Comparative Medicine

Vol 71, No 1
Copyright 2021 February 2021
by the American Association for Laboratory Animal Science Pages 3–45

Overview

A One Health Perspective for Defining

Alexis García1,2,§* and James G Fox2

E. coli is one of the most common species of bacteria colonizing humans and animals. The singularity of E. coli’s genus and
species underestimates its multifaceted nature, which is represented by different strains, each with different combinations of
distinct virulence factors. In fact, several E. coli pathotypes, or hybrid strains, may be associated with both subclinical infection
and a range of clinical conditions, including enteric, urinary, and systemic infections. E. coli may also express DNA-damaging
toxins that could impact cancer development. This review summarizes the different E. coli pathotypes in the context of their
history, hosts, clinical signs, epidemiology, and control. The pathotypic characterization of E. coli in the context of disease in
different animals, including humans, provides comparative and One Health perspectives that will guide future clinical and
research investigations of E. coli infections.

Abbreviations: AA, aggregative adherence; A/E, attaching and effacing; aEPEC, Atypical EPEC; Afa, afimbrial adhesin; AIDA-I,
adhesin involved in diffuse adherence; AIEC, Adherent invasive E. coli; APEC, avian pathogenic E. coli; ATCC, American Type
Culture Collection; BFP, bundle-forming pilus; CD, Crohn disease; cdt, cytolethal distending toxin gene; Clb, colibactin; CNF,
cytotoxic necrotizing factor; CS, coli surface (antigens); DAEC, diffusely adhering E. coli; DB, Dutch Belted; eae, E. coli attaching
and effacing gene; EAEC, Enteroaggregative E. coli; EAF, EPEC adherence factor (plasmid); EAHEC, entero-aggregative-
hemorrhagic E. coli; EAST-1, enteroaggregative E. coli heat-stable enterotoxin; E. coli, Escherichia coli; ED, edema disease; EHEC,
enterohemorrhagic E. coli; EIEC, enteroinvasive E. coli; EPEC, enteropathogenic E. coli; ESBL, extended-spectrum β-lactamase;
Esp, E. coli secreted protein; ETEC, enterotoxigenic E. coli; ExPEC, extraintestinal pathogenic E. coli; fyuA, yersiniabactin receptor
gene; GI, gastrointestinal; Hly, hemolysin; HUS, hemolytic uremic syndrome; IBD, inflammatory bowel disease; LA, localized
adherence; LEE, locus of enterocyte effacement; LPF, long polar fimbriae; LT, heat-labile (enterotoxin); MLST, multilocus sequence
typing; NDM, New Delhi Metallo-β-lactamase; NZW, New Zealand White; pap, pyelonephritis-associated pilus; pks, polyketide
synthase; sfa, S fimbrial adhesin; SLT, Shiga-like toxin; ST, heat-stable (enterotoxin); STEC, Stx-producing E. coli; Stx, Shiga toxin;
tEPEC, typical EPEC; UPEC, uropathogenic E. coli; UTI, urinary tract infection

DOI: 10.30802/AALAS-CM-20-000054

Escherichia coli (E. coli) is the most common bacterial model increasing disability adjusted life years.355,382,570 Furthermore, in
used in research and biotechnology. It is an important cause of humans, E. coli is one of the top-ten organisms involved in coin-
morbidity and mortality in humans and animals worldwide, fections, which generally have deleterious effects on health.270
and animal hosts can be involved in the epidemiology of in- ETEC is also an important etiologic agent of diarrhea in the
fections.240,367,373,452,727 The adaptive and versatile nature of E. coli agricultural setting.183 E. coli-associated extraintestinal infec-
argues that ongoing studies should receive a high priority in the tions, some of which may be antibiotic-resistant, have a tre-
context of One Health involving humans, animals, and the envi- mendous impact on human and animal health. These infections
ronment.240,315,343,727 Two of the 3 E. coli pathogens associated with have a major economic impact on the poultry, swine, and dairy
death in children with moderate-to-severe diarrhea in Asia and industries.70,151,168,681,694,781,797 The pervasive nature of E. coli, and
Africa are classified into 2 E. coli pathogenic groups (also known its capacity to induce disease have driven global research ef-
as pathotypes or pathovars): enterotoxigenic E. coli (ETEC) and forts to understand, prevent, and treat these devastating dis-
enteropathogenic E. coli (EPEC).367 In global epidemiologic eases. Animal models for the study of E. coli infections have
studies, ETEC and EPEC rank among the deadliest causes of been useful for pathogenesis elucidation and development of
foodborne diarrheal illness and are important pathogens for intervention strategies; these include zebrafish, rats, mice, Syr-
ian hamsters, guinea pigs, rabbits, pigs, and nonhuman prima
Received: 02 Jul 2020. Revision requested: 17 Aug 2020. Accepted: 19 Sep 2020.
tes.27,72,101,232,238,347,476,489,493,566,693,713,744,754 Experiments involving hu-
1
Molecular Sciences Research Center, University of Puerto Rico, San Juan, Puerto man volunteers have also been important for the study of infec-
Rico;2Division of Comparative Medicine, Massachusetts Institute of Technology, tious doses associated with E. coli-induced disease and of the role
Cambridge, Massachusetts of virulence determinants in disease causation.129,176,365,400,497,702,703
§Current affiliation: Division of Comparative Medicine, Massachusetts Institute of
Technology, Cambridge, Massachusetts E. coli strains (or their lipopolysaccharide) have also been used
*
Corresponding author. Email: [email protected] for experimental induction of sepsis in animals; the strains used
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Comparative Medicine
February 2021

for these studies, considered EPEC, are not typically involved in consists of core (genes present in all strains), dispensable [genes
systemic disease.140,205,216,274,575,782 absent in greater than or equal to 1 strain(s)], and unique (pres-
This article provides an overview of selected topics related to ent in a particular strain) genes.594,718,765 Because E. coli is char-
E. coli, a common aerobic/facultative anaerobic gastrointestinal acterized by having a mosaic structure (sharing gene clusters
organism of humans and animals.14,277,432,477,716 In addition, we with other isolates), commensals are thought to behave as gene
briefly review: history, definition, pathogenesis, prototype (ar- “donors” and/or “recipients” and in doing so, become patho-
chetype or reference) strains, and features of the epidemiology genic.594,765 In fact, over 90% of the pan-genome is constituted by
and control of specific pathotypes. Furthermore, we describe variable/’accessory’ genes.407
cases attributed to different E. coli pathotypes in a range of ani- Mobile genetic elements, such as bacteriophages and plas-
mal hosts. The review of scientific and historical events regard- mids, and homologous recombination contribute to the evolu-
ing the discovery and characterization of the different E. coli tion of E. coli virulence.282,597,730,776 Furthermore, an experiment
pathotypes will increase clinical awareness of E. coli, which is using mice demonstrated in vivo transduction of a recipient
too often regarded merely as a commensal organism, as a pos- K-12 E. coli (MC4100) with a Shiga toxin (Stx) 1-encoding bacte-
sible primary or co- etiologic agent during clinical investiga- riophage and thereby documented the importance of horizontal
tions. As Will and Ariel Durant write in The Lessons of History: gene transfer on E. coli evolution and virulence potential.2,384,562,647
“The present is the past rolled up for action, and the past is the
present unrolled for understanding”.
E. coli the commensal and E. coli the pathogen
The pathogenicity of E. coli has been investigated in vivo
Beneficial E. coli strains since the 1920s.621,678 However, E. coli is commonly referred to as
E. coli, originally called Bacterium coli commune, was isolated a commensal and its importance as a pathogen may be under-
from a human infant and reported in 1885.185,193 This isolate, cur- appreciated.118,388,391,625 The potentially beneficial attributes dis-
rently identified as National Collection of Type Cultures 86, was played by some E. coli strains, including K-12, Nissle 1917, and
sequenced and found to be genetically similar to E. coli K-12, a HS, do not provide a rationale to exclude the pathogenic po-
laboratory strain that has played a significant role in research tential of other E. coli strains isolated from clinically unaffected
and biotechnology.185,350,374,429 E. coli K-12 was isolated from a hosts. Clinicians should not assume that E. coli identified/
convalescent diphtheria patient without diarrhea or urinary isolated from a clinically unaffected patient is a commensal. A
tract infection (UTI).268,374 The K-12 genetic sequence provides commensal relationship implies that during a host-bacterium
evidence of genetic changes (genomic plasticity) that allows the interaction, the commensal E. coli benefits, while the host is nei-
bacteria to adapt.68,222,391 The phylogenetic and genomic char- ther benefited nor affected.716 However, because E. coli promotes
acteristics of K-12 and National Collection of Type Cultures 86 colonization resistance (or the ability to outcompete pathogens
support their roles as commensal bacteria.185 Another E. coli, trying to colonize), which benefits the host, this host-bacterium
genetically similar to K-12, is B, which probably originated from interaction is arguably mutualistic, providing benefits for both
Institute Pasteur’s Bacillus coli and was used by Delbrück and bacteria and host.14,389,415,491,716 In addition, some E. coli strains are
Luria for bacteriophage studies.150,322,695 In 1969, Delbrück, Lu- facultative pathogens, meaning that they can live as commen-
ria, and Hershey became Nobel Laureates “for their discoveries sals in the gastrointestinal (GI) tract and also become associ-
concerning the replication mechanisms and genetic structure of ated with disease.388,391 Furthermore, host factors must also be
viruses”.720 E. coli B includes strains BL21 and REL606, which considered.566 Even Nissle 1917 can induce systemic disease in
have been used for studies of evolution and recombinant pro- susceptible animal hosts if their immune system and microflora
tein production, respectively.322 BL21 and others strains used for are perturbed.272 Therefore, understanding these relationships
recombinant DNA experiments [such as DH5α, EQ1, and BLR provides the basis for pursuing and performing a comprehen-
(of K-12 background)] have been investigated in animal models sive characterization of an E. coli pathotype upon isolation and
and found to be nonpathogenic.13,115,259 Shedding of BL21 and aids in deciphering its clinical relevance.
EQ1 was still present at week 6 after inoculation in a 1-d old spe-
cific-pathogen-free chick.115 Other laboratory strains of E. coli in-
Identifying serotype and phylogenetic group
clude C [American Type Culture Collection (ATCC) 700078], W
Hosts may be infected with more than one E. coli pathotype
(ATCC 9637), and Crooks (ATCC 8739; GenBank: CP000946.1)
(E. coli coinfection).4,137,669 Therefore, several E. coli isolates from
or Crookes.16,197,279,373,473 E. coli C, which was originally isolated at
a particular host tissue or targeted biologic sample should be
the Lister Institute, exhibits robust biofilm formation and was
selected for characterization. Once E. coli has been isolated on
recently sequenced.373 The W strain was isolated from cemetery
selective culture media (that is MacConkey agar, CHROMID
soil, and its “W” designation alludes to its discoverer, Selman A.
CPS) and identified biochemically (that is API 20E), a basic ap-
Waksman, who also discovered streptomycin and was awarded
proach is to “name” the E. coli by serotype determination. The
the Nobel Prize in 1952.16
gold-standard for serotyping E. coli consists of identification of
A First World War soldier who was resistant to dysentery
the O (O-specific polysaccharide of the lipopolysaccharide) and
was colonized with an E. coli strain that was isolated by Alfred
H (flagellar protein) antigens.118,162,540 Historically, O serotyp-
Nissle and is currently known as the probiotic Nissle 1917 (E.
ing has been performed using sera (antibodies), although cur-
coli O6:K5:H1).34,598,760 E. coli Nissle 1917 (EcN) is commercially
rent techniques take advantage of molecular methods including
available and has been used to treat intestinal disorders includ-
polymerase chain reaction (PCR).162,228,406,540 The E. coli Reference
ing inflammatory bowel disease (IBD), constipation, and diar-
Center at Penn State University performed serotyping and select
rhea.33,34,598,760
molecular characterization of virulence genes in E. coli isolates.
E. coli O9:H4 (HS), isolated from the feces of a healthy human,
Some serotypes are more common within particular pathogenic
is another strain considered to be commensal, and it has been
E. coli groups.500 For example, O157:H7 is a characteristic entero-
useful for studies of colonization and genetics.398,476,594 Genetic
hemorrhagic E. coli (EHEC) serotype.500
studies comparing commensal and pathogenic E. coli have been
useful for the determination of the E. coli pan-genome, which

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The creation of an E. coli reference (ECOR) collection, com- History and pathogenesis. Bacterium coli strains including an
posed of both human and animal isolates, facilitated the study “O55 B5 H7” (strain 3801) have been reported in human infants
of E. coli diversity.118,530 Phylogenetic group determination using a with vomiting and diarrhea.780 Prior to the description of EPEC
multiplex PCR method allowed further classification of the E. coli associated diarrhea, the 2 known mechanisms of E. coli-induced
isolate.48,123,299 During a clinical investigation, classification of E. diarrhea consisted of enterotoxin production and intestinal
coli into the major phylogenetic groups, including A, B1, B2, and mucosa invasion.186,620 These 2 mechanisms of E. coli-induced
D, provided information about epidemiology and virulence.241,328 diarrhea were not involved in the diarrheal disease observed
Another study determined that groups A and B2 were preva- during an EPEC trial in human volunteers.398,400 However, by
lent in humans, whereas A and B1 and D and B1 were prevalent experimentally infecting neonatal pigs with E. coli “055B5H7”,
in nonhuman mammals and birds, respectively.195 In general, a human isolate from a diarrheic patient, investigators dem-
groups A and B1 represent commensal strains, whereas B2 and onstrated attaching and intracellular E. coli, increased density
D represent pathogenic/virulent strains.82,123,333,566 B1 isolates are under the attachment area which was thought to be “a cellular
usually not host-adapted, whereas B2 isolates are host-adapted.770 response to the bacterium”, and microvillus exfoliation in ileal
Sequence type determination is performed using multilocus sections.476,686 The increased density under the attached bacteria
sequence typing (MLST), a molecular technique involving the was found to be due to site-specific concentrations of cytoskel-
sequencing of 7 to 8 house-keeping genes (loci), and using the etal actin, which characterized the A/E lesion; this was dem-
genetic data to classify the E. coli strains and identify poten- onstrated using EPEC strains including E. coli O55:H7 (strain
tially pathogenic clones.124,412,587,776 By calculating homologous 660-79) associated with infant diarrhea.359,360 O55:H7 infant diar-
recombination frequency, investigators can determine if the E. rhea strains are evolutionarily relevant because they gave rise to
coli population is clonal.677,696,776 Currently, E. coli MLST data- EHEC O157:H7.212,770
bases at The Institut Pasteur and Enterobase can be accessed on- Investigations of spontaneous cases of diarrhea in rabbits led
line.124,313,515,721 For example, clonal group ST131 is predominant to the discovery of E. coli O15 (strain RDEC-1), the prototype
among extraintestinal pathogenic E. coli (ExPEC).515 rabbit EPEC which is used experimentally to elucidate EPEC
In summary, when detecting or describing a particular E. coli pathogenesis.101 Infecting New Zealand White (NZW) rabbits
strain, the investigator may use a combination of phylogenetic with RDEC-1 demonstrated that coincidental bacterial adher-
group, sequence type, and serotype, respectively, as illustrated ence to intestinal epithelial cells occurred only when there was
with a pandemic antibiotic resistant clonal group known as a lack of brush border.707 Other experimental studies demon-
B2-ST131-O25b (ST131, the sequence type; O25b, a molecular strated RDEC-1-induced A/E lesions and adherence pedestals
subtype of O25).125,448,611 High-throughput genome sequencing in both pigs and rabbits.476 Another NZW rabbit study, using E.
is useful for rapid molecular characterization of bacteria, in- coli 015:H- (strain U83/39), demonstrated bacterial attachment
cluding their virulence determinants and comparative analy- to goblet cells and absorptive epithelial cells as well as microvil-
sis.11,118,458,462 Long-read sequencing methods such as PacBio are lus border effacement.554
useful for deciphering plasmids that may be involved in anti- The locus of enterocyte effacement (LEE) is a genetic region
biotic resistance.257,550 Finally, these sequencing technologies are known as a pathogenicity island, which has virulence determi-
revealing the heterogeneous nature of E. coli in terms of combi- nants that are necessary for A/E lesions to develop. It encodes
nation of virulence factors, thus expanding their classic pathot- effector proteins and a type III secretion system that operates
ypic designation.92,169,458 as an injector apparatus, translocating effectors into human
or animal cells.192,285,325,690,711 LEE effectors include translocated
intimin receptor, E. coli secreted proteins (Esps), and Map,
E. coli pathotypes, acronyms, and prototypes
among others.690 The chromosomal eaeA (E. coli attaching and
In general, classification of E. coli into specific pathotypes
effacing) gene is necessary for the formation of A/E lesions,
depends on which virulence determinants are encoded and
and the 94-kDa immunogenic protein it encodes is known as
expressed by the E. coli isolates. 500 For example, molecular
intimin.178,323-325 The characteristic A/E phenotype is the result of
methods, including PCR assays with specific primers, can be
EPEC inserting intimin (an outer membrane protein) and trans-
performed to detect particular virulence determinants that are
located intimin receptor (LEE effector) into the host cell.349,690
characteristic of particular E. coli pathotypes. Protein expres-
Other organisms that induce A/E lesions include EHEC and
sion and phenotypic characteristics such as in vitro cell adher-
Citrobacter rodentium.564,690 C. rodentium causes transmissible mu-
ence or cytotoxicity should be confirmed.151,359,361 In general, E.
rine colonic hyperplasia and has been used experimentally in
coli pathotypes are categorized into those that induce disease
mice to study EPEC pathogenesis.409,564,643
within (diarrheagenic) or outside of (extraintestinal) the GI tract.
Prototype. E. coli O127:H6 (E2348/69), originally isolated
However, some strains may be considered hybrids because they
from a diarrheal outbreak in children, is the prototype human
have virulence determinants/characteristics of more than one
EPEC strain. It was used experimentally in humans to elucidate
pathotype.187,425,437,524
virulence and pathogenic potential.176,311,400,500,714 For example, in
a randomized double-blind human volunteer study, E2348/69
Diarrheagenic E. coli caused diarrhea in 100% of the subjects, whereas the eaeA mu-
Enteropathogenic E. coli (EPEC). Definition. EPEC strains do tant caused diarrhea in only 36% of the subjects, demonstrating
not produce Shiga toxin, but induce pathognomonic lesions eaeA was a virulence determinant.176 In another randomized
known as attaching and effacing (A/E) lesions that can be double-blind human volunteer study, E2348/69 caused diarrhea
observed microscopically.476,500 EPEC adheres to the intestinal in 90% of the subjects, whereas the ∆espB mutant caused diar-
epithelium, the microvilli become effaced, actin is polymerized, rhea in 10% of the subjects, indicating that EspB was another im-
and pedestals are formed (Figure 1).476,500 The A/E phenotype, portant virulence determinant with immunogenic properties.703
enterocyte membrane cupping surrounding bacteria adhering Epidemiology and control. Epidemiologically, typical EPEC
to the mucosa, and pedestal formation have been observed in (tEPEC) strains can be isolated from humans and carry the
human tissues.620,640,712,742 EPEC adherence factor (EAF) plasmid, which includes genes

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Figure 1. Transmission electron micrograph showing organisms consistent with E. coli and associated attaching and effacing lesions and pedes-
tals on the cecal mucosal surface of an experimentally infected Dutch Belted rabbit.

encoding bundle-forming pilus (BFP).500,732 Having the plas- of E. coli O157:H7.603,767 Previous reports of cases of hemor-
mid gives EPEC the ability to adhere to HeLa and HEp-2 cells rhagic colitis in the US and Canada were also associated with
with the characteristic localized adherence (LA) pattern/phe- E. coli O157:H7.112,338 Two patients with hemorrhagic colitis and
notype in which cells attach to the cell surface on one or a few O157:H7 infection also developed hemolytic uremic syndrome
sites.25,358,502,642 Atypical EPEC (aEPEC) strains isolated from hu- (HUS), a clinical triad of microangiopathic hemolytic anemia,
mans and animals do not carry the EAF plasmid.500,732 This EAF- thrombocytopenia, and acute renal failure.509,645 An important
negative EPEC can exhibit the localized adherence-like pattern association was discovered while investigating idiopathic HUS
(“poor LA”) in which less-compact bacterial microcolonies/ in 40 children, as 75% of them exhibited evidence of Verotoxin-
clusters are found on a few cells when the assay is performed, producing E. coli infection.344 The production of this toxin by E.
but a long incubation period (6 h) is necessary.361,641 tEPEC strains coli, and its cytopathic effect on Vero cells (Cercopithecus aethiops
are associated with infantile diarrhea in developing countries, kidney cells) had been reported in 1977.364
whereas aEPEC strains are not necessarily associated with clini- Initially, an experiment using infant NZW rabbits reproduced
cal disease,306 although prolonged/persistent diarrhea in chil- O157:H7-associated diarrheal disease in humans, and histopath-
dren has been linked to aEPEC infection.513,531 tEPEC and 2 other ologic lesions were observed in the colon of these animals.542
pathogens, including heat-stable toxin (ST)-producing ETEC Weanling NZW rabbits infected with Verotoxin-producing E.
and Cryptosporidium spp., are associated with death in children coli demonstrated A/E lesions and revealed that epithelial cell
with moderate-to-severe diarrhea.367 Both tEPEC and aEPEC adherence of organisms was most common in cecum (87%), fol-
can be identified using the fluorescent-actin staining test, which lowed by proximal colon (39%), and distal ilea (26%).662 Oral
is used to determine if the bacteria can induce A/E lesions. In inoculation of NZW rabbits with a Stx1-transduced RDEC-1
this test, the A/E lesions are detected as an accumulation of cy- induced enteric lesions, confirming Stx1 as a virulence deter-
toskeletal actin under the attached bacteria.359,361 Definitive dem- minant in EHEC colitis.673 A study using infant NZW rabbits
onstration of protective immunity against EPEC is lacking and experimentally infected with isogenic mutants of an O157:H7
an effective vaccine for humans is not currently available.175,613 HUS-associated human strain demonstrated that stx2 is associ-
An overview of natural EPEC infections in different hosts re- ated with diarrhea and intestinal inflammation, whereas eae and
veals comparative aspects of etiopathogenesis (Figure 2). translocated intimin receptor gene (tir) are important for coloni-
Enterohemorrhagic E. coli (EHEC). Definition. EHEC are Stx- zation and induction of diarrhea.604 Following a report of natural
producing E. coli (STEC) that encode intimin and induce A/E infection of EHEC O153 in Dutch Belted (DB) rabbits with HUS-
lesions. Stxs are also known as Shiga-like toxins or Vero tox- like disease, our laboratory reproduced enteric and glomerular
ins.459,526 The STEC or VTEC designation indicates that a strain lesions in experimentally inoculated DB rabbits.238,243,664 Other
is a Stx producer; however, intimin may not be expressed. In experiments developing a rabbit model of HUS or HUS-asso-
addition to the infamous serotype, O157:H7, other STEC with a ciated central nervous system disease included IV inoculation
variety of serotypes are known collectively as non-O157 strains. of Stxs.28,29,234,242,470,601,784 Using DB rabbits, our laboratory dem-
Some of these strains, including O26 and O111, may originate onstrated that IV Stx2 promoted enteritis and renal injury.242
from aEPEC after transduction with a Stx-encoding bacterio- Another HUS model consisting of IV inoculation of baboons
phage.42,190 EHEC strains can produce Stx 1 and/or 2 (and sub- with Stx, suggested that HUS was more likely to develop after
types/variants); Stx2 production, especially Stx2d, is associated infection with Stx2-producing E. coli than with E. coli strains that
with severe disease.49,179,459 only produced Stx1.665
History and pathogenesis. Outbreak investigations involv- An experimental strategy using streptomycin, with the ob-
ing 47 human cases of GI disease, including watery and hem- jective of promoting EHEC colonization by reducing faculta-
orrhagic diarrhea without pyrexia, in patients that consumed tive intestinal flora, has been used to model EHEC infection
hamburger meat at fast food establishments led to the isolation in mice.492,754 Disease development in streptomycin-treated

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 E. coli Infections in a Range of Hosts

Figure 2. Natural EPEC infections: Hosts, manifestations, and virulence determinants.*, This column includes selected virulence determinants
investigated in the cited references such as E. coli attaching and effacing (eae or eaeA) gene, bundle-forming pilus (bfp or bfpA) gene, and cytole-
thal distending toxin (cdt) gene. Typical E. coli usually encodes the bfpA gene whereas atypical does not. EAF refers to EPEC adherence factor
plasmid. †, not characterized as typical or atypical.

MyD88−/− mice infected with E. coli O157:H7 provided evidence endothelial lesions to the intestine, kidneys, and brain.81,528,529,651
for the role of innate immunity in pathogenesis.97 Another HUS may result from the inhibition of fibrinolysis and fibrin
mouse model to study EHEC pathogenesis involved feeding accumulation after Stx-mediated endothelial injury.709 Micro-
C57BL/6 mice a low protein diet (5% protein) that caused in- scopically, edema and hemorrhages are present in the colon,
testinal epithelial lesions, and upon infection, resulted in neu- and the kidney shows characteristic lesions consisting of glo-
rologic disease and death.376 Oro-gastric inoculation of weaned merular thrombotic microangiopathy.348,600 The central nervous
(17 to 21 d old) BALB/c mice with EHEC has also been used as system, pancreas, and heart may also be affected.271,345,370,463,608,719
a model for renal lesions.84 Colonic lesions and acute tubular ne- Brainstem changes have been identified in rabbits and humans
crosis are observed in germ-free Swiss Webster mice orally inoc- (Figure 3).242,769,784
ulated with EHEC.188,189 Intraperitoneal inoculation of C57BL/6 Prototype. E. coli O157:H7 [strain CDC EDL 933 (ATCC43895)]
mice with Stx2 and lipopolysacharide has been used as a model is the prototype EHEC strain.602,767
of HUS that includes glomerular lesions.347 Clinical aspects. Clinically, performing fecal cultures in hu-
The Stx receptor is known as globotriaosylceramide (Gb3) man patients within a 6-d window of time that diarrhea begins
(also known as CD77) and its anatomic location is thought to di- is important for increasing chances of obtaining an O157:H7
rect the Stx effect by mediating protein synthesis inhibition and positive culture. 710 STEC may or may not ferment sorbitol;
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Figure 3. Multifocal brainstem degeneration in a Dutch Belted rabbit after experimental intravenous Shiga toxin 2 infusion (hematoxylin and
eosin stain, scale bar: 200 µm). Reprinted from García A, Marini RP, Catalfamo JL, Knox KA, Schauer DB, Rogers AB, Fox JG. 2008. Intravenous
Shiga toxin 2 promotes enteritis and renal injury characterized by polymorphonuclear leukocyte infiltration and thrombosis in Dutch Belted
rabbits. Microbes Infect 10:650–656, with permission from Elsevier. Reference 242.

therefore, if selective media based on sorbitol fermentation is was originally identified in E. coli SA53, a water buffalo rectal
used (that is sorbitol-MacConkey agar) to isolate STEC, addi- isolate that is also positive for Stx2.269,486,567,653 In one study, cow
tional testing may be required.51,342,424 Physicians treating these (75%), buffalo (64%), beef from markets (31%) and human (2%)
cases may encounter the clinical dilemma of whether to use LT-producing isolates encode LT-II genes.653
antibiotics. Stxs are encoded in bacteriophages, and the use of The 2 classes of STs are STa (STI) and STb (STII).500,532,763 STp
some antibiotics to treat STEC infection results in bacterial dam- and STh are the 2 STa variants that may be found in human
age, bacteriophage induction, toxin production and disease.353,794 ETEC isolates.326 Human, pig, and cattle isolates may produce
A meta-analysis designed to exclude studies with high risk of STp.326 STa and STb may be found in porcine ETEC strains.475 In
bias and lacking an acceptable HUS definition, found a signifi- one study, isolates with genes encoding adhesin involved in dif-
cant association between antibiotic administration and HUS fuse adherence (AIDA-I) and STb were associated with diarrhea
risk, supporting the recommendation of avoiding antibiotic use in piglets.512 ETEC may also encode the enteroaggregative E. coli
in STEC-infected human patients.229 A recent literature review heat-stable enterotoxin (EAST-1).264,606,638,747,788
however, concluded that although some antibiotics, such as β- History and pathogenesis. The ligated rabbit gut assay, origi-
lactams, may be harmful, others such as fosfomycin can have nally used for Vibrio cholera research, was used to screen E. coli
positive clinical outcomes.340 isolates from human babies, calves, pigs and water.161,715 Many E.
Epidemiology and control. The epidemiology of STEC/EHEC coli isolates from cases of infantile diarrhea induced dilation in
has been well described and includes both zoonotic and food- the ligated rabbit gut assay (positive test result).715 Cattle strains
borne transmission.354 A STEC/EHEC review, emphasizing One were less effective than human isolates.715 Isolates from swine
Health, underscores the interconnections of humans, environ- enteritis and edema disease (ED) and well water were negative
ment, and animals in epidemiology, prevention and control.240 using this assay.715 A pig gut loop assay revealed a heat-labile
Food and vegetables may be contaminated before harvest due enterotoxin in E. coli isolates associated with diarrheal outbreaks
to the use of manure fertilizer, feces from wild or farm animals, in pigs.283 These E. coli strains were not invasive and did not
or contaminated water.131 Transmission can occur in public set- damage the villi, but induced fluid secretion and diarrhea.283 LT
tings such as petting zoos, and prevention guidelines have been and ST enterotoxins were also reported from isolates cultured
published.127,504 Targeting the type III secretion system by vac- from diarrheic human patients.199 The secretory diarrhea caused
cination decreases colonization in animals.453,577,690 The goal of by ETEC was similar to cholera illness.186,628
decreasing STEC transmission to humans by cattle vaccination ETEC can adhere to enterocytes by using multiple surface
may be more feasible than human vaccination, since vaccine fimbriae (pili), which in human strains are known as coli sur-
efficacy determination is difficult in humans due to the low face (CS) antigens.236,500,606 One group586 has provided a com-
disease incidence.341 An overview of natural STEC/EHEC in- prehensive list of CS antigens. These host-specific fimbriae are
fections in different hosts reveals comparative aspects of etio- important for colonization; common ones in strains associated
pathogenesis (Figure 4). with human diarrhea include colonization factor antigen 1
Enterotoxigenic E. coli (ETEC). Definition. ETEC strains can (CFA/1), CS1, CS2, CS3, CS4, CS5, CS6, CS7, CS14, CS17, and
produce heat-labile (LT) and/or ST and are an important cause CS21.236,396,500,586,622,722,778 K88 (F4), K99 (F5), 987P (F6), F41 (F7),
of diarrhea in humans (traveler’s and infant diarrhea) and pig- and F18 are important for colonization in swine.109,235,396,456,757,775
lets.263,397,500,606,736 The 2 serologically distinct LTs are LT-I and In swine, neonatal diarrhea is associated with F5, F6, and F41,
LT-II.305,500,567 LT-I is similar to cholera toxin and consists of LTp whereas postweaning diarrhea is associated with F4 and F18.456
(p, pig) and LTh (h, human) variants because these toxins were Newborn and suckling pig diarrhea and mortality are also as-
identified in pig and human strains, respectively.500,672,684,763 LT-II sociated with F4.456 Coinfections of ETEC and other pathogens
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Figure 4. Natural STEC/EHEC infections: Hosts, manifestations, and virulence determinants. *, This column includes selected virulence deter-
minants investigated in the cited references such as stx genes and Stx production; slt (SLT) refers to Shiga-like toxin (Shiga toxin).

including rotavirus, Salmonella Newport, Crystosporidium parvum, against fimbriae of E. coli or other organisms.219,636 More recently,
and Cystoisospora suis have been reported in young pigs.154,447 subjects who received hyperimmune bovine colostral anti-CS17
ETEC can also induce diarrhea in calves; F5 is commonly associ- orally did not develop diarrhea after challenge with CS17-ex-
ated with these infections, which may be concomitant with Crysto- pressing ETEC.637 The use of the antibiotic colistin (polymyxin
sporidium infections.155,224,629 Infections with rotavirus may increase E) for E. coli infections, including postweaning diarrhea prophy-
susceptibility to ETEC infection and disease in calves.680,739 laxis in pigs, is discouraged, as this antibiotic is a useful thera-
Prototypes. E. coli O78:K80:H11/LT1-STh-STp/CFA/I peutic alternative in humans for Gram-negative infections that
(H10407), originally isolated from the stool of a Vibrio-negative are multidrug-resistant.599 Vaccines administered during preg-
patient with diarrheal disease in Bangladesh, is the prototype nancy impart protection to calves and piglets through inges-
ETEC strain; its genome sequence indicates that it is related to tion of colostrum.183,456,474,494,626 However, control of postweaning
the nonpathogenic E. coli strains K-12, C, and HS.141,200,201,606 The diarrhea in swine by vaccination has been challenging.183 A live
classification of ETEC into different phylogenetic lineages (poly- nonpathogenic E. coli strain positive for F4 (Coliprotec F4) used
phyletic) by MLST suggests that the acquisition of coloniza- for oral vaccination of pigs was reported to confer protection
tion factor and toxin genes by nonpathogenic E. coli results in against diarrhea after weaning.209 Furthermore, a study using 2
ETEC.736 Regarding ETEC in ruminants (lambs and calves), E. live nonpathogenic E. coli strains expressing specific antigenic
coli O101:K99:NM (B41) is the prototype K99 ETEC.314,485,541 In variants of F4 (Coliprotec F4) and F18 as an oral vaccine found
China, E. coli O8:K87:H19 (C83902) is the prototype F4 ETEC of that this vaccination strategy was clinically efficacious for swine
swine.795,796 diarrhea after weaning.493 An overview of natural ETEC infec-
Epidemiology and control. ETEC and cholera have similar tions in different hosts reveals comparative aspects of etiopatho-
clinical presentations of acute watery diarrhea.626,627 ST-ETEC genesis (Figure 5).
(positive for ST gene estA and LT gene eltB or for only estA) is Enteroinvasive E. coli (EIEC). Definition. EIEC strains invade
one of the 3 pathogens associated with death in children with the colonic epithelium and cause bacillary dysentery similar to
moderate-to-severe diarrhea.367 ETEC is a primary cause of Shigella dysenteriae, S. boydii, S. flexneri, and S. sonnei.12,464,549,559,740
traveler’s diarrhea.688,736 In vitro studies suggest that during a MLST and genome sequencing can be used to differentiate
coinfection, ETEC and EPEC may interact and increase disease Shigella spp. and EIEC.142,381 Analyses of the E. coli O124:H30
severity.137 Preclinical studies for ETEC vaccine development (strain M4163 from a cheese-related outbreak in 1971) and E. coli
used an infection model involving owl monkeys (Aotus nan- O143:H26 (strain 4608-58) genome determined that these were
cymaae).615 A phase 1 trial in humans demonstrated protection larger than the Shigella genomes, consistent with gene loss/de-
from ETEC diarrhea using hyperimmune bovine colostral anti- cay in Shigella.213,393 Regarding lactose utilization, which is used
adhesin (anti-CFA/I minor pilin subunit) antibodies, providing for identification on MacConkey agar, strain M4163, strain 4608-
supporting evidence for the development of future vaccines 58, and Shigella were lactose negative, positive, and negative,
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Figure 5. Natural ETEC infections: Hosts, manifestations, and virulence determinants. *, This column includes selected virulence determinants
investigated in the cited references.

respectively. This demonstrated that EIEC lactose utilization Several Shigella strains have been sequenced, and to date, no
is variable.393 Shigella is so similar genetically to EIEC that in- vaccines against human shigellosis are available.619 The develop-
vestigators have proposed its inclusion into the EIEC group, or ment of immunity against Shigella is specific to the serotype to
alternatively, Shigella to be an E. coli sister species.117,563,800 which the host is exposed; this feature is one of the challenges
History and pathogenesis. Investigators of an outbreak affect- of Shigella vaccine development.12,223,399,565 However, cross-pro-
ing people with dysentery/gastroenteritis in 1971 determined tection may be possible because guinea pigs orally immunized
that the source of the infection was imported cheese, which was with a mutant S. flexneri 2a that overexpresses the type III secre-
contaminated with an invasive E. coli O124:B17 that was not tion system were protected against S. dysenteriae and S. sonnei;
enterotoxigenic.426,735 One study reported that invasive E. coli these animals also developed antibodies against EIEC.469 An
strains contained a plasmid (˜140 megadalton) and that inva- overview of natural EIEC infections in different hosts reveals
siveness was established when a plasmid from Shigella flexneri comparative aspects of etiopathogenesis (Figure 6).
was transferred into avirulent E. coli.632 When E. coli O124 strains Enteroaggregative E. coli (EAEC). Definition. EAEC are for-
were inoculated into the eyes of guinea pigs (Sereny test), 6 of mally defined as those E. coli that exhibit an aggregative adher-
17 strains (35%), including one strain from a primate and 5 from ence (AA) pattern on Hep-2 cells and are not enterotoxin (ST or
humans, were positive (caused clouding and/or ulceration of LT) secreting strains.503 However, because the AA pattern has
cornea).294,652 All 6 Sereny test positive O124 strains carried the been observed with aEPEC O125ac:H6, testing for EPEC and
140 megadalton plasmid known as invasion plasmid (pINV) EAEC genes is important if an isolate exhibits the AA pheno-
which was later found to share a basic replicon with pINV from type in vitro.30,404 DNA probes can also be used for EAEC iden-
Shigella spp.294,336,666 tification.533
In general, pathogenesis involves gaining access to the epi- History and pathogenesis. Originally referred to as enteroad-
thelial cell’s basolateral pole through invasion of the M cells herent E. coli or enteroadherent-aggregative E. coli, these strains
found on lymphoid follicles.549 Macrophages with phagocytized exhibit a Hep-2 cell adherence pattern characterized by D-man-
bacteria become apoptotic, expressing IL18 and IL1, followed by nose-resistance, as seen with EPEC.139,397,444-446,501,750,786 Evaluation
the bacteria invading epithelial cells.549 Once inside the epithe- of the Hep-2 cell adherence patterns of E. coli isolates from stools
lial cells, bacteria spread to adjacent cells and induce IL8.549 The of children from Chile revealed an aggregative phenotype, char-
cytokine stimulation induces polymorphonuclear cell transmi- acterized by bacteria autoagglutination or stacked-brick con-
gration that increases the susceptibility of the epithelial cell bar- figuration (aggregative adherence or AA). This phenotype was
rier to the influx of bacteria from the lumen.549 The ipaH genes observed in 84 of 253 (33%) and in 20 of 134 (15%) of strains
encode proteins considered type III secretion system (delivery negative by EPEC adherence factor probe isolated from diar-
apparatus) effectors that have roles in bacterial survival, induc- rhea cases and controls, respectively.500,501 The same aggrega-
tion of host cell apoptosis, and NF-κB inhibition.19,549 tive phenotype was observed in ETEC (3/27; 11%) and in EPEC
Prototype. E. coli O124:NM (NM, nonmotile) (EDL 1284; 929- (2/86; 2%).501 Furthermore, an E. coli strain (#221) isolated from
78) (ATCC 43893), originally isolated from the stool of a human a person who traveled from the US to Mexico was later recog-
in Texas, is the prototype EIEC.15,211,294,585,741 nized to exhibit the AA pattern and to induce diarrhea in human
Epidemiology and control. EIEC O96:H19 has been associated volunteers.401,445,446,749,750
with foodborne human outbreaks in Europe.464,510 Because the The 3 main pathogenesis steps consist of adherence, the pro-
genetic composition and pathogenic mechanism of EIEC and duction of mucus and then production of toxin.301,336,738 AA fim-
Shigella are very similar and EIEC are difficult to identify, fa- briae I (AAF/I) and AAF/II contribute to bacterial adherence
miliarity with Shigella epidemiology and control is useful.117,297 and AA phenotype.146,498,500 AAF variants, including AAF/III,
Shigella spp. also constitute one of the 4 common causes of AAF/IV, and AAF/V, have also been described.40,71,334 The AA
moderate-to-severe diarrhea in pediatric cases from Asia and phenotype can be affected by the composition of the surface
Africa and can acquire antibiotic resistance plasmids from E. protein layer/outer membrane protein.163,755
coli.12,367 E. coli can also acquire antibiotic resistance plasmids EAEC strains induce the intestinal mucosa to produce
from Shigella spp. such as blaCTX-M-55.588,593 Animal E. coli isolates more mucus, creating a biofilm in which the bacteria become
may carry blaCTX-M-55 and related plasmids.410 Our laboratory re- trapped.500 However, biofilm production varies with regard to
ported that macaques can be infected with quinolone-resistant the strain.659,660 EAST-1 may be encoded/produced by some
Shigella flexneri strains that may transfer antibiotic resistance to EAEC and other E. coli pathotypes including ETEC (for exam-
E. coli.420 ple, in prototype strain H10407), EPEC, and EHEC.454,634,635,638,785
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Figure 6. Natural EIEC infections: Hosts, manifestations, and virulence determinants. *, This column includes selected virulence determinants
investigated in the cited references such as genes for type III secretion system effectors including ipaH and virA.464,549

A large plasmid encodes a serine protein autotransporter toxin however, phenotypically, distinguishing features of AIEC in-
known as Pet (plasmid encoded toxin) that is secreted by EAEC clude adherence and invasiveness of the epithelium and sur-
and potentially is involved in its pathogenesis.147,336,505,506 The AA vival with replication inside macrophages.255,440
plasmid (pAA) can encode AAF/I, AAF/II, AAF/III, EAST- History and pathogenesis. E. coli O83:H1 was originally iso-
1, and Pet.40,147,196,750 EAEC are genetically heterogeneous; hori- lated from the affected ileum of a human patient with CD.79,152
zontal and vertical transmission are involved in AA plasmid Another study reported intracellular E. coli in colorectal carci-
inheritance.147 “Typical” strains carry pAA whereas “atypical” noma and adenoma mucosae of humans.701 E. coli can be found
strains do not.751 adhering to and invading the intestinal mucosa of patients with
Prototypes. E. coli O3:H2 (17-2), originally isolated from CD and colon cancer.434 A relative increase in E. coli and a de-
the stools of a diarrheic Chilean infant, is a prototype EAEC crease in a Clostridiales subset in the mucosa is also associated
strain that expresses AAF/I, whereas E. coli O44:H18 (042), with some cases of CD ileitis.31
originally isolated from the diarrheic stool of an infant in Peru, In one study, the percentage of ExPEC strains exhibiting AIEC
expresses AAF/II and is another prototype that can be used phenotype was 6%.440 In another study, human E. coli isolates
as reference.146,147,498,499,502,634 Both 17-2 and 042 encode EAST-1, from colon cancer mucosa were found to encode virulence
and 042 also encodes Pet.196,497 EAEC 55989 encodes AAF/III, genes associated with uropathogenic E. coli (UPEC).89 Further-
was isolated from the stool of a person from the Central African more, isolates from human cases of CD and colorectal cancer
Republic who had HIV and persistent diarrhea, is phylogeneti- were characterized by afimbrial adhesin (afaC) and lpfA expres-
cally related to entero-aggregative-hemorrhagic E. coli (EAHEC) sion whereas isolates from ulcerative colitis and colorectal can-
German hybrid outbreak strains, and is considered a prototype cer encoded afaC and polyketide synthase (pks) pathogenicity
strain.40,92,336,487,730 island.439,582 AIEC strains can also create biofilms efficiently and
Epidemiology and control. EAEC is another common cause of induce inflammation that may be modified by an AIEC’s cellu-
travelers’ diarrhea and has also been associated with persistent lose production.105,191,441 Adding to the complexity of the role of
diarrhea in children and HIV patients.46,47,336,366,445,759 Clinically, E. coli in the etiopathogenesis of IBD, an invasive, LPF-encoding
EAEC causes a persistent diarrhea that can be mucoid.497,500,738 E. coli O126:H27 (strain D92/09) exhibiting AA pattern and also
EAEC was also associated with extraintestinal disease, as EAEC encoding intimin and Shiga toxin 1 was isolated from the ileal
O78:H10 ST10 was isolated from urine of humans with UTI dur- lesions and stools of a CD patient.149 This D92/09 hybrid strain
ing an outbreak in Denmark.73,534,535 Some experimental vaccine was 97% similar to EAHEC O104:H4/2011C-3493 strain from
strategies against EAEC have incorporated AAF as a component the HUS outbreak that occurred in Germany in 2011.149
of the vaccine.80,536 An overview of natural EAEC infections in Prototype. E. coli O83:H1 (LF82), which was originally iso-
different hosts reveals comparative aspects of etiopathogenesis lated from the affected ileum of a human patient with CD, is the
(Figure 7). prototype AIEC strain.79,152
Adherent invasive E. coli (AIEC). Definition. The specific Epidemiology and control. AIEC are associated with intesti-
virulence determinant(s) that define AIEC have not been elu- nal disease, and AIEC epidemiology has not been completely
cidated.118,439 However, the presence of the pic gene and re- elucidated.439 However, a survey of the ECOR collection identi-
sistance to ampicillin can be used to identify AIEC strains.100 fied AIEC in apparently healthy humans and animals including
AIEC strains have been sequenced.122,466,496 Comparative analy- pig, elephant, goat, cougar, and Celebes macaque.590 A possible
ses of AIEC genomes from Crohn disease (CD) patients, mice strategy to protect individuals against AIEC and development
with ileitis, dogs with granulomatous colitis, one non-AIEC of CD incorporates type 1 fimbriae adhesin protein (FimH) an-
genome, and other genomes revealed an overrepresentation tagonists.589,671 An overview of natural AIEC infections in dif-
of genes for propanediol utilization and iron acquisition in ferent hosts reveals comparative aspects of etiopathogenesis
AIEC.174 Also, long polar fimbriae (LPF; lpf operon) are in- (Figure 8).
volved in the interaction of AIEC with Peyer patches and M Diffusely adhering E. coli (DAEC). Definition. Plasmid or chro-
cell translocation.116 mosomal encoded genes give DAEC the ability to adhere to
E. coli designated as AIEC by phylogenetic analysis, clustered HeLa and HEp-2 cells with the characteristic diffuse adherence
by phylogenetic group and not by pathotype and some clus- pattern in which the whole cell surface is covered by bacte-
tered with ExPEC in phylogenetic groups B and D.174 Geneti- ria.25,38,52,502,641,642
cally, AIEC strains share virulence determinants with ExPEC;

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Figure 7. Natural EAEC infections: Hosts, manifestations, and virulence determinants. *, This column includes selected virulence determinants
such as the plasmid-borne transcriptional activator gene (aggR) and also the adherence phenotype investigated in the cited references.

Figure 8. Natural AIEC infections: Hosts, manifestations, and virulence determinants. *, This column includes selected virulence determinants
and phenotypic characteristics investigated in the cited references.

DAEC and EAEC share phylogenetic and adherence charac- originally cloned from plasmid DNA of EPEC O126:H27 (strain
teristics. For example, a phylogenetic tree based on multilocus 2787) from an infant diarrhea case.38,39
enzyme electrophoresis of 20 enzymes revealed 5 overlapping History and pathogenesis. Human volunteers did not develop
clusters constituted by DAEC and EAEC strains that were akin diarrhea after ingestion of either of 2 DAEC strains.702
to the clusters seen with EPEC and EHEC.147,177 Another com- E. coli with Afa/Dr adhesins have been isolated in cases of
mon feature is that EAEC and DAEC adhesins belong to the urinary tract disease or diarrhea.52,62,316,379,386,522,655 The associa-
same Dr superfamily.71 Broadly, DAEC can be differentiated by tion of DAEC with urinary or intestinal disease may be related
whether they express Afa/Dr or Afa/Dr-related adhesins in- in part to the capacity of some DAEC to induce tight-junction
cluding F1845 (from C1845) and AIDA-I.35,52,654,655 AIDA-I was

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Figure 9. Natural DAEC infections: Hosts, manifestations, and virulence determinants. *, This column includes selected virulence determinants
investigated in the cited references.

lesions through secreted autotransporter toxin, one of serine reaching the bladder and inducing inflammation.465 More exten-
protease autotransporters of Enterobacteriaceae.278,421,655,704,705 sive colonization of UPEC may allow it to reach the kidneys and
The genes for afa/dra/daa can be found in various E. coli pa- blood, causing life-threatening disease.465 Experimental mouse
thotypes including STEC and ExPEC.194,387 Furthermore, some models of lethality involving E. coli injection showed that clini-
strains positive for daaC (F1845 accessory gene) and one encoding cal ExPEC isolates classified as phylogenetic group B2 induced
AIDA-I that exhibit DA pattern may also encode eae, be fluores- lethality and encoded relatively more virulence determinants
cent-actin staining test positive, and can be considered aEPEC including pap (pyelonephritis-associated pilus; P fimbriae) and
strains.35,38,655 In addition, AIEC strains from the mucosa of CD hly (α hemolysin) operons.566 Another study using mice found
and colorectal cancer patients may be positive for afa.152,437,582 that fyuA (yersiniabactin receptor), usp (uropathogenic-specific
Prototypes. E. coli O75:NM (C1845) is the prototype DAEC protein), malX (pathogenicity island marker), pap, and phylo-
and was isolated from a child with a 3-wk duration (protracted) genetic group B2 significantly predicted the “killer” status of
diarrheal illness that lacked evidence of other pathogens. 52,99 ExPEC isolates.309,328 ExPEC may also encode other genes associ-
Prototypic UPEC strains include O2 (KS52), a urine isolate from ated with virulence and express α or β hemolysin.151,333,596 How-
a pyelonephritis patient, and O75:K5:H- (IH11128), isolated ever, comparative sequence analysis suggested that no single
from a person with UTI.380,521,655,743 E. coli O75:K5:H- (IH11128) virulence mechanism is used by ExPEC isolates and that ex-
expresses Afa/Dr adhesins and is genetically related to E. coli traintestinal infection in a particular organ is not dependent on
O75:NM (C1845).53 C1845, KS52, and IH11128 express F1845, expression of a single virulence determinant.91,151 A phylogenetic
AfaE-I, and Dr adhesins, respectively.278 group B2 E. coli isolated from a human with fatal hemorrhagic
Epidemiology and control. In France, DAEC was commonly pancreatitis has been classified as a translocating E. coli based on
isolated from hospitalized diarrheic human patients.317 In de- its ability to translocate across epithelial cells into the mesenteric
veloping countries, DAEC is the third most important cause of lymph nodes and blood.22
traveler’s diarrhea after ETEC and EAEC.688 DAEC was one of E. coli can produce toxins that affect the cell cycle (cyclomod-
3 prevalent pathotypes, including EAEC and EPEC, detected ulins), including CNF’s, cytolethal distending toxins (CDTI,
in asymptomatic Peruvian children and was the most preva- CDTII, CDTIII, CDTIV, CDTV), cycle inhibiting factor, and co-
lent in coinfections.4 In Mexico, DAEC was identified in 35% libactin (Clb; encoded by pks).182 Analyses of urosepsis E. coli
of hospitalized diarrheic children.552 An association of DAEC strains determined that encoding CNF-1 and Clb was associated
infection and bloody diarrhea with fever has been reported.551,552 with the B2 phylogenetic group.182 B2 isolates from prostatitis
Vaccines against DAEC have not been reported. However, trav- cases also encoded at least one cyclomodulin including Clb, Cnf,
eler’s diarrhea chemoprophylaxis and chemotherapy have been or Cdt.372 In addition, many E. coli K1 isolates that are associ-
reported.688 An overview of natural DAEC infections in different ated with systemic infections in neonates encode Clb, which is
hosts reveals comparative aspects of etiopathogenesis (Figure important for virulence.241,450 Secreted proteases including serine
9). protease autotransporters of Enterobacteriaceae can also impact
Extraintestinal pathogenic E. coli (ExPEC). Definition. The ac- ExPEC pathogenesis.708
ronym ExPEC has been proposed for use in referring to strains The role of E. coli pathotypes in IBD has been recently re-
associated with diseases outside the GI tract including (but not viewed.467 Previously, hemolytic and necrotoxic E. coli were iso-
limited to) meningitis, urinary tract, and systemic (septicemia) lated from humans with ulcerative colitis; these strains seemed
infections.624 These E. coli strains can also be recognized by the to colonize after relapses.128 A microarray study found genetic
names neonatal meningitis E. coli, UPEC, and sepsis-causing similarities between E. coli isolates from humans with IBD and
E. coli.151 Prostatitis is another manifestation of ExPEC infec- ExPEC.748 B2 phylogenetic group cyclomodulin-expressing E.
tion.372,625 Strains expressing cytotoxic necrotizing factor (CNF)1 coli strains have been detected in colonic biopsies of patients
or CNF2 are referred to as necrotoxigenic E. coli 1 or 2, respec- with colorectal cancer.94 A study of human fecal samples using
tively, and CNF3 has also been described.159,335,538 Necrotoxigenic a quick PCR assay for direct quantification of bacterial genes
E. coli can cause disease in animals and humans.159,332 in stools detected Clb genes in 20% of the samples.261 In several
History and pathogenesis. Initially, hemolysin was proposed different experimental mouse models, Clb is associated with
as a virulence determinant associated with E. coli involved in ex- cancer promotion consistent with its in vitro phenotype, which
traintestinal infections; a later report found that some hemolytic includes megalocytosis and DNA breaks.17,74,136,143,520,592 Paradoxi-
isolates also produced a toxin known as CNF.103,111 E. coli encod- cally, the Nissle 1917 strain used as probiotic also encodes Clb;
ing CNF1 was associated with enteritis/diarrhea of neonates its probiotic activity depends on ClbP, a Clb-activating pepti-
and children.56,102 dase.442,520
UTIs are ascending infections, meaning that intestinal bac- CDT is considered genotoxic and carcinogenic in other ex-
teria (such as UPEC) enter through the urethral orifice before perimental infections.245-247,706 For example, chronic inflammation

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and dysplastic nodules were observed in an A/JCr mouse hypervirulent characteristics warrants investigations of ExPEC
model of liver cancer involving oral inoculation of Helicobacter transmission and clonal expansion.151
hepaticus, which naturally encodes CDT.247 The tumor promoting Human UTI vaccines are available in Europe but not in the
effect of CDT-encoding H. hepaticus was reproducible in a dif- US.465 Experimentally, UTI vaccine targets include antigens
ferent model and organ system; 129/SvEv Rag2 deficient mice related to bacterial iron acquisition.471 The human ExPEC4V
developed intestinal cancer 20 wk after inoculation.245 Also, after vaccine includes 4 different E. coli O antigens and has been eval-
21 wk, intestinal pathology was significantly exacerbated in H. uated in Phase 2 studies.310,312,679 Also, a multiantigen (including
hepaticus-infected 129/SvEv Rag2−/− Il10−/− gpt δ male and fe- 4 surface proteins) vaccine against APEC reduced lesions due to
male mice.246 The fecal and mucosal (cecal and colonic) levels of APEC O2, as well as blood and organ load, after experimental
pks+ E. coli significantly increased in H. hepaticus-infected 129/ challenge in chickens.745 An overview of natural ExPEC infec-
SvEv Rag2−/− Il10−/− gpt δ mice.246 CDT may also be encoded by tions in different hosts reveals comparative aspects of etiopatho-
pks+ E. coli colonizing laboratory rats.377 genesis (Figure 10).
Prototypes. E. coli O4:K6:H5 (J96), isolated from a human pa-
tient with pyelonephritis, is a prototype ExPEC strain express-
Mix and Match: Challenges
ing papG alleles and cnf1.309,330 J96-like strains (O4 serotype) have
Hybrids. Hybrid strains are an emerging public health risk
been isolated from urosepsis, acute cystitis, and bacteremia.330
with associated medical and epidemiologic challenges that be-
E. coli O6:K15:H31 (536) is another pyelonephritis human ar-
hoove the investigation of isolates for an expanded set of viru-
chetypal strain that encodes S fimbrial adhesin (sfa) comparable
lence determinants using techniques such as whole-genome
to some human isolates from newborn cases of meningitis, in-
sequencing.298,524,525,579
cluding RS218 and IHE3034.69,285,286,333 E. coli O18ac:K1:H7 (RS218
In 1998, HUS-outbreak associated E. coli O111:H2 strains were
and IHE3034) (“K1 strains”), isolated in California and Finland,
reported to exhibit STEC and EAEC characteristics, providing a
respectively, are prototype meningitis-associated ExPEC with
prelude to entero-aggregative-hemorrhagic E. coli (EAHEC).480
known genetic sequences.3,153,764,774 E. coli O6:K2:H1 (CFT073)
In 2011, an outbreak of EAHEC O104:H4 associated with sprout
is the prototype acute pyelonephritis-associated (uropatho-
consumption caused close to 4000 cases of acute gastroenteri-
genic) E. coli that has been sequenced.331,408,472,765 Pathogenicity
tis or hemorrhagic colitis (855 HUS cases and 53 deaths).95,724
island differences exist between CFT073, 536, and J96.285,765 E. coli
EAHEC O104:H4 was antibiotic resistant and phenotypically
CFT073 (O6:K2:H1) is genetically related to the probiotic Nissle
produced extended-spectrum β-lactamase (ESBL).50,226,458 Two
1917 (O6:K5:H1).598
O104 patient isolates from this outbreak were sequenced and
Avian pathogenic E. coli (APEC) is considered ExPEC and E.
found to be similar to an EAEC African strain (55989); however,
coli O2:K1:H5 (IMT5155) is the prototype strain isolated from
these 2 isolates contained a Stx-encoding prophage.40,92,458 The
the internal organs of a chicken during an outbreak of colisep-
role of farms as virulent determinant pools for the emergence
ticemia.202,203,402 E. coli ONT:H21 (SCI-07) is another strain classi-
of EAHEC O104:H4 was suggested by a study performed in
fied as APEC due to its molecular characteristics. It was isolated
Germany and Spain, in which the genes characteristic of this
from a laying hen with “swollen head syndrome” signs and has
strain, including stx2, aggR, wzxO104, and fliH4, were identified in
been genetically sequenced.204,614 E. coli OR:H10 (SEPT362), a
samples from one German abattoir that was closer to the out-
hepatic isolate from a septicemic chicken, is another sequenced
break epicenter, and that used animals originating from farms
APEC strain of interest, given it encodes EAST-1, serine protease
near the epicenter.96 Furthermore, genome sequence analyses
autotransporters of Enterobacteriaceae Tsh, and has an enterotoxi-
of sporadic (not outbreak related) O104 strains suggested that
genic-like phenotype.417,613
O104 variants may emerge from other reservoirs and not neces-
E. coli O2:K53,93:H1 (BM2-1) is a prototype bovine CNF-
sarily from the epidemic strain.724
1-expressing hemolytic E. coli strain isolated from the feces of a
EPEC/ETEC hybrids are E. coli strains carrying LEE genes
calf with enteritis.157,158,160E. coli O15:K+:H21 (S5) is a prototype
and expressing type III secretion system effector (EspB) and LT
CNF-2-producing strain isolated from blood of a bacteremic
that appear to have originated from plasmid-acquiring EPEC.298
lamb.561,675
Children/infants were colonized with these EPEC/ETEC strains
Disease in ferrets may be caused by strains positive for cnf1,
in Africa and India.187,298 A study in cattle reported EPEC/ETEC
hlyA, and pap1 including: O4:H-, O4:H5, O6:H-, and O2:H4.428
and EHEC/ETEC isolates.20 STEC and/or EHEC/ETEC hybrids
Rat E. coli strains with potential to cause disease have been
are E. coli strains encoding Stx(s) and ST, and some have been
recently characterized and include O7:H7 (pks+, cdt-, cnf- and
recovered from disease cases that include HUS in young human
pks+, cdt+, cnf-), O166:H6 (pks+, cdt+, cnf-), OM:H6 (pks+, cdt+,
patients in Finland, and animals, including cattle.339,433,524,525,579
cnf-), and O4:H5 (pks+, cdt-, cnf+).377 In mice, E. coli O2:H6/41
The plasmid of Escherichia sp. cryptic lineage 1 O2:H25 (strain
(NC101 strain) is considered a prototypic pks+ strain that, in
7v) from healthy cattle feces encodes a mix of virulence deter-
monoassociation experiments, induces intestinal inflammation
minants from STEC and ETEC plasmids, including K88, which
in interleukin-10 knockout (IL10−/−) mice and also promotes
is usually found in ETEC plasmids from pig isolates.394 Pigs can
invasive carcinoma in IL10−/− mice administered azoxymeth-
harbor ETEC and STEC/ETEC hybrid strains that are resistant
ane.17,351,405
to multiple antibiotics.86
Epidemiology and control. In humans, the clinical presenta-
In Spain, O153:H10-A-ST10 eae-β 1 aEPEC-ExPEC has been
tion of ExPEC infections can vary and these diseases including
isolated from diarrheic humans and canid (fox) feces.169 In
UTIs have significant medical and economic impact.151,220,465,625
France, infection with E. coli O80:H2 (clonal group ST301) was
Given their importance, epidemiologic studies should include
associated with a high percentage of HUS cases (91%), of which
genotypic and phenotypic (protein expression) information re-
3 cases included bacteremia, peritonitis/septic shock, or pancre-
garding ExPEC associated virulence determinants. 151 Antibi-
atic abscess .425,683 The genetic characteristics of E. coli O80:H2,
otic therapy for UTI is hampered by the emergence of resistant
encoding intimin and Stx2 and positive for genes associated
bacterial strains and mechanisms of resistance.471 The dissemi-
with extraintestinal virulence of plasmid pS88, suggest that this
nation of particular clonal groups with antibiotic resistant and
E. coli is an EHEC/ExPEC hybrid.425,557,683 An overview of natural

14
 E. coli Infections in a Range of Hosts

Figure 10. Natural ExPEC infections: Hosts, manifestations, and virulence determinants. *, This column includes selected virulence determi-
nants investigated in the cited references.

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Figure 11. Natural hybrid E. coli infections: Hosts, manifestations, and virulence determinants. *, This column includes selected virulence deter-
minants investigated in the cited references.

hybrid E. coli infections in different hosts reveals comparative not reported.658 Meropenem resistant (NDM-5) E. coli belonging
aspects of etiopathogenesis (Figure 11). to ST167 were isolated from 2 dogs with chronic otitis and a
Mobile drug resistance: Carbapenamase. ESBL-producing bac- human living in the same household in Finland.273 Interspecies
teria are defined by non-susceptibility to extended-spectrum transmission of small col-like plasmids (likely high copy num-
cephalosporins (including third-generation cephalosporins) ber and possibly highly mobile) encoding blaKPC may be epide-
and aztreonam and susceptibility to clavulanic acid.544,595 A pro- miologically important.691 OXA-48 carbapenamase-expressing
posed ESBL nomenclature seeks to add non-susceptibility to E. coli and Klebsiella pneumoniae have been characterized from
carbapenems to this definition.253,756 Carbapenems are used to 6 dogs hospitalized in Germany.692 Carbapenamase-encoding
treat infections caused by ESBL-producing Enterobacteriaceae.544 E. coli have also been isolated from pigs in Germany and Ko-
E. coli carrying ESBL genes have been found in companion ani- rea.218,290,618
mals.104,171,307,726 The recent documentation of ESBL transmission A blaKPC-2-encoding plasmid was detected in an E. coli isolate
leading to bacteremia and death in a human patient treated for from a river in Portugal, suggesting that aquatic environments
C. difficile colitis via fecal microbiota transplantation has raised be reservoirs.573 Surface, drinking, and ground waters can be
concerns regarding donor screening for this therapy.164 a source of E. coli for animals and humans that could subse-
Carbapenem resistance can be transferred by plasmids and quently become vectors.114,288,461,579,766
includes New Delhi Metallo-β-lactamase (NDM), Klebsiella pneu-
moniae carbapenamase (KPC), and oxacillinases (OXA).518,519,756,766 Identification of E. coli in animal host
NDM-1 encoding bacterial strains can be resistant to almost all Nonhuman primates (NHPs). Historically, E. coli has been iso-
antibiotics and represent a global health threat.375,519 NDM-1 lated along with other bacterial or viral pathogens in nonhuman
gene was detected in a Klebsiella pneumoniae isolate from a hu- primates with respiratory or systemic diseases.206,266,543 EPEC
man UTI patient who visited New Delhi, India.789 This patient was isolated from a 20-wk-old simian immunodeficiency virus
was also colonized with an enteric E. coli carrying a plasmid (SIV)-inoculated macaque (Macaca mulatta) at the New England
with NDM-1 gene (blaNDM-1) suggesting in vivo conjugation.789 Regional Primate Research Center that exhibited profuse diar-
In the US, Klebsiella pneumoniae, E. coli, and Enterobacter cloacae rhea and wasting.422 Retrospectively, EPEC was identified as one
human isolates with blaNDM-1 were reported from patients with of the pathogens associated with a similar clinical presentation
a history of medical care in India.113 A study of multidrug-re- in macaques dying with AIDS.422 Other pathotypes that have
sistant Enterobacteriaceae from India, Pakistan, and UK found been isolated from macaques include ExPEC435 and pks+ E. coli214
that NDM-1 encoding isolates consisted mainly of Klebsiella from subclinical cases, and EIEC and EHEC from an outbreak of
pneumoniae and E. coli, and that NDM-1 was mainly found on diarrhea in outdoor-housed macaques.363
plasmids.375 Furthermore, human patient and environmental In New World monkeys, a clinical investigation of acute pro-
(vacuum cleaner dust from patient’s home) ST131 E. coli encod- fuse diarrhea in cotton-top tamarins (Saguinus oedipus) at New
ing blaNDM-1 have been characterized.75,378,558,574 England Regional Primate Research Center led to the isolation
In companion animals, urine (4 canine and one feline), of EPEC O26:HNM encoding BFP.423 Tamarins with intimin-pos-
wound (canine), and nose (canine) E. coli isolates were posi- itive E. coli fecal isolates exhibited higher incidence of colitis and
tive for NDM-1 genes (blaNDM), suggesting that these animals higher active colitis histologic scores.423 The incidence of EPEC
can be a potential reservoir for these resistant strains to infect in cotton-top tamarins, a model of human ulcerative colitis, is
humans; however, the travel history of owners of these pets was
16
 E. coli Infections in a Range of Hosts

reminiscent of the E. coli prevalence in humans with IBD includ- Medicine consensus statement article, if dogs are exhibiting
ing ulcerative colitis.145,368,423,568,633 systemic signs of illness, the use of antibiotics is warranted for
EPEC has also been isolated from common marmosets (Cal- treating granulomatous colitis.418,430 Metagenomic analyses de-
lithrix jacchus) with bloody stools/diarrhea and the genetic termined that the microflora of dogs with IBD (lymphocytic-
sequence of an isolate was determined.296,723 EPEC was mostly plasmacytic duodenitis and mixed lymphocytic-plasmacytic
detected in stool or rectal swab samples from marmosets with duodenitis and neutrophilic duodenitis) is characterized by an
bloody stools (100%), but was also found in samples from diar- abundance of members of the family Enterobacteriaceae, to which
rheic (20%) and clinically healthy (10%) marmosets.295 Another E. coli belongs.783
NHP study that included marmosets found that 27% and 47% Dogs are also reservoirs of ExPEC strains (some papG+) that
of the E. coli isolated from both apparently healthy monkeys can be transmitted to humans.215,329,332 Genotypic analysis re-
and diarrhea/enteritis cases, respectively, were positive for eae, vealed common electrophoretic types of clinical isolates from
suggesting a role of EPEC in diarrheal disease observed in cap- dogs, cats, and humans in different geographic locations, in-
tivity.106 The expression of BFP, a characteristic of tEPEC strains, cluding Florida, Tennessee, and Michigan, suggesting viru-
suggested zoonotic potential.63,106 Marmosets were proposed as a lent clones.772 ExPEC strains isolated from dog feces and urine
human EPEC infection model.106 Laboratory housed marmosets (UTI) were molecularly similar to strains from human clini-
can be colonized with E. coli, including pks+ or cnf+ strains.321,451 cal cases.332,333 The virulence determinants of CNF-1-encoding
Pigs. Pigs can be colonized with EPEC and have shown strains from dogs with diarrhea also suggests involvement in
A/E lesions.233,304 Forty-three STEC strains, mostly encoding UTI.687 ESBL genes have been detected in canine and feline UTI
Stx2e (Stx2 variant associated with porcine edema disease) and isolates and in fecal isolates from healthy animals.134,527 Other
mostly eae negative, were isolated from slaughtered (appar- potential clinical presentations of dogs with ExPEC infection
ently healthy) finisher pigs.346,431 One of these strains (O103:H2) include hemorrhagic pneumonia and fatal pneumonia with con-
could be considered an EHEC, as it was positive for both stx1 comitant canine adenovirus type 2 infection.10,85,293
and eae.346 Pigs can be considered reservoir hosts of STEC/ E. coli is commonly isolated from the uterus of dogs with pyo-
EHEC, including O157, and have been used experimentally to metra; in cases with concurrent UTI, the same E. coli strain may
study infection and disease.76,77,132,280,603,737 Swine can also harbor be the causative agent of both infections.287 Isolates from dogs
EAEC.751 with pyometra or healthy controls encoded virulence determi-
Virulence determinants including Stx2e and F18 adhesin nants associated with ExPEC involved in UTIs.7,167,670 Genotypi-
(found in ETEC) are associated with ED and diarrhea in wean- cally, some isolates from purulent uterine fluid of affected dogs
ling pigs, and AIDA-I (found in DAEC) is proposed to play were similar to those isolated from their saliva, suggesting that
a role as well.517 AIDA-positive Stx2e-negative isolates were dogs can transmit these virulent isolates to humans.7 Within
identified in pigs that did not show signs of postweaning diar- households, the prevalence of E. coli sharing between healthy
rhea, suggesting that they were DAEC strains.517 Some of the dogs and owners was determined to be 4%, 8%, and 8% using
Stx2e-producing E. coli in one study encoded STs including STIp 3 different fingerprinting (genotyping) methods.508 E. coli with
(STp), STII (STb), and EAST1, suggesting that they can be con- similar genotypes or plasmid pattern have been identified in
sidered STEC-ETEC hybrid strains.45,532 A study of postwean- family members and pets, including dogs and a cat.110,761
ing diarrhea in pigs determined that 6% of the E. coli strains Cats. A/E bacteria have been identified by histopathology
encoded CNF-1.729 Hybrid strains with various characteristics and electron microscopy in 2 clinically affected cats with ca-
were isolated from diarrheic piglets and could not be classified tarrhal enteritis; E. coli was isolated from one of them, suggesting
into particular pathotypes.581 the possibility of EPEC infection.576 EPEC O-:NM was isolated
Dogs. Dogs are reservoirs of aEPEC, tEPEC, STEC, and from the feces of a kitten with diarrhea that later resolved.304
EAEC.44,289,371,488,495,584 A/E lesions have been diagnosed in diar- Clinically affected and unaffected cats may be colonized with
rheic 7 to 9 wk old dogs.304,319 However, some EPEC-colonized tEPEC.258,371 aEPEC also colonizes kittens, is associated with
dogs may not exhibit diarrhea.495,584 Isolation of a tEPEC strain terminal illness, and has higher colonization levels in animals
with the same genotype, phenotype, and serotype in a pet dog with diarrhea than in those without diarrhea.249,514,762 However,
with diarrhea and a child from the same household provided in another study, aEPEC were mostly isolated from nondiarrheic
evidence of zoonotic transmission.609 cats.481 Furthermore, E. coli isolates from diarrheic or healthy
Isolates from dogs with GI disease can also be positive for LT cats can be cytotoxic to Vero cells, and stx2 has been detected
and/or ST and thus be considered ETEC, or positive for Stx and in E. coli strains isolated from cats.1,37,43,44 Cats without diarrhea
considered STEC.37,237,537,578,687,761 Isolation of E. coli O157 from a may also harbor EAEC.584
clinically unaffected dog during an outbreak investigation sug- According to genetic analyses, Firmicutes (Clostridiales) were
gested that dogs act as vectors.733 Dog feces collected on dairy abundant in the GI tract of a healthy specific-pathogen-free cat,
farms were positive for E. coli O157.291 Stx, LT, and ST gene and whereas Enterobacteriaceae, Clostridium spp., and E. coli/Shigella
protein expression were detected in fecal samples from Grey- numbers correlated with clinical signs, duodenal mucosal
hounds with and without acute diarrhea.685 Greyhounds have changes and cytokine upregulation in cats with IBD.318,605 The
been used experimentally to study Stx-induced disease.591 virulence determinants of feline IBD-associated E. coli have not
AIEC, similar to LF82 from human CD, have been isolated been reported.318
from colonic mucosa of boxer dogs with granulomatous coli- Healthy cats can also harbor CNF-1 positive E. coli strains in
tis.668 French Bulldog granulomatous colitis may be associated the feces.54 Diarrhea and septicemia in dogs and cats were as-
with E. coli infection and has been described in young (≤ 1 y old) sociated with CNF-positive E. coli.571 An isolate encoding CNF-1
dogs with hematochezia.418 Sequence analysis of a 904 bp 16S and CNF-2 was cultured from one kitten with necrotizing en-
rRNA PCR amplification product from DNA of formalin-fixed terocolitis.514 UTI-associated E. coli isolates from dogs and cats
paraffin embedded colonic tissue identified E. coli LF82 in the may be characterized by a common set of virulence determi-
colon of a laboratory Beagle dog with histiocytic typhlocoli- nants including hly, pap, sfa, and cnf1.215,791 ExPEC infection in
tis.107 According to an American College of Veterinary Internal cats may be associated with severe respiratory disease including

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Figure 12. (A) Ferret naturally infected with E. coli exhibiting signs of mastitis including swollen and erythematous mammary tissue. (B)
Hyperemic and hemorrhagic serosa at the level of the distal cecum adjacent to the junction with the proximal colon in a Dutch Belted rabbit
experimentally infected with enterohemorrhagic E. coli O157:H7; Copyright © American Society for Microbiology, [Infection and Immunity 80,
pages 369-380, 2012]. (C) Global intracellular edematous swelling, increased numbers of heterophils (arrows), and decreased number of erythro-
cytes (“bloodless glomerulus”) in a glomerulus of a Dutch Belted rabbit experimentally infected with enterohemorrhagic E. coli O153 (scale bar:
60 µm); García and colleagues, Renal Injury Is a Consistent Finding in Dutch Belted Rabbits Experimentally Infected with Enterohemorrhagic
Escherichia coli, The Journal of Infectious Diseases, 2006, volume 193, issue 8, pages 1125-1134, by permission of the Infectious Diseases Society of
America. (D) E. coli-associated necrotizing suppurative metritis (pyometra) in a naturally infected “alpha V integrin+/-; alpha v fl/+; Tie 2, Cre+/-”

18
 E. coli Infections in a Range of Hosts

fatal pneumonia.90,302,698 E. coli encoding cyclomodulins such as coli suggestive of EIEC infection were isolated from lambs with
cnf, pks, and cdt have been isolated from feces and vaginal swabs diarrhea.248 ipaH-positive E. coli and other pathotypes, includ-
of specific-pathogen-free inbred laboratory cats with a history ing hybrid-like strains, were isolated in cultures from bulk tank
of infertility, including pyometra, stillbirths, and resorptions.419 milk and raw milk filters.166
Birds. Chickens can be carriers of EPEC and STEC O157, and Septicemia and enteric disease in calves can be associated
chicks less than or equal to 1 d-old can be experimentally colo- with E. coli strains encoding afa-8, east1, clpG, and also viru-
nized with eae-encoding E. coli including O157:H7362,569,649,697 One lence determinants of ExPEC (cnf1, hly, pap), suggesting gene
study found that EPEC colonized the intestine of chickens, pi- exchange between intestinal and extraintestinal isolates.252 The
geons and ducks; pigeons also harbored EHEC210 and are car- bovine E. coli isolates had some features in common with those
riers of STEC/EHEC strains that may encode Stx2f and have from human cancer patients with sepsis.252 Cnf-2-encoding E.
zoonotic potential.165,210,275,362,479,648,682 “Swollen head syndrome” is coli strains have also been isolated from calves with septicemia
a poultry disease caused by E. coli strains that produce another and enteric disease.252,414,539 E. coli isolated from goat and sheep
Stx variant known as VT2y.483,548,630 Chickens with or without feces may express CNF-3 and also encode plasmid-encoded
diarrhea may be infected with ETEC (STII/STb).8 Yolk sac infec- hemolysin/enterohemolysin (ehxA) and eae.538,646 Two EPEC
tion in chickens may be associated with ipaH-positive bacteria, O115:H- isolates from the colon and rectum of an O157:H7-inoc-
suggestive of EIEC.616,617 Pigeons and conures can also be vectors ulated lamb encoded CNF-1, CNF-2, and EAST-1, and another
of EIEC and EAEC, respectively.427,667 In addition, avian organic O115 strain encoding these same virulence determinants was
fertilizer may be contaminated with EAEC and/or EAEC/ isolated from a sheep.9,130 An outbreak of lamb septicemia was
EPEC hybrid strains.583 associated with neonatal E. coli O78 (K46) infection.356,357
APEC are ExPEC strains associated with local or systemic Mammary pathogenic E. coli was proposed as a “pathotype”
colibacillosis; these infections are an important disease category for E. coli strains isolated from cases of mastitis in cows; how-
that economically affects the poultry industry.250,276,449,694 These ever, mastitis-associated E. coli and commensal E. coli could not
strains may be classified into subpathotypes, defined by their be distinguished phylogenetically.392,663 More recently, in vivo
associated clinical presentation, including omphalitis, “swol- experiments indicated that the ferric dicitrate uptake locus (fec
len head syndrome”, and septicemia. 449 APEC can encode locus) is associated with the ability of mammary pathogenic E.
several virulence determinants, and some strains have been coli to induce mastitis.70 Cows develop pelvic inflammatory dis-
proposed to represent human UPEC (ExPEC) or influence hu- ease/metritis, which has been associated with E. coli strains that
man disease by transferring virulence determinants to other encode fyuA.661 These fyuA-encoding E. coli strains, currently
strains.144,202,457,468,610,650,694 Using MLST, APEC and human UPEC known as endometrial pathogenic E. coli, did not encode adhe-
isolates were found to belong to 4 sequence types including sion and invasion genes of enteric or ExPEC strains.661 However,
ST10, ST48, ST117, and ST2016, suggesting zoonotic potential.173 comparative genome analysis of the prototype endometrial
ExPEC strains involved in UTIs and APEC strains may belong pathogenic E. coli strain MS499 indicated that this strain encodes
to the same serogroups and may also be genotypically and phy- ExPEC factors.260
logenetically similar.610 Ferrets. An investigation of gangrenous mastitis in ferrets im-
Ruminants. Ruminants including goats, sheep, and cows are plicated hemolytic E. coli as the causative agent (Figure 12 A).403
well-recognized and thoroughly researched reservoir hosts of This disease had an acute septicemic or peracute presentation.403
STEC/EHEC.41,44,61,65,66,292,799 Some cows are known as super shed- The same organism was also isolated from rectal swab samples
ders that can excrete O157 at estimated levels of greater than 104 of ferrets both with and without mastitis.403 An investigation of
CFU/g of feces, a characteristic that could be epidemiologically E. coli isolates from diarrheic feces, uterus, brain, or mammary
relevant.18,135,507 The recto-anal junction has been identified as a gland of clinically affected ferrets characterized the isolates as β-
lymphoid follicle rich area of the intestine that is colonized by hemolytic and positive for cnf1, hlyA, and pap1.428 These isolates
O157:H7 with aggregative adherent phenotype.135,507 Vaccination were negative for cnf2, eae, stx1, stx2, sta, and stb.428 In another
strategies have been developed for cattle to reduce the level of study, clinical disease, including sudden death or anorexia and
intestinal colonization with EHEC.674 Cattle, sheep, and goats loose mucoid feces (for 12 to 24 h), was observed in captive
can all carry EPEC that may be zoonotic.67,96,133,233,416 black-footed ferrets.83 ETEC (positive for sta and stb) was iso-
Ruminants can also be reservoirs of ETEC, which is shed by lated from clinically affected adults and kits.83 The only isolate
diarrheic newborn calves.61,385,717,773 Virulence determinants of not characterized as ETEC was isolated from kit tissues and was
bovine ETEC isolates include STaP, F41 and K99.413 The K99 plas- positive for cnf1.83 To date, Stx-encoding E. coli have not been
mid was associated with diarrhea in calves and lambs.314,484,541,676 reported in ferrets; however, an experimental model involving
K99 and/or F41 detection in goat kid and lamb E. coli isolates Stx-encoding E. coli infection of streptomycin treated ferrets has
that were not STI or LTI producers suggested that these strains been reported.779
were virulence determinant reservoirs.490 In Bangladesh, 34% Rabbits. Historically, E. coli has been recognized as an agent
of the ruminant E. coli isolates were STEC-ETEC hybrids and that can commonly colonize clinically unaffected rabbits, in-
50% of these were antibiotic resistant.339 Also, ipaH-positive E. cluding Cottontail rabbits (Sylvilagus floridanus), but can also

mouse. E. coli is fluorescently labeled with a green peptic nucleic acid in situ hybridization probe that detected bacteria in the affected and lumi-
nal areas of the uterus. The nuclei of the cells are stained blue with 4’,6’-diamidino-2-phenylindole (DAPI) (no scale bar: x100); Reprinted from
Microbes and Infection18(12), García A, Mannion A, Feng Y, Madden CM, Bakthavatchalu V, Shen Z, Ge Z, Fox JG, Cytotoxic Escherichia coli
strains encoding colibactin colonize laboratory mice, 777-786, Copyright (2016) with permission from Elsevier. (E) Renal section of a mouse natu-
rally infected with cytotoxic E. coli ( pks+) and exhibiting multifocal subacute suppurative pyelonephritis, intraluminal bacteria, and tubular
necrosis (scale bar: 1 mm). (F) Brain section of a mouse naturally infected with cytotoxic E. coli ( pks+) and exhibiting focally extensive subacute
necrohemorrhagic meningoencephalitis (scale bar: 200 µm). Figures 12(E) and 12(F) have been reprinted from Bakthavatchalu and colleagues
(2018) Cytotoxic Escherichia coli strains encoding colibactin isolated from immunocompromised mice with urosepsis and meningitis. PLoS One
13(3): e0194443. doi: 10.1371/journal.pone.0194443, with permission through an open access Creative Commons Attribution (CC BY) license. (C,
E, F are hematoxylin and eosin stained sections).

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February 2021

Figure 13. Reported E. coli pathotypes or hybrids and the animals in which they have been identified. EPEC, enteropathogenic E. coli; STEC,
Shiga toxin-producing E. coli; EHEC, enterohemorrhagic E. coli; ETEC, enterotoxigenic E. coli; EIEC, Enteroinvasive E. coli; DAEC, Diffusely ad-
hering E. coli; ExPEC, Extraintestinal pathogenic E. coli; EAHEC, Entero-aggregative-hemorrhagic E. coli; aEPEC, atypical EPEC; tEPEC, typical
EPEC; EPEC/ETEC, STEC and/or EHEC/ETEC, aEPEC/ExPEC, EHEC/ExPEC, ETEC/DAEC, EIEC/EHEC/EAEC, tEPEC/STEC are hybrids;
X, reported; Empty box, not reported.

induce fatal disease.254,369,790 Similarly, EPEC and STEC/EHEC and F).24 E. coli was identified in a mouse diagnosed with cystic
have been detected or isolated in rabbits with or without clini- endometrial hyperplasia; Clb-encoding E. coli was isolated from
cal signs.59,239,395,572,699 In addition to RDEC-1, EPEC O103 strains the uterine fluid/wall.241 In another study, laboratory rats from
exhibited high pathogenicity along with an inability to ferment various commercial suppliers were colonized by Clb-encoding
rhamnose.58,98 Coinfection with other pathogens may influence E. coli, and some of these isolates also encoded CDT or CNF.377
the severity of EPEC infection.555,644 Particular serotypes may be Currently, E. coli pathotypes are not included in conventional
associated with disease in weaned as compared with suckling health surveillance protocols for mice or rats.
rabbits.553,556 “E. coli O:105” (strain 1056), an invasive E. coli isolated from
Rabbits have been reported as vectors of O157:H7 or non- the ileum of a hamster with proliferative ileitis was shown
O157 STEC strains.23,390,580,639 EHEC O153 infection was associ- experimentally to induce acute enteritis in 32% of Syrian
ated with an outbreak of diarrhea and HUS-like disease in DB hamsters.232 In addition, spontaneous enterocolitis of Syrian
rabbits; characterization of the natural cases lead to the develop- hamsters was associated with coinfection of β-hemolytic E. coli
ment of an experimental model involving oral inoculation (Fig- and Campylobacter-like organisms (now known to be Lawsonia
ure 12 B and C).238,243,545,664,790,793 Rabbits experimentally infected intracellularis).172 Furthermore, E. coli infection is one of the po-
with other EHEC strains by the intraperitoneal route also de- tential etiologies associated with urinary tract disease including
velop disease.281 Other toxigenic E. coli strains that can be found cystitis, cystic calculi, and urolithiasis in guinea pigs,560 appar-
in rabbits include those encoding CNF1 or CNF2.59,60 ently with a disease predisposition in aged females.560 These
Rodents. E. coli has been isolated from mice and rats, particu- clinical conditions of guinea pigs were observed at mean ages of
larly the murine oral cavity, which may harbor E. coli due to 35 mo (cystitis) and 30 mo (cystic calculi and urolithiasis).560 Un-
coprophagia.21,265,411,455,734 In a study of Norway rats in New York fortunately, molecular characterization of hamster and guinea
City, aEPEC was detected in the feces along with other poten- pig E. coli isolates was not reported.172,232,560 Recently, a study
tially zoonotic pathogens.217 In farm environments, rats can be characterizing E. coli isolates from small mammals identified
EHEC/STEC carriers, and experimentally,516 intraperitoneal in- Clb-encoding E. coli in 2 diarrheic pet guinea pigs.207
oculation of recombinant Stx2-expressing E. coli culture super- In a fatal case of septicemia in a chinchilla, Gram-negative
natant has been used to develop a rodent model of HUS.516,798 rods were found adhering to intestinal epithelial cells and EPEC
Lesions of E. coli-infected clinically affected mice include O13:H30 (negative for genes encoding LT, STa, Stb, CNF-1, CNF-
abscesses (subcutaneous and others affecting seminal vesicles, 2, Stx1, Stx2) was isolated from the kidney and spleen.170 E. coli
preputial glands, kidney, uterus), septicemia, pneumonia, or including ETEC and possibly EIEC (ipaH gene amplification)
endometritis (Figure 12 D).24,36,241 Development of spontaneous were detected in fecal samples from peridomestic rodents (Rat-
β-hemolytic E. coli peritonitis in homozygous mutant Myd88tm1Aki tus rattus and Mus musculus) samples from rural Madagascar.93
female and male mice suggested susceptibility due to impaired Figure 13 illustrates the apparent distribution of E. coli pathot-
innate immunity.334 Mice developed hyperplasia and hypertro- ypes or hybrids in a variety of animals based on published stud-
phy of mesothelial cells.334 The intestine of interleukin 10-de- ies. These data reveal that some pathotypes/hybrids have not
ficient mice with intestinal inflammation contained a higher been reported in animals and thus represent opportunities for
number of E. coli O7:K1:H7 than did that of control mice without discovery of new hosts. Also, from an epidemiologic perspec-
disease.777 A study using laboratory mice, including sentinels, tive, these data underscore the potential for E. coli transmission
found that animals were colonized by Clb-encoding (pks+) E. between animals, including zoonotic risks. The combination of
coli, which may confound experimental studies.241 Cases of uro- E. coli diversity and host range generate conditions that could
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in humans and animals will enlighten future investigations and sity and changing landscape: insights for the twenty-first cen-
serve as a comparative medicine reference compendium for the tury. Front Cell Infect Microbiol 6:1–9. https://doi.org/10.3389/
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article serves as a tribute to those investigators, who through
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org/10.1186/1471-2164-12-9.
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We thank Elaine Robbins for assistance with preparation of Figures Uronis JM, Fan TJ, Campbell BJ, Abujamel T, Dogan B, Rogers
1 and 12 for publication and Dr Sebastian E Carrasco for assistance AB, Rhodes JM, Stintzi A, Simpson KW, Hansen JJ, Keku TO,
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