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Appl Environ Microbiol, May 1998, p. 1975-1979, Vol. 64, No. 5
0099-2240/98/$00.00+0
Effect of Dietary Stress on Fecal Shedding of
Escherichia coli O157:H7 in Calves
William C.
Cray Jr.,
Thomas A.
Casey,*
Brad T.
Bosworth, and
Mark A.
Rasmussen
National Animal Disease Center, Agricultural
Research Service, U.S. Department of Agriculture, Ames, Iowa 50010
Received 2 June 1997/Accepted 8 March 1998
 |
ABSTRACT |
Two groups of calves were subjected to dietary stress by
withholding of food beginning 1 or 14 days after inoculation with 1010 CFU of Escherichia coli O157:H7. Following
treatment, neither group had a significant increase in fecal shedding
of E. coli O157:H7. A third group of calves had food
withheld for 48 h prior to inoculation with 107 CFU of
E. coli O157:H7. These calves were more susceptible to infection and shed significantly more E. coli O157:H7
organisms than calves maintained on a normal diet.
| |
TEXT |
Escherichia coli O157:H7
was first associated with human disease during investigations of two
outbreaks of hemorrhagic colitis in 1982 (23). Traceback
studies support an epidemiological link between human disease and the
consumption of undercooked ground beef in 40% of outbreaks in the
United States (6). The association between E. coli O157:H7 and ground beef has been supported by field surveys
which have identified E. coli O157:H7 in 0.3 to 2.2% of
healthy beef and dairy cattle (1, 8, 20). In cattle, the
organism appears to be confined to the gastrointestinal tract and is
shed in feces (4, 9, 20). During slaughter and processing,
meat surfaces may become contaminated by ingesta or feces on the hide
(13).
Reducing the levels of E. coli O157:H7 organisms that enter
slaughter plants would require two interrelated strategies: (i) reducing the number of cattle shedding E. coli O157:H7 and
(ii) reducing the magnitude of shedding (CFU/gram) by those animals infected with the organism. Both strategies may require identification of E. coli O157:H7 reservoirs and vectors as well as
management practices which facilitate transmission of the organism to
cattle or affect the level of shedding. Because of the persistent,
albeit low, levels of E. coli O157:H7 infection in many
herds, cattle have been considered by some to be a reservoir for the
organism (3, 16, 24). During some on-farm surveys, E. coli O157:H7 has also been isolated from the feces of deer, sheep,
dogs, goats, and a horse, as well as from water troughs, fly trap
samples, and bird droppings (7, 15, 18, 19, 21, 22).
There is evidence that suggests that management practices can affect
the level of E. coli O157:H7 shedding by cattle. Three decades ago, Brownlie and Grau demonstrated that the incidence and
numbers of E. coli and Salmonella sp. organisms
in the rumens and feces of cattle and sheep increased after dietary
and/or transportation stress (5, 10). When cattle are
transported, they may experience food deprivation when food is not
available or is refused. During the 1994-1995 USDA-APHIS National
Animal Health Monitoring System's Cattle on Feed Evaluation, fecal
samples from 100 feedlots were tested for E. coli O157:H7.
Cattle which had recently arrived at feedlots had a prevalence of
3.01%, compared to 1.08% for cattle which had been on feed the
longest (2).
The rumens of well-fed cattle represent a hostile environment to
coliforms (14). In well-fed animals, the metabolic
activities of rumen anaerobes produce concentrations (>100 mM) of
volatile fatty acids and pHs of 6.0 to 6.8 which suppress coliform
populations (17). When food is withheld from cattle for 24 to 48 h, reduced levels of substrates for anaerobes result in a
decrease in rumen volatile fatty acid concentrations (<50 mM) and an
increase in rumen pHs (>7.0) (17). In vitro studies have
shown that E. coli isolates, including serotype O157:H7, are
more inhibited by rumen fluid collected from well-fed cattle than from
cattle fasted for 24 to 48 h (17).
In spite of an understanding of the dynamics of rumen coliform
populations, the relationship between coliform populations in the rumen
and feces is unclear. Coliforms that survive the rumen pass into the
lower gut, where the environment is presumably less harsh. Although
total coliform levels in the feces can fluctuate, the effects of
dietary stress on transient coliform populations passing from the rumen
and on resident coliform populations present in the lower gut are
unknown. Assessing the effects of dietary stress on fecal shedding is
confounded by the observation that in well-fed ruminants, there can be
a 1,000-fold variation in daily fecal coliform shedding by a single
animal (11).
In this study, we tested the effect of dietary stress on fecal shedding
of E. coli O157:H7 in experimentally inoculated 3- to
4-month-old weaned calves. On the farm, calves in this age group may
experience dietary stress due to weaning and changes in housing
conditions. Weaned calves, in some on-farm surveys, had higher
prevalences of shedding than preweaned calves or adults (12,
25) and may be important factors in the spread of the organism
within farms.
Calves were purchased from local farms and were housed in accordance
with the guidelines of the American Association for Laboratory Animal
Care. Calves were housed individually in climate-controlled BL-2
containment barns. Some calves within a treatment group had nose-to-nose contact. The calves were allowed to acclimate to their new
environment for 2 weeks prior to experimentation. The calves were fed
twice daily with both pelleted feed (16% protein, 2.5% fat, 8.0%
fiber) and alfalfa hay cubes (15% protein, 1.5% fat, 25% fiber) in
amounts equal to 1% of their body weights. All calves had free access
to water throughout the experiments. Calves remained healthy following
inoculation with E. coli O157:H7. The calves were subjected
to dietary stress by withholding of food for 2 days (beginning with the
first morning meal on day 1 (0 h) followed by a feeding of one-half the
daily ration on the morning of day 3, after which food was withheld for
another 48 h until the afternoon of day 5). All waste was
sterilized by heat in the National Animal Disease Center sewage
treatment facility.
Dietary stress in recently inoculated calves.
In the first
experiment, five experimental and eight control weaned 3- to
4-month-old calves were divided into two groups, with each group having
control calves. The calves were inoculated by stomach tube with
1010 CFU of E. coli O157:H7 strain 3081, as
previously described (9). All calves were fed after
inoculation. Food was subsequently withheld from the diet-stressed
calves according to the dietary stress protocol. Fresh fecal samples
were collected daily from the calves beginning one morning prior to and
for 7 days postinoculation (p.i.). The samples were immediately
processed. One-gram samples were diluted in phosphate-buffered saline
and then plated on MacConkey agar (for total coliform counts) or
TKASMAC (sorbitol MacConkey containing kanamycin [100 µg/ml;
Sigma], ampicillin [100 µg/ml; Sigma], and tellurite [2.5
µg/ml; Sigma]) and incubated for 16 h at 37°C (9).
Enrichment cultures were prepared by adding 10 g of feces to 100 ml of Trypticase soy broth (BBL) containing 0.15% (wt/vol) no. 3 bile
salts (Difco) and tellurite (2.5 µg/ml; Sigma). Cultures were
incubated for 16 h at 37°C, diluted in phosphate-buffered saline, and then plated on TKASMAC as described above. The sensitivity of the direct plating assay is 50 CFU/g (9).
In previous studies, shedding of E. coli O157:H7 strain 3081 by experimentally inoculated preweaned calves and adult cattle that
were well fed reached a peak during the first week p.i. Shedding followed a downward trend over time until levels were undetectable at 7 to 27 weeks p.i. for preweaned calves and 2 to 14 weeks p.i. for adults
(9). Within each age group, there was wide variation among
individuals in the magnitude of shedding. The peak level of shedding
for preweaned calves was 4.0 × 105 to 1.6 × 109 CFU/g; for adults the level of shedding was 1.2 × 105 to 1.0 × 107 CFU/g. Occasionally,
E. coli O157:H7 shedding by an animal varied 1,000-fold over
several days (9). In the present study, total coliform and
E. coli O157:H7 shedding of the well-fed and diet-stressed groups for days 1 to 7 p.i. were compared by repeated-measures analysis of variance (SAS Institute). Shedding of coliforms and E. coli O157:H7 varied widely among animals of both groups,
as did the day of peak shedding (Fig. 1).
During days 1 to 7, the peak level of shedding of total coliforms was
4.3 × 106 to 1.5 × 108 CFU/g for
the fasted calves and 1.5 × 106 to 1.7 × 108 CFU/g for the well-fed controls. Although the ranges of
peak shedding were similar for both groups, the fasted calves shed more
total coliforms than the well-fed controls (P < 0.04).
The peak level of shedding of E. coli O157:H7 was 2.2 × 105 to 5.8 × 107 CFU/g for the fasted
calves and 1.3 × 105 to 5.6 × 107
CFU/g for the well-fed controls. The difference in E. coli
O157:H7 shedding between the fasted and well-fed calves was not
significant (P < 0.91). In a previous study of
experimentally inoculated calves (6 to 8 weeks old), fecal shedding of
E. coli O157:H7 was variable when food was withheld
(4).
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FIG. 1.
Fecal shedding (day 1 to day 7 p.i.) of E. coli O157:H7 and total coliforms by calves maintained on a dietary
stress regimen and calves that were well fed. Calves were inoculated
with 1010 CFU of E. coli O157:H7 on day 0. Calves on the dietary stress regimen had food withheld for 48 h
beginning on day 1, were fed a one-half ration on day 3, and then were
fasted for 48 h until day 5. (A) E. coli O157:H7
recovered from diet-stressed calves. (B) E. coli O157:H7
recovered from well-fed calves. (C) Total coliforms recovered from
diet-stressed calves. (D) Total coliforms recovered from well-fed
calves.
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|
The absence of an increase in shedding of
E. coli O157:H7 by
the diet-stressed group may have been the result of inhibitory
effects
of inoculation into a well-fed rumen. The significant
increase in total
coliform shedding by the fasted calves is consistent
with the results
reported by Brownlie and Grau (
5) and suggests
that
indigenous coliforms are most likely to proliferate during
dietary
stress.
Dietary stress 2 weeks p.i.
Further experiments were conducted
to determine if dietary stress would cause an increase in E. coli O157:H7 shedding in calves colonized with the organism for 2 weeks. On the morning of day 14 p.i., the inoculated control
calves from the previous experiment were placed on the dietary stress
regimen. The group that had been on the dietary stress regimen for days
1 to 5 p.i. continued to be fed the normal daily ration; however,
these calves were not considered to be concurrent controls. The feces
of both groups were monitored for 7 days thereafter (Fig.
2). For most calves, the differences in
shedding of E. coli O157:H7 organisms from day 14 to day 21 were similar to the individual variations seen in preweaned calves and
adults that are well fed (9). However, calf 1 had a
greater-than-100,000-fold increase in E. coli O157:H7 shedding (Fig. 2B). On the day of peak shedding (day 19), E. coli O157:H7 became the predominant coliform (1.1 × 107 CFU/g of 3.3 × 107 CFU/g [total
coliforms]) and exceeded what had previously been the highest E. coli O157:H7 shedding value (1.3 × 106 CFU/g)
observed during the first week p.i. Prior to dietary stress, the
E. coli O157:H7 daily shedding pattern of calf 1 was similar to other members of the group, and its response to dietary stress could
not be predicted. The day following peak shedding, the calf's E. coli O157:H7 counts had declined to less than 1% of total
coliforms. The shedding by calf 1 suggests that dietary stress may lead
to increased shedding of E. coli O157:H7; however, we think
that suppressive ecological factors such as the presence of competing organisms, bacteriocins, lysis by phage, and predation by protozoans may have a role in limiting the increase.
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FIG. 2.
Fecal shedding (day 14 to day 21 p.i.) of E. coli O157:H7 and total coliforms by calves maintained on a dietary
stress regimen and calves that were well fed. Calves were inoculated
with 1010 CFU of E. coli O157:H7 on day 0. Calves that were well fed on day 1 to day 14 p.i. were subjected
to dietary stress by having food withheld for 48 h beginning on
day 15; they were fed a one-half ration on day 17 and then were fasted
for 48 h until day 19, when the normal diet was resumed. Calves
that had been subjected to dietary stress on day 1 to day 5 p.i.
were well fed from day 14 to day 21 p.i. The asterisk indicates
calf 1, which is described in the text. The sensitivity of the
enrichment culture is <50 CFU/g. (A) E. coli O157:H7
recovered from well-fed calves. (B) E. coli O157:H7
recovered from diet-stressed calves. (C) Total coliforms recovered from
well-fed calves. (D) Total coliforms recovered from diet-stressed
calves.
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|
Dietary stress prior to inoculation.
In further experiments to
determine the effects of dietary stress upon susceptibility and
shedding, a different regimen was used. Calves were fasted for 2 days
prior to inoculation with 107 CFU of E. coli
O157:H7. We chose 107 CFU as a minimally effective dose
since previous experiments had demonstrated that only 2 of 5 well-fed
adults inoculated with this dose had detectable shedding (<5.0 × 101 CFU/g) for 1 or 2 days p.i. (9). In this
experiment, we used two groups of four 3- to 4-month-old weaned calves.
In each group, two calves were well fed and two were fasted for 2 days
prior to inoculation. Only three of the four well-fed calves shed at detectable levels, the longest for 3 days (Fig.
3). In contrast, the fasted calves
inoculated with 107 CFU had significantly greater shedding
(P = 0.001), with a peak of 1.4 × 104
to 3.5 × 105 CFU/g during the first week p.i. When
E. coli O157:H7 shedding (day 1 to day 7) of the fasted
calves inoculated with 107 CFU was compared with the
shedding (day 1 to day 7) of well-fed calves (from the first
experiment) inoculated with 1010 CFU, there was no
difference (P = 0.73).
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FIG. 3.
Fecal shedding (day 1 to day 7) of E. coli
O157:H7 by calves that were well fed (solid symbols) or fasted (open
symbols) for 48 h prior to inoculation with 107 CFU of
E. coli O157:H7 on day 0. E. coli O157:H7
organisms were recovered from well-fed calves on day 1 (two of four
calves), day 2 (one of four), and day 3 (one of four). The sensitivity
of the enrichment culture is <50 CFU/g.
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|
The increased susceptibility to infection by the fasted calves is
consistent with in vitro studies in which rumen fluid from
fasted
cattle allowed unrestricted growth of
E. coli O157:H7
(
17).
This suggests that interventions during the time
period when calves
and adults may experience dietary stress may limit
the spread
of
E. coli O157:H7. In anticipation of periods of
dietary stress,
application of treatments which can maintain rumen
function might
decrease susceptibility. Calves and adults could also be
treated
with agents such as bacteriocins or inoculated with select
microbes
to competitively exclude
E. coli O157:H7.
Although an inoculum of greater than 10
7 CFU of in
vitro-grown
E. coli O157:H7 is required to obtain shedding
of greater than
10
5 CFU/g in well-fed calves
(
9), we have observed shedding at
this level in a well-fed
calf inoculated with 10
5 CFU of
E. coli O157:H7
derived from feces (data not shown). It
is reasonable to expect that a
smaller inoculum of feces-derived
E. coli O157:H7 would
cause shedding in fasted calves and adults.
Zhao et al. (
25)
have reported that of 31 positive
E. coli O157:H7
fecal
samples collected from farms, 16 had 10
3 to 10
5
CFU/g while 15 were positive by enrichment culture only. The
inoculation dose of 10
10 CFU used in this study and studies
by Brown et al. (
4) would
require 10
5 g of feces
containing 10
5 CFU/g. Diet-stressed calves and adults would
likely be more susceptible
than well-fed animals to infection and
shedding of
E. coli O157:H7
after ingesting smaller amounts
of feces contaminated with the
organism.
Consistent with previous observations, dietary stress of calves can
cause increased shedding of coliforms. In some infected
animals,
shedding of
E. coli O157:H7 can also increase. Diet-stressed
calves are more susceptible to infection by
E. coli O157:H7
than
are well-fed calves. During marketing, when uninfected calves
are
comingled with calves infected with
E. coli O157:H7, dietary
stress could result in an increase in the prevalence of calves
shedding
E. coli O157:H7.
| |
ACKNOWLEDGMENTS |
We thank Norman Lyon, Robert Morgan, Deb Lebo, and Caryn Hurd
for expert technical assistance and Grace Liu for statistical analysis.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Enteric Diseases
and Food Safety Research Unit, USDA-ARS, National Animal Disease
Center, 2300 Dayton Ave., Ames, IA 50010. Phone: (515) 239-8376. Fax: (515) 239-8458. E-mail: tcasey{at}nadc.ars.usda.gov.
| |
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Appl Environ Microbiol, May 1998, p. 1975-1979, Vol. 64, No. 5
0099-2240/98/$00.00+0
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