GRAPHICAL ABSTRACT

Key Message

• Escherichia coli that are resistant to third-generation cephalosporins, carbapenems, and colistin can colonize the guts and potentially cause extra-intestinal infections and increased transmission in healthcare settings, especially if they are high-risk clones.

• To develop effective infection prevention and control measures against these E. coli strains, it is essential to determine the global prevalence and extent of their dissemination among different niches and hosts, including healthy humans and animals.

• This meta-analysis of 10-year epidemiological and genomic data found profound persistence and transmission of critical priority and high-risk E. coli clones in healthy humans and animals around different locations.

INTRODUCTION

Ecologically, Escherichia coli is a major gut commensal in humans and animals [1]. However, certain strains may express virulence factors and become pathogenic within the gut (e.g., traveler’s diarrhea) or disseminate to other body sites, causing infections such as cholecystitis, pneumonia, neonatal meningitis, sepsis, and urinary tract infections [2,3]. Specifically, extraintestinal pathogenic E. coli consists of 4 pathotypes: neonatal meningitis E. coli, uropathogenic E. coli, avian pathogenic E. coli, and septicemic E. coli [4]. These classifications are based on the original host and the clinical symptoms produced [4]. Moreover, pathogenic E. coli strains in humans and animals can be acquired from contaminated environments, underscoring their relevance within One Health ecosystems [5].

A holistic approach that considers the interconnectedness of human, animal, and environmental health may provide fresh insights into the spread of E. coli and demonstrate its capacity to establish in a wide variety of vertebrate hosts, including humans and food-producing animals [6]. Robust evidence shows that pathogenic E. coli strains can be transmitted from food-producing animals to humans via food [7]. However, the specific impact of foodborne zoonotic E. coli on the overall burden of extraintestinal infections in humans, and the distinct traits that differentiate these strains, remain poorly defined. Recently, reverse zoonosis (transmission from humans to animals) has emerged as a significant issue in infectious disease research due to changes in social environments, such as the increasing number of companion animals and closer interactions with their owners. Livestock farmers or workers may also serve as sources of antibiotic-resistant E. coli strains to animals at the farm level [6].

It is important to note that the burden of E. coli increases exponentially when it carries critical antimicrobial resistance (AMR) mechanisms against last-resort antibiotics used in clinical settings [8]. Such resistance is a major public health concern when mediated by transferable genes or chromosomal point mutations conferring resistance to third-generation cephalosporins (3GCs), colistin (COL), or carbapenems (CARB) [9]. Specifically, COL sulfate is considered one of the final treatment options for severe infections caused by CARB-resistant (CARB^R) E. coli [10]. Resistance mechanisms may be mediated by transferable genes against COL (mcr-1 to 11 and mgrB) and CARB (bla_OXA-48, bla_OXA-244, bla_KPC, bla_SME, bla_NDM, bla_SPM, bla_VIM, bla_GES, and bla_IMI) [11,12]. Moreover, chromosomal point mutations in oprD and pmrB/phoQ genes have been linked to CARB and COL resistance, respectively [11,12]. Furthermore, some variants of extended-spectrum beta-lactamase (ESBL) genes, bla_CTX-M, bla_TEM, and bla_SHV mediate 3GC-resistant (3GC^R) [13].

The World Health Organization (WHO) classifies 3GCs and CARBs as “critically important antimicrobials for human medicine.” However, there has been a significant increase in resistance to these antibiotics [14]. The rise and proliferation of 3GC, CARB, and COL resistance in E. coli primarily result from misuse, irrational use or overprescription in human medicine and illegal use in veterinary medicine and animal husbandry [15]. Host colonization and infections in individuals with CARB^R or COL-resistant (COL^R) E. coli who have not received these last-resort antibiotics or had contact with settings and hosts that are colonized with critically resistant E. coli indicate the evolution and persistence of the resistance genes driven by mobile genetic elements (MGEs) [16,17]. The selection pressure for CARB and polymyxin resistance in gut E. coli may vary by host and geographical region [18,19].

Extensive efforts have been made to identify and characterize critically resistant E. coli in clinically ill humans and animals; however, data on healthy humans and animals remain scarce. Preserving the efficacy of these 3 antibiotic categories (3GC, CARB, and COL) is vital because they are critical to antimicrobial chemotherapy for E. coli infections. Therefore, it is essential to determine whether the gastrointestinal tracts of healthy humans and animals serve as significant ecological niches and transmission pathways for resistance genes and high-risk E. coli strains. Global analyses of these priority E. coli strains in healthy hosts can inform surveillance and infection prevention and control measures. To assess the public health impact of these emergent E. coli strains, we conducted a systematic review and meta-analysis of studies that examined E. coli and its susceptibility to 3GC, CARB, and COL in healthy humans, livestock, and companion animals over the past decade (2014-2024). In addition, epidemiological and genomic analyses were performed to elucidate the transmission pathways of critically resistant and high-risk E. coli lineages.

MATERIALS AND METHODS

This systematic review and meta-analysis included original research and brief communications that reported the detection of E. coli, its resistance, and resistance mechanisms against 3GC, CARB, and COL in healthy humans, livestock, and pets. The entire process—including literature search strategy, selection of articles, data extraction, and results presentation—adhered to the guidelines outlined in the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA; http://prisma-statement.org/PRISMAstatement/check_list.aspx), accessed on October 1, 2024. Articles investigating E. coli and its CARB^R, 3GC^R, and COL^R strains were scrutinized from Scopus, Web of Science, Google Scholar, and PubMed databases. Only original research articles and brief communications published between June 1, 2014 and June 1, 2024 were included. Search terms used included: “Escherichia coli fecal carriage in healthy livestock,” “Escherichia coli fecal carriage in healthy goats,” “Escherichia coli fecal carriage in healthy cattle,” “Escherichia coli fecal carriage in healthy sheep,” “Escherichia coli fecal carriage in healthy ewe,” “Escherichia coli fecal carriage in healthy poultry,” “Escherichia coli fecal carriage in healthy chicken,” “Escherichia coli fecal carriage in healthy horses,” “Escherichia coli fecal carriage in healthy buffaloes,” “Escherichia coli fecal carriage in healthy pigs,” “Escherichia coli fecal carriage in healthy pets,” “Escherichia coli fecal carriage in healthy dogs,” “Escherichia coli fecal carriage in healthy cats,” “Escherichia coli fecal carriage in healthy companion animals,” “Escherichia coli fecal carriage in healthy humans,” “carbapenem-resistant Escherichia coli in healthy livestock,” “carbapenem-resistant Escherichia coli in healthy pets or companion animals,” “carbapenem-resistant Escherichia coli in pets,” “carbapenem-resistant Escherichia coli in healthy humans,” “colistin-resistant Escherichia coli in livestock,” “colistin-resistant Escherichia coli in healthy pets or companion animals,” “colistin-resistant Escherichia coli in pets,” “colistin-resistant Escherichia coli in healthy humans,” “cephalosporin-resistant Escherichia coli in healthy livestock,” “cephalosporin-resistant Escherichia coli in healthy pets or companion animals,” “cephalosporin-resistant Escherichia coli in healthy pets,” “cephalosporin-resistant Escherichia coli in healthy humans,” “ESBL-producing Escherichia coli in healthy livestock,” “ESBL-producing Escherichia coli in healthy pets or companion animals,” “ESBL-producing Escherichia coli in healthy pets,” and “ESBL-producing Escherichia coli in healthy humans.”

Out of the initial 5,034 results (4,932 from databases and 102 from registers), 4,880 articles were eliminated as they did not pertain to E. coli. Additionally, 90 articles were eliminated due to inadequate methodology, or being review papers (Supplementary Material 1). Following this screening process, 64 studies specifically addressing E. coli in healthy humans, pets and livestock were included (Supplementary Materials 1 and 2). Articles solely concentrating on samples from sick or hospitalized humans or animals were excluded. Furthermore, aquatic and wild animals were eliminated because it was difficult to ascertain whether the animals were healthy.

Data from these studies were used to compute the pooled prevalence of 3GC^R (cefotaxime, ceftriaxone, cefepime, ceftazidime, cefixime), CARB^R and COL^R in the pool of non-duplicated E. coli strains reported in the individual studies. Only 12 articles met the criteria for further genomic analyses (Supplementary Material 1).

Samples were collected from feces, anal, rectal, and intestinal swabs from healthy humans and animals. Human gut samples were deemed to be from healthy hosts if the methodology explicitly stated “healthy.” Similarly, animal samples were considered eligible if the study indicated the animals were healthy or if the health status description excluded clinical illness. In these studies, the disc diffusion method was most commonly used to determine inhibition zones, although minimal inhibitory concentration testing via broth dilution and E-tests were used for categorizing COL^R. Specific polymerase chain reaction assays were employed to characterize resistance mechanisms for COL and CARB, and some studies used whole-genome sequencing for further characterization. Genomic data from these strains were obtained from NCBI (https://www.ncbi.nlm.nih.gov/) and were used to determine genetic parameters such as the resistome, sequence types (STs), and plasmid content (Supplementary Material 2).

The conserved signature indels phylogeny database from the Center for Genomic Epidemiology (CGE; https://cge.food.dtu.dk/services/CSIPhylogeny/, accessed October 6, 2024) was used to assess the relatedness of genomes from eligible E. coli strains. Single nucleotide polymorphism (SNP) differences among 50 publicly available E. coli genomes (Supplementary Material 3) were determined by mapping to the E. coli strain K-12 substrain MG1655 reference strain (GenBank accession No. GCA_000005845.2) using default parameters, except that the minimum SNP distance was disabled. Graphical data were incorporated into the phylogenies using iTOL version 6.6. STs were determined using MLST version 2.16 (https://cge.food.dtu.dk/services/MLST/). MGEs and AMR genes were identified using PlasmidFinder and ResFinder from the CGE, while CARD (https://card.mcmaster.ca/analyze/rgi) was used to search for additional AMR genes.

MedCalc version 23.0.2 (MedCalc Software Ltd., Ostend, Belgium) and Comprehensive Meta‐Analysis version 4 (Englewood, NJ, USA) were used for all statistical analyses. All statistical tests were 2-tailed, with p-value <0.05 considered statistically significant. The percentage of 3GC^R, COL^R, and CARB^R strains was calculated using the formula:

Prevalence of critically resistant E. coli=(No. of non-duplicated 3GC^R, COL^R, and CARB^R strains)/(No. of total non-duplicated E. coli strains)

Ethics statement

No ethical approval is necessary as this is a systematic review article.

RESULTS

The prevalence of 3GC^R E. coli from eligible studies ranged from 0.4% (95% confidence interval [CI], 0.2 to 1.0) to 94.4% (95% CI, 49.5 to 99.7) (Figure 1A), with significant heterogeneity among studies (I²=97.6, p<0.001). The overall pooled prevalence of 3GC^R E. coli in healthy humans, pets, and livestock was 22.5% (95% CI, 17.5 to 28.3) (Figure 1A) [20-52].

Subgroup analyses showed pooled prevalence rates (PPs) of 3GC^R E. coli of 12.1% (95% CI, 4.7 to 27.7), 17.8% (95% CI, 13.3 to 23.3), and 41.2% (95% CI, 0.0 to 99.9) in humans, livestock, and pets, respectively. Bivariate analysis showed that livestock had the highest pooled odds of 3GC^R E. coli (odds ratio [OR], 3.13; 95% CI, 1.97 to 4.99; p<0.001) (Table 1).

Data analysis from the present study supports the temporal rise increase of 3GC^R E. coli. The pooled prevalence of 3GC^R E. coli from 2020 to 2024 was significantly higher than that from 2014 to 2019 (27.7 vs. 23.2%; OR, 1.27; 95% CI, 1.17 to 1.37, p<0.001) (Table 1). The pooled prevalence of 3GC^R E. coli in Europe was significantly higher (33.2%; 95% CI, 15.0 to 58.4) than in America (17.9%; 95% CI, 11.7 to 26.4), Asia (16.3%; 95% CI, 10.3 to 24.7) and Africa (15.1%; 95% CI, 8.1 to 26.4) (Table 1). In the 19, 8, and 1 studies on E. coli from healthy humans, livestock and pets, respectively, bla_CTX-M was the most common mechanism of 3GC^R (Figure 2).

The overall pooled prevalence of CARB^R E. coli in healthy humans and animals was 2.2% (95% CI, 1.0 to 4.7) with a significant heterogeneity (I²=95.7, p<0.001) (Figure 1B) [26-28,32-35,39,41,49,51-59]. Subgroup analyses showed PPs of 1.2% (95% CI, 0.3 to 4.1), 1.5% (95% CI, 0.5 to 4.7), and 2.3% (95% CI, 0.9 to 6.0) in humans, livestock, and pets, respectively (p>0.05) (Table 1). A meta-analysis based on continent showed that Asia (OR, 21.55; 95% CI, 10.16 to 45.70; p<0.001) and Africa (OR, 8.49; 95% CI, 3.16 to 22.89; p<0.001) had significantly higher PPs of CARB^R E. coli in healthy humans and animals than were observed in Europe (Table 1).

The bla_NDM gene was the predominant mechanism of resistance in most studies that reported the detection of CARB^R E. coli in healthy humans and animals (Figure 2). Furthermore, the pooled prevalence was significantly higher from 2014 to 2019 than from 2020 to 2024 (1.4 vs. 1.9%, p<0.001) (Table 1).

The overall pooled prevalence of COL^R E. coli was estimated to be 15.5% (95% CI, 10.8 to 21.8) with significant heterogeneity (I²=99.3, p<0.001) (Table 1 and Figure 1C) [20-27,29-32,35-38,40,41,43-51,54,60-78]. Subgroup analyses showed PPs of 13.4% (95% CI, 4.3 to 34.9), 13.0% (95% CI, 7.6 to 21.4), and 6.2% (95% CI, 1.3 to 25.0) in humans, livestock, and pets, respectively (p>0.05) (Table 1). The mcr-1 gene was found to be the predominant gene responsible for COL resistance among studies that reported the detection of COL^R E. coli (Figure 2).

The pooled prevalence of COL^R E. coli was highest in the American continent (24.8%; 95% CI, 11.2 to 46.4), followed by Asia (15.8%; 95% CI, 8.3 to 28.2), but significantly lower in Europe (11.4%; 95% CI, 2.1 to 43.1) and Africa (5.1%; 95% CI, 2.4 to 10.7) (Table 1). As with CARB^R E. coli, the pooled prevalence of COL^R E. coli was significantly higher from 2014 to 2019 than from 2020 to 2024 (14.4 vs. 12.0%; OR, 2.42; p<0.001).

Diverse lineages (over 100 STs) were reported, including 13 international high-risk E. coli clones (ST10, ST38, ST58, ST67, ST69, ST88, ST101, ST131, ST167, ST410, ST457, ST405, ST617, ST648), with ST10 predominating in 17 studies (Table 2) [20-29,53-55,60,71]. COL^R and CARB^R E. coli ST10 were reported on all continents except Oceania (Figure 3). Phylogenomic analyses produced 4 clusters of plasmid-mediated CARB^R and COL^R E. coli strains. High relatedness (<25 SNPs) was observed between E. coli strains of ST940-bla_OXA-181 in humans in Lebanon, high-risk ST617-mcr-1 clone in pigs in China, ST46-mcr-1 in poultry in Tanzania, and high-risk ST1720-mcr-1 in goats in France (Figure 4, Supplementary Material 3).

DISCUSSION

Although E. coli are common commensals in the guts of humans and animals, certain extraintestinal strains can cause bloodstream and urinary tract infections [18]. These extraintestinal strains become particularly difficult to treat when they are resistant to 3GC, CARB, and, ultimately, COL. Studies have indicated that pathogenic E. coli strains can be transmitted from food-producing animals to humans through contaminated animal-derived food (foodborne zoonotic E. coli) [7]. Therefore, it is crucial to determine the trends, global prevalence, and molecular epidemiology of critically resistant E. coli in healthy humans, livestock, and pets over the past decade.

Several systematic reviews and meta-analyses on E. coli in sick humans and animals have been published. To our knowledge, this is the first comprehensive and simultaneous meta-analysis of critical-priority E. coli strains in healthy humans, pets, and livestock. When compared with data from diverse human and animal populations globally, the pooled prevalence of 3GC^R E. coli in this study is slightly comparable to the 17% (95% CI, 11 to 23) in humans and 22% (95% CI, 9 to 34) in animals in Bangladesh [19]; and the 17.6% (95% CI, 15.3 to 19.8) previously estimated in healthy individuals [79]. However, it is lower than the 21.1% (95% CI, 19.1 to 23.2) reported in inpatients in healthcare settings in a global meta-analysis [80]. These variations may result from differences in the persistence of 3GC^R, the use of 3GC in patients, and prior selection pressure. Moreover, our study shows a slight decline in global 3GC^R E. coli prevalence in healthy humans compared to that reported by Bezabih et al. [79]. The discrepancy may be due to the longer study period (January 1, 2000 to April 22, 2021) and larger sample size in the study of Bezabih et al. [79], as opposed to our focus on the last decade (2014-2024). The rise in 3GC^R E. coli may be attributable to the misuse of antibiotics, including cephalosporins, during the 2021-2023 coronavirus disease 2019 (COVID-19) pandemic, driven by panic over unknown diseases [81]. This misuse might have facilitated the spread and persistence of 3GC^R through plasmids in tissues of healthy or asymptomatic individuals [82].

Consistent with previous meta-analyses, bla_CTX-M was the major mechanism of resistance in 3GC^R E. coli (Figure 2). For instance, the study of Son et al. [19] reported the predominance of the bla_CTX-M (70%) gene in ESBL-producing E. coli. Moreover, a meta-analysis revealed that 36.3% of all the pooled E. coli strains harbored the bla_TEM1 gene in South Africa [83]. Furthermore, bla_CTX-M was reported to be the most frequent 3GC^R gene in a global meta-analysis of E. coli strains from swine [84]. It is important to mention that there was no single dominant bla_CTX-M gene subtype globally, as the subtype varied per country and region. This is not unexpected as CTX-M (cefotaximase-Munich) and TEM (Temoniera) are the major groups of hydrolytic enzymes that are encoded by various ESBL gene variants [85]. In this systematic review, multiple forms of CTX-M-type enzymes coexisted in several studies (Supplementary Material 2), indicating a potentially serious problem in treating ESBL-producing E. coli once they disseminate from the gut to other tissues.

The high pooled prevalence of 3GC^R E. coli in Europe may be explained by the fact that most European studies (75%) focused on healthy livestock (Supplementary Material 2), a subgroup that showed the highest pooled prevalence. In Asia, a pooled prevalence of 48.6% (95% CI, 35.1 to 62.1) of 3GC^R E. coli was reported in both healthy and sick individuals [86]; this is not surprising given that our study focused solely on healthy humans.

The WHO strongly recommends the urgent development of new antimicrobial agents and control measures against 3GC^R and CARB^R E. coli [8]. Nonetheless, it is essential to determine the global prevalence and extent of dissemination of these strains among different hosts, including healthy humans and animals.

The pooled prevalence of CARB^R E. coli estimated in this meta-analysis is significantly lower than the 9% reported in Pakistan [87], 9.4% in Nigeria [88], and 29.2% in neonatal sepsis in Africa [89]. These variations likely reflect regional differences in CARB misuse and the endemicity of CARB^R Enterobacterales [90].

A global meta-analysis reported a 5% pooled prevalence of CARB^R E. coli in swine [84], which is higher than the 1.5% pooled prevalence obtained from all livestock data in this study. This discrepancy may be explained by the fact that Hayer et al. [84] focused on pigs—the major reservoir of critical resistance genes in E. coli—and included samples from both sick and healthy swine.

The unexpectedly higher CARB^R E. coli prevalence in pets and livestock is notable, especially since CARB antibiotics are not licensed for animal use. CARB antibiotics are rarely prescribed for severely ill humans in some countries due to the complexity of multidrug-resistant Gram-negative bacterial infections [91]. This situation suggests that animals may acquire CARB^R E. coli strains from their owners or farmers, and vice versa [92,93]. Additionally, the higher rate of CARB^R E. coli in healthy animals might indicate greater bacterial persistence in their guts compared to humans [94].

First, the differences among continents likely reflect varying levels of CARB misuse. In European countries, stringent regulations restrict the use of these drugs to human medicine. Second, the lower prevalence of CARB^R in E. coli from 2020-2024 may be attributed to increased awareness and antimicrobial stewardship programs regarding the public health dangers of CARB use, especially in Europe and North America [95].

The pooled prevalence of COL^R E. coli in this study differs from 28% reported in poultry in Southern Asian countries [96], 5.7% from food and livestock samples [97], and 7.6% among nosocomial strains in India [98]. These variations underscore differences in antibiotic selection pressure, antibiotic use policies, and host susceptibility across countries and sample types. Nevertheless, the high pooled prevalence of COL^R E. coli across all study groups underscores the diminishing effectiveness of COL as a last-resort antimicrobial agent. The ubiquitous presence of the mcr-1 gene in all COL^R E. coli strains from the eligible studies further emphasizes the need for robust monitoring and surveillance programs across all hosts, including healthy ones.

This rapidly emerging global pandemic clone was reported in healthy humans, livestock, and pets (Figure 3).

Several studies have documented the detection of 13 different pandemic E. coli clones, highlighting the importance of understanding the diversity and epidemiology of gut E. coli with extra-intestinal genetic backgrounds in healthy humans and animals. These high-risk clones are associated with increased virulence, AMR, and a propensity to cause outbreaks in both healthcare and community settings. Although these high-risk E. coli strains have been identified in healthy hosts, there is a high likelihood that they could cause infections if translocated from the gut to other tissues or organs.

The diversity and co-carriage of resistance genes—encompassing CARB and 3GC^R, COL, and 3GC^R, or even resistance to all 3 antibiotic categories within a single E. coli strain (Supplementary Material 2)—demonstrate the complexity of AMR and could undermine current control measures.

This systematic review and meta-analysis synthesized data from previously published studies to generate pooled prevalence estimates. However, the study has limitations. First, there was substantial heterogeneity among the included studies, and subgroup and meta-regression analyses did not fully account for this variability. For example, PPs of 3GC^R E. coli in livestock may vary among different livestock species, so some prevalence data cannot be generalized. Second, some studies included in the meta-analysis involved a small number of bacterial strains. Caution is also warranted in interpreting some results due to disproportionate distributions of studies by country and host; for instance, only 2 studies involved healthy pets, and no eligible study was found from the Oceania region.

CONCLUSION

COL^R and 3GC^R are significantly more frequent than CARB^R in gut E. coli. This decade-long epidemiological data underscores the persistence and transmission of critical-priority, high-risk E. coli strains among healthy humans and animals. Consequently, individuals may acquire these strains through occupational exposure to livestock or direct contact with companion animals. Although healthy humans and animals may remain asymptomatic despite harboring these critically resistant, high-risk clones, their potential to transmit these superbugs to immunocompromised individuals is concerning.

Furthermore, this review enhances our understanding of the molecular epidemiology of critical-priority E. coli in healthy hosts, highlighting the importance of molecular surveillance for 3GC^R, CARB^R, and COL^R E. coli. As these high-risk strains become more established in healthy populations, future public health strategies should emphasize a One Health approach supported by genomic sequencing technologies.

Supplementary materials

NOTES

Data availability

All the data generated from this study have been presented in the tables, figures and supplementary materials. However, further requests could be made through the corresponding author (INA).

Conflict of interest

The authors have no conflicts of interest to declare for this study.

Funding

None.

Acknowledgements

None.

Author contributions

Both authors contributed equally to conceiving the study, analyzing the data, and writing this paper.

Figure 1.

Forest and funnel plot and pooled prevalence of (A) third-generation cephalosporin-resistant, (B) carbapenem-resistant, and (C) colistin-resistant Escherichia coli in healthy humans, livestock, and pets. SE, standard error; CI, confidence interval; df, degrees of freedom.

Figure 2.

Frequency of studies that reported the mechanisms of (A) carbapenem, (B) colistin, and (C) third-generation cephalosporin resistance in Escherichia coli from healthy humans and animals. The number of studies used for computing the frequencies is presented in Table 1.

Figure 3.

Distribution pattern of colistin- and carbapenem-resistant Escherichia coli of the global pandemic sequence type 10 clone.

Figure 4.

Phylogenomic analysis of 50 publicly available COL-resistant and CARB-resistant Escherichia coli mapped against the reference strain, E. coli strain. K-12 substrain MG1655 (GenBank accession No. GCA_000005845.2). COL, colistin; CARB, carbapenem; SNP, single nucleotide polymorphism; ST, sequence type.

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