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Prevalence of extended-spectrum-β-lactamase-producing Enterobacteriaceae: first systematic meta-analysis report from Pakistan

Antimicrobial Resistance & Infection Control volume 7, Article number: 26 (2018) Cite this article

Abstract

Background

South-Asia is known as a hub for multidrug-resistant (MDR) bacteria. Unfortunately, proper surveillance and documentation of MDR pathogens is lacking in Pakistan. The alarming increase in the prevalence of extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae is a serious problem. From this perspective, we analysed published data regarding ESBL-producing Enterobacteriaceae in different regions of Pakistan.

Methods

A meta-analysis was performed to determine the prevalence of ESBL-producing Enterobacteriaceae in Pakistan. A Web-based search was conducted in electronic databases, including PubMed, Scopus and PakMedi Net (for non-indexed Pakistani journals). Articles published (in either indexed or non-indexed journals) between January 2002 and July 2016 were included in the study. Relevant data were extracted, and statistical analysis was performed using the Metaprop command of STATA version 14.1.

Results

A total of 68 studies were identified from the electronic data base search, and 55 of these studies met our inclusion criteria. Pakistan’s overall pooled proportion of ESBL-producers was 0.40 (95% CI: 0.34–0.47). The overall heterogeneity was significant (I2 = 99.75%, p < 0.001), and significant ES = 0 (Z = 18.41, p < 0.001) was found. OXA, SHV, TEM and CTX-M were the most commonly found gene variants for ESBLs in these studies.

Conclusion

The prevalence of ESBL-producing Enterobacteriaceae is high in Pakistan. Little is known about the annual frequency of ESBLs and their prevalence in different provinces of Pakistan. No data are available regarding ESBL frequency in Baluchistan. This underscores an urgent demand for regular surveillance to address this antimicrobial resistance problem. Surveillance to better understand the annual ESBL burden is crucial to improve national and regional guidelines.

Background

Antimicrobial resistance has been declared a global threat to public health, as a massive increase in this problem has been observed in different parts of the world [1]. Although the magnitude of the antimicrobial resistance problem differs by country and geographical region, South-Asia is considered to be a major region for multidrug-resistant (MDR) bacteria [2]. The reported frequency of MDRs is increasing, putting strain on the public health organizations that are attempting to control this issue in many countries [3].

The alarming increase in the prevalence of extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae has serious consequences for treatment outcomes [4]. Escherichia coli and Klebsiella spp. are important pathogens isolated from community-acquired and nosocomial-acquired infections, and have been studied extensively [5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22]. The ESBL enzymes produced by these bacteria make them resistant to the first-choice antibiotic therapies that are commonly used. ESBL-positive strains are associated with a delay in the commencement of suitable antibiotic therapy, which consequently lengthens hospital stay and raises hospital costs [23]. Failure of antibiotic therapy is responsible for higher mortality rates in patients infected with these bacteria [24].

Epidemiological studies around the world have investigated the prevalence of ESBL-producing Enterobacteriaceae and they have seen multiple mechanisms of drug-resistance [25,26,27,28,29,30,31,32,33]. Several studies on ESBL infection in Asian-pacific region reported 60–80% of such cases were nosocomial-acquired while, remaining were community-acquired infections [1, 3, 34,35,36,37,38,39]. Over the last decade in Pakistan, an increase in resistance against quinolones has been observed in Enterobacteriaceae [40]. However, not much is known about fluoroquinolone-resistance in ESBLs and its relationship with plasmid-encoded genes.

MDRs are posing a treatment challenge, and are emerging as a major cause of morbidity and mortality worldwide. Unfortunately, proper surveillance and documentation of such pathogens is very limited, especially in developing countries. It has been estimated that more than 70% of antibiotic resistance occurs in the Asia-pacific region of the world, making antimicrobial resistance extremely problematic for Asian countries [1]. In Pakistan, ESBLs are especially problematic in terms of their contribution to the MDR bacteria problem. From this perspective, we analysed all of the available data regarding the prevalence of ESBL-producing isolates in different regions of Pakistan.

Antimicrobial resistance is on the rise. There are many factors associated with increasing antimicrobial resistance, one of which is ESBL production. The distribution of ESBLs differs in different communities, and every community must design their own protocol regarding the prevention and treatment of such infections [41]. Developed countries have annual surveillance systems to monitor the impact of antibiotic resistance as well as to determine the causative agents of antibiotic resistant infections. Such surveillance systems are often inadequate in developing countries. This meta-analysis will improve understanding of the distribution and epidemiology of ESBLs with different gene variants in Pakistan. This study also highlights the need to use molecular techniques to determine the different gene variants associated with ESBL-producing bacteria in Pakistan. To our knowledge, this is the first meta-analysis report from Pakistan, which would aid in updating the national treatment guidelines for ESBL infections. The purpose of this study was to determine the pooled prevalence of ESBL-producing Enterobacteriaceae with different gene variants in Pakistan.

Methods

Study design

This is a descriptive, meta-analysis study and is comprised of different studies reported from within Pakistan.

Literature search and strategy

A Web-based search using the key words: ESBLs, Pakistan, ESBL genes and Enterobacteriaceae, were performed using the electronic databases PubMed, Scopus, PakMedi Net and Web of Science in September 2016. Articles published in the English language were included in the study. A comprehensive search was carried out for publications on the subject of ESBLs from Pakistan. Furthermore, the references cited within the articles were also carefully screened to look for additional relevant publications.

Study selection procedures and criteria

Study selection was carried out by three authors in three steps independently (SH, SA and SR). As a first step, all of the titles and abstracts that were related to the study question were reviewed, and these were included in a group of eligible articles with irrelevant articles being excluded. All articles in the initially selected group were further screened in a second step by reviewing the full details of the articles. As a third step, selected articles were evaluated by other authors specifically for meta-analysis (RAK, NA, H H, SR), which was conducted using software STATA version 14.1 (College Station, Texas, USA) as previously described [42].

All studies were included based on the following criteria 1) studies that reported the prevalence of ESBLs in any province of Pakistan; 2) studies on bacterial strains isolated from human specimen; 3) all relevant national and international full text original research articles; 4) studies with confirmed ESBLs using phenotypic detection methods; 5) studies that used molecular techniques for ESBL gene variants.

Studies were excluded based on the following criteria 1) studies with incomplete information related to phenotypic ESBL detection methods; 2) duplicate articles, case reports, very small datasets (few strains < 15), abstracts/titles only, posters and review articles 3) studies on β-lactamases other than ESBL; 4) studies on animals and environmental strains of non-human origin. After reading the full texts, 13 further articles were removed for miscellaneous reasons [no phenotypic testing for ESBLs was performed (n = 3), case reports (n = 1), duplicates (n = 2), letter or posters (n = 2), studies about MBLs (n = 2), Studies specific on cancer patients and (mettalo-β-lactamases) MBLs (n = 1) and reviews (n = 2)] (Figs. 1 and 2).

Fig. 1
figure1

Flowchart of Systematic literature search and article selection

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Fig. 2
figure2

Proportion estimates of ESBL-producing Enterobacteriaceae in Pakistan. Midpoint of each horizontal line segment shows the proportion estimate of ESBL in each study. Rhombic mark shows the pooled proportion from all studies included

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Data extraction

The data were extracted by SH, SA and SR from the eligible studies and included. The data extracted from eligible studies consisted of; year of publication, year in which study was conducted, name of authors, location where the study was conducted (different provinces of Pakistan), sample size, strains detected ESBL, phenotypic detection techniques including; the double disc synergy test (DDST), the combination disc test (CDST), the epsilometric test (E-Test) and molecular detection techniques for gene variants (PCR) (Tables 1 and 2). Data were extracted and analysed twice to remove any discordance.

Table 1 Distribution of Articles reviewed regarding ESBL-producing clinical isolates in different regions of Pakistan
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Table 2 Proportion estimates of ESBLs in different regions of Pakistan
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Statistical analysis and reporting

Statistical analysis was performed using the Metaprop command in STATA version 14.1 (College Station, Texas, USA) to pool the published data regarding the predominance of ESBLs in different regions of Pakistan. Statistical heterogeneity was calculated using the I2 statistic (measure of inconsistency) at the significance level of 5%. Heterogeneity was used to study the variation in studies using the I2 statistic. The p-values (typically considered significant at 0.05) were used for converting meta-analysis results to defined/known tests of statistics. Random-effects model (REM) was used to estimate the pooled prevalence and 95% CI. A funnel plot and Begg tests were performed to evaluate the publication partiality using data graphically and statistically.

Results

Distribution of articles describing ESBLs in Pakistan

Electronic database searches yielded a total of 68 studies. A total of 55 articles reviewed from four provinces of Pakistan included 14 (25.4%) from Punjab, 23 (41.8%) from the Islamabad/Rawalpindi, 9 (16.4%) from the KPK, while the remaining 9 (16.4%) were from the Sindh. No studies were found from Baluchistan province (Fig. 3 and Table 3). The maximum number of articles on this subject was published in year 2013, followed by 2011, with the number of published articles in Pakistan decreasing afterwards (Fig. 4). In total, 42 (76.4%) of the articles reviewed included cases from in-patient and out-patient departments (OPD), 10 (15%) included patients attending in-patient departments, and 3 (6.3%) included patients attending OPD. A total of 21, 232 ESBL-bacterial isolates were included in the analysis. A total of 53 (96.4%) of the reviewed studies were conducted on both adults and children, while only 2 (3.6%) studies were based solely on the paediatric population. No studies were found on male and females separately (Table 2).

Fig. 3
figure3

Distribution of articles in three regions of Pakistan

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Table 3 Distribution of published articles in different regions of Pakistan
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Fig. 4
figure4

Annual publication of articles in different regions of Pakistan

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Laboratory methods used to estimate the proportion of ESBLs

For the variable phenotype methods, out of 55 studies, 48 (87.3%) had performed the double disc synergism test (DDST). However, only 13 (23.6%) had performed the combination disc test (CDST), and only 5 (9.09%) had performed the epsilometric test (E-Test). None of the studies had used the broth minimum inhibitory concentration (MIC) method. Out of 55 studies, 28 (50.9%) were published in local journals while the remaining 27 (49.1%) were in international journals (Table 2).

Molecular methods used to estimate the proportion of ESBLs

For molecular detection methods, 6 (11%) out of 55 articles reported PCR-based gene detection methods. Among these, 50% of articles reported CTX-M group as the most prevalent group, and CTXM-1 as the most commonly found gene variant. Additionally, CTX-M and TEM combinations were found in 33% of selected articles. One study reported the association of qnrB genes with the appearance of the ESBLs phenotype (Table 1).

Prevalence of ESBLs and their distribution in different geographical areas of Pakistan

Based on the available data (Table 1), Pakistan’s overall pooled proportion of ESBL-production was 0.40 (95% CI: 0.34–0.47). The overall heterogeneity was significant (I2 = 99.75%, p < 0.001), and significant ES = 0 (Z = 18.41, p < 0.001). The pooled proportion of ESBL-production for the Punjab, the Islamabad/Rawalpindi region, the KPK and the Sindh regions was 0.33 (95% CI: 0.21–0.46), 0.50 (95% CI: 0.39–0.62), 0.26 (95% CI: 0.15–0.39) and 0.43 (95% CI: 0.27–0.60) respectively. Significant heterogeneity (I2) for four regions with p < 0.001 is 99.77, 99.46, 99.59 and 99.81% respectively. Significant ES = 0 at p < 0.001 for the Punjab, the Islamabad/Rawalpindi, the KPK and the Sindh regions is Z = 8.32, 12.65, 7.43 and 7.87 respectively (Fig. 2 and Table 2).

Discussion

To address the issue of MDR bacteria, it is necessary to raise awareness about the magnitude of the problem by collecting data about antibiotic-resistance in various countries and regions [1, 29, 43]. The scarcity of studies available from Pakistan warrants attention for future research. Limited data regarding the overall predominance of ESBLs from Pakistan are available, but with no studies specifically from Baluchistan. This is the first meta-analysis about the extent of the ESBL problem in the Pakistani population. This is the first meta-analysis regarding the extent of the ESBL problem in the Pakistani population. However, this meta-analysis finds a high percentage of ESBL-producing Enterobacteriaceae across different geographical regions of Pakistan [5, 7, 12, 20, 44,45,46,47,48,49,50].

This meta-analysis is comprised of different studies reported from within Pakistan. The overall pooled proportion for ESBLs in this meta-analysis for Pakistan was 40% (Table 2). In China, a nationwide survey comprised of 30 different hospitals reported a 46% ESBL proportion, which is quite close to the data reported in our study [51]. A survey conducted in the hospitals of East Africa reported an overall pooled ESBL proportion of 42% (95% CI: 0.34–0.50) [52]. Previous research showed a considerably higher frequency of ESBL in Asian and African countries compared to developed countries [53]. For instance, the German population showed the estimated ESBL proportion in the range of 10 to 15% [54]. Similarly, a report was published from the US in 2012, which was based on the surveillance of ESBLs in nine census regions of the US, and they reported 4 to 12% resistance due to ESBLs [55]. However, among the Asian continent, an increase in ESBL mediated resistance was observed among the Japanese community, where the pooled ESBL proportion increased from 6.3% to 20% in 9 years [56].

These results indicate an extensive and statistically significant degree of disparity in ESBL proportion estimates (p < 0.05). The variation in ESBL occurrence reported in this systematic report may depend on several factors, including the socio-economic status of a society and the availability of antibiotics [57]. Moreover, differences in the sensitivity and specificity of the different methods applied in determining the proportions are also contributing factors. The majority of studies used purely phenotypic approaches, while some studies used molecular methods along with phenotypic testing [7, 9, 16, 17, 44, 47, 49, 58, 59]. Differences in ESBL proportions have been documented from all over the world established by hospital or community-based surveys [60,61,62]. In a study conducted in Ha’Emek Medical Center Israel> 50% ESBL prevalence was reported for community-acquired infections [63]. Whereas studies in Egypt, Cameroon, Bamako, Spain, China, Saudi Arabia, United Kingdom, United States, Latin America between 2004 to 2008 indicated a prevalence of ESBLs between 10 and 61% in different hospital and community settings [63,64,65,66,67,68].

Due to limited resources and a lack of infrastructure, only a few articles (11%) have investigated the molecular characterization and presence of ESBL encoding genes [4, 7, 16, 24, 29, 44, 45, 50, 51, 58]. OXA, SHV, TEM and CTX-M were the most commonly found gene variants in these studies for ESBLs [7, 16, 17, 50, 69]. The CTX-M group was found to be prevalent in 50% of studies reporting utilization of PCR-based molecular detection methods. The CTXM-15 gene variant of CTX-M group 1 has already been reported in many studies in the Asian continent [70,71,72,73]. In particular, CTXM and TEM is a common gene variant combination [7, 50]. One study reported the association of qnrB gene variants with the appearance of an ESBL phenotype, as this gene is involved in fluoroquinolone resistance [17]. However, few studies have reported the incidence of NDM genes, which are responsible for Carbapenem-resistance [52]. There are many reasons for variations in ESBL prevalence in the four studied regions of Pakistan. There may be substrate preferences, higher use of any specific class of antibiotics, co-resistances to other classes of antibiotics, poor health and diagnostic facilities [74, 75]. With this limited available information to hand, it is challenging to plan intensive and effective interventions for combating the problem of resistance.

Conclusion and recommendations

This meta-analysis indicated that there is a high ESBL burden in Pakistan. Few papers are available that address the annual frequency of ESBLs and their distribution in different provinces of Pakistan. No paper is available regarding the frequency of ESBLs in Baluchistan. Only 6 papers that reported gene detection were found. Detection of gene variants in β-lactamase-producing bacteria is essential information for the appropriate and effective treatment of patients. This underscores an urgent demand for regular surveillance to address this antimicrobial resistance issue. National and regional guidelines would be based upon such surveillance in order to understand the annual ESBLs burden. Effective measures such as the establishment of active surveillance and infection control programmes, emphasizing hand hygiene together with coherent antibiotic policies in hospitals and clinics should be implemented to stop and manage the spread of ESBLs in hospitals and communities.

Abbreviations

CDST:

Combination disc test

DDST:

Double disc synergy test

ESBL:

Extended-spectrum β-lactamases

ESBLs:

Extended-spectrum β-lactamase-producing strains

E-Test:

epsilometric test

KPK:

Khyber Pakhtunkhawa

MBLs:

Mettalo-β-lactamases

MDR:

Multidrug-resistant

MIC:

Minimum inhibitory concentration

OPD:

Out-patient department

References

  1. 1.

    Kang C-I, Song J-H. Antimicrobial resistance in Asia: current epidemiology and clinical implications. Infect Chemother. 2013;45:22–31.

    Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Bhatia R, Narain J-P. The growing challenge of antimicrobial resistance in the South-East Asia region-are we losing the battle? Indian J Med Res. 2010;132:482–6.

    PubMed  PubMed Central  Google Scholar 

  3. 3.

    Jean SS, Hsueh P-R. High burden of antimicrobial resistance in Asia. Int J Antimicrob Agents. 2011;37:291–5.

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Pitout JD. Infections with extended-spectrum β-lactamase-producing Enterobacteriaceae. Drugs. 2010;70:313–33.

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Ahmed K, Raja I, Hussain I, Jan M, Nafees M, Jahan Z, Javeed M, Shah G, Latif A. Prevalence of Escherichia coli in suspected urinary tract infected patients and their sensitivity pattern against various Escherichia coli in suspected urinary tract infected patients and their sensitivity pattern against various antibiotics in Gilgit-Baltistan, Pakistan. Pak J Zool. 2014;46:1783–8.

    Google Scholar 

  6. 6.

    Hafeez R, Aslam M, Mir F, Tahir M, Javaid I, Ajmal A. Frequency of extended spectrum β-lactamase producing gram negative bacilli among clinical isolates. Biomedica. 2009;25:112–5.

    Google Scholar 

  7. 7.

    Riaz S, Bashir MF. Phenotypic and molecular characterization of plasmid-encoded extended spectrum β-lactamases produced by Escherichia coli and Klebsiella Spp from Lahore, Pakistan. Trop J Pharmaceut Res. 2015;14:1597–604.

    CAS  Google Scholar 

  8. 8.

    Riaz S, Faisal M, Hasnain S. Antibiotic susceptibility pattern and multiple-antibiotic-resistances (MAR) calculation of extended spectrum β-lactamase (ESBL) producing Escherichia coli and Klebsiella species in Pakistan. Afri J Biotechnol. 2011;10:6325–31.

    Google Scholar 

  9. 9.

    Ejaz H, ul-Haq I, Saqib Mahmood S, Zafar A, Javed M-M. Detection of extended-spectrum β-lactamases in Klebsiella pneumoniae: comparison of phenotypic characterization methods. Pak J Med Sci. 2013;29:788–94.

    Article  Google Scholar 

  10. 10.

    Amin H, Zafar A, Ejaz H, Jameel N-A. Phenotypic characterization of ESBL-producing Enterobacter Cloacae among children. Pak J Med Sci. 2013;29:144–7.

    PubMed  PubMed Central  Google Scholar 

  11. 11.

    Ejaz H, ul-Haq K, Zafa A, Mahmood S, Javed M-M. Urinary tract infections caused by extended spectrum β-lactamase (ESBL) producing Escherichia coli and Klebsiella pneumoniae. Afric J Biotechnol. 2011;10:16661–6.

    Google Scholar 

  12. 12.

    Anwar M. Frequency of extended spectrum β-lactamase producing Klebsiella pnumoniae and Escherichia coli isolates. Biomedica. 2007;23:34–8.

    Google Scholar 

  13. 13.

    Qureshi M, Asif N, Baig S. Evaluation of extended spectrum β-lactamase mediated resistance in Escherichia coli and Klebsiella in urinary tract infection at a tertiary care hospital. Biomedica. 2013;29:78–83.

    Google Scholar 

  14. 14.

    Khan J, Naz N, AbdEl-Salam N-M, Nayab Nayab N, Tabassum A, Hussain H, Ullah R. ESBL determination and antibacterial drug resistance pattern of Klebsiella pneumoniae amongst patients at PIMS Islamabad. Afric J Tradit Complement Alternv Med. 2015;12:70–7.

    Article  Google Scholar 

  15. 15.

    Amin A, Ghumro P-B, Hussain S, Hameed A. Prevalence of antibiotic resistance among clinical isolates of Klebsiella pneumoniae isolated from a tertiary care hospital in Pakistan. Malays J Microbiol. 2009;5:81–6.

    Google Scholar 

  16. 16.

    Habeeb M-A, Sarwar Y, Ali A, Salman M, Haque A. High prevalence of 16S rRNA methylase Rmtb among CTX-M extended-spectrum β-lactamase-producing Klebsiella pneumoniae from Islamabad, Pakistan. Int J Antimicrob Agents. 2013;41:524–6.

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Ali I, Rafaque Z, Ahmed S, Malik S, Dasti J-I. Prevalence of multidrug-resistant uropathogenic Escherichia coli in Potohar region of Pakistan. Asian Pac J Trop Biomed. 2016;6:60–6.

    Article  Google Scholar 

  18. 18.

    Shafiq M, Rahman H, Qasim M, Ayub N, Hussain S, Khan J, Naeem M. Prevalence of plasmid-mediated Ampc β-Lactamases in Escherichia coli and Klebsiella pneumoniae at tertiary care hospital of Islamabad, Pakistan. Eur J Microbiol Immunol. 2013;3:267–71.

    Article  Google Scholar 

  19. 19.

    Ilyas M, Shabeer Ahmad MK, Mazhar K, Sajid A. Susceptibility pattern of extended spectrum β-lactamases positive Escherichia coli isolated from a tertiary care hospital of Peshawar, Pakistan. World Appl Sci J. 2014;30:253–7.

    Google Scholar 

  20. 20.

    Ullah F, Malik S-A, Ahmed J. Antimicrobial susceptibility pattern and ESBL prevalence in Klebsiella pneumoniae from urinary tract infections in the north-west of Pakistan. Afr J Microbiol Res. 2009;3:676–80.

    CAS  Google Scholar 

  21. 21.

    Bari F, Shah H, Wazir R. Frequency and detection of extended spectrum-β-lactamase in Escherichia coli and Klebsiella pneumoniae: a study at lady reading hospital Peshawar. J Postgrad Med Inst. 2015;29:256–9.

    Google Scholar 

  22. 22.

    Riaz S, Faisal M, Hasnain S. Prevalence and comparison of β-lactamase-producing Escherichia coli and Klebsiella Spp from clinical and environmental sources in Lahore, Pakistan. Afr J Microbiol Res. 2012;6:465–70.

    Google Scholar 

  23. 23.

    Ndir A, Diop A, Ka R, Faye PM, Dia-Badiane NM, Ndoye B, Astagneau P. Infections caused by extended-spectrum β-lactamases producing Enterobacteriaceae: clinical and economic impact in patients hospitalized in 2 teaching hospitals in Dakar, Senegal. Antimicrob Resis Infect Control. 2016;5:13–20.

    Article  Google Scholar 

  24. 24.

    Slama TG. Gram-negative antibiotic resistance: there as a price to pay. Crit Care. 2008;12:S4.

    Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Xiao Y-H, Giske CG, Wei Z-Q, Shen P, Heddini A, Li L-J. Epidemiology and characteristics of antimicrobial resistance in China. Drug Resist Updat. 2011;14:236–50.

    Article  PubMed  Google Scholar 

  26. 26.

    Falagas ME, Maraki S, Karageorgopoulos DE, Kastoris AC, Mavromanolakis E, Samonis G. Antimicrobial susceptibility of multidrug-resistant (MDR) and extensively drug-resistant (XDR) Enterobacteriaceae isolates to fosfomycin. Int J Antimicrob Agents. 2010;35:240–3.

    CAS  Article  PubMed  Google Scholar 

  27. 27.

    Savard P, Perl TM. A call for action: managing the emergence of multidrug-resistant Enterobacteriaceae in the acute care settings. Curr Opin Infect Dis. 2012;25:371–7.

    Article  PubMed  Google Scholar 

  28. 28.

    Hoban DJ, Bouchillon SK, Hawser SP, Badal RE. Trends in the frequency of multiple drug-resistant Enterobacteriaceae and their susceptibility to ertapenem, imipenem, and other antimicrobial agents: data from the study for monitoring antimicrobial resistance trends 2002 to 2007. Diagn Microbiol Infect Dis. 2010;66:78–86.

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Kelesidis T, Karageorgopoulos DE, Kelesidis I, Falagas ME. Tigecycline for the treatment of multidrug-resistant Enterobacteriaceae: a systematic review of the evidence from microbiological and clinical studies. J Antimicrob Chemother. 2008;62:895–904.

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Casella T, Rodríguez MM, Takahashi JT, Ghiglione B, Dropa M, Assunção E, Nogueira ML, Lincopan N, Gutkind G, Nogueira MCL. Detection of Bla CTX-M-type genes in complex class 1 integrons carried by Enterobacteriaceae isolated from retail chicken meat in Brazil. Int J Food Microbiol. 2015;197:88–91.

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Chen I-L, Lee C-H, Su L-H, Tang Y-F, Chang S-J, Liu J-W. Antibiotic consumption and healthcare-associated infections caused by multidrug-resistant gram-negative bacilli at a large medical center in Taiwan from 2002 to 2009: implicating the importance of antibiotic stewardship. PLoS One. 2013;8:E65621.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  32. 32.

    Falagas ME, Kastoris AC, Kapaskelis AM, Karageorgopoulos DE. Fosfomycin for the treatment of multidrug-resistant, including extended-spectrum β-lactamase producing, Enterobacteriaceae infections: a systematic review. Lancet Infect Dis. 2010;10:43–50.

    CAS  Article  PubMed  Google Scholar 

  33. 33.

    Coates AR, Halls G, Hu Y. Novel classes of antibiotics or more of the same? Br J Pharmacol. 2011;163:184–94.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Kucheria R, Dasgupta P, Sacks S, Khan M, Sheerin N. Urinary tract infections: new insights into a common problem. Postgrad Med J. 2005;81:83–6.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    David MZ, Daum RS. Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev. 2010;23:616–87.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Kurutepe S, Surucuoglu S, Sezgin C, Gazi H, Gulay M, Ozbakkaloglu B. Increasing antimicrobial resistance in Escherichia coli isolates from community-acquired urinary tract infections during 1998-2003 in Manisa, Turkey. Jpn J Infect Dis. 2005;58:159–62.

    CAS  PubMed  Google Scholar 

  37. 37.

    Song J-H, Jung S-I, Ko KS, Kim NY, Son JS, Chang H-H, Ki HK, Oh WS, Suh JY, Peck KR. High prevalence of antimicrobial resistance among clinical Streptococcus pneumoniae isolates in Asia (an ANSORP study). Antimicrob Agents Chemother. 2004;48:2101–7.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Hsueh P-R, Hoban DJ, Carmeli Y, Chen S-Y, Desikan S, Alejandria M, Ko W-C, Binh TQ. Consensus review of the epidemiology and appropriate antimicrobial therapy of complicated urinary tract infections in asia-pacific region. J Inf Secur. 2011;63:114–23.

    Google Scholar 

  39. 39.

    Sunenshine RH, Wright M-O, Maragakis LL, Harris AD, Song X, Hebden J, Cosgrove SE, Anderson A, Carnell J, Jernigan DB. Multidrug-resistant Acinetobacter infection mortality rate and length of hospitalization. Emerg Infect Dis. 2007;13:97–103.

    Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Yasmin F, Akhtar N, Hameed A. In-vitro synergistic effect of ciprofloxacin with aminoglycosides against multidrug resistant-Pseudomonas aeruginosa. Pak J Pharm Sci. 2013;26:1041–4.

    CAS  PubMed  Google Scholar 

  41. 41.

    Okeke IN, Lamikanra A. Export of antimicrobial drugs by west African travelers. J Travel Med. 2003;10:133–5.

    Article  PubMed  Google Scholar 

  42. 42.

    Nyaga VN, Arbyn M, Aerts M. Metaprop : a Stata command to perform meta-analysis of binomial data. Arch Public Health. 2014;72:1–10.

    Article  Google Scholar 

  43. 43.

    Kumar SG, Adithan C, Harish B, Sujatha S, Roy G, Malini A. Antimicrobial resistance in India: a review. J Nat Sc Biol Med. 2013;4:286–91.

    Article  Google Scholar 

  44. 44.

    Hannan A, Qamar MU, Usman M, Waheed KAI, Rauf K. Multidrug resistant microorganisms causing neonatal septicemia: in a tertiary care hospital Lahore, Pakistan. Afr J Microbiol Res. 2013;7:1896–902.

    CAS  Article  Google Scholar 

  45. 45.

    Hussain M, Hasan F, Shah AA, Hameed A, Jung M, Rayamajhi N, Cha S-B, Yoo HS. Prevalence of class a and Ampc β-Lactamases in clinical Escherichia coli isolates from Pakistan Institute of Medical Science, Islamabad, Pakistan. Jpn J Infect Dis. 2011;64:249–52.

    CAS  PubMed  Google Scholar 

  46. 46.

    Kausar A, Akram M, Shoaib M, Mehmood RT, Abbasi MN, Muhammad A, Aziz H, Asad MJ. Isolation and identification of UTI causing agents and frequency of ESBL (extended Spectrum β-Lactamase) in Pakistan. Amer JPhytomed Clin Ther. 2014;2:963–75.

    Google Scholar 

  47. 47.

    Ali A, Rafi S, Qureshi A. Frequency of extended spectrum β-lactamase producing gram negative bacilli among clinical isolates at clinical laboratories of Army medical college, Rawalpindi. PRO. 2004;2:25–9.

    Google Scholar 

  48. 48.

    Begum S, Hasan F, Hussain S, Shah AA. Prevalence of multidrug-resistant Acinetobacter Baumannii in the clinical samples from tertiary care hospital in Islamabad, Pakistan. Pak J Med Sci. 2013;29:1253–8.

    PubMed  PubMed Central  Google Scholar 

  49. 49.

    Ullah F, Malik SA, Ahmed J. Antibiotic susceptibility pattern and ESBL prevalence in nosocomial Escherichia coli from urinary tract infections in Pakistan. Afric J Biotechnol. 2009;8:3921–6.

    CAS  Google Scholar 

  50. 50.

    Rahman H, Naeem M, Khan I, Khan J, Haroon M, Bari F, Ullah R, Qasim M. Molecular prevalence and antibiotics resistance pattern of class a bla CTX-M-1 and bla TEM-1 β- Lactamases in uropathogenic Escherichia coli isolates from Pakistan. Turk J Med Sci. 2016;46:897–902.

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Zhang J, Zheng B, Zhao L, Wei Z, Ji J, Li L, Xiao Y. Nationwide high prevalence of CTX-M and an increase of CTX-M-55 in Escherichia coli isolated from patients with community-onset infections in Chinese county hospitals. BMC Infect Dis. 2014;14:659–63.

    Article  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Sonda T, Kumburu H, van Zwetselaar M, Alifrangis M, Lund O, Kibiki G, Aarestrup FM. Meta-analysis of proportion estimates of extended-spectrum-β-lactamase-producing Enterobacteriaceae in East Africa hospitals. Antimicrob Resis Infect Control. 2016;5:18–26.

    Article  Google Scholar 

  53. 53.

    Livermore DM. Current epidemiology and growing resistance of gram-negative pathogens. Korean J Intern Med. 2012;27:128–42.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Leistner R, Schröder C, Geffers C, Breier A-C, Gastmeier P, Behnke M. Regional distribution of nosocomial infections due to ESBL-positive Enterobacteriaceae in Germany: data from the German national reference center for the surveillance of nosocomial infections (KISS). Clin Microbiol Infect. 2015;21:255.

    Article  PubMed  Google Scholar 

  55. 55.

    Flamm RK, Sader HS, Farrell DJ, Jones RN. Ceftaroline potency among 9 US census regions: report from the 2010 AWARE program. Clin Infect Dis. 2012;55:S194–205.

    CAS  Article  PubMed  Google Scholar 

  56. 56.

    Castanheira M, Farrell SE, Krause KM, Jones RN, Sader HS. Contemporary diversityof β-Lactamases among Enterobacteriaceae in the nine United States census regions and ceftazidime-avibactam activity tested against isolates producing the most prevalent β-lactamase groups. Antimicrob Agents Chemother. 2014;58:833-838.

  57. 57.

    Spanu T, Luzzaro F, Perilli M, Amicosante G, Toniolo A, Fadda G, Group IES. Occurrence of extended-Spectrum β-Lactamases in members of the family Enterobacteriaceae in Italy: implications for resistance to β-lactams and other antimicrobial drugs. Antimicrob Agents Chemother. 2002;46:196–202.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Mahmood K, Izhar M, Choudhry N, Mujtaba G, Rashid N. Emergence of extended-spectrum-lactamase producing Salmonella Typhi in Pakistan. Afric J Microbiol Res. 2012;6:793–7.

    Google Scholar 

  59. 59.

    Ahmad M, Hassan M, Khalid A, Tariq I, Asad MHHB, Samad A, Mahmood Q, Murtaza G. Prevalence of extended spectrum β-lactamase and antimicrobial susceptibility pattern of clinical isolates of Pseudomonas from patients of Khyber Pakhtunkhwa, Pakistan. Biomed Res Int. 2016:2016–26.

  60. 60.

    Lonchel CM, Meex C, Gangoué-Piéboji J, Boreux R, Assoumou M-CO, Melin P, De Mol P. Proportion of extended-spectrum ß-lactamase-producing Enterobacteriaceae in community setting in Ngaoundere, Cameroon. BMC Infect Dis. 2012;12:53–9.

    Article  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Bourjilat F, Bouchrif B, Dersi N, Claude JDPG, Amarouch H, Timinouni M. Emergence of extended-spectrum beta-lactamases-producing Escherichia coli in community-acquired urinary infections in Casablanca, Morocco. J Infect Dev Ctries. 2011;5:850–5.

    CAS  PubMed  Google Scholar 

  62. 62.

    Muvunyi CM, Masaisa F, Bayingana C, Mutesa L, Musemakweri A, Muhirwa G. Decreased susceptibility to commonly used antimicrobial agents in bacterial pathogens isolated from urinary tract infections in Rwanda: need for new antimicrobial guidelines. Am J Trop Med Hyg. 2011;84:923–8.

    Article  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Colodner R, Rock W, Chazan B, Keller N, Guy N, Sakran W, Raz R. Risk factors for the development of extended-spectrum β-lactamase-producing bacteria in non-hospitalized patients. Euro J Clin Microbiol Infect Dis. 2004;23:163–7.

    CAS  Article  Google Scholar 

  64. 64.

    Tandé D, Jallot N, Bougoudogo F, Montagnon T, Gouriou S, Sizun J. Extended-spectrum β-lactamase–producing Enterobacteriaceae in a Malian orphanage. Emerg Infect Dis. 2009;15:472–4.

    Article  PubMed  PubMed Central  Google Scholar 

  65. 65.

    Valverde A, Coque TM, Sánchez-Moreno MP, Rollán A, Baquero F, Cantón R. Dramatic increase in prevalence of fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae during non-outbreak situations in Spain. J Clin Microbiol. 2004;42:4769–75.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Ho P, Poon WW, Loke S, Leung MS, Chow K, Wong RC, Yip K, Lai EL, Tsang KW. Community emergence of CTX-M type extended-spectrum β-lactamases among urinary Escherichia coli from women. J Antimicrob Chemother. 2007;60:140–4.

    CAS  Article  PubMed  Google Scholar 

  67. 67.

    Rodríguez-Bano J, Navarro MD, Romero L, Martínez-Martínez L, Muniain MA, Perea EJ, Pérez-Cano R. Epidemiology and clinical features of infections caused by extended-spectrum β-lactamase-producing Escherichia coli in non-hospitalized patients. J Clin Microbiol. 2004;42:1089–94.

    Article  PubMed  PubMed Central  Google Scholar 

  68. 68.

    Kader A, Kamath K. Faecal carriage of extended-spectrum beta-lactamase-producing bacteria in the community. East Mediterr Health J. 2009;15:1365–70.

    CAS  PubMed  Google Scholar 

  69. 69.

    Day KM, Ali S, Mirza IA, Sidjabat HE, Silvey A, Lanyon CV, Cummings SP, Abbasi SA, Raza MW, Paterson DL. Prevalence and molecular characterization of Enterobacteriaceae producing NDM-1 carbapenemase at a military hospital in Pakistan and evaluation of two chromogenic media. Diagnostic Microbiol Infect Dis. 2013;75:187–91.

    CAS  Article  Google Scholar 

  70. 70.

    Sheng W-H, Badal RE, Hseuh P-R. Distribution of extended-spectrum β-lactamases (ESBLs), Ampc β-lactamases, and carbapenemases among Enterobacteriaceae isolates causing intra-abdominal infections in Asia-Pacific: the study for monitoring antimicrobial resistance trends (SMART). Antimicrob Agents Chemother. 2013;57:2981-2988.

  71. 71.

    Lahlaoui H, Khalifa ABH, Moussa MB. Epidemiology of Enterobacteriaceae producing CTX-M type extended spectrum β-lactamase (ESBL). Mede Malad Infect. 2014;44:400–4.

    CAS  Article  Google Scholar 

  72. 72.

    Altinkum SM, Ergin S, Bahar H, Torun MM. CTX-M-15 type extended spectrum-lactamase producing Escherichia coli and Klebsiella pneumoniae: a developing problem in infected outpatients and hospitalised patients in Istanbul, Turkey. African J Microbiol Res. 2013;7:692–7.

    CAS  Google Scholar 

  73. 73.

    Chandramohan L, Revell PA. Prevalence and molecular characterization of extended-spectrum-β-lactamase-producing Enterobacteriaceae in a pediatric patient population. Antimicrob Agents Chemother. 2012;56:4765–70.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  74. 74.

    Winokur P, Canton R, Casellas J-M, Legakis N. Variations in the prevalence of strains expressing an extended-spectrum β-lactamase phenotype and characterization of isolates from Europe, the Americas, and the western Pacific region. Clin Infect Dis. 2001;32:94–103.

    Article  Google Scholar 

  75. 75.

    Winokur P, Canton R, Casellas J-M, Legakis N. Regional variation in the prevalence of extended-spectrum β-lactamase–producing clinical isolates in the Asia-Pacific region (SENTRY 1998–2002). Diag Microbiol Infect Dis. 2005;52:323–9.

    Article  Google Scholar 

  76. 76.

    Shah S. Susceptibility patterns of Escherichia coli: prevalence of multidrug-resistant isolates and extended spectrum β-lactamase phenotype. J Pak Med Assoc. 2002;52:132–8.

    Google Scholar 

  77. 77.

    Shah AA, Hasan F, Ahmed S, Hameed A. Prevalence of extended-spectrum β-lactamases in nosocomial and out-patients (ambulatory). Pak J Med Sci. 2003;19:187–91.

    Google Scholar 

  78. 78.

    Mumtaz S, Ahmad M, Aftab I, Akhtar N, Hassan M, Hamid A. Extended spectrum β-lactamases in enteric gram-negative bacilli: related to age and gender. J Ayub Med Coll Abbott. 2007;19:107–11.

    Google Scholar 

  79. 79.

    Khan E, Schneiders T, Zafar A, Aziz E, Parekh A, Hasan R. Emergence of CTX-M group 1-ESBL producing Klebsiella pneumonia from a tertiary care centre in Karachi, Pakistan. J Infect Dev Countr. 2010;4:472–6.

    CAS  Google Scholar 

  80. 80.

    Roshan M, Ikram A, Mirza IA, Malik N, Abbasi SA, Alizai SA. Susceptibility pattern of extended spectrum ß-lactamase producing isolates in various clinical specimens. J Coll Physicians Surg Pak. 2011;21:342–6.

    PubMed  Google Scholar 

  81. 81.

    Hassan A, Usman J, Kaleem F, Omair M, Khalid A, Iqbal M. Frequency and antibiotic susceptibility pattern of amp C β-lactamase producing bacteria isolated from a tertiary care hospital of Rawalpindi, Pakistan. Pak J Med Sci. 2011;27:578–81.

  82. 82.

    Habeeb MA, Haque A, Nematzadeh S, Iversen A, Giske CG. Rapid emergence of ESBL producers in E. coli causing urinary and wound infections in Pakistan. Pak J Med Sci. 2013;29:540–4.

    Article  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Khalid A, Usman J, Kaleem F, Hassan A, Omair M, Anjum R. The frequency and antimicrobial sensitivity pattern of extended spectrum-lactamase (ESBLs) producing gram negative bacilli isolated from urine in a tertiary care hospital of Pakistan. Afric J Microbiol Res. 2013;7:2040–3.

    Article  Google Scholar 

  84. 84.

    Sabir S, Anjum AA, Ijaz T, Ali MA, Rehman MU, Nawaz M. Isolation and antibiotic susceptibility of E. coli from urinary tract infections in a tertiary care hospital. Pak J Med Sci. 2014;30:389–92.

    Article  PubMed  PubMed Central  Google Scholar 

  85. 85.

    Saboor MAM, Waheed U, Anwarullah, Umar M. Prevalence of ESBL producing Enterobacteriaceae in a private hospital in Islamabad. Int J Rehab Sci. 2014;3:18–22.

    Google Scholar 

  86. 86.

    Sohail M, Khurshid M, Saleem HGM, Javed H, Khan AA. Characteristics and antibiotic resistance of urinary tract pathogens isolated from Punjab, Pakistan. Jundishapur J Microbiol. 2015;8:e19272.

    Article  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Ahmed I, Sajed M, Sultan A, Murtaza I, Yousaf S, Maqsood B, Vanhara P, Anees M. The erratic antibiotic susceptibility patterns of bacterial pathogens causing urinary tract infections. EXCLI J. 2015;14:916.

    PubMed  PubMed Central  Google Scholar 

  88. 88.

    Jamil B, Bokhari MTM, Saeed A, Bokhari MZM, Hussain Z, Khalid T, Bukhari H, Imran M, Abbasi SA. Bacteremia: prevalence and antimicrobial resistance profiling in chronic kidney diseases and renal transplant patients. J Pak Med Assoc. 2016;66:705.

    PubMed  Google Scholar 

  89. 89.

    Anwar M, Ejaz H, Zafar A, Hamid H. Phenotypic detection of metallo-β-lactamases in carbapenem resistant Acinetobacter baumannii isolated from pediatric patients in Pakistan. J Pathog. 2016;2016:1–6.

    Article  Google Scholar 

  90. 90.

    Mumtaz S, Ahmed J, Ali L, Hussain H. Prevalence of extended spectrum β-lactamases (ESBL) in clinical isolates from a teaching hospital in Peshawar, Pakistan. Afric J Microbiol Res. 2011;5:2880–4.

    Article  Google Scholar 

  91. 91.

    Iqbal R, Majid A, Alvi IA, Hayat A, Andaleeb F, Gul S, Irfan S, Rahman MU. Multiple drug resistance and ESBL production in bacterial urine culture isolates. Amer J Biosci. 2014;2:5–12.

    CAS  Article  Google Scholar 

  92. 92.

    Jabeen K, Zafar A, Hasan R. Comparison of double disc and combined disc method for the detection of extended spectrum ß-lactamases in Enterobacteriaceae. J Pak Med Asso. 2003;53:534–7.

    CAS  Google Scholar 

  93. 93.

    Jabeen K, Znfar A, Hasan R. Frequency and sensitivity pattern of extended spectrum β-lactamase producing isolates in a tertiary care hospital laboratory of Pakistan. J Pak Med Assoc. 2005;55:436.

    PubMed  Google Scholar 

  94. 94.

    Ahmed E, Durrani M, Qamar S, Kharal S. Detection of extended spectrum β-lactamase (ESBL) producing organisms in Enterobacteriaceae Family like Escherichia coli (E. coli) and Klebsiella pneumoniae by double disc diffusion method (DDDM). Pak J Pharmacol. 2009;26:25–30.

    Google Scholar 

  95. 95.

    Jabeen K, Zafar A, Irfan S, Khan E, Mehraj V, Hasan R. Increase in isolation of extended spectrum beta lactamase producing multidrug resistant non typhoidal Salmonellae in Pakistan. BMC Infect Dis. 2010;10:101–6.

    Article  PubMed  PubMed Central  Google Scholar 

  96. 96.

    Khan E, Ejaz M, Zafar A, Jabeen K, Shakoor S, Inayat R, Hasan R. Increased isolation of ESBL producing Klebsiella pneumoniae with emergence of carbapenem resistant isolates in Pakistan: report from a tertiary care hospital. J Pak Med Assoc. 2010;60:186–9.

    PubMed  Google Scholar 

  97. 97.

    Afridi, F.I., B.J. Farooqi, And A. Hussain, Frequency of extended spectrum beta lactamase producing Enterobacteriaceae among urinary pathogen isolates. J Coll Physicians Surg Pak. 2011;21:741-744.

    PubMed  Google Scholar 

  98. 98.

    Hassan SA, Jamal SA, Kamal M. Occurrence of multidrug resistant and ESBL producing E. coli causing urinary tract infections. J Basic Appl Sci. 2011;7:39–43.

    CAS  Google Scholar 

  99. 99.

    Afridi FI, Farooqi BJ. Activity of β-lactam β-lactamase inhibitor combinations against extended spectrum β-lactamase producing Enterobacteriaceae in urinary isolates. J Coll Physicians Surg Pak. 2012;22:358–62.

    PubMed  Google Scholar 

  100. 100.

    Ullah F, Malik SA, Ahmed J. Antimicrobial susceptibility and ESBL prevalence in Pseudomonas aeruginosa isolated from burn patients in the north-west of Pakistan. Burns. 2009;35:1020–5.

    Article  PubMed  Google Scholar 

  101. 101.

    Mirza SH, Salman M, Khurshid U, Wiqar MA. CTX-M ESBL enzyme in Escherichia coli from urology patients in Rawalpindi, Pakistan. J Pak Med Assoc. 2006;56:576–80.

    PubMed  Google Scholar 

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Acknowledgments

We would like to acknowledge the staff of Citilab and Research center Lahore and Department of Statistical and Actual Sciences, University of the Punjab, Lahore, for providing unconditional support for completion of this work.

Funding

No funding was received for this study.

Availability of data and materials

The data sets analyzed during the current study are available from the corresponding author.

Declaration

This study is part of Ph. D thesis of Samyyia Abrar.

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Affiliations

  1. Department of Microbiology and Molecular Genetics, University of the Punjab, Lahore, Pakistan

    Samyyia Abrar, Shahida Hussain, Noor Ul Ain, Hayat Haider & Saba Riaz

  2. Citilab and Research center, Lahore, Pakistan

    Saba Riaz

  3. College of Statistical and Actuarial Sciences, University of the Punjab, Lahore, Pakistan

    Rehan Ahmad Khan

Authors
  1. Samyyia Abrar
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  2. Shahida Hussain
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  3. Rehan Ahmad Khan
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  4. Noor Ul Ain
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  5. Hayat Haider
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  6. Saba Riaz
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Contributions

SR is the supervisor and conceived the idea; SH gathered data, analysed data and contributed to draft preparation; SA rechecked the data, contributed to data analysis and contributed to draft preparation; NA and MH analysed data and contributed to draft preparation; RA worked on statistical analysis; all authors read, revised and approved the final version of the manuscript.

Corresponding author

Correspondence to Saba Riaz.

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Ethics approval and consent to participate

The study was approved by local ethics committee (CitiLab and Research Centre Ref # 27th − 17 CLRC/ 27th).

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The authors declare that they have no competing interests.

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Abrar, S., Hussain, S., Khan, R.A. et al. Prevalence of extended-spectrum-β-lactamase-producing Enterobacteriaceae: first systematic meta-analysis report from Pakistan. Antimicrob Resist Infect Control 7, 26 (2018). https://0-doi-org.brum.beds.ac.uk/10.1186/s13756-018-0309-1

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Keywords

  • MDR
  • ESBLs
  • Enterobacteriaceae
  • Meta-analysis
  • Pakistan

Antimicrobial Resistance & Infection Control

ISSN: 2047-2994

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