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9
Application of Microbiological
Criteria to Foods
and Food Ingredlients
INTRODUCTION
In preceding chapters, conditions necessary for establishing meaningful
microbiological criteria were presented. In this chapter recommendations
are given regarding the need or lack thereof for microbiological criteria
for each of 22 food products or groups of products. The subcommittee
elected not to give specific recommendations relative to microbiological
limits but chose instead to emphasize that any criteria that are developed
should be realistic and should be based on relevant background infor-
mation. Although the organization of the individual sections of this chapter
may vary for each of the foods or groups of foods, the subcommittee has
attempted to address the following basic issues in each section: (1) the
sensitivity of the food products relative to safety and quality, (2) the
needs for a microbiological standards and/or guidelinets), (3) assessment
of information necessary for establishment of a criterion if one seems to
be indicated, and (4) where the criterion should be applied.
The following foods and food groups are included in this chapter in the
order in which they are listed below:
A. Dairy Products
B. Raw Meats
C. Processed Meats
D. Raw (Eviscerated, Ready
To-Cook) Poultry
E. Processed Poultry Products
184
F. Eggs and Egg Products
G. Fish, Molluscs, and
Crustaceans
H. Fruits and Vegetables
I. Fruit Beverages
J. Low-Acid Canned Foods
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APPLICATION TO FOODS AND FOOD INGREDIENTS
K. Acid Canned Foods
L. Water Activity-Controlled
Canned Foods
M. Cereals and Cereal Products
N. Fats and Oils
O. Sugar, Cocoa, Chocolate,
and Confectioneries
P. Spices
A. DAIRY PRODUCTS
Introduction
185
Q. Yeasts
R. Formulated Foods
S. Nuts
T. Miscellaneous Additives
U. Bottled Water, Processing
Water, and Ice
V. Pet Foods
Microbial growth in the more perishable dairy products, i.e., pasteurized
milks, condensed milks, ice cream mixes, creams, cottage cheese, and
fermented milks, often results in development of objectionable flavors
and textural changes. Even under conditions of good production, pro-
cessing, distribution, and storage (including care in the home) such changes
are inevitable and may be expected to occur within two to three weeks or
less. However, the high acidity of cottage cheese and fermented milks
and the high heat treatment given to ultrapasteurized milk permits some-
what longer shelf-life. Recognition of the perishability of these products
has led to the common practice of "sell by date" labelling as a means of
alerting distributors and consumers to the products' limited shelf-life. On
the other hand, the relatively stable dairy products, i.e., dried milks,
evaporated milk, sterilized milk, ice cream, ripened cheese, butter, and
sweetened condensed milk, may remain free of microbiologically induced
deterioration for several months or years.
In the early part of this century, health of dairy animals and production,
processing, and distribution practices were often poor. At that time, un-
pasteurized milk was a major vehicle for transmission to humans of dis-
eases such as typhoid, diphtheria, septic sore throat, tuberculosis, and
brucellosis (Bryan, 19831. Recognition of these problems by government
and industry led to a series of recommendations embodied in the Milk
Ordinance of 1924 and an interpretion of these recommendations in the
Code in 1927. This model milk ordinance, now titled the "Grade A Milk
Ordinance" (see below), is an example of the application of the HACCP
system to a major food industry.
Maintenance of the quality and safety of dairy products, which includes
optimum shelf-life, is now a well-accepted industry responsibility and is
a necessity for economic survival in this highly competitive industry.
Furthermore, it has become traditional for the public to expect, if not
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186 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRlTERlA
demand, high-quality products that are safe and esthetically acceptable.
Therein lies the basis for current safety and quality assurance programs
of regulatory agencies and of industry. As a component of such programs,
microbiological criteria play an important role.
Sensitivity of Products Relative to Quality
Currently, most state and local regulatory agencies utilize almost ex-
clusively the Grade A Pasteurized Milk Ordinance (USPHS/FDA, 1978)
and USDA Standards for Grades of Dairy Products (USDA, 1975) as the
bases for their regulatory programs for dairy products. As an integral part
of these two documents, microbiological criteria are specified for most
products (see Chapter 8, Table 8-41. Furthermore, the testing of dried
milk products for Salmonella is provided for in accordance with a Mem-
orandum of Understanding (FDA, 1975) (see Chapter 81.
There can be little doubt that application of microbiological criteria has
contributed significantly to the provision of high-quality, safe dairy prod-
ucts. With the exception noted below and as needs are uncovered by future
investigations and research, there appears to be no basis for imposing
more severe standards or additional criteria. Industry imposes on itself
criteria far more stringent than those that must be met to avoid the like-
lihood of noncompliance. This has the salutary effect of providing rea-
sonable assurance that products are esthetically acceptable and that aerobic
plate count levels are maintained well below those likely to cause dete-
riorative changes within a reasonable shelf-life period.
One of the exceptions referred to above is the bacterial count limit for
Grade 2 raw milk for manufacturing purposes as specified in the USDA
"Standards for Grades" (USDA, 19751. Recent research has revealed the
potential for heat-resistant enzymes of microbial origin to be involved in
the deterioration of processed dairy products held for prolonged storage
periods. Furthermore, these enzymes have been implicated in lowered
cheese yields. Psychrotrophs are among the principal organisms that pro-
duce these enzymes and because of modern milk-handling practices, they
can comprise a large proportion of the microflora of raw milk. Thus,
bacterial count levels as high as the 3 million per ml permitted in Grade 2
milk would appear to be excessive. Consideration might well be given to
modifying this standard. Certainly, lower count levels are easily attained
through application of modern milk-handling practices.
Sensitivity of Products Relative to Safety
Currently the microbiological safety of dairy products can be assured
only through application of three preventive measures. These are:
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APPLICATION TO FOODS AND FOOD INGREDIENTS
187
(1) pasteurization or more severe heat treatments; (2) prevention of post-
heat treatment contamination; and, (3) for certain products, end-product
testing for microorganisms and toxins for certain products. Microbiol-
ogical criteria are useful in the application of the preventive measures
listed above.
Current standards for coliforms as specified in the Grade A Pasteurized
Milk Ordinance and the USDA Standards for Grades are useful in detecting
post-heat treatment contamination. However, failure to find these organ-
isms in finished products or at critical control points does not necessarily
indicate the absence of post-heat treatment contaminants.
Dried Milk
There is ample justification for continued finished-product testing and
surveillance of dried milk products for the presence of Salmonella. These
products are susceptible to Salmonella contamination and are often used
without further heat treatment for fluid consumption as recombined milk
or as ingredients in formulated foods. Furthermore, these recombined or
formulated products are often consumed by high-risk populations. Monthly
reports of the USDA's Salmonella surveillance program (USDA, 1980)
administered in accordance with the USDA/FDA Memorandum of Un-
derstanding (FDA, 1975) reveal a continuing low level of Salmonella-
positive environmental samples and finished products from dried milk
plants. Concurrent with the USDA/FDA programs, industry conducts ex-
tensive testing. Subsequent routine follow-up procedures undoubtedly have
prevented contaminated product from reaching the market.
The above-mentioned program as well as FDA surveillance of products
offered for import should be continued, strengthened when indicated, and
reviewed periodically to ascertain that sampling plans, including methods
used, are consistent with the hazards presented and in accord with current
developments in methodology and with appropriate statistical concepts.
Reference is here made to the USDA document entitled "Salmonella
Surveillance Program" (USDA, 19801. This document refers to the Na-
tional Academy of Sciences publication An Evaluation of the Salmonella
Problem (NRC, 1969) and states that the report classifies dried milk and
dried milk product in Food Category II and proposes acceptance of a lot
on the basis of all negative results on twenty-nine 25-g samples (n = 291.
The USDA document states "Instead of analyzing 25-g samples this In-
struction provides a procedure whereby each test shall comprise a com-
posite of four 100-g samples." It further states that, "based on low
incidence of contamination, this procedure provides comparable sensitivity
and permits greater coverage at a reduced cost." In this case n = 16.
The sampling plan applies to finished products analyzed quarterly in ac
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188 EVALUATION OF TlIE ROLE OF MICROBIOLOGICAL CRITERIA
cordance with the surveillance program. This subcommittee does not agree
that a sampling plan of n = 16 provides "comparable sensitivity" to the
recommended plan where n = 29, though obviously it must agree that
the cost is reduced. In essence the USDA Quarterly Surveillance Program
should require the analysis of Weather than 1 composite sample. In this
case the sampling plan would be n = 32, which would be only slightly
more stringent than the plan recommended by the Salmonella committee.
In practice, on a quarterly basis, the USDA collects samples from 3 days'
production (preferably consecutive days). Four samples of product from
each day are drawn, for a total of 12 samples. The four samples for each
day are composited to yield a 400-g analytical unit that is analyzed for
Salmonella. Thus, the quarterly finished-product surveillance consists of
the analysis of three 400-g samples for a given plant. If the plant produces
products other than a nonfat dried milk, i.e., buttermilk and whey, a
separate set of 12 samples is taken from the dryerts) that is (are) used for
each product. If the plant has several dry-milk dryers, each with its own
bagging head, the product from only one dryer is sampled. The "Instruc-
tion" directs that alternately a different dryer be sampled on each suc-
cessive quarterly survey. This subcommittee believes that samples should
be drawn from each dryer since each is an integral unit of production
equipment. At the time of the quarterly survey three environmental samples
are also collected, these being waste material from the vacuum cleaner,
air filters, and tailings. When the surveillance on a plant's production
shows a positive test, a letter is sent to the plant manager informing him
of the single positive test and the three available options by which the
positive product can be handled. These options appear to be adequate to
provide reasonable assurance that contaminated product will not reach the
market. They provide that the day's production having the positive Sal-
monella test shall be either:
1. segregated, reprocessed and the reprocessed product tested for Sal-
monella;
2. segregated and disposed of in a manner that poses no health problem
to humans or animals, e.g., USDA certification that the product was
discarded in a sanitary landfill; or
3. retested (verification test) at the rate of twelve 100-g samples. For
test purposes the laboratory will composite 4 samples for a total of
3 tests in = 481. If none of the composites shows a positive test,
the results are interpreted as meaning that the incidence of Salmonella
is insignificant, and the day's production may be used for human
purposes. If one or more of the composites shows a positive test,
the day's production represented by the test is then handled as in
OCR for page 189
APPLlCATlON TO FOODS ID FOOD INGREDIENTS
189
(1) or (2) above, i.e., segregated, reprocessed, and retested or dis-
posed of. In addition, eight 100-g samples are collected from product
manufactured on each of two days immediately preceding the day(s)
in which the positive product was noted and this rate of sampling
and testing is also performed on each day's production made sub-
sequent to the day(s) having a positive product test until the plant
effects a complete cleanup of its drying facilities. This procedure
would represent a sampling plan of n = 32, a plan comparable in
stringency to that recommended by the Salmonella committee.
If, in connection with a quarterly survey, more than one of the three
finished product samples are positive, then verification testing (as outlined
above) is not permitted. Positive lots are reconstituted and repasteurized
or disposed of in a manner that poses no threat to human or animal health.
The plant ~nanager is requested to furnish a list of production back to at
least two days prior to the positive lot and up to the time of special cleanup.
The list should show the date of manufacture, lot number, number of
containers in each lot, and the present location of the product. "Because
of possible serious contamination, the product should be recalled from
distribution channels and held for sampling and testing for Salmonella."
In this connection eight samples are drawn from each day's production
held from distribution. If all eight test results on a day's production are
negative, that product may be released for use or distribution. If a positive
test is obtained on product for any day, all the product for that day shall
be disposed of in such a manner so as to pose no health problem to humans
or animals. This subcommittee believes that the actions taken subsequent
to the detection of positive lots at time of quarterly surveillance sampling
are adequate for the purposes intended.
The effectiveness of cleanup (required as part of one of the three options
indicated above) is determined on the basis of tests made on product
manufactured subsequent to cleanup. Sampling involves the collection of
eight 100-g samples on each of three production days immediately fol-
lowing the cleanup (n = 321. In this instance, if a lot is declared positive,
there is no option for verification testing; management must dispose of
the product "in such a manner as to pose no health problem to humans
or animals" or reprocess the lot and again test it for Salmonella. Fur-
thermore, three environmental samples are taken presumably on each post-
cleanup production day.
The environmental sampling program is an integral part of the USDA
Salmonella Surveillance Program. Concomitant collection of environ-
mental samples at the time quarterly finished-product samples are taken
materially strengthens the program. Experience has taught that if a Sal
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190 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA
monella problem exists within a milk-dr~ving plant, one is far more apt to
detect this problem through the analysis of environmental samples than
through finished product analysis. Thus, given an adequate finished prod-
uct sampling plan (n = 29-30) combined with the testing of environmental
samples, there is reasonable assurance that if all samples are negative, a
serious Salmonella problem did not exist at the time of the quarterly
inspection. Furthermore, the sampling programs followed in verification
tests have a stringency comparable to that recommended by the Salmonella
committee (NRC, 19691. The overall weakness of the program lies in the
fact that (1) samples are collected only on a quarterly basis; (2) sampling
plans used at time of quarterly sampling are not sufficiently stringent, i.e.,
consistent with recommendations of the NAS/NRC Salmonella report (NRC,
19691; and (3) in plants having more than one dryer for a given product,
the product from only one of the dryers is sampled. Thus, the USDA
surveillance program cannot substitute for in-house surveillance by the
processor. As with the USDA program on eggs and egg products, the
control of the Salmonella hazard in dry milk requires continuous testing
of finished product and environmental samples by the processor. The
present USDA program is to be commended and should be strengthened
as indicated above and continued, with the realization that it is not a
substitute for microbiological control by the manufacturer. Accordingly,
the dry milk industry should be encouraged to test finished products reg-
ularly and in accordance with sampling plans recommended in the NAS/
NRC Salmonella report.
Cheese
Cheese is the second dairy product for which finished product testing
for presence of a pathogen or its toxins may be indicated. The organism
of primary concern is Staphylococcus aureus; although pathogenic Esch-
erichia cold have caused some concern. Also, the recent series of outbreaks
of brucellosis due to unripened raw goat milk queso blanco cheese sold
primarily from roadside vendors in the Houston, Texas area has empha-
sized the hazard of cheese made from unpasteurized milk (Perkins et al.,
19834. As in the case of the hazard of raw milk consumption, pasteurization
of milk used in the manufacture of this cheese is the only rational means
of control. Routine microbiological testing would not serve as an effective
control measure.
Certain cheese varieties have served as the vehicle involved in outbreaks
of staphylococcal food poisoning. Others, although not involved in out-
breaks, have been shown to permit the buildup of potentially hazardous
levels of S. aureus under certain conditions of manufacture. Although few
OCR for page 191
APPLICATION TO FOODS AND FOOD INGREDIENTS
191
outbreaks have been reported in the United States in recent years, the
problem does persist. The nature and control of the problem, including
application of microbiological criteria, has been reviewed recently (ICMSF,
1980, 19851. The following is a brief summary of these considerations.
The hazard of staphylococcal food poisoning presented by cheese is
limited largely to hard varieties, i.e., Cheddar and similar types and Swiss
or Emmenthaler. Although S. aureus has been demonstrated to grow in
certain other varieties, i.e., Gouda, Brick, Roquefort, Blue, and Moz-
zarella, their involvement in outbreaks has been rare or unreported (ICMSF,
19801. At some point during manufacture and subsequent handling, the
first group of cheeses undergoes a sufficiently long period at moderate
temperatures, which permits growth of lactic starter cultures. Impairment
of such growth during these periods permits relatively unrestricted growth
of various other organisms that may be present, including S. aureus. If
the initial population and period of time of favorable growth conditions
are sufficient, the number of S. aureus may reach several million per gram
of product, at which point hazardous levels of enterotoxin may be present.
Adequate heat treatment of cheese milk, good sanitary practices to avoid
post-heat treatment contamination, and unimpaired starter culture activity
are essential elements of good manufacturing practices for control of
S. aureus in cheese.
Appropriate analytical methods are available for the testing of cheese
and the monitoring of critical control points in cheese manufacture. Ad-
equate and relatively simple methods for detection and enumeration of
S. aureus in cheese are available. S. aureus enterotoxins may be detected
with specificity, although the procedures are somewhat complicated. Fur-
thermore, a rapid test for staphylococcal thermonuclease is sufficiently
reliable for determining whether a particular lot of cheese may contain
enterotoxin or whether it may be safely released for distribution (see
Chapter 15 of ICMSF, 19851.
At present the incidence of staphylococcal food poisoning by domest-
ically produced cheese does not justify routine testing by regulatory agen-
cies. However, industry should be encouraged to (l) routinely monitor
critical control points for presence or indication of staphylo.~occal growth
and to (2) test all cheese for S. aureus and/or thermonuclease if abnormal
lactic culture activity occurred during manufacture or if other conditions
that might lead to extensive staphylococcal growth were encountered. FDA
should routinely test all susceptible cheese varieties offered for import for
presence of thermonuclease. This routine testing is advisable as regulatory
agencies generally do not have knowledge of the cheese production con-
ditions. Lots positive for thermonuclease should be further tested for
presence of enterotoxins.
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192 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA
Outbreaks of foodborne illness due to certain pathogenic strains of
E. cold in imported Camembert cheese occurred in the United States in
1971. These were the first documented foodborne outbreaks due to E.
cold to be reported in the United States. Nevertheless, they caused con-
siderable concern about cheese as a vehicle for transmission of pathogenic
E. cold to humans. No further outbreaks of cheeseborne illness due to
E. cold were reported until 1983. In 1983 several outbreaks occurred again,
resulting from consuming imported soft cheese (Brie and Camembert) of
French origin. Investigations were not completed at time of this writing,
but they seem to indicate that a certain strain of E. cold (027: H20) pro-
ducing a heat-stable toxin was the causative organism (Francis and Davis,
19841. .
Following the first episode in 1971 certain control measures were in-
troduced by the French government and the industry. Apparently these
measures were effective in view of the 12-year interval between the two
series of outbreaks. However, now it would appear prudent for FDA to
initiate appropriate research relative to the E. cold problem in soft cheese
as well as the routine testing of soft cheese offered at import, i.e., Ca-
membert, Brie, and similar varieties, for the presence and quantitative
level of E. colt. Such studies would serve to further delineate the problem
and assist in development of an appropriate control program.
Fluidt Milk
.
Milkborne disease outbreaks caused by consuming legally purchased
contaminated raw milk as well as raw milk cheese (see preceding dis-
cussion of queso blanco cheese) continue with regularity. Even certified
raw milk, which is produced under the most exacting sanitary conditions,
continues to cause outbreaks (Werner et al., 19841.
Recently, Bryan (1983) reviewed the epidemiology of milkborne dis-
eases and concluded, as many others have done previously j that pasteur-
ization is an essential process in providing milk that is free of disease-
producing microorganisms. Application of microbiological criteria, al-
though useful, cannot assure that contaminated raw milk will be detected.
The problems of preventing the sale and consumption of raw milk have
been emphasized in a recent editorial by Chin (1982) (see Appendix F).
The sale of raw milk is still legal in some 20 states in spite of the fact
that infectious disease professionals consider the scientific case against
raw milk to be irrefutable. Nevertheless, the legal aspects involved in
preventing the sale of raw milk are complex and provide impediments
toward that end. Unfortunately, the small segment of the dairy industry
that engages in public sale of raw milk for fluid consumption, deliberately
or through ignorance of the consequences, continues to make available to
OCR for page 193
APPLICATION TO FOODS AND FOOD INGREDIENTS
193
consumers a product that sometimes is hazardous. The subcommittee
agrees with Dr. Chin's conclusion that, "It is the responsibility of all
health professionals to see that the public and the policymakers are ade-
quately informed about the scientific findings so that public policy on raw
milk may be compatible with scientific knowledge and protective of the
public's health."
References
Bryan, F. L.
1983 Epidemiology of milk-borne diseases. J. Food Prot. 46:637-649.
Chin, J.
1982 Raw milk: A continuing vehicle for the transmission of infectious disease agents in
the United States. J. Infect. Dis. 46: 440-441.
FDA (Food and Drug Administration)
1975 Memorandum of Understanding USDA/FDA on Salmonella Inspection of Dry Milk
Plants. No. FDA 225-75-4002. Washington, D.C.: U.S. Department of Agriculture.
Francis, B. J., and J. P. Davis
1984 Update: gastrointestinal illness associated with imported semi-soft cheese. Morb.
Mort. Weekly Rpt. 33: 16, 22.
ICMSF (International Commission on Microbiological Specifications for Foods)
1980 Milk and milk products. Pp. 470-520 in Microbial Ecology of Foods. Vol. 2. Food
Commodities. New York: Academic Press.
1985 Microorganisms in Foods. 2. Sampling for microbiological analysis: Principles and
specific applications. 2nd Ed. In preparation.
NRC (National Research Council)
1969 An Evaluation of the Salmonella Problem. Committee on Salmonella. Washington,
D.C.: National Academy of Sciences.
Perkins, P., A. Rogers, M. Key, V. Pappas, R. Wende, J. Epstein, M. Thapar, F. Jensen,
T. L. Gustafson, and E. Young
1983 Brucellosis Texas. Morb. Mort. Weekly Rpt. 32:548-553.
USDA (U.S. Department of Agriculture)
1975 General specifications for approved dairy plants and standards for grades of dairy
products. Federal Register 40(198):47910-47940.
1980 Salmonella Surveillance Program. DA Instruction No. 918-72. Washington, D.C.:
U.S. Department of Agriculture.
USPHS/FDA (U.S. Public Health Service/Food and Drug Administration)
1978 Grade A Pasteurized Milk Ordinance. 1978 Recommendations. PHS/FDA Publ. No.
229. Washington, D.C.: U.S. Government Printing Office.
Werner, S. B., F. R. Morrison, G. L. Humphrey, R. A. Murray, and J. Chin
1984 Salmonella dublin and raw milk consumption California. Morb. Mort. Weekly Rpt.
33: 196-198.
B. RAW MEATS
Sensitivity of Products Relative to Safety and Quality
The microbiological condition of retail cuts of red meat (beef, pork,
and lamb) is the result of a series of conditions and events including:
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194 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA
1. the health and condition of the live animal;
2. slaughtering-dressing practices;
3. conditions of chilling of the carcass such as rate of cooling, tem-
perature, and humidity;
4. sanitary conditions and practices during fabrication of a carcass into
primal, subprimal, and retail cuts;
5. packaging conditions such as air versus vacuum-packaging;
6. conditions of distribution and storage (time-temperature profiles);
7. handling of cuts in food service establishments and in the home
(proper refrigerated storage, adequate heat treatment, avoiding cross-con-
tamination).
Following is a brief summary of these conditions and events as they
relate to shelf-life and wholesomeness of meat and the potential need for
microbiological criteria. For more detailed information, the reader is re-
ferred to the following reports (APHA, 1984; Ayres, 1955, 1960; ICMSF,
1980; Ingram and Roberts, 1976; and Roberts, 19741.
Conditions prior to slaughter can have an impact on the microbiological
condition of meat. Muscle tissue from carcasses of animals that have
undergone prolonged muscular activity or long-term stress (lack of feed,
temperature changes) before slaughter is often dark, firm, and dry (DFD
meat), contains little or no glucose and has a higher pH ~-6.0) than that
of unstressed animals (approximately 5.51. Under aerobic storage con-
ditions, normal meat spoils when glucose is exhausted and amino acids
are attacked. In DFD meat, however, amino acids are attacked without
delay. The high pH of vacuum-packaged DFD meat allows the devel-
opment of Serratia liquefaciens and Alteromonas putrefaciens, which pro-
duce off-odors. For these reasons DFD meat spoils more rapidly than
normal meat (Gill and Newton, 19811. Stress also may increase the prev-
alence of Salmonella in pigs as they are transported from production units
to slaughtering facilities (Ingram, 1972; Williams and Newell, 19701.
Microorganisms associated with the live animal are located primarily
on the surface of the animal (hide, hair, hooves) and in the gastrointestinal
tract. The number of microorganisms in the muscle tissue (intrinsic bac-
teria) of healthy animals is small (Gill, 1979~. Carcasses of normal, healthy
animals appear to have considerable residual ability to maintain tissue
sterility. It is often reported that muscle tissue from stressed animals is
more likely to contain "intrinsic" bacteria. It is possible that certain forms
of stress depress the immune defense mechanisms and therefore allow the
survival of bacteria that otherwise would have been destroyed.
Sources of microbial contamination of a carcass include: the anima
(surface and gastro-intestinal tract), workers, clothing of workers, utensils
OCR for page 297
APPLICATION TO FOODS AND FOOD INGREDIENTS
297
Kokal, D., and D. W. Thorpe
1969 Occurrence of Escherichia cold in almonds of nonpareil variety. Food Technol. 23(2):93-
98.
Marth, E. H., and B. G. Calanog
1976 Toxigenic fungi. In Food Microbiology: Public Health and Spoilage Aspects, M. P.
DeFigueiredo and D. F. Splittstoesser, eds. Westport, Conn.: AVI Publishing.
Meyer, M. T., and R. H. Vaughn
1969 Incidence of Escherichia cold in black walnut meats. Appl. Microbiol. 18:925-931.
Schaffner, C. P., K. Mosbach, V. C. Bibit, and C. H. Watson
1967 Coconut and Salmonella infection. Appl. Microbiol. 15:471-475.
T. MISCELLANEOUS ADDITIVES
A number of food additives used by the food industry are derived from
animals, plants, or microorganisms. Three of the larger classes of additives
are gums, enzymes, and food colors. Only limited published information
is available regarding the microbiology of these substances.
Sensitivity of Products Relative to Safety and Quality
Gums
Gums hydrate in water to form viscous solutions or dispersions and
thus exhibit useful suspending, dispersion, and stabilizing properties. They
function in foods as emulsifiers, gelling agents, binders, flocculating agents,
film farmers, foam stabilizers, release agents, and lubricants. With this
range of functional properties, they are widely used in dairy products,
sauces, pie fillings, whipped toppings, salad dressings, puddings, and
jellies.
The sources of these useful polysaccharides are the resinous exudates
of trees (acacia, karaya, tragacanth), seeds (locust bean, guar), seaweed
(agar, alginates, carrageenan), and microorganisms (xanthan). Starches
and pectins from plants and gelatin from animals (Cottrell and Baird,
1980) are also used. Synthetic hydrocolloids include starch derivatives
and modified celluloses (Whistler and Zysk, 1978~.
The highest microbial populations in the major botanical gums (about
108/g) have been found in raw, unprocessed acacia, carrageenan, and
tragacanth (Souw and Rehm, 1975, 19761. Pretreated products such as
alginates, carrageenan powder, locust bean gum, and guar flour yielded
lower counts. The predominant organisms in the unprocessed gums were
the Bacillus species and Streptococcus faecalis; Escherichia coli, how-
ever, was not recovered. Coagulase-positive staphylococci with counts of
up to 105/g have been found in tragacanth and locust bean; Clostridium
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298 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA
perfringens has been recovered from these two gums as well as from
acacia.
Most gums will support bacterial growth when sufficient moisture is
present. Enzymes secreted by Bacillus species can degrade gels and gum
solutions reducing viscosity. Gums most susceptible to degradation are
tragacanth, acacia, karaya, guar, locust bean, carrageenan, and sodium
alginates (Souw and Rehm, 1975, 1976~.
Enzymes
The enzymes added to foods consist mainly of carbohydrates (amylase,
cellulase, invertase, pectinase, etc.) and proteases (e.g., papain and rennet).
Plants, animals, and microorganisms are sources of the enzymes.
Little is known about the microbiology of enzyme preparations. Animal
and microbial rennets, the enzymes whose microbiology has been studied
most extensively, may yield high counts but appear to be free of pathogenic
bacteria (de Becze, 19701. Never has a health problem been traced to the
use of an enzyme per se in food processing (Pariza and Foster, 19831.
Colors
Natural colors, including annatto, anthocyanins, beet red, carotene,
carmine, and saffron, have long been added to foods. Except for carmine,
which comes from an insect, these colors are derived from plants. They
are extracted into oil or aqueous systems from seeds, skins, or flowers.
There are virtually no published data about the microbiological quality
of natural food colors. Some anthocyanins have limited antimicrobial
activity and thus may restrict growth of certain microorganisms. The one
recorded disease outbreak traced to a food color was due to salmonellae
in carmine. Salmonella cabana was found to be responsible although
additional samples of insects contained Salmonella newport and Salmo-
nella enteritidis (Lang et al., 19671.
Need for Microbiological Criteria
Since many of these additives are raw agricultural products, the usual
indices such as APCs usually would be of little value. The type of criteria
that might be applied would depend upon end use of the additive. For
example, additives to be used in canned foods should not be a significant
source of heat-resistant bacterial spores. At present there is little published
information to suggest that microbiological criteria would be useful for
most gums, enzymes, and colors. This also was the conclusion of a
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APPLICATION TO FOODS AND FOOD INGREDIENTS
299
committee of FAD/WHO who examined the subject a number of years
ago (de Becze, 19701.
References
Cottrell, I. W., and J. K. Baird
1980 Gums. Pp. 45-66 in Vol. 12 of Kirk-Othmer Encyclopedia of Chemical Technology,
3rd Ed. New York: John Wiley and Sons.
de Becze, G. I.
1970 Food enzymes. Critical Reviews in Food Technology 1(4): 479-518.
Lang, D. J., L. J. Kunz, A. R. Martin, S. A. Schroeder, and L. A. Thomson
1967 Carmine as a source of nosocomial salmonellosis. N. Eng. J. Med. 276:829-832.
Pariza, M. W., and E. M. Foster
1983 Determining the safety of enzymes used in food processing. J. Food Prot. 46:453
468.
Souw, P., and H. J. Rehm
1975 IV. Microbiological degradation of three plant exudates and two seaweed extracts.
Z. Lebensm. Unters.-Forsch. 159(5): 297-304.
1976 V. Degradation of the galactomannans guar gum and locust bean gum by different
bacilli. European J. Appl. Microbiol. 2: 47-58.
Whistler, R. L., and J. R. Zysk
1978 Carbohydrates. Pp. 535-555 in Vol. 4 of Kirk-Othmer Encyclopedia of Chemical
Technology, 3rd Ed. New York: John Wiley and Sons.
U. BOTTLED WATER, PROCESSING WATER, AND ICE
Sensitivity of Products Relative to Safety and Quality
Drinking water has been and still is an important vehicle for transmitting
disease-causing agents (bacteria, viruses, parasites, chemicals) to man.
From 1977-1981, 189 outbreaks of water-related diseases involving an
estimated 49,453 persons occurred in the United States (CDC, 1979, 1980,
1981, 1982 a,b). As for foodborne disease outbreaks, these figures should
not be the basis for firm conclusions about the true incidence of waterborne
disease outbreaks as it is most likely many times greater than that reported.
Of the 189 outbreaks, 100 (53%) were of unknown etiology and were
designated "acute gastrointestinal illness" (AGI). The remaining 89 (47%)
outbreaks were of a confirmed etiology: Giardia (31), chemical (27),
Shigella (9), Norwalk agent (7), Salmonella (5), Campylobacter (3), Parvo-
virus-like agent (3), hepatitis A (2), Vibrio cholerae Of (1), and Rotavirus
(11. In none of these outbreaks, however, were bottled waters identified
as vehicles.
Public interest in pure, better-tasting water has created a large demand
for bottled drinking water. Bottled water is defined by FDA (1982a) as
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300 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA
water that is sealed in bottles or other containers and intended for human
consumption.
The following types of bottled drinking water are available (APHA,
1984~:
Spring or Well Water. This water is taken directly from a spring or
well and bottled with minimum treatment.
2. Specially Prepared Drinking Water. This is water in which the
mineral content has been adjusted and controlled to improve the taste.
The source may be a public water supply or a well.
3. Purified Water. This water conforms to the United States Pharma
copeia standard (USP, 1980) for purified water with minerals removed to
less than 10 mg/l. Water can be "purified" by distillation, ion-exchange
treatment, or reverse osmosis. Method of preparation must be indicated.
Only water prepared by distillation can be called "distilled water."
4. Fluoridated Water. Fluoride has been added to drinking water at the
optimum concentration as set forth in the FDA Quality Standards (FDA,
1982a).
No definition or quality standard for "mineral" water has yet been
established in the United States.
In view of the potential for water-related illnesses in humans, it is
essential that bottled water be from a safe source (spring, artesian well,
drilled well, municipal water supply, or other source) and that it be pro-
cessed, bottled, held, and transported under sanitary conditions.
Water containing small numbers of enteric pathogens can cause disease
in humans, whereas the same organisms ingested with food may require
larger quantities of bacteria. Small amounts of water taken between meals
pass the pyloric area with very little delay. Under such conditions enteric
pathogens are hardly exposed to the bactericidal effect of gastric juice and
reach the duodenum virtually unchanged (Levine and Nalin, 1976; Mossel
and Oei, 19751. When the same bacteria are ingested with solid food,
intragastric retention times are considerable. This results in a reduction
in viable bacterial cells in individuals with normal gastric secretions.
In the United States, few published data are available on the micro-
biological condition of bottled drinking water or on the incidence of human
disease outbreaks resulting from their use. According to two reports (EPA,
1972; Geldreich et al., 1975), the bacteriological quality of freshly bottled
water varied greatly from brand to brand and from sample to sample within
brand. Only 10% of samples had an initial APC greater than 500/ml.
Coliforms were detected in 6 of 129 samples but only two of these samples
exceeded the USPHS Drinking Water Standards. One of these samples
also contained fecal coliforms and the other contained Pseudomonas aeru
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APPLICATION TO FOODS AND FOOD INGREDIENTS
301
ginosa. During storage of bottled water pulsating changes in aerobic plate
counts frequently occurred. Over 90% of counts of 10,000 bacteriological
analyses of bottled water in California in 1977 were less than 100 per ml
at time of bottling (Sheneman, 19831. Over 99.8% of these samples were
free of coliforms.
Although there is no epidemiological evidence that bottled water pro-
cessed in the United States has been a public health problem, bottled water
has been cited as a cause of human disease in other parts of the world.
For example, bottled noncarbonated mineral water was implicated as one
of the primary vehicles involved in a cholera epidemic in Portugal in 1974
(Blake et al., 19771.
FDA microbiological standards for bottled water (FDA, 1982a) are
based on the presence of coliforms. With the multiple tube fermentation
method not more than one unit in a sampling of 10 (subsamples) shall
have a MPN of 2.2 or more coliforms per 100 ml and no analytical unit
shall have a MEN of 9.2 or more coliforms per 100 ml. With the membrane
filter method, not more than one of the analytical units in the sample shall
have 4.0 or more coliforms per 100 ml and the arithmetic mean of the
coliform density of the sample shall not exceed one coliform per 100 ml.
The FDA GMPs for bottled water (FDA, 1982b) require coliform anal-
ysis at least once a week of a representative sample from a batch or segment
of a continuous production run for each type of bottled drinking water
produced during a day's production. Additionally, source water obtained
from other than public water systems is to be sampled and analyzed for
coliforms at least once each week. In addition, at least once each three
months, a bacteriological swab and/or rinse count should be made from
at least four containers and closures selected just before filling and sealing.
No more than one of the four samples may exceed more than one bacterium
per ml of capacity or one colony per cm2 of surface area. All samples
shall be free of coliforms.
In addition to the federal standards, state and local microbiological
criteria and good manufacturing practice codes exist to monitor the pro-
duction, processing, and distribution of bottled drinking water (Wehr,
19821. To promote high standards of quality in the bottled water industry,
the International Bottled Water Association has published a technical man-
ual containing a quality control program to assure compliance with FDA
standards (IBWA, 19831. The American Sanitation Institute (ASI) inspects
all IBWA-member plants for conformance with the regulations.
The indigenous microflora of bottled drinking water usually consists of
gram-negative bacteria belonging to genera such as Pseudomonas, Cy-
tophaga, Flavobacterium, and Alcaligenes. Although no total count is
specified, good-quality drinking water at time of bottling usually contains
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302 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA
less than 100 bacteria per ml (APHA, 1984~. Higher initial counts represent
a lack of good manufacturing practices. The presence of coliform bacteria
in bottled water indicates either a lack of good manufacturing practices
and/or a potential health problem. Ozone may be applied as a disinfectant
just prior to bottling. Some surviving bacteria may multiply in the water
after the ozone has dissipated.
No one microorganism or group of microorganisms can serve as an
ideal indicator of pollution of various types of water. Although many
organisms such as Aeromonas, Streptococcus, Escherichia colt, fecal col-
iforms, coliforms, sulfite-reducing Clostridium, P. aeruginosa, Vibrio,
and E. cold phages have been suggested as potential indicator organisms
of drinking water safety, total coliforms appear at the present to be the
best indicator organisms (Ptak and Ginsberg, 19771.
Processing Water and Ice
Water is used extensively in the food-processing industry. It comes in
direct contact with major food commodities such as meat, poultry, fish,
fruits, vegetables, and cheese curd during washing or chilling operations.
In addition, water is used in the cleanup operations of equipment and
utensils that come in contact with food. Water also is used as an ingredient
in the preparation of foods. Ice is used widely to chill foods such as fish
and poultry and is added to some foods as in the preparation of some
processed meats. In many food-processing industries, water is chlorinated
to control levels of microorganisms, for example in cooling water of
canning plants. Chlorination of processing water requires an understanding
of needed chlorine concentration, effect of water characteristics such as
pH on available chlorine, and proper testing procedures to periodically
examine for available chlorine (FPI, 19821.
Water used in food production and processing can be a source of spoilage
microorganisms and, if obtained from a nonpotable source or subsequently
contaminated, it can be a source of pathogens. Several outbreaks of food-
borne disease have been associated with or traced to the use of contam-
inated water, e.g., salmonellosis from fish (Gangarosa et al., 1968), typhoid
fever from canned corned beef (Howie et al., 1968), and yersiniosis from
tofu (Nolan et al., 19824.
Need for Microbiological Criteria
There is no epidemiological evidence to indicate that bottled water as
available currently in retail channels offers a significant health hazard to
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APPLICATION TO FOODS AND FOOD INGREDIENTS
303
the American public. Therefore, there appears to be little evidence of need
for additional or modifications of criteria currently in FDA regulations.
However, the commercial vending of bottled water including import sup-
plies and the variety of sources from which water for bottling is obtained
has proliferated. These recent increases suggest that a periodic reassess-
ment should be made of practices in this industry relative to the micro-
biological quality and safety of bottled water offered to the public.
Water or ice that comes in contact with or becomes part of a food should
be from a potable supply and the microbiological criteria for them should
meet the standards set for drinking water (Greenberg et al., 19811.
Where Criteria Should Be Applied
Microbiological examination of bottled drinking water for compliance
with standards or guidelines should be camed out on samples collected
at the processing plant. Examination of samples for APC at the retail level
has little merit.
References
APHA (American Public Health Association)
1984 Compendium of Methods for the Microbiological Examination of Foods. 2nd Ed.,
M. L. Speck, ed. Washington, D.C.: APHA.
Blake; P. A., M. L. Rosenberg, J. Florencia, J. B. Costa, L. D. P. Quintino, and E. J. Gangarosa
1977 Cholera in Portugal, 1974. II. Transmission by bottled mineral water. Am. J. Epi-
demiol. 105 :344-348.
CDC (Centers for Disease Control)
1979 Foodborne and Waterborne Disease Outbreaks. Annual summary 1977. Atlanta: Cen
ter for Disease Control.
1980 Water-related Disease Outbreaks. Annual Summary 1978. Atlanta: Centers for Disease
Control.
1981 Water-related Disease Outbreaks. Annual Summary 1979. Atlanta: Centers for Disease
Control.
1982a Water-related Disease Outbreaks. Annual Summary 1980. Atlanta: Centers for Disease
Control.
1982b Water-related Disease Outbreaks. Annual Summary 1981. Atlanta: Centers for Disease
Control.
EPA (U.S. Environmental Protection Agency)
1972 Bottled water study. A pilot survey of water bottlers and bottled water. Washington,
D.C.: Water Supply Division, EPA.
FDA (Food and Drug Administration)
1982a Quality standards for foods with no identity standards, bottled water. Code of Federal
Regulations 21 CFR 103 (as corrected in Federal Register 47(205):47003-47004.)
1982b Processing and bottling of bottled drinking water. Code of Federal Regulations 21
CFR 129.
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304 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA
FPI (The Food Processors Institute)
1982 Canned Foods, Principles of Thermoprocess Control, Acidification and Container
Closure Evaluation, 4th Ed. Washington, D.C.: FPI.
Gangarosa, E. J., A. L. Bisno, E. R. Eichner, M. D. Treger, M. Goldfield, W. E. DeWitt, T.
Fodor, S. M. Fish, W. J. Dougherty, J. B. Murphy, J. Feldman, and H. Vogel
1968 Epidemic of febrile gastroenter~tis due to Salmonella Java traced to smoked whitefish.
Am. J. Pub. Health 58:114-121.
Geldreich, E. E., H. D. Nash, D. J. Reasoner, and R. H. Taylor
1975 The necessity of controlling bacterial populations in potable waters Bottled water
and emergency water supplies. J. Amer. Water Works Assoc. 67:117-124.
Greenberg, A. E., J. J. Conners, D. Jenkins, and M. A. H. Franson
1981 Standard Methods for the Examination of Water and Wastewater, 15th Ed. Wash-
ington, D.C.: American Public Health Association.
Howie, J. W.
1968 Typhoid in Aberdeen, 1964. J. Appl. Bacter~ol. 31:171-178.
IBWA (International Bottled Water Association)
1983 International Bottled Water Association Technical Bulletin, Winter. Alexandria, Va.
IBWA.
Levine, R. J., and D. R. Nalin
1976 Cholera is primarily waterborne in Bangladesh. Lancet 2:1305.
Mossel, D. A. A., and H. Y. Oei
1975 Person-to-person transmission of enters bacterial infection. Lancet 1:751.
Nolan, C., N. Hands, J. Ballard, J. Allard, and J. Kobayashi
1982 Outbreak of Yersinia enterocolitica Washington State. Morb. Mort. Weekly Rpt.
31 :562-564.
Ptak, D. J., and W. Ginsberg
1977 Bacterial indicators of drinking water quality. Pp. 218-221 in Bacterial Indicators/
Health Hazards Associated with Water. Spc. Techn. Publ. 635. Philadelphia: Amer-
ican Society for Testing and Materials.
Sheneman, J.
1983 Memorandum from the California Food and Drug Section. Water bottling plants
bacteriological analysis summary. In International Bottled Water Association, Tech-
nical Bulletin, Winter. Alexandria, Va.: IBWA.
USP (United States Pharrnacopeia)
1980 Purified water. P. 851 in The United States Pharmacopeia. Rockville, Maryland: U.S.
Pharmacopeial Convention.
Wehr, H. M.
1982 Attitudes and policies of governmental agencies on microbial criteria for foods an
update. Food Technol. 36(9):45-54, 92.
V. PET FOODS
Companion animals of man have been a source of diseases, including
salmonellosis, in humans (Morse and Duncan, 1974, 1975; Morse et al.,
1976; Pace et al., 1977) and contaminated pet foods have at times been
incriminated as the original cause (Pace et al., 19771. Interest in the
microbiology of these foods is influenced by the above and the fact that
certain pet foods, mainly canned products, are at times consumed by
humans.
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APPLICATION TO FOODS AND FOOD INGREDIENTS
Sensitivity of Products Relative to Safety and Quality
305
Although the true incidence of salmonellosis in animals is unknown
(NRC, 1969), Salmonella are widely distributed in warm- and cold-blooded
species and have been isolated from dogs, cats, horses, caged birds, turtles,
frogs, skunks, raccoons, opossums, and others. The role of pets in the
distribution of Salmonella has been recognized in a report by the Com-
mittee on Salmonella (NRC, 19691:
Of the many routes by which man can acquire salmonellosis, special mention should
be made of household pets, including dogs, cats, turtles, chicks and ducklings.
.
Pet animals can become infected with Salmonella by a wide variety of
routes, e.g., through coprophagy, by direct contact with infected animals,
through eating diseased carrion and wildlife, and by the consumption of
contaminated pet food. The latter is probably the least important source
since the present day incidence of Salmonella in commercial pet food is
very low (Pace et al., 1977~.
Pet foods, which are sold predominantly for dogs and cats, may be
marketed as canned, intermediate moisture (aw 0.80-0.90), or dried prod-
ucts. Canned pet foods are terminally heat processed in hermetically sealed
containers and are commercially sterile. They are subject to the regulations
for low-acid canned foods and when in compliance are not of public health
concern. Intermediate moisture pet foods and the dry products are given
a heat process, generally during extrusion and pelleting, that will destroy
the vegetative cells of pathogenic bacteria. The prevention of recontam-
ination following heating, then, is the critical control step in their pro-
cessing. Monitoring of environmental samples as well as finished product
for Salmonella is thus important.
Recontamination of dry pet food with Salmonella is of special concern
because water is often added to the food prior to feeding. Significant
growth of the pathogen can occur if the food is held at ambient temperature
for an extended time period following rehydration. A potential would then
exist not only for infection of the pet but for cross-contamination of
household items such as equipment, utensils, and human foods.
Need for Microbiological Criteria
Canned pet foods are subject to the regulations for low-acid foods and
thus the main applications of criteria are to assure that ingredients are free
of bacterial spores that might survive the thermal process.
Dry and intermediate moisture pet foods should be free of Salmonella,
and a standard exists for this pathogen (U.S. Congress, 19801. Specifi-
cations and guidelines for these products are especially useful if applied
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306 EVALUATION OF THE ROLE OF MICROBIOLOGICAL CRITERIA
at critical control points identified within a HACCP system. Guidelines
and specifications serve to:
1. assess suitability, including safety, of incoming ingredients (The
elimination of salmonellae from feed ingredients, particularly those of
animal origin, would greatly reduce the occurrence of these organisms in
finished pet foods, but this goal does not appear to be readily attainable
at this time [USDA, 1978] . );
2. identify acceptable ingredient suppliers;
3. assess control effectiveness at critical control points in manufactur-
~ng;
4. determine the acceptability of a finished product.
Information Necessary for Establishment of a Criterion
if One Seems To Be Indicated
Extensive information is available regarding those feed ingredients that
may be contaminated with Salmonella (ICMSF, 1980) and therefore may
require specifications that limit this pathogen. Information is also available
on the occurrence of Salmonella in pets (Morse, 1978), and in pet foods
(D'Aoust, 1978; ICMSF, 1980; Pace et al., 19771. It is advisable for pet
food manufacturers to conduct appropriate microbiological surveillance
studies that will generate the information required for the development of
guidelines.
Where Criteria Should Be Applied
Analyses for salmonellae might be conducted on the packaged product.
Guidelines and specifications would best be applied at the plant processing
level as components of an ongoing HACCP program. Their application
at critical control points and on the finished product should assist in
minimizing the contamination of pet foods with undesirable microorgan-
isms.
References
D'Aoust, J. Y.
1978 Salmonella in commercial pet foods. Can. Vet. J. 19:99-100.
ICMSF (International Commission on Microbiological Specifications for Foods)
1980 Microbial Ecology of Foods. Vol 2. Food Commodities. New York: Academic Press.
Morse, E. V.
1978 Salmonellosis and pet animals. In Proceedings of the Salmonellosis Seminar. Wash-
ington, D.C.: U.S. Department of Agriculture.
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APPLICATION TO FOODS AND FOOD INGREDIENTS
307
Morse, E. V., and M. A. Duncan
1974 Salmonellosis An environmental health problem. J. Am. Vet. Med. Assoc. 165: 1015-
1019.
1975 Canine salmonellosis: Prevalence, epizootiology, signs, and public health signifi-
cance. J. Am. Vet. Med. Assoc. 167:817-820.
Morse, E. V., M. A. Duncan, D. A. Estep, W. A. Riggs, and B. O. Blackburn
1976 Canine salmonellosis: A review and report of dog to child transmission of Salmonella
enteritidis. Am. J. Publ. Health 66:82-84.
NRC (National Research Council)
1969 An Evaluation of the Salmonella Problem. Committee on Salmonella. Washington,
D.C.: National Academy of Sciences.
Pace, P. J., K. J. Silver, and H. J. Wisniewski
1977 Salmonella in commercially produced dried dog food: Possible relationship to a human
infection caused by Salmonella enteritidis serotype Havana. J. Food Prot. 40(5):317-
321.
U.S. Congress
1980 Federal Food, Drug and Cosmetic Act, as amended. Washington, D.C.: U.S. Govt.
Printing Office.
USDA (U.S. Department of Agriculture)
1978 Recommendations for Reduction and Control of Salmonellosis. A Report of the U.S.
Advisory Committee on Salmonella. Washington, D.C.: USDA.
Representative terms from entire chapter:
critical control
