Pre-harvest interventions to reduce carriage of E.

coli O157 by harvest-ready feedlot cattle

G.H. Loneragana, , ,
M.M. Brashearsb
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doi:10.1016/j.meatsci.2005.04.005
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Abstract
Escherichia coli O157 is an important cause of food-borne illness. The primary reservoir
for this organism is cattle and at present the major site of control is within abattoirs.
Recent data have highlighted the importance of the pathogen load entering abattoirs on
harvest-ready feedlot cattle. The likelihood for in-plant intervention failure increases as
the proportion of cattle carrying E. coli O157 within a pen increases. Pre-harvest reduction
of E. coli O157 colonization will require targeted intervention strategies and should
reduce contamination of carcasses thereby enhancing public health. Several pre-harvest
interventions show substantial promise, such as specific strains of direct-fed microbials,
vaccine technology, sodium chlorate, and neomycin sulfate, whereas others such as
Brown Seaweed or chlorination of water have little or no detectable benefit. Selection of
validated interventions strategies will be important as efforts to control pre-harvest
carriage of E. coli O157 increase.

Keywords

Food safety;
E. coli O157;
Interventions;
Feedlot;
Cattle

1. Introduction
Escherichia coli serotype O157 has been well characterized as a food-borne pathogen
( Wells et al., 1983). This organism possesses several important virulence factors that
contribute to its importance in public health such as intimin, shiga toxins, and
enterohemolysins ( LeBlanc, 2003). Children and the elderly appear at greatest risk for
developing disease and subsequent complications (e.g., hemolytic uremic syndrome)
after exposure to E. coli O157 ( Taylor, White, Winterborn, & Rowe, 1986). Each year there
are an estimated 70,000 cases of E. coli O157-induced disease, which in turn results in
several thousand hospitalizations and approximately 60 deaths ( Mead et al., 1999).
However, the number of illnesses reported by Mead and colleagues relies heavily on
assumptions and as such they have calculated their estimates using a 20-fold under-

reporting of bloody diarrhea. Moreover, these estimates do not reflect recent evidence of
a substantial decline in the reported number of cases ( Anonymous, 2004).
Disease attributed to this pathogen can occur in outbreaks but the majority of cases are
sporadic or not associated with an outbreak situation. Exposure to livestock, particularly
cattle, livestock facilities, or consumption of beef products are frequently identified as risk
factors for disease (Chapman, 2000,Kassenborg et al., 2004, Smith et al., 2004, Varma et
al., 2003 and Wells et al., 1983). As a consequence, much effort has focused on better
understanding the epidemiology of this organism in cattle, particularly cattle housed in
feedlots. Based on the current information, it appears that the initial infection with this
organism occurs early in life and does not induce protective immunity from subsequent
colonization (Gannon et al., 2002 and Laegreid et al., 1999). At the feedlot, prevalence
varies seasonally with greatest recovery of E. coli O157 occurring in warmer months
( Barkocy-Gallagher et al., 2003 and Anonymous, 2001). Based on various large-scale
studies, it can be determined that E. coli O157 is ubiquitous among cattle operations and
more variation in prevalence occurs pen-to-pen than from feedlot-to-feedlot (Hancock et
al., 1997, Sargeant et al., 2004a, Sargeant et al., 2004b and Smith et al., 2001).
As a consequence of this pen-to-pen variation, it has been possible to evaluate pen-level
variation in prevalence at the time of harvest and subsequent likelihood of carcass
contamination. In a study performed by Elder et al. (2000), the authors recovered E.
coli O157 from 26.2%, 13.0%, 43.4%, 18.3%, and 1.9% of fecal samples, hides, preevisceration carcasses, post-evisceration carcasses, and carcasses post-intervention,
respectively. Importantly, they reported that the pre-harvest prevalence (prevalence in
feces or on hides) was associated (r = 0.58, 95% CI 0.270.78, P < 0.01) with prevalence
of carcasses positive at any site (pre- or post-evisceration, or post-intervention). In
another study, Ransom et al. (2003)visited feedlots immediately prior to shipment to an
abattoir and then sampled hides and carcasses from these pens of cattle during harvest.
In pens of cattle with a fecal prevalence greater than 20%, they recovered E. coli O157
from 22.5%, 46.3%, 12.5%, 2.5%, and 0.6%, of hides, colons, pre-evisceration carcasses,
post-evisceration carcasses and carcasses in the cooler, respectively. The risk of pathogen
recovery was less in pens of cattle in which 20% or less of the fecal pats were positive. In
these pens, E. coliO157 was recovered from 5.7%, 7.1%, 7.1%, 0.0%, and 0.0%, of hides,
colons, pre-evisceration carcasses, post-evisceration carcasses and carcasses in the
cooler, respectively. Visits to packing plants and recovered E. coli O157 from 75.7% of
hides, 14.7% of pre-evisceration carcasses, 3.8% of post-evisceration carcasses, 0.3% of
post-intervention samples and 0.0% of chilled carcasses ( Arthur et al., 2004). In addition,
they reported that E. coli O157 prevalence on hides was associated (R2 = 0.68, P < 0.05)
with the prevalence on pre-evisceration carcasses.
There are two salient points that arise from the three studies briefly discussed above. The
first is that in-plant interventions are highly effective at reducing E. coli O157
contamination on carcasses. The second is that despite the efficacious in-plant
interventions, if the pathogen load on hides (as estimated by prevalence) entering the
plant is large then the likelihood for carcass contamination (even in the cooler) increases.
These data stress the importance of pre-harvest manipulation of E. coli O157 carriage, as
greater carriage is more likely to result in an in-plant intervention failure. If it is possible
to reduce prevalence of E. coli O157 pre-harvest, then presumably carcass contamination

and human exposure would also be decreased and consequently, public health may
benefit.

2. Avenues for pre-harvest control

It is possible to broadly categorize options for pre-harvest control of E. coli O157 into two
avenues. The first is modification of an existing management strategy such as
manipulation of a feed ingredient or frequency with which water troughs are washed. The
second avenue for control is development and implementation of novel targeted
intervention technologies. If the former method of control were possible, then it would be
preferable, as modifying an existing management practice could be implemented
expeditiously with minimal impact on feedlot operations. The second avenue would
require significant investment in development and implementation. The challenges of the
latter should not be underestimated as many feedlots may be reluctant to invest the time
and resources required to implement a technological change whose immediate benefit
does not directly related to day-to-day feeding of cattle.
Unfortunately, studies to date have failed to identify a single management practice that is
consistently associated with E. coli O157 prevalence and importantly, can readily be
modified. One study identified an association with muddy pen surfaces and E. coli O157
prevalence but this variable was not shown to be statistically associated with prevalence
in another study ( Sargeant et al., 2004b and Smith et al., 2001). Effectively, the only
factor consistently associated with carriage is a temporal (seasonal) one ( BarkocyGallagher et al., 2003 and Anonymous, 2001), which is not necessarily modifiable. Even in
studies where water troughs have been repeatedly cleaned or pens sanitized, no
significant impact on prevalence was detected ( Elder & Keen, 1999).
Given our present understanding of the epidemiology of E. coli O157 in feedlot cattle, preharvest control will require development and implementation of pre-harvest
interventions. This paper is not meant to serve as a clearinghouse for information on all
potential interventions but rather, we will provide information on specific interventions
that are currently available for use or are pending regulatory approval and substantive
studies have been performed in settings to facilitate inferential judgment on their
potential efficacy in commercial feedlots. Focus has been placed on interventions that
appear to exert a positive impact. Interventions with little or no benefit such as
chlorination of water ( LeJeune et al., 2004) orAscophyllum nodosum (Brown Seaweed or
TASCO14) are not discussed but it is important to note that not all proposed interventions
are efficacious.
Some of the studies reported herein have estimated the prevalence of E. coli O157 in
feces while others have estimated prevalence on hides or both. Hides appear to be the
major source for carcass contamination. Presumably, feces are the major source of E.
coli O157 for hide contamination. If this is so, then benefits could be achieved with an
intervention directed at reducing hide contamination if applied just prior to harvest.
Additionally, long-term control could be achieve with an intervention directed at reducing
colonization at the rectoanal junction ( Naylor et al., 2003) and other sites within the
gastrointestinal tract. Such interventions are reliant on an association between fecal
prevalence and hide prevalence.
To evaluate and describe the relationship between fecal and hide E. coli O157 prevalence,
we used logistic regression techniques on a series of published ( Loneragan & Brashears,

2005) and unpublished data. These data were derived from six commercial feedlot
studies and included cattle housed in 122 pens. Representative fecal and hide samples
were collected from 2846 animals. The outcome variable of interest was pen-level
binomial response variable (i.e., positive samples/possible events) and the independent
variable was fecal prevalence as a continuous variable from 0 to 1. This analysis was
performed using the GLIMMIX procedure for SAS (release 9.1.2, Cary, NC). Overall, 17.7%
and 22.3% of fecal and hide samples were positive, respectively. E. coli O157 was
detected in feces or on hides in 90.2% of pens. In those pens with at least one positive
animal (either feces or hides), the prevalence was 19.9% and 25.3%. In the final logistic
model, hide prevalence was associated with fecal prevalence (P < 0.01); the model with
parameter estimates was:
Turn MathJaxon

where p is the expected hide prevalence at a given fecal prevalence. This model and the
95% confidence limits of the p are depicted in Fig. 1.

Fig. 1.
Model of hide prevalence as predicted by fecal prevalence (solid line). The dashed lines represent
the 95% confidence limits of the prediction. The Y-axis represents the predicted pen-level E.
coli O157 prevalence on hides (dependent variable) and the X-axis represents pen-level fecal
prevalence (independent variable).
Figure options

The importance of this model is that we do not necessarily have to place less importance
on studies in which an intervention was associated with a significant reduction in
prevalence where only feces were collected. Based on the model above, one can infer
that prevalence on hides should also be reduced.

3. Pre-harvest interventions
3.1. Direct-fed microbials

This broad category includes probiotics and competitive exclusion. Most of the applied
research in this area has focused on a specific Lactobacillus-based direct-fed microbial.
The specific strain that appears to be most efficacious based on the current body of
literature is NP51 (otherwise known as NPC747). In a study by Brashears, Galyean,
Loneragan, Mann, and Killinger-Mann (2003a), this and another strain, NPC750, were
evaluated in feedlot cattle housed in five head pens. Averaged over the duration of the
study, the likelihood of recovery of E. coli O157 from feces was 49% lower in animals
receiving NP51 compared to controls (OR = 0.51%, 95% CI 0.30.8, P < 0.01). The effect
of NPC750 was less so with only a 30% reduction in the likelihood of recovery relative to
the controls (OR = 0.7%, 95% CI 0.5B1.1, P = 0.12). A significant benefit of
both Lactobacillus strains was detected for hide contamination at harvest (P < 0.05). In a
subsequent study, Younts, Galyean, Loneragan, Elam, and Brashears (2004) observed a
similar benefit with a 58% reduction in fecal prevalence in animals administered NP51.
Interestingly, when fed with another strain of Lactobacillus, the benefit lessened
particularly when NP51 was included at a lower dose (10 6 vs. 109 NP51 cells per head per
day). As with the previous study, benefits were also observed for hide contamination.
Salient points from these studies indicate that dose and selection of bacterial strains to
include in a direct-fed microbial product appear to be important. Selection of strains was
highlighted by research performed by Brashears, Jaroni, and Trimble (2003b) in which
they evaluated approximately 650 candidate strains. Through a systematic series of
studies, including the strains ability to inhibit E. coli O157, five promising strains were
identified, one of which was NP51. The practical importance of strain variation in
observed response is that if the wrong direct-fed microbial strain is selected then
conceivably, E. coli O157 shedding and resultant hide contamination could inadvertently
be increased rather than the desired decrease.
To evaluate the effect of NP51 dose, Younts-Dahl et al. (2005) evaluated three daily doses
of 107, 108, and 109 NP51 cells per head. Averaged over time, the highest dose provided
the greatest reduction, which amounted to a 77% lower likelihood of E. coli O157
recovery compared to controls (OR = 0.23%, 95% CI 0.10.4, P < 0.01). While the lower
doses also resulted in reduce shedding averaged over time compared to the controls,
their benefit was not as great. A similar benefit was observed in hide samples collected at
slaughter. This study also highlighted the importance of appropriate strain selection as
inclusion of anotherLactobacillus strain in addition to NP51 actually resulted in increased
fecal shedding and hide contamination at slaughter compared to controls (OR = 1.53%,
95% CI 0.64.0, P = 0.37). This product, NP51, is commercially available and at the time
of manuscript submission, and approximately 10% of the fed cattle in the US are fed this
product (personal communication, Douglas Ware, Nutrition Physiology Corporation).
Another potentially promising direct-fed microbial is an Enterococcus-based product. As
yet, no peer-reviewed publications in which the benefits of this product have been
reported are available. However, company data are encouraging; even though prevalence
was quite low, animals fed this candidate direct-fed microbial were 56% less likely to
have E. coli O157 recovered from their feces.
Competitive exclusion using non-pathogenic E. coli appears to be a practical option in
confined animal feeding operations ( Tkalcic et al., 2003 and Zhao et al., 2003). This
application has largely been restricted to artificially infected animals; however, results
appear promising.

More research is needed for Enterococcus- and E. coli-based direct-fed microbials before
wholesale recommendations can be given. However, preliminary work is encouraging and
warrants consideration as promising future pre-harvest interventions.

3.2. Vaccine technology

Development of vaccine technology would hold great practical application within the beef
industry because (1) cattle producers are familiar with administration of vaccines; (2)
incorporation into existing management of cattle would be fairly simple; (3) vaccines
could be used in all sectors of the industry, not just confined animal feeding operations.
Eliciting an immune response within the gastrointestinal tract and other challenges
associated with developing an efficacious vaccine whose outcome would be decreased E.
coliO157 carriage should not be underestimated. For example, natural exposure does not
induce protective immunity. Despite the many challenges, it appears vaccines may be a
viable pre-harvest intervention of the future.
Investigators administered a vaccine containing type III secreted proteins to feedlot cattle
on three occasions 21 days apart (Potter et al., 2004). Averaged over the feeding period,
8.8% and 21.3% of vaccinates and controls, respectively, were positive for E. coli O157 in
their feces. These data indicate an average vaccine efficacy of 58.7%, i.e., 58.7% lower
risk of recovery of E. coli O157 in vaccinates vs. controls. Hide contamination was not
estimated in this study. As described above, however, hide contamination is directly
correlated with fecal shedding and one would expect such a vaccine to demonstrate
comparable reduction in the proportion of hides positive for E. coli O157 at harvest.
Another bacterin vaccine has also been evaluated and has demonstrated the potential to
reduce prevalence of E. coli O157 in feces and on hides at harvest (personal
communication, Keith Belk, Colorado State University).

3.3. Sodium chlorate

Sodium chlorate is metabolized within facultative anaerobic bacteria to highly toxic
chlorite (Anderson et al., 2001b). Ultimately, sodium chlorate acts as a suicide substrate
for certain bacteria within the gastrointestinal tract. In preliminary studies of cattle and
sheep challenged with E. coli O157, sodium chlorate effectively reduced pathogen
carriage ( Callaway et al., 2002 and Callaway et al., 2003). These studies used cattle and
sheep artificially inoculated with specific strains of E. coli O157 and the animals were fed
potassium nitrate to up-regulate the nitrate reductase enzyme. Because of these factors,
extrapolation to an expected benefit in naturally infected feedlot cattle not consuming
supplemental potassium nitrate is tenuous. However, there is no reason to suspect that
sodium chlorate would not be an efficacious pre-harvest intervention.
A potential benefit beyond E. coli O157 control is that sodium chlorate could be used for a
variety
of
food-borne
pathogens
that
are
facultative
anaerobic
such
as Salmonella and Shield. In fact, an in vitro evaluation of sodium chlorate demonstrated
bactericidal effects among Salmonella Typhimurium DT104; a similar benefit was
observed
in
pigs
artificially
inoculated
with Salmonella ( Anderson
et
al.,
2000 and Anderson et al., 2001a).

3.4. Neomycin sulfate

Intuitively, E. coli O157 colonization within the gastrointestinal tract might be modified by
the use of antimicrobial drugs. Of E. coli O157 isolates recovered from naturally infected
animals, all were susceptible to neomycin sulfate (personal communication, Robert Elder,
Seaboard Farms, Inc.). This antimicrobial drug is approved for in-feed or in-water
administration to cattle for the control or treatment of colibacillosis and because of its
route of administration, can be applied to entire groups of animals.
In a commercial feedlot study in which neomycin sulfate was included in the water for 2
days, fecal shedding and hide contamination were markedly reduced in harvest-ready
cattle (P < 0.01 for both models; unpublished data). In the control and treated cattle, E.
coli O157 was recovered from 22.1% and 0.4% of feces and 50.0% and 2.5% of hides,
respectively. This represents a 98.2% and 95.0% reduction in fecal and hide recovery,
respectively. As hide contamination is indicative of cumulative fecal contamination over
time and because samples were collected approximately 24 h after the second days
administration of neomycin sulfate, it is unclear why such an effect was seen on hides. It
is possible that (1) the presence of neomycin in feces prevented successful recovery of
viable E. coli O157 cells on hides; or (2) hide carriage is more dynamic than previously
thought. It seems highly improbable that animal sampling inadvertently led to selection
of negative animals in the treated group and positive animals in the controls simply due
to chance. Moreover, in another commercial feedlot study (personal communication, Keith
Belk, Colorado State University), a similar effect in feces and on hides was seen in
response to neomycin sulfate administration to harvest-ready cattle.
The use of antimicrobial drugs, particularly in-feed products, in animal agriculture is
becoming increasingly contentious. As it currently stands, a label change will be required
before neomycin sulfate can be used to control E. coli O157 in cattle. In the event of such
a label change, adoption of neomycin sulfate as a pre-harvest intervention to control E.
coli O157 will likely generate much debate. The conventional applications of antimicrobial
drugs in animal agriculture are to improve animal health or the efficiency of production.
The use of neomycin sulfate would be to reduce the load of E. coli O157 entering packing
plants, i.e., a potential human health benefit. The argument concerning neomycin sulfate
use, therefore, will have to weigh the potential benefits for public health against the
potential costs in terms of favoring development of resistance.

4. Conclusions
Based on the studies outlined above, it is clear that several interventions show
considerable promise. Other candidate interventions that may be beneficial but are at
present in the early developmental phase and are beyond the scope of this manuscript.
Currently, the only available intervention that has been broadly evaluated is the NP51containing direct-fed microbial.
Other interventions that are presently available, such as the Enterococcus-based directfed microbials, require additional validation before one should recommend their use.
Several challenges exist for those interventions that require regulatory approval. E.
coli competitive exclusion products, sodium chlorate, and neomycin sulfate all require
approval by the Food and Drug Administration (FDA). Such approvals are time consuming
and costly. Animal vaccines are traditionally licensed by the Center for Veterinary
Biologics (CVB) within the US Department of Agriculture and are intended to improve

animal health. A vaccine to reduce intestinal carriage of E. coli O157 would have little if
any benefit to animal health and be administered to cattle solely to improve public
health. As such, it is unclear if the CVB will license E. coliO157 vaccines or if they will fall
under the regulatory authority of the FDA. The FDA-approval process for vaccines is far
more convoluted, time consuming, and costly than that of the CVB. Ultimately, the costs
associated with FDA licensing may make the vaccines prohibitively expensive for routine
use. It is the opinion of the authors that vaccines to reduce the carriage of E. coli O157 in
cattle should be licensed by the CVB. If so, the products could be available sooner and
the associated licensing costs would be less.
Regardless of the challenges associated with approval and implementation of pre-harvest
interventions, the potential for efficacious, on-farm control of E. coli O157 exists. The
Food Safety and Inspection Service has reported a reduction in the percentage of positive
trim samples, while the Centers for Disease Control and Prevention have reported a
reduction in the incidence of E. coli O157-induced human illnesses ( Table 1). It is likely
that much of the former (and potentially some of the latter) reduction is attributable to inplant interventions and management. Some of the reductions may also be due to the
adoption of the NP51-containing direct-fed microbial. Another possibility analogous to the
emergence of E. coli O157 is that newly emerging serotypes may be replacing the O157.
Table 1.
Food Safety and Inspection Service (FSIS) reported ground beef samples positive for E. coli O157
and Centers for Disease Control and Prevention (CDC) estimate for human incidence of E.
coli O157 induced illnesses based on FoodNet data
Source of data
Year

FSIS CDC

200
0

0.72

2.0

200
1

0.87

1.6

200
2

0.73

1.7

200
3

0.35

1.1

200
4

0.17

Not available
Table options

Implementation of efficacious pre-harvest interventions should reduce the failure rate of

in-plant interventions. In other words, reducing the prevalence of E. coli O157 carried by
cattle entering abattoirs will improve the efficiency of in-plant interventions. This should
improve the safety of beef, reduce the public exposure to this pathogen, and improve
public health.

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by

treatment

with