LETTER TO THE EDITOR

Duration of Stool Colonization in Healthy Medical Students with

Extended-Spectrum-␤-Lactamase-Producing Escherichia coli
xtended-spectrum ␤-lactamase (ESBL)-producing Enterobac-
E teriaceae have been of concern for many years, and clinicians,
microbiologists, infection control practitioners, and hospital epi-
demiologists are struggling to overcome them. It is necessary to
characterize the epidemiology of ESBL-producing microorgan-
isms because clinical infections often occur after gut colonization
(5). The prevalence and risk factors of gut colonization with ESBL-
producing Enterobacteriaceae among healthy people have been in-

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vestigated in many previous studies (3, 7, 8). However, the dura-
tion of gut colonization with these resistant bacteria among
healthy people in the community has not yet been described. In
this study, we performed a prospective study to investigate the
duration of stool colonization and variables associated with pro-
longed duration of colonization by ESBL-producing E. coli among
healthy Chinese medical students.
This study was performed at Fujian Medical University (Fu-
zhou, China). From 24 August through 24 December 2011, 100
second-year medical students were randomly recruited. None of
those included had been exposed to antibiotics or to a hospital
environment within 3 months. Informed consent was obtained
from all participants. Each subject self-collected and submitted
fecal samples every 2 weeks, with a total follow-up goal of 4
months. Undiluted stool samples were cultured on chromID
ESBL plates (bioMérieux, France) and incubated at 35°C for 24 h.
Isolates were identified by conventional biochemical methods (4).
ESBL-producing E. coli was confirmed using the double-disk syn-
ergy test according to the CLSI procedure (1).
The prevalence of ESBL-producing fecal E. coli in these stu-
dents was dynamically observed in this study (Fig. 1). The total
sample size for each of nine time periods during the study was 92,
84, 88, 91, 95, 91, 94, 80, and 64. Forty-one students fully partici-
pated in the whole experiment. Of these subjects, the median age
was 21 years (range, 20 to 23 years), and 68% (28 of 41 subjects)
were male. The median duration of colonization with ESBL-pro-
ducing E. coli in these students was 59 days (range, 14 to 112 days).
Twenty-eight (68%) of the 41 students remained colonized at the
time of the last sample collection. Ten students (24%) who took
antibiotics during the study did not have a significantly longer
duration of stool colonization than those who did not receive
antibiotics (median duration of colonization, 60 days versus 58
days; P ⫽ 0.883). The duration of colonization was not associated
with sex.
To our knowledge, this is the first study to show that gut colo-
nization with ESBL-producing E. coli in healthy young persons
could last more than 4 months. Furthermore, in this study, the
stool carriage rate of ESBL-positive E. coli remained at a surpris-
ingly high level. However, even in China, where antibiotics are
used without strict regulation, the 71.9 to 90.1% prevalence of
ESBL-producing E. coli among healthy young persons is astonish-
ingly high.
Horizontal transmission may account for the high prevalence
of ESBL-producing E. coli in stool samples among these students.
First, horizontal transmission from patient sources to the medical
students is probably one important factor. It is worth noting that
FIG 1 Prevalence of ESBL-producing E. coli in the gut of healthy medical
students in China. The total sample size for each of nine time periods during
the study was 92 (day 0), 84 (day 14), 88 (day 28), 91 (day 42), 95 (day 56), 91
(day 70), 94 (day 84), 80 (day 98), and 64 (day 112).
in China, the rate of ESBL-producing E. coli clinical isolates was
almost 60% (2, 9). It is also possible that horizontal transmission
of ESBL-producing E. coli from patient sources to the medical
students could have occurred, because some of the students could
have been exposed to the hospital or outpatient environment
more than 3 months prior to the start of the study, or they could
have been exposed to colonized hospital personnel prior to the
start of the study, as well as during the study. Second, horizontal
transmission among the students before the start of the study, as
well as during the study, is another possible factor that accounts
for the high rate of stool colonization with ESBL-producing E. coli
in our study.
Furthermore, in this study, the lack of significant association
between recent antibiotic exposure or hospitalization and the du-
ration of stool colonization suggest that other risk factors besides
recent antibiotic use might contribute to the prolonged duration
of fecal colonization among healthy young people in the commu-
nity. As discussed elsewhere, antimicrobial use in nonhuman
medicine, such as in food animals and agriculture, probably poses
direct and indirect impacts on human health (6). Therefore, con-
sidering the astonishingly high prevalence of ESBL-producing E.
coli in the gut flora of healthy young people (Fig. 1), strict control
measures of antibiotic usage in all respects, rather than only in
human medicine, are drastically needed to combat stool coloniza-
tion of antimicrobial-resistant bacteria in healthy humans, espe-
cially in China.
Published ahead of print 11 June 2012
Address correspondence to Bin Li, leonlee307@hotmail.com.
Copyright © 2012, American Society for Microbiology. All Rights Reserved.
doi:10.1128/AAC.00171-12

4558 aac.asm.org Antimicrobial Agents and Chemotherapy p. 4558 – 4559 August 2012 Volume 56 Number 8
 Letter to the Editor

ACKNOWLEDGMENTS 7. Sasaki T, et al. 2010. High prevalence of CTX-M ␤-lactamase-producing

The authors report no conflicts of interest.
This work was supported by the Innovation and Entrepreneurship
Training Program for Fujian College students (grant C12037).
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Bin Li
Department of Clinical Laboratory, Union Hospital, Fujian Medical University,
Fujian, China
Yang Zhong
Xiao-chun Fu
Yi-hui Qiu

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