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APPENDIX B
POSS IBLE H~ MATH EFFECTS
OF SUBTHERAPEUTIC ANTIMICROBIAL USE AS PESTICIDES
Robert N. Goodman1
The need for antibiotics to control bacterial diseases is
greater for perennials than it is for annuals because annual
plants (e.g., wheat, soybeans, tomatoes, etc.) can be bred
for resistance to diseases more quickly. Consider how few new
varieties of apples have appeared on the market during the past
25 years. However, if antibiotics are used to control a disease,
the emergence of resistance to that antibiotic is greater when
a species remains in place for decades and is treated annually
for the same bacterial disease. Therefore, the problem of re-
sistance to antibiotics must be evaluated in these circumstances.
As early as the 1950's, investigators were aware that treat-
ment of plants with antibiotics could result in the emergence of
antibiotic-resistant organisms and allergenic effects in people who
applied the pesticides as well as in the consumers of the treated
plants (Logue _ al., 1958~. Among the earliest studies on the
mode of uptake of antibiotics by plants and their mode of action
against the organisms causing plant disease were those of Goodman
and Dowler (1958) and Goodman and Goldberg (1960~. Subsequently,
the ease with which resistance to streptomycin might be developed
In vitro by the target organism Erwinia amylovora was studied
and the resulting antibiot~-resistant organisms were used as
markers to study pathogenesis of plant disease (Ayers et al.,
1979; Goodman, 1963~. In further studies, antibiotics were used
to develop selective media to isolate specific bacterial species
(Crosse and Goodman, 1973~.
ANTIBIOTICS AS PESTICIDES
It is difficult to determine the types and quantities of
antibiotics used as pesticides since exact production figures are
regarded as confidential information by industry. Nonetheless,
some estimates can be provided.
The primary antibiotic used to control plant disease is
streptomycin. Throughout the United States, approximately 10,000
kg of streptomycin is used in a typical year for various diseases,
Department of Plant Pathology, University of Missouri, Columbia.
79
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80
predominantly fire blight in apples and pears. The use of strep-
tomycin against bacterial spot of tomatoes and peppers, soft rot
of potatoes, bacterial blight of celery, and tobacco pathogens
seems to be increasing as does its application to beans to con-
trol halo blight.
Approximately 1,000 kg of tetracycline is used annually
to control fire blight of apples and pears (when resistance to
streptomycin is a problem) nationwide and bacterial spot of
peaches in the Eastern United States. This amount also includes
administration of tetracycline by infusion to control the infec-
tion of palm and other ornamental species by mycoplasmas. These
amounts are approximate and vary, often substantially, from year
to year with disease prevalence (Pfizer, Inc., personal communi-
cation, 1979~.
THE USE OF PENICILLIN TO CONTROL PLANT PATHOGENS
There is no evidence to indicate that penicillin is used to
any extent to control plant disease.
Most plant pathogens are Gram negative, and only members
of the genus Corynebacterium, which comprise comparatively few
plant pathogenic species, are Gram-variable and sensitive to
penicillin. Hence, the value of the penicillins as therapeutic
agents for plant diseases is extremely low. This antibiotic
might have limited future application since some pathological
disorders in plants that were previously believed to be of viral
origin have recently been shown to be caused by rickettsia-like
organisms (RLO) and to be unexpectedly sensitive to penicillin
(Markham et al., 1975; Ulrychova' et al., 1975~. Where penicillin
therapy is being tested experimentally, the most common route
of administration is infusion.
THE DISPOSITION OF ANTIBIOTICS USED AS PESTICIDES
Antibiotics applied to plants have a relatively short
half-life and undergo a tremendous dilution factor when applied
either as a foliar spray or through infusion (Ulrychova' et al.,
1975~. Streptomycin may persist in plant tissues for more than
a year (Goodman, 1962, 1963~; however, once these tissues are
exposed to natural decay processes, antibiotics are quickly
degraded.
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81
INGESTION OF ANTIBIOTIC RESIDUES BY ANIMALS AND HUMANS
Both humans and animals could be exposed to antibiotics used
as pesticides as a result of ingesting apples, pears, and peaches;
however, the levels in pears at harvest are below those detectable
by sensitive bioassay (Goodman, 1962~.
Antibiotic bioassay procedures were developed for assaying
antibiotic residues in fruit and vegetable tissue (Goodman et al.,
1958; Morgan et al., 1955~. The residual levels determined by
these procedures were subsequently used as the basis for feeding
trials with volunteers (Goldberg et al., 1961~. Ingestion by ani-
mals is not a real concern at present since plants used as animal
feeds are not being treated with antibiotics for disease control.
There has been a great deal of experimentation to disinfest
and disinfect seeds assumed to be contaminated or infected by bac-
terial pathogens (Lockhart et al., 1976;- Sutton and Bell, 1954~.
Although this type of antibiotic therapy has not been used widely
in general practice, this technique is fairly promising and should
not contribute a significant hazard to the health of animals or
humans. It appears to be the ideal process for controlling plant
diseases, particularly when resultant antibiotic residues would be
at low levels. The dilution of antibiotic concentrations in the
germinating seedlings would continue through growth and maturity
of the plant. At harvest, concentrations of the antibiotic in
tissue would be beyond detection (Goodman, 1962~.
BACTERIAL RESISTANCE
The emergence of resistance in target organisms resulting
from prolonged use of antibiotics under field conditions has
concerned plant pathologists for some time. In the spring of
1953 streptomycin was first used in Missouri to control Erwinia
amylovora, a Gram-negative member of Enterobacteriaceae that
causes blight in apples and pears (Murneek, 1952~. Since that
time, streptomycin has been used regularly in the fruit-growing
regions of Missouri and other states. There has been no evidence
of the emergence of resistant strains of E. amylovora in Missouri,
although there have been frequent efforts to detect resistance in
that state and in New York where streptomycin has been used for
almost three decades (Beer and Norelli, 1976~. However, in 1971
California investigators found considerable evidence that resist-
ance to streptomycin has emerged in E. amylovora (Moller et al.,
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82
1972), possibly because there have been significantly more appli-
cations of streptomycin per growing season in orchards in the West
than in the East.
In apple orchards in Missouri and in the Eastern States strep-
tomycin is used to control fire blight an average of 3 to 4 times
(a maximum of 6 times) during the growing season. However, the anti-
biotic has been applied as many as 13 to 15 times in pear orchards
in the Far West where the disease develops continuously over the
longer growing season. The selective pressure of 15 applications
of streptomycin clearly uncovered those members of the E. amylovora
population that were resistant to streptomycin, in some cases in
concentrations as high as 500 ~g/ml (Moller et al., 1972~. This has
never occurred in orchards in the East. Furthermore, laboratory
attempts to develop streptomycin-resistant mutants of E. amylovora
are successful only with the greatest difficulty (Shaffer and Goodman,
1962).
Using the gradient plate technique, restreaking an inoculum
on plates containing streptomycin in increasing concentrations from
O to 10 Vigil, from O to 100 ~g/1, and, finally, from O to 1,000
g/ml eventually produces mutants with resistance to 1,000 ~g/ml
after 35 to 40 days. Apparently, the frequency of mutations with
significant resistance to streptomycin in this organism is extremely
low.
By far the largest number of species of bacterial plant patho-
gens with resistance to antibiotics are in the genus Pseudomonas,
and the second largest number reside in the genus Xanthomonas (yellow
Pseudomonadaceae). Antibiotics have been used for many years in
attempts to control diseases caused by these bacterial species.
However, after only two or three applications it became apparent
that large proportions of resident populations were not susceptible
to concentrations of antibiotics well over 500 ~g/ml (Cox and Hayslip,
1957; Crossan and Krupka, 1955~. Hence, the efficacy of antibiotics
for the control of bacterial diseases has been narrowed to precious
few species.
HISTORY OF ANTIBIOTIC USE AS PESTICIDES
The first report of an antibiotic used to control a plant bacterial
pathogen appeared as a note in Phytopathology in 1952. The antibiotic
was thiolutin, and the researcher was Murneek (1952~. Since that time,
almost all antibiotics with either antibacterial or antifungal activity
have been screened at one time or another against a wide spectrum of
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83
pathogens affecting plants (Goodman, 1959). Antifungal antibio-
tics have been successful only upon rare occasions, the most
effective being cycloheximide (Whiffin, 1950~. However, with
the advent of systemic as well as prophylactic organic fungicides,
interest in antifungal antibiotics to control fungal plant dis-
eases waned precipitiously. The use of streptomycin has persisted
for approximately 26 years and is now an accepted practice in the
production of apples and pears and in many parts of this country.
Recently, there has been renewed interest in the use of the tetra-
cyclines to control infections of a number of ornamental plants,
especially southern palms, by mycoplasma-like organisms (MOO).
Experiments have shown that infusion of 1 to 1.5 g of oxytetracy-
cline in 10 to 20 ml of water into a single palm tree causes
remission of the disease for more than a year (Arai et al., 1967;
Bowyer and Calavan, 1974; McCoy and Gwin, 1977; Rosenberger and
Jones, 1977~. As mentioned previously, MLO disorders of plants,
formerly thought to be viral in origin, seem to be adequately con-
trolled by penicillin (Markham et al., 1975; Ulrychova et al.,
1975).
EPIDEMIOLOGICAL STUDIES
Perhaps the single most important question that should be
asked in epidemiological studies is whether the transfer of anti-
biotic resistance genes from the ubiquitous colifonms to plant
bacterial pathogens, or vice versa, has resulted from the use of
antibiotics to control plant diseases. Experiments that have
been conducted In vitro clearly show that resistance genes can be
transferred from Escherichia cold and Shigella flexneri to Erwinia
amylovora under laboratory conditions (Chatterjee and Starr,
1973a) and that reciprocal transfer of resistant genes from E.
amylovora to E. cold and other human and plant pathogens also occur
_
(Chatterjee and Starr, 1973b). One must ask whether the levels of
antibiotic titer achieved in the control of plant diseases, either
by infusion or spray application, are sufficiently high to support
the emergence of the resistant forms of pathogens or epiphytic
saprophytic species (U.S. Environmental Protection Agency, 1978~.
Rollins _ al. (1975) reported that in a 44-day feeding ex-
periment more than 2 but less than 10 fig of oxytetracycline per
gram of diet is required to increase significantly the proportion
of resistant colifonm bacteria in the intestine of a dog. The
infusion of pear trees with oxytetracycline results in residues of
approximately 0.0043 ~g/ml oxytetracycline in plant tissue, less
than 1/500 of the amount known to select for resistant microflora
when administered daily. However, higher levels of streptomycin
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84
have been observed (Goodman, 1959~. Hence, it is reasonably
clear that the treatment of plant tissue with antibiotics to
control plant disease can and does result in comprehensive
residual levels of these substances.
Concentrations likely to be found in plant tissue can,
after prolonged feeding periods, give rise to the development
of resistant coliforms in the gut flora of laboratory animals
(Goldberg et al., 1958, 1959) and humans (Goldberg et al., 1961~.
This was observed with both streptomycin and oxytetracycline.
The investigators also noted that the resistant organisms were
transient in the gut flora of the test subjects. Unfortunately,
comprehension of R plasmids at that time was nil, and further
study of specific antibiotic-resistant isolates was not attempted.
Recent studies have addressed the emergence of tetracycline
resistance in humans exposed to subtherapeutic levels of this
antibiotic (Graber et al., 1979~. The resulting data are not
particularly conclusive (Goldberg et al., 1959) because the study
was not as comprehensive as it might have been. Future studies
should use larger populations. Perhaps then more meaningful com-
parisons could be made.
The experiences with oxytetracycline or tetracyclines as
pesticides have not been sufficiently long nor have they been
sufficiently widespread to provide enough test subjects for com-
prehensive epidemiological studies among agriculturalists. This
is not the case, however, for streptomycin. As indicated earlier
in this report, streptomycin has been used in apple orchards for
the control of E. amylovora on a regular and routine basis since
1953 (Goodman, 1953~. The applicators of the antibiotic, at least
in Missouri, represent a stable population that can be tested for
both the presence of resistant coliforms in their gut flora and
inordinate allergenic responses to this antibiotic. The studies
of Chatterjee and Starr (1973a, b) clearly show that R factors
from coliforms can be transferred to E. amylovora and other enter-
obacteria and that the reverse is also possible. The extent to
which resistant coliforms occur in the applicators of streptomycin
in Missouri might be reinvestigated (Goldberg et al., 1958, 1960~.
Research should be conducted to determine categorically that strep-
tomycin does not have some adverse physiological affects on agri-
cultural workers exposed to this drug. The applicator population
in Missouri could be examined for an inordinate number demonstrat-
ing the clinical symptoms involved. There is little doubt that the
examinations could be conducted on between 20 and 25 adult males
who have applied streptomycin in apple orchards annually for at
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85
least 10 years. The concentrations of the antibiotic sprays (at
150 ~g/ml) applied by these men are extremely high. The applica-
tors could be examined in winter prior to the short spraying
season, which begins in m~d-April and ends in June, and at the
termination of the spraying season. Residual levels of streptomy-
cin could be sought in both blood and stool samples, and the latter
could also be examined for the presence of resistant coliforms.
Patch tests or other procedures for allergenic responses could be
performed (Goldberg et al., 1960~.
RESISTANT MYCOPLASt~S
There is no evidence to suggest that administration of tetra-
cyclines to plants has resulted in the emergence of antibiotic-
resistant mycoplasmas. Failure to detect resistance, however, may
be the result of technical problems related to the culturing of
mycoplasmas or MLO's found in plants In vitro. Consequently, whether
resistance, if it occurs, is due to plasmids cannot be determined.
The manner in which oxytetracycline is used to control MLO disorders,
mainly by infusion or injection procedures (Rosenberger and Jones,
1977), appears to present little risk of hazardous exposure either
to the general population or to the applicators. Simple procedures
such as the use of rubber gloves and masks should protect the appli-
cator from contamination. The low volatility and small concentra-
tions of these antibiotics in plant tissue suggest that secondary
contamination of humans would also be rather rare. Under unusual
circumstances, however, such as when animals ingest treated plant
tissue in large quantities, resistant microorganisms might be found
in their gut flora.
POSSIBLE HEALTH HAZARDS TO HUMANS FROM R-FACTOR TRANSFER
Another point that might be discussed more fully concerns the
development of resistance to streptomycin in Erwinia amylovora, a
species that is currently combatted routinely with this antibiotic.
Brief mention was made earlier in this report that the emergence of
resistance to streptomycin by this species is rare in nature but
when it has occurred it has been widespread. Laboratory studies
have shown that streptomycin-resistant mutants of Erwinia amylovora
are extremely rare (Shaffer and Goodman, 1962~. Following are some
features of the streptomycin-resistant mutants that have been re-
covered. First, many are not as well adapted to the natural environ-
ment as the wild type virulent forms. They are often completely
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86
avirulent, lacking extracellular polysaccharide (EPS) (Ayers
et al., 1979), which some investigators believe to be necessary,
_ priori, for pathogenicity. It also appears that the production
of EPS is not controlled by plasmids.
Antibiotic usage to suppress or eradicate bacterial infec-
tion in plant cuttings, which are used in vegetative propagation,
will probably be expanded. This type of chemotherapy can offer
minimal opportunity for the emergence of significant levels of
antibiotic resistance in the gut flora of the applicator or of
the eventual consumer of the plant. However, plant pathogens
carrying the R factor may emerge.
The possible increase in the environment of plant pathogens
carrying R factors and their transfer to a ubiquitous plant sapro-
phyte such as Erwinia herbicola and vice versa may be possible.
Furthermore, human clinical strains of E. herbicola appear to
-
possess similar plasmid transfer capabilities (Chatterjee et al.,
1978~. However, the amount of antibiotics contributed to the
environment via plant pesticides must be comparatively small.
Unfortunately, it-factor transfer In the field from plant pathogens
to saprophytes on human or animal pathogens has not been adequately
assessed (Cho et al., 1975~. A few well conceived field experi-
ments conducted regionally could provide the necessary answers and
the likely assurances that antibiotics as plant pesticides do not
constitute a significant hazard to human health.
CONCLUSIONS
Although exceptional progress has been made in the control
of fungal diseases of plants, the control of bacterial disorders
in plants has been only minimally successful. In general, the
use of antibiotics as pesticides represents an extremely small
fraction of the total use of antibiotics in therapy of humans and
animals and in the production of animal tissues as food. In the
few instances when antibiotics have been successful there appear
to have been no obvious deleterious effects to either the applicator
or the consumer. Experimentation exploring new and improved anti-
biotics to control bacterial diseases of plants should be synchro-
nized with efforts in laboratories that can adequately test the
safety of the new procedures.
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87
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Ishida. 1967. Ef feet of antibiotics on the growth of
Mycoplasma. J. Antibiot. (Tokyo) Series A 20:246-253.
Ayers, A. R., S. B. Ayers, and R. N. Goodman. 1979. Extracellu-
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Beer, S. V. 1976. Fire blight control with streptomycin sprays
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Beer, S. V., and J. L. Norelli. 1976. Streptomycin-resistant
Erwinia amylovora not found in western New York pear and
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Bennett, R. A., and E. Billing. 1975. Development and proper-
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Bowyer, J. W., and E. C. Calavan. 1974. Antibiotic sensitivity
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Chatterjee, A. K., and M. P. Starr. 1973a. Gene transmission among
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Chatterjee, A. K., and M. P. Starr. 1973b. Transmission of lac
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Chatterjee, A. K., M. K. Behrens, and M. P. Starr. 1978. Genetic
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Cox, R. S., and N. C. Hayslip. 1957. Recent developments on
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_
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go
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258.
-
Representative terms from entire chapter:
plant disease
