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OCR for page 203
APPENDIX G
TRANSMIS S ION OF FOOD-BORNE D ISEASE S
IMPLICATIONS OF THE SUBT~RAPEUTIC USE OF ANTIMICROBIALS
,
Jackson S. Risers
The major food-borne bacterial diseases in the United States
are caused by salmonellae, staphylococci, and Clostridium botulinum
(Center for Disease Control, 1977b) (Table 1~. The number of out-
breaks of food poisoning by salmonellae and staphylococci is with-
out doubt greatly underestimated because many outbreaks are unre-
ported and undiagnosed. Because of its acute onset and rapid course,
staphylococcal food poisoning, in particular, is not often brought
to the attention of any medical authority.
The statistics of C. botulinum food poisoning, because it is
a much more serious disease in terms of its life-threatening poten-
tial, are much more accurate. However, since there is no known or
suspected connection between _ botulinum food poisoning and the
use of antibiotics at subtherapeutic levels in animal feeds, it
will not be discussed further in this paper.
Salmonellosis is ubiquitous. It occurs usually as entero-
colitis, usually of only a few days duration, and it is frequently
caused by food-borne salmonellae. This form of salmonellosis is
acutely uncomfortable and may cause humans to be absent from work
for one or several days. The disease frequently involves a visit
to a physician and, occasionally, hospitalization for a short
period. It is generally agreed that antibiotic treatment is con-
traindicated since it does not shorten the course of the disease
or lessen the severity of the symptoms (Hook and Johnson, 1972~.
Moreover, such treatment is likely to prolong the fecal excretion
of the organisms (Aserkoff and Bennett, 1969~.
SALMONELLOSIS IN FOOD ANIMALS AND HUMANS
Salmonellae infect both warm-blooded and cold-blooded ani-
mals. In 1977, 5,243 Salmonella isolates from nonhuman sources
were reported to the U.S. Department of Agriculture (USDA) and
the Center for Disease Control (CDC). Of the total nonhuman iso-
lates, 28% (1,474) were obtained from chickens and turkeys, 25%
(1,313) were of porcine origin, and 14X (713) were of bovine origin
(CDC, 1979~. Five of the 10 serotypes most frequently isolated
Consultant, Agricultural Division of American Cyanamid Co.,
Princeton, N.J.
203
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204
TABLE 1
Confirmed Outbreaks of Food-Borne Disease, by Etiology, 1976
Outbreaks t Cases
Organism Number ~ Number %b
Salmonella 28 21.2 1,169 32.7
Staphylococcus 26 19. 7 930 26.0
Clostridium botulinum 23 17.440 1.1
Clostridium perfringens 6 4.5509 14.2
Shigella 6 4.5273 7.6
Bacillus cereus 2 1. 563 1.8
Yersinia enterocolitica 1 0.8286 8.0
TOTAL 92 69.63,270 91.4
From Center for Disease Control, 1977b.
Percent of all (bacterial, chemical, parasitic, and viral) food-borne
disease outbreaks in the United States.
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205
from animals (Table 2) were also among the 10 serotypes most
f requently isolated from humans (Table 3 ~ . S. typhimurium, in-
cluding var. Copenhagen, comprised 35. 5% of the Herman isolates
reported and 19. 7% of the isolates from nonhuman sources. It is
by far the most frequently isolated serotype.
Although the greatest number of isolates from nonhuman
sources was obtained from swine, the inc idence of Salmonella In
healthy market-ready swine varies greatly trom place to place.
In 1975, a survey was conducted at a slaughterhouse in each of
three hog-producing areas (Gustafson et al., 1976~. The purpose
of the survey was to determine the incidence of Salmonella in
healthy swine at market and to see what percent of them might be
harboring salmonellae with resistance to more than one antibiotic.
Of 151 hogs sampled in Pennsylvania, 54 (35.77) had salmonellae
and none had multiply resistant salmonellae. Of 251 hogs sampled
in Iowa, 26 (10.3%) had salmonellae and one had multiply resistant
salmonellae. Of 256 hogs sampled in Georgia, 215 had salmonellae
(83.9%) and 9 (3.5%) had multiply resistant salmonellae. These
data suggest that only a few hogs harbor multiply antibiotic-
resistant salmonellae.
THE EFFECT OF SUBTHERAPEUTIC TETRACYCLINES ON SALMONELLAE IN
_
DOMESTIC ANIMALS
In April 1973, the Food and Drug Administration (FDA) issued
a statement requiring the manufacturers of tetracyclines and cer-
tain other drugs to show, by April 20, 1974, that the use of these
drugs in animal feeds did not increase the Salmonella reservoir in
animals and poultry raised for meat (FDA, 1973~.
low.
The FDA Bureau of Veterinary Medicine (BVM) then issued a set
of human health safety criteria for the drug manufacturers to meet
in order to demonstrate that the Salmonella reservoir in meat ani-
mals was not increased by the subtherapeutic levels of the drugs in
feed. BVM and the manufacturers designed protocols for experiments
to determine the effect of the drug on the quantity, prevalence,
and duration of shedding and the resistance characteristics of the
Salmonella in animals consuming subEherapeutic levels of antibiotics
in their feed. By April 20, 1974, these experiments had been con-
ducted and the manufacturers had reported the results to the BVM.
The experiments that were published are described briefly be
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206
TABLE 2
10 Someone Z Ma Serotypes Most Frequently Isolated from
Nonhuman Sources, 1977
Serotype
Number of isolates reported, by source b
Feed Chickens Turkeys Swine Cattle TOTAL
typhimurium ~10 67 17 194 310 1,033
anatum
derby25 514 264 1 378
cholerae-suisd1 00 332 4 345
11 11107 69 24 314
agona3 2535 28 85 271
Heidelberg1 75113 3 1 236
saint-paul3 2182 7 1 219
san-die~o
Panama 9 012 147 1 188
infantis 3 818 18 7 165
0 1104 1 0 112
.
TOTAL 66 267 5921,063 4343,261
PERCENT OF TOTAL OF
ALL SEROTYPE S
ISOLATED 39 44 6881 6162
TOTAL OF ALL SEROTYPES
ISOLATED 168 608 8661,313 7135,243
oFrom CDC, 1979.
Also includes isolates from other animals and environmental samples.
CIncludes var. Copenhagen.
War. kunzendorf.
. _
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207
TABLE 3
10 Sa~oneZZa Serotypes Most Frequently Isolated
from Human Sources, 1977
1
i
SerotypeNumber Percent Rank in 1976
typhimurium9,690 35.3 1
newport2,187 8.0 4
Heidelberg1,741 6.3 2
enteritidis1,472 5.4 5
infantis1,304 4.7 6
agona1,229 4.5 3
saint-paul580 2.1 7
typhi549 2.0 8
montevideo470 1.7 12
oranienburg440 1.6 9
TOTAL19,662 71.6
TOTAL OF ALL SEROTYPES27,462
a
From CDC, 1979.
bIncludes var. Copenhagen.
100
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208
EXPERIMENTS IN SWINE
Gutzmann _ al. (1976) divided 30 5- to 6-week-old pigs, each
weighing approximately 7 kg, into three groups of 10. One group
was given chlortetracycline at 220 g/metric ton of feed. A second
group was given AUREO S.P 250, at a level that supplied 110 g of
chlortetracycline, 110 g of sulfamethazine, and 55 g of penicillin
G per metric ton of feed.
The third group was given the nonmedicated basal ration. On
the sixth day of medication, all three groups were given in their
feed 100 billion cfu (colony-forming units) per pig of a nalidixic-
acid-resistant, tetracycline-sensitive strain of Salmonella typhi-
murium of swine origin. A fourth group of 10 pigs from the same
breeding was kept as an unmedicated, uninfected control. Fecal
samples were taken at 1, 2, 6, 9, 15, 22, and 26 days after admin-
istration to detect and enumerate salmonellae.
As shown in Figure 1, chlortetracycline at 220 g/metric ton
of feed substantially reduced the number of salmonellae shed. The
effect of AUREO SeP 250 was somewhat less, but calculation of the
total area under each curve, equivalent to the total number of sal-
monellae shed by each group, showed a 22.5% reduction in the number
of salmonellae shed by the group on chlortetracycline and a 9.6Z
reduction in salmonellae shed by the group on AUREO S.P 250. The
duration of shedding and number of animals shedding salmonellae was
no different in the medicated than in the unmedicated groups. By
plating the fecal samples on agar containing nalidixic acid and
chlortetracycline, it was possible to learn whether the infecting
salmonellae had acquired tetracycline resistance from the tetracy-
cline-resistant E. cold which the pigs were known to have. Only a
-
few tetracycline-resistant Salmonella were found in six of 172
fecal samples, and these occurred in unmedicated as well as medi-
cated pigs. Thus, it could be concluded that the drug had not
selected for resistance.
An experiment by another manufacturer (Evangelist) et al.,
1975; Girard _ al., 1976) was conducted in a manner very similar
to that described above except that oxytetracycline at 150 g/ton
of feed or oxytetracycline at 150 g plus neomycin atj150 g/ton of
feed was given to medicated groups. Figure 2 shows the quantity
of Salmonella tYPhimurium shed.
As in the previously described experiment the medicated groups
shed substantially fewer salmonellae than did the unmedicated group.
OCR for page 209
209
7
6
in
8
a, 5
-
c'
lo- 4 _
o
3
; _
2 _
1
< Unmedicated
in\ I\ AUREO S' P 250 (to supply 110 9
\ \ chlortetracycline, 1109 sulfametha
zine and 55 9 penicillin G/metric
If feed)
\ ~
hi,
Chlortetracycline,
ZO g/metric ton of feed
\
_N
in,
in_
-_
1 1 1 1 1 1 1
1 2 6 9 15 22 26
DAYS (Postinoculation with 1 X 1 o1 1 cfu S. typhimurium)
FIGl~RF 1. Summary of Salmonella typhimurium isolations from
swine. From Gutzmann_ al., 1976, with permis-
sion from the authors and the American Journal of
Veterinary Research.
OCR for page 210
210
J
m
-
-
7r
Unmedicated
6
4
\~
1
lo
Oxytetracycline
_ 150 g/ton
\
\
Neomycin +
Oxytetracycline,
~50 9 each/ton
-
-
-
I I I
7 10 14 21 28
1 1 ,
DAYS (Postinoculation with 1.4 X 1 o1 1 salmonellae)
FIGURE 2. Number of salmonellae recovered from swine feces.
From Evangelisti et al., 1975, and Girard et al.,
1976.
OCR for page 211
211
There was no difference in duration of shedding between the medi-
cated and unmedicated groups. Only two resistant isolates were de-
tected in the medicated groups. None was seen in the unmedicated
group.
EXPERIMENTS IN CALVES
.
Layton et al. (1975) divided 24 4-week-old calves into three
groups of eight calves each. One group was given 350 mg of
chlortetracycline per head per day in feed, and the other group
was given 350 mg of chlortetracycline plus 350 mg of sulfamethazine
per head per day in feed. These levels were supplied by a weighed
amount of a concentrate containing the desired amount of the anti-
microbial. The third group was not medicated. After 5 days of
medication, each calf 9as infected orally via stomach tube with
approximately 6.5 x 10 cfu of a nalidixic-acid-resistant, anti-
biotic-sensitive strain of Salmonella typhimurium of bovine ori
gin. Fecal samples were obtained at 1, 2, 6, 9, 15, 22, and 26
days after infection and examined for the number of salmonellae.
Figure 3 shows that the number of salmonellae from the medicated
groups was lower than that from the unmedicated group at each
sampling. The group on chlortetracycline shed 38.0Z fewer salmo-
nellae. The group on the combination shed 28.6% fewer salmonel-
lae. The duration and prevalence of shedding was slightly greater
in the unmedicated than in the medicated group. Salmonellae that
were resistant to chlortetracycline were recovered from five calves
in the unmedicated group, three calves in the chlortetracycline-
medicated group, and one calf in the group on the combination.
Only a very small fraction of the salmonellae In any of these sam-
ples was resistant, and in only two instances were resistant orga-
nisms isolated more than once from the same calf. In no instance
did the resistant organisms become established in a calf.
In another experiment (Evangelist) et al., 1975; Girard et ale
1976), run in much the same way, three groups of 10 calves each,
averaging approximately 85 kg per calf, were given feed containing
oxytetracycline at 350 mg per head per day or oxytetracycline and
neomycin in an amount calculated to give each calf 350 mg of each
drug per head per day. One group was not medicated. The results
of this experiment were very similar to the previously described
experiment in calves. The number of salmonellae shed is shown in
Figure 4. The duration and prevalence of shedding in the medicated
groups were considerably less than in the unmedicated group. No
tetracycline-resistant salmonellae were detected.
OCR for page 212
212
.~
/
J
l
105
104
in
LU
c'
1 03
1o2
lo1
_ ~\
~ \` \Nonmedicated
\ ~ \ Chlortetracycline + Sulfamethazine
\~350 mg each/head/day
~ \
Chlortetracycline, 350 mg/head/da~',
1 1 1 1 1 1 1
1 2
6 9
15
22 26
DAYS (Postinoculation with 6.5 X 109 cfu S. typhimurium)
FIGURE 3. Salmonella typhimurium isolated from feces of infected
.
calves (expressed as geometric means). From Layton et
al., 1975, with permission from the authors and Zentral-
blatt fuer Veterinaermedizin Reibe B.
OCR for page 213
213
6
. ~
2
~ 2
LL
J
m
4
o
/\lonmedicated
Oxytetracycl ins,
350 mg/head/day
r~~l ~~ I ---r~~~'~l~~
2 4 7 10 14 21 28
Neomycin +
\ Oxytetracycline,
350 mg each/head/day
~'
\/ ~-~
DAYS (Postinoculation with 1.10 X 1 o1 ] salmonellae)
FIGURE 4. Number of salTnonellae recovered from calves feces.
From Evangelisti et al., 1975, and Girard et al.,
1976.
OCR for page 251
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OCR for page 252
252
1975 outbreaks of disease from Staphylococcus exceeded those from
Salmonella, although Salmonella ranked first in 1976. Because
staphylococcal enterotoxin is heat-stable, it is not destroyed by
cooking. While meat products are frequently implicated in outbreaks
of staphylococcal food-poisoning, investigation frequently reveals
that the food has been contaminated by a food handler who is a
carrier of an enterotoxin-producing strain of staphylococcus or who
has a staphylococcus-infected wound (Bryan, 1978; CDC, 1977b).
This contamination of meat by staphylococci of human origin
was confirmed in a study by Sinell et al. (1975) in the Federal
Republic of Germany. These investigators examined 3,065 cultures
of staphylococci from slaughtered pigs, meat plant equipment, and
other sources including human beings. Strains originating from
swine produced significantly less (21%) enterotoxin than did strains
from clinical specimens obtained in hospitals (approximately 40%~.
Enterotoxin was not produced by any of 39 phage group II strains, a
group that is considered to be specific to animals. The strains
from animals were more frequently resistant to antibiotics than were
the strains from the hospital. In 1973, before the German govern-
ment banned the use of tetracycline in animal feed, there was a high
incidence of resistance to tetracycline. In 1974, after the ban,
a survey showed that the incidence of resistance to tetracycline in
cultures from pigs had dropped but that the incidence of resistance
to bacitracin had become very high. Strains of staphylococci iso-
lated in a meat plant in 1974 continued to have a high incidence
of resistance to both tetracycline and bacitracin.
Domestic animals and pets can become carriers of strains of
staphylococci of phage types that are frequently associated with
human disease (Pagano et al., 1960~. During the school year 1956-
1957 an unusual number of senior students at the University of
Pennsylvania School of Veterinary Medicine were afflicted with
furuncles, deep cutaneous abscesses, cellulitis, and paronychia.
The epidemic continued through the following 2 years. Staphylo-
coccus aureus phage type 80/81 was repeatedly isolated from these
.
lesions. This strain was resistant to penicillin, streptomycin,
the tetracyclines, and, occasionally, to erythromycin but was
sensitive to chloramphenicol and novobiocin.
A survey of students, faculty, and other employees of the
school revealed that only the senior students who spent much of
their time in the clinic and the faculty of the clinic had a high
incidence of this strain in their external Hares. They frequently
became carriers after contact with a student with an active lesion.
OCR for page 253
253
Sporadic culturing of swabs from lesions of animals in the clinic
revealed the existence of type 80/81 strain on only three occa-
sions, whereas random swabbing of the nostrils of the animals failed
to show it. In 1959 a systematic swabbing of the nostrils of the
animals showed the strain to be present in cows, horses, goats, and,
most frequently, in dogs. There was no proof that the organism was
transmitted from an animal to a human.
The animal-to-person transfer of antibiotic-resistant S. aureus
of human type 80/81 was suggested by Wallace et al. (1962~. Eight
of 287 cows tested yielded staphylococci type 80/81 with resistance
to streptomycin, tetracycline, and penicillin, and sensitivity to
chloramphenicol, neomycin, novobiocin, oleandomycin, and carbomycin.
The cows all had mastitis. Some cases were so severe that the ani-
mals had to be destroyed.
Three people in the family that operated the dairy studied by
Wallace _ al. also yielded type 80/81 with the same resistance
pattern when swabs were taken from their nares and from two boils on
the father at different times and from one boil and the sore throat
of an 18-month-old child. Here again the spread from animal to per-
son is putative. The organism could have spread from the humans to
the animals. Antibiotic resistance in staphylococci from mastitic
cows is common because large amounts of antibiotics are used in
intramammary infusions to treat the mastitis, which may clear up
but frequently recurs.
Another study on antibiotic-resistant S. aureus from dairy herds
was reported by Devriese and H~mmez (1975~. In 1971 and from July
1972 to June 1973 they isolated 68 methicillin-resistant strains of
_ aureus from milk samples from mastitic cows in 20 Belgian dairy
herds. In the 1972-1973 survey 52 methicillin-resistant strains
were isolated on nine farms, representing 50% of all S. aureus iso-
lated on those farms. A determination of the biological and phage-
types of the methicillin-resistant strains suggested that they were
actually strains from humans and might have had a common human source,
but that seems highly speculative.
In summary, food poisoning due to Staphylococcus aureus entero-
toxin is frequently reported in the United States, England, and Wales.
It often involves meat products, but upon investigation it is fre-
quently found that the food was contaminated by a human carrier or
one with a staphylococcal lesion. There is no evidence that the use
of antibiotics in animal feed is in any way involved.
OCR for page 254
254
Frequently, staphylococci of phase types usually considered to
be of human origin have been found in pets and dairy cows. It is
likely that these organisms were transferred from humans and were
resistant when they were acquired by the cows, but they may have
become resistant during treatment for mastitis by antibiotic intra-
mammary infusion. It is highly unlikely that the resistance arose
due to the use of antibiotics in the feed of the cows since that is
a rather uncommon practice in the dairy industry in the United
States.
CONCLUSIONS
Salmonellosis is the most important of the food-borne diseases
that may be transmitted from animals to humans. There is a large
pool of Salmonella in domestic animals, carcasses are contaminated
with Salmonella at the slaughterhouse, and outbreaks of food-borne
salmonellosis due to contaminated food of animal origin are a seri-
ous threat to human health and an economic problem. It is not clear
that the Salmonella on the food originated in the animals. Moreover,
when antibiotic resistance has occurred, it does not seem to have
been due to the use of antibiotics in animal feed.
It seems likely that antibiotic-resistant E. cold in animals
does not play a significant role in colonizing the human intestine.
If these organisms do colonize temporarily, it is unlikely that they
transfer their R factor to the human flora. Carcasses are contami-
nated at the slaughterhouse with E. coli--some of which is resistant
to antibiotics, but it is doubtful that more than a few of these
organisms reach the consumer. The organisms on the meat are probably
of human or environmental origin.
Plasmids for antibiotic resistance and enterotoxin production
can coexist in an _ cold cell and can be transferred together ex-
perimentally. Cells containing both genes would have no survival
advantage over cells containing the R factor alone in animals
receiving antibiotics in feed since a high percentage of the cells
would already be resistant.
Food poisoning in the United States due to Staphylococcus
enterotoxin is second only to salmonellosis as a food-borne disease.
It often involves meat products, but upon investigation, it is fre-
quently found that the food was contaminated by a human carrier or
one with a Staphylococcus-infected lesion. Staphylococci of phase
types usually considered to be of human origin have been found in
pets and dairy cows. There is no evidence that the use of antibio-
tics in animal feed is in any way involved.
OCR for page 255
255
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OCR for page 256
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r
Representative terms from entire chapter:
frequently isolated
