Poirel 2018

Antimicrobial Resistance
in Escherichia coli
LAURENT POIREL,1,2,3 JEAN-YVES MADEC,4 AGNESE LUPO,4
ANNE-KATHRIN SCHINK,5 NICOLAS KIEFFER,1
PATRICE NORDMANN,1,2,3 and STEFAN SCHWARZ5
1
Emerging Antibiotic Resistance Unit, Medical and Molecular Microbiology, Department of Medicine,
University of Fribourg, Fribourg, Switzerland; 2French INSERM European Unit, University of Fribourg
(LEA-IAME), Fribourg, Switzerland; 3National Reference Center for Emerging Antibiotic Resistance
(NARA), Fribourg, Switzerland; 4Université de Lyon – Agence Nationale de Sécurité Sanitaire (ANSES),
Unité Antibiorésistance et Virulence Bactériennes, Lyon, France; 5Institute of Microbiology and Epizootics,
Centre of Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, Berlin, Germany
ABSTRACT Multidrug resistance in Escherichia coli has become agents in human medicine also occurs through the
a worrying issue that is increasingly observed in human but massive use of antimicrobial agents in veterinary medicine,
also in veterinary medicine worldwide. E. coli is intrinsically such as tetracyclines or sulfonamides, as long as all those
susceptible to almost all clinically relevant antimicrobial agents, determinants are located on the same genetic elements.
but this bacterial species has a great capacity to accumulate
resistance genes, mostly through horizontal gene transfer.
The most problematic mechanisms in E. coli correspond to INTRODUCTION
the acquisition of genes coding for extended-spectrum
β-lactamases (conferring resistance to broad-spectrum
Escherichia coli is a bacterium with a special place in
cephalosporins), carbapenemases (conferring resistance to the microbiological world since it can cause severe in-
carbapenems), 16S rRNA methylases (conferring pan-resistance fections in humans and animals but also represents a
to aminoglycosides), plasmid-mediated quinolone resistance significant part of the autochthonous microbiota of the
(PMQR) genes (conferring resistance to [fluoro]quinolones), different hosts. Of major concern is a possible trans-
and mcr genes (conferring resistance to polymyxins). mission of virulent and/or resistant E. coli between ani-
Although the spread of carbapenemase genes has been mals and humans through numerous pathways, such
mainly recognized in the human sector but poorly recognized
as direct contact, contact with animal excretions, or via
in animals, colistin resistance in E. coli seems rather to be
related to the use of colistin in veterinary medicine on a the food chain. E. coli also represents a major reservoir
global scale. For the other resistance traits, their cross-transfer of resistance genes that may be responsible for treatment
between the human and animal sectors still remains
controversial even though genomic investigations indicate Received: 9 May 2018, Accepted: 16 May 2018,
that extended-spectrum β-lactamase producers encountered Published: 12 July 2018
in animals are distinct from those affecting humans. Editors: Frank Møller Aarestrup, Technical University of Denmark,
Lyngby, Denmark; Stefan Schwarz, Freie Universität Berlin, Berlin,
In addition, E. coli of animal origin often also show Germany; Jianzhong Shen, China Agricultural University, Beijing,
resistances to other—mostly older—antimicrobial agents, China, and Lina Cavaco, Statens Serum Institute, Copenhagen,
including tetracyclines, phenicols, sulfonamides, Denmark
trimethoprim, and fosfomycin. Plasmids, especially Citation: Poirel L, Madec J-Y, Lupo A, Schink A-K, Kieffer N,
multiresistance plasmids, but also other mobile genetic Nordmann P, and Schwarz S. 2018. Antimicrobial resistance in
elements, such as transposons and gene cassettes in Escherichia coli. Microbiol Spectrum 6(4):ARBA-0026-2017.
doi:10.1128/microbiolspec.ARBA-0026-2017.
class 1 and class 2 integrons, seem to play a major role in
Correspondence: Laurent Poirel, [email protected]
the dissemination of resistance genes. Of note, coselection and
© 2018 American Society for Microbiology. All rights reserved.
persistence of resistances to critically important antimicrobial
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Poirel et al.
failures in both human and veterinary medicine. An in- In animals, E. coli is one of the leading causes of
creasing number of resistance genes has been identified diarrhea, together with other pathogens such as rota-
in E. coli isolates during the last decades, and many of virus, coronavirus, Cryptosporidium parvum, or a com-
these resistance genes were acquired by horizontal gene bination of these (4). These enterotoxigenic E. coli
transfer. In the enterobacterial gene pool, E. coli acts as a (ETEC) strains bind and colonize the intestinal epithe-
donor and as a recipient of resistance genes and thereby lium through adhesins expressed in the context of fim-
can acquire resistance genes from other bacteria but briae, such as the F4 (formerly designated K88), F5
can also pass on its resistance genes to other bacteria. In (K99), F6 (987P), F17, and F18 fimbriae (5). ETEC also
general, antimicrobial resistance in E. coli is considered produces various enterotoxins, of which heat-labile and
one of the major challenges in both humans and animals heat-stable toxins and/or enteroaggregative heat-stable
at a worldwide scale and needs to be considered as a real toxin 1 (EAST1) lead to diarrhea. ETEC affects various
public health concern. animal species, mostly young animals, particularly food-
This chapter gives an update of antimicrobial resis- producing animals (piglets, newborn calves, chickens)
tance in E. coli of animal origin by focusing on resistance but also companion animals such as dogs. In livestock,
to those classes of antimicrobial agents mainly used in diarrhea is considered one of the major diseases, which
veterinary medicine and to which E. coli isolates of ani- can propagate among animals with possibly significant
mal origin are known to exhibit resistance. consequences at the herd/flock level. Diarrhea is ob-
served in pigs and calves during the first 3 to 5 days of
life and in pigs 3 to 10 days after weaning. The trend
E. COLI IN ANIMALS: A PATHOGENIC toward early weaning in several countries and conti-
AND A COMMENSAL BACTERIUM nents may have played a significant role in the rising
“Colibacillosis” is a general term for a disease caused occurrence of postweaning diarrhea in the pig sector. As
by the bacterium E. coli, which normally resides in a consequence, lethal ETEC infections in animals can
the lower intestines of most warm-blooded mammals. also occur as a result of severe dehydration and elec-
Hence, E. coli is a versatile microorganism with a num- trolyte imbalance.
ber of pathogenic isolates prone to cause intestinal and E. coli infections in animals are not restricted to young
extra-intestinal infections, while most others are harm- individuals but occur in adults as well. As mentioned
less for their host and refer to commensalism. The path- above, extra-intestinal pathogenic E. coli is responsible
ogenic E. coli isolates can be classified into different for infections of the lower and upper urinary tract, par-
pathotypes, or pathovars, where each pathotype causes ticularly in companion animals (6, 7). In poultry, avian-
a different disease (1). The intestinal pathogenic E. coli pathogenic E. coli causes colibacillosis initiated in the
pathovars are responsible for disorders in the gut rang- respiratory tract by inhalation of fecal dust before
ing from mild diarrhea to severe colitis, while the spreading further in the whole body, causing septicemia,
extra-intestinal pathogenic E. coli pathovars are mostly pericarditis, and mortality (8). In dairy cattle, mastitis
asymptomatic inhabitants of the intestinal tract that is a common inflammatory response of the mammary
cause extra-intestinal diseases after migrating to other gland, significantly decreasing milk production and
parts of the body, such as the urinary tract or the blood causing dramatic economic losses, with E. coli being
stream (2). Animal diseases due to E. coli can also be one of the major causes—together with Staphylococcus
caused by E. coli isolates originating from the environ- aureus, Streptococcus uberis, Streptococcus agalactiae,
mental reservoir or other infected individuals. Patho- and Streptococcus dysgalactiae (9, 10). In particular,
genic and nonpathogenic E. coli differ by the acquisition E. coli is responsible for more than 80% of cases of acute
or loss of virulence-associated traits associated with mastitis where the severe clinical signs are induced by
E. coli pathogenicity. The number of genes present in the the lipopolysaccharide (LPS) as a primary virulence fac-
E. coli genome varies from 4,000 to 5,000 genes, with tor followed by the subsequent release of inflammatory
approximately 3,000 genes shared by the different iso- mediators (11). Nonetheless, it is broadly considered that
lates, whereas the others mostly correspond to coloni- mastitis in dairy cattle due to E. coli is neither associated
zation or virulence determinants. Advanced insights in with specific E. coli serovars nor involves a common set
the genomic plasticity of E. coli have been possible by of virulence factors shared among E. coli isolates.
the use of whole-genome sequencing, providing a better E. coli infections in animals are subjected to various
understanding of the core and accessory genomes of pharmaceutical treatments including antimicrobials.
pathogenic and commensal E. coli isolates (3). For instance, ampicillin, streptomycin, sulfonamides,
2 ASMscience.org/MicrobiolSpectrum
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Antimicrobial Resistance in Escherichia coli
or oxytetracyclines are commonly used to treat bovine cases, it more likely reflects the selective impact of the use
mastitis, but broad-spectrum cephalosporins and fluo- of antimicrobials—and particularly of broad-spectrum
roquinolones also have indications through systemic cephalosporins such as ceftiofur—on the commensal
or local administration depending on the severity of E. coli microbiota. In broilers, such a situation has be-
the clinical symptoms (12) and the resistance properties come a point of major concern on a global scale since
of the causative E. coli isolates. Nonetheless, the role of broad-spectrum cephalosporins are both of critical im-
antimicrobials in the treatment of coliform mastitis is portance in human medicine and not authorized for use
becoming more and more open to debate. Recommen- in poultry. In addition to national actions taken, mostly
dations provided for veterinarians refer to the prefera- in Europe, to restrict the use of critically important an-
ble use of first-line antimicrobial agents and avoidance timicrobial agents in animals, the use of antimicrobial
of antimicrobial therapy during the dry-off period of agents as growth promoters has been banned in animals
dairy cattle. Global data and trends on the antimicro- in Europe since 2006, but it is still common practice in
bial resistance of E. coli in mastitis have been highlighted most countries. Altogether, since antimicrobial agents
in several national reports and vary among countries have a major impact on the gut microbiota where E. coli
even though relevant comparisons are difficult. To date, resides, multidrug-resistant E. coli, such as ESBL/AmpC-
the global picture indicates that antimicrobial suscepti- producing E. coli, has become one of the main indicators
bility of E. coli in mastitis remains high. In particular, to estimate the burden of antimicrobial resistance in
extended-spectrum β-lactamases (ESBLs) or overex- animals and other sectors in a One Health perspective.
pressed cephalosporinases (AmpCs) produced by E. coli
and conferring resistance to broad-spectrum cephalo-
sporins have been sporadically isolated from milk sam- RESISTANCE TO β-LACTAMS
ples (13–16). Those families of antimicrobial agents may There are numerous genes in E. coli of human and ani-
also be prescribed in newborns affected by diarrhea. mal origin that confer resistance to β-lactams. Some
Again, action plans against antimicrobial resistance in of them, such as blaTEM-1, are widespread in E. coli
the animal sector constantly advise veterinarians to use from animals but code only for narrow-spectrum
antimicrobials prudently and emphasize the need to con- β-lactamases that can inactivate penicillins and amino-
sider all other preventive and therapeutic options and penicillins. However, in recent years, genes that code
restrict the use of antimicrobial agents to those situations for ESBLs/AmpCs have emerged in E. coli from humans
where it is indispensable (17). For instance, strategies and animals. Most recently, genes coding for carbapen-
to prevent and treat neonatal diarrhea should include emases have also been detected occasionally in E. coli
not only the prescription of antimicrobials but also good of animal origin. Because of the relevance of these latter
colostrum management practices to ensure adequate two groups of β-lactamases, the following subsections
passive immunity and appropriate oral or intravenous provide more detailed information on ESBLs, AmpCs,
fluid therapy to compensate for dehydration, acidosis, and carbapenemases.
and electrolyte imbalance (18). Global hygiene proce-
dures at the farm level and vaccinations are also essential Clavulanic-Acid Inhibited Class A ESBLs
measures for improvement in antimicrobial stewardship. ESBLs belong mostly to class A of the Ambler classifi-
In contrast to mastitis, ESBL/AmpC genes have been cation (22) and group 2be according to the updated
abundantly reported in E. coli originating from the di- functional classification of β-lactamases by Bush and
gestive tract in animals. This includes pathogenic E. coli Jacoby (23). ESBL-producing strains of E. coli are clin-
recovered from diarrheic samples of young animals, yet ically relevant in veterinary medicine since they confer
it remains highly difficult to confirm that a specific resistance to penicillins, aminopenicillins, and cephalo-
E. coli isolate is responsible for the intestinal disease. sporins, including the third-generation cephalosporins
More importantly, ESBL/AmpC genes have been widely ceftiofur and cefovecin and the fourth-generation ceph-
recognized in commensal E. coli isolated from fecal alosporin cefquinome, which are approved veterinary
samples of various food-producing and companion drugs. Thus, ESBLs may be the cause of treatment fail-
animals through selective screenings using cephalospo- ures and limit the therapeutic options of veterinarians,
rin-containing media (19–21). High prevalence rates of because they have been identified in increasing numbers
ESBL/AmpC-producing E. coli were found in certain in E. coli of food-producing and companion animals
settings and countries, such as in the veal calves sector in worldwide (24, 25). ESBL-producing E. coli from ani-
Europe and in broiler production worldwide. In those mals has been isolated not only from infection sites, but
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Poirel et al.
also from the feces of healthy individuals (26–29). this resistance is based on ESBL production or another
Moreover, ESBL-producing E. coli has also been detected β-lactamase. Moreover, the molecular identification of
in wild animals, emphasizing the wide distribution of ESBL genes in monitoring programs is not systematic.
these resistance determinants (30). The nonharmonized methodology is also reflected in
TEM- and SHV-ESBLs were among the first described sampling plans and therefore in the origin of the E. coli
ESBLs in the 1980s, and they were predominant until isolates, e.g., healthy or diseased animals (33). Never-
2000. Since then, CTX-M-ESBLs emerged and have theless, the European Food Safety Authority compiled
been predominantly identified in commensal and path- a scientific opinion which states that the prevalence
ogenic ESBL-producing E. coli isolates of human and of resistance to cefotaxime in food-producing animals
animal origin around the world (31, 32). The reason for varies by country and animal species. In addition, the
this shift remains unknown, despite many investigations ESBL genes blaCTX-M-1, blaCTX-M-14, blaTEM-52, and
and surveillance studies. It is difficult to compare prev- blaSHV-12 were identified as the most common ones
alence data of ESBL-producing E. coli isolates because along with a wide range of other blaCTX-M, blaTEM, and
several resistance-monitoring programs register the re- blaSHV variant genes (34) (Table 1).
sistance rates for cephalosporins in E. coli isolates of A large study conducted in Germany analyzed
animal origin but do not necessarily confirm whether ESBL-producing E. coli isolates collected from diseased
TABLE 1 Examples of acquired ESBL genes in E. coli of animal origin from Europe, the U.S., Latin America,
Africa, and Asia
ESBL gene Geographical origin Source Sequence type(s) Reference

blaCTX-M-1 Denmark Pig 10, 189, 206, 453, 542, 744, 910, 1406, 1684 2739, 257
4048, 4052, 4053, 4056,
Sweden Poultry 57, 135, 155, 219, 602, 752, 1594, 1640 258
Great Britain Poultry 4, 10, 57, 88, 155, 371, 1515, 1517, 1518, 1549, 1550 259
Switzerland Poultry, cattle, pig 48, 83, 305, 525, 528, 529, 533, 534, 536, 540 260
The Netherlands Veal calves 10, 58, 88, 117, 162, 224, 354, 448, 617, 648, 744, 973 21
France Dairy cattle 23, 58 13
Germany Dairy cattle 10, 117, 540, 1431, 5447 14
Germany Swine, cattle, 10, 23, 83, 100, 131, 167, 362, 453, 648, 43
poultry, horse 925, 973, 1684, 2699
Germany Dog 10, 23, 69, 160, 224 28
U.S. Dog, cat 23, 38, 44, 68, 69, 131, 167, 405, 410, 443, 261
648, 1011, 1088, 5174, 5206, 5220
blaCTX-M-14 The Netherlands Veal calves 10, 57, 952 21
France Dairy cattle 10, 23, 45, 58 13
China Pig, poultry 10, 155, 206, 224, 359, 405, 602, 648, 2929, 2930, 2962 262
China Dog 10, 38, 104, 131, 167, 405, 648, 146, 3630 97
blaCTX-M-15 UK Poultry 57, 156 259
UK Dog 131, 410, 1284, 2348, 4184 99
The Netherlands Veal calves 58, 59, 88, 361, 410, 648 21
Germany Livestock 10, 88, 90, 167, 410, 617, 648 263
Germany Dairy cattle 10, 361, 1508 14
Germany, Denmark, Spain, Dog, horse 131 264
France, the Netherlands
Germany, Italy Dog, cat, cattle, horse 648 96
Germany Dog 410, 3018 28
U.S. Dog, cat 23, 38, 44, 68, 69, 131, 167, 405, 410, 443, 617, 648, 261
1011, 1088, 5174, 5206, 5220
Mexico Dog 410, 617 138
China Dog 10, 38, 44, 69, 73, 75, 131, 302, 405, 648, 1700, 2375 97
Nigeria Poultry 10, 405 221
blaSHV-12 Spain, Germany Wild bird, dog, poultry 23, 57, 117, 155, 362, 371, 453, 616, 1564, 2001 39
China Dog 10, 75, 131, 167, 405, 648, 2375, 3058 97
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food-producing animals in the GERM-Vet monitoring majority of ESBL genes are plasmid-located, whereas
program from 2008 to 2014 (35). This study detected the integration of ESBL genes in the chromosomal DNA
the gene blaCTX-M-1 in 69.9% of the ESBL producers, of E. coli of animal origin has been rarely described (47–
followed by blaCTX-M-15 in 13.6%, blaCTX-M-14 in 49). The most prevalent replicon types identified among
11.7%, blaTEM-52 in 1.9%, and blaSHV-12 in 1.4%. The ESBL-carrying plasmids from E. coli are IncF, IncI1,
genes blaCTX-M-3 and blaCTX-M-2 were identified in 1.0% IncN, IncHI1, and IncHI2, but plasmids of other repli-
and 0.5%, respectively. The distribution of ESBL genes con types also play a role in the dissemination of ESBL
varies with regard to the different animal hosts and the genes (47). The study by Day and co-workers identified
isolation sites; for example, ESBL-producing E. coli were 16 ESBL genes on 341 transferable plasmids, belonging
isolated more frequently from cases of enteritis in calves to 19 replicon types (36). Despite this complexity, some
than from cases of bovine mastitis (35). Moreover, the plasmids that carry ESBL genes seem to be more suc-
geographical location also plays a role. For instance, cessful than others. Plasmids carrying blaCTX-M-15 and
the study by Day and co-workers identified the gene belonging to the IncF family had been detected in
blaCTX-M-1 as the most common among bovine ESBL- the pandemic E. coli clone O25:H4-ST131 (47). The
producing E. coli from Germany, while the gene ESBL gene blaCTX-M-1 was frequently identified on
blaCTX-M-15 was most frequent in E. coli isolates of bo- plasmids belonging to the IncN or IncI1 families,
vine origin from the United Kingdom (36). In ESBL- while blaCTX-M-14 was detected on IncK plasmids, and
producing E. coli isolates from European companion blaCTX-M-3 on IncL/M plasmids (47). IncI1, IncK, and
animals, the gene blaCTX-M-1 was most common, but the IncX plasmids carried the ESBL gene blaSHV-12 (39). A
gene blaCTX-M-15 was also frequently identified (24, 37). plasmid multilocus sequence typing scheme assigns
In the United States, the gene blaCTX-M-15 was predom- members of the most common plasmid families to pSTs
inant among ESBL-producing E. coli from urinary to trace epidemic plasmids (47). Some plasmids harbor
tract infections of companion animals (38). The gene additional resistance genes besides the ESBL gene, which
blaCTX-M-14 was less frequent in Europe, but in Asia may facilitate the coselection and persistence of ESBL
among the most common ESBL genes in poultry, com- gene-carrying plasmids even without the selective pres-
panion animals, and humans (24). The ESBL gene sure of β-lactams, when the respective antimicrobial
blaSHV-12 was not frequently reported but was identified agents are used (14, 43).
in ESBL-producing E. coli from poultry, dogs, and wild Many studies have tried to figure out whether ESBL-
birds in Spain and Germany (39). producing E. coli identified in humans might originate
Worldwide, the most common ESBL gene in E. coli from animal reservoirs. Most of those studies could
isolates of human origin is blaCTX-M-15, which is mainly not find an obvious link, and most often, it was clearly
associated with the pandemic E. coli clone O25:H4- shown that there was no link at all, animals and humans
ST131 (40). This clone has been rarely identified representing reservoirs of different clonal lineages that
in animals and if so, mostly in companion animals (24, possessed various ESBL determinants (50, 51). Never-
25, 41, 42). The production of various ESBLs has been theless, a Dutch study showed that a significant number
demonstrated in animal E. coli isolates of a wide vari- of either human- or poultry-associated ESBL-producing
ety of multilocus sequence types (24, 35, 36, 43) (Table E. coli isolates harbored genetically indistinguishable
1). According to Ewers and colleagues, an exclusive ESBL-encoding plasmids, suggesting that plasmids might
linkage of a specific bla gene or a distinct host with a be common vehicles that are likely transmitted through
certain sequence type (ST) is not evident (24). Never- the food chain (52). Indeed, numerous studies have
theless, ESBL-producing E. coli belonging to certain pointed out that chickens may represent a significant
STs have been more frequently detected among animals reservoir of ESBLs, which has become a considerable
and humans than others, namely ST10, ST23, ST38, concern worldwide, although broad-spectrum cephalo-
ST88, ST131, ST167, ST410, and ST648, which are sporins are not approved for use in the poultry sector.
supposed to facilitate the spread of ESBL genes (25, 36, ESBL-producing E. coli has been reported as a cause of
43, 44). infections in broilers and laying hens but also as a col-
The dissemination of ESBL genes among E. coli from onizer of living chickens and a contaminant of chicken
animals is mainly driven by horizontal gene transfer. meat at retail in several European and non-European
ESBL genes are associated with several insertion se- countries, including countries in which the use of anti-
quences (ISs), such as ISEcp1, ISCR1, IS26, and IS10, microbial agents has been reduced following national
transposons such as Tn2, and integrons (43, 45, 46). The action plans in veterinary medicine (53).
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Poirel et al.
Acquired AmpC Cephalosporinases previously been identified from human bacteremia. The
Although class A ESBL enzymes are the most com- blaCMY-2 gene was mainly found on IncI1 plasmids,
mon sources of acquired resistance to broad-spectrum as reported with human isolates. Therefore, there was a
cephalosporins in E. coli, class C β-lactamases, also significant correlation between the genetic features of
known as AmpC-type enzymes, confer high-level resis- those isolates and those known for human isolates in the
tance to those antimicrobial agents (54). The main United States, showing that seagulls were likely colo-
plasmid-encoded AmpC enzymes are CMY-, DHA-, nized by human isolates. This is an example showing
and ACC-type β-lactamases, with a higher prevalence that migratory birds crossing long distances, such as
of CMY-type enzymes worldwide (55). In animals, the along the eastern United States coastline, may be reser-
majority of identified AmpC enzymes have been of the voirs and therefore sources of such multidrug-resistant
CMY type (Table 2) (25, 56). A recent study performed isolates, as is also exemplified in South America and
in Denmark identified CMY-2-producing E. coli isolates Europe (62, 63).
from poultry meat, poultry, and dogs (57). The study
showed that the dissemination of blaCMY-2 was mainly Acquired Carbapenemases
due to the spread of IncI1-γ and IncK plasmids. In Carbapenemases have been rarely identified in animal
Sweden, though there are, in general, low rates of re- E. coli. This is likely the consequence of a very weak
sistance to broad-spectrum cephalosporins, the occur- selective pressure (if any) by carbapenems, since those
rence of CMY-2-producing E. coli was demonstrated antimicrobial agents are not (or only in rare cases for
when Swedish chicken meat, Swedish poultry, and im- individual non-food-producing animals) prescribed in
ported chicken meat were examined (58). The occur- veterinary medicine. Nevertheless, there has been some
rence of CMY-2-producing E. coli in the Swedish broiler concern in recent years since carbapenemase-producing
sector has been attributed to importation of 1-day old bacteria, including E. coli, have been isolated from ani-
chicks from the United Kingdom, where broad-spectrum mals worldwide (64–66).
cephalosporins had been administered prophylactically The first carbapenemase determinant identified in an
to the young birds before exportation (59). It has also animal E. coli isolate was VIM-1, which was recovered
been shown that migratory birds may be colonized with from a pig in Germany (67) (Table 3). Since then, other
CMY-2-positive E. coli (60). In a study conducted in VIM-1-producing E. coli isolates have been identified
Florida, a series of clonally unrelated CMY-2-producing in different pig farms in the same country (68, 69). This
E. coli isolates were recovered from feces of seagulls carbapenemase has so far never been found elsewhere
(61). They belong mainly to phylogroup D, correspond- in animal isolates. Other identified carbapenemases in
ing to human commensal isolates, but some STs had E. coli are NDM-1 and NDM-5. NDM-1 has been iden-
TABLE 2 Examples of acquired blaCMY-2 genes in E. coli of animal origin from Europe, the North and South America,
Asia, and Africa
Geographical origin Source Sequence type(s) Reference

Germany Pig 625 265
Spain Wild bird 10 266
(yellow-legged gull)
Denmark, Germany, Poultry and poultry 10, 23, 38, 48, 68, 69, 88, 93, 115, 117, 131, 206, 212, 219, 297, 350, 57
France meat, dog 361, 372, 405, 410, 428, 448, 457, 546, 616, 746, 754, 919, 963,
1196, 1056, 1303, 1518, 1585, 1594, 1640, 1775, 2040, 2144,
2168, 2196, 2558, 3272, 3574, 4048, 4124, 4125, 4240, 4243
Portugal Poultry 57, 117, 429, 2451 267
Switzerland Poultry meat 38, 1564 268
Switzerland Poultry 3, 9, 61, 527, 530, 535, 539
Austria Wild bird (rook) 224 60
U.S. Poultry meat 131 269
Brazil Poultry 453, 457, 1706 270
China Pig, poultry 10, 48, 69, 101, 155, 156, 354, 359, 362, 457, 648, 1114, 1431, 271
2294, 2690, 3014, 3244, 3245, 3269, 3376, 3402, 3403, 3404
Japan Cattle 1284, 2438 272
Japan Dog 10, 354, 493, 648, 3557 273
Tunisia Poultry 117, 155, 2197 274
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TABLE 3 Examples of acquired carbapenemase genes in E. coli of animal origin from Europe, North and South America,
Africa, Australia, and Asia
Carbapenemase
gene Geographical origin Source Sequence types Reference
blaNDM-1 China, U.S. Dog, cat, pig 167, 1695, 1585, 1721, 359 70, 275, 276
blaNDM-5 China, Algeria, India Dog, pig, cow, duck 48, 54, 90, 156, 165, 167, 410, 648, 1114, 1178, 74, 75, 277–279
1234, 1437, 2439, 3331, 4429, 4463, 4656
blaVIM-1 Germany Seafood, pig 10, 88 67, 68, 280, 281
blaIMP-4 Australia Silver gull 48, 58, 167, 189, 216, 224, 345, 354, 541, 542, 744, 76
746, 1114, 1139, 1178, 1421, 2178, 4657, 4658,
blaOXA-48 Germany, U.S., France, Dog, cat, chicken 38, 372, 648, 1196, 1431 77–79, 261
Lebanon, Algeria
blaOXA-181 Italy Pig 359, 641 80
blaKPC-2 Brazil Dog 648 287
tified in the United States and in China, in isolates re- conversely, this epidemiology just reflects the conse-
covered from dogs, cats, and pigs (70, 71). NDM-5 has quence of a higher prevalence in humans that may
been detected in China, India, and Algeria, from cattle, eventually target animals through an environmental
poultry, dogs, cats, and fish (72–75). The gene encoding dissemination. Since the occurrence of carbapenemase-
IMP-4 has been identified in E. coli isolates recovered producing Enterobacteriaceae in animals is marginal, it
from silver gulls in Australia (76). Interestingly, the therefore does not correspond to a significant threat to
OXA-48 carbapenemase, which is the most prevalent human medicine (65).
carbapenemase in human enterobacterial isolates in
Europe, has been found in E. coli isolates recovered from
dogs, cats, and chickens in Germany, France, Lebanon, RESISTANCE TO QUINOLONES
Algeria, and the United States (37, 77–79). Finally, the AND FLUOROQUINOLONES
OXA-181 enzyme, which is a variant of OXA-48 in- Quinolones and fluoroquinolones are important anti-
creasingly reported in humans, has recently been iden- microbial agents for treating various types of infections
tified in animals as well, being found in clonally in both humans and animals. They are known to be
unrelated E. coli isolates recovered from pigs in Italy bactericidal against virtually all bacteria. Resistance to
(80). Even though the class A β-lactamase KPC is one these antimicrobial agents is usually due to mutations in
of the most commonly identified carbapenemases in the drug targets, namely, the genes for DNA gyrase and
human isolates in some parts of the world, including in topoisomerase IV, but other mechanisms such as re-
North America, China, and some European countries duced permeability of the outer membrane, protection of
(Italy, Greece, Poland), it has not yet been identified in the target structures, or upregulated efflux pumps may
animal E. coli isolates so far (81, 82), except for a single also play a role (83).
blaKPC-2-carrying isolate from a dog in Brazil that suf-
fered from a urinary tract infection (287). Resistance to (Fluoro)Quinolones by
Overall, and notably, the different carbapenemase Chromosomal Target Site Mutations
genes that have been identified among animals in dif- The primary target of (fluoro)quinolones in E. coli is
ferent countries reflect the types of carbapenemases the gyrase, which consists of two GyrA subunits and
known to be the most prevalent in human isolates in two GyrB subunits. Topoisomerase IV constitutes a sec-
those countries. Considering that carbapenems are not ondary target in Gram-negative bacteria. This enzyme
used in veterinary medicine, it remains to be determined consists of two ParC and two ParE subunits. Most
which antimicrobial selective pressure is responsible for mutations were found within the quinolone resistance-
the selection of such carbapenemase producers in ani- determining region, which is between Ala67 and Gln107
mals. Penicillins, however, are excellent substrates for in GyrA, and most frequently mutations occur at codons
any kind of β-lactamases, including carbapenemases, 83 and 87 (83). Single mutations in the gene gyrA may
and therefore their use might correspond to a selective confer resistance to quinolones, but for resistance to
pressure anyhow. In addition, it remains to be evaluated fluoroquinolones, further mutations within gyrA and/or
whether animals may act as potential sources of trans- parC are needed. Most parC mutations occur at codons
mission of those resistance traits toward humans or if, 80 and 84 (83). In clinical E. coli isolates from com-
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Poirel et al.
panion animals, different combinations of mutations plasmids belonging to the IncF family (100). The gene
were detected at codons 83 and 87 in gyrA and at qepA was identified in E. coli of companion animal or-
codons 80 and 84 in parC (84, 85). Mutations within igin belonging to different STs (97). Plasmids of the IncF
gyrA and parC were also described in E. coli isolates family harbored qepA in E. coli from food-producing
originating from diseased food-producing animals and companion animals (101). The PMQR gene oqxAB
(86, 87). was identified in unrelated E. coli isolates from food-
producing animals and located on different plasmids
Resistance to (Fluoro)Quinolones by belonging to the IncF and IncHI2 families (102). The
Plasmid-Borne Resistance Mechanisms case of OqxAB is peculiar since this resistance determi-
Since the identification of the first plasmid-mediated nant confers reduced susceptibility not only to quino-
quinolone resistance (PMQR) determinant, qnrA1, in lones (such as flumequine), but also to other drugs such
1997, there is serious concern about the global dis- as trimethoprim and chloramphenicol that are also used
semination of PMQR genes (88, 89). Several plasmid- in veterinary medicine. Therefore, this resistance deter-
encoded resistance mechanisms have been identified, minant encompasses different families of antimicrobial
including (i) Qnr-like proteins (QnrA, QnrB, QnrC, agents to which resistance (or reduced susceptibility) can
QnrD, and QnrS) which protect DNA from quinolone be coselected (103).
binding, (ii) the AAC(6′)-Ib-cr acetyltransferase that
modifies certain fluoroquinolones such as ciprofloxacin
and enrofloxacin, and (iii) active efflux pumps (QepA RESISTANCE TO AMINOGLYCOSIDES
and OqxAB). Overall, these resistance determinants Aminoglycosides are drugs of natural origins whose
do not confer a high level of resistance to quinolones (or producers can be found in the genus Streptomyces (104,
fluoroquinolones), but rather, confer reduced suscepti- 105) and Micromonospora, and they are often used
bility to those antimicrobial agents. However, they in combination with another antimicrobial (mostly a
might contribute to the selection of isolates exhibiting β-lactam) to exploit their rapid bactericidal action for
higher levels of resistance through additional chromo- treating complicated infections such as sepsis, pneumo-
somally encoded mechanisms (89). nia, meningitis, and urinary tract/abdominal infections,
PMQRs have been identified widely among human both in humans and animals, including food-producing
isolates but also among animal isolates. Especially in animals and companion animals (106). The most fre-
China, numerous studies have shown high prevalences quently used molecules in veterinary medicine are
of Qnr, AAC(6′)-Ib-cr, and QepA determinants among neomycin and derivatives of streptomycin. Gentamicin,
food-producing animals (86, 90), and some studies kanamycin, and paromomycin are used as well. Amikacin
highlighted an increased prevalence through the years is reserved for the treatment of infections in pets and
(91). A Europe-wide retrospective study identified the horses (106).
genes qnrS1 and qnrB19 in E. coli isolates from food- Aminoglycosides affect a broad spectrum of patho-
producing animals, namely, poultry, cattle, and pigs gens among Gram-negative and -positive bacterial spe-
(92). PMQRs were detected not only in food-producing cies, interfering with translation (107). Two major issues
animals, but also in companion animals. In E. coli iso- could limit the therapeutic power of these important
lates from diseased companion animals, the genes qnrS1, molecules: the first is linked to their toxicity. Never-
qnrB1, qnrB4, and qnrB10 were identified (84). The theless, this issue is managed by opportune therapeutic
gene qnrB19 was described in equine E. coli isolates regimens based on recent advances in the understanding
(93, 94). The replicon types often associated with plas- of aminoglycoside pharmacodynamics (108). The sec-
mids that carried the PMQR genes qnrS1 and qnrB19 ond issue is the emergence of bacterial resistance linked
are IncN and IncX but also include several others (47, to the usage of aminoglycosides, which has disseminated
94, 95). globally. The following subsections provide an overview
In E. coli belonging to several STs of companion an- of mechanisms of resistance toward aminoglycosides
imal origin, the gene aac(6′)Ib-cr was identified (96–99). and their epidemiology in E. coli of animal origin.
This gene was located on plasmids of the IncF family,
and a blaCTX-M ESBL gene, usually blaCTX-M-15, was Resistance to Aminoglycosides
often colocated (96, 98). Furthermore, aac(6′)Ib-cr was by Target Modifications
described in E. coli isolates from the feces of French Resistance to aminoglycosides can develop by target
cattle, where it was also colocated with blaCTX-M-15 on mutations involving the 16S RNA and/or the S5 and
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S12 ribosomal proteins (107, 109, 110). However, this isolate was multidrug-resistant, notably harboring the
strategy is successful in conferring high-level resistance blaCMY-2, blaOXA-181, and mcr-1 genes (80). Recently,
only in bacterial species with a limited number of copies two E. coli isolates producing RmtB were reported from
of 16S RNA encoding operons. E. coli harbors seven diseased bovines in France. The gene colocalized on an
copies of such operons, making the establishment of IncF33:A1:B1 plasmid with blaCTX-M-55 and in one
aminoglycoside resistance by point mutations rather isolate also with the fosA3 gene (124). The RmtD vari-
improbable. ant has been found less frequently. Other than the report
Modification of the target site of aminoglycosides from Yang et al. (123), another recent report has been
can be achieved also by methylation of residues G1405 published from Brazil, on one E. coli isolate from a dis-
and A1408 of site A of the 16S RNA, resulting in high- eased horse producing RmtD and harboring the blaCTX-
level resistance to amikacin, tobramycin, gentamicin, M-15 and aac(6′)-Ib-cr genes (125). The RmtE methylase
and netilmicin (109). The 16S RNA methylases, includ- was reported for the first time from commensal E. coli
ing ArmA, RmtA/B/C/D/E/F/G/H, and NmpA, originated isolates from healthy calves in the United States (126).
from natural aminoglycoside producers as self-defense Later, two E. coli isolates were identified as RmtE pro-
against antimicrobial production (104). The first detec- ducers in diseased food-producing animals in China,
tion of ArmA dates back to 2003, when Galimand from 2002 to 2012 (127). Reports on RmtA are also
and colleagues reported the enzyme in a Klebsiella quite infrequent, with a recent one from Zou et al., who
pneumoniae isolate from a human and the respective found a frequency of 10% of rmtA gene occurrence
gene on a conjugative plasmid (111). Since then, the among 89 E. coli isolates from giant pandas in China
armA gene has been reported in several enterobacteria, (128). To the best of our knowledge, RmtF/G/H en-
Acinetobacter baumannii, and Pseudomonas aeruginosa zymes have not yet emerged in E. coli, and NmpA has
isolates (112–116). The dissemination of the armA gene never been reported from animals. Overall, it can be
is favored by its location on the composite transposon stated that methylases have not widely disseminated
Tn1548, which also carries genes coding for sulfonamide since their discovery, probably for reasons related to
resistance, which in turn is located on self-transmissible fitness (129, 130). An exception is in China, where
plasmids belonging to several incompatibility groups probably the antimicrobial usage, not only relative to
(117). Emergence of ArmA in E. coli from animals was aminoglycosides, may play a role in the emergence
reported in 2005 in Spain in one pig (118), whereas the and dissemination of these enzymes. On the contrary,
first report of E. coli producing RmtB was in 2007 in aminoglycoside-modifying enzymes have disseminated
China by Chen and co-workers who reported a preva- globally, and an overview of those most frequently en-
lence of 32% (n = 49/152) among healthy pigs in farms countered in animals is provided in the next subsection.
(119). In an investigation conducted in China in 2008,
Du et al. reported the presence of ArmA and RmtB in Resistance to Aminoglycosides
E. coli from diseased poultry, with an occurrence of 10% by Enzymatic Inactivation
(n = 12/120) (120). Later, Liu et al. reported the presence The inactivation of aminoglycosides is conducted by
of E. coli ArmA and RmtB producers among various enzymes which modify the molecules so that they become
food-producing animals in 2009 to 2010, with an oc- unable to reach or bind to the target site. Currently, three
currence of 1.27% and 11.5% for ArmA and RmtB, types of aminoglycoside-modifying enzymes are known,
respectively (n = 2 and 18/157) (121). RmtB was found in and according to the modifying group that is linked to the
E. coli isolates associated with bovine mastitis in China in aminoglycosides, they are classified as acetyltransferases,
2013 to 2014, with an occurrence of 5.3% (n = 13/245) nucleotidyltransferases, and phosphotransferases.
(122). Yang and colleagues reported the presence of E. The aminoglycoside acetyltransferases catalyze the
coli producing RmtD in diseased chickens in 2012 to addition of an acetyl group (CH3CO) to an amine group
2014 in China. The enzyme co-occurred with RmtB with (–NH2) at positions 1, 2, 3, or 6 of the aminoglycoside
a prevalence of 8.3% (n = 3/36). In the same study, other structure, which determines the subgroup of the enzyme
methylases were found, namely, RmtB together with (131). For each enzyme, several variants have been re-
ArmA in 8.3% of isolates (n = 3/36), RmtB alone in ported, and they are usually defined by a roman number.
72.2% of isolates (n = 26/36), and ArmA in 11.1% of AAC(3)-II/IV and AAC(6)-Ib are the most frequently
isolates (n = 4/36) (123). encountered acetyltransferases among E. coli of human
More recently, a scattered porcine E. coli isolate and animal origins. They have been globally reported
harboring the armA gene was detected in Italy. The from several hosts (128, 132–140).
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Poirel et al.
Among aminoglycosides, the nucleotidyltransferases ESBL genes (blaCTX-M-55, blaCTX-M-15, or blaCTX-M-123)

ANT(2″) and ANT(3″) are most commonly found in on plasmids of 78 to 138 kb in size. In a recent French
Gram-negative bacteria. ANT(2″) and ANT(3″) are study, the emergence of plasmids carrying multiple re-
encoded by the genes aadB and aadA, respectively (131), sistance determinants including fosA3, blaCTX-M-55,
which are both frequently located on gene cassettes in rmtB, and mcr-1 was reported in various animal species
class 1 integrons. These genes have also spread globally, (124). In that study, it was speculated that this plasmid
and they have been found in E. coli from animals in- could have an Asian origin since blaCTX-M-55 is the sec-
cluding pets, wild animals, and food-producing animals ond most prevalent ESBL gene in that part of the world.
(134, 141–148). In 2013, the complete sequence of the 76,878-bp plas-
Among the aminoglycoside phosphotransferases, mid pHN7A8 from a dog in China was determined. This
APH(6)-Ia and APH(6)-Id encoded by the strA and strB plasmid represents a F33:A–:B–-type epidemic plasmid
genes, respectively, are most commonly encountered in that carried the resistance genes blaCTX-M-65, fosA3, and
E. coli worldwide. They mediate resistance to strepto- rmtB (166). Plasmids with similar fosA3 regions were
mycin and are frequently associated with a unique mo- reported from E. coli isolates of pig (167), duck (168),
bile element, sometimes together with the aph(3″)-I/II and chicken origin (169). The widespread occurrence
genes mediating kanamycin resistance. These resistance of the fosA3 gene in China was demonstrated in a study
mechanisms have been found in several hosts including that identified 12/892 E. coli isolates as fosA3-positive.
wild rabbits (145), cattle (149–152), poultry (153, 154), These isolates originated from pigs, chickens, ducks, a
and swine (155–157). goose, and a pigeon (170). Furthermore, the analysis of
1,693 E. coli isolates from various animal species iden-
tified 97 fosA3-positive isolates from beef cattle, pigs,
RESISTANCE TO FOSFOMYCIN broiler chickens, stray cats, stray dogs, and wild rodents
Fosfomycin inhibits the MurA enzyme, which is in- in China (171). Recently, several epidemic fosA3-
volved in peptidoglycan synthesis. The use of fosfo- carrying multiresistance plasmids of diverse incompati-
mycin in veterinary medicine is limited to the treatment bility groups have been identified to be disseminated
of infections caused by a number of Gram-positive and among E. coli from pigs, dairy cattle, and chickens in
Gram-negative pathogens, including E. coli, mainly in northeast China (162). Some of these plasmids have been
piglets and broiler chickens (158, 159). Two major fos- sequenced completely, including the plasmids pECM13
fomycin resistance mechanisms have been described: from cattle (113,006 bp, IncI1, and coharboring blaCTX-
(i) mutations in the glpT and uhpA/T genes encoding M-14, rmtB, aadA2, and blaTEM-1), pECB11 from chicken
proteins involved in the fosfomycin uptake system and [92,545 bp, F33:A–:B–, and coharboring blaCTX-M-55,
(ii) the acquisition of fosfomycin-modifying enzymes floR, cfr, blaTEM-1, tet(A), strA, and strB], and pECF12
such as the metalloenzymes FosA, FosB, and FosX or from chicken [77,822 bp, F33:A–:B–, and coharboring
the kinases FomA and FomB (160). Most of the fos-like blaCTX-M-3, rmtB, tet(A), strA, and strB]. E. coli isolates
genes are plasmid-borne, and plasmids carrying the fos from pigs harboring the fosA3 gene were also detected in
genes commonly carry additional resistance genes (124, Taiwan (172).
161, 162) that increase the risk of coselection of fosfo-
mycin resistance under the selective pressure by other
antimicrobial agents. RESISTANCE TO TETRACYCLINES
A considerable number of studies report acquired Tetracyclines are widely used in veterinary medicine.
fosfomycin resistance among E. coli of animal origin. A summary of sales data in the 25 European Union
Isolates carrying the plasmid-mediated fosA gene have and European Economic Area countries revealed that
been reported from companion animals. The first cases tetracyclines accounted for 37% of the total sales of
were reported in China in 2012 and 2013 from dogs and veterinary antimicrobial agents, followed by penicillins
cats (163). Another study described a high prevalence (23%) (173). As a consequence of the selective pressure
of FosA3-producing E. coli in pets and their owners, imposed by the widespread use of tetracyclines, many
highlighting the transmission of fosfomycin-resistant bacteria—including E. coli—have developed tetracy-
E. coli isolates between humans and animals (164). cline resistance. According to the tetracycline resistance
Another Chinese study described the fosA3 gene in gene nomenclature center (https://faculty.washington
E. coli from fresh pork and chicken meat (165). In that .edu/marilynr/), nine tetracycline efflux genes [tet(A),
study, the fosA3 gene was often found together with tet(B), tet(C), tet(D), tet(E), tet(G), tet(J), tet(L), and
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tet(Y)], two tetracycline resistance genes encoding ribo- tet(E) + tet(M) + tet(A) + tet(B) + tet(C) (n = 1) (180). In
some protective proteins [tet(M) and tet(W)], and one 33 E. coli isolates from cases of septicemia among laying
gene coding for an oxidoreductase that inactivates tet- hens in Switzerland, the genes tet(A) and tet(B) were
racyclines [tet(X)] have been identified in E. coli. The found in 21 and 10 isolates, respectively, while two
major mechanisms of tetracycline resistance encoun- isolates carried neither tet(A), tet(B), nor tet(C) (177). In
tered in E. coli of animal origin include (i) the active the same study, the genes tet(A) and tet(B) were detected
efflux by proteins of the major facilitator superfamily in eight and nine E. coli isolates from urinary tract
and (ii) ribosome protection. A PubMed search for tet- infections in dogs and cats, respectively. The same two
racycline resistance genes in E. coli of animal origin tet genes were also found in E. coli isolates from healthy
revealed that not all of these 12 tet genes occur in E. coli dogs and cats in Spain (181). A large-scale study of tet
from animal sources. The following examples provide genes in 325 nonclinical E. coli isolates from various
an overview of the distribution of tet genes among E. coli animal sources in the United States identified the gene tet
from various animal sources. (B) in isolates from a goose, a duck, and a deer; the genes
Among 155 E. coli isolates from fecal samples of tet(A) and tet(B) in isolates from turkeys, cats, goats, and
cattle in Korea, the genes tet(A), tet(B), and tet(C) were cows; tet(A), tet(B), and tet(C) in isolates from dogs,
detected in 72, 70, and nine isolates, respectively. Two sheep, and horses; and tet(A), tet(B), tet(C), and tet(M)
isolates each carried tet(A) + tet(B) or tet(B) + tet(C) in isolates from pigs and chickens (182). However, in
(174). In 99 E. coli isolates from bovine mastitis in the that study neither tet(E) nor tet(G), tet(L), or tet(X) were
United States collected from 1985 to 1987 and in 2009, detected in the 325 E. coli isolates. Among 58 tetracy-
the genes tet(A), tet(B), and tet(C) were detected, with cline-resistant E. coli isolates from giant pandas, the
tet(C) being present in more than half of the investigated genes tet(A), tet(E), and/or tet(C) were detected in 33, 24,
isolates in each of the two time periods (175). Of 129 and four isolates, respectively (128).
E. coli isolates from cases of bovine mastitis in the These examples show that different tet genes—alone
United States, 68 carried the gene tet(C), while another or in combination with others—occur at different fre-
14 isolates harbored tet(C) + tet(A) (176). A study in quencies in E. coli isolates from different animal sources
Switzerland identified the genes tet(A), tet(B), and tet(A) and/or geographic regions. In general, the genes tet(A)
+ tet(B) in 24, 16, and two E. coli isolates from bovine and tet(B) were the most prevalent tetracycline resistance
mastitis (177). In the same study, the genes tet(A), tet(B), genes in E. coli of animal origin. Both of these genes
tet(C), and tet(A) + tet(B) were detected in 60, five, one, are part of small nonconjugative transposons, Tn1721
and two E. coli isolates, respectively, from diarrhea and [tet(A)] (183) and Tn10 [tet(B)] (184), which are often
enterotoxemia in pigs (177). In 99 tetracycline-resistant integrated into conjugative and nonconjugative plas-
E. coli isolates from pigs in Spain, the genes tet(A) (n = mids. Several of the aforementioned examples revealed
46), tet(B) (n = 12), and tet(A) + tet(B) (n = 28) but also the presence of more than a single tet gene in the same
tet(A) + tet(M) (n = 11) and tet(A) + tet(B) + tet(M) (n = isolate. This might be explained by the observation
2) were detected (178). The tet(M) gene was shown by that several tet genes are frequently found on plasmids
Southern blot hybridization to be located on plasmids. or other mobile genetic elements which may have been
In a study in Germany, either the genes tet(A) (n = 71), acquired by the respective E. coli isolates at different
tet(B) (n = 46), and tet(C) (n = 3) alone or the times and under different conditions. When other resis-
combinations of the genes tet(A) + tet(B) (n = 2), tet(A) + tance genes are colocated with a tet gene on the same
tet(C) (n = 2), tet(A) + tet(D) (n = 3), tet(A) + tet(M) (n = plasmid, such a plasmid can be acquired under the se-
1), tet(B) + tet(M) (n = 2), tet(B) + tet(C) (n = 2), and tet lective pressure imposed by the use of antimicrobial
(B) + tet(D) + tet(M) (n = 1) were detected in E. coli from agents other than tetracyclines. Multidrug resistance
pigs (179). Among 283 tetracycline-resistant extra-in- plasmids that also carry tet genes have been detected in
testinal pathogenic E. coli isolates from pigs in China, E. coli from bovine mastitis in Germany. Here, the gene
the genes tet(A) (n = 68), tet(B) (n = 141), tet(C) (n = 3), tet(A) was located on IncHI2/IncP plasmids of ca. 225 kb,
tet(D) (n = 1), and tet(G) (n = 108) were identified (156). which also harbored the resistance genes blaCTX-M-2,
A wide variety of tet genes was also seen among 73 blaTEM-1, sul1, sul2, dfrA1, and aadA1 (14). IncI1 plas-
tetracycline-resistant E. coli isolates from broilers in mids that range in size from 90 to 120 kb and carry the
Iran, including the gene tet(E) alone (n = 1) or in the resistance gene tet(A) along with the genes blaSHV-12,
combinations tet(E) + tet(C) (n = 4), tet(E) + tet(D) + tet aadA1, cmlA1, and aadA2 or the genes blaSHV-12, qacG,
(M) (n = 2), tet(E) + tet(D) + tet(A) + tet(G) (n = 3), and and aadA6 were identified in E. coli isolates from wild
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Poirel et al.
birds, dogs, and poultry in Spain or Germany (39). In Among 102 E. coli isolates from pigs in China, 91
canine E. coli isolates from Brazil, several multiresis- (89%) were resistant to chloramphenicol. The genes
tance plasmids were identified. These included (i) a ca. catA1 and catA2 but also the cassette-borne gene cmlA
250-kb IncFIB/IncHI2 plasmid that carried the gene were detected in 58%, 49%, and 65%, respectively, of
tet(B) together with the resistance genes blaCTX-M-2, the chloramphenicol-resistant isolates. In addition, the
sul1, aadA29, strA, and strB; (ii) a ca. 240-kb IncFIC gene floR was detected in 57% of the florfenicol-resistant
plasmid that harbored the tet(A) gene together with the isolates and in 52% of chloramphenicol-resistant iso-
resistance genes blaCMY-2, cmlA, floR, strA, strB, sul1, lates (188). In a study of 318 ETEC, non-ETEC from
sul3, and aadA7; (iii) a 240-kb IncHI2 plasmid with cases of diarrhea, and commensal E. coli isolates from
the resistance genes blaCTX-M-2, sul1, aadA29, strA, and healthy pigs in Canada, the genes catA1, cmlA, and floR
strB; and (iv) a 40-kb IncFIB/IncN plasmid with the were detected among the chloramphenicol-resistant iso-
resistance genes tet(A), sul1, dfrA16, and dfrA29 (185). lates. The gene catA1 was significantly more frequent in
Lastly, an 81-kb plasmid that carried the resistance ETEC than in non-ETEC and commensal E. coli (189).
genes qnrS1, blaCTX-M-14, blaTEM-1, floR, and tet(A) was The genes floR and cmlA were detected among 48 E. coli
found in an E. coli isolate from a pig in China (186). isolates from calves with diarrhea. Of the 44 isolates for
These few examples illustrate that tet gene-carrying which florfenicol MICs were ≥16 mg/liter, 42 carried the
multiresistance plasmids occur in E. coli of different floR gene. Twelve E. coli isolates were positive for cmlA,
animal species in different parts of the world. Given the and their corresponding chloramphenicol MICs were
widespread use of tetracyclines in veterinary medicine, ≥32 mg/liter. In addition, eight isolates were positive for
such plasmids not only facilitate the dissemination of floR and cmlA, and their florfenicol and chlorampheni-
certain tet genes, but also support the coselection and col MICs were ≥64 mg/liter (190). In a study of antimi-
persistence of other resistance genes. crobial resistance in German E. coli isolates from cattle,
pigs, and poultry, not further specified catA genes were
found in seven isolates from cattle and six isolates each
RESISTANCE TO PHENICOLS from pigs and poultry. Moreover, cmlA1-like genes were
Phenicols are broad-spectrum antimicrobial agents of detected in a single isolate from cattle, six isolates from
which nonfluorinated (e.g., chloramphenicol) and fluo- pigs, and three isolates from poultry. The floR gene was
rinated (e.g., florfenicol) derivatives are used in veteri- not detected (191). Among 116 avian-pathogenic E. coli
nary medicine. Due to its toxicity and important adverse isolates from chickens in Egypt, 98 (84.5%) were resis-
effects in humans, such as dose-unrelated irreversible tant to chloramphenicol. The resistance genes catA1,
aplastic anemia, dose-related reversible bone marrow catA2, and cmlA were found in 86, four, and eight
suppression, and Gray syndrome in neonates, chloram- isolates, respectively, while the genes catA3 and cmlB
phenicol and its derivatives thiamphenicol and azidam- were not detected (192). Among 102 chloramphenicol-
fenicol were banned in 1994 in the European Union resistant E. coli isolates from horses in the UK, 75 har-
from use in food-producing animals (187). Currently, bored the gene catA1. The remaining 27 isolates were
the use of nonfluorinated phenicols in animals is limited PCR negative for the genes catA2, catA3, and cmlA,
to the treatment of companion animals and pets. How- while the presence of the genes floR and cfr was not
ever, the fluorinated derivative florfenicol is licensed for tested (193). The cassette-borne chloramphenicol resis-
the treatment of bacterial infections in food-producing tance genes catB3 and cmlA6 were identified in four and
animals (187). two canine E. coli isolates, respectively, all from the
Phenicol resistance in E. coli of animal origin is me- United States. The gene catB3 was located together with
diated by three major mechanisms: (i) enzymatic inac- the resistance genes aacA4 and dfrA1, and the gene
tivation of nonfluorinated phenicols by chloramphenicol cmlA6 was located together with the genes aadB and
acetyltransferases encoded by cat genes, (ii) active efflux aadA1 in class 1 integrons of different sizes (194). In a
of nonfluorinated phenicols (cmlA genes) or fluorinated study of 62 E. coli isolates from dogs in Iran, three
and nonfluorinated phenicols (floR genes) by major facil- isolates harbored the cmlA gene, whereas six isolates
itator superfamily proteins, and (iii) target site methylation were positive for the floR gene (195). Among 36 chlor-
by an rRNA methylase encoded by the multiresistance amphenicol- and florfenicol-resistant E. coli isolates
gene cfr, which confers resistance to five classes of anti- from dogs suffering from urinary tract infections in
microbial agents, including fluorinated and nonfluorinated Taiwan, all isolates harbored the cmlA gene and 18
phenicols (187). carried the floR gene (196). The cmlA gene was also
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detected in two chloramphenicol-resistant E. coli isolates China, the cfr gene was detected on plasmids of ca. 30 kb
from fecal samples of free-range Iberian lynx (143). Of in E. coli isolates from pigs (204). The complete se-
89 E. coli isolates from giant pandas, 28 and 23 were quence of the 37,672-bp plasmid pSD11, again from
resistant to chloramphenicol and florfenicol, respective- E. coli of porcine origin in China, was reported by Sun
ly. The floR gene was detected in 23 isolates and the and colleagues (205). The colocation of cfr with the
cmlA gene in nine isolates, with two isolates carrying ESBL gene blaCTX-M-14b on the 41,646-bp plasmid
both genes. The cfr gene was not detected in any of the pGXEC3 from a porcine E. coli isolate was reported in
isolates, and cat genes were not tested (128). The genes 2015 (206). In the same year, another cfr-carrying
catA1 and cmlA were also detected in two and one plasmid, the conjugative 33,885-bp plasmid pFSEC-01,
multiresistant E. coli isolates, respectively, from shellfish was reported (207). Although this plasmid was found in
in Vietnam (197). a porcine E. coli isolate, it closely resembled in its struc-
The genes catA1, cmlA, and floR are often found on ture the plasmid pEA3 from the plant pathogen Erwinia
plasmids. In bovine E. coli from the United States, the amylovora. Most recently, another six cfr-carrying
floR gene was located on large plasmids of 225 kb (190), E. coli isolates—five from pigs and one from a chicken—
which were larger than those found in E. coli from sick were identified. In all cases, the cfr gene was located as
chickens (198). Southern blot analysis confirmed the the only resistance gene on plasmids of either 37 or 67 kb.
presence of the cmlA gene on plasmids of >100 kb in Two of these plasmids were completely sequenced: the
E. coli from pigs (199). Conjugation assays identified 37,663-bp IncX4 plasmid pEC14cfr and the 67,077-bp
two distinct class 1 integrons that linked cmlA to the F14: A–: B– plasmid pEC29cfr (161).
streptomycin/spectinomycin resistance genes aadA1 and
aadA2 and to the sulfonamide resistance genes sul1 or
sul3 (199). Transformation experiments conducted with RESISTANCE TO SULFONAMIDES
Canadian E. coli from pigs revealed that aadA and sul1 AND TRIMETHOPRIM
were located together with catA1 on a large ETEC plas- Sulfonamides and trimethoprim are synthetic antimi-
mid (189). Plasmids that harbored the gene cmlA also crobial agents that inhibit different steps in the folic
carried the resistance genes aadA and sul3. Moreover, acid synthesis pathway. Each of these agents acts in a
plasmids that harbored the genes aadB and floR also bacteriostatic manner, whereas the combination of a
carried sul2, tet(A), blaCMY-2, strA, and strB but occa- sulfonamide with trimethoprim results in synergistic
sionally also aac(3)-IV (189). Among Brazilian E. coli bactericidal actions on susceptible organisms; as such,
from dogs, a 35-kb IncF/IncFIB plasmid was identified the combination is referred to as a “potentiated” sul-
that harbored the genes strA and strB, and an unusual fonamide. Sulfonamides and trimethoprim have been
class 1 integron with the genes dfrA12, aadA2, cmlA1, used for decades in animals and humans. Acquired re-
and aadA1 linked to a sul3 gene (185). The ca. 35-kb sistance mechanisms have been frequently identified,
plasmid pMBSF1 from porcine E. coli in Germany car- mainly due to (i) mutational modifications in the genes
ried the floR gene together with the genes strA and strB encoding the target enzymes, namely, the dihydroptero-
(200). The floR gene was also detected on conjugative ate synthase or dihydrofolate reductase, respectively, or
plasmids ranging in size from 110 to 125 kb from bovine (ii) the acquisition of sul genes encoding dihydropteorate
E. coli in France. All these plasmids mediated additional synthetases that are insensitive to sulfonamides or dfr
resistances to sulfonamides, streptomycin, ampicillin, genes encoding dihydrofolate reductases that are insen-
and/or trimethoprim (201). These examples show that sitive to trimethoprim (208).
phenicol resistance genes can also be coselected under
the selective pressure imposed by nonphenicol antimi- Resistance to Sulfonamides
crobial agents. In E. coli from food-producing and companion ani-
The multiresistance gene cfr—originally identified in mals, sulfonamide resistance is mediated by any of the
staphylococci of animal origin—was also found to be following three sul genes: sul1, sul2, or sul3. The sul1
functionally active in E. coli (202). The gene cfr was first gene is particularly widespread because it is part of
reported in E. coli from a nasal swab of a pig in China the 3′-conserved segment of class 1 integrons (209). As
(203). Later, it was identified on the 135,615-bp IncA/C such, the sul1 gene is often found together with other
multiresistance plasmid pSCEC2 from a pig in China. antimicrobial resistance genes that are located on gene
This plasmid also harbored the resistance genes sul2, cassettes in the variable part of class 1 integrons (209).
tet(A), floR, strA, and strB (157). In another study in Class 1 integrons are present in E. coli from healthy and
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Poirel et al.
diseased food-producing animals, companion animals, dfrA12) (210), horses (dfrA1, dfrA9, dfrA12, dfrA17)
and wildlife all over the world as illustrated in the fol- (193, 210), pigs (dfrA1, dfrA5, dfrA8, dfrA12, dfrA13,
lowing examples. In Germany, 58 of 417 E. coli isolates dfrA14, dfrA16, dfrA17) (144, 156, 210, 228, 229),
from diseased swine, horses, dogs, and cats, collected in cattle (dfrA1, dfrA8, dfrA12, dfrA17) (14, 215, 229),
the BfT-GermVet monitoring study, harbored class 1 chickens (dfrA1, dfrA5, dfrA12, dfrA14, dfrA16) (144,
integrons (210). Other studies identified class 1 229), and giant pandas (dfrA1, dfrA7, dfrA12, dfrA17)
integrons in E. coli from healthy and diseased dogs (128). In contrast to dfrA genes, dfrB genes have rarely
in Brazil (185), in clinical avian E. coli isolates in the been detected in E. coli from animals. A dfrB4 gene and
United States (211), in E. coli from lizards in Indonesia a dfrA17 gene were detected in class 1 integrons from
(212), in Shiga toxin-producing E. coli from cattle in the sea lions (230). In the study by Seputiené et al. (229), the
United States (213), in E. coli from free-range reindeer in dfrA8 gene was located in neither class 1 nor in class
Norway (214), in calf-pathogenic E. coli in China (215), 2 integrons. Moreover, only seven of the 13 dfrA14
in E. coli from pigs in Denmark (216), and even in E. coli genes in E. coli isolates of animal origin were integron-
from giant pandas in China (128). Class 1 integrons associated. In previous studies of E. coli from food-
including the sul1 gene are often located on plasmids, producing animals, a functionally active dfrA14 gene
including ESBL-gene-carrying multiresistance plasmids was found outside an integron but inserted into a
(14, 216–218). plasmid-borne strA gene (220, 231).
The gene sul2 is also widely disseminated among
E. coli of various animal species in different parts of the
world. It has been found in E. coli from pigs in Canada RESISTANCE TO POLYMYXINS
(219) and Denmark (216), in food-producing animals in Colistin (also known as polymyxin E) is a polypeptide
Kenya (220), in poultry in Nigeria (221) and Germany antimicrobial agent that targets the LPS in the outer
(222), and in horses in the Czech Republic (93). The sul2 membrane of Gram-negative bacteria (232). Colistin
gene is often linked to the streptomycin resistance genes is widely used in veterinary medicine, mainly for the
strA-strB. Similarly to sul1, the sul2 gene is commonly treatment or prevention of intestinal infections, partic-
found on plasmids that also harbor other antimicrobial ularly neonatal and postweaning diarrhea in pigs and
resistance genes (93, 157, 220, 221, 223). intestinal infections in poultry and cattle (233). Very
The gene sul3 was first described in 2003 in E. coli recently, due to the considerable concerns that colistin
isolates from pigs in Switzerland (224). Since then, this resistance might be transferable from animals to hu-
gene has been identified mostly on plasmids in E. coli mans, specific regulations on the use of colistin have
from pigs in the United States (199), Canada (219), and been set up in Europe under the umbrella of the Euro-
Denmark (216); from poultry in Germany (222); and pean Medicines Agency (234). In April 2017, a ban of
from dogs in Spain (138) and Brazil (185). Several re- colistin as a growth promoter also became effective in
ports described the sul3 gene to be linked to other re- China (235). Colistin is active against various species
sistance genes, such as the macrolide resistance gene of Enterobacteriaceae, including E. coli, whereas others
mef(B) (225), and to unusual class 1 integrons (39, 185, such as Proteus spp. and Serratia spp. are intrinsically
199, 226). resistant (232). Resistance to colistin can be due to mu-
tations in chromosomal genes or to acquired resistance
Resistance to Trimethoprim genes.
Numerous dfr genes that confer trimethoprim resistance
have been detected in Enterobacteriaceae and other Chromosome-Encoded Polymyxin Resistance
Gram-negative bacteria. Based on their sizes and struc- Polymyxin resistance in E. coli isolates may be related
tures, they have been divided into two major groups, to genes encoding LPS-modifying enzymes. The operon
dfrA and dfrB (227). The dfrA genes code for proteins of pmrCAB codes for three proteins, namely, a phospho-
152 to 189 amino acids, while the dfrB-encoded proteins ethanolamine phosphotransferase PmrC, a response
are only 78 amino acids in size. Most of the dfrA and regulator PmrA (also called BasR), and a sensor kinase
dfrB genes found in E. coli of animal origin are located protein PmrB (also called BasS) (232). Mutations either
on gene cassettes that are inserted into class 1 or class in PmrA or in PmrB have been found to be responsible
2 integrons. Some examples are given for dfrA genes for polymyxin resistance in E. coli isolates recovered
that have been identified in E. coli from dogs (dfrA1, from poultry in Spain (236). However, most of the
dfrA12, dfrA17, dfrA29) (138, 185, 210), cats (dfrA1, mutations leading to polymyxin resistance in that op-
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eron or in others, such as the PhoPQ two-component sequence identity with mcr-1 and was located on an
system or its regulator MgrB, have been identified in IncX4 plasmid. The mcr-2 gene has been sporadi-
human E. coli isolates. Ongoing studies are being con- cally identified so far (248). In addition, further mcr
ducted to evaluate whether the same mechanisms might genes—mcr-3 to mcr-7—and variants thereof have been
be responsible for polymyxin resistance in animal iso- described. Among them, the mcr-3 gene was initially
lates. In one such study, mutations in the genes pmrA, identified together with 18 additional resistance genes
pmrB, mgrB, phoP, and phoQ of E. coli isolates from on the 261-kb IncHI2-type plasmid pWJ1 from por-
pigs were identified (237). cine E. coli (249). The mcr-3 gene showed 45.0% and
47.0% nucleotide sequence identity to mcr-1 and mcr-2,
Plasmid-Mediated Polymyxin Resistance respectively. So far, ten variants of mcr-3, designated
In November 2016, the first plasmid-borne polymyxin mcr-3.2 to mcr-3.11, have been identified, with the mcr-
resistance gene was identified. This gene was designated 3.2 gene being originally detected in E. coli from cattle
mcr-1, and it encodes the MCR-1 phosphoethanolamine in Spain (250). A recent study in France reported the
transferase (238). Production of MCR-1 leads to the spread of a single E. coli clone harboring mcr-3 in the
modification of the lipid A moiety of the LPS, resulting veal calves sector from 2011 to 2016 (251). The com-
in a more cationic LPS and, consequently, to resistance bination in those isolates of mcr-3 and blaCTX-M-55,
to polymyxins. Production of MCR-1 in E. coli leads an ESBL gene that is highly prevalent in Asian countries
to a 4- to 8-fold increase in the MICs of polymyxins and rarely detected in Europe, may suggest the intro-
(232). duction and further dissemination of mcr-3 in that spe-
The mcr-1 gene has been detected mainly in E. coli cific animal setting due to international trade. The mcr-4
isolates but also in other Enterobacteriaceae genera, gene was detected among E. coli from pigs in Spain and
such as Salmonella, Shigella, Klebsiella, and Ente- Belgium that suffered from postweaning diarrhea (252).
robacter (239). This gene has now been identified The gene mcr-5 and a variant, designated mcr-5.2, have
worldwide, in both animal and human isolates. The mcr- recently been found in E. coli from pigs (253).
1 gene has been found to be located on plasmids of
various incompatibility groups (IncI2, IncHI2, IncP, Epidemiology of mcr-1
IncX4, IncY, IncFI, and IncFIB) and variable sizes (58 to The mcr-1 gene is a resistance gene identified in human
251 kb) (232). A few reports showed that it may be and animal E. coli isolates. Its occurrence in animal
colocated with ESBL-encoding genes and/or other re- isolates is quite elevated (232), and it has been identified
sistance genes (71, 240–244); nonetheless, most of the worldwide. MCR-1-producing E. coli isolates have been
reports identified mcr-1 as the sole resistance gene on the identified in several food-producing animals and meat,
respective plasmids. This may suggest that a polymyxin- including chickens and chicken meat, pigs and piglets,
related selective pressure is responsible for the mcr-1 cattle, calves, and turkeys (254, 255) (Table 4). Those
acquisition, with corresponding plasmids providing no isolates are from many Asian countries (Cambodia,
other obvious selective advantage. Upstream of the mcr- China, Japan, Laos, Malaysia, Taiwan, Singapore,
1 gene, the ISApl1 insertion sequence element is fre- Vietnam, India, Pakistan, South Korea), from Europe
quently identified, although it is often, but not always, (Belgium, Denmark, France, Germany, Portugal, Italy,
also identified downstream of it. Recent studies dem- the Netherlands, Spain, Sweden, Switzerland, the UK),
onstrated that the mcr-1 gene is mobilized by transpo- the Americas (Argentina, Brazil, Canada, the U.S.,
sition when bracketed by two copies of ISApl1 that form Ecuador, Bolivia, Venezuela), Australia, and Africa
a composite transposon structure (242, 245). So far, 11 (Algeria, Egypt, South Africa, Tunisia). Worryingly, a
variants of the mcr-1 gene, designated mcr-1.2 to mcr- recent study performed in China identified a series of
1.12 have been identified, with mcr-1.3 being found in MCR-1-producing E. coli isolates recovered from
E. coli from chickens in China (246), mcr-1.8 in E. coli poultry, with many of the isolates coproducing the
from poultry in Brunei (GenBank accession no. carbapenemase NDM-1 (71). In addition, such multi-
KY683842.1), mcr-1.9 in E. coli from swine in Portugal drug-resistant isolates were recovered from flies and
(KY964067.1), and mcr-1.12 in E. coli from pork in dogs present in the same farm environment, thus high-
Japan (LC337668.1). lighting that those latter animals might also constitute
Recently, the plasmid-mediated colistin-resistance sources of transmission (71). Additionally, some studies
mcr-2 gene was identified in E. coli isolates recovered highlighted that mcr-1-positive E. coli may be also
from piglets in Belgium (247). It shared 77% nucleotide present in the environment or in food, being, for in-
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TABLE 4 Examples of acquired mcr genes in E. coli of animal origin from Europe, North and South America, and Asia
Geographical
mcr gene origin Source Sequence type(s) Reference
mcr-1 China Pig 238
China Pig 242
China Pig 48, 54, 90, 156, 165, 167, 410, 1114, 1178, 1437, 277
2439, 3331, 4429, 4463, 4656
China Poultry 10, 48, 58, 77, 88, 101, 117, 178, 215, 361, 501, 542, 616, 617, 648, 246
744, 761, 870, 873, 952, 971, 1290, 1431, 1642, 2345, 2491, 2599,
3044, 3133, 3481, 3944, 5542, 5815, 5865, 5879, 5909, 6050,
Vietnam Reptiles 117, 1011 282
South Korea Poultry, pig 1, 10, 88, 101, 156, 162, 226, 410, 1141, 2732 283
Germany Pig 1, 10, 846 240
Germany Pig (manure), fly, dog 10, 342, 1011, 5281 256
France Cattle 241
Italy Poultry (meat) 602 243
U.S. Pig 132, 3234 284
Venezuela Pig 452 285
Brazil Magellanic penguin 10 286
mcr-1.3 China Poultry 155 246
mcr-1.8 Brunei Poultry 101 KY683842.1a
mcr-1.9 Portugal Pig KY964067.1a
mcr-1.12 Japan Pig LC337668.1a
mcr-2 Belgium Pig, cattle 10, 167 247
mcr-3 China Pig 1642 249
France Cattle 744 251
mcr-3.2 Spain Cattle 533 250
mcr-4 Spain, Belgium Pig 10, 7029 252
mcr-5 Germany Pig 29, 349 253
mcr-5.2 Germany Pig 1494 253
GenBank accession number.

a
stance, identified in rivers but also in Asian imported multidrug resistance in E. coli may lead to difficult-to-
vegetables in Switzerland (243). The environmental treat infections, but even more importantly, it constitutes
emission of MCR-1-producing and multiresistant E. coli a major and shared reservoir of resistance determi-
isolates was recently stressed by studying the close sur- nants to most families of antimicrobial agents across a
roundings of pig farms in Germany (256). vast number of animal species, including humans. Even
Dating the emergence of mcr-1-positive E. coli isolates though the different transmission pathways of resistant
remains difficult, although a Chinese study retrospec- E. coli isolates from animals to humans remain to be
tively identified mcr-1-positive isolates from chickens clarified and their relative importance quantified, some
in the 1980s (255) and as early as 2005 in veal calves in data may support the role of the food chain since those
France (254). It seems, therefore, that the emergence of bacteria have been demonstrated as common colonizers
mcr-positive isolates, at least in animals, is not a recent of foodstuffs at retail in many countries and continents.
event. Very likely, there has been some silent dissemi- Other routes of transmission may include direct contacts
nation of mcr genes through the past decades, and the with animals or indirect transfers through the environ-
current situation shows ongoing further dissemination ment. Since E. coli is a bacterium that is widely spread in
rather than an emerging phenomenon. all sectors, antimicrobial resistance in E. coli in animals
has led to numerous cross-sectorial and joint initiatives,
encompassing translational research, epidemiology, and
CONCLUSIONS surveillance in both human and veterinary medicine. It is
Antimicrobial resistance in E. coli is an issue of the now considered that the battle against the increased
utmost importance since it occurs in both the human and occurrence of antimicrobial resistance in E. coli from
animal sectors in a One Health perspective. In animals, humans cannot be won without acting on a very large
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scale. To tone down some current and alarming specu- 13. Dahmen S, Métayer V, Gay E, Madec JY, Haenni M. 2013. Charac-
lations, and in view of all the studies that have been terization of extended-spectrum β-lactamase (ESBL)-carrying plas-
mids and clones of Enterobacteriaceae causing cattle mastitis in France.
conducted during recent years, it is, however, likely that Vet Microbiol 162:793–799 http://dx.doi.org/10.1016/j.vetmic.2012.10
the occurrence of carbapenemase-producing E. coli in .015.
animals does not represent a significant threat for human 14. Freitag C, Michael GB, Kadlec K, Hassel M, Schwarz S. 2017. De-
health (31). In contrast, recent data have demonstrated tection of plasmid-borne extended-spectrum β-lactamase (ESBL) genes in
Escherichia coli isolates from bovine mastitis. Vet Microbiol 200:151–156
that animals are very significant reservoirs of plasmid- http://dx.doi.org/10.1016/j.vetmic.2016.08.010.
mediated colistin resistance genes—mostly present in 15. Su Y, Yu CY, Tsai Y, Wang SH, Lee C, Chu C. 2016. Fluoroquinolone-
E. coli isolates—which may represent a further risk for resistant and extended-spectrum β-lactamase-producing Escherichia coli
from the milk of cows with clinical mastitis in southern Taiwan. J Micro-
humans.
biol Immunol Infect 49:892–901 http://dx.doi.org/10.1016/j.jmii.2014
.10.003.
ACKNOWLEDGMENTS 16. Timofte D, Maciuca IE, Evans NJ, Williams H, Wattret A, Fick JC,
This work was supported by the Swiss National Science Foun- Williams NJ. 2014. Detection and molecular characterization of Esche-
dation (projects FNS-407240_177381 and 40AR40_173686) richia coli CTX-M-15 and Klebsiella pneumoniae SHV-12 β-lactamases
and by the University of Fribourg. from bovine mastitis isolates in the United Kingdom. Antimicrob Agents
Chemother 58:789–794 http://dx.doi.org/10.1128/AAC.00752-13.
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Antimicrobial Resistance

ESBL gene Geographical origin Source Sequence type(s) Reference

Geographical origin Source Sequence type(s) Reference

Among aminoglycosides, the nucleotidyltransferases ESBL genes (blaCTX-M-55, blaCTX-M-15, or blaCTX-M-123)

GenBank accession number.

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