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cerned?
APPENDIX H
FOOD CONTAMINATION
William E. Pace1
When considering the effects on human health of subtherapeuti~
use of antibiotics in animal feeds, the food scientist must first
consider the order of events that could lead to possible adverse
effects. To develop a systematic approach, one must face a number
of questions that are ultimately related but do-not lend themselves
to a simple sequential consideration. Among these are:
· With what potential human health effects should we be con
· Do epidemiological data indicate that real problems exist
today or could exist in the future?
~ What diseases may be involved?
· Might the use of antibiotics in animal feeds play a direct
or indirect role in increasing the incidence or in complicating
the treatment of diseases?
· What lines of communication connect animals and humans in
the chain of events that might result in manifestation of adverse
effects?
· Do processing and storage significantly decrease antibio-
tic residues?
· Are there beneficial effects from the presence of anti-
biotics in.foods?
· Is the attention given to foods of foreign origin similar
to that given to foods originating in the United States?
use?
· What recommendations should be made regarding antibiotic
Office of the Surgeon General, Headquarters, U.S. Air Force,
Balling Air Force Base, Washington, D.C.
262
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263
CONCERNS
There are two general areas of concern: the toxic effect
of antibiotic residues and the potentiation of disease by anti-
biotic-microorganisms. The former is far simpler to approach
than is the latter.
TOXIC EFFECTS
Manifestation of a toxic effect requires only that a sus-
ceptible individual be exposed to the antibiotic residues.
Mercer (1975) reported that approximately 7.2X of a test popu-
lation was hypersensitive to penicillin and that ingestion of
as little as 10 units has produced mild reactions. Furthermore,
he stated that neomycin has cross-sensitization properties with
streptomycin and that 5.7% of a test population was sensitive to
neomycin. These data alone are adequate to indicate that there
is a strong and definite potential for toxic effects from anti-
biotic residues. However, measures to control or eliminate such
effects are relatively simple to define. Although the suscept-
ibility of a population cannot be changed easily, steps can be
taken to avoid or to minimize exposure. Most if not all of
those steps are already in routine use.
APPROVAL OF USE
The use of antibiotics in animal feeds must be limited to
those that are safe, have proven efficacy, and can readily be
detected in the tissues or products of the animals receiving
them. All of these criteria must be met before the Food and Drug
Administration (FDA) will approve a New Animal Drug Application
(NADA). After approval has been granted, our concerns must then
turn to detecting illicit use (concentrations in feed exceeding
those authorized, inadequate or improper mixing procedures, com-
bining with unapproved additives, etc.), ensuring adherence to
prescribed withdrawal periods, and sampling of market-ready pro-
ducts for residue analyses. Responsibility for residue analysis
of meats, poultry, and their products is vested in the U.S. De-
partment of Agriculture (USDA). The FDA is responsible for
analysis of dairy products.
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264
SAMPLING FOR RES IDUE ANALYSES
Mussman (1973) stated that two types of sampling programs are
used by the USDA. Each is designed to provide a different kind of
information. One, an "objective" program, is aimed at determining
the nationwide extent of a specific residue and identifying herds
or flocks that require detailed examination. The other, a "selec-
tive" program, is designed to define problems identified by the
objective program. Analysis for specific antibiotics involves the
combined use of bioassay and thin-layer or gas chromatographic
techniques.
EFFECTS OF PROCESSING AND STORAGE ON RES IDUES
Morrison and Munro (1969) have commented on the destruction
of drug residues in foods by food processing and storage. Liter-
ature cited by them indicates that cooking causes significant
reductions of tetracyclines in chicken, fish, and beef. Data
presented by Mercer (1975) indicate a marked reduction in levels
of penicillin in the kidney, liver, and muscle of chickens, swine,
and lambs following frozen storage for as short a time as 8 days.
In the United States, fresh poultry reaches the market within 1
to 2 days whereas fresh beef and pork require from 1 to 3 weeks.
By intention, frozen products reach the market weeks or even
months after processing. The changes in levels of antibiotic
residues during storage and preparation add an additional margin
of safety for the antibiotic-susceptible consumer. Assays must
continue to be performed as quickly as possible after slaughter
when residue levels are highest and most readily detectable.
ANTIBIOTIC-RESISTANT MICROORGANISMS
One must decide which organisms pose potential adverse health
effects as a first step in considerations of antibiotic-resistant
microorganisms. Since transferable antibiotic resistance is known
to occur only in Gram-negative organisms (Baldwin, 1970), we can
narrow our considerations relatively safely to those Gram-negative
organisms found most frequently in meats and meat products. There-
fore, the group is narrowed to some species of salmonellae, Shigella,
coliforms, Vibrio, Campylobacter, Yersinia, Pasteurella, Brucella,
Neisseria, Haemophilus, Pseudomonas, Achromobacter' Proteus, Flavo-
bacterium, and Alcaligenes.
Since the latter five are not known to
include pathogens, we can probably afford to omit them from further
consideration. The shigellae are well known as enteric pathogens,
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265
while the involvement of V~brio, Campylobacter, and Yersinia in
gastrointestinal disturbance is becoming more apparent. Brucella
in milk and dairy products must continue to be of concern because
of brucellosis.
The salmonellae and the coliforms (especially Escherichia coli)
deserve our greatest attention, the former because they are known
animal and human pathogens that are transferred between the two and
the latter because they are almost ubiquitous, are routinely used
as indicators of inadequate hygienic practices, are routinely present
in the human alimentary tract, can easily transfer drug resistances,
and have an increasingly recognized role in outbreaks of gastroin-
testinal disorders in humans. Review articles and reports of origi-
nal research (Groves et al., 1970; Gustafson, 1975; Howe et al.,
1976; Kobland, 1975; Licczardello et al., 1968; Linton et al., 1977,
in press; Newell and Williams, 1971; Patterson, 1969; Walton, 1970,
1971; Weissman and Carpenter, 1969) reveal an extremely wide varia-
tion in the reported incidence of salmonellae and E. cold on animal
carcasses in slaughterhouses or the ma rket. Figures for salmonellae
incidence range from 34X for chickens (Licciardello et al., 1968) to
84% for pork carcasses (Kobland, 1975), and to 74% for beef carcasses
(Weissman and Carpenter, 1969~. One paper cites a rate of 9X for
carcasses of ducks and turkeys (Patterson, 1969~. Figures reported
for the incidence of E. cold contamination range from 97X for pig
carcasses (Walton, 1971), to 73% for beef carcasses (Walton, 1971),
and to 81% for chicken carcasses (Lipton et al., in press). These
variations appear to be due to differing levels of sanitation in
processing plants, to the use or nonuse of bactericidal preparations
in rinse waters and in chill tanks, to variations in sampling proce-
dures, and to differences in culture techniques. Several of these
authors also reported antibiotic resistance in E. cold in up to
58.57` of the isolates from chickens (Lipton et al., in press), up to
797 of those from pork (Walton, 1970), and up to 39% of those from
cattle (Walton, 1970~. Antibiotic resistance was also reported in
up to 23% of the salmonellae isolated from pigs (Kobland, 1975~. It
is safe to conclude that both resistant_ cold and Salmonella can
probably be found frequently in carcasses of all species of meat
animals. There is little available data upon which to assess the
level of contamination by these organisms.
SOURCES OF CONTAMINANTS
E. cold is routinely found in the gut of both domestic animals
and humans. Even minor transgressions in proper sanitary practices
in slaughterhouses readily result in contamination of carcasses,
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266
which most often results from spillage of intestinal contents
during removal of the viscera. Salmonellae, while in no way
"normal" inhabitants, are found in the intestinal tract of ani-
mals very frequently. Most authorities agree that the primary
source of salmonellae in domestic animals is contaminated feed
or contaminated protein supplements. Groves et al. (1970), in
a study of salmonellae contamination of slaughter pigs, reported
isolation of the organisms from feed on 33% of the farms surveyed
and in pigs from 33.3% of the farms (correlation between the two
was not specified). Conversely, work cited by Edel et al. (1974)
indicated that pigs gained little or no salmonellae infection
from pelletized feed. However, they also cited data showing that
the use of pelletized feed alone did not prevent salmonellae in-
fections and concluded that environmental influences must also
play a major role.
Lapses in enforcement of proper hygienic practices rapidly
lead from salmonellae and E. cold contamination of the gut to
contamination of the carcasses, slaughter equipment, the slaugh-
ter environment, and the processing environment to the finished
product and on to the kitchens in private homes and institutions.
There, unknown to the preparer, cross-contamination to other
foods occurs frequently.
The hide of cattle and the skin of hogs are routinely contam-
inated by intestinal contents. Jensen and Hess (1941) concluded
that these constituted the main source of organisms for carcass con-
tamination. Intestinal contents also readily contaminate transp-
ortation facilities and holding pens where other animals are subse-
quently contaminated, many of which are young animals later shipped
to farms or to heavily concentrated populations in fattening pens.
During transportation animals are subjected to major stress and may
become sick. The therapeutic use of certain antibiotics in treating
these sick animals could lead to rapid dissemination of resistant
strains if the animals are not isolated during therapy. Threlfall
_ al. (1978) have proposed that similar circumstances might
possibly have been involved in the recent outbreaks of salmonellosis
in Britain involving the chloramphenicol-resistant strain of Salmo-
nella phage type 204. Datta (1965) stated that some resistance
factors carry resistance to as many as seven different drugs. Van
Houweling (1967) noted that exposure to an antibiotic could result
in transfer of resistance to other antibiotics as well because of
the linkage of resistance genes.
As early as 1943, Stuart and McNally showed that eggs are not
contaminated by the parent bird during egg formation or laying.
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267
They confirmed that the egg, shell and all, is deposited in the
nest in a sterile condition. Sound eggs from normal chickens
are contaminated after laying by coming into contact with the
external body or feet of birds or with the nest. Therefore,
efforts to reduce contamination of shell eggs should be aimed at
environmental factors rather than at the physiological processes
of egg formation.
VALUE OF ANTIBIOTICS IN FOODS
Since there is no question regarding the potential dangers
of antibiotic residues in foods, one must also ask whether such
residues also have beneficial effects. Such effects have been
clearly demonstrated. Chlortetracycline and oxytetracycline were
formerly approved by the FDA in concentrations of 5 to 7 ppm for
delaying microbial spoilage of fresh poultry, scallops, shrimp,
and eviscerated fish. Approval for these uses was withdrawn in
1966 because small residues could sometimes be detected in the
products after they were cooked. According to the Food, Drug,
and Cosmetic Act, residues of any drug in tissues of animals re-
ceiving the products are considered as food additives, the same
as when they are added directly. Furthermore, the use of any
food additive in a manner other than that approved by the FDA
is regarded as an adulteration and renders the food ineligible
for interstate shipment. An FDA-approved use of antibiotics will
not result in the presence of residues (or at least not al ter a
specified withdrawal period has been observed).
CONTROLLING CONTAMINATION BY PATHOGENS
One might ask whether antibiotics might be used in animal
feeds to reduce the incidence of pathogens in the gut of live
animals, hence reducing the potential for carcass and environ-
mental contamination leading ultimately to the consumer. Smith
and Tucker (1978) recently commented that the administration of
feed containing neomycin to broilers a few days prior to slaugh-
ter is being advocated and practiced in Britain as a means of
reducing the proportion of birds shedding salmonellae. Their
studies using 500 g/long ton (1,016 kg), i.e., 480 g/kg, for 9
days produced only a slight reduction. The use of 225 g/long
ton ~ 221 g/kg) for 2 days also produced only a slight reduction
in the proportion of birds shedding salmonellae but resulted in
the emergence of enormous populations of E. cold that possessed
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multiple, transmissible-type antibiotic resistance in the ali-
mentary tract of the treated chickens. Childers et al. (1977)
suggested very strongly that environmental controls within
the slaughterhouse are the most appropriate, and possibly the
safest and simplest, means of reducing contamination of car-
casses by pathogenic organisms. Transporting and holding swine
in sanitized surroundings prior to slaughter did not effectively
reduce contamination of carcasses with either salmonellae or E.
colt. However, several relatively minor modifications of the
evisceration procedures were effective in reducing contamination
levels to between 12X and 20% as opposed to between 50% and 63%
in control carcasses. The significant changes were the instilla-
tion of greater care on the part of workers to avoid spillage of
intestinal contents and to wash their hands and disinfect cutt-
ing knives in chlorine solutions before handling a new carcass.
Studies by Mosley et al. (1976) had indicated that hypochlorites
and iodophors were similar in effectiveness and that both were
superior to quaternary ammonium compounds in reducing levels of
Gram-negative organisms, including salmonellae, on stainless-
steel surfaces.
INSPECTION OF FOREIGN-ORIGIN MEATS
All control activities mentioned so far have concerned pro-
ducts of U.S. origin. Since the volume of imported products is
rather extensive, we should address this topic also. The respon-
sibility for reviewing foreign programs regulating meat produc-
tion and for inspecting imported meats, poultry, and products of
meat and poultry is vested in the Foreign Programs Branch, Field
Operations Division, Meat and Poultry Inspection Program, Food
Safety and Quality Service of the USDA (McEnroe, 1971~.
Review of foreign programs was initiated in 1966 to assess
the effectiveness of meat and poultry inspection programs in
those countries that desired to export their products to the
United States. The Federal Meat Inspection Act of 1907, amended
in 1938 and revised by the Wholesome Meat Act of 1967, requires
that countries that export meats or meat products to the United
States have facilities, sanitation standards, and inspection
practices at least equal to our own. Section 20 of the Act also
requires visits by U.S. experts to ensure compliance of foreign
plants. In describing the program, Lyons (1971) stated that
official certification by the USDA also requires the concurrence
of the Department of State. Furthermore, foreign products are
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269
accepted only when the country's inspection program and the stan-
dards in the processing plant have been certified as meeting U.S.
standards.
Most plants are visited at least annually. Those with minor
problems are visited more frequently. Products originating from
authorized plants in recognized countries must still be accompanied
by a certificate signed by a qualified representative stating that
the meat or meat product comes from animals that passed veterinary
ante-mortem and post-mortem inspection, that it is wholesome and
free of preservatives, and that it is otherwise in compliance with
U.S. requirements. Meat products (but not fresh carcass meats) are
then sampled at the port of entry by USDA officials and are sub-
jected to incubation and to laboratory analyses for pesticides,
antibiotics, and other chemical residues. Basically, the program
relies on evaluation of the inspection program of the foreign coun-
try, inspection of the plants of origin, reliance on the validity
of certification, and dependence on the quality control programs
of the importing U.S. firms. Microbial analyses would be performed
only as part of the sampling programs discussed above.
USDA officials do maintain close contact with their counter-
parts in foreign countries and are well aware of the animal hus-
bandry and food preservation practices in these countries. In case
there are significant variances from our own practices, the inspec-
tion program can be adjusted to focus on any specific problems that
might be anticipated. The status of these programs was confirmed
via personal communication (C. S. Johnson, Veterinary Staff Officer,
Meat and Poultry Inspection Training Program, FSQS/USDA, Dinton,
Texas, personal communication, 1979~.
SUMMARY
There is no question that the use of subtherapeutic levels
of antibiotics in animal feeds has resulted in increasing the
amount of animal protein available to the world's consumers. This
increase is due to increased growth rates and to the control of low
grade infections which often reduce the efficiency of feed utiliza-
tion. On the other hand, it becomes more and more apparent that
sanitation is the ultimate key to controlling initial levels of
carcass and product contamination and that proper refrigeration is
the key to controlling multiplication of those few unavoidable mi-
crobial contaminants that will still continue to slip through. The
use of antibiotics or other agents as preservatives or shelf-life
extenders can be used too easily to cover up poor quality control
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270
or to compensate for inadequate or improper animal husbandry prac-
tices. This may not hold entirely true in some developing nations
where refrigeration and rapid transportation are less than adequate.
In those cases, benefits to be gained would have to be balanced
against the degree of risk involved.
It appears that the primary need today is a vastly stepped-up
educational program aimed at producers, processors, service person-
nel, and consumers. Such a program must stress the importance of
sanitation and personal hygiene at every step, the essentiality of
avoiding cross-contamination, and the fact that products of animal-
origin are not (and are not intended to be) sterile and must be
handled accordingly. The effectiveness of public health programs
in the United States has contributed greatly to a healthier popu-
lation with an enhanced nutritional status, but they have also
produced a nation of consumers who take for granted the safety of
the products they consume and who know little about what precau-
tionary measures they should take or why. Because the government
has helped to create this problem, it has a responsibility to con-
tinue to protect the consumers from themselves.
RECOMMENDATIONS
Frog the view of the food scientist, several recommendations
are in order:
1. FDA's criteria for approval of NADA's should remain as
they are.
2. Sampling for antibiotic residues in meats, poultry, and
their products should be increased.
3. Sampling for pathogens and determination of their anti-
biotic resistance should be significantly increased, especially
for items of foreign origin.
4. USDA's Meat and Poultry Inspection Programs should place
increased emphasis on in-plant sanitation, especially on measures
that might reduce carcass contamination.
5. The Center for Disease Control should determine the anti-
biotic resistance of cultures of all Gr~m-negative organisms involved
in outbreaks of human illness (especially when food-borne transmis-
sion is known or suspected). When unusual resistance patterns are
recognized, follow-up epidemiological studies should be initiated to
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271
conf irm or to rule out involvement of subtherapeutic use of ant
biotics in animal feeds.
-
6. Intergovernmental exchange progran~s should be established
to exchange data from studies recommended in 5. This is especially
significant for countries that export or Sport foods for human
consumption to or from the United States.
7 . FDA and state animal regulatory officials should strongly
encourage isolation of animals that are on antibiotic therapy.
8. Extensive educational programs such as those descry bed in
the summary should be initiated.
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272
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Baldwin, R. A. 1970. The development of transferable drug re-
sistance in Salmonella and its public health implications.
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Childers, A. B., E. E. Keahey, and A. W. Kotula. 1977. Reduc-
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Edel, W., M. van Schothorst, P. A. M. Guin£e, and E. H. Kampelmacher.
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Groves, B. I., N. A. Fish, and D. A. Barnum. 1970. An epidemiolog-
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Gustafson, R. H. 1975. Antibiotic sensitivity in Salmonella iso-
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Linton, A. H., K. Howe, C. L. Hartley, M. Clements, and A. D.
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_
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Mosley, E. B., P. R. Elliker, and H. Hays. 1976. Destruction of
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Patterson, J. T. 1969. Salmonellae in meat and poultry, poultry
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Appl. Microbiol. 17:899-902.
Representative terms from entire chapter:
antibiotic resistance
