Phenotypic and Genotypic Prevalence of Extended-Spectrum β-Lactamase-Producing Escherichia coli : A Systematic Review and Meta-Analysis in Iran

Abstract

Background:

Despite the existence of discrete and varied studies regarding extended-spectrum β-lactamase-producing Escherichia coli (ESBL-EC) in Iran, a comprehensive analysis on the prevalence of ESBL-EC has not yet been carried out. The current study analyzed published data regarding ESBL-EC in different regions of Iran to gain insight into this significant subject.

Methods:

A meta-analysis was performed using Comprehensive Meta-Analysis Software (version 2.2; Biostat) to determine the prevalence of ESBL-EC in Iran. A web-based search was conducted in electronic databases, including PubMed, Scopus, and Web of Sciences. The eligibility of articles published between 2008 and 2018 was assessed, and relevant data were extracted for statistical analysis. A random-effects model was used based on the heterogeneity test. Publication bias was determined using Begg's rank correlation and Egger's weighted regression methods.

Results:

Among 31,135 studies examined, 61 met inclusion criteria and were included for review. Iran's overall pooled proportion of ESBL-EC was 43.2% (confidence interval [95% CI] 39.2–47.3), and the overall heterogeneity (I²) between studies was significantly high (93.5%, p = 0.00). The most prevalent of ESBLs in E. coli was CTX-M and TEM, with prevalence of 31.2% (95% CI 25.4–37.6), 27.6% (95% CI 22.7–33.2), respectively.

Conclusion:

The available studies show a high rate of ESBL-EC in Iran. This result highlights a need for appropriate and rapid methods for estimating ESBL infection, which can help our understanding of the actual epidemiology of ESBL and provide protocols for the prevention and control of infection.

Introduction

Extended-spectrum β-lactamases (ESBLs) are the most common resistance mechanism of Gram-negative bacteria against β-lactam antibiotics.¹ These enzymes are able to hydrolyze aztreonam and third-generation cephalosporins but not carbapenems (imipenem and meropenem) or cephamycins (cefoxitin, cefotetan). ESBL enzymes are inhibited by clavulanic acid, tazobactam, and sulbactam. Based on Ambler's structural classification, which relies on sequence similarity, most of these enzymes belong to class A β-lactamases.^2,3 The most important β-lactamase genes are variants of CTX-M, SHV, TEM, VEB, GES, PER, TLA, and OXA, which are found mostly in Escherichia coli (E. coli) and Klebsiella spp.^4–6

The presence of these resistance genes on mobile genetic elements such as plasmids results in their dissemination within and between bacterial species.⁷ Many ESBL-producing strains of E. coli and Klebsiella pneumoniae are multidrug resistant and the emergence of these organisms is now a serious concern for the development of therapies against bacterial infection.^8,9 In a recent study, some of the new drugs active against multidrug-resistant bacteria, including ESBL-producing ones, were reported. Among them, ceftazidime–avibactam and ceftolozane–tazobactam have already received U.S. Food and Drug Administration (FDA) approval.¹⁰ The conjugative transfer of multidrug resistance-mediating plasmids are of major concern and represents the urgent need of molecular analysis for pathogens harboring them.⁴ Infections caused by extended-spectrum β-lactamase-producing E. coli (ESBL-EC) are increasing globally, in both hospitals¹¹ and community environments,¹² and these multidrug-resistant organisms have higher mortality rates and medical costs than those due to non-β-lactamase-producing strains.¹³ Thus, the surveillance of these ESBL-EC is remarkable for clinical care, and it is important to take into consideration the needs of careful choosing of antibiotic therapy to control this issue in many countries. Phenotypic approaches to determine the prevalence of ESBL-EC isolated from various clinical samples as well as detection of genes conferring resistance against many life-saving antibiotics have shown the increased incidence of infections due to the presence of these E. coli strains and may explain a probable cause of antibiotic treatment failure in Iran and other countries.^14–16 However, to date, no data on this subject from a comprehensive study in Iran have become available.

The present systematic review and meta-analysis was performed based on the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement¹⁷ to determine the prevalence of ESBL-EC with different gene variants in Iran (Supplementary Table S1).

Methods

Search strategy and selection criteria

For this systematic review and meta-analysis, a literature search was performed to identify articles reporting infections caused by ESBL-EC strains among Iranian patients. Two reviewers searched three major electronic databases (PubMed, Web of Science, and Scopus) from January 2008 to December 2018. The search terms included ^“E. coli” or “E. coli,” “extended-spectrum β-lactamases” or “ESBLs” together with “Iran.” The search was limited to published articles containing the desired keywords in the English language. Identified publications were then checked individually to eliminate any duplicates or irrelevant articles. To be eligible for inclusion, articles had to report both phenotypically detected ESBL-EC and the presence of at least one ESBL-coding gene by the PCR method among these isolates. Comments, editorials, reviews, letters, case reports, congress abstracts, meta-analyses, systematic reviews, and overlapping studies were not examined. Nonhuman studies and articles in which ESBL production detection was only restricted to either phenotypic or genotypic methods were also excluded.

Data extraction and definitions

The following details were extracted from all screened articles: first author's name; duration of study; year of publication; city in which the study was conducted; total number of isolates; and prevalence of phenotypically detected ESBL-EC and genes encoding ESBLs.

Quality assessment of studies

A quality assessment was performed independently by two authors using a checklist provided by the Joanna Briggs Institute (JBI).¹⁷ Any disagreements were resolved through discussion with a third author. The checklist consisted of 10 questions to which the reviewers responded individually for each study. A “Yes” answer for each question received a point. Scores ranged from 0 to 10, and studies that attained >7 points were entered into the review.

Statistical analysis

Comprehensive Meta-Analysis v.2.2 (Biostat, Englewood, NJ) was used for the meta-analyses. Based on the heterogeneity between different studies, the random-effects model was used. Statistical heterogeneity among the included studies was assessed using Cochran's Q and the inconsistency I² tests. In cases of significant heterogeneity (p < 0.1 or I² >50%), the random-effects model was applied; otherwise, the fixed-effects model (p > 0.1 and I² <50%) was used. Funnel plots, Begg's test, and Egger's test were used to detect publication bias, and p < 0.05 was regarded as statistically significant.

Results

Results of the critical appraisal (JBI checklist) of the included studies are presented in Supplementary Table S1. Sixty-one studies presented a low risk of bias (quality assessment score >7).

Electronic database searches yielded a total of 3,135 studies. After removal of duplicates, the titles and abstracts of 2,863 articles were screened, of which 123 were included in the full-text screening (Fig. 1). Sixty-one studies met the inclusion criteria and were included in the main meta-analysis (Table 1).^18–78 The pooled prevalence of phenotypically detected ESBL-EC was 43.2% (confidence interval [95% CI] 39.2–47.3). The pooled prevalence rates of detected CTX-M, TEM, SHV, OXA-48, and VEB genes were 31.2% (95% CI 25.4–37.6), 27.6% (95% CI 22.7–33.2), 9.8% (95% CI 6.7–14), 8.3% (95% CI 4.1–15.9), and 2.3% (95% CI 1.2–4.4), respectively (Table 2). Heterogeneity between studies was determined by the random-effects model, and the results were as follows: I² = 93.5, p = 0.00 for ESBL-EC; I² = 96, p = 0.00 for CTX-M, I² = 95, p = 0.00 for TEM, I² = 95, p = 0.00 for SHV, I² = 93, p = 0.00 for OXA-48, and I² = 90, p = 0.00 for VEB (Table 2). As shown in Table 2, no publication bias was revealed for ESBL-EC (Begg's test, p = 0.4, Egger's test, p = 0.5), CTX-M (Begg's test, p = 0.5, Egger's test, p = 0.3), or TEM (Begg's test, p = 0.4, Egger's test, p = 0.4), but was observed for SHV (Begg's test, p = 0.004, Egger's test, p = 0.0009). For OXA-48, no publication bias was revealed by Begg's test (p = 0.5), but it was detected by Egger's test (p = 0.01). The prevalence rate of ESBL-EC as well as those of SHV, CTX-M, TEM, and VEB genes were determined in forest plots (Fig. 2). The publication bias among the evaluated articles was assessed using funnel plots (Fig. 3).

FIG. 1.

Summary of the literature search and study selection.

FIG. 2.

Forest plot of studies included in the meta-analysis in the present meta analysis: prevalence of (A) ESBL-EC, (B) the CTX-M gene among ESBL-EC (C) the TEM gene among ESBL-EC, (D) the SHV gene among ESBL-EC, (E) the OXA-48 gene among ESBL-EC, (F) the VEB gene among ESBL-EC. ESBL-EC, extended-spectrum β-lactamase-producing Escherichia coli.

FIG. 3.

Funnel plot of publication bias for the included studies in the present meta analysis: prevalence of (A) ESBL-EC, (B) the CTX-M gene among ESBL-EC, (C) the TEM gene among ESBL-EC, (D) the SHV gene among ESBL-EC, and (E) the OXA-48 gene among ESBL-EC. The asymmetric shape of the funnel plots indicates bias in the meta-analysis. Each study is represented by a circle.

Table 2.

Meta-Analysis of Extended-Spectrum β-Lactamase-Producing Escherichia coli and Genes Encoding Extended-Spectrum β-Lactamases

Subgroups	No. of study	Prevalence (95% CI)	n/N	Heterogeneity test, I² (%)	Heterogeneity test, p	Begg's test	Egger's test
ESBL^-producing E. coli*	61	43.2 (39.2–47.3)	4,591/10,438	93.5	0.000	0.4	0.5
ESBLs-genes
CTX-M	44	31.2 (25.4–37.6)	2,381/7,362	96	0.000	0.5	0.3
TEM	44	27.6 (22.7–33.2)	1,976/7,249	95	0.000	0.4	0.4
SHV	36	9.8 (6.7–14)	804/6,237	95	0.000	0.004	0.0009
OXA-48	5	8.3 (4.1–15.9)	159/1,537	93	0.000	0.5	0.01
VEB	2	2.3 (1.2–4.4)	9/396	90	—	—	—

extended spectrum beta-lactamase.

CI, confidence interval.

Table 1.

Characteristics of Studies Included in the Meta-Analysis

Study	Enrollment time	Published time	Province	Total No. of E. coli	Phenotypically ESBLs producers		ESBL genes detected by PCR
Study	Enrollment time	Published time	Province	Total No. of E. coli	No. of ESBL-EC	Detection method	CTX-M	SHV	TEM	OXA-48	PER	VEB	GES
Mirzaee¹⁸	2006	2008	Tehran	160	89	Combined disk	34	—	—	—	—	—	—
Mirzaee¹⁹	2007–2008	2009	Tehran	250	140	Combined disk	50	—	—	—	—	—	—
Shahcheraghi²⁰	2006–2007	2010	Tehran	260	125	Phenotypic confirmatory test	53	15	63	—	—	—	—
Soltan Dallal²¹	Not determined	2010	Tehran	200	128	Combined disk	—	—	74	—	—	—	—
Kalantar²²	2007–2008	2010	Kerman	138	94	Combined disk	22	48	60	—	—	—	—
Pakzad²³	2007–2008	2011	Tehran	150	42	Disk diffusion	—	11	40	—	—	—	—
Soltan Dallal²⁴	2009	2011	Tehran	200	128	DDST	99	—	—	—	—	—	—
Soltan Dallal²⁵	2009–2010	2011	Tabriz	188	82	Combined disk	69	—	—	—	—	—	—
Sharifi Yazdi²⁶	2008–2009	2011	Tehran	200	115	Combined disk	—	—	74	—	—	—	—
Sharifi Yazdi²⁷	2009–2010	2011	West Azerbaijan	188	56	Combined disk	49	—	—	—	—	—	—
Moosavian²⁸	2007–2008	2012	Dezful	271	78	Combined disk	—	1	31	—	—	—	—
Nakhaei²⁹	2009	2012	Mashhad	111	37	DDST	35	5	21	—	—	—	—
Zaniani³⁰	2009–2010	2012	Mashhad	82	25	Combined disk	—	6	5	—	—	—	—
Hashemi³¹	2010–2011	2013	Hamedan	82	25	Disk diffusion method	—	4	2	—	—	—	—
Soltan Dallal³²	Not determined	2013	Tehran	200	128	DDST	—	7	—	—	—	—	—
Abdi³³	2010–2011	2014	Tehran	100	20	DDST	87	65	82	—	—	—	—
Khoshvaght³⁴	2012–2013	2014	Zanjan	36	19	Disk diffusion	12	—	8	—	—	—	—
Kargar³⁵	2011–2012	2014	Jahrom	206	17	DDST	—	2	5	—	—	—	—
Mansouri³⁶	2007–2008	2014	Kerman	338	148	Combined disk	45	—	—	—	—	—	—
Hemati³⁷	2012	2014	Hamedan	132	56	Disk diffusion	—	18	37	—	—	—	—
Gholipour³⁸	2011–2012	2014	Isfahan	245	107	DDST	—	8	13	—	—	—	—
Manouchehri^{3 9}	Not determined	2015	Sari	120	66	Combined disk	40	—	—	—	—	—	—
Memariani⁴⁰	2011–2013	2015	Tehran	42	9	Combined disk	8	17	8	—	—	—	—
Rezai⁴¹	Not determined	2015	North of Iran	327	100	MIC test	28	44	49	—	—	8	—
Zeighami⁴²	2012–2013	2015	Zanjan	200	66	Combined disk	50	37	31	—	—	—	—
Zamani⁴³	2012	2015	Shiraz	376	202	Combined disk	185	—	—	—	—	—	—
Alizade⁴⁴	2013	2015	Kerman	216	56	DDST	52	—	—	—	—	—	—
Sedighi⁴⁵	2010–2011	2015	Hamedan	120	33	DDST	34	2	9	—	—	—	—
Arabi⁴⁶	2007–2012	2015	Ilam, Tehran	144	72	Disk diffusion	24	48	76	—	—	—	—
Shayan⁴⁷	2011–2012	2015	Zahedan	90	37	Combined disk	3	—	29	—	—	—	—
Ghorbani-Dalini⁴⁸	2010	2015	Shiraz	54	7	DDST	11	17	45	—	—	—	—
Harifi⁴⁹	2011–2012	2015	Mashhad	200	85	Disc diffusion	—	23	65	—	—	—	—
Hasani⁵⁰	2014	2015	North west of Iran	146	128	DDST	135	111	105	—	—	—	—
Moosavi⁵¹	Not determined	2015	Sanandaj	100	27	Combined disk	2	—	—	—	—	—	—
Peerayeh⁵²	2009–2010	2016	Tehran	63	35	Combined disk	13	—	24	—	—	—	—
Dizaji⁵³	Not determined	2016	Tabriz	100	46	Combined disk	—	—	23	—	—	—	—
Bialvaei⁵⁴	2012–2013	2016	Tehran, Kurdistan, Sistan and Baluchestan, Mazandaran, Khuzestan, Fars	198	54	Disk diffusion	151	—	—	—	—	—	—
Akya⁵⁵	2012–2013	2016	Kermanshah	240	67	Combined disk	61	—	—	—	—	—	—
Damavandi⁵⁶	2013–2014	2016	Shahrekord	200	90	DDST	—	—	—	17	—	—	—
Tabar⁵⁷	2015	2016	Semnan	109	29	combined disc	20	—	—	—	—	—	—
Sharifi-Rad⁵⁸	2014	2016	Shiraz	295	107	DDST	—	—	97	—	—	—	—
Haghighatpanah⁵⁹	2015	2016	North of Iran	160	83	DDST	72	—	27	—	—	—	—
Jafari⁶⁰	2013–2014	2016	Ahvaz	150	24	Disk diffusion	52	8	28	—	—	—	—
Bagheri-Nesami⁶¹	2014–2015	2016	North of Iran	69	6	DDST	—	6	1	—	—	1	1
Tayebi⁶²	2013–2014	2016	Sari	225	97	DDST	14	31	45	—	—	—	—
Namaei⁶³	2012–2013	2017	Birjand	384	168	Disk diffusion	66	25	43	—	—	—	—
Kalantar-Neyestanaki⁶⁴	2014–2015	2017	Kerman	86	84	BETA-lactamase disk Test	64	2	53	—	—	—	—
Koshesh⁶⁵	2014–2015	2017	Kerman	105	42	DDST	—	1	32	—	—	—	—
Yousefi-Fatmesari⁶⁶	2015	2017	Kermanshah	95	24	Combined disc	11	1	9	—	—	—	—
Goudarzi⁶⁷	2015–2016	2017	Tehran	290	150	DDST and combined disc	120	76	106	—	—	—	—
Hojabri⁶⁸	2015–2016	2017	Semnan	339	115	Combined disk	—	56	84	15	—	—	—
Solgi⁶⁹	2015–2016	2017	Not determined	32	26	Disk diffusion	23	3	17	—	—	—	—
Zamani⁷⁰	2015–2016	2017	Rasht	70	37	Combined disc	11	4	22	—	—	—	—
Karami⁷¹	2016	2017	Tehran, Ilam, Mazandaran	192	153	DDST	21	23	26	14	—	—	—
Soltan-Dallal⁷²	2013–2014	2018	Not determined	50	4	Combined disc	4	—	—	—	—	—	—
Roshani⁷³	2014–2015	2018	Tehran	56	38	Combined disc	37	—	—	—	—	—	—
Hashemizadeh⁷⁴	2014–2015	2018	Kerman	351	163	Combined disk	124	2	122	21	—	—	—
RohamRad⁷⁵	2015	2018	Tehran	100	63	Combined disk	71	44	62	—	—	—	—
Mansour Amin⁷⁶	2015–2016	2018	Ahwaz	32	23	Disk diffusion	21	—	28	—	—	—	—
Shahbazi⁷⁷	2016–2017	2018	Tehran	120	81	Combined disk	76	12	80	—	—	—	—
Moghanni⁷⁸	2015	2018	Mashhad	455	235	Combined disk	222	21	115	92	—	—	—

DDST, Double-Disk Synergy Test; ESBL-EC, extended-spectrum β-lactamase-producing Escherichia coli.

Discussion

To the best of our knowledge, this is the first systematic review and meta-analysis addressing the prevalence of phenotypically detected ESBL-EC and ESBL genes among isolates recovered from patients in Iran. Based on this meta-analysis, a high rate of ESBL-EC was detected phenotypically (43.2%; 95% CI 39.2–47.3) in Iran. A lower prevalence of ESBL-EC was reported in other Middle Eastern countries, such as Egypt (36%)⁷⁹ and Saudi Arabia (33%).⁸⁰ However, the high prevalence of this phenotype in Iran is highlighted more when compared with developed countries such as Denmark (1.5%),⁸¹ France (3.3%),⁸² and Germany (8.0%).⁸³ The overall pooled proportion of ESBL-producing Enterobacteriaceae was estimated to be 42% in East Africa, which is close to the data reported in the current study.⁸⁴ In general, there are several possible factors, which may account for the variations observed between the present study and other reports. One of them is the difference between the sensitivity and specificity of phenotypic methods applied for ESBL detection in various studies.⁸⁴ The socioeconomic status of a society and availability of antibiotics which result in self-medication, consumption of counterfeit drugs, improper dosage, and nonadherence to antibiotic therapy^84,85 may explain the higher prevalence of antibiotic resistance, particularly that of ESBL, in developing countries than in developed nations. Poor knowledge about antibiotic resistance as well as irrational use of antibiotics have contributed to the progressive loss of bacterial sensitivity to antibiotics and dissemination of resistant strains of bacteria, with substantial clinical and economic impact⁸⁶ such as treatment failure or increase morbidity and mortality in serious infections. Making both physicians and health care workers aware of this problem may prevent the mistreatment of infections and promote strong hygiene practices, which will ultimately reduce the risk of the spread of resistant infections in communities, even those with the most advanced and sophisticated health care systems.

Despite the high costs and limited availability of methods for detecting gene variants in β-lactamase-producing bacteria, the available methods allow for a more accurate characterization of resistance mechanisms among clinical isolates and provide necessary information for the appropriate and successful treatment of patients. Some ESBL genes, such as TEM and SHV, are mutant derivatives of established plasmid-mediated β-lactamases, while others are mobilized from environmental bacteria (e.g., CTX-M).⁷ It was noted that the most common gene variants in Iranian studies are those encoding CTX-M, TEM, and SHV, whereas only five and two studies reported the presence of OXA-48 and VEB genes, respectively. Based on statistical analysis, the most prevalent ESBL genes were CTX-M (31.2%) and TEM (27.6%); the former was less prevalent than mentioned by Abrar et al.,⁸⁷ who reported the prevalence of the CTX-M group (50%) in studied articles from Pakistan. The global prevalence of CTX-M ESBLs has been increasing since 2000,⁸⁸ and E. coli from the family Enterobacteriaceae is the predominant carrier of these genes.^89,90 The global spread of CTX-M genes is fundamentally due to their horizontal gene transfer on conjugative plasmids,⁹¹ which may be an important explanation for the high incidence of CTX-M β-lactamase-producing E. coli in the present study as well as other reported investigations from Tunisia⁹² and China.⁹³ However, other possible reasons contribute to the global dissemination of this gene, such as the clonal spread of virulent strains of E. coli carrying CTX-M group genes, the possible colonization of CTX-M variants in some animal gut and raw meat used for human consumption, contamination of the environment, and poor standards of sanitation which result in increased cycling of CTX-M-producing E. coli between humans and the environment, particularly in developing countries.^94,95 Finally, higher carriage rates of the CTX-M group-producing E. coli among individuals with ethnic origins in the Middle East or South Asia than in Europeans⁹⁵ may explain the current findings of a significant upward trend in ESBL community carriage rates in Iran, which is not only located in the Middle East, but is also known as a host country for Afghan and Pakistani immigrants. Although no report is available regarding the frequency of ESBLs in Afghanistan, the high acquisition of ESBL Enterobacteriaceae by French military personnel assigned to Afghanistan⁹⁶ and the indication of a high ESBL burden in Pakistan⁸⁶ may confirm the last explanation as one of the probable factors responsible for the high prevalence of ESBL genes in Iran. Moreover, result showing the worldwide predominance of sequence type 131(ST131) clone, as an explanation for alarming increase in the isolation of CTX-M-15-producing E. coli isolates, was also confirmed in a recent comparative analysis reported from Iran, which found a predominance of CTX-M-15 among ESBL-producing ST131 E. coli isolates and so, a significant association of ST131 with CTX-M-15.⁹⁷

Although the current systematic review and meta-analysis addressed key points in the prevalence of ESBL-E. coli from Iran, a number of limitations must be taken into account. Only published articles resulting from an English search were considered, so language bias should be considered. Furthermore, various areas in Iran have not been screened to target the subject of the current meta-analysis. Variations in study outcomes resulted mainly from differences in the different mix of in- and outpatients between studies and may also vary throughout the study period. The observed heterogeneity contributed to the variations in findings too. A further limitation is that the small sample sizes in a few studies caused wide CIs in some subanalyses.

It was ultimately attained that the high prevalence of ESBL-EC in Iran indicated in the present meta-analysis calls for active surveillance systems for monitoring the presence and spread of these organisms. The findings also highlight the necessity of developing proper screening guidelines for ESBL detection as well as targeted strategies to manage patients colonized with ESBL-EC and prevent antibiotic resistance in the community. Applying novel approaches such as patient-held electronic records⁹⁸ would also improve communication between physicians and laboratories, aid in managing medications, and restrict further transmission of disease to the wider community.

Footnotes

Disclosure Statement

No competing financial interests exist.

Funding Information

This research has been supported by Tehran University of Medical Sciences & Health Services grant 97-01-30/38060.

Supplementary Material

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