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Prevalence of [bla.sub.CTX-M] Gene among Extended-Spectrum [beta]-Lactamases Producing Klebsiella pneumoniae Clinical Isolates in Iran: A Meta-Analysis.


Extended-spectrum [beta]-lactamases (ESBLs) are bacterial enzymes that confer resistance to penicillins, broad-spectrum oxyimino-cephalosporins and aztreonam, but suppressed by serine-type [beta]-lactamase inhibitors (e.g. clavulanic acid). ESBLs can be encoded through both chromosome and plasmid genes, and more than ten families have been so far documented to be associated with ESBLs, including CTX-M, SHV, TEM, PER, VEB, BES, GES, TLA, SFO, and OXA. (1-3) CTX-M-type ESBLs are plasmid-encoded enzymes that have been detected in at least 26 bacterial species. CTX-Ms are the most prevalent ESBLs in Enterobacteriaceae particularly in Escherichia coli, Klebsiella pneumoniae, and Proteus mirabilis. (1,3-5) A member of the Enterobacteriaceae family, K. pneumoniae strains are ubiquitous in nature and exist specifically in natural environments and on mucosal surfaces of mammals. This microorganism is an opportunistic bacterial pathogen that commonly causes different infections in human. (6-8) K. pneumoniae is one of the major ESBLs-producing bacteria. ESBLs-producing K. pneumoniae is more prevalent in Asia and South America, (9) and has recently been listed as one of the six drug-resistant pathogens for which few potentially effective drugs are available. (10) The worldwide spread of CTX-M-producing K. pneumoniae is a major concern in most continents such as Asia. (11-13) Recently, high rate of CTX-M enzymes (as high as 58.5%) among ESBLs-producing K. pneumoniae isolates have been reported in many countries including Brazil, (12) Spain, (14) Korea, (15) etc.

To date, several studies have examined the prevalence of CTX-Ms in ESBLs-producing K. pneumoniae clinical isolates in different geographical regions of Iran. Nevertheless, the average rate of CTX-M enzymes among ESBLs-producing K. pneumoniae isolates has not been clearly identified in Iran. Therefore, in this meta-analysis, we reviewed published studies regarding the prevalence of [bla.sub.CTX-M] gene among ESBLs-producing K. pneumoniae clinical isolates in Iran and presented an overall relative frequency (RF).

Materials and Methods

Search Strategy

To identify all related published studies, we searched PubMed, Scopus, EBSCO, Embase, Google Scholar, Scirus and four Persian scientific search engines including IranMedex, IRANDOC, Magiran, and scientific information database (SID) in both English and Persian. The medical subject headings (MESH) and keywords used for the search were "Enterobacteriaceae" and "Klebsiella pneumoniae or K pneumoniae" and "Extended-spectrum [beta]-lactamases or ESBLs" and "CTX-M" and "Iran". The searched keywords were adapted to the primary language of the database. We also searched the references cited in these articles to find other relevant articles. Selected articles were published between July 2010 and July 2016 and all of them were in English.

Inclusion Criteria

Among obtained articles/abstracts, those with the following features were included in the study: a- Articles that have assessed the prevalence of [bla.sub.CTX-M] gene

b- Clinical isolates that were collected from Iranian hospitals

c- Clinical isolates that were taken from patients (both inpatients and outpatients)

d- Samples that only belonged to the genus Klebsiella, species pneumoniae

e- Phenotypic confirmatory ESBL test (either combination disk test or double disc synergy test) which were used to detect ESBL production

f- Only ESBLs-producing isolates which were confirmed by phenotypic ESBL test.

Exclusion Criteria

Studies with at least one of the following criteria were excluded from our study:

a- Samples that were totally/partially selected from ESBLs collections

b- The origin of samples (region or population) was not clear

c- Unclear report of the results

Statistical Analysis

Statistical analysis was executed by the STATA software, version 11.0 (StataCorp, College Station, TX, USA). The overall RF of CTX-M in Iran was pooled by forest plot using the Meta-Analyst software. Heterogeneity among studies was assessed by Cochrane's Q-test and [I.sup.2] measurement, which was interpreted as the proportion of total variation contributed among study variants. A P[less than or equal to]0.10 and an [I.sup.2] value [greater than or equal to]50% shown significant heterogeneity. A random-effect model was applied in the incidence of significant heterogeneity; if not, a fixed-effect model was executed.


According to heterogeneity test, random model methods were performed for meta-analysis tests (P<0.001). The [I.sup.2]>50% indicated the presence of heterogeneity in our pooled analysis.

Out of all papers found by the search of databases, 24 articles matched our inclusion criteria (20 full-text articles and 4 abstracts) selected for our pooled analysis (16-35) (table 1). A detailed flowchart showing the selection process is presented in figure 1. These studies were conducted in 10 provinces and 11 cities of Iran. The prevalence of ESBLs among K pneumoniae clinical isolates varied from 28% in Kerman (21) to 74% in Tehran, (19) with the mean of 49%. The prevalence of [bla.sub.CTX-M] gene among ESBLs-producing K. pneumoniae clinical isolates varied from 7.7% in Tabriz (19) to 100% in Mashhad, Tehran and Zahedan, (23,33,35) with the mean of 56.7%. In Tehran, the capital city of Iran, the prevalence of [bla.sub.CTX-M] gene among ESBLs-producing K. pneumoniae clinical isolates varied from 20.6% to 100%, with the mean of 61.7%. (18,19,27-33) Pooled estimation of K. pneumoniae samples revealed that 55.9% (95% CI=43.0-68.9) of strains are CTX-M positive. Figure 2 demonstrates the forest plot of the relative frequency of [bla.sub.CTX-M] gene among different studies performed in Iran.


In recent years, numerous studies by Iranian researchers have been conducted to identify [bla.sub.CTX-M] gene variants among ESBLs-producing K. pneumoniae clinical isolates. Based on these studies, this review presented a meta-analysis to show the prevalence of [bla.sub.CTX-M] gene among ESBLs-producing K. pneumoniae clinical isolates in Iran. Based on our results, the CTX-M-type ESBLs-producing K. pneumoniae is less frequent in western cities compared to central and eastern cities. The mean prevalence of ESBLs among K. pneumoniae clinical isolates in Iran was 49% that, on average, 56.7% of these isolates (ESBLs-producing isolates) possessed [bla.sub.CTX-M] gene. Lee et al., (11) in their study on K. pneumoniae clinical isolates in 9 Asian countries have shown that ESBLs-production rates differed amongst the studied countries. The percentage of ESBLs-producers was low in Hong Kong and Taiwan (7.7% and 8.3%, respectively), but was high in South Korea, India, and Thailand (66.7%, 57.1%, and 55.3%, respectively). Moreover, they showed that 72.8% of ESBLs-producing isolates were possessed [bla.sub.CTX-M] gene which amongst, [bla.sub.CTX-M-15] was the major variant. Similarly, in Iran, the sequencing results in some studies demonstrated that the major variants of [bla.sub.CTX-M] gene among ESBLs-producing K. pneumoniae clinical isolates are [bla.sub.CTX-M-15] (23,26,29,30,32,35-37) followed by [bla.sub.CTX-M-8], (35,36) [bla.sub.CTX-M-3] and [bla.sub.CTX-M-22]. (26) From a regional stand, Iran has a higher mean prevalence of [bla.sub.CTX-M] gene among ESBLs-producing K. pneumoniae clinical isolates compared to reports from neighboring countries including Turkey (30%), (38,39) Saudi Arabia (35.3%), (40,41) Iraq (45.2%), (42,43) and Bahrain (10%) (44) as well as lower mean prevalence compared to Pakistan (96.9%), (45,46) Kuwait (100%), (47) and United Arab Emirates (64.4%). (48) In a continental perspective, Iran has a lower mean prevalence of [bla.sub.CTX-M] gene among ESBLs-producing K. pneumoniae clinical isolates compared to reports from East Asian countries (78.8%). (11,49) At the international level, mean prevalence of [bla.sub.CTX-M] gene among ESBLs-producing K. pneumoniae clinical isolates in Iran is higher than USA (26.4%), (50) Russia (34.9%), (51) and South Africa (7.4%) (39) as well as lower than Brazil (62.1%) (12,52) and Argentina (61.1%) (39) in Latin America and some European countries (84.5%). (9,53-56)

Our study had some limitations, including lack of published data from certain regions of Iran and the unavailability of some in-press articles that were excluded from our study.


In conclusion, this study showed that the prevalence of CTX-M-type ESBLs-producing K. pneumoniae is diverse in different regions of Iran, and the central and eastern regions have higher RF compared to western regions.


The authors appreciate all individuals who willingly participated in the present study. This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflict of Interest: None declared.


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Ebrahim Eskandari-Nasab (1,) (2), MSc;

Mehdi Moghadampour (3), MSc;

Arezoo Tahmasebi (4), MSc

(1) Genetic of Non-Communicable Disease Research Center, Zahedan University of Medical Sciences, Zahedan, Iran;

(2) Department of Clinical Biochemistry, School of Medicine, Zahedan University of Medical Sciences, Zahedan, Iran;

(3) Department of Microbiology, School of Medicine, Isfahan University of Medical Sciences, Isfahan, Iran;

(4) Department of Statistical and Actuarial Sciences, University of Western Ontario (UWO), London, ON, Canada


Mehdi Moghadampour, MSc; Department of Microbiology, School of Medicine, Isfahan University of Medical Sciences, P. O. Box: 81746-73461, Isfahan, Iran

Tel: +98 913 9351772

Fax: +98 31 36688597


Received: 01 November 2016

Revised: 20 December 2016

Accepted: 01 January 2017

What's Known

* Several studies have examined the prevalence of CTX-Ms in ESBLs-producing K. pneumoniae clinical isolates in different geographical regions of Iran.

* The average rate of CTX-M enzymes among ESBLs-producing K. pneumoniae isolates has not been clearly identifed in Iran.

What's New

* We reviewed published studies regarding the prevalence of [bla.sub.CTX-M] gene among ESBLs-producing K. pneumoniae clinical isolates in Iran and presented an overall relative frequency (RF).

* The overall RF of [bla.sub.CTX-M] gene among ESBLs-producing K. pneumoniae clinical isolates in Iran is 56.7%.
Table 1: Characteristics of studies included in meta-analysis

City     Hospitals name         Sample  Number
                                size    of isolates
                                        carrying the
                                        [bla.sub.CTX-M] gene

Ahvaz    Golestan, Razi         26       7
Arak     Educational hospitals  41      36
         of Medical University
Ilam     Emam Khomaini,         43      10
         Mostafa Khomaini,
Ilam     Emam Khomaini,         17       5
         Mostafa Khomaini,
Kashan   Hospitals in Kashan    35      28
Kerman   Afzali Poor, Kashani,  33      16
Kerman   Hospitals in Kerman    31       6
Mashhad  Qaem, 17-Shahrivar      9       9
Shiraz   Namazi                 36      25
Tabriz   Emam Reza              45       7
Tabriz   Sina                   45      26
Tabriz   Emam Reza              21       4
Tabriz   Emam Reza              13       1
Tehran   10 hospitals           102     73
Tehran   3 general and          77      45
         2 private hospitals
Tehran   Hospitals in Tehran    72      45
Tehran   Milad                  68      14
Tehran   Taleghani, Mofid       48      30
Tehran   Taleghani, Mofid       48      28
Tehran   Mofid                  19      18
Tehran   Milad                  37      10
Tehran   Loghman-E Hakim,       17      17
         Imam Khomeini,
Zabol    Amir Al-Momenin        20      13
Zahedan  Ali ibn Abi Talib,     51      51
         Khatamal Anbiya,
City     Relative            Study                    Year
         frequency           team (reference no.)     published
         of [bla.sub.CTX-M]
         gene (%)

Ahvaz     26.9               Khosravi et al. (16)     2013
Arak      87.8               Safari et al. (17)       2013
Ilam      23.3               Ghafourian et al. (18)   2012
Ilam      29.4               Ghafourian et al. (19)   2011
Kashan    80                 Firoozeh et al. (20)     2014
Kerman    48.5               Mansouri et al. (21)     2014
Kerman    20                 Mansouri et al. (22)     2012 (abstract)
Mashhad  100                 Moghaddam et al. (23)    2014
Shiraz    69.4               Ghasemi et al. (24)      2013
Tabriz    15.5               Ghafourian et al. (25)   2011
Tabriz    57.8               Pormohammad et al. (26)  2014 (abstract)
Tabriz    19                 Ghafourian et al. (18)   2012
Tabriz     7.7               Ghafourian et al. (19)   2011
Tehran    71.6               Nematzadeh et al. (27)   2011
Tehran    58.4               Nasehi et al. (28)       2010

Tehran    62.5               Peerayeh et al. (29)     2014 (abstract)
Tehran    20.6               Ghafourian et al. (18)   2012
Tehran    62.5               Hashemi et al. (30)      2014
Tehran    58.3               Taherpour et al. (31)    2013
Tehran    94.7               Karimi et al. (32)       2012
Tehran    27                 Ghafourian et al. (19)   2011
Tehran   100                 Derakhshan et al. (33)   2014
Zabol     65                 Saeidi et al. (34)       2014
Zahedan  100                 Shahraki-Zahedani        2016
                             et al. (35)
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Author:Eskandari-Nasab, Ebrahim; Moghadampour, Mehdi; Tahmasebi, Arezoo
Publication:Iranian Journal of Medical Sciences
Article Type:Report
Geographic Code:7IRAN
Date:Jul 1, 2018
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