Content uploaded by Prem R. Meena Ph.D
Author content
All content in this area was uploaded by Prem R. Meena Ph.D on Dec 26, 2023
Content may be subject to copyright.
Letters in Applied Microbiology, 2022, 76,1–12
https://doi.org/10.1093/lambio/ovac016
Advance access publication date: 14 December 2022
Review Article
Extraintestinal pathogenic Escherichia coli (ExPEC)
reservoirs, and antibiotics resistance trends: a one-health
surveillance for risk analysis from “farm-to-fork”
Prem Raj Meena, Priyanka Priyanka, Arvind Pratap Singh*
Public Health and Genomics Laboratory, Department of Microbiology, School of Life Sciences, Central University of Rajasthan, Ajmer 305817,
India
∗Corresponding author. Department of Microbiology, School of Life Sciences, Central University of Rajasthan, Ajmer 305817, Rajasthan, India. E-mail:
arvindpsingh@curaj.ac.in;prajcsirigib@gmail.com
Abstract
Extraintestinal pathogenic Escherichia coli (ExPEC) associated infections are signicant health concerns for both animals and humans. ExPEC
strains are associated with various infections in humans, i.e. urinary tract infections, meningitis, septicemia, and other infections. Over the few
years, several studies revealed, food animals act as a reservoir for ExPEC pathovars, but there is no information about the agricultural sector.
In particular, the extensive use of antibiotics in food animals and agricultural settings could be signicantly contributed to the emergence of
antibiotic-resistant pathogens. However, global outbreaks of food-borne illnesses from contaminated food have made a signicant concern for
both public health and food safety. This review focuses on the reservoirs for ExPEC and their potential circulation between animals, humans, and
environment. In this, we rst report that the agricultural setting could be the reservoir of ExPEC and can play a role in disseminating antimicrobial-
resistant ExPEC. A thorough understanding of ExPEC ecology, reservoirs, and transmission dynamics can signicantly contribute to reducing the
burden of ExPEC-associated infections. Overall, the study provides the important data on the current state of knowledge for different reservoirs
with dynamic, dissemination, and transmission of antimicrobial-resistance ExPEC in animals, humans, and environment in the “One-Health”
context.
Signicance and impact of study:
Extraintestinal pathogenic Escherichia coli (ExPEC) are important pathogens that cause diverse diseases such as urinary tract infections, sep-
ticemia, and meningitis in humans. Animals are recognized as a reservoir for humans-associated ExPEC, but whether the agricultural sectors
are sources of human-associated ExPEC is still debatable. Antimicrobial resistant is a global threat to public health and food safety. This review
provides evidence of different reservoirs with possible dynamic dissemination of antimicrobial-resistant ExPEC in animals, humans, and environ-
ment in the “One-Health” context. This study also provides new insights into the extent and possible human health implications of agricultural
products contaminated with ExPEC.
Keywords: Extraintestinal pathogenic Escherichia coli, Reservoirs, Antimicrobial resistance, Public health, Food safety, One-Health
Introduction
Food-borne infections are one of the most signicant growing
concerns to both human and animal health, along with food
safety worldwide. This is because every year, a large amount of
population is affected due to contaminated food consumption
(Bélanger et al. 2011, Rouger et al. 2017). Food products are
the primary vehicle for transmitting pathogenic bacteria, es-
pecially Salmonella and Escherichia coli (E. coli)(Ahmedand
Shimamoto 2014). Although many E. coli strains are harm-
less and commensals, there is a subset that has the ability
to cause both intestinal infections and extraintestinal infec-
tions (Kaper et al. 2004). Based on the host and site of in-
fection, extraintestinal pathogenic E. coli (ExPEC) incorpo-
rates into the following different pathotypes: uropathogenic
E. coli (UPEC) is responsible for urinary tract infections (UTI);
avian pathogenic E. coli (APEC) causes the most common dis-
ease “colibacillosis” in poultry; and septicemia-associated E.
coli (SEPEC) and neonatal meningitis-causing E. coli (NMEC)
are responsible for septicemia and neonatal meningitis, respec-
tively (Johnson and Russo 2002, Skippen et al. 2006, Crox-
all et al. 2011, Banerjee et al. 2013, Denamur et al. 2021,
Meena et al. 2021). Furthermore, extraintestinal infections in
humans have a high incidence rate, and they are phylogeneti-
cally and epidemiologically distinct from the commensal and
diarrheagenic E. coli (Poolman and Wacker 2016,Wasi
´
nski
2019). ExPEC is dened by the several genotypic and phe-
notypic criteria (Manges and Johnson 2017,Wasi´
nski 2019).
Notably, E. coli is distinguished into eight main phylogenetic
groups: A, B1, B2, C, D, E, F, and cryptic clade I (Clermont
et al. 2013, Markland et al. 2015, Beghain et al. 2018). Most
of the ExPEC strains belong to group B2 and, to a lesser ex-
tent, group D (Russo and Johnson 2000,2003, Mohamed et
al. 2015, Manges 2016, Meena et al. 2021), whereas both
groups A and B are often associated with commensal E. coli.
In contrast, to enteric pathotypes, ExPEC strains, especially
UPEC, NMEC, and SEPEC in humans, do constitute a sig-
nicant cause of morbidity or mortality worldwide (Manges
2016).
Traditionally, food-borne infections have been limited to
those affecting the gastrointestinal tract. However, growing
number of studies have been linking food-borne infections
with extraintestinal infections, especially UTIs (Nordstrom
Received: February 25, 2022. Revised: October 12, 2022. Accepted: November 8, 2022
C
The Author(s) 2022. Published by Oxford University Press on behalf of Applied Microbiology International. All rights reserved. For permissions, please
e-mail: journals.permissions@oup.com
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
2Meena et al.
et al. 2013,Singer2015, Meena et al. 2021). Although it is dif-
cult to retrace the origin of ExPEC causing human infections,
it is well-accepted that the transmission of ExPEC from ani-
mals to humans occurs through various routes, such as con-
taminated food, retail meat, and direct contact with domestic
animals (Bélanger et al. 2011). Over the years, several stud-
ies conducted in different geographic areas have discussed the
role of food animals (especially chicken and pig) as a reser-
voir of ExPEC strains (Xia et al. 2011a, Manges and Johnson
2012, Stromberg et al. 2017, Meena et al. 2021). Whether or
not the agricultural foods and environmental source could act
as an alternative source for ExPEC, remains debatable. This
has raised serious concerns for both human and animal health
as well as for food safety. The continuous increase in popu-
lation is directly associated with an increase in the demand
of food-products consumption, resulting in turn, in socio-
economic changes in the food production system, thereby in-
creasing animal food-borne zoonosis. In this study, we look to
summarize the reservoirs and the global outbreak of ExPEC,
and then, go on to dene a possible route that is resistant to
the transmission of antimicrobial ExPEC strains, under the
“One-Health” context.
ExPEC in the “One-Health” concept
Food products from food animals (e.g. meat, egg, etc.), along
with agricultural food products (vegetables and fruits) are
contaminated with bacteria such as E. coli,Salmonella,Liste-
ria,andCampylobacter, which are responsible for many bac-
terial infections in humans (Mitchell et al. 2015, Stromberg
et al. 2017, Heredia and García 2018, Mellata et al. 2018,
Priyanka et al. 2021). Interestingly, a comparison of a
large number of poultry, dog, and cat isolated and human-
associated ExPEC shows the presence of virulence-associated
genes including pap,hlyA,iroN,sfa-foc,iutA,andkps operon
(Johnson et al. 2008a,b,Anastasietal.2010). Our pervious
study has reported data on pathogenic E. coli, especially in-
testinal pathogenic E. coli (InPEC) present in agricultural food
products (Priyanka et al. 2021). A recent study has suggested
that some strain of ExPEC and InPEC share a common viru-
lence factor, which can cause both intestinal and extraintesti-
nal infections (Denamur et al. 2021). This possibly is a new
research puzzle, wherein, we need to understand whether agri-
cultural foods do act as reservoirs for ExPEC. In this review,
we show the possible route of transmission of ExPEC under
different environment settings.
The “One-Health” concept may be dened as the unique
inextricable interaction between humans, animals, and
pathogens sharing the same environment (Cantas and Suer
2014). Transmission of ExPEC in the “One-Health” cycle
occurs from animals to humans, and vice versa, and from
agricultural food to both human and animals, and vice
versa through (i) animal’s bite and scratches; and (ii) cross-
contamination from animal products due to improper han-
dling of processed food. Additionally, it may be noted that (iii)
farmers and health workers are at risk exposure to zoonotic
bacteria; they can be a carrier of the zoonotic bacteria and
spread to other humans. Importantly, (iv) even soil and wa-
ter may be contaminated by manure, which in turn, contains
various pathogenic bacteria (Flynn 1999, Schauss et al. 2009,
Cantas and Suer 2014,Choetal.2020). Existing literature
provided evidence that pathogenic E. coli from both animals
and humans can cross the host species’ barrier (Johnson and
Clabots 2006, Johnson et al. 2008b,2009b,Singer2015).
Reservoirs for ExPEC in “One-Health”
The potential reservoirs for the E. coli strains that causes ex-
traintestinal infections in humans include several non-human
reservoirs, such as food animals, retail meat commodities,
sewage, and other environmental sources (Sojka and Car-
naghan 1961, Manges 2016, Manges and Johnson 2017,
Meena et al. 2021). However, the main reservoir of ExPEC
includes the human intestinal tract, but does not cause any
disease in the gut; they colonize there and persist until they
nd an opportunity to cause infection (Manges and Johnson
2017). Studies on molecular epidemiology of environmental
ExPEC that cause infection in humans, recovered from sewage
(sequence types: ST69, ST131), domestic (ST69), and wild an-
imals (ST533, ST69, etc.), along with other environmental
sources, suggested that there are several potential reservoirs
for human ExPEC (Gibbs et al. 2007, Hamelin et al. 2007,
Ewers et al. 2010, Dhanji et al. 2011,Dolejskaetal.2011,
Platell et al. 2011, Manges 2016). Food animal associated Ex-
PEC lineage, such as ST131, ST69, ST394, and ST95 possess
virulence properties that contribute to their ability to cause
extraintestinal infection in humans and animals alike.
It is well-accepted that the transmission of ExPEC from an-
imals to humans happens through various routes, such as con-
taminated food, retail meat, and direct contact with domestic
animals. There is a similarity between some food animal and
human ExPEC, and these strains can cause UTIs in humans;
these infections have recently been referred to as food-borne
UTI or FUTIs (Nordstrom et al. 2013,Singer2015). In cat-
tle, ExPEC can cause UTIs and bovine mastitis. Notably, Ex-
PEC is widespread in animal’s reservoirs,where they can cause
infections. The poultry industry endures severe losses due to
colibacillosis, airsacculities, and septicemia caused by APEC
(Bélanger et al. 2011). Further, in cattle also, ExPEC, especially
mammary pathogenic E. coli causes bovine mastitis, which is
an important economic problem due to the reduction of milk
production and thereby it makes the milk below standard for
commercial sale (Fairbrother and Nadeau 2006; Goulart and
Mellata 2022). Apart from economics losses connected with
decreased milk production, sporadic cases of death of cow can
occur after per-acute course of mastitis (Bélanger et al. 2011).
Moreover, domestic companion animals such as dogs and cats
also suffer from infections caused by ExPEC (Johnson et al.
2008a,2008b,2009b). Thus, there is a need to study the food
and food animal reservoir for human ExPEC; this would lead
to pay specic attention to ExPEC lineage that impacts a large
fraction of infection and is important for public health and
food safety.
Environmental reservoirs of ExPEC
Many environmental sources, including surface water, rain-
water, wild animal, sewage, and wastewater efuents, have
been investigated as possible potential reservoirs of ExPEC
(Manges and Johnson 2017). Among all, sewage may con-
tribute signicantly to the environmental dissemination or cir-
culation of ExPEC due to the presence of a high concentra-
tion of humans and animal fecal waste (Manges and John-
son 2017, Manges et al. 2019). Studying environmental reser-
voirs is challenging because these sources tend to contain E.
coli from multiple sources, e.g. sewage may contain human,
animal, and industrial waste. The survival of ExPEC dur-
ing sewage treatment leads to possible environmental con-
tamination of ExPEC. Several studies have provided evidence
that 60% of sewage isolated E. coli shows genetical similar-
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
The antimicrobial-resistant trend in food-borne pathogens 3
ities to ExPEC belonging to phylogenetic groups B2 and D
(Anastasi et al. 2010, Mokracka et al. 2011, Sarowska et al.
2019). Notably, two critical ExPEC lineages were identied in
sewage sources, including E. coli O25: H4-B2-ST131 and E.
coli O11/O17/O77: K52: H18-D-ST69, in treated sewage ef-
uent and river water (Boczek et al. 2007, Dhanji et al. 2011,
Dolejska et al. 2011, Finn et al. 2020). Despite sewages treat-
ment, ExPEC can persist throughout the sewage treatment
process, which leads to the risk of high contamination in sur-
face water. Thus, investigation of the treatment process and
movement of ExPEC in treated water is needed, since these
sources may participate in environmental circulation of Ex-
PEC pathotypes that cause diseases in both humans and an-
imals. Several studies have identied antimicrobial resistance
(AMR) and pathogenic E. coli in natural bodies of waterway
(Hamelin et al. 2007, Luna et al. 2010, Abhirosh et al. 2011,
Manges and Johnson 2017). Some research groups that iso-
lated E. coli from lake and river water showed that 73% of
lake and 23% from river isolated E. coli qualied as UPEC,
with most E. coli belonging to the phylogenetic group B2 and
D (Hamelin et al. 2006,2007, Finn et al. 2020). In addi-
tion, in a study from coastal marine sediments, 40% E. coli
belonged to the phylogenetic group B2 and D with ExPEC-
associated virulence genes (Luna et al. 2010). In Australia,
it has been seen that rainwater is contaminated by ExPEC
(Ahmed et al. 2011). Additionally, some other studies have
documented that 68% of rain barrels, used as a potable wa-
ter source were contaminated by ExPEC (Ahmed et al. 2011).
Further, several other studies have also documented that
extended spectrum β-lactamase (ESBL)-producing ExPEC-
associated STs such as ST23 complex, ST533, ST69, ST131,
ST405, ST10, and ST648 were colonized and persisted in
wild birds. Notably among these, ST23 complex, ST648,
and ST33 were associated with UTIs (Tartof et al. 2005,
Moulin-Schouleur et al. 2007, Lau et al. 2008, Johnson et al.
2008c, Bonnedahl et al. 2009,2010, Guenther et al. 2010,
2011, Manges 2019, Belas et al. 2022). Recently, one study
from Bangladesh showed the presence of antibiotics resis-
tant ExPEC strains in drinking water sources (Mahmud et al.
2020).
Animal reservoirs for ExPEC
ExPEC is an important cause of various infections; and ani-
mals are recognized as a reservoir for human ExPEC. Impor-
tantly, human-associated ExPEC are also found in pig farm
and retail pork meat. There is not much research conducted,
but few studies show the pork products contaminated with
ExPEC (Vincent et al. 2010, Jakobsen et al. 2010b,2011).
A study was conducted by Mange et al. in which reported
women experiencing UTI were more likely to report frequent
pork consumption (Mange et al. 2007). In Denmark and Nor-
way, an ExPEC lineage ST131 was detected from pork prod-
ucts, which is associated with UTI (Trobos et al. 2009, Manges
and Johnson 2017). Additionally, few studies reported that
ExPEC lineage isolated from pork and beef shows similarity
with human-associated ExPEC O11/O17/O77: K52: H18-D-
ST69 (Ramchandani et al. 2005, Vincent et al. 2010, Jakobsen
et al. 2011, Manges and Johnson 2017). Surveys of the in-
fections associated with E. coli in pets, and surveillance stud-
ies at veterinary hospitals show the dissemination of geneti-
cally related antibiotics resistance ExPEC in cats, dogs, and
other animals that live in close contact with humans (Platell
et al. 2010,2011, Manges and Johnson 2017). However, ev-
idence shows that the prevalence of ExPEC-associated viru-
lence genes was lower in pork than chicken meat (Cortés et
al. 2010, Jakobsen et al. 2010b,Bergeronetal.2012,Dinget
al. 2012, Mitchell et al. 2015). Much current effort is directed
toward determining the contribution of food animals origi-
nated ExPEC strains, in turn, associated with various infec-
tions both in humans and animals (Russo and Johnson 2003,
Kabir 2010, Mitchell et al. 2015, Mellata et al. 2018). Close
contact between a household pet (dog and cat) and people of-
fers favorable conditions for zoonotic transmission of bacte-
ria (Messenger et al. 2014). In addition, closely related ExPEC
strains have been isolated from human and their companion
animals, e.g. an E. coli strain O1: K1: H7-B2-ST95 shared
>45% similarity with UTI-causing E. coli strain (Johnson et
al. 2006). Similarly, an E. coli strain O1: K1: H7-B2-ST73 re-
covered from family members and their dog, which infected
both the humans and dogs, caused UTI (Murray et al. 2004,
Johnson and Clabots 2006, Manges and Johnson 2017). The
human ExPEC lineages O6: K15: H31: B2-ST127 and O4:
K54: H5-B2-ST492 were recovered from dogs, cats, and hu-
mans (Johnson et al. 2001, Manges and Johnson 2017). In
Denmark and Norway, E. coli strain, ST131, was detected in
pork (Trobos et al. 2009). Another study documented that
∼50% E. coli of canine fecal samples qualied for ExPEC,
which in turn, was showing genotypic and phenotypic simi-
larity to human ExPEC (Platell et al. 2010,2011). Some ev-
idences also supported that both beef and cattle are reser-
voirs for ExPEC; but, it has been seen that the prevalence
of ExPEC is very low in beef cattle sources (Johnson et al.
2009a,Xiaetal.2011b). Other studies reported contami-
nated pork products with ExPEC (Vincent et al. 2010, Jakob-
sen et al. 2010b,Xiaetal.2011a); while a study exhib-
ited the genotypic similarity between pig isolated E. coli and
poultry isolated ExPEC (Cortés et al. 2010). Evidence for
beef cattle reservoirs for human-associated ExPEC seems to
be very weak; in fact, only one isolate from cow was ef-
fectively similar to human-isolated ExPEC O11/17/77: K52:
H18-D-ST69 (Ramchandani et al. 2005). Likewise, in Aus-
tralia, three antimicrobial-resistant human ExPEC lineages
O25: H4-B2-ST131, O/11O17/O77: K52: H18-D-ST69, and
O15: K52: H1-B2-ST393 were isolated from companion an-
imals (Platell et al. 2010, Manges and Johnson 2017). These
ndings demonstrate that the spread of ExPEC strains is not
limited to humans, which supports the hypothesis of ExPEC
transmission between animals with humans.
Poultry as a reservoir for ExPEC
It is hypothesized that poultry products act as a reservoir for
human ExPEC (Manges and Johnson 2012, Manges 2016,
Manges and Johnson 2017). Centers for Disease Control and
Prevention published a report on the zoonotic risk of ExPEC
on public health and transmission of ExPEC through chicken
meat (Vincent et al. 2010,Bergeronetal.2012,Moraetal.
2012). More importantly, two recent studies have also demon-
strated the ability of chicken-sourced ExPEC strains to cause a
diverse range of extraintestinal infections in an animal model
with relation to putative ExPEC pathotypes (Stromberg et
al. 2017, Mellata et al. 2018). APEC and human-associated
ExPEC have similar phylogenetic backgrounds and share sim-
ilar virulence genes (Manges and Johnson 2012). Evidence
shows that the APEC strain (O1: K1: H7) is highly similar
to isolated human UPEC and NMEC strains (Johnson et al.
2007, Jørgensen et al. 2019). Extensive genetic similarity be-
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
4Meena et al.
tween APEC and human-associated ExPEC has been docu-
mented, causing disease in poultry and humans, respectively
(Rodriguez-Siek et al. 2005, Johnson et al. 2007,2012,Mora
et al. 2009,2012, Jørgensen et al. 2019). The experimental
evidence shows APEC strains ability to cause UTIs in hu-
mans (Zhao et al. 2009, Kathayat et al. 2021). One system-
atic review has been conducted that addresses the potential of
food-borne transmission of ExPEC, but is focused on ESBL–
producing ExPEC (Lazarus et al. 2015, Ramos et al. 2020).
However, several studies in the last few years also show
that poultry and poultry products, especially chicken, could
be a reservoir of ExPEC (Johnson et al. 2003,2008c,2009c,
2017, Rodriguez-Siek et al. 2005, Bonnet et al. 2009,Lyhs
et al. 2012, Meena et al. 2021). There is some growing evi-
dence that ExPEC strains isolated from humans and chicken
share a similar clonal background, which established a valu-
able data line that provides signicant information poultry
could act as a reservoir of ExPEC (Rodriguez-Siek et al.
2005, Moulin-Schouleur et al. 2007, Johnson et al. 2008c,
Manges 2016). Additionally, colibacilloses strains that are iso-
lated from the avian intestinal tract, feces, and environmen-
tal source, which is highly similar to human ExPEC strains
(Johnson et al. 2007,Ewersetal.2009,Moraetal.2009,
2010). Notably, most similarities between APEC and human
ExPEC belong to phylogenetic groups B2 and serogroups O1,
O2, and O18; these three serogroups are mostly prevalent
in ExPEC, especially in APEC (Jeong et al. 2021). Although
the direct transmission of ExPEC has not been demonstrated,
the abundant evidence set the similar link between ExPEC re-
covered from food animal product’s and human isolated Ex-
PEC. Several groups of E. coli O25: H4: ST131 and other
ExPEC lineages (ST69/ST394/ST95/ST10/ST117) have been
identied in poultry, which can cause extraintestinal infections
in both human and poultry (Vincent et al. 2010,Bergeron
et al. 2012, Aslam et al. 2014). In Sweden, 50% of ESBL-
producing E. coli lineage ST69/394/95/10, and ST117 were
recovered from domestic chicken retail meat (Agersø et al.
2014, Egervärn et al. 2014). Similarly, in Finland, ∼22% of
human-associated ExPEC was recovered from retail poultry
meat (Lyhs et al. 2012). Additionally, in India, our study rst
time reported that the poultry is the reservoir for multidrug-
resistant (MDR) ExPEC and ExPEC associated pathotypes,
such as UPEC, NMEC, APEC, and SEPEC (Meena et al.
2021,2022). Overall, these studies show the similarity be-
tween APEC and human-associated ExPEC and seem to indi-
cate that APEC stains also behave as a zoonotic pathogen and
cause infections in poultry and as well as in human (Kaper et
al. 2004, Rodriguez-Siek et al. 2005,Ewersetal.2007, John-
son et al. 2007,2008c, Moulin-Schouleur et al. 2007,Moraet
al. 2009,2012,Zhaoetal.2009, Bauchart et al. 2010,Tiven-
dale et al. 2010).
Human-associated ExPEC in poultry
Recently, researchers gave more attention to food-borne bac-
terial transmission, especially retail meat associated ExPEC,
to proposed chain of food-borne ExPEC infections (Jakobsen
et al. 2010a, Overdevest et al. 2011, Stromberg et al. 2017,
Meena et al. 2021). A systematic study was conducted by
Vincent et al. on the outbreak of ExPEC from related infec-
tions (Vincent et al. 2010). Several groups of E. coli O25: H4:
ST131 and another ExPEC lineage (ST69, ST394, ST95, ST10,
and ST117) have been identied in poultry, which can cause
extraintestinal infections in both human and poultry (Vin-
cent et al. 2010, Johnson et al. 2011,Bergeronetal.2012,
Aslam et al. 2014). In Sweden, a large proportion (50%) of
retail meat was found contaminated with ESBL-producing
or AmpC-producing E. coli, especially lineages ST69, ST394,
ST95, ST10, and ST117 were recovered (Agersø et al. 2014,
Egervärn et al. 2014, Manges 2016). In Canada, a specic Ex-
PEC lineage, O25: H4-B2-ST131 have been identied in poul-
try retail chicken meat, which is genetically similar to a human
UTI causing strain (Vincent et al. 2010). Similarly, in Finland,
22% of human-associated ExPEC was recovered from poul-
try meat (Lyhs et al. 2012). Notably, Danish researchers iso-
lated ExPEC from humans and imported poultry meat, and
identied closely related ExPEC based on virulence genotype
(Jakobsen et al. 2011). The same group recovered a ExPEC
lineage D-ST69 from broiler and chicken meat, which have
the zoonotic potential ability in mouse UTI model (Jakobsen
et al. 2011). Studies in the Netherlands provide evidence of
ESBL-producing E. coli lineage ST10, ST58, ST117, and ST10;
isolated from poultry or retail meat chicken, with indistin-
guishable ESBL genes (blaCTX-M-1 and blaTEM-52) (Leverstein-
van Hall et al. 2011). In another study, ESBL-producing E.
coli from human infections stool retail chicken meat and from
human blood samples, which all share common STs, includ-
ing ST10, ST117, ST168, and ST23 (Leverstein-van Hall et al.
2011, Overdevest et al. 2011). Several studies in North Amer-
ica and Canada recovered highest level of ExPEC in poultry
and evidence of clusters of ExPEC from chicken meat and hu-
man infections that were similar (Vincent et al. 2010,Aslam
et al. 2014).
Human-associated ExPEC and outbreak from food
animals
Food-borne bacteria typically associated with food derived
from animals like retail meat, egg, milk, etc. However, these
foods are now commonly consumed because of their impor-
tance in a balanced diet. Over the last few years, several
outbreaks of food-borne illness caused by pathogenic bac-
teria, such as InPEC and ExPEC, have been associated with
the consumption of animal-origin food products, especially
meat (Bergeron et al. 2012). Pathogenic E. coli strains, es-
pecially ExPEC,are among the signicant infectious bacte-
ria, which are frequently implicated in outbreaks of food-
borne illnesses, linked with the consumption of retail poul-
try meat, pork, and beef (Table 1). ExPEC can be colonized,
persist in humans and animal’s intestinal tract, and act as
reservoirs for pathogenic E. coli strains. Several ExPEC lin-
eage have shown contributions in overall ExPEC infections
in humans, including O25b: H4-B2-ST-131, O25a: H4(a)-D-
ST648, O11/O17/O77: K52: H18-D-ST69, O15: K52H1-D-
ST393, and O15: K52H1-D-ST117, A-ST-10, D-ST104, etc.
(Manges and Johnson 2017, Manges et al. 2019). Escherichia
coli O11/O17/O77: K52H18-D-ST69 (also known as CgA,
for “clonal group A”) was identied as an initial outbreak of
extraintestinal infections in Berkeley, California, Calgary as-
sociated with UTI (George and Manges 2010, Pitout 2012b,
Mohamed et al. 2015). In North America, several studies
have shown the outbreak of ExPEC lineage ST10, ST23, and
ST131, which was associated with UTIs in humans (Vincent
et al. 2010, Leverstein-van Hall et al. 2011).
Additionally, E. coli O15: K52: H1-D-ST393 was recog-
nized for the rst outbreak of extraintestinal infections, back
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
The antimicrobial-resistant trend in food-borne pathogens 5
Ta b l e 1 . Summary of major human-associate ExPEC groups with their non-human source (food-animal reservoirs) and associated characteristics.
ExPEC strains/or
lineages
Food animal
sources Associated characteristic
Year rst
isolates Reference/Country Reference
Poultry Beef/Cattle Swine
ESBL-
production
Antimicrobial-
Resistance
E. coli O15:K12: H1 1986 London, UK (Phillips et al. 1988,George
and Manges 2010)
E. coli O15:K52:
H1-D-ST393
1986 Spain (Phillips et al. 1988,Pratset
al. 2000)
E. coli O78: H10 1991 Copenhagen (Olesen et al. 1994)
E. coli O25:H4: B2
-ST131
1992 Canada (Platell et al. 2011, Manges
and Johnson 2012)
E. coli
O11/O17/O73/O77:K12:
H18
1991 USA, Spain (Manges et al. 2001, Vincent
et al. 2010, Blanco et al.
2011)
E. coli-A∗-ST10 1991 Copenhagen (Leverstein-van Hall et al.
2011, Overdevest et al.
2011, Olesen et al. 2012)
E. coli-A
∗-D-ST117 1991 The Netherlands,
Canada
(Vincentetal.2010,
Leverstein-van Hall et al.
2011, Manges and Johnson
2012,Moraetal.2012)
E. coli O1/O2/18:
K1:H7: B2 -ST95
1997 France (Mora et al. 2009, Vincent et
al. 2010, Riley 2014)
E. coli O6:
H1-B2-ST73
2000 UK (Gibreel et al. 2012, Manges
and Johnson 2012, Riley
2014)
E. coli
O11/O17/O77:K52:H18D-
ST69
1990 California (Johnson et al. 2011,
Manges and Johnson 2012,
Riley 2014)
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
6Meena et al.
in 1986 in London, UK (Phillips et al. 1988); subsequently, it
was identied across Europe (Messenger et al. 2014). More
recently, in the UK, an ESBL-producing strain of E. coli
O6: H1-B2-ST73 was reported as a leading cause of hu-
man extraintestinal infections (Platell et al. 2010, Gibreel et
al. 2012). In Australia, three ExPEC lineage O25: H4-B2-
ST131, O11/O17/O77: K2: H18-D-ST69, and O15: K52: H1-
D-ST393 were identied in companion animals (Platell et al.
2010). Severe ExPEC O11: K52: H18-D-ST-69 were also iden-
tied in Calgary, Canada, in 2000 (Manges 2016). In retail
poultry meat, several human-associated ExPEC lineage has
been identied, E. coli O25: H4-ST131 and other ExPEC lin-
eage ST69, ST394, ST95, ST10, ST58, and ST117 were iden-
tied in poultry meat in both Sweden and the Netherlands
(Leverstein-van Hall et al. 2011, Egervärn et al. 2014). In
North America, several studies have shown the outbreak of
ST10, ST23, and ST131 ExPEC lineage, was associated with
UTIs in humans (Vincent et al. 2010, Leverstein-van Hall et
al. 2011). Escherichia coli ST117 and ST10, which are rec-
ognized as human sepsis associated, were isolated from retail
chicken meat in the Netherlands and Canada (Vincent et al.
2010,Moraetal.2012). This study highlighted the impor-
tance of these ExPEC lineages, among these lineages, ST131,
ST69, and ST393 mainly associated with different ExPEC in-
fections (Blanco et al. 2011). ST131 E. coli alone was esti-
matedtocause∼17% of extraintestinal infections (Johnson
et al. 2009b), more importantly, these ExPEC lineages are be-
coming increasing MDR (Manges and Johnson 2017).
Source of contamination
Animal food commodities such as meat, pork, egg, and milk
and fresh produce such as fruits and vegetables refer to the
establishment of the food safety chain in the “farm-to-fork”
model (Crump et al. 2002). The emergence of the variant dis-
ease has raised awareness of the essential contaminated food
products. However, limited attention has been given to the role
of ExPEC contamination of food products in human food-
borne illness. ExPEC can contaminate animal’s carcasses at
slaughterhouses or cross-contaminate other food commodi-
ties, leading to human illness. Moreover, food preparation and
storage producing food items may also introduce ExPEC dur-
ing the processing environment. Transmission of ExPEC from
poultry to humans happens through contaminated meat con-
sumption, but another plausible route could be an environ-
mental source (water and soil), which is contaminated by ma-
nure or fecal of birds and wild and domestic animals (Duriez et
al. 2008,Grahametal.2008, Guenther et al. 2010). Several re-
searchers have demonstrated human-to-human transmission
of ExPEC unambiguously (Foxman et al. 1997, Jakobsen et al.
2010b, Ulleryd et al. 2015). Investigation provides some evi-
dence, which supports that sewage water contains high con-
centration of human fecal waste that could play a vital role in
ExPEC transmission (Hamelin et al. 2006, Boczek et al. 2007,
Holcomb et al. 2020). Therefore, it is possible that the con-
tamination of fruits and vegetables occurred in elds or dur-
ing food processing (Vincent et al. 2010,Ratheretal.2017).
Some studies also reported that ExPEC was found even in
the aquatic ecosystem (Hamelin et al. 2007, Rayasam et al.
2019). Chicken-to-chicken transmission of ExPEC has been
noted through pecking or inhalation of contaminated fecal
dust and death in poultry (Stromberg et al. 2017). Transmis-
sion of ExPEC between chickens can increase the tness of
ExPEC strains colonized in chickens; this in turn, could in-
crease the rate of dissemination of ExPEC in poultry food
products, which leads to the transmission of ExPEC in hu-
mans (Xia et al. 2011b). Although meat is generally consid-
ered a vehicle to transmit ExPEC, a recent study shows that
various ExPEC strains disseminate via meat (Johnson et al.
2003,2005). Although there is no doubt concerning the po-
tential of ExPEC transfer to humans from different animal
food products, which might be a result of the mishandling
and/or undercooked meat. But it is still a challenge for the
researcher to determine the direction of ExPEC transmission.
Although the unidirectional transfer from animals to humans
via egg and meat, and human-to-human transmission via hos-
pital contact and sexual transmission is considered important
in opposite to bidirectional transfer. A more intensive inves-
tigation should be required to understand the entire complex
of environmental dissemination route of ExPEC.
In our speculation, the transmission of ExPEC could be to
agro-ecosystems by using contaminated water for irrigation
and animal manure used as fertilizer. It is well accepted that
animal fecal (cattle and poultry) has been used as a fertilizer
since long, which contains antibiotic ExPEC (Ramchandani et
al. 2005; Meena et al. 2021; Meena et al. 2022). ExPEC can
be transferred from contaminated manure/irrigation water to
agricultural system and can be transmitted to both human and
animals (Fig. 1). Cross-contamination of ExPEC could be be-
tween animal food and agricultural food items during food
processing at similar environmental surface. In previous stud-
ies, it has been shown that the direct dissemination of ExPEC
happens between food animals (pig, beef, and chicken) and
people associated with animal agriculture or are in close con-
tact with animals slaughtered (Marshall et al. 1990,Vanden
Bogaard et al. 2001).
Antimicrobial resistance in ExPEC: impact on public
health
Globally, AMR is one of the most rapidly growing global
threat that affect human and animal health, food safety, and
the environment at large (Laxminarayan et al. 2013). Over
the recent years, a growing body of evidence suggests that fre-
quent and inappropriate use of antibiotics in clinical settings,
as well as in non-clinical settings, such as in veterinary, have
resulted in accelerating the pace of antimicrobials that are cru-
cial for both human and veterinary medicines (Laxminarayan
et al. 2013, Thanner et al. 2016). The increase in resistance is
eroding the effectiveness of critically and highly important an-
timicrobials (Meena et al. 2022). Nearly all-important classes
of antibiotics extensively and frequently used for both humans
and veterinary not only act as therapeutic agents, but also
for growth promotion in food animals (Van den Bogaard et
al. 2001, Van Boeckel et al. 2014,2015). Therefore, the an-
tibiotics selection pressure for resistance in bacteria in food
animals is high; consequently, their faecal microbiota contain
a relatively high portion of resistance bacteria (van den Bo-
gaard and Stobberingh 1999, Van den Bogaard et al. 2001,
Larsson and Flach 2022). Additionally, the high prevalence
of AMR bacteria in food animals play an important role, not
only in human and animal health, but also in horizontal gene
transfer of resistance genes to nonpathogenic/commensal bac-
teria of gut microbiota (Laxminarayan et al. 2013). More im-
portantly, dissemination of resistance strains from animal to
human can be through direct contact between animals and
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
The antimicrobial-resistant trend in food-borne pathogens 7
Figure 1. Systematic representation of how to t ExPEC in the “One-Health” paradigm, which shows the circulation of ExPEC between
agricultural-product, food-animals, and in humans.
Figure 2. Systematic model representation possible route of antibiotic resistance ExPEC spreads through food-producing animals and Environmental
food product (s).
humans or through the indirect contact like environmental
spread via consumption of contaminated food (Van den Bo-
gaard et al. 2001).
The emergence of food-borne illnesses linked with animal’s
consumption produces food products; growing food safety
and public health issues are related to animal’s food prod-
ucts in human exposure to antimicrobial-resistant bacteria.
Both in developed and developing countries, the clinical and
some community data showed the burden of AMR (Laxmi-
narayan et al. 2013, Laxminarayan and Chaudhury 2016,
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
8Meena et al.
Meena et al. 2022). Antimicrobial has been extensively used in
animal husbandry for preventing diseases, reduce infections,
and to increase feed productions. Up to late 1990s, all Ex-
PEC major groups were susceptible to rst-line antibiotics
such as ampicillin and trimethoprim-sulfamethoxazole (SXT)
(Laxminarayan and Chaudhury 2016). The rising prevalence
in ExPEC of resistance to all rst-line drugs makes the treat-
ment of such infections increasingly challenging. Antibiotics
used by humans provide additional selection pressure when
ExPEC enters the human population. In human, UPEC-origin
UTIs are conventionally treated with ampicillin or combina-
tion of trimethoprim-sulfamethoxazole. But, through the fre-
quent use of these antibiotics, it’s observed that UPEC shows
resistance against these agents (Smith et al. 2007,Wieseret
al. 2010, Meena et al. 2022). MDR bacteria have been de-
ned as bacteria resistant to at least one agent in three or more
antimicrobial classes (Magiorakos et al. 2012). According to
the World Health Organization (WHO), antibiotics resistance
has been recognized as a global health problem for the last
many decades, and it is one of the top health challenges in the
21st century (World Health Organization 2021). From a pub-
lic health perspective, use of antimicrobials in food-producing
animals for growth promoter is banned in European countries,
but still used in other countries worldwide (Bonnet et al. 2009,
Grave et al. 2010). Notably, the food animal intestinal micro-
biota is served as a reservoir for antimicrobial-resistant deter-
minates of ExPEC, so there is a need to clarify the ecological
behavior and antimicrobial-resistant pattern ExPEC in terms
of public health and food safety. Therefore, MDR emerging
among ExPEC has created signicant economic and public
health concerns (Meena et al. 2022).
According to a survey in the USA, global consumption of
antibiotics in animals and in agricultural settings have in-
creased; 80% of antibiotics are annually used for animal agri-
culture, which effectively is very high, as compared to hu-
mans (Pavlin et al. 2009, Van Boeckel et al. 2015, Manyi-
Loh et al. 2018, Tiseo et al. 2020). Although the prevalence
and spread of antibiotic-resistant ExPEC in clinical settings
have been well studied, antibiotic-resistant ExPEC from food-
animal origin have been limited. Thus, there is a need for
more systematic studies to better understand animals and
food animal product’s possible role in human exposure to
antimicrobial-resistant bacteria. Notably, the agricultural sec-
tor may be a vehicle for transmitting antimicrobial-resistant
ExPEC in humans or animals. The systematic representation
of the circulation of antimicrobial-resistant ExPEC in humans
via animals to agricultural products under the “One-Health”
paradigm illustrated in (Fig. 2).
Over the past decade, several studies in the context of
North and South America have shown 20% to 45% of E. coli
strains, which were resistant to front-line antimicrobials, such
as cephalosporin’s, quinolones, and sulfamethoxazole (Fox-
man 2010, Pitout 2012a, Mellata 2013). Prevalence of an-
tibiotics resistant ExPEC in food animals differs signicantly
from country to country and it depends on variations in an-
tibiotics usage. Initially tetracycline-resistant was reported in
1961, a period in which, tetracycline-containing feed was used
in the poultry sector (Sojka and Carnaghan 1961). There are
highly successful lineages or groups, which are MDR, and
are responsible for most human extraintestinal infections. For
example, E. coli O25: H4-ST131, a globally disseminated
strain has been shown to be responsible for up to 60% of
all E. coli infections, and account for up to 78% of infections
caused by uoroquinolone-resistant ExPEC. The increase of
AMR among ExPEC strains is complicated to therapeutic pur-
pose, and poses a serious concern for human health and food
safety.
Conclusion
Several outbreaks of food-borne illnesses have been linked
with the consumption of food animal origins commodities
such as meat, egg, etc., mainly caused by ExPEC strain. It’s
well known that animals are reservoirs for InPEC, but whether
environmental and agricultural food are a source for hu-
man infection associated with ExPEC is still a matter of de-
bate. Food animals and their products are hypothesized to
be reservoirs and vehicles for antimicrobial resistant and Ex-
PEC to both workers and consumers. As antimicrobials are
commonly used in animals for treatment and feed produc-
tions, one must note that there is extensive use of antimi-
crobial agents in food animals for production. Thus, food
animals associated with ExPEC typically exhibit MDR phe-
nomenon. Further, the use of antimicrobials in agriculture,
farm, and veterinary eld also favor the dissemination of
antimicrobial-resistant ExPEC in animals to the environment.
Antimicrobial-resistant ExPEC could be spread in the envi-
ronment from farm waste, and could be transferred from an-
imals to humans through food animals’ commodities. The in-
appropriate use of antibiotics in humans also plays a vital role
in this complex problem, and this could make it more compli-
cated to treat infections caused by MDR ExPEC. So there is a
need to reduce the antimicrobial effect, and instead use alter-
native approaches to limit the spread of AMR, both in animals
and humans.
In summary, our review for the rst time hypothesized un-
der a global context that agricultural foods, such as vegeta-
bles and fruits, could be alternative reservoirs for ExPEC,
they could play a vital role in transmitting ExPEC to both
human and animals. This review summarized the evidence
that food-borne organisms are a signicant cause of ExPEC
infections in humans, and are resistant to clinically induced
antibiotics. More importantly, this study reveals information
that could aid in novel preventive and control strategies,
which ultimately leads to managing food-borne illnesses. This
would potentially reduce the risk of human contamination
by antimicrobial-resistant ExPEC. Furthermore, understand-
ing these organism reservoirs, transmission chains, and the
epidemiologic association would help nd a way to reduce
the infection burden at large.
Acknowledgments
The author is thankful to other authors, and gratefully ac-
knowledges the Central University of Rajasthan, Ajmer India.
Conict of interest
None declared.
Funding
This work was supported by the Department of Science and
Technology, Science and Engineering Research Board (No.
SB/YS/LS-98/2014 and EEQ/2017/000496), Government of
India.
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
The antimicrobial-resistant trend in food-borne pathogens 9
Author contributions
P.R.M. and A.P.S. conceived the idea of the review; P.R.M.
wrote the paper and generated all the gures. P.P. helped in re-
vision of the manuscript and all authors revised and approved
the nal version of manuscript.
Data availability
The authors conrm that the data supporting the ndings of
this study are available within the article.
References
Abhirosh C, Sherin V, Thomas A et al. Potential public health signif-
icance of faecal contamination and multidrug-resistant Escherichia
coli and Salmonella serotypes in a lake in India. Public Health Rep
2011;125:377–9.
Agersø Y, Jensen JD, Hasman H et al. Spread of extended spectrum
cephalosporinase-producing Escherichia coli clones and plasmids
from parent animals to broilers and to broiler meat in a production
without use of cephalosporins. Foodborne Pathog Dis 2014;11:740–
6.
Ahmed AM, Shimamoto T. Isolation and molecular characterization
of Salmonella enterica,Escherichia coli O157: H7 and Shigella
spp. from meat and dairy products in Egypt. Int J Food Microbiol
2014;168-169:57–62.
Ahmed W, Hodgers L, Masters N et al. Occurrence of intestinal and
extraintestinal virulence genes in Escherichia coli isolates from rain-
water tanks in Southeast Queensland, Australia. Appl Environ Mi-
crobiol 2011;77:7394–400.
Anastasi E, Matthews B, Gundogdu A et al. Prevalence and persis-
tence of Escherichia coli strains with uropathogenic virulence char-
acteristics in sewage treatment plants. Appl Environ Microbiol
2010;76:5882–6.
Aslam M, Toufeer M, Bravo CN et al. Characterization of extraintesti-
nal pathogenic Escherichia coli isolated from retail poultry meats
from Alberta, Canada. Int J Food Microbiol 2014;177:49–56.
Banerjee R, Johnston B, Lohse C et al.The clonal distribution and diver-
sity of extraintestinal Escherichia coli isolates vary according to pa-
tient characteristics. Antimicrob Agents Chemother 2013;57:5912–
7.
Bauchart P, Germon P, Brée A et al. Pathogenomic comparison of hu-
man extraintestinal and avian pathogenic Escherichia coli–search
for factors involved in host specicity or zoonotic potential. Microb
Pathog 2010;49:105–15.
Beghain J, Bridier-Nahmias A, Le Nagard H et al. ClermonTyping:
an easy-to-use and accurate in silico method for Escherichia genus
strain phylotyping. Microb Genom 2018;4:e000192.
Bélanger L, Garenaux A, Harel J et al.Escherichia coli from animal
reservoirs as a potential source of human extraintestinal pathogenic
E. coli.FEMS Immunol Med Microbiol 2011;62:1–10.
Belas A, Marques C, Menezes J et al. ESBL/pAmpC-producing Es-
cherichia coli causing urinary tract infections in non-related com-
panion animals and humans. Antibiotics 2022;11:559.
Bergeron CR, Prussing C, Boerlin P et al. Chicken as reservoir for ex-
traintestinal pathogenic Escherichia coli in humans, Canada. Emerg
Infect Dis 2012;18:415.
Blanco J, Mora A, Mamani R et al. National survey of Escherichia coli
causing extraintestinal infections reveals the spread of drug-resistant
clonal groups O25b: H4-B2-ST131, O15: H1-D-ST393 and CGA-
D-ST69 with high virulence gene content in Spain. J Antimicrob
Chemother 2011;66:2011–21.
Boczek LA, Rice EW, Johnston B et al. Occurrence of antibiotic-
resistant uropathogenic Escherichia coli clonal group a in wastewa-
ter efuents. Appl Environ Microbiol 2007;73:4180–4.
Bonnedahl J, Drobni M, Gauthier-Clerc M et al. Dissemination of Es-
cherichia coli with CTX-M type ESBL between humans and yellow-
legged gulls in the south of France. PLoS One 2009;4:e5958.
Bonnedahl J, Drobni P, Johansson A et al. Characterization, and com-
parison, of human clinical and black-headed gull (Larus ridibundus)
extended-spectrum β-lactamase-producing bacterial isolates from
Kalmar, on the southeast coast of Sweden. J Antimicrob Chemother
2010;65:1939–44.
Bonnet C, Diarrassouba F, Brousseau R et al. Pathotype and antibiotic
resistance gene distributions of Escherichia coli isolates from broiler
chickens raised on antimicrobial-supplemented diets. Appl Environ
Microbiol 2009;75:6955–62.
Cantas L, Suer K. Review: the important bacterial zoonoses in “one
health” concept. Front Public Health 2014;2:144.
Cho S, Jackson C, Frye J. The prevalence and antimicrobial resistance
phenotypes of Salmonella,Escherichia coli and Enterococcus sp. in
surface water. Lett Appl Microbiol 2020;71:3–25.
Clermont O, Christenson JK, Denamur E et al. The clermont Es-
cherichia coli phylo-typing method revisited: improvement of speci-
city and detection of new phylo-groups. Environ Microbiol Rep
2013;5:58–65.
Cortés P, Blanc V, Mora A et al. Isolation and characterization of po-
tentially pathogenic antimicrobial-resistant Escherichia coli strains
from chicken and pig farms in Spain. Appl Environ Microbiol
2010;76:2799–805.
Croxall G, Hale J, Weston V et al. Molecular epidemiology of ex-
traintestinal pathogenic Escherichia coli isolates from a regional
cohort of elderly patients highlights the prevalence of ST131
strains with increased antimicrobial resistance in both commu-
nity and hospital care settings. J Antimicrob Chemother 2011;66:
2501–8.
Crump JA, Grifn PM, Angulo FJ. Bacterial contamination of animal
feed and its relationship to human foodborne illness. Clin Infect Dis
2002;35:859–65.
Denamur E, Clermont O, Bonacorsi S et al. The population genet-
ics of pathogenic Escherichia coli.Nat Rev Microbiol 2021;19:
37–54.
Dhanji H, Murphy NM, Akhigbe C et al. Isolation of uoroquinolone-
resistant O25b: H4-ST131 Escherichia coli with CTX-M-14
extended-spectrum β-lactamase from UK river water. J Antimicrob
Chemother 2011;66:512–6.
Ding Y, Tang X, Lu P et al. Clonal analysis and virulent traits of
pathogenic extraintestinal Escherichia coli isolates from swine in
China. BMC Vet Res 2012;8:1–7.
Dolejska M, Frolkova P, Florek M et al. CTX-M-15-producing Es-
cherichia coli clone B2-O25b-ST131 and Klebsiella spp. isolates
in municipal wastewater treatment plant efuents. J Antimicrob
Chemother 2011;66:2784–90.
Duriez P, Zhang Y, Lu Z et al. Loss of virulence genes in Escherichia
coli populations during manure storage on a commercial swine farm.
Appl Environ Microbiol 2008;74:3935–42.
Egervärn M, Börjesson S, Byfors S et al.Escherichia coli with extended-
spectrum beta-lactamases or transferable AmpC beta-lactamases
and Salmonella on meat imported into Sweden. Int J Food Microbiol
2014;171:8–14.
Ewers C, Antão E-M, Diehl I et al. Intestine and environment
of the chicken as reservoirs for extraintestinal pathogenic Es-
cherichia coli strains with zoonotic potential. Appl Environ Micro-
biol 2009;75:184–92.
Ewers C, Grobbel M, Stamm I et al. Emergence of human pandemic
O25: H4-ST131 CTX-M-15 extended-spectrum-β-lactamase-
producing Escherichia coli among companion animals. J Antimicrob
Chemother 2010;65:651–60.
Ewers C, Li G, Wilking H et al. Avian pathogenic, uropathogenic,
and newborn meningitis-causing Escherichia coli: how
closely related are they? Int J Med Microbiol 2007;297:
163–76.
Fairbrother J, Nadeau E. Escherichia coli: on-farm contamination of
animals. Rev Sci Tech 2006;25:555–69.
Finn TJ, Scriver L, Lam L et al. A comprehensive account of Es-
cherichia coli sequence type 131 in wastewater reveals an abundance
of uoroquinolone-resistant clade a strains. Appl Environ Microbiol
2020;86:e01913–01919.
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
10 Meena et al.
Flynn K. Overview of public health and urban agriculture: water, soil
and crop contamination and emerging urban zoonoses. CFP Re-
port No. 30. International Development Research Centrem (IDRC).
1999.
Foxman B. The epidemiology of urinary tract infection. Nat Rev Urol
2010;7:653–60.
Foxman B, Zhang L, Tallman P et al. Transmission of uropathogens
between sex partners. J Infect Dis 1997;175:989–92.
George D, Manges A. A systematic review of outbreak and
non-outbreak studies of extraintestinal pathogenic Escherichia
coli causing community-acquired infections. Epidemiol Infect
2010;138:1679–90.
Gibbs PS, Kasa R, Newbrey JL et al. Identication, antimicrobial
resistance proles, and virulence of members from the family
Enterobacteriaceae from the feces of yellow-headed blackbirds
(Xanthocephalus xanthocephalus) in North Dakota. Avian Dis
2007;51:649–55.
Gibreel TM, Dodgson AR, Cheesbrough J et al. Population structure,
virulence potential and antibiotic susceptibility of uropathogenic Es-
cherichia coli from Northwest England. J Antimicrob Chemother
2012;67:346–56.
Goulart DB, Mellata M. Escherichia coli mastitis in dairy cattle: etiol-
ogy, diagnosis, and treatment challenges. Front Microbiol 2022;13.
https://doi.org/10.3389/fmicb.2022.928346
Graham JP, Leibler JH, Price LB et al. The animal-human interface and
infectious disease in industrial food animal production: rethinking
biosecurity and biocontainment. Public Health Rep 2008;123:282–
99.
Grave K, Torren-Edo J, Mackay D. Comparison of the sales of veteri-
nary antibacterial agents between 10 European countries. J Antimi-
crob Chemother 2010;65:2037–40.
Guenther S, Ewers C, Wieler LH. Extended-spectrum beta-lactamases
producing E. coli in wildlife, yet another form of environmental pol-
lution? Front Microbiol 2011;2:246.
Guenther S, Grobbel M, Lübke-Becker A et al. Antimicrobial resis-
tance proles of Escherichia coli from common European wild bird
species. Vet Microbiol 2010;144:219–25.
Hamelin K, Bruant G, El-Shaarawi A et al. A virulence and antimicro-
bial resistance DNA microarray detects a high frequency of virulence
genes in Escherichia coli isolates from Great Lakes recreational wa-
ters. Appl Environ Microbiol 2006;72:4200–6.
Hamelin K, Bruant G, El-Shaarawi A et al. Occurrence of virulence
and antimicrobial resistance genes in Escherichia coli isolates from
different aquatic ecosystems within the St. Clair River and Detroit
River areas. Appl Environ Microbiol 2007;73:477–84.
Heredia N, García S. Animals as sources of food-borne pathogens: a
review. Anim Nutr 2018;4:250–5.
Holcomb DA, Knee J, Sumner T et al. Human fecal contamination of
water, soil, and surfaces in households sharing poor-quality sanita-
tion facilities in Maputo, Mozambique. Int J Hyg Environ Health
2020;226:113496.
Jakobsen L, Garneau P, Kurbasic A et al. Microarray-based detection
of extended virulence and antimicrobial resistance gene proles in
phylogroup B2 Escherichia coli of human, meat and animal origin.
J Med Microbiol 2011;60:1502–11.
Jakobsen L, Hammerum AM, Frimodt-Møller N. Detection of clonal
group a Escherichia coli isolates from broiler chickens, broiler
chicken meat, community-dwelling humans, and urinary tract infec-
tion (UTI) patients and their virulence in a mouse UTI model. Appl
Environ Microbiol 2010a;76:8281–4.
Jakobsen L, Spangholm DJ, Pedersen K et al. Broiler chickens, broiler
chicken meat, pigs and pork as sources of ExPEC related vir-
ulence genes and resistance in Escherichia coli isolates from
community-dwelling humans and UTI patients. Int J Food Micro-
biol 2010b;142:264–72.
Jeong J, Lee J-Y, Kang M-S et al. Comparative characteristics and
zoonotic potential of avian pathogenic Escherichia coli (APEC)
isolates from chicken and duck in South Korea. Microorganisms
2021;9:946.
Johnson JR, Clabots C. Sharing of virulent Escherichia coli clones
among household members of a woman with acute cystitis. Clin In-
fect Dis 2006;43:e101–8.
Johnson JR, Clabots C, Kuskowski MA. Multiple-host sharing,
long-term persistence, and virulence of Escherichia coli clones
from human and animal household members. J Clin Microbiol
2008a;46:4078–82.
Johnson JR, Delavari P, O’Bryan TT et al. Contamination of re-
tail foods, particularly Turkey, from community markets (Min-
nesota, 1999–2000) with antimicrobial-resistant and extraintestinal
pathogenic Escherichia coli.Foodbourne Pathog Dis 2005;2:38–49.
Johnson JR, Delavari P, Stell AL et al. Molecular comparison of extrain-
testinal Escherichia coli isolates of the same electrophoretic lineages
from humans and domestic animals. J Infect Dis 2001;183:154–9.
Johnson JR, Johnston B, Clabots CR et al. Virulence genotypes and phy-
logenetic background of Escherichia coli serogroup O6 isolates from
humans, dogs, and cats. J Clin Microbiol 2008b;46:417–22.
Johnson JR, Kuskowski MA, Menard M et al. Similarity between hu-
man and chicken Escherichia coli isolates in relation to ciprooxacin
resistance status. J Infect Dis 2006;194:71–78.
Johnson JR, Menard M, Johnston B et al. Epidemic clonal groups of
Escherichia coli as a cause of antimicrobial-resistant urinary tract
infections in Canada, 2002 to 2004. Antimicrob Agents Chemother
2009a;53:2733–9.
Johnson JR, Menard ME, Lauderdale T-L et al. Global distribution and
epidemiologic associations of Escherichia coli clonal group a, 1998–
2007. Emerg Infect Dis 2011;17:2001–9.
Johnson JR, Miller S, Johnston B et al. Sharing of Escherichia coli se-
quence type ST131 and other multidrug-resistant and urovirulent E
.colistrains among dogs and cats within a household. J Clin Micro-
biol 2009b;47:3721–5.
Johnson JR, Murray AC, Gajewski A et al. Isolation and molecular char-
acterization of nalidixic acid-resistant extraintestinal pathogenic
Escherichia coli from retail chicken products. Antimicrob Agents
Chemother 2003;47:2161–8.
Johnson JR, Porter SB, Johnston B et al. Extraintestinal pathogenic and
antimicrobial-resistant Escherichia coli, including sequence type 131
(ST131), from retail chicken breasts in the United States in 2013.
Appl Environ Microbiol 2017;83:e02956–16.
Johnson JR, Russo TA. Extraintestinal pathogenic Escherichia coli: “the
other bad Ecoli”. J Lab Clin Med 2002;139:155–62.
Johnson TJ, Kariyawasam S, Wannemuehler Y et al. The genome se-
quence of avian pathogenic Escherichia coli strain O1: K1: H7
shares strong similarities with human extraintestinal pathogenic E.
coli genomes. JBacteriol2007;189:3228–36.
Johnson TJ, Logue CM, Johnson JR et al. Associations between mul-
tidrug resistance, plasmid content, and virulence potential among
extraintestinal pathogenic and commensal Escherichia coli from hu-
mans and poultry. Foodborne Pathog Dis 2012;9:37–46.
Johnson TJ, Logue CM, Wannemuehler Y et al. Examination of the
source and extended virulence genotypes of Escherichia coli con-
taminating retail poultry meat. Foodborne Pathog Dis 2009c;6:
657–67.
Johnson TJ, Wannemuehler Y, Johnson SJ et al. Comparison of ex-
traintestinal pathogenic Escherichia coli strains from human and
avian sources reveals a mixed subset representing potential zoonotic
pathogens. Appl Environ Microbiol 2008c;74:7043–50.
Jørgensen SL, Stegger M, Kudirkiene E et al. Diversity and population
overlap between avian and human Escherichia coli belonging to se-
quence type 95. MSphere 2019;4:e00333–00318.
Kabir S. Avian colibacillosis and salmonellosis: a closer look at epidemi-
ology, pathogenesis, diagnosis, control and public health concerns.
Int J Environ Res 2010;7:89–114.
Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli.Nat Rev
Microbiol 2004;2:123–40.
Kathayat D, Lokesh D, Ranjit S et al. Avian pathogenic Escherichia
coli (APEC): an overview of virulence and pathogenesis factors,
zoonotic potential, and control strategies. Pathogens 2021;10:
467.
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
The antimicrobial-resistant trend in food-borne pathogens 11
Larsson D, Flach C-F. Antibiotic resistance in the environment. Nat Rev
Microbiol 2022;20:257–69.
Lau SH, Reddy S, Cheesbrough J et al. Major uropathogenic Es-
cherichia coli strain isolated in the Northwest of England iden-
tied by multilocus sequence typing. J Clin Microbiol 2008;46:
1076–80.
Laxminarayan R, Chaudhury RR. Antibiotic resistance in India: drivers
and opportunities for action. PLoS Med 2016;13:e1001974.
Laxminarayan R, Duse A, Wattal C et al. Antibiotic resistance—the
need for global solutions. Lancet Infect Dis 2013;13:1057–98.
Lazarus B, Paterson DL, Mollinger JL et al. Do human extrain-
testinal Escherichia coli infections resistant to expanded-spectrum
cephalosporins originate from food-producing animals? A system-
atic review. Clin Infect Dis 2015;60:439–52.
Leverstein-van Hall M, Dierikx C, Cohen Stuart J et al. Dutch patients,
retail chicken meat and poultry share the same ESBL genes, plasmids
and strains. Clin Microbiol Infect 2011;17:873–80.
Luna G, Vignaroli C, Rinaldi C et al. Extraintestinal Escherichia coli
carrying virulence genes in coastal marine sediments. Appl Environ
Microbiol 2010;76:5659–68.
Lyhs U, Ikonen I, Pohjanvirta T et al. Extraintestinal pathogenic Es-
cherichia coli in poultry meat products on the nnish retail market.
Acta Vet Scand 2012;54:1–6.
Mahmud ZH, Kabir MH, Ali S et al. Extended-spectrum beta-
lactamase-producing Escherichia coli in drinking water samples
from a forcibly displaced, densely populated community setting in
Bangladesh. Front Public Health 2020;8:228.
Magiorakos AP, Srinivasan A, Carey RB et al. Multidrug-resistant, ex-
tensively drug-resistant and pandrug-resistant bacteria: an interna-
tional expert proposal for interim standard denitions for acquired
resistance. Clin Microbiol Infect 2012;18:268–81.
Manges A. Escherichia coli and urinary tract infections: the role of
poultry-meat. Clin Microbiol Infect 2016;22:122–9.
Manges AR. Escherichia coli causing bloodstream and other extrain-
testinal infections: tracking the next pandemic. Lancet Infect Dis
2019;19:1269–70.
Manges AR, Geum HM, Guo A et al. Global extraintestinal
pathogenic Escherichia coli (ExPEC) lineages. Clin Microbiol Rev
2019;32:e00135–18.
Manges AR, Johnson JR. Food-borne origins of Escherichia coli causing
extraintestinal infections. Clin Infect Dis 2012;55:712–9.
Manges AR, Johnson JR. Reservoirs of extraintestinal pathogenic Es-
cherichia coli.Microbil Spectr 2017;3:159–177.
Manges AR, Johnson JR, Foxman B et al. Widespread distribution of
urinary tract infections caused by a multidrug-resistant Escherichia
coli clonal group. NEnglJMed2001;345:1007–1013.
Manges AR, Smith SP, Lau BJ et al. Retail meat consumption and the
acquisition of antimicrobial resistant Escherichia coli causing uri-
nary tract infections: a case-control study. Foodborne Pathog Dis
2007;4:419–31.
Manyi-Loh C, Mamphweli S, Meyer E et al. Antibiotic use in agriculture
and its consequential resistance in environmental sources: potential
public health implications. Molecules 2018;23:795.
Markland S, LeStrange K, Sharma M et al. Old friends in new places:
exploring the role of extraintestinal E.coliin intestinal disease and
foodborne illness. Zoonoses Public Health Rep 2015;62:491–6.
Marshall B, Petrowski D, Levy SB. Inter- and intraspecies spread of Es-
cherichia coli in a farm environment in the absence of antibiotic
usage. Proc Nat Acad Sci 1990;87:6609–13.
Meena P, Yadav P, Hemlata H et al. Poultry-origin extraintestinal Es-
cherichia coli strains carrying the traits associated with urinary tract
infection, sepsis, meningitis and avian colibacillosis in India. J Appl
Microbiol 2021;130:2087–101.
Meena PR, Priyanka P, Rana A et al. Alarming level of single or mul-
tidrug resistance in poultry environments-associated extraintestinal
pathogenic Escherichia coli pathotypes with potential to affect the
One Health. Environ Microbiol Rep 2022;14:400–11.
Mellata M. Human and avian extraintestinal pathogenic Escherichia
coli: infections, zoonotic risks, and antibiotic resistance trends.
Foodborne Pathog Dis 2013;10:916–32.
Mellata M, Johnson JR, Curtiss R, III. Escherichia coli isolates from
commercial chicken meat and eggs cause sepsis, meningitis and uri-
nary tract infection in rodent models of human infections. Zoonoses
Public Health 2018;65:103–13.
Messenger AM, Barnes AN, Gray GC. Reverse zoonotic disease
transmission (zooanthroponosis): a systematic review of seldom-
documented human biological threats to animals. PLoS One
2014;9:e89055.
Mitchell NM, Johnson JR, Johnston B et al. Zoonotic potential of Es-
cherichia coli isolates from retail chicken meat products and eggs.
Appl Environ Microbiol 2015;81:1177–87.
Mohamed M, Owens K, Gajewski A et al. Extraintestinal pathogenic
and antimicrobial-resistant Escherichia coli contamination of 56
public restrooms in the greater Minneapolis-St. Paul metropolitan
area. Appl Environ Microbiol 2015;81:4498–506.
Mokracka J, Koczura R, Jabło ´
nska L et al. Phylogenetic groups, viru-
lence genes and quinolone resistance of integron-bearing Escherichia
coli strains isolated from a wastewater treatment plant. Antonie Van
Leeuwenhoek 2011;99:817–24.
Mora A, Herrera A, Mamani R et al. Recent emergence of clonal group
O25b: K1: H4-B2-ST131 ibeA strains among Escherichia coli poul-
try isolates, including CTX-M-9-producing strains, and compari-
son with clinical human isolates. Appl Environ Microbiol 2010;76:
6991–7.
Mora A, López C, Dabhi G et al. Extraintestinal pathogenic Escherichia
coli O1: K1: H7/NM from human and avian origin: detection of
clonal groups B2 ST95 and D ST59 with different host distribution.
BMC Microbiol 2009;9:132.
Mora A, López C, Herrera A et al. Emerging avian pathogenic
Escherichia coli strains belonging to clonal groups O111:
H4-D-ST2085 and O111: H4-D-ST117 with high virulence-
gene content and zoonotic potential. Vet Microbiol 2012;156:
347–52.
Moulin-Schouleur M, Répérant M, Laurent S et al. Extraintestinal
pathogenic Escherichia coli strains of avian and human origin: link
between phylogenetic relationships and common virulence patterns.
J Clin Microbiol 2007;45:3366–76.
Murray AC, Kuskowski MA, Johnson JR. Virulence factors pre-
dict Escherichia coli colonization patterns among human
and animal household members. AnnInternMed2004;140:
848–9.
Nordstrom L, Liu CM, Price LB. Foodborne urinary tract infections:
a new paradigm for antimicrobial-resistant foodborne illness. Front
Microbiol 2013;4:29.
Olesen B, Kolmos HJ, Ørskov F et al. Cluster of multiresistant Es-
cherichia coli O78: H10 in Greater Copenhagen. Scand J Infect Dis
1994;26:406–10.
Olesen B, Scheutz F, Andersen RL et al. Enteroaggregative Escherichia
coli O78: H10, the cause of an outbreak of urinary tract infection.
J Clin Microbiol 2012;50:3703–11.
Overdevest I, Willemsen I, Rijnsburger M et al. Extended-spectrum β-
lactamase genes of Escherichia coli in chicken meat and humans,
The Netherlands. Emerg Infect Dis 2011;17:1216.
Pavlin BI, Schloegel LM, Daszak P. Risk of importing zoonotic dis-
eases through wildlife trade, United States. Emerg Infect Dis
2009;15:1721.
Phillips I, King A, Rowe B et al. Epidemic multiresistant Escherichia coli
infection in West Lambeth health district. Lancet 1988;331:1038–
41.
Pitout J. Extraintestinal pathogenic Escherichia coli: a combination
of virulence with antibiotic resistance. Front Microbiol 2012a;3:
9.
Pitout JD. Extraintestinal pathogenic Escherichia coli: an update on an-
timicrobial resistance, laboratory diagnosis and treatment. Expert
Rev Anti Infect Ther 2012b;10:1165–76.
Platell JL, Cobbold RN, Johnson JR et al. Commonality among
uoroquinolone-resistant sequence type ST131 extraintestinal
Escherichia coli isolates from humans and companion an-
imals in Australia. Antimicrob Agents Chemother 2011;55:
3782–7.
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
12 Meena et al.
Platell JL, Cobbold RN, Johnson JR et al. Clonal group distribu-
tion of uoroquinolone-resistant Escherichia coli among humans
and companion animals in Australia. J Antimicrob Chemother
2010;65:1936–8.
Poolman JT, Wacker M. Extraintestinal pathogenic Escherichia coli,a
common human pathogen: challenges for vaccine development and
progress in the eld. J Infect Dis 2016;213:6–13.
Prats G, Navarro F, Mirelis B et al.Escherichia coli serotype O15:
K52: H1 as a uropathogenic clone. J Clin Microbiol 2000;38:
201–9.
Priyanka M, Raj P, Meghwanshi KK et al. Leafy greens as a potential
source of multidrug-resistant diarrhoeagenic Escherichia coli and
Salmonella.Microbiology 2021;167:001059.
Ramchandani M, Manges AR, DebRoy C et al. Possible animal origin of
human-associated, multidrug-resistant, uropathogenic Escherichia
coli.Clin Infect Dis 2005;40:251–7.
Ramos S, Silva V, Dapkevicius MLE et al.Escherichia coli as commen-
sal and pathogenic bacteria among food-producing animals: health
implications of extended spectrum β-lactamase (ESBL) production.
Animals 2020;10:2239.
RatherIA,KohWY,PaekWKet al. The sources of chemical con-
taminants in food and their health implications. Front Pharmacol
2017;8:830.
Rayasam SD, Ray I, Smith KR et al. Extraintestinal pathogenic Es-
cherichia coli and antimicrobial drug resistance in a Maharash-
trian drinking water system. Am J Trop Med Hyg 2019;100:
1101.
Riley L. Pandemic lineages of extraintestinal pathogenic Escherichia
coli.Clin Microbiol Infect 2014;20:380–90.
Rodriguez-Siek KE, Giddings CW, Doetkott C et al. Compari-
son of Escherichia coli isolates implicated in human urinary
tract infection and avian colibacillosis. Microbiology 2005;151:
2097–110.
Rouger A, Tresse O, Zagorec M. Bacterial contaminants of poultry
meat: sources, species, and dynamics. Microorganisms 2017;5:50.
Russo TA, Johnson JR. Proposal for a new inclusive designation for ex-
traintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect
Dis 2000;181:1753–4.
Russo TA,Johnson JR. Medical and economic impact of extraintestinal
infections due to Escherichia coli: focus on an increasingly impor-
tant endemic problem. Microbes Infect 2003;5:449–56.
Sarowska J, Futoma-Koloch B, Jama-Kmiecik A et al. Virulence factors,
prevalence and potential transmission of extraintestinal pathogenic
Escherichia coli isolated from different sources: recent reports. Gut
Pathog 2019;11:10.
Schauss K, Focks A, Heuer H et al. Analysis, fate and effects of
the antibiotic sulfadiazine in soil ecosystems. Trends Anal Chem
2009;28:612–8.
Singer RS. Urinary tract infections attributed to diverse ExPEC strains
in food animals: evidence and data gaps. Front Microbiol 2015;6:
28.
Skippen I, Shemko M, Turton J et al. Epidemiology of infections caused
by extended-spectrum β-lactamase-producing Escherichia coli and
Klebsiella spp.: a nested case–control study from a tertiary hospital
in London. J Hosp Infect 2006;64:115–23.
Smith JL, Fratamico PM, Gunther NW. Extraintestinal pathogenic Es-
cherichia coli.Foodborne Pathog Dis 2007;4:134–63.
Sojka W, Carnaghan R. Escherichia coli infection in poultry. Res Vet
Sci 1961;2:340–52.
Stromberg ZR, Johnson JR, Fairbrother JM et al. Evaluation of
Escherichia coli isolates from healthy chickens to determine
their potential risk to poultry and human health. PLoS One
2017;12:e0180599.
Tartof SY, Solberg OD, Manges AR et al. Analysis of a uropathogenic
Escherichia coli clonal group by multilocus sequence typing. J Clin
Microbiol 2005;43:5860–4.
Thanner S, Drissner D, Walsh F. Antimicrobial resistance in agriculture.
MBio 2016;7:e02227–02215.
TiseoK,HuberL,GilbertMet al. Global trends in antimicrobial use in
food animals from 2017 to 2030. Antibiotics 2020;9:918.
Tivendale KA, Logue CM, Kariyawasam S et al. Avian-pathogenic Es-
cherichia coli strains are similar to neonatal meningitis E. coli strains
and are able to cause meningitis in the rat model of human disease.
Infect Immun 2010;78:3412–9.
Trobos M, Christensen H, Sunde M et al. Characterization of
sulphonamide-resistant Escherichia coli using comparison of sul2
gene sequences and multilocus sequence typing. Microbiology
2009;155:831–6.
Ulleryd P, Sandberg T, Scheutz F et al. Colonization with Escherichia
coli strains among female sex partners of men with febrile urinary
tract infection. J Clin Microbiol 2015;53:1947–50.
Van Boeckel TP, Brower C, Gilbert M et al. Global trends in antimicro-
bial use in food animals. Proc Natl Acad Sci 2015;112:5649–54.
Van Boeckel TP, Gandra S, Ashok A et al. Global antibiotic consump-
tion 2000 to 2010: an analysis of national pharmaceutical sales data.
Lancet Infect Dis 2014;14:742–50.
Van den Bogaard A, London N, Driessen C et al. Antibiotic resistance
of faecal Escherichia coli in poultry, poultry farmers and poultry
slaughterers. J Antimicrob Chemother 2001;47:763–71.
van den Bogaard AE, Stobberingh EE. Antibiotic usage in animals.
Drugs 1999;58:589–607.
Vincent C, Boerlin P, Daignault D et al. Food reservoir for Escherichia
coli causing urinary tract infections. Emerg Infect Dis 2010;16:88.
Was i ´
nski B. Extra-intestinal pathogenic Escherichia coli–threat con-
nected with food-borne infections. Ann Agric Environ Med
2019;26:532–7.
Wieser A, Romann E, Magistro G et al. A multiepitope subunit vaccine
conveys protection against extraintestinal pathogenic Escherichia
coli in mice. Infect Immun 2010;78:3432–42.
World Health Organization. Antimicrobial resistance. 2021. https://ww
w.who.int/news-room/fact-sheets/detail/antimicrobial- resistance
(11 October 2022 data last accessed).
Xia X, Meng J, McDermott P et al.Escherichia coli from retail meats
carry genes associated with uropathogenic Escherichia coli, but are
weakly invasive in human bladder cell culture. J Appl Microbiol
2011a;110:1166–76.
XiaX,MengJ,ZhaoSet al. Identication and antimicrobial resistance
of extraintestinal pathogenic Escherichia coli from retail meats. J
Food Prot 2011b;74:38–44.
Zhao L, Gao S, Huan H et al. Comparison of virulence factors and
expression of specic genes between uropathogenic Escherichia
coli and avian pathogenic E. coli in a murine urinary tract
infection model and a chicken challenge model. Microbiology
2009;155:1634–44.
Downloaded from https://academic.oup.com/lambio/article/76/1/ovac016/6896395 by Central University of Rajasthan user on 26 February 2023
