobacteriaceae are not usually
considered an indicator of pathogen presence since there
are many species in this family that are not associated
with human or animal gut flora.
4.3. Zero tolerance
Zero tolerance standards generate considerable
debate because they are considered overbearing for
national industries and importing countries. One such
standard is zero tolerance for it>/it> that applies only
to a few countries. For instance, in Australia and New
Zealand, there should be no L. monocytogenes in 525-
g samples of packaged cooked, cured or salted meat or
heat-treated meat and pâté (Food Standards, Australia,
New Zealand, 2002). However, the greatest debate over
the effectiveness of such a standard has occurred over
the US Zero Tolerance Policy that was developed in
1989, partly as a result of a large outbreak of listeriosis
arising from Hispanic style cheese (Ryser & Marth,
Table 3
EU HACCP verification: daily log mean values for cattle, sheep, goats
and horses
Daily log mean values Acceptable Marginal range Unacceptable
(cfu/cm2) range ( >m but 4M) range (> M)
Total viable <2.8 2.8–4.3 >4.3
Enterobacteriaceae <0.8 0.8–1.8 >1.8
n c m M
5 0 – –
5 1 100 per g 1000 per g
5 0 – –
5 0 – –
5 1 0 –
5 1 1000 per g 10000 per g
1999). If the pathogen is found in RTE products,
including meats, in either of two 25-g samples of a food,
the product is considered unadulterated, and usually a
voluntary recall is initiated, whether the origin of the
food is domestic or imported (Shank et al., 1996).
Between 1989 and 1993, the rate of illness from L.
monocytogenes declined 44%, but there was an increase
in 1998 because of a large outbreak (CDC, 1999).
Another large outbreak occurred in 2002, with an asso-
ciated large recall (Anon., 2002c). In addition, it is esti-
mated that there are about 2500 cases and 500 deaths
estimated each year from listeriosis in the United States
(Mead et al., 1999). All this information indicates that
the current policy is only partially effective. If all con-
sumer meals of RTE foods contained no L. mono-
cytogenes, there should be no illnesses, assuming all
listeriosis is foodborne from RTE foods. Clearly,
although the policy may reduce contamination, it does
not eliminate it. The reasons may be multiple: industry
does not test RTE foods at processing because a posi-
tive result would mean an automatic recall; industries
check the product but do not report positive findings;
government testing is by nature limited and thus some
RTE foods sold in the US may contain low levels of the
pathogen; raw ingredients may be contaminated or
occasionally errors occur in processing plants so that
the product is sufficiently contaminated that sporadic
cases or outbreaks occur; the organism grows well in
some RTE foods under refrigerated conditions if stored
for many days, and thus consumer practices may deter-
mine the level of L. monocytogenes consumed. The
actual number of cases even in a country like the USA is
not known, because surveillance for sporadic cases of
listeriosis is difficult to carry out effectively since symp-
toms are not distinctive, physicians rarely take clinical
specimens for analysis, and clinical laboratories do not
routinely look for the organism. Invasive listeriosis is
much more likely to be detected than listerial gastro-
intestinal illness, since the former cases are usually hos-
pitalized (FDA/FSIS/CDC, 2001). The best available
US data are based on studies conducted at FoodNet
sites (Mead et al., 1999). Although it is normally recog-
nized that relatively high levels of the pathogen are
 E.C.D. Todd / Meat Science 66 (2003) 33–43
required for illness—some of the population would be
sufficiently immunocompromised, including pregnant
women to be infected with lower doses (FDA/FSIS/
CDC, 2001). This zero tolerance policy has been ques-
tioned by many countries and the US industry as unat-
tainable, increasing production costs, limiting trade,
with minimal benefit to public health. It also curtails
industry’s willingness to test for the pathogen. Listeria
policies in other countries vary in their approaches. In
Canada, categories for action are based on RTE foods
with a history of outbreaks, supporting growth or not,
storage for more or less than 10 days, and with action
levels of absence to 100 cfu/g (Farber & Peterkin, 2000).
In Denmark, there are six categories of foods, with
action levels of 10–100 cfu/g, and in Germany there are
four categories of foods, with action levels of 100 cfu/g
to 10 000 cfu/g (FAO, 1999; Farber & Peterkin, 2000).
United Kingdom legislation only applies to dairy pro-
ducts. Incidence rates in countries not having a zero
tolerance policy do not seem to be higher than the few
that do, including the USA and Australia (Ross, 2003).
In summary, approaches to setting of microbiological
standards vary considerably from country to country.
Some have many standards, others few; some standards
are for pathogens, others for indicator organisms; the
action levels vary from zero tolerance to differing
amounts of pathogen but these amounts vary between
countries (e.g. Tables 1 and 2). For some countries, E.
coli O157:H7 is specified whereas in the UK and Canada
it is VTEC (verotoxigenic E. coli). VTEC is not the same
as E. coli 01 57:H7 or enterhaemorrhagic E. coli, but
identical to Shiga-like toxigenic E. coli, a term does not
appear in other microbial standards. The foods to which
the standards apply do not necessarily have the same
descriptions and there is usually no background to give
the rationale. How standards were decided within coun-
tries. Were these based on scientific studies or expert
opinion? Were any kinds of survey studies of pathogens
and/or indicator organisms in different meat commod-
ities done to establish a baseline level to know to what
extent the industry has to improve? There are differences
in analytical methods and sampling plans. Were stan-
dards ‘‘lifted’’from those of other countries without
consideration of local situations? Have some standards
been in place as a result of a crisis decision taken decades
ago and not revisited? Were any stakeholders involved in
the process? How strong is the industry and/or consumer
lobby in a country to bring pressure on governments to
create, modify or drop standards? These questions are
often difficult to determine because of lack of transpar-
ency in the standard-setting process, but probably few
have been developed through a rational scientific process
relating to some kind of targeted public health goal for a
pathogen, save a general one of reducing the associated
illness. The use of risk assessment is a key component of
the rational approach and these are now starting to be
37
(FAO/WHO, 2001; FDA/FSIS/CDC, 2001; ICMSF
1998).
Enforcement approaches vary, and this can be a
source of concern, as illustrated by the remarks of Har-
kin and Marler (Anon., 2002b; Kernellu, 2002b; Marler,
2002). Another issue is perceived unfair trading prac-
tices. For example, European farmers are complaining
they are subject to the highest standards in the world on
environment, veterinary, food safety and animal welfare
requirements, but imported meat and chicken products
from developing countries are subject only to sporadic
testing by the EU and these farmers think that some
countries like the USA continue to maintain bans on
imports due to supposedly science-based reasons, even
though they are seen as trade issues (Harris, 2002b,
2000d).
5. Limits of microbiological testing
E.coli O157:H7 or Salmonella may not be good can-
didates for verifying process control because they are
not uniformly distributed, their numbers are usually too
low for quantitative recovery, and rapid and inexpen-
sive methods for their recovery are not readily available.
Although governments may respond to political pres-
sure to carry out surveys of meat and poultry products,
finding a positive sample is serendipitous. Some pro-
cessors/packers test for the presence of E. coli 01 57:H7
and other pathogens to meet certain purchase specifica-
tions in contractual agreements or to meet export
requirements. However, industry or government testing
programs for E. coli O157:H7 do little to assure the
safety of the finished product. For example, if the pre-
valence of E. coli 01 57:H7 (or any other pathogen) is
1% in a combo of ground meat that is to be used to
make a lot of hamburgers, then 300 hamburgers from
that lot would have to be analyzed to be 95% confident
that E. coli O157:H7 is absent (ICMSF, 1997). Neither
government nor industry wants to expend resources on
routine testing of these kinds of multiple samples. In
2002, the USDA will require that all federally inspected
plants handling raw beef products have an intervention
step built into their Hazard Analysis Critical Control
Point (HACCP) programs, including ground beef, non-
intact beef destined for grinding and intact beef trim-
mings destined for grinding, and that FSIS review all
such plant’s HACCP plans to ensure compliance.
beginning 60 days after the requirement is published for
large plants; 90 days for small plants; and 120 days for
very small plants. Recently FSIS has recognized that E.
coli O157:H7 is present more frequently on meat than
previously thought, based on a draft risk assessment
and more sensitive analytic methods (USDA, 2002). It is
now requiring beef plants to reassess their HACCP
plans and the effectiveness of the CCPs in controlling E.
38 E.C.D. Todd / Meat Science 66 (2003) 33–43
coli 0157:H7 with mandatory verification testing for E.
coli 0157:H7 in slaughter and deboning operations, in
addition to the existing requirements for raw beef
grinding establishments. Plants have to demonstrate
that a food safety hazard is not reasonably likely to
occur. When an E. coli 0157:H7 positive is found, more
extensive sampling by FSIS of suppliers will occur,
including sampling of trim. All lots made with the same
raw materials from a single source are implicated by a
positive finding unless the plant has scientific reasons to
treat lots separately. In addition, there is a request for
grinders to avoid mixing raw materials from different
grinders so as to make a trace-back to source easier if E.
coli O157:H7 is found in a sample. All this is to reduce
the frequency of contamination in meat reaching the
retailer. It does not relate directly to a targeted reduc-
tion of disease caused by E. coli 0157:H7, especially as
meat is only one food vehicle transmitting the pathogen,
and therefore any decline in disease statistics cannot be
automatically attributed to this program.
In another example, USDA set the criteria for its
Salmonella Performance Standard for HACCP (USDA,
1996) for meat based on three separate surveys. These
surveys show that their baseline data indicate that dif-
ferent levels of Salmonella and E. coli are expected on
carcasses of hogs, beef cattle, and dairy cows (Table 4).
This approach has been criticized by Brown et al. (2000)
and Gill (2001). They ask what the basis is for the tol-
erance for Salmonella in ground beef being higher than
for beef or cow carcasses? Although it may be true that
the contamination level is higher, should a higher toler-
ance be permitted? The conclusion that pathogens are
less hazardous on some animals than others ‘‘is simply
ridiculous’’, and that these criteria were set not on the
risks to consumers (based on a risk assessment) but on
limited survey data. They continue to argue that since
pathogens are only rarely found on raw meat, counts of
indicator organisms with a log normal distribution are
preferable for establishing a baseline level, since dis-
tributions for these are more predictable than for
pathogens. Even though generic E. coli counts cannot
predict when E. coli 0157:H7 may be present, variation
from such a distribution at different steps in a process
can be seen as a contamination problem that needs rec-
Table 4
USDA Salmonella performance standard for HACCP
Product Percent No. of Maximum
positive for samples allowable
Salmonella tested (n) positives (c)
Steers/heifers 1.0 82 1 Under the GATT/SPS Agreement, SPS measures
Cows/bulls 2.7 58 2 based on appropriate standards, codes and guidelines
Ground beef 7.5 53 5 developed by Codex Alimentarius are deemed necessary
Hogs 8.7 55 6 to protect human health. But are existing micro-
Fresh pork sausages 30.0 53 18
Broilers 20.0 51 12
tifying at the particular steps. For example, Gill and
McGinnis (2000) showed that E. coli cfu/100 cm2 (25
samples) increased from 1.45 to 4.80 logs from carcass
to collection of trimmings in tubs. Brown et al. (2000)
and Gill (2001) argue that proper survey data with dis-
tributions can allow Food Safety Objectives (FSOs) to
be set based on the best performances achieved, and for
beef products, FSOs for indicator organisms were con-
sidered preferable to those for pathogens. A FSO is a
statement of the maximum frequency and/or concen-
tration of a microbiological hazard in a food at the time
of consumption that provides the appropiate level of
protection. HACCP performance should be related to
these FSOs, not small sample 2-class attribute plans
(presence or absence only). The Subcommittee on
Microbiological Performance Standards for Raw Meat
and Poultry Draft Recommendations to USDA (Ker-
nellu, 2002a) recommended that data collected by
USDA to verify a plant’s HACCP system should not be
used to develop a performance standard for Salmonella
in ground beef. USDA should conduct another nation-
wide, federally inspected plant microbiological survey
for each raw ground product of interest designed to
provide statistically unbiased estimates of the true pre-
valence of bacteria of concern over 12 consecutive
months, and be stratified by plant size, production by
volume, month and region. The Subcommittee draft
report states it is still not known if HACCP standards
help protect consumers from foodborne illnesses. The
Report continues to note that not all foodborne disease
cases have dropped with the onset of performance
standards, and in fact, in 2002, CDC found that some
foodborne infections increased or did not change sub-
stantially (GAO, 2002; Vugia et al., 2002). However, a
risk assessment approach could be valuable in helping
achieve public health goals; one example is a FAO/
WHO risk assessment that showed that a reduced pre-
valence of Salmonella-infected broiler flocks is directly
proportional to a reduction in human infections from
poultry (FAO/WHO, 2001), if it is possible to distin-
guish between illnesses arising from Salmonella in poul-
try and those from Salmonella in other foods. The
Subcommittee challenged the food industry to be inno-
vative with new technologies to be more effective, and
they plan to be thinking through alternatives to current
performance standards.
6. Which comes first—the standard or the policy?
biological standards appropriate or adequate to protect
health? From the USDA FSIS Policy on E. coil
 E.C.D. Todd / Meat Science 66 (2003) 33–43
O157:H7 as an Adulterant (USDA, 1998) as developed
a nationwide sampling program in federally inspected
plants and retail stores that process ground beef, a
mandatory implementation of HACCP and testing for
bacteria in plants that slaughter and grind meat and
poultry, and increased funding for food safety research
to detect E. coil O157:H7. Although these seem to be
positive actions, in respect to a food safety issue, it is
hard to show that these directly relate to reduction of
haemolytic uraemic syndrome or infection with the
pathogen in the US (Kernellu, 2002a). In Canada, the
Health Canada Raw Foods of Animal Origin Policy
uses the level of generic E. coil as indicative of the extent
of faecal contamination and hence an indicator of
increased potential risk even if the relationship is not
linear (Health Canada, 2000a, 2000b; Todd, 2000). A
13-month Canadian Redmeat Baseline Study for Total
Plate Counts and generic E. coli in several thousand
samples is currently being carried out (Z. Nanjee,
Canadian Food Inspection Agency, Ontario, personal
communication), and will demonstrate what industry is
currently capable of doing in terms of hygiene, but does
not attempt to relate these to human illness levels.
7. Public health goals
Public health goals have traditionally been the
ALARA type (as low as reasonably achievable), where
management focuses on existing strategies, such as
industry reaching some degree of a microbial level, or
an education approach for the public. Achievable levels
are initially set as the standard, and then subsequently
lowered as the industry performance improves. The
rationale behind this is if the industry can continually
improve there will eventually be no contamination of
concern. However, in primary food production it is very
difficult to eliminate or even control pathogen entry into
the food supply. Also, unlike chemicals, even a few
organisms can grow to large numbers through abuse at
any subsequent step in the food chain including in the
home. Managers evaluate the performance of the avail-
able risk management options and select the option(s)
that will achieve the ALARA. Industry and government
are familiar with this approach and to work effectively it
needs to be used by most of the industry affected.
However, it cannot meet a specific public health goal
because it is driven by the capability and willingness of
industry and ‘‘reasonably achievable’’ may not be
enough to see real reduction in disease, or it is only
linked to disease reduction in a general sense. In addi-
tion, it tends not to encourage new technologies to be
developed, although HACCP and customer specifica-
tions for meat has initiated new decontamination stra-
tegies. ALARA approaches include the US HACCP
Pathogen Reduction Regulation using industries current
39
best practices, and the US and Canadian policies for E.
coli O157:H7 in ground beef in which risks are to be
reduced by different types of existing interventions
(Health Canada, 2002; USDA, 1996).
The development of HACCP principles and quantita-
tive risk assessments has allowed governments to con-
sider more seriously a risk-based approach to managing
a food supply (ICMSF, 1998). Generic frameworks for
managing foodborne risks have already been outlined
(FAO, 1997). A new approach to risk management has
been proposed to have standards linked to public health
objectives (ICMSF, 2001; WHO, 2000; FAO/WHO/
German Federal Ministry for Consumer Protection,
2002). No country has yet implemented this approach,
although some components of it are already in place. In
short, this safety risk management system determines an
Acceptable Level of Protection (ALOP) with a defined
time line for improvement. On the assumption that dose
response data exist for the pathogen causing the disease,
a FSO can be established, such as a 5-log reduction of
the pathogen during the production of food (ingredients
through to the consumer), so that the consumer is
exposed to a dose that will cause fewer illnesses. Indus-
try and government work out performance and process
or product criteria to meet these objectives, and these
may or may not include GHPs, HACCP, and micro-
biological testing of the final product at production.
An ALOP is currently defined as the level of protec-
tion deemed appropriate in establishing a sanitary or
phytosanitary measure to protect human, animal or
plant life or health. This approach recognizes that there
will be differences between countries but agreement
within a country on the ALOP. It also assumes that
there is a single level above which the risk is unac-
ceptable and below which the risk is acceptable. Under
this scenario, an ALOP is derived by determining the
incidence of a particular disease and recommend a pro-
gram to reduce this disease over a period of time, e.g.,
10–50% reduction in a foodborne disease (10 cases to 9
or 5 cases per 100 000 population) by 2010. This
approach requires there be practical ways to achieve this
through specific programs and a realistic timeframe. It
offers a flexible approach to achieve this goal (through
FSO) and encourages industry innovation. However, no
internationally or nationally acceptable recommenda-
tions have yet been made relative to ALOPs and FSOs.
The USA has initiated an ALOP approach with the
recommendations included in the Healthy People 2010
report (Office of Disease Prevention and Health Pro-
motion, 2000), with goals for a 50% reduction of sal-
monellosis, campylobacteriosis, listeriosis, E. coli
infections and toxoplasmosis from 2000 to 2010. Since
all of these diseases can be meat-borne, FSOs could be
set for pathogens in specific meat products, or more gen-
eric levels for indicator organisms in all meat products.
To set FSOs would require risk assessments of these
40 E.C.D. Todd / Meat Science 66 (2003) 33–43
diseases with dose response curves. For instance, the
goal of decreased incidence of listeriosis to 0.25 cases
per 100 000 could be linked to FSOs, since dose
response data are available through the FDA/FSIS/
CDC (2001) and FAO/WHO (2001) risk assessments for
L. monocytogenes in RTE foods, although these are still
in draft forms. FSOs for indicator organisms, however,
could not be determined from dose response curves, and
another approach for these must be sought.
Canada has a policy on raw foods of animal origin
(RFAO) that is still being developed with a steering
committee with broad representation and stakeholder
input (Health Canada, 2000a, 2000b). General recom-
mendations include identifying the strengths and weak-
nesses in the current food safety management system, a
HACCP based risk management approach, and the
establishment of FSOs. One purpose of the policy is to
strengthen the existing control measures for foodborne
illness in Canada for which there is a lack of success.
For meat products, these are E. coli 0157:H7 in beef,
Campylobacter and Salmonella in poultry, and Tox-
oplasma in raw meat. Some specific recommendations
have been made to improve slaughter, grinding, and
processing operations to lower the risks, and include
irradiation as a possible final pasteurization step. How-
ever, FSOs have not yet been set with links to ALOPs.
8. Food safety objectives
Since a FSO is a maximum frequency and/or concen-
tration of a microbiological hazard in a food at the time
of consumption to provide an appropriate level of pro-
tection, it should be quantifiable and measurable.
However, the FSO has to be achievable by the affected
industry within a specified period of time. Once there is
agreement on this, the responsible government agency
can recommend process or performance criteria and
consumer educational programs. A process criterion is
more likely to be a time/temperature combination to
achieve the desired kill step to satisfy the FSO. A per-
formance criterion may be a reduction in pathogen load
or a limit to any increase in numbers. Since the FSO is
meant to take into account some degree of consumer
action, the performance criterion will be more stringent
than the FSO if growth in the stored product is expec-
ted, but less stringent if the product is to be cooked.
Microbiological criteria also have a role to play by
communicating the level of hazard that is considered
tolerable for consumer protection (i.e. to achieve the
ALOP), and can be incorporated into control measures
such as GHP and HACCP. For FSOs and criteria to be
effective requires a high degree of compliance. Educa-
tional programs can supplement performance criteria
but their impact is difficult to quantify.
9. Examples of potential FSOs: control in fermented
sausages in the USA and Canada
Both the USA and Canada have similar approaches
to control pathogens in fermented sausages which apply
the FSO approach even if they are not called as such.
FSIS has proposed five options to either achieve the
recommended 5-log10 relative reduction of E. coli
0157:H7 or control for its presence in a fermented meat
product containing beef (USDA, 2001). However, this
would be essentially the same as having a FSO of 5 since
subsequent recontamination and growth are probably
not significant in these types of products
1. 68.8
C (135
F) for 4 mm: assumes l000/g in raw
sausage blend (based on 5-D kill for Salmonella/
E. coli O157:H7 in beef);
2. 5-D kill based on research data of processor;
3. 2-D kill of E. coli 0157:H7 at level of 41/g
(negative for 15 samples of 25 g=1/125 g) in raw
sausage blend;
4. Hold and test final product negative for E. coli
O157:H7 in 30 samples25 g (1/250 g);
5. New technology shown to have a 5-D kill.
FSIS has also proposed a rule (FSIS, 2001) listing
lethality requirements for fermented RTE products. The
rule proposes a 6.5-log10 reduction of Salmonella in fin-
ished products containing meat, and 7-log10 reduction
in products containing poultry. This rule is still in the
development stage, and will probably be released in its
final format late 2003.
In Canada, control of VTEC and Salmonella in fer-
mented sausages allows choices which are consistent
with the FSO approach (Health Canada, 2000, 2002),
and allows the use of performance and microbiological
criteria as does the US policy:
1. Specified time and temperature heating, e.g.
130
F for 121 mm, or 145
F for 4 min but no
requirement for testing for E. coli O157:H7 or
Salmonella;
2. Manufacturing processes, e.g. heating, acidity,
drying, with a 5-D reduction in E. coli 0157:H7
verified by challenge studies;
3. Microbiological end-product testing to be done
on each production lot (3025 g samples) and
the lot held pending reception of results, which
are to be kept for 24 months. If any product is
positive for E. coli 0157:H7 or Salmonella, the
entire lot must be submitted to a minimum 5-D
reduction process or be destroyed;
4. Implement a HACCP system at the establish-
ment which includes testing of raw meat and
batter, and use a manufacturing process (fer-
mentation and holding, heating and/or drying)
 E.C.D. Todd / Meat Science 66 (2003) 33–43
which has been scientifically validated as
achieving at least 2-D reduction of E. coli
0157:H7;
5. Alternate process scientifically validated against
E. coli 0157:H7.
These examples show that even if two countries work
independently, they can develop, through the existing
scientific processes, appropriate performance criteria or
standards, which are could well be considered FSOs.
Also, it is possible to allow industry different options in
achieving a FSO, ranging from ingredient checks with
less heat, to all the control in the heating process, to
checking compliance with end-product testing and
holding the product until results are negative, to new
ways of eliminating the pathogen of concern.
10. Example of a performance criterion developed to
satisfy a FSO (modifed from ICMSF (2001) and
FAO/WHO (2002) and M. van Schothorst (personal
communication)
Pâté has been implicated as a vehicle for listeriosis.
This is because liver is heat-treated but can be reconta-
minated either before packaging or later by the con-
0). Thus, the contribution of the
sumer at home. Then, it may be kept for many days in
the refrigerator, that may allow for growth of the
pathogen. The ALOP is set at 1 case/1 000 000 from
consumption of pâté in a country, e.g. 270 cases in the
USA annually. From an existing L. monocytogenes dose
response assessment curve, such as those developed by
FDA/FSIS/CDC (2001) or FAO/WHO (2001), the FSO
would have to be < 100 L. monocytogenes cfu/g to
achieve this. Information on the process indicates that
the initial level of the source meat (liver) is 1 cfu/g (H0)
and there is a 3-log kill step (thousand fold reduction) in
the production of the pâté (R1). However, recontami-
nation by L. monocytogenes may occur at processing
(before packaging), retail (repackaging) or in the home
(multiple reuse), but is assumed to be low (total of 1 cfu/
g (
IRC) Total growth of L. monocytogenes in the
recontaminated product at retail and/or at home is
assumed to be a 50-fold increase based on limited sur-
vey data (
IG). No further reduction step is anticipated
such as heating the pâté by the consumer (R2). The for-
mula given in ICMSF
X X
Ho  Rþ IRCþ1 4 FSO ½all log 10 units
Where H0=initial level;
R=total reduction;
I total
increase, which may separated into recontamination
(
IRC) and growth (
IG) does not fit the pâté scenario
where there are two independent sets of contamination
(initial (Ho) and after processing (H1). A revised for-
mula, (McMasters and Todd, personal communication)
41
where growth is allowed for both the contamination
incidents together, demonstrates the exposure scenario
better. Using this method, log values are calculated after
the two instances of contamination, growth and reduc-
tion are added together:
  
ho
log10 þ h1 i1 4 FSO
ro
Where h0 and h1 are initial
Q and subsequent contamina-
tion levels, respectively; ro=the product of all reduc-
tion factors for the original contamination; and
i1=the product of all of the increase factors asso-
ciated with the second contamination, all in non-log
values. With the numbers given above, the results are
shown below
  
1
log10 þ 1 50 ¼ log10 ð50:005Þ ¼ 1:7 4 2
1000
This shows that the final level of contamination
would be less than the FSO of 2 with the data provided.
The scenario above is a simple one where no growth Q is
anticipated in the survivors after heat treatment ( ro),
and there is a noQ reduction after growth from the second
contamination ( r1
initial contamination to achieving a FSO is minimal
(0.005). However, if the storage period were substantial,
the initial contamination and growth of survivors (a
likely scenario for pâté in a home refrigerator) would
have to be taken into consideration. Process criteria can
be determined in a similar way to FSOs, but for differ-
ent steps in the process (at farm, processing, distribu-
tion, retail). The criteria at one level becomes the Ho at
the next level in the farm to fork continuum until the
final FSO at the consumer level is reached.
11. Setting food safety objectives (FSOs) at the inter-
national level
Under the GATT/SPS Agreement, SPS measures
based on appropriate standards, codes and guidelines
developed by Codex Alimentarius for food are deemed
necessary to protect human health. Codex is expressing
interest in linking public health goals such as ALOPs
with FSOs for industry to achieve. These FSOs are set
at the national level but should be considered through
international consultation. From these can come per-
formance criteria, process/product criteria, and GHP
and HACCP procedures. Inherent in this approach is
that member countries should be introducing policies to
reduce foodborne disease internally as well as reducing
risks to consumers in exported products. However, it is
not known whether FSOs can reasonably be set for all
countries, particularly those that are in the development
42 E.C.D. Todd / Meat Science 66 (2003) 33–43
stage of their public health infrastructure and establish-
ing new trade agreements, or for all food commodities.
Initially, baseline data on contamination levels in food
products would need to be carried out, access to rele-
vant dose response data obtained, the state of the
industry to achieve meaningful FSOs determined, and
cost-benefit studies to establish the value of proceeding
with a FSO approach conducted. These types of studies
take resources and are unlikely to be carried out by
most developing countries in the near future.
Unfortunately, foodborne outbreaks continue to
occur, and present policies seem to the public unable to
make much difference in their frequency or severity in
many countries around the world. The ALOP/FSO
approach to reducing foodborne disease is in the initial
stages of formulation and discussion, and it is uncertain
whether it will work in all pathogen/food combinations.
Certainly, the Codex Committee on Food Hygiene is
still debating the value of policies relating to ALOPs
and FSOs. Can the new approach work (ALOP/FSO/
risk assessments/performance and product criteria), or
is it still too complicated and uncertain to explore in a
regulatory setting? Even if governments like this
approach, what about industry and purchasing specifi-
cations from suppliers to buyers—will they insist on
their microbiological criteria even if there is no rela-
tionship to reduction of disease? Like HACCP, it will
take a long time for the different stakeholders in food
safety to understand and effectively implement this
approach, but if it can be achieved the public will be
able to see the public health goal of reduced foodborne
diseases to programs being implemented jointly by gov-
ernment and industry, and complemented by educa-
tional strategies for the consumer. Prescriptive
regulations with microbiological standards have a role
to play in reducing disease, but perhaps not as large a
role as was believed in the past. All the stakeholders
have to be willing to share in the responsibility and the
solutions in having safer food. Having a clear link
between reducing numbers of illnesses in a country and
levels of contamination achievable through appropiate
performance standards, innovative approaches by the
food industry, and actions that consumers can take to
prevent contamination and growth of pathogens, will
help reach targeted goals set by government, industry
and consumer groups. It will also change the ways gov-
ernments develop regulations. In a recent survey in the
USA, 360 representatives of industry, government aca-
demia, consumer protection organizations, trade asso-
ciations and consultants were asked to rank 10
statements on microbiological food safety and the food
production chain (Hall, 2002). Of the 231 respondents,
the top concern was a more consistent application of
HACCP by industry and government for assuring the
safety of the US food supply. Increased use of micro-
biological finished product testing ranked very low,
which reinforces the current view that that microbial
limits, standards or guidelines have to be used with
caution. Interestingly, there were no questions that
control of pathogens in the food supply could be related
to reduction of foodborne disease, such as the above
consideration of ALOP and FSOs. In addition, the
development of a global foodborne disease surveillance
network that might help in detecting pathogens in both
domestic and imported products was given a very low
priority by the stakeholders. Therefore, it seems that a
strong case has to be made to show that control pro-
grams need to be transparently linked to fewer cases of
disease. Otherwise, there will be little enthusiasm or
funding for this approach to making food safer.
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