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REVIEW
Extended-Spectrum Beta-Lactamases Producing
Escherichia coli in South America: A Systematic
Review with a One Health Perspective
Carlos Bastidas-Caldes
1,2
, Daniel Romero-Alvarez
3,4
, Victor Valdez-Vélez
1
,
Roberto D Morales
1
, Andrés Montalvo-Hernández
1
, Cicero Gomes-Dias
5
, Manuel Calvopiña
3
1
One Health Research Group, Faculty of Engineering and Applied Sciences, Universidad de las Américas, Quito, Ecuador;
2
Doctoral Program in Public
and Animal Health, Faculty of Veterinary Medicine, University of Extremadura, Cáceres, Spain;
3
One Health Reserch Group, Faculty of Medicine,
Universidad de las Américas, Quito, Ecuador;
4
Biodiversity Institute and Department of Ecology & Evolutionary Biology, The University of Kansas,
Lawrence, KS, USA;
5
Department of Basic Health Sciences, Federal University of Health Sciences of Porto Alegre, Porto Alegre, Brazil
Correspondence: Carlos Bastidas-Caldes, One Health Research Group, Faculty of Engineering and Applied Sciences, Universidad de las Américas,
Quito, 170124, Ecuador, Tel +593 983 174949, Email cabastidasc@gmail.com
Purpose: Extended-spectrum beta-lactamase-producing (ESBL) Enterobacteriaceae, which includes Escherichia coli, has emerged as
a global health threat. ESBL enzymes including CTX-M, TEM, and SHV are the most detected. Here, a systematic review was
developed to assess the status of ESBLs in E. coli considering studies performed in the human, animal, food, and environmental realms
in South America.
Methods: Following PRISMA guidelines, a systematic review was performed using the PubMed database as a primary source to
identify studies containing data on ESBL-producing E. coli in South America. To obtain a comprehensive sample, studies in English,
Spanish, and Portuguese were included from 1990 to April 2021. Inclusion such as the reporting of sample origin and diagnostic
method and exclusion criteria such as review/letter articles were established to complete data extraction steps.
Results: Amongst 506 articles retrieved, 130 met the inclusion criteria. Brazil reported 65 (50%) of publications, followed by
Argentina, and Ecuador with 11.5% each. According to the category of studies, human studies represented the 56%, animals the 20%,
environmental the 11%, and food studies the 6%. Interestingly, studies assessing more than one category (ie, interdisciplinary)
represented the 7%. Prevalence of ESBL producing E. coli in animal, food, and environmental studies was widely superior compared
to human sources. In clinical studies, Brazil presented the greatest diversity in terms of ESBLs, featuring CTX-M, TEM, SHV, TOHO,
OXA, and AmpC. CTX-M enzymes were the most frequent variants with 89.4% detections.
Conclusion: The present One Health review of 130 studies conducted over the past 21 years found ESBLs producing E. coli
distributed across human, animal, food, and environmental samples across South America. There is a need to increment studies in
underrepresented countries and to strengthen multi-sectoral antimicrobial resistance research and surveillance. This information can be
used as basis for subsequent implementation of monitoring programs, targeting potential critical points of transmission sources.
Keywords: extended-spectrum beta-lactamase, Escherichia coli, South America, One Health
Introduction
The antimicrobial resistance phenomena existed long time before humans were implementing antibiotics.
1
Bacteria have
several mechanisms to evade the action of antimicrobials. One of the most important in humans, animals, and the
environment is the enzyme-mediated breaking of the beta-lactam ring of penicillin and its derivatives. Penicillins are the
widest group of antibiotics.
2
Enzyme-mediated resistance is a worldwide public health problem recognized by the World Health Organization
(WHO) due to its rapid expansion and the generation of multidrug-resistant (MDR) bacteria that are increasingly difcult
to eliminate.
3,4
The current increase and dispersion of penicillin, carbapenem, and cephalosporin resistance is driven by a
group of enzymes known as beta-lactamases. These enzymes, commonly found in well-known human environments,
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Received: 22 April 2022
Accepted: 4 August 2022
Published: 30 September 2022
have been discovered in apparently unsuitable localities such as soils or glaciers in Antarctica, which have probably
never encountered beta-lactam antibiotics previously.
5
Beta-lactamases enzymes were rst described in 1940, England; isolated from an E. coli, which prompted antibiotic
resistance research.
6,7
In early 1980s, TEM-1, TEM-2 (isolated from a patient in Temoneira in Athens, Greece), and SHV-1
(sulfhydryl variable, active site) circulating beta-lactamases were found capable to hydrolyze the beta-lactamic ring of
cephalosporins
8
and therefore resistance was soon reported.
9
Single-point mutations in these enzymes allowed beta-lactamases
to break penicillin and its derivatives, as well as the rst, the second, and third generation cephalosporins, and even
monobactams.
10–13
In 1988 and 1989, the rst isolate of SHV-ESBL was found in clinical samples from Argentina and Chile, respectively.
14
Since then, different types of enzymes have been detected in South America with different predominating enzymes, namely,
TEM and SHV, and CTX-M, the latter currently being the most widespread ESBL group in the region.
7
Apart from human detections, beta-lactamases have been found in non-human specimens, animals, and the environ-
ment. The presence of ESBL genes in aquatic ecosystems has been studied in E. coli in different parts of the world, for
example, in Mur River in Europe (ie, Austria)
15
and in Yamato River in Asia (Japan)
16
with bla
CTX-M-1
and bla
CTX-M-14
as the most prevalent ESBL genes, respectively.
Livestock and other animals used as food sources are a well-known reservoir of antibiotic-resistant microorganisms,
despite the lack of literature exploring this topic. For example, few studies have explored veterinary sources of ESBLs, in
stark contrast with the amount of data from humans.
17
In 1988, ESBLs were detected for the rst time in a dog in Japan
with a strain of CTX-M-3-producing E. coli. ESBL types SHV-1, TEM-1, and OXA have been frequently described in E.
coli and Salmonella spp. of animals and food of animal origin in Spain, Germany, the US, and the United Kingdom (UK).
17
In South America, as in the rest of the world, human clinical studies of ESBLs in E. coli are abundant.
18
Conversely, the
current status of beta-lactam resistance in non-clinical scenarios such as their presence in healthy carriers, food matrices, animals,
and the environment is scarce.
19
Nevertheless, evidence suggests that limited access to public health services and lack of hygiene
can contribute to the spread of ESBLs within communities.
13,20
Moreover, the use of antibiotics as growth promoters in livestock
animals favors the dissemination of different types of beta-lactamases CTX-M in food matrices.
2,21
Finally, the poor management
of hospital wastewater may result in discharge of multidrug-resistant coliforms (such as E. coli ESBL+) into natural waterbodies.-
22
All this evidence demonstrates the importance of conducting studies using a One Health approach, namely, understanding the
dynamics surrounding human and animal health, and the environment, to develop strategies to monitor and control beta-lactam
resistance.
23
Due to the aforementioned arguments, in this study we have aimed to develop a systematic review of the current
status of ESBLs in one of the most relevant and ubiquitous bacteria, E. coli, in South America, considering studies
performed in the human, animal, and environmental realms to present a comprehensive summary offering updated
information for practitioners across different elds.
Methods
Protocol and Search Strategy
This systematic review was developed according to the Preferred Reporting Items for Systematic Reviews and Meta-
Analyses (PRISMA) guidelines.
24
The scientic literature was obtained from the NCBI-PubMed database on April 5th,
2021, including studies in English, Spanish, and Portuguese published since 1990 until 2021. Search terms included
“Escherichia coli” AND “ESBL” OR “beta-lactamase” OR “β-lactamase”, plus the names of countries/territories that
belong the South American region: ie, “Ecuador” OR “Peru” OR “Brazil” OR “Argentina” OR “Chile” OR “Colombia”
OR “Venezuela” OR “Uruguay” OR “Paraguay” OR “Bolivia” OR “Suriname” OR “Guyana” OR “French Guiana”. All
terms included the PubMed Title/Abstract criterion so that only studies that contained the searched keywords in their title
and/or in their abstract were considered.
Additional articles found manually in Scopus, SciELO, and latindex databases were also included in this review.
These articles were not found in the initial search because their title and/or abstract not included the search terms
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mentioned above; however, they had other keywords such as “CTX-M”, “resistomes”, “multidrug-resistant” or “multi-
resistant”. These studies presented relevant epidemiological information related to CTX-M beta-lactamases.
Study Selection
The selection of the studies was carried out by two separate reviewers (VV and AM) using the Rayyan QCRI
bibliographic manager to review only titles and abstracts of the selected articles. The rst phase consisted in the removal
of duplicated studies and the inclusion of those related to E. coli and South America while excluding reviews/letters and
studies not focused on ESBLs.
After the rst round of selection, a detailed review of the selected articles was implemented. During this eligibility
phase, only those studies conducted in humans, animals, and/or the environment with complete information (ie, sample
origin and ESBL positive cases detected either by phenotypic or molecular tests) were included for the nal analysis. At
this stage, exclusion criteria allowed the rejection of [1] case reports, [2] studies in Enterobacteriaceae and other bacterial
families that did not report data on ESBLs in E. coli, [3] articles unavailable in full-text, and [4] studies conducted in
regions different from South America.
Data Extraction
Studies selected were tabulated and introduced in a Microsoft Excel 2016 spreadsheet with their general information (ie,
author, year, country, and URL). Data to be evaluated included (i) detection methods, (ii) type and origin of samples, (iii)
prevalence of E. coli, (iv) prevalence of E. coli with ESBL phenotype, (v) prevalence of E. coli with ESBL genotype, (vi)
ESBL types, and (vii) identication of clones by multi-locus sequence typing (MLST) of clinical importance. The three-
prevalence parameters (points iii, iv, and v) were independently reported for each South American country; these values
were obtained by dividing the number of samples found in each category (E. coli, E. coli with ESBL phenotype, and E.
coli with ESBL genotype) with the total sample size (n). Relevant data are presented in statistical graphs.
Data Analysis
Descriptive statistics were obtained for all the studied parameters (eg, sample origin and source, E. coli prevalence, etc.)
and are shown with 95% condence intervals when appropriate. ESBL types and CTX-M variants were further
categorized using descriptive statistics and their proportions were depicted per country in maps of the region using
barplots and pie charts according to each of the established categories, that is, human clinical cases, human healthy
carriers, animal, food, and environmental studies using R programming language version 3.6.3 and QGIS 2.18 “Las
Palmas”.
Results
Studies Included
The total number of articles found in PubMed from 1990 to April 2021 was 500; additionally, six articles were also
included from SciElo and Latindex databases for a total of 506 articles. During the rst screening phase, 321 studies were
excluded because they were either reviews/letters or articles that deviate from the theme of this review. During the
eligibility phase, 55 studies were discarded due to their lack of detail. A total of 130 articles were included in this review
(Figure 1).
ESBLs Detection Methods for E. coli
From the 130 articles included, 25 used phenotypic tests, the three commonest being the disc diffusion, the minimum
inhibitory concentration (MIC), and the VITEK system; the latter also used for bacterial identication. On the other hand,
14 articles used molecular tests including PCR (ie, either endpoint, multiplex, or quantitative) and sequencing to
determine the presence of beta-lactamase coding genes. Ninety-one publications (70%) used both phenotypic and
molecular tests for gene and bacteria identication.
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Classication of Studies
The studies were classied into six categories according to the origin of the sample: two categories for human studies
(clinical cases and healthy carriers), followed by animal, food, environmental, and interdisciplinary studies, here labeled
as those analyzing more than one category at the same time. More than half of the studies corresponded to human
samples (56%; n=73/130). From them, 52% (n=68/130) corresponded to isolations from human clinical studies and 4%
(n=5/130) corresponded to studies on human healthy carriers, the smallest category on our analysis. Samples isolated
from animals and the environment corresponded to 20% (n=26/130) and 11% (n=14/130), respectively. Interdisciplinary
studies corresponded to 7% (n=9/130). Samples isolated from food corresponded to the 6% of the publications studied
(n=8/130).
Figure 1 PRISMA ow diagram for study categorization and selection of the 130 studies included in this systematic review. Data came from PubMed and additional
databases between 1990–2021.
Notes: Adapted from Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Syst Rev. 2021;10:89.25
Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/legalcode).
Abbreviation: ESBL, extended spectrum beta-lactamases.
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In addition, animal samples were sub-classied into birds, companion animals, livestock, and wild animals (Figure 2).
Birds were investigated in more than half of animal-oriented studies (51%; n=18/35), followed by domestic animals
(23%; n=8/35), farm animals (20%; n=7/35), and wild animals (6%; n=2/35; Figure 2A). A subcategorization of birds
showed that poultry was the most studied with 61% (n=11/18) of publications, followed by urban species such as doves
and pigeons with 28% (n=5/18), and migratory bird data in 11% of studies (n=2/18; Figure 2B). A subcategorization of
livestock showed that cattle and pigs represented 46% (n=5/11) and 36% (n=4/11) of the, respectively, farm animals
studied (Figure 2C). It is important to mention that in some publications, more than one type of farm animal was studied.
ESBL Producing E. coli Studies per Country
Fifty percent of the studies (n=65/130) was carried out in Brazil, followed by Argentina, and Ecuador with 11.5% (n=15/
130) each. As it can be seen, Brazil exceeds with 50 studies to all other countries (Figure 3). It is worth noting that a
fraction of the studies identied (n=7/130) were developed in more than one country; thus, at least 5.4% of the studies
occurred as international multicenter approaches.
As expected, a further categorization of sample type per country showed the predominance of samples from human
clinical origin (Figure 3). For example, in Brazil, 46.2% (n=30/65) of the included studies corresponded to clinical
isolations; moreover, in Venezuela, 100% of their research (n=12/12) were focused on nosocomial samples. Brazil,
despite having the highest number of studies in the region, lacked studies on human healthy carriers. This pattern was
similar across the rest of the countries analyzed, namely, predominance of human clinical samples followed by either one
or two studies including any of the other studied categories (ie, healthy carriers, animal, or environmental sample types).
Exceptions included French Guiana with a unique study focused on human healthy carriers, and Ecuador (n=15 studies)
with at least one publication across each sample type category (Figure 3).
Prevalence and Distribution of ESBLs Producing E. coli
In South America, the prevalence of ESBLs at the level of the animal, food, and environment was larger than the
prevalence from human sources (ie, either clinical cases or healthy carriers) (Table 1). The same pattern was evident in
each country analyzed. Brazil presented the greatest number of samples of each category except for the healthy carriers,
where data were absent. Details of these results per country are described in Supplementary Table 1.
ESBL Types and Enzymes Variants
Human Clinical Studies
The total number of ESBLs genes in clinical samples was 3509. The South American distribution of ESBLs based on the
selected studies shows that Brazil was the country with the highest number of detections with 21.3% (n=788/3701). Also,
Brazil presented the highest diversity of ESBL types reporting CTX-M, TEM, SHV, TOHO, OXA, and AmpC enzymes.
Figure 2 Classication and sub-classication of ESBLs producing E. coli studies developed in animal samples. (A) General classication of animals identied and their
distribution in number of studies and percentages (n;%). (B) Animal studies in birds: sub-groups identied and their distribution in number of studies and percentages. (C)
Animal studies in livestock: sub-groups identied and their distribution in number of studies and percentage.
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Surprisingly, PER-2 enzymes were only found in Uruguay. CTX-M enzymes were the most prevalent in South America
with at least 89.4% (n=3309/3701) identications. CTX-M enzymes variants recognized were usually reported as
unspecied across countries/territories with few exceptional publications. For instance, multiple Bolivian studies reported
the presence of CTX-M-1 (50.8%; n=67/132). Similarly, studies from Uruguay consistently reported the presence of
CTX-M-15 (59.5%, n=47/79). These results are shown in more detail in Figure 4 and Supplementary Table 2.
Human Healthy Carriers Studies
Epidemiological data focused on isolations from healthy carriers in South America were limited. Only Ecuador, Peru,
Bolivia, and French Guiana reported ESBLs from this category; thus, the total number of ESBLs in this context was 204.
The enzymes CTX-M (96%; n=195/204) and TEM (4%; n=9/204) were the only ESBLs found. The CTX-M-2 enzyme
variants were most prevalent in Peru (47.7%; n=31/65) and Bolivia (43.7%; n=21/48). In French Guiana, the enzyme
CTX-M-1 was the most signicant variant with a prevalence of 46.1% (n=6/13). Conversely, only CTX-M-55 enzyme
Figure 3 Categorization of 130 studies included in this systematic review from PubMed and additional databases between 1990–2021. Color bars represent the number of
studies conducted in South American countries and number of studies per country categorized by sample type examined.
Table 1 Prevalence of E. coli Isolates According to Their Sample Sourc. Comparison of Prevalence of ESBL Determination by
Phenotypic and Genotypic Methods Across Six Categories in 130 Studies from South America Between 1990 and 2021 (N=203057)
Categories of Sample Sample Size E. coli Isolates Phenotype of
ESBL-Producing E. coli
Genotype of
ESBL-Producing E. coli
(N) (n) % [95% CI] (n) (%) [95% CI] (n) (%) [95% CI]
Clinical (H) 185,203 28,348 15.3 [0.151–0.155] 3719 13.1 [0.12–0.14] 3509 1.9 [0.018–0.02]
Healthy Carriers (H) 7861 1105 14.1 [0.133–0.149] 490 6.2 [0.057–0.067] 139 1.8 [0.02–0.2]
Animal 6616 3607 54.5 [0.533–0.557] 1418 21.4 [0.204–0.224] 1195 18.1 [0.1–0.2]
Food 1860 1401 75.3 [0.733–0.773] 193 10.4 [0.09–0.118] 580 31.2 [0.3–0.333]
Environment 1517 553 36.5 [0.341–0.389] 191 12.6 [0.109–0.143] 187 12.3 [0.106–0.14]
Abbreviations: N, total samples of each category; H, human samples; 95% CI, 95% condence Intervals.
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variants were reported in Ecuador (n=69/69). These results are depicted in more detail in Figure 5 and Supplementary
Table 2.
Animal Studies
Six South American countries reported epidemiologic data in animals. The total number of ESBLs in animal samples was
1191. ESBL types identied included CTX-M, TEM, SHV, PER-2, and AmpC. CTX-M enzymes were the most
prevalent (64.5%; n=768/1191). CTX-M enzyme variants featured included CTX-M-1 in Ecuador (28.4%; n=50/176)
and Chile (63.3%; n=124/196); CTX-M-2 in Brazil (40.2%; n=127/316); and CTX-M-8 in Brazil (23.4%; n=74/316),
Argentina (56.7%; n=17/30), and Uruguay (56.4%; n=22/39). Many CTX-M variants were recorded in Ecuador although
the higher proportion (56.2%, n=99/176) of cases was represented by unknown variants. In Peru, only CTX-M-15
enzymes were reported (n=11/11). These results can be observed in more detail in Figure 6 and Supplementary Table 2.
Figure 4 Distribution of ESBLs types (A) and CTX-M enzyme variants (B) in clinical human studies developed in South America. Unspecied = CTX-M enzyme present but
variant unreported. Pie charts are showing the maximum and minimum percentages for each country. Complete information can be found in the main text and
Supplementary Table 2.
Figure 5 Distribution of ESBLs types (A) and CTX-M enzyme variants (B) identied in the context of healthy carriers human studies developed in South America. Pie charts
are showing the maximum and minimum percentages for each country; complete information can be found in the main text and Supplementary Table 2.
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Food Studies
Only two countries (Ecuador and Brazil) published studies about ESBL detection in food. The total number of ESBLs in
food samples was 520, among them, CTX-M, TEM, SHV, and AmpC were identied. CTX-M enzymes were the most
prevalent (73.6%; n=383/520). Considering CTX-M variants, CTX-M-1 in Ecuador with 66.1% (n=109/165) and CTX-
M-2 in Brazil with 63.3% (n=138/218) were found. These results can be observed in detail through Figure 7 and
Supplementary Table 2.
Environmental Studies
Environmental studies were found in ve South American countries. The total number of ESBLs in environmental
samples was 276. ESBL types identied included CTX-M, TEM, SHV, TOHO, OXA, and AmpC. Similar as it was
Figure 6 Distribution of ESBLs types (A) and CTX-M enzyme variants (B) identied in animals and developed in South America. Unspecied = CTX-M enzyme present but
variant unreported. **Others = Variants of CTX-M enzymes with <1% of prevalence. Pie charts are showing the maximum and minimum percentages for each country;
complete information can be found in the main text and Supplementary Table 2.
Figure 7 Distribution of ESBLs types (A) and CTX-M enzyme variants (B) identied in food and developed in South America. *Others = Variants of CTX-M enzymes with
<1% of prevalence. Pie charts are showing the maximum and minimum percentages for each country; complete information can be found in the main text and in
Supplementary Table 2.
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obtained in results from the other categories (ie, human clinical cases, human healthy carriers, animals, and food studies),
CTX-M enzymes were the most prevalent (71.4%; n=197/276). Among CTX-M variants, CTX-M-1 in Colombia
(68.1%; n=49/72), CTX-M-2 in Peru (72.7%; n=8/11), and CTX-M-55 in Ecuador (50%; n=8/16) were reported. In
Brazil, CTX-M variants were unknown in most cases, representing 43.3% (n=42/97) of all detections. In Bolivia, CTX-
M-3 was the variant detected in their unique report (n=1/1). These results can be traced in detail in Figure 8 and
Supplementary Table 2.
Clones of Epidemiological Importance
A total of 59 different clones were described in 31 studies. The clone E. coli ST131 represented 48.4% of the total of
detected clones in the studies (n=15/31), followed by ST10 with 29% (n=9/31). The clones ST405, ST648, and ST38
accounted for 13% (n=4/31) each; ST410 and ST744 for 10% (n=3/31) each; followed by clones ST90, ST117, and
ST155 representing the 6.4% (n=2/31). All the remaining clones were represented by a single detection across the
reporting studies (3%; n=1/31 each; Supplementary Table 3). It is worth to mention that the presence of these clones was
conditioned to their detection per country; thus, Brazil was the country that reported more clones (55%; n=38/59)
followed by Peru (17.4%; n=12/59), Ecuador, Uruguay (11.6%; n=8/59 each), Chile (5.8%; n=4/59), and single reports of
clones from Colombia, Argentina, and French Guiana (1.4%; n=1/59 each).
Discussion
The present systematic review of the literature provides relevant information on the distributions of ESBLs in E. coli in
South America. To our knowledge, this is the rst attempt that addresses the presence of ESBLs across different
categories, going beyond human-derived clinical samples, to also consider samples from human healthy carriers, animals,
environmental, and food isolations, echoing calls of multidisciplinary, One Health approaches, to comprehend the
presence of antibiotic resistance mechanisms.
Of the 130 studies included in this review, Brazil contributed with more than half the research of this topic (n=65/130;
Figure 3). These results correspond with evidence showing different levels of scientic production in South America
where Brazil is recognized as a regional leader.
25–28
The other South American countries had at least one publication on
ESBLs producing E. coli,
29
which is far from ideal and should prompt efforts to understand beta-lactam resistance and
their importance in public health.
2,3
Despite the low scientic production of Ecuador compared to the rest of South
Figure 8 Distribution of ESBLs types (A) and CTX-M enzyme variants (B) identied in the environment and developed in South America. Unspecied = CTX-M enzyme
present but variant unreported. *Others = Variants of CTX-M enzymes with <1% of prevalence. Pie charts are showing the maximum and minimum percentages for each
country; complete information can be found in the main text and Supplementary Table 2.
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American countries,
27,28
Ecuador was the country with the second highest research contribution in the region in this
review (n=15/130), together with Argentina (Figure 3).
Considering the limitations of many South American laboratories (eg, logistics, equipment, infrastructure, others),
30,31
we
expected that the inclusion of molecular tests that require higher costs and increased technical expertise
32
would have been
lower compared to phenotypic tests. Consequently, in this review, phenotypic tests (n=25/130) were implemented in 11 more
publications than molecular tests (n=14/130); however, most of the publications used both phenotypic and molecular tests
(70%; n=91/130) for identication, which allows a more precise detection and therefore improvement of ESBLs epidemio-
logical surveillance in E. coli.
33
Some human clinical or environmental studies used molecular methods directly for ESBLs
genes’ detection. Ideally, both detection methods should be implemented since neither is exempt from limitations. First,
methods such as PCR are less effective in the presence of unknown mutations of new unreported ESBL variants, especially
when these mutations appear at primer hybridization sites.
33
Second, methods based on disk diffusion can report problems
with interpretation when co-resistance events occur.
34
Thus, new techniques for identifying ESBLs are being developed and
have proven to be more sensitive, specic, efcient, and even provide other advantages such as point-of-care detections.
35
One
of the more recent options is the CRISPR-Cas9-based detection method with optical DNA mapping, which was used to
identify bla
CTX-M-15
and bla
CTX-M-14
genes in E. coli from clinical urinary tract infections in Sweden.
36
Up to 52% (n=68/130) of studies corresponded to human clinical samples, which depicts the lack of research about
antimicrobial resistance from non-human oriented sources.
19
For example, for this review, Venezuela contributed with
publications only within this category (Figure 3). Reviews such as that of Guzmán et al
37
expose the clinical situation in
Venezuela but lack an analysis of antimicrobial resistance from animals, food products, or the environment.
Among the categories established in our review, ESBL detections from human healthy carriers, at the community
level, were mostly underrepresented (n=5/130; Figure 3). Onduru et al evidenced a similar pattern in a review for African
countries
38
where human clinical studies represented the 74%, while studies performed on healthy carriers contributed
only with the 15%. It is known that healthy carriers are an important reservoir for the transmission of beta-lactamases and
therefore act as spreaders to healthy individuals or environmental settings. Further studies including surveillance at these
scales might unveil a hidden pattern for the epidemiology of bacterial resistance in human populations.
39,40
For this review, One Health studies were categorized as interdisciplinary, considering that they analyzed samples
across different interfaces: human-animal,
41–43
human-environment,
44,45
human-food,
46
animal-environment,
47
human-
animal-food,
48
and animal-food-environment.
49
The number of interdisciplinary studies included in this review was low
(7%; n=9/130; Figure 3). Similarly, O’Neal et al review for Central America
50
and Escher et al review for Africa
51
found
small numbers of One Health-related studies. Thus, apart from South America, other world regions also struggle to
incorporate One Health approaches to their experimental designs; a reality that might be tackled with international
cooperation, executing multi-sectorial action plans as proposed by the WHO.
52
Many of the clinical studies included in
the present review were “international multicenter studies”, which are characterized by promoting joint research across
several countries, albeit these alliances are usually focused on human clinical samples.
53
These types of studies might be
a good example to follow to include a cooperative approach to address questions in the ecology and veterinary elds.
Considering animal publications, those for human consumption were more studied than other groups. Of these, 61%
came from poultry in birds and 82% from bovines and swine in livestock. This can be explained due to awareness of the
impact of antibiotic use as prophylactic treatment or most commonly as growth promoters for fattening. There is
extensive evidence showing how this practice promotes the spread and therefore the risk of zoonotic antibiotic resistance
mechanism contaminations through the food chain.
54–56
Nevertheless, for this review, urban and migratory birds
contributed with the 28% and 11% of ESBLs in E. coli, respectively. Recently, studies of migratory birds have
incriminated their feces in the environment as possible contributors to the international spread of antimicrobial
resistance.
57–59
Studies focusing on this animal group should be encouraged to assess the validity of this hypothesis.
Veterinary publications have noticed a zoonotic transmission risk from pet animals, favored by their proximity to their
owners.
60–62
A similar trend can be stressed for the potential spillover of ESBLs; however, studies from pet animals were
also underrepresented in our systematic review with only a 23%. Studies focused on wild animals were even less
represented in our review (6%; n=2/35; Figure 2A). Wildlife might be an important source for the spread of resistance
mechanisms as they act as bridges between the urban and sylvatic environments, especially mammals.
63
Another
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example is that, in Brazil, shes have been found to contribute to the spread of ESBLs in natural waterbodies and its
marine fauna.
64,65
In South America, higher values of ESBL producing E. coli prevalence were obtained from animal, food, and
environmental sources compared to human samples (Table 1). In our review, one of these results showed a prevalence of
E. coli with ESBL genotype of 18.1% in animals and 12.3% in the environment compared to 1.9% in clinical studies.
These results were analogous among the majority of South American countries and similar to observations in Tanzania,
the Netherlands, and other regions of the world where ESBLs from animal and environmental sources showed between a
10 to 20% higher prevalence than humans.
66–68
Therefore, although apparently many of the E. coli resistance mechan-
isms are acquired in the clinical setting, prevalence in animals and environmental sources predominate and should be
further studied.
CTX-M enzymes were the most prevalent, with more than 50% detections in each country and category analyzed in
this review (ie, human clinical samples, human healthy carriers, animal, food, and environment; Figures 4–8). Similar
results have been reported in the rest of the world. For example, in Africa CTX-M prevalence reaches an 81.5%.
38
In
Iran, CTX-M enzyme prevalence reached 31.2% followed by TEM with 27.6%.
69
It is worth to mention that the
prevalence analyzed here only accounted for E. coli, thus it might be an underestimation if including other bacterial
species such as K. pneumoniae, which usually harbor TEM or SHV enzymes.
70–72
Apart from the best-known enzymes (ie, TEM, SHV, and CTX-M), TOHO, reported for the rst time in Japan in
1993,
73
was also found in South America among human clinical and environmental studies (Figures 4A and 8A). Thus,
in little less than three decades, TOHO enzymes have spread to a completely different region albeit its low prevalence
(<0.1%; n=1/3701). Other types of beta-lactamases that are worth highlighting are the OXA (<0.1%; n=17/3701) and
AmpC (<0.1%; n=9/3701) enzymes. Both show a different resistance spectrum to the most common resistant enzymes.
OXA enzymes can hydrolyze more effectively antibiotics such as carbapenems,
74
while AmpC is not inhibited by
clavulanic acid.
75
The ESBL enzymes PER-2, with similar spectrum to TEM and SHV enzymes,
76
were only found in
Uruguay with a low prevalence (Figure 4A). However, Celenza et al
76
have reported PER-2 isolated from
Enterobacteriaceae in Bolivian hospitals, which suggests the existence of PER-2-carrying E. coli in this country.
Although detected, CTX-M enzyme variants were poorly reported (Figure 4B). Detection of variants is one of the
most important clinical data because each one has differences in their antibiotic response.
77–79
It is worth noting that in
other regions of the world such as Nigeria, Tunisia, and the Netherlands, CTX-M-15 variant isolated from clinical
settings is usually detected with a prevalence ranging from 67.9% to 83.3%.
80–82
Considering animal studies, the presence of CTX-M-8 enzyme variant was frequently described in countries such as
Brazil, Argentina, and Uruguay (Figure 6B). Because CTX-M-8 was rst isolated from Enterobacteriaceae in Brazil,
83
the most likely scenario involves it spread across animals from neighboring countries, despite the lack of reports of CTX-
M-8 in Chile, Peru, and Ecuador according to our review. For these countries, the variants CTX-M-1 and CTX-M-15
were detected, as has been seen in goat samples from Tunisia, pigs from Portugal, horses from the UK, and processed
beef from Germany.
84–87
From food studies, the main types of CTX-M enzymes detected included the CTX-M-1 in Ecuador and the CTX-M-2
in Brazil (Figure 7B); results were consistent with reports from Germany
88,89
and Algeria
90
where the CTX-M-1 variant
is the most prevalent. However, as only few studies address the presence of antibiotic resistant enzymes in food-related
sources, more research is granted to conrm their role as a mechanism of spread with public health consequences.
The enzymes of type TOHO, OXA, and AmpC from environmental studies were found only in Brazil (Figure 8A).
These types of ESBLs had an overall low prevalence. For CTX-M enzyme variants from environmental sources, there
was a great variability of detection across South American countries, namely, the enzyme CTX-M-1 in Colombia, CTX-
M-3 enzyme in Ecuador/Bolivia, and the CTX-M-2 enzyme in Peru/Brazil (Figure 8B). Lines of research that go beyond
the simple detection of ESBLs in the environment should be encouraged as has been done in other regions of the world.
For example, in Nigeria, Lebanon, Vietnam, and India, there are studies assessing the impact of antibiotic release on
hospital wastewater correlated with patterns on resistance acquisition in E. coli.
91–94
Research from the UK, Tanzania,
and the Dominican Republic
95–97
have revealed the importance of IncF plasmids found in natural waterbodies. Being a
conjugative plasmid, IncF is related to the dissemination of bla
CTX-M-15
by horizontal gene transfer.
98,99
Finally, other
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exemplary studies show how activated sludge from wastewater treatment plants can be a source of high prevalence of
CTX-M as demonstrated in Japan,
100
Austria,
101
and India.
102
The E. coli clones ST131 and ST10 were found across South America (Supplementary Table 3). These results are
consistent with a study conducted in Canada in which 96/209 (46%) E. coli strains corresponded to the clonal complex
ST131
103
and with one developed in the Netherlands where from 112 strains belonging to E. coli, 21% belonged to ST131 and
17% to ST10,
82
demonstrating the worldwide high prevalence of the ST131 clone. These clones are known to be a major
reservoir of plasmids carrying resistant genes to multiple antibiotics, including bla
TEM
, bla
SHV
, and bla
CTX-M
.
104
The inuence
of international travel on the dissemination of these clones has been studied in countries such as Germany, where the ST131
clone ranges between 19% and 30%, or the Netherlands, where the ST131 clone prevalence reaches a 21.4%.
82,105
For the
purposes of this argument, it is worth to mention that Woerther et al
106
reported the international clone ST10 in healthy carriers
from a remote community at French Guiana, which begs the question on how this clone was acquired within an isolated
population.
Limitations
Our results are based on a systematic review of published academic literature. Potentially, there is relevant information
among the grey literature (eg, thesis) that might complement the results presented here; however, we rely on the quality
of peer-review publications to assess the status of E. coli ESBLs in South America with certainty. Similarly, our analysis
excluded articles in the category of “reviews” that sometimes present pieces of original research, but we believe that their
overall contribution in the presented information may be negligible. Furthermore, while we comprehensibly reviewed
each of the 130 manuscripts included in this study, data heterogeneity across different countries and publications is a
challenge that was overcome with some heuristic categorizations, which are the basis of any systematic review.
Finally, it is worth noticing that although manuscripts included in the present review were considered of high quality
by the individual assessment of their results, we are aware that potentially some of them might be published in journals
considered predatory. We believe that science should be judged by their ndings instead of the journal in which it was
published, and for this review we can trust in the reliability of the studies analyzed.
Conclusions
ESBLs producing E. coli in South America are widely distributed and show a high diversity of enzyme variants. ESBLs
in human samples are the most studied, mainly in those linked to hospital environments (inpatient and outpatient).
However, ESBLs in food and animal samples are the most prevalent. Countries such as Brazil present more studies on
ESBL surveillance involving various sample sources. CTX-M enzymes are the most common and diverse of the types of
beta-lactamases found and show a high prevalence across all the studied categories. ST131 and ST10 are the most
widespread clones in the studies included in this review.
In order to fully characterize the situation of E. coli ESBLs in South America, a greater contribution from under-
represented countries of the region should be encouraged. These contributions ideally should emphasize the role of
sources different from human clinical settings such as animals, environmental, and food matrices, together with
detections from human healthy carriers. Concerns related to transmission of resistant mechanisms among human healthy
carriers, zoonotic sources, as well as the spread of ESBLs in aquatic ecosystems, reveal the importance of developing
studies beyond the human clinical-centered view of health. Furthermore, the importance of animal and environmental
health should be explored since ESBL genes in both realms have been detected in South America and the rest of the
world.
Efforts to increase the epidemiological surveillance of the region to detect predominant types of ESBLs and the
presence of new variants, as well as the distribution of ST clones, should be a priority considering their different roles in
antibiotic resistance and their traceability to detect infection sources. At this point, the inclusion of both phenotypic and
molecular tests, as well as the development of new detection techniques, should facilitate surveillance efforts to further
the understanding of ESBL distribution in South America.
Finally, the information presented in this review can be used as basis for subsequent implementation of monitoring
programs, targeting potential critical points of transmission sources. Following the One Health concept, the development
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of contingency plans in different areas like hospitals, broiler breeding sites, and wastewater treatment plants might
contribute to the identication of resistant enzymes and their spreading, which ideally should be controlled if not
completely halted; within this objective, a multi-sectoral and multi-disciplinary cooperation will be of utmost importance.
Acknowledgments
Our thanks to the Universidad de las Américas for nancing the APCs of this work. Special thanks to Adriana Gallegos-
Ordoñez for her help in proofreading of English language and support in the writing of this work.
Supplementary Materials
To a better description of ndings of this work, the following supporting information can be downloaded. Supplementary
Table 1: Number of samples identied (frequencies) and % prevalence of E. coli, E. coli with ESBL phenotype, and E.
coli with ESBL genotype in South America from human clinical samples, human healthy carriers, animal, food, and
environmental studies. Data from 130 studies included in systematic review between 1990 and 2021. Supplementary
Table 2: Percentages of different beta-lactamase enzymes identied across South American countries and CTX-M
variants for human clinical samples, human healthy carriers, animal, food, and environmental studies. Data from 130
studies included in systematic review between 1990 and 2021. Supplementary Table 3: E. coli ST clones found in studies
in South America per country and author. Data from 130 studies included in systematic review between 1990 and 2021.
Supplementary Table 4: Summary Data Base and list of studies included in the systematic review and general data from
130 studies included between 1990 and 2021. Supplementary Table 5: List of additional references included in the
systematic review.
107–225
Disclosure
The authors report no conicts of interest in this work.
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