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
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.
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.
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 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
* 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.
* 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, Ghaem Ilam Emam Khomaini, 17 5 Mostafa Khomaini, Ghaem Kashan Hospitals in Kashan 35 28 Kerman Afzali Poor, Kashani, 33 16 Bahonar 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, Milad Zabol Amir Al-Momenin 20 13 Zahedan Ali ibn Abi Talib, 51 51 Khatamal Anbiya, Buali 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|
|Date:||Jul 1, 2018|
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