Elevated risk of carrying gentamicin-resistant Escherichia coli among U.S. poultry workers.
ABSTRACT Antimicrobial use in food-animal production is an issue of growing concern. The application of antimicrobials for therapy, prophylaxis, and growth promotion in broiler chicken production has been associated with the emergence and dissemination of antimicrobial-resistant enteric bacteria. Although human exposure to antimicrobial-resistant bacteria through food has been examined extensively, little attention has been paid to occupational and environmental pathways of exposure.
Our objective was to measure the relative risk for colonization with antimicrobial-resistant Escherichia coli among poultry workers compared with community referents.
We collected stool samples and health surveys from 16 poultry workers and 33 community referents in the Delmarva region of Maryland and Virginia. E. coli was cultured from stool samples, and susceptibility to ampicillin, ciprofloxacin, ceftriaxone, gentamicin, nitrofurantoin, and tetracycline was determined for each E. coli isolate. We estimated the relative risk for carrying antimicrobial-resistant E. coli among poultry workers compared with community referents.
Poultry workers had 32 times the odds of carrying gentamicin-resistant E. coli compared with community referents. The poultry workers were also at significantly increased risk of carrying multidrug-resistant E. coli.
Occupational exposure to antimicrobial-resistant E. coli from live-animal contact in the broiler chicken industry may be an important route of entry for antimicrobial-resistant E. coli into the community.
- SourceAvailable from: Ahmed Thabet[Show abstract] [Hide abstract]
ABSTRACT: Avian colibacillosis is an infectious disease of chickens caused by avian pathogenic Esch-erichia coli (APEC). Respiratory viruses and Mycoplasma infections cause damage to the respiratory system of chickens and predispose them to APEC. The APEC field isolates have begun showing increased antimicrobial resistance, leading to failure of treatment and increas-ing treatment costs and production losses. The objective of this study was to investigate the susceptibility of APEC to different antimicrobial combinations by using minimum inhibitory concentration and checkerboard tests. All 18 APEC isolates were resistant to amoxicillin, cla-vulanic acid, doxycycline, oxytetracycline, and erythromycin, whereas 71 and 76% of these isolates were resistant to ciprofloxacin and enrofloxacin, respectively. Fosfomycin had the best activity against the resistant isolates, followed by gentamicin, spectinomycin, and florfenicol, with resistant percentages of 35, 41, 47, and 53%, respectively. A total of 46 antibiotic com-binations were used to test each E. coli field isolate using the checkerboard technique. On the basis of checkerboard results for synergistic and partial synergistic activities, the combinations of amoxicillin-clavulanic acid, ciprofloxacin-fosfomycin, oxytetracycline-erythromycin, oxy-tetracycline-florfenicol, amoxicillin-gentamicin, oxytetracycline-spectinomycin, and spectino-mycin-erythromycin were the best in vitro antimicrobials, with synergistic and partial synergis-tic activities in more than 80% of the E. coli field isolates. Further in vivo studies are needed to correlate the in vitro susceptibility results with field efficacy studies to reduce economic losses in the poultry industry.
- [Show abstract] [Hide abstract]
ABSTRACT: Land application is a practical use of municipal Class B biosolids and manure that also promotes soil fertility and productivity. To date, no study exists comparing biosolids to manure microbial risks. This study used quantitative microbial risk assessment to estimate pathogen risks from occupational and public exposures during scenarios involving fomite, soil, crop, and aerosol exposures. Greatest one-time risks were from direct consumption of contaminated soil or exposure to fomites, with one-time risks greater than 10. Recent contamination and high exposures doses increased most risks. and enteric viruses provided the greatest single risks for most scenarios, particularly in the short term. All pathogen risks were decreased with time, 1 d to14 mo between land application and exposure; decreases in risk were typically over six orders of magnitude beyond 30 d. Nearly all risks were reduced to below 10 when using a 4-mo harvest delay for crop consumption. Occupational, more direct risks were greater than indirect public risks, which often occur after time and dilution have reduced pathogen loads to tolerable levels. Comparison of risks by pathogen group confirmed greater bacterial risks from manure, whereas viral risks were exclusive to biosolids. A direct comparison of the two residual types showed that biosolids use had greater risk because of the high infectivity of viruses, whereas the presence of environmentally recalcitrant pathogens such as and maintained manure risk. Direct comparisons of shared pathogens resulted in greater manure risks. Overall, it appears that in the short term, risks were high for both types of residuals, but given treatment, attenuation, and dilution, risks can be reduced to near-insignificant levels. That being said, limited data sets, dose exposures, site-specific inactivation rates, pathogen spikes, environmental change, regrowth, and wildlife will increase risk and uncertainty and remain areas poorly understood.Journal of Environmental Quality 01/2012; 41(6):2009-23. · 2.35 Impact Factor
- [Show abstract] [Hide abstract]
ABSTRACT: Avian colibacillosis is an infectious disease of chickens caused by avian pathogenic Escherichia coli (APEC). Respiratory viruses and Mycoplasma infections cause damage to the respiratory system of chickens and predispose them to APEC. The APEC field isolates have begun showing increased antimicrobial resistance, leading to failure of treatment and increasing treatment costs and production losses. The objective of this study was to investigate the susceptibility of APEC to different antimicrobial combinations by using minimum inhibitory concentration and checkerboard tests. All 18 APEC isolates were resistant to amoxicillin, clavulanic acid, doxycycline, oxytetracycline, and erythromycin, whereas 71 and 76% of these isolates were resistant to ciprofloxacin and enrofloxacin, respectively. Fosfomycin had the best activity against the resistant isolates, followed by gentamicin, spectinomycin, and florfenicol, with resistant percentages of 35, 41, 47, and 53%, respectively. A total of 46 antibiotic combinations were used to test each E. coli field isolate using the checkerboard technique. On the basis of checkerboard results for synergistic and partial synergistic activities, the combinations of amoxicillin-clavulanic acid, ciprofloxacin-fosfomycin, oxytetracycline-erythromycin, oxytetracycline-florfenicol, amoxicillin-gentamicin, oxytetracycline-spectinomycin, and spectinomycin-erythromycin were the best in vitro antimicrobials, with synergistic and partial synergistic activities in more than 80% of the E. coli field isolates. Further in vivo studies are needed to correlate the in vitro susceptibility results with field efficacy studies to reduce economic losses in the poultry industry.The Journal of Applied Poultry Research 09/2012; 21(1):595. · 0.59 Impact Factor
VOLUME 115 | NUMBER 12 | December 2007 • Environmental Health Perspectives
Antimicrobial-resistant bacteria including
Escherichia coli are common contaminants of
the industrial broiler chicken environment
(Hayes et al. 2004; Khan et al. 2005). Studies
conducted in Europe indicate that poultry
growers and poultry-house workers are at risk
of exposure to these and other pathogens
(Ojeniyi 1989; van den Bogaard et al. 2001).
Similar studies must be conducted in the
United States in order to measure occupa-
tional exposure to antimicrobial-resistant
E. coli in the U.S. broiler chicken industry.
Antimicrobial use has been integral to the
industrialization of food-animal production.
Over the past half century, food-animal pro-
duction has changed from a largely entrepre-
neurial system run by independent farmers to
an industrial mode of production in which a
small number of companies control all aspects
of production, from breeding and feed formu-
lation to slaughter and distribution of con-
sumer products. This shift in both the
organization and methods of production has
allowed for the reliable, high-throughput pro-
duction of food animals on a scale not seen in
human history. In the United States alone,
> 9 billion food animals are produced annually
(U.S. Department of Agriculture 2004).
Antimicrobials have been used in food-animal
production since the early days of their discov-
ery (Viola and DeVincent 2006). Although
exact figures are unavailable, it is currently
estimated that at least half of all of the anti-
microbials consumed in the United States are
used in food-animal production (Steinfeld
et al. 2006). Antimicrobials are used for multi-
ple purposes including outbreak control,
prophylaxis, and growth promotion. The
antimicrobials approved for use in the U.S.
food-animal industry include many drugs of
critical importance to human medicine.
Sixteen antimicrobial agents from 10 anti-
microbial classes are currently approved for use
in U.S. poultry production (Appendix 1).
Among these, gentamicin (GEN) is reported
to be the most commonly used antimicrobial
(Luangtongkum et al. 2006).
The use of antimicrobials in industrial
food-animal production selects for anti-
microbial-resistant bacterial populations.
Antimicrobial-resistant bacteria have been
detected in animal wastes (Jindal et al. 2006),
animal bedding (Kelley et al. 1998), air both
inside (Chapin et al. 2005) and downwind
(Gibbs et al. 2006) of animal feeding opera-
tions, in groundwater near animal feeding
operations (Anderson and Sobsey 2006), and
in consumer meat and poultry products
(Food and Drug Administration 2006).
There is substantial evidence that anti-
microbial use in food-animal production
contributes to the burden of antimicrobial-
resistant diseases in human populations
through foodborne routes of exposure.
Examples include infections with fluoro-
quinolone-resistant Campylobacter (Gupta
et al. 2004), vancomycin-resistant Enterococci
(VRE) (Bonten et al. 2001), multidrug-
resistant Salmonella (Molbak 2006), and
multidrug-resistant E. coli (Ramchandani
et al. 2005). Additional pathways likely exist
through exposure to contaminated environ-
mental media in and around animal produc-
tion facilities as well as contact with animals
in the occupational setting.
Some of the seminal reports connecting
antimicrobial use in food-animal production
with antimicrobial-resistant human infections
and colonization involved studies of farmers
and their families (Levy 1978; Levy et al.
1976). These early reports have been con-
firmed by more recent case studies (Fey et al.
2000; Oppegaard et al. 2001). Occupational
epidemiology studies of European broiler
farmers and turkey farmers, as well as broiler
and turkey slaughterhouse workers, indicated
that these populations were at increased risk
of colonization with antimicrobial-resistant
E. coli and Enterococcus because of their
occupational exposure to these animals
(Stobberingh et al. 1999; van den Bogaard
et al. 1997, 2001, 2002). To date, no studies
have been published assessing the occupa-
tional exposures to antimicrobial-resistant
Address correspondence to L.B. Price, The Johns
Hopkins University School of Medicine, 4940 Eastern
Ave., B-3-North, Baltimore, MD 21224-2780 USA.
Telephone: (410) 550-9080. Fax: (410) 550-1169.
We thank C. Resnick for her technical and organi-
zational contributions and her extreme dedication to
this project; C. Morrison for her collaboration and
dedication to health and rights of poultry workers on
the Delmarva Peninsula; J. Abraham for advice
regarding statistical modeling and epidemiologic
analysis; P. Charache for advice regarding microbial
analyses; K. Nachman, R. Gardner, M. Nweke,
D. Ross, D. Marshall, P. Harmon, A. Chu, K. Brown,
K. Stoltenberg, D. Nelson, E. Moody, J. Richman,
and C. Sanchez for volunteering their skills for
recruitment, questionnaire administration, and sam-
ple collection; and finally all of the study participants.
This project was funded in part by grants from the
Johns Hopkins Center for a Livable Future, the
Winslow Foundation, the Clayton Baker Trust, and
the National Institute for Occupational Safety and
Health. L.B.P. and J.P.G. were both funded by pre-
doctoral fellowships from the Johns Hopkins Center
for a Livable Future.
The authors declare they have no competing
Received 23 February 2007; accepted 2 September
Elevated Risk of Carrying Gentamicin-Resistant Escherichia coli among
U.S. Poultry Workers
Lance B. Price,1,2Jay P. Graham,2Leila G. Lackey,2Amira Roess,2Rocio Vailes,2and Ellen Silbergeld2
1The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA; 2The Johns Hopkins University Bloomberg School of
Public Health, Baltimore, Maryland, USA
BACKGROUND: Antimicrobial use in food-animal production is an issue of growing concern. The
application of antimicrobials for therapy, prophylaxis, and growth promotion in broiler chicken
production has been associated with the emergence and dissemination of antimicrobial-resistant
enteric bacteria. Although human exposure to antimicrobial-resistant bacteria through food has
been examined extensively, little attention has been paid to occupational and environmental
pathways of exposure.
OBJECTIVE: Our objective was to measure the relative risk for colonization with antimicrobial-
resistant Escherichia coli among poultry workers compared with community referents.
METHODS: We collected stool samples and health surveys from 16 poultry workers and 33 community
referents in the Delmarva region of Maryland and Virginia. E. coli was cultured from stool samples,
and susceptibility to ampicillin, ciprofloxacin, ceftriaxone, gentamicin, nitrofurantoin, and tetracycline
was determined for each E. coli isolate. We estimated the relative risk for carrying antimicrobial-
resistant E. coli among poultry workers compared with community referents.
RESULTS: Poultry workers had 32 times the odds of carrying gentamicin-resistant E. coli compared
with community referents. The poultry workers were also at significantly increased risk of carrying
multidrug-resistant E. coli.
CONCLUSIONS: Occupational exposure to antimicrobial-resistant E. coli from live-animal contact in
the broiler chicken industry may be an important route of entry for antimicrobial-resistant E. coli
into the community.
KEY WORDS: antibiotic, antimicrobial, aminoglycoside, chickens, Escherichia coli, gentamicin,
occupational exposure, poultry, resistance, worker. Environ Health Perspect 115:1738–1742
(2007). doi:10.1289/ehp.10191 available via http://dx.doi.org/ [Online 4 September 2007]
enteric bacteria incurred by workers in the
U.S. broiler industry.
The U.S. broiler industry is estimated to
employ > 200,000 people (U.S. Poultry and
Egg Association 2006), and the industrializa-
tion of production has resulted in the division
of labor into specific tasks. Most broiler
houses are owned and operated by indepen-
dent farmers called “growers.” Growers typi-
cally raise chickens under contract with
production companies or integrators. At the
end of the grow-out period, chickens are cap-
tured by people called “catchers,” placed into
cages, and transported to the slaughtering
facilities. Once delivered to the slaughter-
house, the broilers are removed from the cages
and shackled to semiautomated slaughter lines
by people called “live hangers.” Thus, grow-
ing, catching, and hanging are the three tasks
with the most intensive live-animal exposures.
For example, a catcher will capture and cage
thousands of chickens in a single workday
(Goodman 2006). Defining risks for these
highly exposed populations may have rele-
vance to understanding the dissemination of
antimicrobial-resistant bacteria more generally
In the present study, we compared the risk
of antimicrobial-resistant E. coli colonization
among poultry workers (i.e., growers, catch-
ers, and live hangers) and rural community
referents. We cultured stool samples for
E. coli and determined the susceptibility of
isolates to six different antimicrobials. We
estimated the relative risk for colonization
with antimicrobial-resistant E. coli among
poultry workers compared to referents.
Materials and Methods
The present study was designed as a conve-
nience sample of poultry workers and commu-
nity residents in the eastern shore region of
Maryland and Virginia. The study complied
with all U.S. regulations regarding research on
human subjects and was approved by the Johns
Hopkins Medical Institutions Committee on
Human Subjects Research. All human subjects
provided written informed consent prior to
participating in the study.
Study site and enrollment. Subjects were
recruited and enrolled 29 April–1 May 2005
and 4–5 December 2005 at several sites in
southern Maryland and Virginia on the
Delmarva Peninsula. This region is among
the top five broiler chicken regions in the
United States, producing > 600 million
chickens annually. Subjects were recruited
and enrolled into the study using a conve-
nience-sampling approach, leveraging public
notices (fliers and newspaper advertisements),
personal outreach through a local non-
governmental organization (Delmarva Poultry
Justice Alliance), and door-to-door inquiries
in neighborhoods known to be populated by
poultry workers. The study excluded anyone
< 18 years of age, those employed in the
medical industry, those working in a poultry
processing plant, and those who had traveled
outside the United States in the past
3 months. A modest incentive ($25 gift cer-
tificate) was offered to those willing to com-
plete a questionnaire and provide stool
samples for analysis.
Questionnaire. After meeting the mini-
mum inclusion criteria for the overall health
study, subjects were administered a face-to-face
questionnaire consisting of three parts. Part 1
covered demographic information including
sex, race, and level of education; employment
status within the past 6 months; health insur-
ance status; and primary source of health care
(i.e., doctor’s office, hospital, workplace, or
other). Part 2 included nonoccupational risks
for exposure to antimicrobial-resistant E. coli
from animal sources such as well water,
ground red meat, and poultry consumption,
and the presence of pets in the household.
Part 3 was directed to those reporting recent
or current employment in the broiler chicken
industry, and requested information on job
title (catcher, grower, or live hanger), dura-
tion of employment, average frequency of
exposure over the course of a week, and days
worked in the week immediately before study
participation. Subjects were also asked about
availability and use of personal protective
equipment. Finally, subjects were asked
whether clothing worn at work was laundered
at home. All data were collected under com-
plete confidentiality; after enrollment, each
subject was identified solely by an alpha-
Stool collection and culture. Participants
were provided a stool sample collection kit
(Fisher Scientific, Pittsburgh, PA) and were
asked to produce and collect a sample on site
or to take the kit home and return a sample
within 4 hr of collection. Stool samples were
transferred to Enteric Plus transport media
(Meridian Bioscience, Cincinnati, OH)
(Wasfy et al. 1995) and kept at 4°C until they
were cultured in the laboratory within 72 hr of
arrival. Enterobacteriaceae was cultured from
the transport media on standard Violet Red
Bile Glucose Agar (Oxoid, Hampshire, UK)
and on Violet Red Bile Glucose Agar supple-
mented with one each of the following anti-
microbials: ampicillin (AMP), 16 µg/mL;
ciprofloxacin (CIP), 2 µg/mL; ceftriaxone
(CEF), 32 µg/mL; GEN, 8 µg/mL; and tetra-
cycline (TET), 8 µg/mL (i.e., each sample was
cultured on six different media formulations).
Isolates were purified twice on the same
medium on which they were isolated. All iso-
lates were stored at –80°C until they were
tested for antimicrobial susceptibility as
described below. Selective antimicrobials were
used to increase the sensitivity of the assay for
detecting resistant E. coli strains among a mix
of resistant and susceptible strains within the
Susceptibility testing. Minimal inhibitory
concentrations were determined by the agar
dilution method using E. coli ATCC 25922
and E. coli ATCC 35218 (both from
American Type Culture Collection, Manassas,
VA) as reference strains as recommended by
guidelines of the Clinical and Laboratory
Standards Institute (2002). The dilution
ranges (resistance breakpoints) were as follows:
AMP, 0.25–32 (32); CIP, 0.004–8 (4); CEF,
0.06–64 (64); GEN, 0.25–16 (16); NIT,
2–256 (128); and TET, 1–16 (16).
Species identification. Isolates were identi-
fied to the species level using the Microbact
12A (12E) Gram-Negative Identification
System—Strip Format (Oxoid). Following the
protocol provided by the manufacturer, isolates
were cultured for 24 hr on Mueller-Hinton
blood agar, confirmed oxidase-negative, sus-
pended in a saline solution, and incubated for
24 hr in a test strip containing 12 distinct sub-
strates commonly used for Enterobacteriaceae
species identification. Strips were scored based
on color change, and results were correlated
with genus and species using the Microbact
2000 Identification Package, V2.03 for
Windows (Oxoid). Only those isolates posi-
tively identified as E. coli were used for out-
Sample scoring. Stool samples were plated
on six different agars as described above; there-
fore, up to six isolates were cultured from each
participant (i.e., one isolate per agar formula-
tion). If ≥ 1 of the E. coli isolates from a
participant’s stool sample was resistant to an
antimicrobial, the sample was scored as resis-
tant. If any single isolate from a participant’s
stool culture was resistant to ≥ 2 anti-
microbials, the sample was scored as multidrug
resistant. In total, eight different antimicrobial
resistance outcomes were measured: AMP
resistance, CIP resistance, CEF resistance,
GEN resistance, NIT resistance, TET resis-
tance, antimicrobial resistance (any of the six),
and multidrug resistance (≥ 2).
Data entry. Questionnaire data were
entered into a database using EpiData 3.1
(Lauritsen and Bruus 2005) by two different
researchers. Referencing the original question-
naires allowed for inconsistencies between the
independent entries to be rectified.
Statistical analyses. We used odds ratios,
Fisher’s exact tests, and chi-square analyses to
assess the associations between exposure (poul-
try worker vs. community reference) and the
eight outcomes. Bivariate logistic regression
was used to measure these associations while
adjusting for self-reported antibiotic use dur-
ing the month before sample collection. All
statistical analyses were performed using Stata
8.0 (StataCorp, College Station, TX).
High gentamicin-resistant E. coli among U.S. poultry workers
Environmental Health Perspectives • VOLUME 115 | NUMBER 12 | December 2007
Seventy-one people were enrolled into our
study, but 49 subjects were included in the
analyses presented here. Nine people were
excluded because they shared a residence with
a poultry worker, and 13 were excluded
because E. coli was not recovered from their
stool samples. There was not a significant
difference in the proportion of poultry work-
ers and community referents dropped for
lack of an E. coli culture; therefore, their
exclusion did not affect the internal validity of
Poultry workers (n = 16) and community
referents (n = 33) were similar with respect to
most of the general characteristics assessed in
the study (Table 1). There were fewer poultry
workers who reported completing high school
than community referents, but we did not
consider this to be a potential confounder for
the analyses presented here.
Most nonoccupational risk factors for
colonization with antimicrobial-resistant
E. coli were similar between the two exposure
groups. Poultry workers and community refer-
ents were similar with respect to self-reported
exposures to potential sources of animal-asso-
ciated antimicrobial-resistant E. coli, including
ground red meat, poultry, and well-water con-
sumption, as well as keeping pets (Table 2).
The two groups were also similar in the pro-
portion of participants who sought health care
in the month before the study. However,
poultry workers were more than two times as
likely as referents to report antibiotic use dur-
ing this same period (Table 2). Self-reported
antibiotic use was associated with increased
odds for all eight outcomes of interest
(Table 3) and therefore was included in multi-
variate logistic regression models.
Poultry workers had 32 times the odds of
being colonized with GEN-resistant E. coli
compared with community referents
(Table 4). AMP-resistant and TET-resistant
E. coli carriage was common among both
groups and not significantly different between
them (Table 4). In contrast, CIP-, CEF-, and
NIT-resistant E. coli were uncommon in both
groups— too rare to calculate relative risk esti-
mates. Nine different multidrug-resistance
patterns were identified among the E. coli
strains collected (Appendix 2). Carriage of
multidrug-resistant E. coli was significantly
more common in poultry workers and was
largely attributable to the disproportionate
prevalence of GEN resistance (Table 4).
Adjusting for self-reported antibiotic use in
multivariate logistic analyses did not change
the overall trends and had little effect on the
individual associations (Table 4).
This is the first U.S.-based study to assess
the risk for colonization with antimicrobial-
resistant E. coli from occupational exposure to
live chickens in the broiler chicken industry.
The results presented here confirm similar
studies in Europe showing that poultry farmers
and slaughterhouse workers were at excess risk
for colonization with antimicrobial-resistant
E. coli (van den Bogaard et al. 2001).
In the present study, 50% of the poultry
workers were colonized with GEN-resistant
E. coli. This was in stark contrast to the pro-
portion of community referents colonized
with GEN-resistant E. coli (3%) and to the
rates reported among hospital isolates (6.3%)
(Friedland et al. 2003). Aminoglycosides are
not absorbed through the gastrointestinal
tract; therefore, human use is limited to intra-
venous, intramuscular, subcutaneous, and
topical administration. The inability to
administer GEN orally limits outpatient use;
thus, there is probably minimal selection of
GEN-resistant E. coli in the community. In
contrast, GEN has been reported to be the
most commonly used antimicrobial in broiler
production, where it is administered prophy-
lactically to day-old chicks to prevent bacterial
Price et al.
VOLUME 115 | NUMBER 12 | December 2007 • Environmental Health Perspectives
Table 1. Participant characteristics [percent (no.)]
for community referents (CR; n = 33) and poultry
workers (PW; n = 16).
Age [years (mean ± SD)]
< High school
> High school
42.5 ± 13.1 46.4 ± 8.3
aHealth insurance data were missing for one CR.
*Significantly different between exposure groups (p < 0.05).
Table 2. Nonoccupational risk factors [percent
(no.)] for antimicrobial-resistant E. coli carriage
exposure in community referents (CR; n = 33) and
poultry workers (PW; n = 16).
Antibiotic use previous month
Health care in previous month
Consume ground red meat
Drinking water source
Table 3. Odds of antimicrobial-resistant E. coli among participants reporting any antibiotic use during the
month before the study.
Users (n = 12)
Nonusers (n = 27)
OR (95% CI) Resistance p-Value
Abbreviations: CI, confidence interval; MDR, multidrug resistant; OR, odds ratio; R, resistant to ≥ 1 antimicrobials (super-
script indicates resistance to a specific antimicrobial).
Table 4. Odds of antimicrobial-resistant E. coli among poultry workers and community referents.
Antimicrobial- resistant cases
PW % (no.)
OR (95% CI)
OR (95% CI)
CR % (no.)
Abbreviations: CI, confidence interval; CR, community referent; MDR, multidrug resistant; PW, poultry worker; R, resistant
to ≥ 1 antimicrobials (superscript indicates resistance to a specific antimicrobial).
aBased on logistic regression model adjusting for self-reported use of any antibiotics during the month before sample
infections (Luangtongkum et al. 2006). GEN
resistance is common among poultry-associ-
ated enteric bacteria. A recent survey revealed
that 69% of avian pathogenic E. coli isolates
were resistant to GEN (Zhao et al. 2005).
The disproportionately high prevalence of
GEN-resistant E. coli among the poultry
workers in the present study is consistent with
the hypothesis that poultry workers are at
increased risk of becoming colonized with
antimicrobial-resistant E. coli resulting from
occupational exposures to these strains in the
broiler chicken environment.
We acknowledge the limitations of the
present study, particularly the small sample
size. The study design was a community-
based convenience sample necessitated by the
fact that poultry workers in contact with live
poultry are unorganized and often contracted
by integrators. Thus, there was no reliable
way to recruit subjects through labor organi-
zations or employers. The sample size was fur-
ther limited by our inability to culture E. coli
from the stools of 13 participants. Culture
recovery might have been improved by using
a type of medium more selective for E. coli.
Stool sample cultivability may also have been
reduced because of variable delays between
the time participants collected their stool
samples and the time they delivered them to
researchers (participants were requested to do
so within 4 hr). There was not a significant
difference in the proportion of poultry work-
ers and community referents dropped from
the analysis due to negative cultures; there-
fore, the internal validity of the study was not
affected by this limitation.
We did not ascertain health outcomes that
may have been related to antimicrobial-
resistant E. coli colonization, but the increased
colonization rates among poultry workers may
be associated with increased health risks in this
population. Poultry-associated multidrug-
resistant strains of E. coli have been shown to
cause urinary tract infections and sepsis in the
community (Manges et al. 2006; Ramchandani
et al. 2005). Furthermore, antibiotic-resistant
E. coli can serve as a reservoir of mobile resis-
tance determinants that can be transferred to
pathogenic bacterial species (Blake et al. 2003).
Thus, harboring E. coli with these determinants
may increase one’s risk for developing an
Colonization with antimicrobial-resistant
E. coli may also pose a health risk to poultry
workers’ families and community contacts.
Community-based studies indicate that
strains of antimicrobial-resistant E. coli are
often shared among family members and
between domestic partners (Hannah et al.
2005; Lietzau et al. 2006). In addition to the
fecal–oral route, poultry workers’ household
contacts may be exposed to antimicrobial-
resistant E. coli from contaminated work
clothes (88% of poultry workers in the pre-
sent study reported laundering their work
clothes at home; data not shown).
To determine whether colonization by
E. coli is transient or long-term among poultry
workers, prospective studies complemented by
detailed genetic analysis will be required.
Likewise, such analyses can reveal whether
mobile resistance elements are transferring
resistance to native microbial flora in poultry
workers. Additional studies will also be neces-
sary to evaluate the potential for negative
health outcomes associated with colonization
by antimicrobial-resistant E. coli and to deter-
mine risks of exposure for household contacts
of poultry workers.
A number of U.S. poultry producers have
announced that they have substantially
reduced their antimicrobial consumption by
discontinuing the use of antimicrobial growth
promoters (antimicrobials added to feed to
promote growth) (Weise 2006). GEN is not
approved for growth promotion in the United
States; therefore, consumption rates will be
unaffected by decreases in antimicrobial
growth promoters. The decision by Tyson
Foods (Springdale, AR), one of the nation’s
largest poultry producers, to stop using antibi-
otics altogether for chickens marketed fresh in
the United States could result in a substantial
reduction in GEN use; however, this change
will be implemented at less than half of their
U.S. production facilities (Associated Press
2007). Furthermore, it is unclear whether this
new antimicrobial use policy will be imple-
mented at Tyson’s foreign production plants.
Occupational exposure to live animals in the
broiler chicken industry may be an important
route of entry for antimicrobial-resistant bac-
teria into the community. The present study
revealed a disproportionately high rate of colo-
nization with GEN-resistant E. coli among
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