Literature DB >> 29854757

Drug Resistance Patterns of Escherichia coli in Ethiopia: A Meta-Analysis.

Kald Beshir Tuem1, Abadi Kahsu Gebre1, Tesfay Mehari Atey2, Helen Bitew3, Ebrahim M Yimer1, Derbew Fikadu Berhe1.   

Abstract

BACKGROUND: Antimicrobial drug resistance is a global threat for treatment of infectious diseases and costs life and money and threatens health delivery system's effectiveness. The resistance of E. coli to frequently utilized antimicrobial drugs is becoming a major challenge in Ethiopia. However, there is no inclusive countrywide study. Therefore, this study intended to assess the prevalence of E. coli resistance and antimicrobial-specific resistance pattern among E. coli clinical isolates in Ethiopia.
METHODS: Articles were retrieved from PubMed, Embase, and grey literature from 2007 to 2017. The main outcome measures were overall E. coli and drug-specific resistance patterns. A random-effects model was used to determine pooled prevalence with 95% confidence interval (CI), using DerSimonian and Laird method. In addition, subgroup analysis was conducted to improve the outcome. The study bias was assessed by Begg's funnel plot. This study was registered in PROSPERO as follows: PROSPERO 2017: CRD42017070106.
RESULTS: Of 164 articles retrieved, 35 articles were included. A total of 19,235 study samples participated in the studies and 2,635 E. coli strains were isolated. Overall, E. coli antibacterial resistance was 45.38% (95% confidence interval (CI): 33.50 to 57.27). The resistance pattern ranges from 62.55% in Addis Ababa to 27.51% in Tigray region. The highest resistance of E. coli reported was to ampicillin (83.81%) and amoxicillin (75.79%), whereas only 13.55% of E. coli isolates showed resistance to nitrofurantoin.
CONCLUSION: E. coli antimicrobial resistance remains high with disparities observed among regions. The bacterium was found to be highly resistant to aminopenicillins. The finding implies the need for effective prevention strategies for the E. coli drug resistance and calls for multifaceted approaches with full involvement of all stakeholders.

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Year:  2018        PMID: 29854757      PMCID: PMC5960519          DOI: 10.1155/2018/4536905

Source DB:  PubMed          Journal:  Biomed Res Int            Impact factor:   3.411


1. Background

Escherichia coli (E. coli) is one of the most widespread bacteria throughout the world. Some strains of E. coli can cause serious illness for humankind [1] including urinary tract infections [2-4], bloodstream infections [5], skin infection, otitis media [6, 7], and diarrhea [8]. E. coli resistance to antimicrobials is creating trouble to the healthcare system worldwide [9, 10]. This complicates treatment outcomes, increases the cost of treatment, and limits the therapeutic options that contribute to the global spectra of a postantimicrobial age in which some of the most effective drugs lose their efficiency [11]. The bacterium is becoming highly resistant to conventionally used antibiotics (to both the newer and older medicines) as evidenced by many previous studies [12-16]. Adaptive resistance was supposed to be the main mechanism for the development of resistance including that to lethal doses of the antimicrobials [17]. Antimicrobial resistance of E. coli in developing countries including Ethiopia is reported to be one major reason for failure of treatment of infectious diseases [18]. A number of studies conducted in Ethiopia from various clinical settings show increments in the prevalence of antimicrobial resistance patterns of E. coli [6, 19, 20]. However, there is no comprehensive and aggregated nationwide study to show the pattern of antimicrobial resistance in E. coli. Hence, the purpose of this meta-analysis was to sum up the available data and to establish the pooled prevalence and antimicrobial resistance of E. coli in Ethiopia.

2. Methods

This study was conducted in a similar approach to Eshetie et al. (2016) [21] and according to the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) Checklist [22] (additional S1 file).

2.1. Study Selection

A systematic literature search was conducted in PubMed and Embase, and also manual search for articles potentially relevant to our study was identified. We built our search strategy by combining the three main arms (Table 1): E. coli, drugs-related terms, and Ethiopia.
Table 1

Searching strategies including search arm and terms used in the study.

Search armSearch terms
1 E. coli Escherichia coli” OR “E. coli”
2Drug and/or resistance“antibiotic resistance” OR “drug resistance” OR “drug resistance, microbial” OR “drug resistance, microbial” OR “antibacterial resistance” OR “antibiotic resistance” OR “antimicrobial resistance”
3Ethiopia“Ethiopia”

The word “OR” was used to combine search terms within each arm and the word “AND” was used to connect the three search arms (#1 AND #2 AND #3).

Among the citations extracted, abstracts were reviewed to retrieve the clinical studies on E. coli colonization. Articles that were relevant, by title and abstract, were accessed in full text to determine those that provided sufficient information to be included in our meta-analysis. Finally, the references cited by each eligible study were screened to identify additional articles.

2.2. Inclusion and Exclusion Criteria

Studies included in this meta-analysis were those that had extractable data on the prevalence of drug resistance of E. coli on a human in Ethiopian hospitals or research centers and were only published from 2007 to 2017 and were only in English language.

2.3. Outcome of Interest

The main outcome of interest was the prevalence of drug resistance or antimicrobial susceptibility of E. coli among the total E. coli clinical isolates. The prevalence was calculated by dividing the numbers of resistant E. coli isolates by the total number of clinically isolated E. coli. As a secondary outcome of interest, we had also calculated the pooled resistance pattern of E. coli isolates to specific antibiotics.

2.4. Data Extraction and Assessment of Quality of Study

Screening by title, abstract, and full text and data extraction were done independently by two authors (Kald Beshir Tuem and Abadi Kahsu Gebre) at each step and Derbew Fikadu Berhe was involved in consensus for discrepancies (if any) between the two authors (Kald Beshir Tuem and Abadi Kahsu Gebre). In cases of insufficient data, the authors reviewed the full text of the article for further information and clarification. The extracted data from each article were summarized into a spreadsheet. References and data for each study were carefully cross-checked to ensure that no overlapping data were present and to maintain the integrity of the meta-analysis. Information extracted from each paper was region, study area, study design, study population, culture specimens, number of E. coli isolated, the average percentage of resistant E. coli, antimicrobial resistance rate of E. coli, and references. With all the articles used in this study being cross-sectional, the score for the quality of the study was assessed using the modified Newcastle-Ottawa scale for the representativeness of sample, appropriateness of sample size, response rate, validity of method, strategy to control confounding factors, reliability of outcome determination, and appropriate statistical analyses. The quality score (Table 2) disagreements were resolved by consensus and a final agreed-upon rating was assigned to each study (S2 file) [58].
Table 2

Summary of 35 studies reporting the prevalence and resistance pattern of E. coli in different parts of Ethiopia.

ReferencesRegionStudy areaStudy periodStudy designStudy populationCulture specimensStudy samplesNumber of E. coli isolatedAverage %resistant E. coliNOS quality score out of 7
Abejew et al., 2014 [23] AmharaDessieJanuary to March 2012RCSTest results of patients diagnosed with UTIUrine248641051.86
Kibret and Abera, 2014 [24]DessieRPatientsMid-stream morning urine140420353.26
Kibret and Abera, 2011 [25]DessieRPatientsUrine, ear discharge, pus swab from wounds, and eye discharge3,14944644.26
Azene and Beyene, 2011 [26]DessieRPatents with wound infectionsWound swab5998249.86
Alebachew et al., 2016 [27]GondarMarch 1 to May 2, 2013CSHIV patientsBlood1000144.47
Alemu et al., 2012 [28]GondarMarch 22 to April 30, 2011CSPregnant women attending ANCUrine3851929.27
Wondimeneh et al., 2014 [29]GondarJanuary to May 2013CSFistula patients“Clean-catch” mid-stream urine specimen53659.36
Wondimu et al., 2013 [30]GondarDecember 2011 to June 2012CSBlood donated from donors at blood bankblood13720.77
Eshetie et al., 2015 [31]GondarFebruary to May 2014CSUTI-suspected patientsUrine44211248.04
Tiruneh et al., 2014 [32]GondarSeptember 1, 2011, to June 30, 2012CSUTI-suspected patientsUrine28412068.04
Eshetie et al., 2016 [33]GondarFebruary to June 2014CSPatients with UTIUrine44611238.86
Mulu et al., 2017 [34]Debre MarkosJanuary 2015RPatientsPus/swab from wound, urine, ear discharge, blood, stool, urethral or cervical discharge, nasal or throat swab, and CSF5753931.56
Abera and Kibret, 2014 [35]West GojjamNovember 2009 to February 2010CSAdult patients who underwent trachomatous trichiasis surgeryConjunctival swabs14132026.55
Adugna et al., 2015 [36]Bahir DarDecember 2011 to February 2012CSChildren below five years of age with acute diarrheaStool sample42220442.87
Demilie et al., 2012 [37]Bahir DarOctober 2010 to January 2011CS Pregnant womenClean-catch urine3671641.74
Derbie et al., 2017 [38]Bahir DarJanuary 2015RPatientsUrine4467255.35
Melaku et al., 2012 [39]Bahir DarApril to August 2010CSPatientsUrine12543387.86
Mulu et al., 2012 [40]Bahir DarOctober 2010 to January 2011CSPatientsWound swab and venous blood samples294853.16
Wondemagegn et al., 2015 [41]Bahir DarMay to November 2013CSWomen of reproductive ageVaginal swab40910550.57

Dereje et al., 2017 [42]Central EthiopiaAddis AbabaFebruary to May 2015CSFistula patientsClean-catch mid-stream urine2106538.27
Dessie et al., 2016 [43]Addis AbabaOctober 2013 and March 2014CSSurgical site infected patientsWound swab1072468.46
Desta et al., 2016 [44]Addis AbabaDecember 2012CSAll age groups patientsFecal samples/swabs26723583.07
Mamuye, 2016 [45]Addis AbabaAugust 2013 to January 2014CSOutpatient and inpatient and pregnant womenMid-urine samples4245352.25
Legese et al., 2017 [46]Addis AbabaJanuary to March 2014CSSepticemia and UTI-suspected patientsBlood and urine322672.96

Ramos et al., 2014 [47] OromiaWest ArsiJuly to December 2013CSLeprosy patientsPus produced by ulcer681735.85
Derese et al., 2016 [48] Dire DawaFebruary 18, 2015, to March 25, 2015CSPregnant womenUrine specimens186934.46
Beyene and Tsegaye, 2011 [49]JimmaApril to June 2010CSUTI cases patientsUrine228727.15
Debalke et al., 2014 [50]JimmaSeptember to December 2012CSHIV/AIDS patientsUrine4813136.67
Mama et al., 2014 [51]JimmaMay to September 2013CSPatients with wound infectionWound swab1502961.66
Mulualem, 2012 [52]JimmaFebruary to March 2007CSInpatients and outpatientsUrine, sputum, stool, and wound3596745.76
Zenebe et al., 2011 [53]JimmaOctober 27, 2009, to March 26, 2010CSFebrile patientsVenous blood260425.06

Nigussie and Amsalu, 2017 [54] SNNPHawassaJune to October 2014CSDiabetic patientsMid-stream urine2401147.77
Amsalu et al., 2016 [55]HawassaJanuary 2012 to December 2014RCSPatients registered at microbiology lab bookPus, ear discharge, nasal swab, urine, genital swab, CSF, and stool5103564.07
Tadesse et al., 2014 [56]HawassaMarch to September 2012CSPregnant women attending ANCMid-stream urine2441656.36

Wasihun et al., 2015 [57]TigrayMekelleMarch to October 2014PCSFebrile patientsVenous blood5141627.56

Total 19,235 2,635

ANC: antenatal clinic, CSF: cerebrospinal fluid, CS: cross-sectional, PCS: prospective cross-sectional, R: retrospective review of culture, RCS: retrospective cross-sectional, SNNP: Southern Nations, Nationalities, and Peoples, UTI: urinary tract infection, —: no data.

2.5. Quality Control

The quality of eligible studies was checked independently by two authors (Kald Beshir Tuem and Abadi Kahsu Gebre) using a set of predetermined criteria such as research design quality of paper, completeness of extractable information, and employed methods for E. coli isolation. The study bias was measured by Begg's funnel plot [59]. This study was registered in PROSPERO as follows: PROSPERO 2017: CRD42017070106.

2.6. Data Analysis

A random-effects model was used to determine pooled prevalence, subgroup analysis, and 95% confidence interval (CI) by employing the approach of DerSimonian and Laird [60]. Variances and CIs were stabilized using Freeman-Tukey arc-sine methodology [61]; the reason is that using the standard approach of inverse variance method to calculate pooled prevalence does not work well in meta-analysis of single-arm study because, for studies with small or large prevalence, the inverse variance method causes the variance to become small and the calculated CI may be outside of the range [62]. Heterogeneity of study results was assessed using I2 test and significant heterogeneity was considered at p < 0.10 and I2 > 50% [60, 63]. Statistical analyses were performed using Open Meta-Analyst (version 3.13) and Comprehensive Meta-Analysis (version 3.1). In addition, we performed subgroup analyses according to the region of the country and the mechanism of action of the tested drugs to improve the specificity of the assessment.

3. Results

From Embase, PubMed, and manual searching, we found 164 potentially relevant studies, of which 35 were included for analysis (Figure 1).
Figure 1

Flowchart shows selected articles for meta-analysis.

The study design of all included articles (35) was cross-sectional study. In these studies, a total of 19,235 study samples participated, from which 2,635 E. coli strains were isolated. The published studies were from four regions in Ethiopia (Table 2) which include the federal capital city of Ethiopia, Addis Ababa. No report was obtained from other regions in the country (Afar, Benishangul-Gumuz, Gambella, and Somali). Most of the studies indicated that various specimens had been utilized for screening of E. coli; particularly multisite swabbing was performed from different parts of the body, including skin, nasal, eye, ear, urethra, throat, vagina, or genital area (Table 2), and other biological fluids like blood, urine, pus, stool, and cerebrospinal fluid (CSF) were taken for test. A total of 2,635 E. coli strains were isolated from these various sites. The lowest and highest proportions of E. coli resistance were reported, respectively, from Bahir Dar (55.20%) and Mekelle (27.50%) cities. The average prevalence of E. coli resistance was also noted in different regions of Ethiopia; Addis Ababa region was ranked first (62.55%, 95% CI: 38.28–6.83%), followed by Southern Nations, Nationalities, and Peoples of Ethiopia (58.14%, 95% CI: 48.69–67.58%), Amhara (47.83%, 95% CI: 39.77–55.89%), and Oromia (42.86%, 95% CI: 32.77–52.95%), whereas relatively low magnitude of E. coli resistance was reported from Tigray region (27.51%, 95% CI: 16.14–38.88%) (Figures 2 and 3).
Figure 2

Proportion of E. coli resistance in different regions of Ethiopia, 2007–2017. Values in parenthesis indicated 95% CI of E. coli resistance in different regions of Ethiopia.

Figure 3

Subgroup analysis of E. coli antibacterial resistance according to regions of Ethiopia.

Subgroup analyses (Figure 3) were carried out based on the region (Addis Ababa, Amhara, Oromia, SNNP, and Tigray) and the mechanism of action of the drugs (cell wall synthesis inhibitors, protein synthesis inhibitors, DNA synthesis inhibitors, and antimetabolites). A paper-based analysis in our study showed that the overall E. coli resistance in Ethiopia was 48.87% (95% CI: 42.17–55.57%) with highest prevalence in the capital city, Addis Ababa, 62.55% (95% CI: 38.28–86.83%) (Figure 3). As presented in Figure 4 and Table 3, the pooled prevalence of E. coli resistance was 45.38% (95% CI: 33.50–57.27%), and high resistance rates were observed to ampicillin, 83.81% (95% CI: 76.95–90.67%), amoxicillin, 75.79% (95% CI: 64.26–87.32%), tetracycline, 67.18% (95% CI: 58.89–75.47%), trimethoprim-sulfamethoxazole, 57.47% (95% CI: 58.89–75.47%), and cephalothin, 56.69% (95% CI: 33.74–79.64%). A relatively low level of nitrofurantoin resistance was observed, 13.55% (95% CI: 5.83–21.27%).
Figure 4

Forest plot of the pooled percentage and confidence interval of E. coli resistance to antibacterial drugs in Ethiopia from 2007 to 2017.

Table 3

Percentage of pooled antibacterial resistance rates of E. coli in Ethiopia, 2007–2017.

StudiesAntibacterial
AMLAMPAMCKFCROTEDOCECNKCIPNAFNORSXT
Abejew et al., 2014 [23]84.680.0---42.346.982.264.549.094.434.020.028.313.310.4---75.8
Abera and Kibret, 2014 [35]------------4025---35---40---4---------15
Adugna et al., 2015 [36]---86.847.5------76---36.2---37.2---6.9------9.3---
Alebachew et al., 2016 [27]---100100---0100---0---0---0---0---100
Alemu et al., 2012 [28]10010036.8---052.6---0---5.3---0------026.3
Beyene and Tsegaye, 2011 [49]100100------028.6---0---0---14.300---28.6
Debalke et al., 2014 [50]---88------4------0------------5201696
Demilie et al., 2012 [37]7581.737.5------68.8---37.5---31.218.818.843.86.32556.2
Derbie et al., 2017 [38]---89.178.6------66.1---------27.6---64.4---252764.5
Dereje et al., 2017 [42]------21.6---24.6------32.2---53.8---56.9---40------
Derese et al., 2016 [48]77.877.8------066.7---11.1---0---11.144.444.4---11.1
Dessie et al., 2016 [43]---95.870.8---83.383.3---25---54.2---66.7------------
Desta et al., 2016 [44]------9398---------------63---78------------
Eshetie et al., 2015 [31]---92.960.7---17.953.6---64.3---57.1---10.725------50
Kibret and Abera, 2014 [24]87.3------56.933.980.16137.493.724.5---34.1---3.8---72.1
Kibret and Abera, 2011 [25]86------59.537.472.4---35.389.413---19.9---3.66.562.9
Azene and Beyene, 2011 [26]85.0------64.766.771.433.336.151.914.4---7.7---------67.1
Mama et al., 2014 [51]---100---100627944.865.5---51.7---3441---44.855
Mamuye, 2016 [45]75.579.2---32.145.383.071.730.2---22.6---54.773.620.867.922.6
Melaku et al., 2012 [39]85.7100---------81.6---83.7------------------------
Mulu et al., 2017 [34]2533.3------3.3757513069.6---18.2------23.111.1
Mulualem et al., 2012 [52]868670.1---973.1---35.8---3---20.9------16.456.7
Mulu et al., 2012 [40]9078------55.666.766.70---44.444.444.466.722.244.467
Nigussie and Amsalu, 2017 [54]---10036.4---63.6------------72.7---18.2---09.181.8
Ramos et al., 2014 [47]64.770.65.9---5.941.229.435.341.211.8---29.4---------58.8
Wasihun et al.2015 [57]------6.7---60---40------13.3---6.7---26.7606.7
Wondimeneh et al., 2014 [29]5066.7------50100---16.7---66.7---50------66.766.7
Wondimu et al., 2013 [30]---33.30---000000---33.3---------0
Zenebe et al., 2011 [53]0100---0075---100---75---00------100
Amsalu1 et al., 2016 [54]---10026.1---45.7------64.3---60.6---56.2------68.890
Tadesse et al., 2014 [56]---68.8---------------------43.8------------18.881.2
Tiruneh et al., 2014 [32]87.583.3---------79.2---58.3---44.2---46.7---------76.7
Legese et al., 2017 [46]100---100------83.3---66.7---66.7---------066.7100
Eshetie et al., 2016 [33]---98.242------43.8---54.5---52.7---0.917------64.3
Wondemagegn et al., 2015 [41]8073.3---------73.3---------26.7---20------2060

AMC: amoxicillin-clavulanic acid, AML: amoxicillin, AMP: ampicillin, C: chloramphenicol, CIP: ciprofloxacin, CN: gentamicin, CRO: ceftriaxone, DO: doxycycline, E: erythromycin, F: nitrofurantoin, K: kanamycin, KF: cephalothin, NA: nalidixic acid, NOR: norfloxacin, SXT: trimethoprim/sulfamethoxazole, TE: tetracycline, ---: not done.

Comparing the prevalence of E. coli resistance among the antibacterial drugs, subgroup analysis (Figure 5) revealed that the cell wall synthesis inhibitors account for the greatest resistance percentage, 59.37% (95% CI: 36.21–82.53%), and DNA synthesis inhibitors account for the lowest resistance percentage, 26.14% (95% CI: 33.50–57.27%).
Figure 5

Subgroup analysis of pooled percentage and confidence interval of E. coli resistance to antibacterial drugs according to drug mechanism of action.

There was a high level of heterogeneity by random model methods (I2 = 97.89%; p < 0.01). Hence, the included studies have been conducted in different study settings, study periods, and study populations, which could have an effect on the heterogeneity of the included studies. The symmetry of funnel plot showed small study bias, which yielded insignificant effect.

4. Discussion

Antibiotic resistance continues to be a major global challenge in the management of bacterial infection. The trouble behind antibiotic resistance is highly marked in undeveloped or developing countries, including Ethiopia, where infectious diseases are highly prevalent [64]. Factors responsible for an increase in rates of antimicrobial resistance include misuse/overuse of antibiotics by healthcare professionals and general public and inadequate surveillance systems due to lack of reliable microbiological techniques leading to the inappropriate prescription of antibiotics [33]. Antimicrobial resistance in E. coli has increased worldwide and its susceptibility patterns show substantial variation in different geographical locations [5]. To date, the overall epidemiology and burden of multidrug resistance (MDR) bacteria have not been fully understood, especially in resource-limited countries including Ethiopia [64, 65]. To the best of our knowledge, this is the first meta-analysis study conducted to determine the pooled prevalence of E. coli prevalence and resistance in Ethiopia. Our result revealed that E. coli strains displayed diverse resistance patterns, with percentages varying slightly based on sample type and geographical distribution. Based on the tested antimicrobials, the overall E. coli resistance in Ethiopia was nearly 50% (45.38% (95% CI: 33.50–57.27%)). Developing countries have comparatively higher risk factors associated with MDR strains than the developed ones [64, 66]. Resistance to antibacterial agents is a normal evolutionary process for microorganisms, but it is highly aggravated by continuous deployment of antimicrobial drugs in treating infections [67, 68]. It is claimed that more than half of drugs are prescribed, sold, or dispensed without following standard protocols, and the situation is more pronounced in developing countries including Ethiopia [69]. Sosa et al. (2010) reported that antibiotic usage in most of the low-income countries is generally unregulated, which is a prime factor for the occurrence of resistant bacterial strains [64]. This implies that antibiotics are being used widely and inappropriately in resource-limited countries including Ethiopia. This may lead to an increase in the occurrence of drug-resistive bacterial strains such as E. coli. In our study, the regional prevalence of E. coli resistance was estimated, and the subgroup analysis showed that the highest prevalence of E. coli resistance (62.55%) was noted in Addis Ababa city, which was almost two times higher than Tigray region (27.51%). The observed variation might be due to differences in study location, hospital setup, and antimicrobial utilization. Subgroup analysis also showed that E. coli strains exhibited higher resistance with cell wall inhibitors, specifically aminopenicillins (ampicillin and amoxicillin), followed by protein synthesis inhibitors, mainly to tetracycline, and lesser resistance prevalence to nitrofurantoin. In line with our data, globally, E. coli strains were reported to be highly resistant to the above-mentioned antibiotics, mainly to aminopenicillins [70, 71]. Săndulescu (2016) reported that E. coli showed low resistance to nitrofurantoin, which is in line with the present finding. Moreover, our finding indicated the higher magnitude of E. coli resistance. This may imply the need for intervention in prescribing and using antibacterial against E. coli infections. Interventional strategies may include creating public awareness, maintaining hand hygiene, applying infection prevention protocols, and maintaining environmental sanitation, which are encouraged for preventing infection. In addition to these, promoting health education, maintaining continuous professional educations, and advocating rational prescribing habits are evidently effective in the minimization of the unwanted use of antibiotics, which in turn decrease selective pressure of resistant strains.

5. Conclusion

In this meta-analysis, the pooled E. coli resistance is considerably high. E. coli strains were highly resistant to ampicillin but showed lesser resistance to nitrofurantoin. Adopting safety protocols and implementing proper antibiotic prescription policies could be potential interventional strategies to address the emerging resistance of E. coli.
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Authors:  Mengistu Hailemariam; Tsegaye Alemayehu; Bereket Tadesse; Netsanete Nigussie; Asnakech Agegnehu; Techilo Habtemariam; Mulubrhan Ali; Enkosilassie Mitiku; Elshaday Azerefegne
Journal:  Sci Rep       Date:  2021-10-05       Impact factor: 4.379

8.  Prevalence and drug resistance patterns of Gram-negative enteric bacterial pathogens from diarrheic patients in Ethiopia: A systematic review and meta-analysis.

Authors:  Achenef Melaku Beyene; Mucheye Gezachew; Desalegn Mengesha; Ahmed Yousef; Baye Gelaw
Journal:  PLoS One       Date:  2022-03-16       Impact factor: 3.240

9.  Emergence of NDM-5-Producing Escherichia coli in a Teaching Hospital in Chongqing, China: IncF-Type Plasmids May Contribute to the Prevalence of bla NDM- 5.

Authors:  Hua Zou; Xiaojiong Jia; Hang Liu; Shuang Li; Xianan Wu; Shifeng Huang
Journal:  Front Microbiol       Date:  2020-03-06       Impact factor: 5.640

10.  Optical maps of plasmids as a proxy for clonal spread of MDR bacteria: a case study of an outbreak in a rural Ethiopian hospital.

Authors:  Yii-Lih Lin; Tsegaye Sewunet; Sriram Kk; Christian G Giske; Fredrik Westerlund
Journal:  J Antimicrob Chemother       Date:  2020-10-01       Impact factor: 5.790

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