- Open Access
Review and analysis of the overlapping threats of carbapenem and polymyxin resistant E. coli and Klebsiella in Africa
Antimicrobial Resistance & Infection Control volume 12, Article number: 29 (2023)
Carbapenem-resistant Enterobacterales are among the most serious antimicrobial resistance (AMR) threats. Emerging resistance to polymyxins raises the specter of untreatable infections. These resistant organisms have spread globally but, as indicated in WHO reports, the surveillance needed to identify and track them is insufficient, particularly in less resourced countries. This study employs comprehensive search strategies with data extraction, meta-analysis and mapping to help address gaps in the understanding of the risks of carbapenem and polymyxin resistance in the nations of Africa.
Three comprehensive Boolean searches were constructed and utilized to query scientific and medical databases as well as grey literature sources through the end of 2019. Search results were screened to exclude irrelevant results and remaining studies were examined for relevant information regarding carbapenem and/or polymyxin(s) susceptibility and/or resistance amongst E. coli and Klebsiella isolates from humans. Such data and study characteristics were extracted and coded, and the resulting data was analyzed and geographically mapped.
Our analysis yielded 1341 reports documenting carbapenem resistance in 40 of 54 nations. Resistance among E. coli was estimated as high (> 5%) in 3, moderate (1–5%) in 8 and low (< 1%) in 14 nations with at least 100 representative isolates from 2010 to 2019, while present in 9 others with insufficient isolates to support estimates. Carbapenem resistance was generally higher among Klebsiella: high in 10 nations, moderate in 6, low in 6, and present in 11 with insufficient isolates for estimates. While much less information was available concerning polymyxins, we found 341 reports from 33 of 54 nations, documenting resistance in 23. Resistance among E. coli was high in 2 nations, moderate in 1 and low in 6, while present in 10 with insufficient isolates for estimates. Among Klebsiella, resistance was low in 8 nations and present in 8 with insufficient isolates for estimates. The most widespread associated genotypes were, for carbapenems, blaOXA-48, blaNDM-1 and blaOXA-181 and, for polymyxins, mcr-1, mgrB, and phoPQ/pmrAB. Overlapping carbapenem and polymyxin resistance was documented in 23 nations.
While numerous data gaps remain, these data show that significant carbapenem resistance is widespread in Africa and polymyxin resistance is also widely distributed, indicating the need to support robust AMR surveillance, antimicrobial stewardship and infection control in a manner that also addresses broader animal and environmental health dimensions.
Antimicrobial resistance (AMR) is of growing concern as multidrug resistant organisms (MDRO) become more prevalent globally, undermining the efficacy of medicines needed for the treatment of infections and threatening patient safety and economic wellbeing . Carbapenem-resistant Enterobacterales (CRE) infections are of particular concern as treatment options are highly limited  with carbapenems considered critical drugs for treatment of infections with documented or suspected resistance to alternative antimicrobials. Healthcare environments are the dominant source of human exposure to MDRO such as CRE  but exposure may also occur in the community, where organisms spread not only after transfer from patients exposed in healthcare settings, but also through contact with food, animals, and the environment [4,5,6,7,8].
Resistance to carbapenems arises through intrinsic or acquired mechanisms . Acquired resistance [9,10,11,12,13,14] typically occurs due to carbapenemase enzymes encoded on plasmids or other genetic elements that are readily transferred among organisms [2, 15]. Major resistance determinants present worldwide include expression of Class A Klebsiella pneumoniae carbapenemases (KPC), Class B metallo-β-lactamases such as New Delhi metallo-β-lactamases (NDM), Verona integron-encoded metallo-β-lactamases (VIM), Imipenemase metallo-β-lactamases (IMP), and Class D oxacillinase β-lactamases (OXA), and alterations in outer membrane proteins (OMP) . The polymyxin antibiotics, including polymyxin E (colistin) and polymyxin B, hereon in referred to as polymyxin(s), are polycationic peptides widely used until the 1970s, when largely abandoned as less toxic antibiotics became available [16, 17]. Currently, as one of few antimicrobial classes effective against CRE, polymyxins have regained importance. Determinants of acquired polymyxin resistance include transferable plasmid encoded mobile colistin resistance (mcr) genes as well as chromosomally encoded genes such as mgrB, phoP/phoQ, and pmrA/pmrB [16, 18]. The risk of organisms acquiring both carbapenem and polymyxin resistance is alarming as it severely limits treatment options. While rare to date, such dual resistance has been increasingly documented [19,20,21,22].
Despite the association of MDRO with excess morbidity, mortality and costs, major gaps exist in surveillance, particularly in under-resourced areas . The WHO Global Action Plan to Tackle AMR (GAP-AMR) provides a roadmap for the treatment and prevention of resistant infections . Since 2014, WHO has encouraged collection of data on carbapenem susceptibility and has published the limited available data in reports of the Global Antimicrobial Resistance Use and Surveillance System (GLASS) [1, 25,26,27]. In 2018, noting that only 7 of 47 WHO Africa nations had reported data on CRE to WHO [12, 28,29,30], we developed search and metanalytic approaches to utilize data from diverse sources to estimate and map carbapenem resistance and related genotypes in the WHO Africa region. We were able to identify and analyze data from 31 of 47 nations  documenting carbapenem-resistant Escherichia coli or Klebsiella spp. in 22, typically at low to moderate levels . We subsequently refined these approaches to characterize carbapenem and polymyxin resistance and their concerning overlaps in Southeast Asia .
Since our initial study, reporting on carbapenem resistance in Africa has increased [32,33,34] but comprehensive analyses are not available. Information on polymyxin resistance is more limited but recent reviews document mcr plasmids as causes of resistance in several African nations [35, 36]. The 2020 WHO GLASS report included only 10 of 54 nations reporting data on carbapenems and just 4 on polymyxins. Given these persistent data gaps there is a major unmet need for information to inform medical and public health investments, strategies and practices. We applied our previously-developed approaches to locate available useful data on polymyxin/colistin resistance and related genes, as well as to broadly update analyses of carbapenem resistance to reflect emerging data and extend the scope of study to all continental Africa. The results provide a comprehensive database and maps of carbapenem and polymyxin resistance in Africa, documenting the significant ongoing spread of both throughout the continent.
Literature review and other data sources
Three comprehensive Boolean searches were constructed and utilized to query scientific and medical databases (Embase, Global Health, PubMed and Web of Science). Grey literature sources including ProMED-mail , ResistanceMap  and HealthMap  were also examined for data from African nations, as described [2, 31]. Data were further supplemented by review and, where meeting criteria, extraction of relevant primary data located based on citations identified through included studies or from other referenced reviews and meta-analyses, as well as directly utilizing data from World Health Organization GLASS reports [1, 25,26,27] and author correspondence. As detailed previously, for nations with fewer than 4 reports from these sources, manual Google Scholar searches were conducted and additional sources such as African Journals Online, Bioline International and Global Index Medicus were hand-searched for relevant documents .
As described [2, 31], search strategies were designed and executed to capture data describing susceptibility or resistance, and/or related genotypic findings, of Escherichia coli and Klebsiella isolates from humans. The searches (search operators capitalized) generally followed the structure of place (e.g. terms for Africa OR country names) AND terms for AMR (including general OR specific AMR terms OR synonym drug terms) AND species/mechanisms (including resistance enzymes and plasmid-mediated genotypes). As detailed (Additional file 1) the search strings also contained MeSH terms to optimize sensitivity while enhancing specificity. The first database search updated data from the WHO Africa Region nations (United Nations geoscheme) through 31 December 2019 . The second search identified data published from 1 January 1996 to 31 December 2019 on carbapenem susceptibility or resistance for seven African countries not included in our original report (Djibouti, Egypt, Libya, Morocco, Tunisia, Somalia, and Sudan) . The final search for 1 January 1996 to 31 December 2019 identified data for polymyxin susceptibility or resistance for all African nations.
Exclusion and inclusion criteria and data collection
Two authors (DMV and AYB) screened search result titles and excluded irrelevant materials. Remaining studies were examined for relevant information regarding carbapenem and/or polymyxin(s) susceptibility and/or resistance amongst E. coli and Klebsiella isolates from humans. Minimum criteria for inclusion in the study database were description of study design and sampling process, characteristics of participants, places and dates of data collection and use of recognized, standardized testing methods at the time of performance. Studies not including these data elements were excluded. Data were extracted and coded from studies meeting criteria and any coding questions resolved through mutual agreement amongst researchers.
Underlying data from 313 reports in our previous dataset  on carbapenem resistance in WHO Africa nations (from searches through 31 June 2017) were also incorporated into the current dataset. If a newly found study reported data duplicative of or overlapping with that included in earlier analyses, only the original report was included. We also examined the results of database searches for similar reports (e.g. in terms of country, dates and species) to detect potentially duplicative or overlapping reporting of the same data. In circumstances where searches yielded duplicative or overlapping data, the most complete study was utilized unless both included unique data, in which case any additional details from the second report were included on a separate line of the database without duplicate reporting. When a study provided potentially important findings, but substantive uncertainties were present, authors were contacted, when possible, for clarification. Outreach to authors was made for 167 studies and responses obtained for 85, of which 55 were included in the manuscript (see acknowledgements).
Database construction, definitions and data entry
A structured Microsoft Excel Version 1808 (Microsoft Corp., Redmond, WA, USA) template with predefined attributes was developed and utilized, as described [2, 31]. Data extracted included study characteristics, patient populations, and phenotypic and genotypic carbapenem and polymyxin resistance. Study type was classified as clinical laboratory-based, case series, outbreak, or surveillance, and populations were classified as from acute or chronic healthcare facilities, community-based, travelers or unknown . Selected subpopulations, if studied, were defined by clinical attributes (e.g. pregnant, intensive care unit, clinical syndrome), travel status (e.g. immigrants, refugees) and/or occupation (e.g. farmers, students, healthcare workers). WHO age classification was utilized where applicable, unless age was otherwise classified by authors [31, 40].
Reports on subsets of laboratory isolates selected based on their resistance properties were coded noting the selection criteria utilized (e.g. ESBL or CRE). If results of susceptibility testing to multiple carbapenems were reported, all data were entered in the database with the value for the drug with the highest percentage resistance then used to represent overall carbapenem resistance, so long as the numbers of isolates tested for each drug were similar. On occasions where the differences in total numbers of isolates tested against different carbapenems were large (e.g. an order of magnitude), we used results from the drug with the most isolates tested to represent resistance. Isolates reported as having intermediate susceptibility were classified as resistant. For studies presenting disaggregated susceptibility results (e.g. by ESBL status), data were reaggregated to reflect resistance in the entire original set of isolates. Documentation of specific carbapenem or polymyxin resistance-associated genotypes was recorded whenever available. For quality control, all database entries were checked and confirmed by an additional reviewer.
Defining the presence of resistance and/or specific resistance genotypes
Any report of at least one carbapenem and/or polymyxin-resistant E. coli or Klebsiella isolate, or an isolate with a resistance-associated genotype, signified the presence of resistance in that nation. This included findings of phenotypic resistance or resistance inducing genotypes in any isolate, whether from population-based studies or narrower studies of outbreaks, case series, highly selected subpopulations, or from studies of isolates themselves selected for known resistance to any antibiotic(s) including carbapenem and polymyxin.
Crude national resistance proportion estimates
Analysis was conducted using R version 3.5.2 (R Core Team, 2014). To estimate crude national resistance proportions, data from studies with a minimum number of isolates tested (20 for carbapenems and 10 for polymyxin, given the paucity of available data) that were deemed to originate from reasonably ‘generalizable’ populations (i.e. representative of individuals in overall healthcare populations), were aggregated and analyzed across studies. These estimates excluded any data from outbreaks or from studies reporting resistance in certain highly selected subpopulations (burn injury, oncology or transplantation) that typically have levels of resistance significantly greater than general acute-care populations. Similarly, data reporting resistance among organisms selected based on their known resistance to any antibiotic were not considered generalizable and therefore not included in resistance estimates.
To better reflect recent resistance, crude resistance proportions were calculated using data available on isolates collected from 2010 onward. If the total of generalizable E. coli or Klebsiella isolates tested for susceptibility to carbapenems or polymyxin(s) from 2010 onward was at least 100, we calculated that nation’s mean and, across qualifying studies, median resistance proportions using R v.3.5.2. For nations with at least 100 generalizable isolates of E. coli or Klebsiella, a crude estimated median resistance category was assigned consistent with prior studies [2, 31] as follows: not detected, low (< 1%), moderate (1–5%) or high (> 5%). If the total of generalizable isolates for a nation was less than 100, a category of either ‘Insufficient isolates – Resistance detected’ or ‘Insufficient isolates – Resistance not detected’ was assigned.
Geocoding and mapping
ArcGIS Desktop 10.6 (ESRI, Redlands, CA, USA) was used to map median resistance proportions and genotypes at the national level. Sample origin was geocoded at facility level, or to the closest local administrative unit such as City or State/Province using Google Maps.
The supplementary material, including search strings (Additional file 1) and outputs (Additional file 2), explanation of data elements extracted for analyses (Additional file 3), and all study data (Additional file 4) are available through Mendeley.
The searches yielded 8631 studies of which 1191 passed initial screening and 749 then met inclusion criteria. Three were in French, all others were in English. Because a given study may contain data on more than one organism, sets of isolates, or populations, the 749 study documents yielded a total of 1479 unique data reports together providing data on carbapenem and/or polymyxin resistance from 48 of 54 African countries. Three nations (Egypt, Nigeria and South Africa) accounted for 647 (43.7%) of all reports in the database. In contrast, no relevant reports were identified from 6 nations and nearly 30 nations each accounted for less than 1% of reports.
Selected general attributes of the data reports are displayed in Table 1. Six hundred and ninety-two (46.8%) reported on E. coli, while 787 (53.2%) were on Klebsiella spp. More than half of the data reports (67.5%) were from clinical laboratory-based studies, while 22.6% were from case series, 8.2% from surveillance and 2% from outbreaks. Aside from 34.6% of reports of multiple sample sources, most reports were of isolates from urine (23.3%) or blood (20.6%). Subject ages were reported as all (30%), adults (20.2%) and children (13.1%) or as unknown (34.2%). The majority (83.4%) of reports included isolates collected in acute healthcare settings, others included community-based settings (29.0%), chronic health-care facilities (0.5%), unknown healthcare settings (4.2%), travelers (1.0%) and unknown sources (1.7%).
Carbapenem resistance: overview of data from all years
There were a total of 1341 data reports, derived from 708 studies, providing data on carbapenem susceptibility from 48 of 54 nations (Table 2). These included 622 (46.4%) on E. coli isolates and 719 (53.6%) on Klebsiella from 48 and 42 nations, respectively. Of the total 1341 reports, 879 (65.5%) were from nations in WHO Africa (including 313 incorporated from the earlier analysis ) while 462 (34.5%) were from the other African nations. Phenotypic and or genotypic carbapenem resistance was reported among either species in 40 of 48 nations (83.3%) from which data were available. Specifically, resistance was detected among E. coli in 36 of 48 nations (75%) with available data and among Klebsiella in 35 of 42 (83.3%). There were no data available on E. coli or Klebsiella from 6 nations (Burundi, Comoros, Lesotho, Liberia, Seychelles and Swaziland) while data were available on E. coli but not Klebsiella from an additional 6 (Cape Verde, Djibouti, Eritrea, Guinea, Lesotho, Somalia and South Sudan). Tables 3 and 4 present national-level carbapenem resistance data for all years studied, including whether resistance was reported, specific genotypes detected and, for samples from generalizable studies, percent mean resistance.
Carbapenem resistance among more recent E. coli isolates
Table 5 displays carbapenem resistance data for E. coli based on samples collected in 2010 and later, including the mean and range of resistance percentages across studies, and, for nations with at least 100 generalizable isolates since 2010, crude estimated national resistance proportions (median across qualifying reports). Three nations (Egypt, Mali and Sudan) had high estimated resistance. Eight (Benin, Malawi, Mauritania, Mauritius, Morocco, Nigeria, Rwanda and Uganda) had moderate estimated resistance, and resistance in 14 nations (Algeria, Burkina Faso, Chad, Ethiopia, Ghana, Kenya, Libya, Madagascar, Niger, Senegal, South Africa, Tanzania, Tunisia and Zambia) was estimated as low. Resistance was not detected among ≥ 100 E. coli isolates from either the Democratic Republic of the Congo or Mozambique. Among nations with insufficient E. coli isolates to allow estimates, resistance was detected in nine (Angola, Cameroon, Congo, Côte d’Ivoire, Djibouti, Gambia, Sao Tome and Principe, Sierra Leone and Togo) and not detected in 11 (Botswana, Cape Verde, Central African Republic, Equatorial Guinea, Eritrea, Gabon, Guinea, Guinea-Bissau, Somalia, South Sudan and Zimbabwe). No relevant data were identified from Namibia. Resistance data for E. coli are mapped in Fig. 1a.
Carbapenem resistance among more recent Klebsiella isolates
Median carbapenem resistance among recent Klebsiella isolates (Table 6) was estimated as high in 10 nations (Egypt, Ethiopia, Kenya, Libya, Madagascar, Malawi, Mauritius, Nigeria, Sudan and Tunisia). Six nations had moderate estimated resistance (Cameroon, Democratic Republic of the Congo, Ghana, Morocco, South Africa and Zambia), while resistance in 6 others (Algeria, Côte d’Ivoire, Gabon, Namibia, Rwanda and Tanzania) was estimated as low. Burkina and Mauritania had no resistance detected in ≥ 100 isolates. Among nations with insufficient Klebsiella isolates to allow estimates, resistance was detected in 11 (Angola, Benin, Chad, Equatorial Guinea, Gambia, Mali, Sao Tome and Principe, Senegal, Sierra Leone, Togo and Uganda) and not detected in 5 (Botswana, Central African Republic, Guinea-Bissau, Mozambique and Niger). No relevant data were identified from 8 nations (Cape Verde, Congo, Djibouti, Eritrea, Guinea, Somalia, South Sudan and Zimbabwe). Resistance data for Klebsiella are mapped in Fig. 1b.
Carbapenem resistance genotypes
There were 94 data reports from 25 nations identifying at least one carbapenem resistance associated genotype among E. coli isolates (Table 3 and Fig. 2). The most common were blaOXA-48 and blaOXA-181, detected in 14 and 10 nations respectively. blaVIM was identified in 6 nations and blaNDM, blaNDM-1 and blaNDM-5 each reported in 5. blaGES was identified in 3 nations and blaNDM-4, blaOXA, and blaVIM-1 each identified in 2. blaDIM-1, blaIMP, blaIMP-1, blaKPC, blaKPC-2, blaOXA-58, blaVIM-2 and blaVIM-19 were each noted in one nation.
For Klebsiella spp., there were 187 reports from 24 nations identifying at least one carbapenem resistance genotype (Table 4 and Fig. 2). As also noted for E. coli, blaOXA-48 and blaOXA-181 were most common, detected in 14 and 10 nations, respectively. blaKPC was identified in 8 nations, blaNDM-5 and blaVIM in 6, with blaIMP, blaNDM and blaNDM-1 each found in 5. blaKPC-2 was identified in 3 nations and blaIMP-1, blaNDM-4, blaOXA and blaVIM-1 were each identified in 2. blaDIM-1, blaGES, blaKPC-3, blaVIM-2 and blaVIM-19 were each identified in 1 nation.
Polymyxin resistance: overview of data from all years
We found 341 unique data reports, derived from 208 studies, reporting data on polymyxin susceptibility from 33 of 54 African nations (Table 2). These reports included 158 (46.3%) on E. coli and 183 (53.7%) on Klebsiella, originating from 33 and 24 nations, respectively. Resistance was phenotypically or genotypically identified in 23 of the 33 nations (69.6%) from which any data were available. Tables 7 and 8 present national-level polymyxin resistance data for all years studied, including whether resistance was reported, specific genotypes detected and, for samples from generalizable studies, percent mean resistance.
Polymyxin resistance among more recent E. coli isolates
Polymyxin resistance was identified among more recent E. coli isolates from 21 of 33 nations where either phenotypic or genotypic testing was performed (Table 9). Among 11 nations where at least 100 relevant E. coli isolates from 2010 onwards were tested, median polymyxin resistance was estimated as high in Burkina Faso and Côte d’Ivoire, moderate in Mauritania, low in Algeria, Egypt, Morocco, Nigeria, South Africa and Tunisia, and was not detected in Libya and Mauritius. Although resistance was detected, there were insufficient isolates to support estimates for 10 nations (Cameroon, Ethiopia, Ghana, Kenya, Niger, Sao Tome and Principe, Senegal, Sudan, Tanzania and Uganda). Similarly, there were 10 nations with insufficient E. coli isolates to support estimates where resistance was not detected (Angola, Benin, Chad, Congo, Djibouti, Eritrea, Malawi, Mozambique, Somalia and Togo). No relevant data were found from 18 nations (Botswana, Cape Verde, Central African Republic, Democratic Republic of the Congo, Equatorial Guinea, Gabon, Gambia, Guinea, Guinea-Bissau, Madagascar, Mali, Namibia, Rwanda, Sierra Leone, South Sudan, Zambia and Zimbabwe). Resistance data for E. coli are mapped in Fig. 3a.
Polymyxin resistance among more recent Klebsiella isolates
Polymyxin resistance was identified among more recent Klebsiella isolates from 18 of 24 nations where either phenotypic or genotypic testing was performed (Table 10). Resistance was detected in all 8 nations with at least 100 generalizable Klebsiella isolates studied (Algeria, Egypt, Libya, Mauritania, Mauritius, Morocco, South Africa and Tunisia), and was estimated as low in each. Among nations with insufficient isolates to support a resistance estimate, resistance was detected in 8 (Ethiopia, Ghana, Niger, Nigeria, Senegal, Sudan, Tanzania and Uganda) and not detected in 7 (Angola, Benin, Burkina Faso, Cameroon, Kenya, Malawi and Togo). No studies were identified from 25 nations (Botswana, Cape Verde, Central African Republic, Chad, Congo, Côte d’Ivoire, Democratic Republic of the Congo, Djibouti, Equatorial Guinea, Eritrea, Gabon, Gambia, Guinea, Guinea-Bissau, Madagascar, Mali, Mozambique, Namibia, Rwanda, Sao Tome and Principe, Sierra Leone, Somalia, South Sudan, Zambia and Zimbabwe). Resistance data for Klebsiella are mapped in Fig. 3b.
Polymyxin resistance genotypes
Genotypic determinants of polymyxin resistance in E. coli were characterized in 15 data reports on isolates from 7 nations (Table 7 and Fig. 2), with mcr-1 found in all (Algeria, Egypt, Nigeria, Sao Tome and Principe, South Africa, Sudan and Tanzania). phoPQ/pmrAB and mgrB were identified in E. coli from Egypt and South Africa. Among Klebsiella, genotypic polymyxin resistance determinants were identified in 12 reports on isolates from 7 nations (Table 8 and Fig. 2). mcr-1 was identified in Egypt, South Africa and Sudan, and mcr-8 in Algeria. mgrb was reported from six nations (Algeria, Egypt, Libya, Nigeria, South Africa and Tunisia), and phoPQ/pmrAB identified from 4 (Algeria, Egypt, South Africa and Tunisia).
Documented geographic overlaps of carbapenem and polymyxin resistance
Overlapping resistance to carbapenems and polymyxin(s) among E. coli or Klebsiella, whether phenotypic and/or genotypic, was documented in 23 nations with overlapping genotypic resistance present in 9 (Fig. 2). Specific geographic overlaps between NDM carbapenemases and mcr genetic determinants were identified in 6 nations (Algeria, Egypt, Nigeria, South Africa, Sudan and Tanzania).
We searched for and conducted meta-analyses and mapping of available data on carbapenem and polymyxin resistance in E. coli and Klebsiella isolates from humans in Africa. These analyses, which included 1479 unique data reports through the end of 2019, show that resistance to each of these important antibiotic classes has become increasingly widespread on the continent.
The availability of a large amount of additional data since our prior report on WHO Africa nations  provided substantive new insights into the distribution of carbapenem resistance and its genotypic determinants, with resistance documented in approximately ¾ of African nations (compared to less than half previously for WHO Africa ). Carbapenem resistance among Klebsiella was significant in most countries with sufficient isolates to support a resistance estimate and categorized as high in 10, and moderate and low in 6 nations respectively. Among E. coli, estimated resistance was generally somewhat lower: high in 3, moderate in 7, and low in 14 nations with sufficient isolates. Levels of carbapenem resistance appeared high in contiguous areas of Northern and Eastern Africa (e.g. for Klebsiella in Libya, Egypt, Sudan, Ethiopia and Kenya, Fig. 1b). The most widespread genes conferring carbapenem resistance in both species, including in that area, were blaOXA-48, blaNDM-1 and blaOXA-181. Taken together, the analyses document continuing continent-wide spread of carbapenem resistance and of a broad variety of transferrable resistance plasmids, raising concerns about the future reliability of carbapenems.
Given their importance in treating resistant infections, and the paucity of available data, we also searched for and analyzed available information on polymyxin susceptibility. We located data on polymyxin susceptibility for E. coli and/or Klebsiella spp. isolates from 33 of 54 African nations, with resistance identified in 23 of those 33 nations (69.7%) from which any data were available. For the small minority of nations with ≥ 100 isolates studied from 2010 and later, estimated resistance among E. coli to polymyxins was high in 2, moderate in 1 and low in 6. Although resistance was estimated as high in two nations, estimates were based on relatively limited isolate and study numbers, and, in many cases, older methods of susceptibility testing, and should be interpreted with caution. Estimated resistance to polymyxins was low among Klebsiella in all 8 nations with sufficient isolates to support an estimate. Polymyxin resistance genetic determinants were evaluated among E. coli and Klebsiella in 7 nations each, with the mobile mcr-1 determinant shown to be predominant, consistent with recent reviews of the genetics of colistin resistance in E. coli both globally  and in Africa .
Our analyses also show, even based on limited information available from many areas (particularly with respect to polymyxins), that geographic overlapping of carbapenem and polymyxin resistance has become common and widespread, with 23 nations having documented phenotypic and/or genotypic resistance for both. Furthermore, overlapping plasmid mediated resistance to the two drug classes was documented in 9 nations, including the presence of both NDM carbapenemases and mcr genetic determinants in 6. These findings document highly concerning ongoing risks from transferrable resistance, including, were blaNDM and mcr to be acquired by the same organism(s), the risk of infections not susceptible to currently available antibiotics.
Despite efforts to enhance surveillance, major information gaps remain. For example, searches yielded no data on polymyxin resistance from 21 nations, and 6 nations with no available data on carbapenem resistance. Furthermore, even from countries where data were available, there were often less than 100 recent isolates studied, not meeting minimal pre-specified criteria to support crude estimation of resistance proportions.
It is important to note a number of limitations of these analyses, discussed in detail previously [2, 31]. Despite use of predefined study inclusion criteria and employment of common data elements, the inherently diverse data sources, time periods and locations, as well as study designs and methods, mean that inferences must be made with caution and the data should be interpreted in the context of the timing, location and populations studied. Interested readers can access further details, including the primary data from individual reports on specific nations, in the supplemental material (Additional file 4). In addition, susceptibility testing methods and standards for breakpoints to interpret their results have evolved considerably over time and often differ among laboratories. Therefore, comparability of results across laboratories, nations and time periods may be affected by such differences. For carbapenems, minimum inhibitory concentrations considered susceptible have decreased over time, meaning that some decrease in the proportion of isolates susceptible may be expected due to changing standards. There are also major caveats with respect to the interpretation of reported polymyxin susceptibility testing results. Rather than utilizing currently recommended broth microdilution methods, most studies were performed using previously employed disk diffusion methods which may be inconsistent and may overestimate susceptibility. Therefore, while the presence and spread of resistance to polymyxins is well documented, often at both phenotypic and genotypic levels, rate estimates must be interpreted with caution.
Looking at the totality of the data, despite well over a thousand data reports from hundreds of studies, the available information from many countries was limited or, in some cases, absent. Additionally, lag periods between data acquisition and reporting, along with the analysis time since the searches included in the current study, which utilized data available through December 31, 2019, mean that the continued documentation and spread of resistance to new areas is fully expected. Thus, the non-detection of resistance in a nation should not be considered as evidence that resistance was or is absent. Ensuring a more complete picture of resistance distribution and rates will require both ongoing surveillance and continued updating of data and analyses. As also noted, where resistance proportions have been estimated, these should generally be considered to be crude approximations based on non-random reporting and samples, although in our prior study of Southeast Asia  the results from similarly performed meta-analyses generally tracked with national surveillance where available. Similarly, available genotypic data are even more limited, with laboratories often assaying for a limited number of specific genotype(s) rather than broadly characterizing isolates with multiplex or sequence-based methods, likely leading to under-detection of less recognized or uncommon genotypes. Other potential factors may also affect the representativeness of the data, including the tendency toward publication of positive results and the likelihood that laboratories performing susceptibility testing may be located in more urban and regional centers, typically associated with more complex care and drug resistance. We attempted to address such issues by searching not only for positive but also for negative results such as in publications where susceptibility testing was reported but not as the focus of the studies.
Despite such limitations, the findings show the widespread and overlapping presence of carbapenem and polymyxin resistance among E. coli and Klebsiella isolates from humans in Africa and highlight the urgent need to better address remaining gaps in surveillance, including to systematically determine and track rates of carbapenem and polymyxin resistance, and to monitor for the emergence of dually resistant organisms. To do so will require adequate support for sustainable laboratory and epidemiologic capacity, as stressed by both WHO  and the African Union and Africa CDC . Robust ongoing longitudinal AMR surveillance is also critical to inform antibiotic stewardship initiatives [41, 43]. Furthermore, the widespread nature of the CRE and polymyxin resistance threats reinforces the importance of strong infection prevention and control in healthcare facilities [41, 44]. Beyond enhanced stewardship of antimicrobials and measures to contain the spread of MDRO in healthcare, the continuing use of important antimicrobials, including colistin, in animal production remains a problem that must be fully addressed . Resistant organisms may also be present in and spread through waste water, including from healthcare facilities , agriculture, and aquaculture .
Carbapenem resistance among E. coli and Klebsiella is widely distributed in Africa, and documented in 40 of 54 nations. Although resistance rates for nations with sufficient isolates to support estimates were typically low to moderate, high rates (> 5%) were found in several nations, including 10 nations with high rates among Klebsiella. Although far less data are available concerning polymyxins, resistance was documented in 23 of 33 nations with available data. The most widespread resistance associated genotypes were, for carbapenems, blaOXA-48, blaNDM-1 and blaOXA-181 and, for polymyxins, mcr-1, mgrB, and phoPQ/pmrAB. Overlapping phenotypic and/or genotypic resistance to both carbapenems and polymyxins was documented in 23 nations, including the presence of both transferrable NDM carbapenemases and mcr determinants of polymyxin resistance in 6. These findings point to ongoing and significant risks to patient safety and public health from carbapenem and polymyxin resistance. Despite progress in recent years, resistance appears to be spreading and numerous data gaps remain, indicating the need to fully support robust AMR surveillance, antimicrobial stewardship and infection control in a manner that also addresses animal and environmental health dimensions. A One Health approach that enhances surveillance and reduces both the inappropriate use of critical antibiotics and the spread of resistant organisms in all relevant settings is essential .
Availability of data and materials
The dataset supporting the conclusions of this article is available in the Harvard Dataverse repository, https://doi.org/10.7910/DVN/JIJH3W. The dataset(s) supporting the conclusions of this article is also included within the article as Additional file 4.
World Health Organization (WHO). Global antimicrobial resistance surveillance system (GLASS) report: early implementation 2020 [Internet]. Geneva, Switzerland; 2020. Available from: https://apps.who.int/iris/bitstream/handle/10665/332081/9789240005587-eng.pdf?ua=1%0Ahttp://www.who.int/glass/resources/publications/early-implementation-report-2020/en/%0Ahttp://apps.who.int/iris/bitstream/10665/188783/1/9789241549400_eng.pdf?ua=1
Mitgang EA, Hartley DM, Malchione MD, Koch M, Goodman JL. Review and mapping of carbapenem-resistant Enterobacteriaceae in Africa: using diverse data to inform surveillance gaps. Int J Antimicrob Agents. 2018;52(3):372–84. https://doi.org/10.1016/j.ijantimicag.2018.05.019.
Codjoe F, Donkor E. Carbapenem resistance: a review. Med Sci. 2017;6(1):1.
Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci USA. 2018;115(15):E3463–70.
Torres NF, Chibi B, Kuupiel D, Solomon VP, Mashamba-Thompson TP, Middleton LE. The use of non-prescribed antibiotics; prevalence estimates in low-and-middle-income countries. A systematic review and meta-analysis. Arch Public Heal. 2021;79(1):1–15.
Köck R, Daniels-Haardt I, Becker K, Mellmann A, Friedrich AW, Mevius D, et al. Carbapenem-resistant enterobacteriaceae in wildlife, food-producing, and companion animals: a systematic review. Clin Microbiol Infec. 2018;24:1241–50.
Kelly AM, Mathema B, Larson EL. Carbapenem-resistant Enterobacteriaceae in the community: a scoping review. Int J Antimicrob Agents. 2017;50(2):127–34. https://doi.org/10.1016/j.ijantimicag.2017.03.012.
Katale BZ, Misinzo G, Mshana SE, Chiyangi H, Campino S, Clark TG, et al. Genetic diversity and risk factors for the transmission of antimicrobial resistance across human, animals and environmental compartments in East Africa: a review. Antimicrob Resist Infect Control. 2020. https://doi.org/10.1186/s13756-020-00786-7.
Osano E, Arakawa Y, Wacharotayankun R, Ohta M, Horii T, Ito H, et al. Molecular characterization of an enterobacterial metallo β-lactamase found in a clinical isolate of Serratia marcescens that shows imipenem resistance. Antimicrob Agents Chemother. 1994;38(1):71–8.
Yigit H, Queenan AM, Anderson GJ, Domenech-Sanchez A, Biddle JW, Steward CD, et al. Novel carbapenem-hydrolyzing β-lactamase, KPC-1, from a carbapenem-resistant strain of Klebsiella pneumoniae. Antimicrob Agents Chemother. 2001;45(4):1151–61.
Walsh TR. Emerging carbapenemases: a global perspective. Int J Antimicrob Agents. 2010;36(SUPPL. 3):S8. https://doi.org/10.1016/S0924-8579(10)70004-2.
Lee CR, Lee JH, Park KS, Kim YB, Jeong BC, Lee SH. Global dissemination of carbapenemase-producing Klebsiella pneumoniae: epidemiology, genetic context, treatment options, and detection methods. Front Microbiol. 2016;7:1–30.
Munoz-Price LS, Poirel L, Bonomo RA, Schwaber MJ, Daikos G, Cormican M, et al. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect Dis. 2013;13(9):785–96.
Logan LK, Weinstein RA. The epidemiology of Carbapenem-resistant enterobacteriaceae: the impact and evolution of a global menace. J Infect Dis. 2017;215(Suppl 1):S28-36.
Diene SM, Rolain JM. Carbapenemase genes and genetic platforms in gram-negative bacilli: enterobacteriaceae, Pseudomonas and Acinetobacter species. Clin Microbiol Infect. 2014;20(9):831–8. https://doi.org/10.1111/1469-0691.12655.
Poirel L, Jayol A, Nordmanna P. Polymyxins: antibacterial activity, susceptibility testing, and resistance mechanisms encoded by plasmids or chromosomes. Clin Microbiol Rev. 2017;30:557–96.
Li J, Nation RL, Turnidge JD, Milne RW, Coulthard K, Rayner CR, et al. Colistin: the re-emerging antibiotic for multidrug-resistant Gram-negative bacterial infections. Lancet Infect Dis. 2006;6(9):589–601.
Aghapour Z, Gholizadeh P, Ganbarov K, Bialvaei AZ, Mahmood SS, Tanomand A, et al. Molecular mechanisms related to colistin resistance in enterobacteriaceae. Infect Drug Resist. 2019;12:965–75.
Shen Z, Hu Y, Sun Q, Hu F, Zhou H, Shu L, et al. Emerging carriage of NDM-5 and MCR-1 in Escherichia coli from healthy people in multiple regions in China: a cross sectional observational study. EClinicalMedicine. 2018;6:11–20. https://doi.org/10.1016/j.eclinm.2018.11.003.
Zheng B, Dong H, Xu H, Lv J, Zhang J, Jiang X, et al. Coexistence of MCR-1 and NDM-1 in clinical Escherichia coli Isolates. Clin Infect Dis. 2016;63(10):1393–5.
Huang H, Dong N, Shu L, Lu J, Sun, Qiaoling, Waichi Chan E, Chen S, et al. Colistin-resistance gene mcr in clinical carbapenem-resistant Enterobacteriaceae strains in China, 2014–2019. Emerg Microbes Infect. 2020;9(1):237–45.
Mediavilla JR, Patrawalla A, Chen L, Chavda KD, Mathema B, Vinnard C, et al. Colistin- and carbapenem-resistant Escherichia coli harboring mcr-1 and blaNDM-5, causing a complicated urinary tract infection in a patient from the United States. MBio. 2016;7(4):1–4.
Bartsch SM, Mckinnell JA, Mueller LE, Miller LG, Gohil SK, Huang SS, et al. Potential economic burden of carbapenem-resistant Enterobacteriaceae (CRE) in the United States. Clin Microbiol Infect. 2017;
World Health Organization. Global Antimicriobial Resistance Surveillance System (GLASS) [Internet]. 2021 [cited 2022 Oct 4]. Available from: https://www.who.int/initiatives/glass
World Health Organization (WHO). Antimicrobial resistance: global report on surveillance [Internet]. 2014. Available from: https://www.who.int/antimicrobial-resistance/publications/surveillancereport/en/
World Health Organization (WHO). Global antimicrobial resistance surveillance system (GLASS) report: early implementation 2016–2017 [Internet]. Geneva, Switzerland; 2017. Available from: https://apps.who.int/iris/bitstream/handle/10665/259744/9789241513449-eng.pdf
World Health Organization (WHO). Global antimicrobial resistance surveillance system (GLASS) report: early implementation 2017–2018 [Internet]. Geneva, Switzerland; 2018. Available from: https://apps.who.int/iris/bitstream/handle/10665/279656/9789241515061-eng.pdf?ua=1
Berrazeg M, Diene SM, Medjahed L, Parola P, Drissi M, Raoult D, et al. New Delhi metallo-beta-lactamase around the world: an eReview using google maps. Eurosurveillance. 2014;19(20):1–14.
Manenzhe RI, Zar HJ, Nicol MP, Kaba M. The spread of carbapenemase-producing bacteria in Africa: a systematic review. J Antimicrob Chemother. 2015;70(1):23–40.
Tadesse BT, Ashley EA, Ongarello S, Havumaki J, Wijegoonewardena M, González IJ, et al. Antimicrobial resistance in Africa: a systematic review. BMC Infect Dis. 2017;17(1):1–17.
Malchione MD, Torres LM, Hartley DM, Koch M, Goodman JL. Carbapenem and colistin resistance in Enterobacteriaceae in Southeast Asia: review and mapping of emerging and overlapping challenges. Int J Antimicrob Agents. 2019;54(4):381–99.
Ssekatawa K, Byarugaba DK, Wampande E, Ejobi F. A systematic review: the current status of carbapenem resistance in East Africa. BMC Res Notes. 2018;11(1):1–9. https://doi.org/10.1186/s13104-018-3738-2.
Irek EO, Amupitan AA, Obadare TO, Aboderin AO. A systematic review of healthcare-associated infections in Africa: an antimicrobial resistance perspective. Afr J Lab Med. 2018. https://doi.org/10.4102/ajlm.v7i2.796.
Okomo U, Akpalu ENK, Le Doare K, Roca A, Cousens S, Jarde A, et al. Aetiology of invasive bacterial infection and antimicrobial resistance in neonates in sub-Saharan Africa: a systematic review and meta-analysis in line with the STROBE-NI reporting guidelines. Lancet Infect Dis. 2019;19(11):1219–34. https://doi.org/10.1016/S1473-3099(19)30414-1.
Dadashi M, Sameni F, Bostanshirin N, Yaslianifard S, Khosravi-Dehaghi N, Nasiri MJ, et al. Global prevalence and molecular epidemiology of mcr-mediated Colistin resistance in Escherichia coli clinical isolates: a systematic review. J Glob Antimicrob Resist. 2021. https://doi.org/10.1016/j.jgar.2021.10.022.
Olowo-Okere A, Yacouba A. Molecular mechanisms of colistin resistance in africa: a systematic review of literature. Germs. 2020;10(4):367–79.
ProMED-Mail. International Society for Infectious Diseases [Internet]. [cited 2022 Oct 4]. Available from: https://www.promedmail.org/
Center for Disease Dynamics Economics and Policy. Resistance Map. [Internet]. [cited 2022 Oct 4]. Available from: https://resistancemap.cddep.org/
HealthMap. HealthMap - virus and contagious disease surveillance [Internet]. [cited 2022 Oct 4]. Available from: https://healthmap.org/en/
World Health Organization (WHO). The use of antiretroviral drugs for treating and preventing HIV infection Recommendations for a public health approach [Internet]. 2nd ed. World Health Organisation (WHO). Geneva; 2016. Definition of key terms. Available from: https://www.ncbi.nlm.nih.gov/books/NBK374295/
World Health Organization (WHO). Antimicrobial stewardship programmes in health-care facilities in low- and middle-income countries: a WHO practical toolkit [Internet]. Vol. 1, JAC-Antimicrobial Resistance. 2019. Available from: https://www.who.int/publications/i/item/9789241515481
Africa Centres for Disease Control and Prevention. African Union Framework for Antimicrobial Resistance Control 2020–2025 [Internet]. 2020. Available from: https://africacdc.org/download/african-union-framework-for-antimicrobial-resistance-control-2020-2025/
Africa Centres for Disease Control and Prevention. African antibiotic treatment guidelines for common bacterial infections and syndromes. 2021. Available from: https://africacdc.org/download/african-antibiotic-treatment-guidelines-for-common-bacterial-infections-and-syndromes-2/
World Health Organization (WHO). Guidelines for the prevention and control of carbapenem-resistant Enterobacteriaceae, Acinetobacter baumannii and Pseudomonas aeruginosa in health care facilities [Internet]. Geneva; 2017. Available from: https://www.who.int/publications/i/item/9789241550178
Dhaouadi S, Soufi L, Hamza A, Fedida D, Zied C, Awadhi E, et al. Co-occurrence of mcr-1 mediated colistin resistance and β-lactamase-encoding genes in multidrug-resistant Escherichia coli from broiler chickens with colibacillosis in Tunisia. J Glob Antimicrob Resist. 2020;22:538–45.
WHO, FAO, OIE. Technical brief on water, sanitation, hygiene and wastewater management to prevent infections and reduce the spread of antimicrobial resistance [Internet]. 2020. Available from: https://www.who.int/water_sanitation_health/publications/wash-wastewater-management-to-prevent-infections-and-reduce-amr/en/
Mendelson M, Brink A, Gouws J, Mbelle N, Naidoo V, Pople T, et al. The One Health stewardship of colistin as an antibiotic of last resort for human health in South Africa. Lancet Infect Dis. 2018;18(9):e288–94.
Abderrahim A, Djahmi N, Pujol C, Nedjai S, Bentakouk MC, Kirane-Gacemi D, et al. First case of NDM-1-producing Klebsiella pneumoniae in Annaba University Hospital, Algeria. Microb Drug Resist. 2017;23(7):895–900.
Agabou A, Lezzar N, Ouchenane Z, Khemissi S, Satta D, Sotto A, et al. Clonal relationship between human and avian ciprofloxacin-resistant Escherichia coli isolates in North-Eastern Algeria. Eur J Clin Microbiol Infect Dis. 2016.
Belbel Z, Lalaoui R, Bakour S, Nedjai S, Djahmi N, Rolain JM. First report of colistin resistance in an OXA-48- and a CTX-M-15 producing Klebsiella pneumoniae clinical isolate in Algeria due to PmrB protein modification and mgrB inactivation. J Glob Antimicrob Resist. 2018;14:158–60.
Bentroki AA, Gouri A, Yakhlef A, Touaref A, Gueroudj A, Bensouilah T. Antibiotic resistance of strains isolated from community acquired urinary tract infections between 2007 and 2011 in Guelma (Algeria). Ann Biol Clin (Paris). 2012;70(6):666–8.
Berrazeg M, Drissi M, Medjahed L, Rolain JM. Hierarchical clustering as a rapid tool for surveillance of emerging antibiotic-resistance phenotypes in Klebsiella pneumoniae strains. J Med Microbiol. 2013. https://doi.org/10.1099/jmm.0.049437-0.
Berrazeg M, Hadjadj L, Ayad A, Drissi M, Rolain JM. First detected human case in Algeria of mcr-1 plasmid-mediated colistin resistance in a 2011 Escherichia coli isolate. Antimicrob Agents Chemother. 2016;60(11):6996–7.
Betitra Y, Teresa V, Miguel V, Abdelaziz T. Determinants of quinolone resistance in Escherichia coli causing community-acquired urinary tract infection in Bejaia, Algeria. Asian Pac J Trop Med. 2014.
Cuzon G, Bentchouala C, Vogel A, Héry M, Lezzar A, Smati F, et al. First outbreak of OXA-48-positive carbapenem-resistant Klebsiella pneumoniae isolates in Constantine, Algeria. Int J Antimicrob Agents. 2015. https://doi.org/10.1016/j.ijantimicag.2015.08.005.
Epelboin L, Robert J, Tsyrina-Kouyoumdjian E, Laouira S, Meyssonnier V, Caumes E. High rate of multidrug-resistant gram-negative bacilli carriage and infection in hospitalized returning travelers: a cross-sectional cohort study. J Travel Med. 2015;22(5):292–9.
Gauthier L, Dortet L, Cotellon G, Creton E, Cuzon G, Ponties V, et al. Diversity of carbapenemase-producing Escherichia coli isolates in France in 2012–2013. Antimicrob Agents Chemother. 2018. https://doi.org/10.1128/AAC.00266-18.
Gharout-Sait A, Touati A, Benallaoua S, Guillard T, Brasme L, de Champs C. CTX-M from community-acquired urinary tract infections in Algeria. Afr J Microbiol Res. 2012;6(25). Available from: http://www.academicjournals.org/ajmr/abstracts/abstracts/abstract2012/5July/Gharout-Sait et al.htm
Gharout-Sait A, Touati A, Guillard T, Brasme L, de Champs C. Molecular characterization and epidemiology of cefoxitin resistance among Enterobacteriaceae lacking inducible chromosomal ampC genes from hospitalized and non-hospitalized patients in Algeria: description of new sequence type in Klebsiella pneumoniae iso. Brazil J Infect Dis. 2015. https://doi.org/10.1016/j.bjid.2014.12.001.
Agabou A, Pantel A, Ouchenane Z, Lezzar N, Khemissi S, Satta D, et al. First description of OXA-48-producing Escherichia coli and the pandemic clone ST131 from patients hospitalised at a military hospital in Algeria. Eur J Clin Microbiol Infect Dis. 2014.
Hecini-Hannachi A, Bentchouala C, Lezzar A, Laouar H, Benlabed K, Smati F. Multidrug-resistant bacteria isolated from patients hospitalized in intensive care unit in University Hospital of Constantine, Algeria (2011–2015). Afr J Microbiol Res. 2016;10(33):1328–36.
Iabadene H, Messai Y, Ammari H, Alouache S, Verdet C, Bakour R, et al. Prevalence of plasmid-mediated AmpC β-lactamases among Enterobacteriaceae in Algiers hospitals. Int J Antimicrob Agents. 2009;34(4):340–2.
Labid A, Gacemi-Kirane D, Timinouni M, Amoura K, Rolain J-M. High prevalence of extended spectrum beta-lactamase (ESBL) producers in fatal cases of pediatric septicemia among the Enterobacteriaceae in the pediatric hospital of Annaba, Algeria. Afr J Microbiol Res. 2014;8(9):947–54.
Lagha N, Abdelouahid D-E, Hassaine H, Robin F, Bonnet R. First characterization of CTX-M-15 and DHA-1 -lactamases among clinical isolates of Klebsiella pneumoniae in Laghouat Hospital, Algeria. Afr J Microbiol Res. 2014;8(11):1221–7.
Lagha N, Hassaine H, Robin F, Bonnet R, Abdelouahid D-E. Prevalence and molecular typing of extended-spectrum -lactamases in Escherichia coli, Enterobacter cloacae and Citrobacter freundii isolates from Laghouat Hospital, Algeria. Afr J Microbiol Res. 2016;10(35):1430–8.
Loucif L, Chelaghma W, Helis Y, Sebaa F, Douniazed Baoune R, Zaatout W, et al. First detection of OXA-48-producing Klebsiella pneumoniae in community-acquired urinary tract infection in Algeria. J Glob Antimicrob Resist. 2018;12:115–6.
Loucif L, Kassah-Laouar A, Saidi M, Messala A, Chelaghma W, Rolain JM. Outbreak of OXA-48-producing Klebsiella pneumoniae involving a sequence type 101 clone in Batna University Hospital, Algeria. Antimicrob Agents Chemother. 2016.
Mairi A, Pantel A, Sotto A, Lavigne JP, Touati A. OXA-48-like carbapenemases producing Enterobacteriaceae in different niches in Algeria: clonal expansion, plasmid characteristics and virulence traits. Eur J Clin Microbiol Infect Dis. 2018.
Mairi A, Touati A, Ait Bessai S, Boutabtoub Y, Khelifi F, Sotto A, et al. Carbapenemase-producing Enterobacteriaceae among pregnant women and newborns in Algeria: prevalence, molecular characterization, maternal-neonatal transmission, and risk factors for carriage. Am J Infect Control. 2019;47(1):105–8.
Medboua-Benbalagh C, Touati A, Kermas R, Gharout-Sait A, Brasme L, Mezhoud H, et al. Fecal carriage of extended-spectrum beta-lactamase-producing enterobacteriaceae strains is associated with worse outcome in patients hospitalized in the pediatric oncology unit of Beni-Messous Hospital in Algiers. Algeria Microb Drug Resist. 2017;23(6):757–63.
Aggoune N, Tali-Maamar H, Assaous F, Benamrouche N, Naim M, Rahal K. Emergence of plasmid mediated carbapenemase OXA-48 in a Klebsiella pneumoniae strain in Algeria. J Glob Antimicrob Resist. 2014. https://doi.org/10.1016/j.jgar.2014.06.001.
Mellouk FZ, Bakour S, Meradji S, Al-Bayssari C, Bentakouk MC, Zouyed F, et al. First detection of VIM-4-producing Pseudomonas aeruginosa and OXA-48-producing Klebsiella pneumoniae in Northeastern (Annaba, Skikda) Algeria. Microb Drug Resist. 2017;23(3):335–44.
Messai Y, Benhassine T, Naim M, Paul G, Bakour R. Prevalence of β-lactams resistance among Escherichia coli clinical isolates from a hospital in Algiers. Rev Esp Quimioter. 2006.
Messai Y, Iabadene H, Benhassine T, Alouache S, Tazir M, Gautier V, et al. Prevalence and characterization of extended-spectrum β-lactamases in Klebsiella pneumoniae in Algiers hospitals (Algeria). Pathol Biol. 2008. https://doi.org/10.1016/j.patbio.2008.05.008.
Nabti LZ, Sahli F, Hadjadj L, Ngaignam EP, Lupande-Mwenebitu D, Rolain J-M, et al. Autochthonous case of mobile colistin resistance gene mcr-1 from a uropathogenic Escherichia coli isolate in Sétif Hospital Algeria. J Antimicrob Resist. 2019;19:356–7.
Nabti LZ, Sahli F, Ngaiganam EP, Radji N, Mezaghcha W, Lupande-Mwenebitu D, et al. Development of real-time PCR assay allowed describing the first clinical Klebsiella pneumoniae isolate harboring plasmid-mediated colistin resistance mcr-8 gene in Algeria. J Glob Antimicrob Resist. 2020;20:266–71. https://doi.org/10.1016/j.jgar.2019.08.018.
Nedjai S, Barguigua A, Djahmi N, Jamali L, Zerouali K, Dekhil M, et al. Prevalence and characterization of extended spectrum β-lactamases in Klebsiella-Enterobacter-Serratia group bacteria. Algeria Med Mal Infect. 2012. https://doi.org/10.1016/j.medmal.2011.10.001.
Potron A, Rondinaud E, Nordmann P, Poirel L, Rondinaud E, Nordmann P. Intercontinental spread of OXA-48 beta-lactamase-producing Enterobacteriaceae over a 11-year period, 2001 to 2011. Surveill Outbreak Reports. 2013;18(31). Available from: www.eurosurveillance.org
Ramdani-Bouguessa N, Manageiro V, Jones-Dias D, Ferreira E, Tazir M, Caniça M. Role of SHV β-lactamase variants in resistance of clinical Klebsiella pneumoniae strains to β-lactams in an Algerian hospital. J Med Microbiol. 2011. https://doi.org/10.1099/jmm.0.030577-0.
Ramdani-Bouguessa N, Mendonça N, Leitão J, Ferreira E, Tazir M, Caniça M. CTX-M-3 and CTX-M-15 extended-spectrum β-lactamases in isolates of Escherichia coli from a hospital in Algiers. Algeria J Clin Microbiol. 2006. https://doi.org/10.1128/JCM.01445-06.
Robin F, Aggoune-Khinache N, Delmas J, Naim M, Bonnet R. Novel VIM metallo-β-lactamase variant from clinical isolates of Enterobacteriaceae from Algeria. Antimicrob Agents Chemother. 2010. https://doi.org/10.1128/AAC.00017-09.
Aggoune N, Tali-Maamar H, Assaous F, Guettou B, Laliam R, Benamrouche N, et al. Wide spread of oxa-48-producing enterobacteriaceae in algerian hospitals: a four years’ study. J Infect Dev Ctries. 2018;12(11):1039–44.
Rodriguez-Martinez JM, Nordmann P, Fortineau N, Poirel L. VIM-19, a metallo-β-lactamase with increased carbapenemase activity from Escherichia coli and Klebsiella pneumoniae. Antimicrob Agents Chemother. 2010;54(1):471–6.
Sassi A, Loucif L, Gupta SK, Dekhil M, Chettibi H, Rolain JM. NDM-5 carbapenemase-encoding gene in multidrug-resistant clinical isolates of Escherichia coli from Algeria. Antimicrob Agents Chemother. 2014. https://doi.org/10.1128/AAC.02818-13.
Touati A, Benallaoua S, Forte D, Madoux J, Brasme L, de Champs C. First report of CTX-M-15 and CTX-M-3 β-lactamases among clinical isolates of Enterobacteriaceae in Béjaia, Algeria. Int J Antimicrob Agents. 2006.
Toumi S, Meliani S, Amoura K, Rachereche A, Djebien M, Djahoudi A. Multidrug-resistant Gram-negative bacilli producing oxacillinases and Metallo-β-lactamases isolated from patients in intensive care unit - Annaba hospital - Algeria (2014–2016). J Appl Pharm Sci. 2018;8(7):107–13.
Yagoubat M, Ould El-Hadj-Khelil A, Malki A, Bakour S, Touati A, Rolain JM. Genetic characterisation of carbapenem-resistant Gram-negative bacteria isolated from the University Hospital Mohamed Boudiaf in Ouargla, southern Algeria. J Glob Antimicrob Resist. 2017;8:55–9.
Yahiaoui M, Robin F, Bakour R, Hamidi M, Bonnet R, Messai Y. Antibiotic resistance, virulence, and genetic background of community-acquired uropathogenic Escherichia coli from Algeria. Microb Drug Resist. 2015;21(5):516–26.
Yanat B, Machuca J, Díaz-De-Alba P, Mezhoud H, Touati A, Pascual Á, et al. Characterization of plasmid-mediated quinolone resistance determinants in high-level quinolone-resistant enterobacteriaceae isolates from the community: first Report of qnrD gene in Algeria. Microb Drug Resist. 2017;23(1):90–7.
Yanat B, Machuca J, Yahia RD, Touati A, Pascual Á, Rodriguez-Martinez JM, et al. First report of the plasmid-mediated colistin resistance gene mcr-1 in a clinical Escherichia coli isolate in Algeria. Int J Antimicrob Agents. 2016;48(6):760–1.
Yousfi H, Hadjadj L, Dandachi I, Lalaoui R, Merah A, Amoura K, et al. Colistin- and carbapenem-resistant Klebsiella pneumoniae clinical isolates: Algeria. Microb Drug Resist. 2019;25(2):258–63.
Zenati F, Barguigua A, Nayme K, Benbelaïd F, Khadir A, Bellahsene C, et al. Characterization of uropathogenic ESBL-producing Escherichia coli isolated from hospitalized patients in western Algeria. J Infect Dev Ctries. 2019;13(4):291–302.
Ahmed ZB, Ayad A, Mesli E, Messai Y, Bakour R, Drissi M. CTX-M-15 extended-spectrum β-lactamases in Enterobacteriaceae in the intensive care unit of Tlemcen Hospital, Algeria. East Mediterr Heal J. 2012;
Aouf A, Gueddi T, Djeghout B, Ammari H. Frequency and susceptibility pattern of uropathogenic enterobacteriaceae isolated from patients in Algiers. Algeria J Infect Dev Ctries. 2018;12(4):244–9.
Ayad A, Drissi M, de Curraize C, Dupont C, Hartmann A, Solanas S, et al. Occurence of ArmA and RmtB aminoglycoside resistance 16S rRNA methylases in extended-spectrum β-lactamases producing Escherichia coli in Algerian hospitals. Front Microbiol. 2016;7(SEP).
Bakour S, Sahli F, Touati A, Rolain JM. Emergence of KPC-producing Klebsiella pneumoniae ST512 isolated from cerebrospinal fluid of a child in Algeria. New Microbes New Infect. 2015;3(C):34–6.
Belbel Z, Chettibi H, Dekhil M, Ladjama A, Nedjai S, Rolain JM. Outbreak of an armA Methyltransferase-producing ST39 Klebsiella pneumoniae clone in a pediatric Algerian hospital. Microb Drug Resist. 2014.
Kieffer N, Nordmann P, Aires-De-Sousa M, Poirel L. High prevalence of carbapenemase-producing Enterobacteriaceae among hospitalized children in Luanda, Angola. Antimicrob Agents Chemother. 2016.
Poirel L, Goutines J, Aires-De-Sousa M, Nordmann P. High rate of association of 16S rRNA methylases and carbapenemases in enterobacteriaceae recovered from Hospitalized Children in Angola. Antimicrob Agents Chemother. 2018;62(4):1–7.
Ahoyo AT, Baba-Moussa L, Anago AE, Avogbe P, Missihoun TD, Loko F, et al. Incidence of infections due to Escherichia coli strains producing extended spectrum betalactamase, in the Zou/Collines Hospital Centre (CHDZ/C) in Benin. Med Mal Infect. 2007.
Ahoyo TA, Bankolé HS, Adéoti FM, Gbohoun AA, Assavèdo S, Amoussou-Guénou M, et al. Prevalence of nosocomial infections and anti-infective therapy in Benin: Results of the first nationwide survey in 2012. Antimicrob Resist Infect Control. 2014. https://doi.org/10.1186/2047-2994-3-17.
Anago E, Ayi-Fanou L, Akpovi CD, Hounkpe WB, Agassounon-Djikpo Tchibozo M, Bankole HS, et al. Antibiotic resistance and genotype of beta-lactamase produci.g Escherichia coli in nosocomial infections in Cotonou, Benin. Ann Clin Microbiol Antimicrob. 2015.
Dougnon V, Koudokpon H, Hounmanou YMG, Azonbakin S, Fabiyi K, Oussou A, et al. High prevalence of multidrug-resistant bacteria in the centre hospitalier et Universitaire de la Mère et de l’Enfant Lagune (CHU-MEL) reveals implications of poor hygiene practices in healthcare. SN Compr Clin Med. 2019;1(12):1029–37.
Koudokon H, Dougnon V, Hadjadj L, Kissira I, Fanou B, Loko F, et al. First Sequence Analysis of genes mediating extended-spectrum beta-lactamase (ESBL) bla-TEM, SHV-and CTX-M production in isolates of enterobacteriaceae in Southern Benin. Int J Infect. 2018. https://doi.org/10.5812/iji.83194.
Mousse W, Sina H, Wele M, Chabi N, Nouvlessounon DD, Bade FT, et al. Molecular characterization and Antibiotic resistance profiles of Escherichia coli extended-spectrum β-lactamases producer strains isolated from urine samples in Benin. Eur Sci J. 2018;14(30):323–37.
Mpinda-Joseph P, Anand Paramadhas BD, Reyes G, Maruatona MB, Chise M, Monokwane-Thupiso BB, et al. Healthcare-associated infections including neonatal bloodstream infections in a leading tertiary hospital in Botswana. Hosp Pract. 2019;47(4):203–10.
Amana MD, Wend-Kuni TRY, Aminata BY, Mahoukede ZT, Serge S, Koudbi ZJ, et al. Detection of multidrug-resistant enterobacteria simultaneously producing extended-spectrum β- lactamases of the PER and GES types isolated at Saint Camille Hospital Center, Ouagadougou, Burkina Faso. Afr J Microbiol Res. 2019;13(26):414–20.
Ouédraogo AS, Sanou S, Kissou A, Poda A, Aberkane S, Bouzinbi N, et al. Fecal carriage of enterobacteriaceae producing extended-spectrum beta-lactamases in hospitalized patients and healthy community volunteers in Burkina Faso. Microb Drug Resist. 2017;23(1):63–70.
Ouedraogo A-S, Sanou M, Kissou A, Sanou S, Solaré H, Kaboré F, et al. High prevalence of extended-spectrum β-lactamase producing enterobacteriaceae among clinical isolates in Burkina Faso. BMC Infect Dis. 2016. https://doi.org/10.1186/s12879-016-1655-3.
Reid CS, Bonkoungou K. Vesico-umbilical fistula in a child with severe vesico-ureteral reflux and bladder diverticulum. Trop Doct. 2017;47(3):271–3.
Sanou M, Ky A, Ouangre E, Bisseye C, Sanou A, Nagalo BM, et al. Characterization of bacterial flora in community peritonitis carried out in Burkina Faso. Pan Afr Med J. 2014. https://doi.org/10.11604/pamj.2014.18.17.3157.
Toy T, Pak GD, Duc TP, Campbell JI, El Tayeb MA, Von Kalckreuth V, et al. Multicountry distribution and characterization of extended-spectrum beta-lactamase-associated gram-negative bacteria from bloodstream infections in Sub-Saharan Africa. Clin Infect Dis. 2019;69(S6):449–58.
Zongo KJ, Dabire AM, Compaore LG, Sanou I, Sangare L, Simpore J, et al. First detection of bla TEM, SHV and CTX-M among Gram negative bacilli exhibiting extended spectrum -lactamase phenotype isolated at University Hospital Center, Yalgado Ouedraogo, Ouagadougou, Burkina Faso. Afr J Biotechnol. 2015;14(14):1174–80.
Frida ST, Karim OA, Theodora ZM, Dorcas O-Y, Theophane YA, Florencia DW, et al. Prevalence of lower genital tract infections in women: case of Saint Camille Hospital of Ouagadougou from 2015 to 2018. Int J Curr Res. 2019;11(10):7721–7.
Guira O, Tiéno H, Sagna Y, Yaméogo TM, Zoungrana L, Traoré S, et al. Antibiotic susceptibility of bacteria isolated from diabetic foot infections and prospects for empiric antibiotic therapy in Ouagadougou (Burkina Faso). Med Sante Trop. 2015;25(3):291–5.
Guiral E, Gonçalves Quiles M, Munoz L, Moreno-Morales J, Aejo-Cancho I, Salvador P, et al. Emergence of resistance to quinolones and B-lactam antibiotics in enteroaggregative and enterotoxigenic Escherichia coli causing traveler’s diarrhea. Antimicrob Agents Chemother. 2019;63(2):e01745-e1818.
Konaté A, Dembélé R, Guessennd NK, Kouadio FK, Kouadio IK, Ouattara MB, et al. Epidemiology and antibiotic resistance phenotypes of diarrheagenic Escherichia coli responsible for infantile gastroenteritis in Ouagadougou, Burkina Faso. Eur J Microbiol Immunol. 2017;7(3):168–75.
Kpoda DSS, Guessennd N, Bonkoungou JI, Ouattara MB, Konan F, Ajayi A, et al. Prevalence and resistance profile of extended-spectrum beta -lactamases-producing Enterobacteriaceae in Ouagadougou, Burkina Faso. Afr J Microbiol Res. 2017;11(27):1120–6.
Maltha J, Guiraud I, Kaboré B, Lompo P, Ley B, Bottieau E, et al. Frequency of severe malaria and invasive bacterial infections among children admitted to a rural hospital in Burkina Faso. PLoS ONE. 2014. https://doi.org/10.1371/journal.pone.0089103.
Metuor-Dabire A, Zongo JK, Zeba B, Ouédraogo RT, Moussawi J, Baucher M, et al. First detection of SHV-type extended spectrum B-Lactamases in the University Hospital Complex Paediatric Charles de Gaulle (CUP-CDG) of Ouagadougou in Burkina Faso. J Asian Sci Res. 2014;4(5):214–21.
Ouédraogo AS, Compain F, Sanou M, Aberkane S, Bouzinbi N, Hide M, et al. First description of IncX3 plasmids carrying blaOXA-181 in Escherichia coli clinical isolates in Burkina Faso. Antimicrob Agents Chemother. 2016;60(5):3240–2.
Ateudjieu J, Bita’a LB, Guenou E, Chebe AN, Chukuwchindun BA, Goura AP, et al. Profile and antibiotic susceptibility pattern of bacterial pathogens associated with diarrheas in patients presenting at the Kousseri regional hospital Anne, Far North, Cameroon. Pan Afr Med J. 2018. https://doi.org/10.11604/pamj.2018.29.170.14296.
Lonchel CM, Melin P, Gangoué-Piéboji J, Assoumou MCO, Boreux R, De Mol P. Extended-spectrum β-lactamase-producing Enterobacteriaceae in Cameroonian hospitals. Eur J Clin Microbiol Infect Dis. 2013;32(1):79–87.
Ngalani OJT, Mbaveng AT, Marbou WJT, Ngai RY, Kuete V. Antibiotic resistance of enteric bacteria in HIV-infected patients at the Banka Ad-Lucem Hospital, West Region of Cameroon. Can J Infect Dis Med Microbiol. 2019.
Yeika EV, Foryoung JB, Efie DT, Nkwetateba EA, Tolefac PN, Ngowe MN. Multidrug resistant Proteus mirabilis and Escherichia coli causing fulminant necrotising fasciitis: a case report. BMC Res Notes. 2018. https://doi.org/10.1186/s13104-018-3413-7.
Betbeui A, Kamga H, Toukam M, Mbakop C, Lyonga E, Bilong S, et al. Phenotypic Detection of Extended Spectrum Beta-Lactamase and Carbapenemases Produced by Klebsiella spp Isolated from Three Referrals Hospitals in Yaounde, Cameroon. Br Microbiol Res J. 2015.
Dehayem M, Ngassam E, Mendane F, Balla V, Saji J, Sobngwi E, et al. OP67 Bacteriology of diabetic foot infections and susceptibility to antimicrobial agents in Cameroon. Diabetes Res Clin Pract. 2014;103:S27.
Dortet L, Poirel L, Anguel N, Nordmann P. New Delhi metallo-β-lactamase 4-producing Escherichia coli in Cameroon. Emerg Infect Dis. 2012.
Founou LL, Founou RC, Allam M, Ismail A, Essack SY. Draft genome sequence of an extended-spectrum β-lactamase (CTX-M-15)-producing Escherichia coli ST10 isolated from a nasal sample of an abattoir worker in Cameroon. J Glob Antimicrob Resist. 2018;14:68–9.
Founou LL, Founou RC, Ntshobeni N, Govinden U, Bester LA, Chenia HY, et al. Emergence and spread of extended spectrum β-lactamase producing enterobacteriaceae (ESBL-PE) in pigs and exposed workers: a multicentre comparative study between Cameroon and South Africa. Pathogens. 2019;8(1).
Gangoue-Pieboji J, Koulla-Shiro S, Ngassam P, Adiogo D, Ndumbe P. Antimicrobial activity against gram negative bacilli from Yaounde Central Hospital, Cameroon. Afr Health Sci. 2006;
Gangoué-Piéboji J, Miriagou V, Vourli S, Tzelepi E, Ngassam P, Tzouvelekis LS. Emergence of CTX-M-15-producing enterobacteria in Cameroon and characterization of a blaCTX-M-15-carrying element. Antimicrob Agents Chemother. 2005;49(1):441–3.
Lonchel CM, Meex C, Gangoue-Piebogji J, Boreux R, Assoumou M-CO, Melin P, et al. Proportion of extended-spectrum ß-lactamase-producing Enterobacteriaceae in community setting in Ngaoundere, Cameroon. BMC Infect Dis. 2012;
Farra A, Frank T, Tondeur L, Bata P, Gody JC, Onambele M, et al. High rate of faecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae in healthy children in Bangui, Central African Republic. Clin Microbiol Infect. 2016;
Rafai C, Frank T, Manirakiza A, Gaudeuille A, Mbecko J-R, Nghario L, et al. Dissemination of IncF-type plasmids in multiresistant CTX-M-15-producing Enterobacteriaceae isolates from surgical-site infections in Bangui, Central African Republic Clotaire. BMC Microbiol. 2015;15(15).
Kengne M, Dounia AT, Nwobegahay JM. Bacteriological profile and antimicrobial susceptibility patterns of urine culture isolates from patients in Ndjamena. Chad Pan Afr Med J. 2017. https://doi.org/10.11604/pamj.2017.28.258.11197.
Mahamat OO, Lounnas M, Hide M, Dumont Y, Tidjani A, Kamougam K, et al. High prevalence and characterization of extended-spectrum ß-lactamase producing Enterobacteriaceae in Chadian hospitals. BMC Infect Dis. 2019. https://doi.org/10.1186/s12879-019-3838-1.
Mahamat OO, Lounnas M, Hide M, Tidjani A, Benavides J, Diack A, et al. Spread of NDM-5 and OXA-181 Carbapenemase-Producing Escherichia coli in Chad. Antimicrob Agents Chemother. 2019;63(11):1–5.
Ndoutamia G, Yandai FH, Nadlaou B. Antimicrobial resistance in extended spectrum β-lactamases (ESBL)-producing Escherichia coli isolated from human urinary tract infections in Ndjamena, Chad. African J Microbiol Res. 2015.
Yandaïab F, Zongoa C, Moussac A, Bessimbayea N, Tapsobaa F, Savadogoa A, et al. Prevalence and antimicrobial susceptibility of faecal carriage of Extended-Spectrum β -lactamase (ESBL) producing Escherichia coli at the “ Hôpital de la M ère et de l’Enfant ” in N’ Djamena. Chad Sci J Microbiol. 2014;3:25–31.
Yandai FH, Ndoutamia G, Nadlaou B, Barro N. Prevalence and resistance profile of Escherichia coli and Klebsiella pneumoniae isolated from urinary tract infections in N’Djamena. Tchad Int J Biol Chem Sci. 2019;13(4):2065–73.
Moyen R, Ahombo G, Nguimbi E, Ontsira NE, Niama RF, Yala GC, et al. Activity of beta-lactam antibiotics and production of beta-lactamases in bacteria isolated from wound infections in Brazzaville, Congo. African J Microbiol Res. 2014;
Mpelle FL, Ngoyi ENO, Kayath CA, Nguimbi E, Moyen R, Kobawila SC. First report of the types TEM, CTX-M, SHV and OXA-48 of beta-lactamases in Escherichia coli, from Brazzaville, Congo. Afr J Microbiol Res. 2019;13(8):158–67.
Abe IA, Koffi M, Sokouri PD, Ahouty BA, N’djetchi MK, Simaro S, et al. Assessment of drugs pressure on Escherichia coli and Klebsiella spp. uropathogens in patients attending Abobo-Avocatier Hospital, North of Abidjan (Côte d’Ivoire). African J Microbiol Res. 2019;13(29):658–66.
Breurec S, Guessennd N, Timinouni M, Le TAH, Cao V, Ngandjio A, et al. Klebsiella pneumoniae resistant to third-generation cephalosporins in five African and two Vietnamese major towns: Multiclonal population structure with two major international clonal groups, CG15 and CG258. Clin Microbiol Infect. 2013.
Guessend KN, Toty AA, Gbonon MC, Dondelinger M, Toe E, Ouattara MB, et al. CTX-M-15 extended-spectrum-Β-lactamase among clinical isolates of enterobacteriaceae in Abidjan. Côte d’Ivoire Int J Biol Res. 2017;2(3):5–8.
Guessennd N, Bremont S, Gbonon V, Kacou-NDouba A, Ekaza E, Lambert T, et al. Qnr-type quinolone resistance in extended-spectrum beta-lactamase producing enterobacteria in Abidjan, Ivory Coast. Pathol Biol. 2008.
Maataoui N, Mayet A, Duron S, Delacour H, Mentre F, Laouenan C, et al. High acquisition rate of extended-spectrum beta-lactamase-producing Enterobacteriaceae among French military personnel on mission abroad, without evidence of inter-individual transmission. Clin Microbiol Infect. 2019;25(5):631.e1-631.e9.
Moroh JLA, Fleury Y, Tia H, Bahi C, Lietard C, Coroller L, et al. Diversity and antibiotic resistance of uropathogenic bacteria from Abidjan. Afr J Urol. 2014;20(1):18–24.
Müller-Schulte E, Tuo MN, Akoua-Koffi C, Schaumburg F, Becker SL. High prevalence of ESBL-producing Klebsiella pneumoniae in clinical samples from central Côte d’Ivoire. Int J Infect Dis. 2020;91:207–9.
Irenge LM, Ambroise J, Bearzatto B, Durant JF, Chirimwami RB, Gala JL. Whole-genome sequences of multidrug-resistant Escherichia coli in South-Kivu Province, Democratic Republic of Congo: characterization of phylogenomic changes, virulence and resistance genes. BMC Infect Dis. 2019;19(1).
Irenge LM, Kabego L, Kinunu FB, Itongwa M, Mitangala PN, Gala JL, et al. Antimicrobial resistance of bacteria isolated from patients with bloodstream infections at a tertiary care hospital in the Democratic Republic of the Congo. S Afr Med J. 2015;105(9):752–5.
Irenge LM, Kabego L, Vandenberg O, Chirimwami RB, Gala JL. Antimicrobial resistance in urinary isolates from inpatients and outpatients at a tertiary care hospital in South-Kivu Province (Democratic Republic of Congo). BMC Res Notes. 2014.
Plantamura J, Bousquet A, Védy S, Larréché S, Bigaillon C, Delacour H, et al. Molecular epidemiological of extended-spectrum β-lactamase producing Escherichia coli isolated in Djibouti. J Infect Dev Ctries. 2019;13(8):753–8.
Abdallah HM, Wintermans BB, Reuland EA, Koek A, Naiemi N Al, Ammar AM, et al. Extended-spectrum β-lactamase- and carbapenemase-producing enterobacteriaceae isolated from Egyptian patients with suspected blood stream infection. PLoS ONE. 2015;10(5).
Mohamed NM, Youssef AAF. In vitro activity of tigecycline and comparators against gram-negative bacteria isolated from a tertiary hospital in Alexandria, Egypt. Microb Drug Resist. 2011;17(4):489–95.
Mohamed T, Yousef LM, Darweesh EI, Khalil AH, Meghezel EM. Detection and characterization of carbapenem resistant enterobacteriacea in Sohag University Hospitals, Egypt. J Med Microbiol. 2018;27(4):61–9.
Mohammed ESH, Fakhr AE, El Sayed HM, Al Johery SAE, Hassanein WAG. Spread of TEM, VIM, SHV, and CTX-M β -Lactamases in Imipenem-Resistant Gram-Negative Bacilli Isolated from Egyptian Hospitals. Int J Microbiol. 2016;2016.
Mohsen L, Ramy N, Saied D, Akmal D, Salama N, Abdel Haleim MM, et al. Emerging antimicrobial resistance in early and late-onset neonatal sepsis. Antimicrob Resist Infect Control. 2017;6(1).
Moore KL, Kainer MA, Badrawi N, Afifi S, Wasfy M, Bashir M, et al. Neonatal sepsis in Egypt associated with bacterial contamination of glucose-containing intravenous fluids. Pediatr Infect Dis J. 2005;24(7):590–4.
Mukhtar A, Abdelaal A, Hussein M, Dabous H, Fawzy I, Obayah G, et al. Infection complications and pattern of bacterial resistance in living-donor liver transplantation: a multicenter epidemiologic study in Egypt. Transplant Proc. 2014;46(5):1444–7.
Nazeih S, Serry F, Abbas H. Study on increased antimicrobial resistance among bacteria isolated from ICUs Zagazig University Hospitals. Zagazig J Pharm Sci. 2019;28(1):13–25.
Newire EA, Ahmed SF, House B, Valiente E, Pimentel G. Detection of new SHV-12, SHV-5 and SHV-2a variants of extended spectrum beta-lactamase in Klebsiella pneumoniae in Egypt. Ann Clin Microbiol Antimicrob. 2013. https://doi.org/10.1186/1476-0711-12-16.
Nour I, Eldegla HE, Nasef N, Shouman B, Abdel-Hady H, Shabaan AE. Risk factors and clinical outcomes for carbapenem-resistant Gram-negative late-onset sepsis in a neonatal intensive care unit. J Hosp Infect. 2017;97:52–8.
Osama R, Bakeer W, Fadel S, Amin M. Association of carbapenem and colistin resistance in pathogenic Gram negative bacteria. J Pure Appl Microbiol. 2019;13(2):733–9.
Abdelaziz MO, Bonura C, Aleo A, El-Domany RA, Fasciana T, Mammina C. OXA-163-producing Klebsiella pneumoniae in Cairo, Egypt, in 2009 and 2010. J Clin Microbiol. 2012;50(7):2489–91.
Osman KM, Kappell AD, Elhofy F, Orabi A, Mubarak AS, Dawoud TM, et al. Urinary tract infection attributed to Escherichia coli isolated from participants attending an unorganized gathering. Future Microbiol. 2018;13(7):745–56.
Östholm-Balkhed Å, Tärnberg M, Nilsson M, Nilsson LE, Hanberger H, Hällgren A. Travel-associated faecal colonization with esbl-producing enterobacteriaceae: Incidence and risk factors. J Antimicrob Chemother. 2013;68(9):2144–53.
Poirel L, Abdelaziz MO, Bernabeu S, Nordmann P. Occurrence of OXA-48 and VIM-1 carbapenemase-producing Enterobacteriaceae in Egypt. Int J Antimicrob Agents. 2013;41(1):90–1.
Principe L, Mauri C, Conte V, Pini B, Giani T, Rossolini GM, et al. First report of NDM-1-producing Klebsiella pneumoniae imported from Africa to Italy: evidence of the need for continuous surveillance. J Glob Antimicrob Resist. 2017;8:23–7.
Putnam SD, Riddle MS, Wierzba TF, Pittner BT, Elyazeed RA, El-Gendy A, et al. Antimicrobial susceptibility trends among Escherichia coli and Shigella spp. isolated from rural Egyptian paediatric populations with diarrhoea between 1995 and 2000. Clin Microbiol Infect. 2004;10(9):804–10.
Ramadan H, Gupta SK, Sharma P, Ahmed M, Hiott LM, Barrett JB, et al. Circulation of emerging NDM-5-producing Escherichia coli among humans and dogs in Egypt. Zoonoses Public Health. 2020;67(3):324–9.
Ramadan H, Rasha B, Mona IS, Lamiaa A. Random amplified DNA polymorphism of Klebsiella pneumoniae isolates from Mansoura University Hospitals, Egypt. Afr J Microbiol Res. 2015;9(9):621–30.
Rizk DE, El-Mahdy AM. Emergence of class 1 to 3 integrons among members of Enterobacteriaceae in Egypt. Microb Pathog. 2017;112:50–6.
Saied GM. Microbial pattern and antimicrobial resistance, a surgeon’s perspective: retrospective study in surgical wards and seven intensive-care units in two university hospitals in Cairo. Egypt Dermatol. 2006;212(SUPPL. 1):8–14.
Saied T, Elkholy A, Hafez SF, Basim H, Wasfy MO, El-Shoubary W, et al. Antimicrobial resistance in pathogens causing nosocomial bloodstream infections in university hospitals in Egypt. Am J Infect Control. 2011;39(9):e61–5.
Abdelaziz MO, Bonura C, Aleo A, Fasciana T, Calà C, Mammina C. Cephalosporin resistant Escherichia coli from cancer patients in Cairo. Egypt Microbiol Immunol. 2013;57(5):391–5.
Salem MM, Muharram M, Alhosiny IM. Distribution of classes 1 and 2 Integrons among Multi Drug Resistant E. coli Isolated from Hospitalized Patients with Urinary Tract Infection in Cairo, Egypt. Aust J Basic Appl Sci. 2010;4(3):398–407.
Sallam SA, Arafa MA, Razek AA, Naga M, Hamid MA. Device-related nosocomial infection in intensive care units of Alexandria University Students Hospital. East Mediterr Heal J. 2005;11(1/2):52–61.
Samah SE-K, Ghada E-SM, Amr ME-S, Dina SAE. Resistance genes to sulphonamide in commensal Escherichia coli isolated from stool of patients in Mansoura University Children Hospital. African J Microbiol Res. 2016;10(33):1363–70.
Samra MA-A, Ali NK, El-Madboly AAE. Detection of Multi-Drug Resistant Klebsiella pneumoniae in Al-Zahraa University Hospital. Egypt J Hosp Med. 2019;75(6):3006–12.
See I, Lessa FC, ElAta OA, Hafez S, Samy K, El-Kholy A, et al. Incidence and Pathogen Distribution of Healthcare-Associated Infections in Pilot Hospitals in Egypt. Infect Control Hosp Epidemiol. 2013;34(12):1281–8.
Seifert H, Blondeau J, Dowzicky MJ. In vitro activity of tigecycline and comparators (2014–2016) among key WHO ‘priority pathogens’ and longitudinal assessment (2004–2016) of antimicrobial resistance: a report from the T.E.S.T. study. Int J Antimicrob Agents. 2018;52(4):474–84.
Selim S, Aziz MA, El-Alfay S, Zakaria H. Incidence and Antibiotics Resistance of Staphylococci and Escherichia coli Isolated from Diabetic Urinary Tract Infection Patients in Egypt. J Pure Appl Microbiol. 2019;13(3):1697–702.
Shaker OA, Gomaa HE, Elmasry SA, Abdel Halim RM, Abdelrahman AH, Kamal JS. Evaluation of combined use of temocillin disk and mastdisks inhibitor combination set against polymerase chain reaction for detection of carbapenem-resistant enterobacteriaceae. Open Access Maced J Med Sci. 2018;6(2):242–7.
Shash RY, Elshimy AA, Soliman MY, Mosharafa AA. Molecular characterization of extended-spectrum β-lactamase enterobacteriaceae isolated from egyptian patients with community- and hospital-acquired urinary tract infection. Am J Trop Med Hyg. 2019;100(3):522–8.
Shehab El-Din EMR, El-Sokkary MMA, Bassiouny MR, Hassan R. Epidemiology of neonatal sepsis and implicated pathogens: A Study from Egypt. Biomed Res Int. 2015;2015.
Abdelaziz MO, Bonura C, Aleo A, Fasciana T, Mammina C. NDM-1- and OXA-163-producing Klebsiella pneumoniae isolates in Cairo, Egypt, 2012. J Glob Antimicrob Resist. 2013;1(4):213–5.
Soliman AM, Khalifa HO, Ahmed AM, Shimamoto T, Shimamoto T. Emergence of an NDM-5-producing clinical Escherichia coli isolate in Egypt. Int J Infect Dis. 2016;48:46–8.
Soliman AM, Zarad HO, Nariya H, Shimamoto T, Shimamoto T. Genetic analysis of carbapenemase-producing Gram-negative bacteria isolated from a university teaching hospital in Egypt. Infect Genet Evol. 2020;77.
Talaat M, El-Shokry M, El-Kholy J, Ismail G, Kotb S, Hafez S, et al. National surveillance of health care–associated infections in Egypt: developing a sustainable program in a resource-limited country. Am J Infect Control. 2016;44(11):1296–301.
Tohamy EY, Abo-Zeid AM, Shaheen AA, El-Awadi SF. Nosocomial Infection in Surgical Hospital in Zagazig University. J Agric Sci Ain Shams Univ. 2006;14(1):133–45.
Tohamy ST, Aboshanab KM, El-Mahallawy HA, El-Ansary MR, Afifi SS. Prevalence of multidrug-resistant Gram-negative pathogens isolated from febrile neutropenic cancer patients with bloodstream infections in Egypt and new synergistic antibiotic combinations. Infect Drug Resist. 2018;11:791–803.
Wasfi R, Elkhatib WF, Ashour HM. Molecular typing and virulence analysis of multidrug resistant Klebsiella pneumoniae clinical isolates recovered from Egyptian hospitals. Sci Rep. 2016;6.
Wassef M, Abdelhaleim M, Abdulrahman E, Ghaith D. The role of OmpK35, OmpK36 porins, and production of β-lactamases on imipenem susceptibility in Klebsiella pneumoniae clinical isolates, Cairo. Egypt Microb Drug Resist. 2015;21(6):577–80.
Wassef M, Abdelhaleim M, Ghaith D, El-Mahdy Y. Emerging New Delhi metallo-β-lactamase-1-type-producing Gram-negative bacteria isolated from Cairo University Pediatric Hospital, Cairo. Egypt J Glob Antimicrob Resist. 2016;7:84–7.
Younus H-EMA, Jiman-Fatani AAM. Spontaneous bacterial peritonitis in Egyptian and Saudi patients with liver cirrhosis. J King Abdulaziz Univ Med Sci. 2011;18(3):29–46.
Youssef MM, Rizk HA, Hassuna NA. Phenotypic and genotypic characterization of extended-spectrum β-lactamase-producing enterobacteriaceae in asymptomatic bacteriuria in pregnancy. Microb Drug Resist. 2019;25(5):731–8.
Abdel-Hady H, Hawas S, El-Daker M, El-Kady R. Extended-spectrum β-lactamase producing Klebsiella pneumoniae in neonatal intensive care unit. J Perinatol. 2008;28(10):685–90.
Yousseff AS, El Feky SAM, El-Asser SA, Allah RAMA. Microorganisms isolated from surgical wounds infection and treatment with different natural products and antibiotics. Int J Med Heal Sci. 2013;7(6):236–9.
Zafer MM, El-Mahallawy HA, Abdulhak A, Amin MA, Al-Agamy MH, Radwan HH. Emergence of colistin resistance in multidrug-resistant Klebsiella pneumoniae and Escherichia coli strains isolated from cancer patients. Ann Clin Microbiol Antimicrob. 2019;18(1):1–8. https://doi.org/10.1186/s12941-019-0339-4.
Zaki AE, Amer WH, Elezz AAA, Mohamed WM. Study of some enteropathogens causing acute diarrhea in infants and children less than 5 years old. Egypt J Med Microbiol. 2019;28(2):145–51.
Zaki MES. Extended spectrum β-lactamases among gram-negative bacteria from an Egyptian pediatric hospital: a two-year experience. J Infect Dev Ctries. 2007;1(3):269–74.
Zayed ME, Alharbi SA, Masoud IM, Ammar RA. Utilization of bacteria as virulence agents for urinary tract infectionin Egyptian patients. Biosci Biotechnol Res Asia. 2012;9(2):521–30.
Zowawi H, Thomas M, Abdelrahman S, Shabban M, Harris P, Paterson D. Molecular characterization of multidrug-resistant gram-negative bacilli in Egypt: a snapshot study. J Infect Public Health. 2019;12(1):130.
Abdelhamid SM, Abozahra, Rania R. Expression of the fluoroquinolones efflux pump genes acrA and mdfA in Urinary Escherichia coli isolates. Polish J Microbiol. 2017;66(1):25–30.
Abdelkader MM, Aboshanab KM, El-Ashry MA, Aboulwafa MM. Prevalence of MDR pathogens of bacterial meningitis in Egypt and new synergistic antibiotic combinations. PLoS ONE. 2017;12(2).
Abdel-Moaty MM, Mohamed WS, Abdel-All SM, El-Hendawy HH. Prevalence and molecular epidemiology of extended spectrum beta-lactamase producing Escherichia coli from hospital and community settings in Egypt. J Appl Pharm Sci. 2016;6(01):042–7.
Abd-Elmonsef MME, Elsharawy D, Abd-Elsalam AS. Mechanical ventilator as a major cause of infection and drug resistance in intensive care unit. Environ Sci Pollut Res. 2018;25:30787–92.
Abdelsalam MFA, Abdalla MS, El-Abhar HSED. Prospective, comparative clinical study between high-dose colistin monotherapy and colistin–meropenem combination therapy for treatment of hospital-acquired pneumonia and ventilator-associated pneumonia caused by multidrug-resistant Klebsiella pneumoniae. J Glob Antimicrob Resist. 2018;15:127–35.
Abdulall AK, Tawfick MM, El Manakhly AR, El Kholy A. Carbapenem-resistant Gram-negative bacteria associated with catheter-related bloodstream infections in three intensive care units in Egypt. Eur J Clin Microbiol Infect Dis. 2018;37(9):1647–52.
Abduo EM, El-Kholy J, Abdou S, Hafez S, Omar N, Talaat M. Incidence and Microbial Etiology of Surgical Site Infections at Select Hospitals in Egypt. Am J Infect Control. 2016;44(6):S52–3.
Abou-Dobara MI, Deyab MA, Elsawy EM, Mohamed HH. Antibiotic susceptibility and genotype patterns of Escherichia coli, Klebsiella pneumoniae and Pseudomonas aeruginosa Isolated from urinary tract infected patients. Polish J Microbiol. 2010;59(3):207–12.
Alabsi MS, Ghazal A, Sabry SA, Alasaly MM. Association of some virulence genes with antibiotic resistance among uropathogenic Escherichia coli isolated from urinary tract infection patients in Alexandria, Egypt: a hospital-based study. J Glob Antimicrob Resist. 2014;2(2):83–6.
Al-Agamy MHM, Ashour MSE-D, Wiegand I, Mohamed Al-Agamy MH, Ashour MSED, Wiegand I. First description of CTX-M beta-lactamase-producing clinical Escherichia coli isolates from Egypt. Int J Antimicrob Agents. 2006;27(27):545–8.
Ali MMM, Ahmed SF, Klena JD, Mohamed ZK, Moussa TAA, Ghenghesh KS. Enteroaggregative Escherichia coli in diarrheic children in Egypt: molecular characterization and antimicrobial susceptibility. J Infect Dev Ctries. 2014;8(5):589–96.
Aly MEA, Essam TM, Amin MA. Antibiotic resistance profile of E. coli strains isolated from clinical specimens and food samples in Egypt. Int J Microbiol Res. 2012;3(3):176–82.
Amer WH, Elsweikh SAR, Hablas NM. Comparative study between beta-lactam/beta-lactamase inhibitors as alternatives for carbapenems in the treatment of extended-spectrum beta-lactamase-producing Enterobacteriaceae. Infect Dis Clin Pract. 2019;27(3).
Amira MEG, Areej MEM, Hemat KAEL, Ramadan HI, Heba IA. Phenotypic and genotypic detection of β-lactams resistance in Klebsiella species from Egyptian hospitals revealed carbapenem resistance by OXA and NDM genes. Afr J Microbiol Res. 2016;10(10):339–47.
Ashour HM, El-Sharif A. Species distribution and antimicrobial susceptibility of gram-negative aerobic bacteria in hospitalized cancer patients. J Transl Med. 2009;19:7.
Attia H, Szubin R, Yassin AS, Monk JM, Aziz RK. Draft genome sequences of four metallo-beta-lactamase-producing multidrug-resistant Klebsiella pneumoniae clinical isolates, including two colistin-resistant strains, from Cairo, Egypt. Am Soc Mircobiol. 2019;8(7). Available from: https://doi.org/10.1128/MRA
Aziz MA, El-Kholy I, Abdo A, Selim S. Influence of multi drug resistance Gram negative bacteria in liver transplant recipient. African J Microbiol Res. 2013;7(41):4857–61.
Azzab MM, El-Sokkary RH, Tawfeek MM, Gebriel MG. Multidrug-resistant bacteria among patients with ventilator-associated pneumonia in an emergency intensive care unit, Egypt. East Mediterr Heal J. 2016;22(12).
Bassyouni RH, Gaber SN, Wegdan AA. Fecal carriage of extended-spectrum β-lactamase- and AmpC- producing Escherichia coli among healthcare workers. J Infect Dev Ctries. 2015;9(3):304–8.
Bathoorn E, Friedrich AW, Zhou K, Arends JP, Borst DM, Grundmann H, et al. Latent introduction to the Netherlands of multiple antibiotic resistance including NDM-1 after hospitalisation in Egypt, August 2013. Eurosurveillance. 2013;18(42).
EL Bedewy RMS. Multi drug resistant bacteria and its antibiotic susceptibility at percutanous endoscopic gastrostomy (PEG) tube site of long term care facility elderly residents. Egypt J Hosp Med. 2017;68(2):1094–100.
Behiry IK, Abada EA, Ahmed EA, Labeeb RS. Enteropathogenic Escherichia coli associated with diarrhea in children in Cairo. Egypt Sci World J. 2011;11:2613–9.
Biedenbach D, Bouchillon S, Hackel M, Hoban D, Kazmierczak K, Hawser S, et al. Dissemination of NDM metallo-beta-lactamase genes among clinical isolates of Enterobacteriaceae collected during the SMART global surveillance study from 2008 to 2012. Antimicrob Agents Chemother. 2015;59(59):826–30.
Eida M, Nasser M, El-Maraghy N, Azab K. Pattern of hospital-acquired pneumonia in Intensive Care Unit of Suez Canal University Hospital. Egypt J Chest Dis Tuberc. 2015;64(3):625–31.
El Awady BA, Anan MG, Gohar HA, Saleh MH. Detection of carbapenemase-producing enterobacteriaceae using chromogenic medium, ChromidID OXA-48, in critical care patients of kasr Al-Ainy hospital in Egypt. J Pure Appl Microbiol. 2017;11(4):1655–64.
El Kholy A, Baseem H, Hall GS, Procop GW, Longworth DL. Antimicrobial resistance in Cairo, Egypt 1999–2000: a survey of five hospitals. J Antimicrob Chemother. 2003;51(3):625–30.
El Metwally HAR, Ibrahim HAH, El-Athamna MN, Amer MA, El MHAR, Ibrahim HAH, et al. Multiplex PCR for detection of diarrheagenic Escherichia coli in Egyptian children. J Med Sci. 2007;7(2):255–62.
Elawady B, Ghobashy M, Balbaa A. Rapidec carba NP for detection of carbapenemase-producing enterobacteriaceae in clinical isolates: a cross-sectional study. Surg Infect (Larchmt). 2019;20(8):672–6.
El-Badawy MF, Tawakol WM, El-Far SW, Maghrabi IA, Al-Ghamdi SA, Mansy MS, et al. Molecular identification of aminoglycoside-modifying enzymes and plasmid-mediated quinolone resistance genes among Klebsiella pneumoniae clinical isolates recovered from Egyptian patients. Int J Microbiol. 2017;2017.
El-Badawy MF, Tawakol WM, Maghrabi IA, Mansy MS, Shohayeb MM, Ashour MS. Iodometric and Molecular Detection of ESBL Production among Clinical Isolates of E. coli Fingerprinted by ERIC-PCR: The First Egyptian Report Declares the Emergence of E. coli O25b-ST131clone Harboring blaGES. Microb Drug Resist. 2017;23(6):703–17.
El-Din R, Elbaset A, Naim A. Epidemiology, Phenotyping and Antimicrobial Susceptibility Profile of Enterohaemrrhagic Escherichia coli Strains Isolated from Cases of Diarrhea. Br Microbiol Res J. 2015;8(4):546–53.
El-Din RAE-HA, El-Sanosy MG. Phenotypic Study on Some Virulence Factors and Molecular Screening of Aminoglycoside Resistance among Klebsiella pneumoniae Strains Isolated from Urinary Tract Infections in Pediatric Cases in Egypt. Microbiol Res J Int. 2018;26(2):1–11.
Elgendy SG, Abdel Hameed MR, El-Mokhtar MA. Tigecycline resistance among Klebsiella pneumoniae isolated from febrile neutropenic patients. J Med Microbiol. 2018;67(7):972–5.
El-Kazzaz SS, El-khier NTA. AmpC and metallo beta-lactamases producing Gram negative bacteria in patients with hematological malignancy. Afr J Microbiol Res. 2015;9(18):1247–54.
El-latif RSA, Elbadawy NE, El-Hady HA. Checkboard antimicrobial susceptibility testing of multidrug resistant Klebsiella pneumoniae isolated from patients with ventilator associated pneumonia. Egypt J Med Microbiol. 2012;21(4):89–98.
ElMahallawy HA, Zafer MM, Amin MA, Ragab MM, Al-Agamy MH. Spread of carbapenem resistant Enterobacteriaceae at tertiary care cancer hospital in Egypt. Infect Dis (Auckl). 2018;50(7):560–4.
El-Mahdy R, El-Kannishy G, Salama H. Hypervirulent Klebsiella pneumoniae as a hospital-acquired pathogen in the intensive care unit in Mansoura, Egypt. GERMS [Internet]. 2018;8(3):140–6. Available from: www.germs.ro
El-Masry EA, Melake NA, Taher IA. Phenotypic and Molecular Characterization of Extended-Spectrum P-Lactamase Producing Klebsiella spp. from Nosocomial Infections in Egypt. Int Med J. 2019;26(5):376–80.
El-Moghazy A-N, Tawfick MM, El-Habibi MM. Prevalence, antimicrobial susceptibilities and molecular characterization of enteric bacterial pathogens isolated from patients with infectious diarrhoea in Cairo. Int J Curr Microbiol Appl Sci. 2016;5(4):553–64.
Elnahriry SS, Khalifa HO, Soliman AM, Ahmed AM, Hussein AM, Shimamoto T, et al. Emergence of plasmid-mediated colistin resistance gene mcr-1 in a clinical Escherichia coli isolate from Egypt. Antimicrob Agents Chemother. 2016;60(5):3249–50.
Elraghy NA, Zahran WA, Makled AF, El-Sebaey HM, El-Hendawy GR, Melake NA, et al. Enterobacteriaceae nosocomial uropathogens at Menoufia University Hospitals: phenotypic characterization and detection of resistance genes using real-time PCR. Menoufia Med J. 2016;29(4):855–61.
El-Sahrigy SAF, Shouman MG, Ibrahim HM, Rahman AMOA, Habib SA, Khattab AA, et al. Prevalence and anti-microbial susceptibility of hospital acquired infections in two pediatric intensive care units in Egypt. Open Access Maced J Med Sci. 2019;7(11):1744–9.
Elsherif RH, Ismail DK, El-Kholy YS, Gohar NM, Elnagdy SM, Elkraly OA. Integron-mediated multidrug resistance in extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae isolated from fecal specimens in Egypt. J Egypt Public Health Assoc. 2016;91(2):73–9.
El-Sweify MA, Gomaa NI, El-Maraghy NN, Mohamed HA. Phenotypic detection of carbapenem resistance among Klebsiella pneumoniae in Suez Canal University Hospitals, Ismailiya, Egypt. Int J Curr Microbiol Appl Sci. 2015;4(2):10–8.
Elzayat MAA, Barnett-Vanes A, Dabour MFE, Cheng F, Abdel-Aziz Elzayat M, Barnett-Vanes A, et al. Prevalence of undiagnosed asymptomatic bacteriuria and associated risk factors during pregnancy: a cross-sectional study at two tertiary centres in Cairo, Egypt. BMJ Open [Internet]. 2017;7. Available from: http://bmjopen.bmj.com/
Esmat MM, Saif A, Islam A. Diabetic foot infection: bacteriological causes and antimicrobial therapy. J Am Sci. 2012;8(10):389–93.
Fahmey SS. Early-onset sepsis in a neonatal intensive care unit in Beni Suef, Egypt: bacterial isolates and antibiotic resistance pattern. Korean J Pediatr. 2013;56(8):332–7.
Fam N, Leflon-Guibout V, Fouad S, Aboul-Fadl L, Marcon E, Desouky D, et al. CTX-M-15-producing Escherichia coli clinical isolates in Cairo (Egypt), including isolates of clonal complex ST10 and clones ST131, ST73, and ST405 in both community and hospital settings. Microb Drug Resist. 2011;17(1):67–73.
Fattouh M, Nasr El-Din A, Abdelgalil W. Bacteriologic and immunologic profile of blood stream infected patients in intensive care unit of Sohag University Hospital, Egypt. Int J Curr Microbiol Appl Sci. 2014;3(8):265–81.
Fouda R, Soliman MS, ElAnany MG, Abadeer M, Soliman G. Prevalence and risk factors of MRSA, ESBL and MDR bacterial colonization upon admission to an Egyptian medical ICU. J Infect Dev Ctries. 2016;10(4):329–36.
Gamal D, Fernández-Martínez M, El-Defrawy I, Ocampo-Sosa AA, Martínez-Martínez L. First identification of NDM-5 associated with OXA-181 in Escherichia coli from Egypt. Emerg Microbes Infect. 2016;5.
Gamal D, Fernández-Martínez M, Salem D, El-Defrawy I, Montes LÁ, Ocampo-Sosa AA, et al. Carbapenem-resistant Klebsiella pneumoniae isolates from Egypt containing blaNDM-1 on IncR plasmids and its association with rmtF. Int J Infect Dis. 2016;43:17–20.
Gawad WE, Helmy OM, Tawakkol WM, Hashem AM. Antimicrobial resistance, biofilm formation, and phylogenetic grouping of uropathogenic Escherichia coli isolates in Egypt: the role of efflux pump-mediated resistance. Jundishapur J Microbiol. 2018;11(2).
Ghaith DM, Mohamed ZK, Farahat MG, Aboulkasem Shahin W, Mohamed HO. Colonization of intestinal microbiota with carbapenemase-producing Enterobacteriaceae in paediatric intensive care units in Cairo. Egypt Arab J Gastroenterol. 2019;20(1):19–22.
Ghaith DM, Zafer MM, Said HM, Elanwary S, Elsaban S, Al-Agamy MH, et al. Genetic diversity of carbapenem-resistant Klebsiella pneumoniae causing neonatal sepsis in intensive care unit, Cairo. Egypt Eur J Clin Microbiol Infect Dis. 2020;39(3):583–91.
Aamir MM, Abu El-Wafa WM, Ali AE, Hamouda, Hayam M, Mourad FE. Prevalence of Multidrug Resistant Bacteria Causing Late-Onset Neonatal Sepsis. Int J Curr Microbiol Appl Sci. 2015;4(5):172–90
Grisold AJ, Hoenigl M, Ovcina I, Valentin T, Fruhwald S. Ventilator-associated pneumonia caused by OXA-48-producing Escherichia coli complicated by ciprofloxacin-associated rhabdomyolysis. J Infect Chemother. 2013;19(6):1214–7.
Hasanin A, Eladawy A, Mohamed H, Salah Y, Lotfy A, Mostafa H, et al. Prevalence of extensively drug-resistant gram negative bacilli in surgical intensive care in Egypt. Pan Afr Med J. 2014;19.
Hashem AA, Taha SA, Anani MM. Antibiotic Susceptibility Pattern and Biofilm Production of Multidrug-Resistant Organisms (MDROs) Isolated from Suez-Canal University Hospitals. Egypt J Med. 2018;27(4):113–21.
Hassan A, Mohamed S, Mohamed M, El-Mokhtar M. Acute exacerbations of chronic obstructive pulmonary disease: etiological bacterial pathogens and antibiotic resistance in Upper Egypt. Egypt J Bronchol. 2016;10(3):283–90.
Hassan EA, Elsherbiny NM, Abd El-Rehim AS, Soliman AMA, Ahmed AO. Health care-associated infections in pre-transplant liver intensive care unit: Perspectives and challenges. J Infect Public Health. 2018;11(3):398–404.
Hassan MA, Tamer TM, Rageh AA, Abou-Zeid AM, Abd El-Zaher EHF, Kenawy ER. Insight into multidrug-resistant microorganisms from microbial infected diabetic foot ulcers. Diabetes Metab Syndr Clin Res Rev. 2019;13(2):1261–70.
Hawser SP, Badal RE, Bouchillon SK, Hoban DJ, Biedenbach DJ, Cantón R, et al. Monitoring the global in vitro activity of ertapenem against Escherichia coli from intra-abdominal infections: SMART 2002–2010. Int J Antimicrob Agents. 2013;41(3):224–8.
Hefzy EM, Hassuna NA. Fluoroquinolone-resistant sequence type 131 subgroups O25b and O16 among extraintestinal Escherichia coli Isolates from community-acquired urinary tract infections. Microb Drug Resist. 2017;23(2):224–9.
Helal SF, El-Rachidi NGE, AbdulRahman EM, Hassan DMA. The presence of blaKPC-mediated resistance in Enterobacteriaceae in Cairo University hospitals in Egypt and its correlation with in vitro carbapenem susceptibility. J Chemother. 2014;26(2):125–8.
Henderson J, Ciesielczuk H, Nelson SM, Wilks M. Community prevalence of carbapenemase-producing organisms in East London. J Hosp Infect. 2019;103(2):142–6.
Abbas HA, Kadry AA, Shaker GH, Goda RM. Impact of specific inhibitors on metallo-β-carbapenemases detected in Escherichia coli and Klebsiella pneumoniae isolates. Microb Pathog. 2019;132:266–74.
Iman FEG, Marwa AM, Doaa AY. Phenotypic and genotypic methods for detection of metallo beta lactamases among carbapenem resistant Enterobacteriaceae clinical isolates in Alexandria Main University Hospital. Afr J Microbiol Res. 2016;10(1):32–40.
Kamel NA, Abouelwafa MM, El-tayeb WN, Aboshanab KM. Antibacterial resistance pattern of aerobic bacteria isolated from patients with diabetic foot ulcers in Egypt. Afr J Microbiol Res. 2014;8(31):2947–54.
Kamel NA, El-tayeb WN, El-Ansary MR, Mansour MT, Aboshanab KM. Phenotypic screening and molecular characterization of carbapenemase-producing Gram-negative bacilli recovered from febrile neutropenic pediatric cancer patients in Egypt. PLoS ONE. 2018;13(8).
Khalaf NG, Eletreby MM, Hanson ND. Characterization of CTX-M ESBLs in Enterobacter cloacae, Escherichia coli and Klebsiella pneumoniae clinical isolates from Cairo, Egypt. BMC Infect Dis. 2009;9.
Khalifa HO, Soliman AM, Ahmed AM, Shimamoto T, Hara T, Ikeda M, et al. High carbapenem resistance in clinical gram-negative pathogens isolated in Egypt. Microb Drug Resist. 2017;23(7):838–44.
Khalil MAF, Elgaml A, El-Mowafy M. Emergence of multidrug-resistant New Delhi metallo-β-lactamase-1-producing Klebsiella pneumoniae in Egypt. Microb Drug Resist. 2017;23(4):480–7.
Khalil MAF, Hager R, Abd-El Reheem F, Mahmoud EE, Samir T, Moawad SS, et al. A study of the virulence traits of carbapenem-resistant Klebsiella pneumoniae Isolates in a Galleria mellonella model. Microb Drug Resist. 2019;25(7):1063–71. https://doi.org/10.1089/mdr.2018.0270.
Labib JR, Ibrahim SK, Salem MR, Youssef MRL, Meligy B. Infection with gram-negative bacteria among children in a tertiary pediatric hospital in Egypt. Am J Infect Control. 2018;46(7):798–801.
Lashin GMA, Tohamy EY, Askora AA, Mahmoud FE-Z. Use of probiotic acid bacteria for the control of multidrug resistant bacteria isolated from clinical infections. Bull Fac Sci Zagazig Univ. 2017;39:61–81.
Lob SH, Hoban DJ, Young K, Motyl MR, Sahm DF. Activity of imipenem/relebactam against Gram-negative bacilli from global ICU and non-ICU wards: SMART 2015–2016. J Glob Antimicrob Resist. 2018;15:12–9.
Abdallah HM, Alnaiemi N, Reuland EA, Wintermans BB, Koek A, Abdelwahab AM, et al. Fecal carriage of extended-spectrum β-lactamase- and carbapenemase-producing Enterobacteriaceae in Egyptian patients with community-onset gastrointestinal complaints: a hospital-based cross-sectional study. Antimicrob Resist Infect Control. 2017. https://doi.org/10.1186/s13756-017-0219-7.
Mahdi WKM, Abd H, Ahmed A, Abo M, Euoon E, Mohamed MH. Extended Spectrum-lactamase producing Klebsiella pneumoniae in Neonatal Units of Minya Governorate. Int J Curr Microbiol App Sci. 2014;3(12):787–800.
Malek MM, Amer FA, Allam AA, El-Sokkary RH, Gheith T, Arafa MA. Occurrence of classes I and II integrons in Enterobacteriaceae collected from Zagazig University Hospitals, Egypt. Front Microbiol. 2015;6.
Metwally L, Gomaa N, Attallah M, Kamel N. High prevalence of Klebsiella pneumoniae carbapenemase-mediated resistance in K. pneumoniae isolates from Egypt. East Mediterr Heal J. 2013;19(11):947–52.
Mohamad EA, El Shalakany AH. Detection of biofilm formation in uropathogenic bacteria. Egypt J Med Microbiol. 2015;24(1):49–458.
Mohamed DS, Ahmed EF, Mahmoud AM, El-Baky RMA, John J. Isolation and evaluation of cocktail phages for the control of multidrug-resistant Escherichia coli serotype O104: H4 and E. coli O157: H7 isolates causing diarrhea. FEMS Microbiol Lett. 2018;365(2).
Mohamed ER, Ali MY, Waly NGFM, Halby HM, El-baky RMA. The inc FII plasmid and its contribution in the transmission of blaNDM-1 and blaKPC-2 in Klebsiella pneumoniae in Egypt. Antibiotics. 2019;8(4):1–12.
Mohamed ER, Aly SA, Halby HM, Ahmed SH, Zakaria AM, El-Asheer OM. Epidemiological typing of multidrug-resistant Klebsiella pneumoniae, which causes paediatric ventilator-associated pneumonia in Egypt. J Med Microbiol. 2017;66(5):628–34.
Al-Agamy MH. Genetic basis of cefotaxime resistant isolates of Klebsiella pneumoniae from Cairo. Afr J Microbiol Res. 2012. https://doi.org/10.5897/AJMRX11.022.
Mohamed M, El-Mokhtar M, Hassan A. Bacterial profile and antibiotic susceptibility patterns of acute exacerbation of chronic obstructive pulmonary disease in Assiut University Hospitals, upper Egypt; a one-year prospective study. Br Microbiol Res J. 2015;7(6):288–305.
Mohamed MAES, Eman SA. Antibacterial resistance pattern among Escherichia coli strains isolated from Mansoura hospitals in Egypt with a special reference to quinolones. Afr J Microbiol Res. 2015;9(9):662–70.
Shatalov A. Prevalence and antibiotic resistance pattern of Escherichia coli and Klebsiella pneumoniae in Urine Tract Infections at the La Paz Medical Center, Malabo, Equatorial Guinea. Open J Med Microbiol. 2015;5:177–83.
Ehlkes L, Pfeifer Y, Werner G, Ignatius R, Vogt M, Eckmanns T, et al. No evidence of carbapenemase-producing Enterobacteriaceae in stool samples of 1,544 asylum seekers arriving in Rhineland-Palatinate, Germany, April 2016 to March, 2017. Eurosurveillance. 2019;24(8).
Gashaw M, Berhane M, Bekele S, Kibru G, Teshager L, Yilma Y, et al. Emergence of high drug resistant bacterial isolates from patients with health care associated infections at Jimma University medical center: A cross sectional study. Antimicrob Resist Infect Control. 2018;7(1).
Gebre-Sealssie S. Antimicrobial resistance patterns of clinical bacterial isolates in Southwestern Ethiopia. Ethiop Med J. 2007;45(4):363–70.
Gizachew Z, Kassa T, Beyene G, Howe R, Yeshitila B. Multi-drug resistant bacteria and associated factors among reproductive age women with significant bacteriuria. Ethiop Med J. 2019;1:31–43.
Kalayu AA, Diriba K, Girma C, Abdella E. Incidence and Bacterial etiologies of surgical site infections in a public hospital, Addis Ababa, Ethiopia. Open Microbiol J. 2020;13(1):301–7.
Legese MH, Weldearegay GM, Asrat D. Extended-spectrum beta-lactamase- and carbapenemase-producing Enterobacteriaceae among Ethiopian children. Infect Drug Resist. 2017;10:27–34.
Moges F, Eshetie S, Abebe W, Mekonnen F, Dagnew M, Endale A, et al. High prevalence of extended-spectrum beta-lactamase-producing Gram-negative pathogens from patients attending Felege Hiwot Comprehensive Specialized Hospital, Bahir Dar, Amhara region. PLoS ONE. 2019;14(4).
Moges F, Mengistu G, Genetu A. Multiple drug resistance in urinary pathogens at Gondar College of Medical Sciences Hospital, Ethiopia. East Afr Med J. 2002;8(415–419):415–9.
Saba MG. Magnitude of Extended-spectrum Beta-lactamase, AmpC Beta-lactamase and Carbapenemase producing gram negative bacilli isolated from clinical specimens at International Clinical Laboratories, Addis Ababa, Ethiopia. [Addis Ababa, Ethiopia]: Addis Ababa University; 2018.
Teklu DS, Negeri AA, Legese MH, Bedada TL, Woldemariam HK, Tullu KD. Extended-spectrum beta-lactamase production and multi-drug resistance among Enterobacteriaceae isolated in Addis Ababa, Ethiopia. Antimicrob Resist Infect Control. 2019;8(1).
Ten Hove RJ, Tesfaye M, ten Hove WF, Nigussie M. Profiling of antibiotic resistance of bacterial species recovered from routine clinical isolates in Ethiopia. Ann Clin Microbiol Antimicrob. 2017;
Abayneh M, Tesfaw G, Abdissa A. Isolation of Extended-Spectrum beta-lactamase-(ESBL-) Producing Escherichia coli and Klebsiella pneumoniae from Patients with Community-Onset Urinary Tract Infections in Jimma University Specialized Hospital, Southwest Ethiopia. Can J Infect Dis Med Microbiol. 2018;2018.
Tuem KB, Desta R, Bitew H, Ibrahim S, Hishe HZ. Antimicrobial resistance patterns of uropathogens isolated between 2012 and 2017 from a tertiary hospital in Northern Ethiopia. J Glob Antimicrob Resist. 2019;18:109–14.
Tufa TB, Andre F, Abdissa S, Achim K, Colin M, Klaus P, et al. Resistance to third generation cephalosporin due to tem and CTX-M-1 type extended-spectrum beta-lactamase genes among clinical isolates of gram-negative bacilli in Asella, Central Ethiopia. Antimicrob Resist Infect Control. 2019;8((Suppl 1)P51):40–1.
Zeynudin A, Pritsch M, Schubert S, Messerer M, Liegl G, Hoelscher M, et al. Prevalence and antibiotic susceptibility pattern of CTX-M type extended-spectrum β-lactamases among clinical isolates of gram-negative bacilli in Jimma, Ethiopia. BMC Infect Dis. 2018;18(1).
Alemayehu T, Ali M, Mitiku E, Hailemariam M. The burden of antimicrobial resistance at tertiary care hospital, southern Ethiopia: A three years’ retrospective study. BMC Infect Dis. 2019;19(1).
Alemu M. Extended Spectrum Beta-lactamase producing E. coli and K. pneumoniae carriage among under five years children in Addis Raey public health center, Addis Ababa, Ethiopia. [Addis Ababa, Ethiopia]: Addis Ababa University; 2018.
Beyene D, Bitew A, Fantew S, Mihret A, Evans M. Multidrug-resistant profile and prevalence of extended spectrum β-lactamase and carbapenemase production in fermentative Gram-negative bacilli recovered from patients and specimens referred to National Reference Laboratory, Addis Ababa, Ethiopia. PLoS One. 2019;14(9).
Dadi BR, Abebe T, Zhang L, Mihret A, Abebe W, Amogne W. Drug resistance and plasmid profile of uropathogenic Escherichia coli among urinary tract infection patients in Addis Abeba. J Infect Dev Ctries. 2018;12(8):608–15.
Desta K, Woldeamanuel Y, Azazh A, Mohammod H, Desalegn D, Shimelis D, et al. High gastrointestinal colonization rate with extended-spectrum β-lactamase-producing Enterobacteriaceae in hospitalized patients: Emergence of carbapenemase-producing K. pneumoniae in Ethiopia. PLoS ONE. 2016;11(8).
Eshetie S, Unakal C, Gelaw A, Ayelign B, Endris M, Moges F. Multidrug resistant and carbapenemase producing Enterobacteriaceae among patients with urinary tract infection at referral Hospital, Northwest Ethiopia. Antimicrob Resist Infect Control. 2015;4(1).
Eshetu B, Gashaw M, Berhane M, Abdissa A, McClure EM, Goldenberg RL, et al. Intravenous fluid contaminated with Klebsiella oxytoca as a source of sepsis in a preterm newborn: case report. Am J Infect Control. 2019;47(7):840–2.
Rerambiah LK, Ndong J-C, Massoua PMM, Medzegue S, Elisee-Ndam M, Mintsa-Ndong A, et al. Antimicrobial profiles of bacterial clinical isolates from the Gabonese National Laboratory of Public Health: data from routine activity. Int J Infect Dis. 2014;29:48–53.
Moussounda M, Diene SM, Dos Santos S, Goudeau A, François P, Mee-Marquet N van der A. Emergence of bla NDM-7 producing enterobacteriaceae in Gabon 2016. Emerg Infect Dis. 2017;23(2):2–4.
Presterl E, Zwick RH, Reichmann S, Aichelburg A, Winkler S, Kremsner PG, et al. Frequency and virulence properties of diarrheagenic Escherichia coli in children with diarrhea in Gabon. Am J Trop Med Hyg. 2003;69(4):406–10.
Rogombe SM, Jean K, Mimbila M, Kamgaing EK, M’ella RM, Pambou RKM ep. N, et al. The epidemiological aspects and evolution of nosocomial infection in Hospital, neonatology unit of Angondje Teaching. Neonatal Pediatr Med. 2018;4(2).
Schaumburg F, Alabi A, Kokou C, Grobusch MP, Köck R, Kaba H, et al. High burden of extended-spectrum β-lactamase-producing enterobacteriaceae in Gabon. J Antimicrob Chemother. 2013;68(9):2140–3.
Sanneh B, Kebbeh A, Jallow HS, Camara Y, Mwamakamba LW, Ceesay IF, et al. Prevalence and risk factors for faecal carriage of Extended Spectrum Î2-lactamase producing Enterobacteriaceae among food handlers in lower basic schools in West Coast Region of The Gambia. PLoS One. 2018;13(8).
Agyekum A, Fajardo-Lubián A, Ansong D, Partridge SR, Agbenyega T, Iredell JR. blaCTX-M-15 carried by IncF-type plasmids is the dominant ESBL gene in Escherichia coli and Klebsiella pneumoniae at a hospital in Ghana. Diagn Microbiol Infect Dis. 2016;
Labi AK, Obeng-Nkrumah N, Bjerrum S, Enweronu-Laryea C, Newman MJ. Neonatal bloodstream infections in a Ghanaian Tertiary Hospital: Are the current antibiotic recommendations adequate? BMC Infect Dis. 2016;16(1).
Mohammed J, Hounmanou YMG, Thomsen LE. Antimicrobial resistance among clinically relevant bacterial isolates in Accra: a retrospective study. BMC Res Notes. 2018;11(1):254.
Obeng-Nkrumah N, Labi AK, Addison NO, Labi JEM, Awuah-Mensah G. Trends in paediatric and adult bloodstream infections at a Ghanaian referral hospital: a retrospective study. Ann Clin Microbiol Antimicrob. 2016.
Obeng-Nkrumah N, Twum-Danso K, Krogfelt KA, Newman MJ. High levels of extended-spectrum beta-lactamases in a major teaching hospital in Ghana: The need for regular monitoring and evaluation of antibiotic resistance. Am J Trop Med Hyg. 2013;
Opintan JA, Newman MJ. Prevalence of antimicrobial resistant pathogens from blood cultures: results from a laboratory based nationwide surveillance in Ghana. Antimicrob Resist Infect Control. 2017;6(1).
Quansah E, Barnie PA, Acheampong DO, Obiri-Yeboah D, Mills RO, Asmah E, et al. Geographical distribution of β-lactam resistance among Klebsiella spp. From selected health facilities in Ghana. Trop Med Infect Dis. 2019;4(3).
Agyepong N, Govinden U, Owusu-Ofori A, Essack SY. Multidrug-resistant gram-negative bacterial infections in a teaching hospital in Ghana. Antimicrob Resist Infect Control. 2018;7(1).
Amankwa R, Tay SC, Agbenorku P, Frimpong E, Gyampomah TK, Osei Sampene PP. Bacteriological profile of burn wound isolates in a burns center of a tertiary hospital. J Acute Dis. 2017;6(4):181–6.
Ayibieke A, Sato W, Mahazu S, Prah I, Addow-Thompson J, Ohashi M, et al. Molecular characterisation of the NDM-1encoding plasmid p2189-NDM in an Escherichia coli ST410 clinical isolate from Ghana. PLoS ONE. 2018;13(12).
Bourafa N, Chaalal W, Bakour S, Lalaoui R, Boutefnouchet N, Diene SM, et al. Molecular characterization of carbapenem-resistant Gram-negative bacilli clinical isolates in Algeria. Infect Drug Resist. 2018;11:735–42.
Codjoe FS, Donkor ES, Smith TJ, Miller K. Phenotypic and genotypic characterization of carbapenem-resistant gram-negative bacilli pathogens from hospitals in Ghana. Microb Drug Resist. 2019;25(10):1449–57.
Eibach D, Campos CB, Krumkamp R, Al-Emran HM, Dekker D, Boahen KG, et al. Extended spectrum beta-lactamase producing Enterobacteriaceae causing bloodstream infections in rural Ghana, 2007–2012. Int J Med Microbiol. 2016.
Janssen H, Janssen I, Cooper P, Kainyah C, Pellio T, Quintel M, et al. Antimicrobial-resistant bacteria in infected wounds, Ghana, 2014. Emerg Infect Dis. 2018;24(5):916–9.
Christian KG-S, Bernard N, Edwin MTY, Arhin AA, Ken A, Roland A, et al. Resistance pattern of uropathogenic bacteria in males with lower urinary tract obstruction in Kumasi, Ghana. Afr J Microbiol Res. 2014;
Isendahl J, Turlej-Rogacka A, Manjuba C, Rodrigues A, Giske CG, Nauclér P. Fecal carriage of ESBL-producing E. coli and K. pneumoniae in Children in Guinea-Bissau: a hospital-based cross-sectional study. PLoS ONE. 2012.
Kagia N, Kosgei P, Ooko M, Wafula L, Mturi N, Anampiu K, et al. Carriage and acquisition of extended-spectrum β-lactamase-producing Enterobacterales among Neonates Admitted to Hospital in Kilifi, Kenya. Clin Infect Dis. 2019;69(5):751–9.
Kariuki S, Corkill JE, Revathi G, Musoke R, Hart CA. Molecular characterization of a novel plasmid-encoded cefotaximase (CTX-M-12) found in clinical Klebsiella pneumoniae isolates from Kenya. Antimicrob Agents Chemother. 2001;45(7):2141–3.
Kariuki S, Revathi G, Corkill J, Kiiru J, Mwituria J, Mirza N, et al. Escherichia coli from community-acquired urinary tract infections resistant to fluoroquinolones and extended-spectrum beta-lactams. J Infect Dev Ctries. 2007;1(3):257–62.
Kassim A, Omuse G, Premji Z, Revathi G. Comparison of Clinical Laboratory Standards Institute and European Committee on Antimicrobial Susceptibility Testing guidelines for the interpretation of antibiotic susceptibility at a University teaching hospital in Nairobi, Kenya: A cross-sectional stud. Ann Clin Microbiol Antimicrob. 2016;
Kiiru J, Kariuki S, Godderis BM, Butaye P. Analysis of β-lactamase phenotypes and carriage of selected β-lactamase genes among Escherichia coli strains obtained from Kenyan patients during an 18-year period. BMC Microbiol. 2012;
Kiiru J, Kariuki S, Goddeeris BM, Revathi G, Maina TW, Ndegwa DW, et al. Escherichia coli strains from Kenyan patients carrying conjugatively transferable broad-spectrum β-lactamase, qnr, aac(6’)-ib-cr and 16s rRNA methyltransferase genes. J Antimicrob Chemother. 2011;66(7):1639–42.
Kohli R, Omuse G, Revathi G. Antibacterial susceptibility patterns of blood stream isolates in patients investigated at the Aga Khan university Hospital, Nairobi. East Afr Med J. 2010;
Maina D, Omuse G, Revathi G, Adam RD. Spectrum of microbial diseases and resistance patterns at a private teaching hospital in Kenya: Implications for clinical practice. PLoS One. 2016;
Ndung’u C, Muigai AWT, Kenyatta J, Kariuki S. Prevalence and antibiotic resistance patterns of Escherichia coli among hospitalised patents at Thika District Hospital. East Afr Med J. 2014;91(6):185–90.
Nibogora C, Nyerere AK, Nguigi CW, Makau P. Phenotypic and Genotypic Characterization of Antibiotics Resistance Klebsiella pneumoniae Isolated from Clinical Samples at The Nairobi Hospital, Kenya. J Biol Agric Healthc. 2018;8(19–29).
Njagi LN, Odera S, Mutua F. Antimicrobial susceptibility patterns of urinary bacteria amongst paediatric patients at the Nairobi Hospital, Kenya. East Afr Med J. 2015;92(3).
Oneko M, Kariuki S, Muturi-Kioi V, Otieno K, Otieno VO, Williamson JM, et al. Emergence of community-acquired, multidrug-resistant invasive nontyphoidal Salmonella disease in Rural Western Kenya, 2009–2013. Clin Infect Dis. 2015;61:S310–6.
Poirel L, Revathi G, Bernabeu S, Nordmann P. Detection of NDM-1-producing Klebsiella pneumoniae in Kenya. Antimicrob Agents Chemother. 2011;
Shah M, Kathiiko C, Wada A, Odoyo E, Bundi M, Miringu G, et al. Prevalence, seasonal variation, and antibiotic resistance pattern of enteric bacterial pathogens among hospitalized diarrheic children in suburban regions of central Kenya. Trop Med Health. 2016;
Swierczewski BE, Odundo EA, Koech MC, Ndonye JN, Kirera RK, Kirera CP, et al. Surveillance for enteric pathogens in a case-control study of acute diarrhea in Western Kenya. Trans R Soc Trop Med Hyg. 2013;
Taitt CR, Leski TA, Erwin DP, Odundo EA, Kipkemoi NC, Ndonye JN, et al. Antimicrobial resistance of Klebsiella pneumoniae stool isolates circulating in Kenya. PLoS One. 2017;12(6).
Tornberg-Belanger SN, Rwigi D, Brander RL, Tickell KD, McGrath CJ, Muraya M, et al. Prevalence of antimicrobial resistance in commensal E. coli from children dischrarged from hospital in western Kenya. Am Soc Trop Med Hyg. 2019;101(S5):553.
Wangai FK, Masika MM, Lule GN, Karari EM, Maritim MC, Jaoko WG, et al. Bridging antimicrobial resistance knowledge gaps: The East African perspective on a global problem. PLoS One. 2019;14(2).
Aduda DSO, Macharia IM, Mugwe P, Oburra H, Farragher B, Brabin B, et al. Bacteriology of chronic suppurative otitis media (CSOM) in children in Garissa district, Kenya: A point prevalence study. Int J Pediatr Otorhinolaryngol. 2013;77(7):1107–11.
Apondi OE, Oduor OC, Gye BK, Kipkoech MK. High prevalence of multi-drug resistant Klebsiella pneumoniae in a tertiary teaching hospital in Western Kenya. African J Infect Dis. 2016;
Ayoyi AO, Kikuvi G, Bii C, Kariuki S. Prevalence, aetiology and antibiotic sensitivity profile of asymptomatic bacteriuria isolates from pregnant women in selected antenatal clinic from Nairobi, Kenya. Pan Afr Med J. 2017;26.
Carattoli A, Villa L, Poirel L, Bonnin RA, Nordmann P. Evolution of IncA/C blaCMY-2-carrying plasmids by acquisition of the blaNDM-1 carbapenemase gene. Antimicrob Agents Chemother. 2012;56(2):783–6.
Henson SP, Boinett CJ, Ellington MJ, Kagia N, Mwarumba S, Nyongesa S, et al. Molecular epidemiology of Klebsiella pneumoniae invasive infections over a decade at Kilifi County Hospital in Kenya. Int J Med Microbiol. 2017;307(7):422–9.
Juma A, Caroline N. Antimicrobial susceptibility profiles and prevalence of ESBLs among E. coli isolates recovered from people working in hospitality industry within Nairobi, Kenya. East Afr Med J [Internet]. 2017;94(6):445–58. Available from: https://www.researchgate.net/publication/328334021
Frickmann H, Köller T, Hagen RM, Ebert K-P, Müller M, Wenzel W, et al. Molecular epidemiology of multidrug-resistant bacteria isolated from Libyan and Syrian patients with war injuries in two Bundeswehr hospitals in Germany. Eur J Microbiol Immunol. 2018;8(1):1–11.
Hammerum AM, Larsen AR, Hansen F, Justesen US, Friis-Møller A, Lemming LE, et al. Patients transferred from Libya to Denmark carried OXA-48-producing Klebsiella pneumoniae, NDM-1-producing Acinetobacter baumannii and meticillin-resistant Staphylococcus aureus. Int J Antimicrob Agents. 2012;40(2):191–2.
Kaase M, Eckmanns T, Pfennigwerth N, Szabados F, Gatermann S. PRP08 Carbapenemases found in patients from Libyia. Int J Med Microbiol. 2012;302:91.
Kieffer N, Ahmed MO, Elramalli AK, Daw MA, Poirel L, Álvarez R, et al. Colistin-resistant carbapenemase-producing isolates among Klebsiella spp. and Acinetobacter baumannii in Tripoli, Libya. J Glob Antimicrob Resist. 2018;13:37–9.
Kocsis E, Savio C, Piccoli M, Cornaglia G, Mazzariol A. Klebsiella pneumoniae harbouring OXA-48 carbapenemase in a Libyan refugee in Italy. Clin Microbiol Infect. 2013;19(9).
Kraiem AG, Zorgani A, Elahmer O, Hammami A, Chaaben BM, Ghenghesh KS. New Delhi metallo-β-lactamase and OXA-48 carbapenemases in gram-negative bacilli isolates in Libya. Libyan J Med. 2015;10.
Lafeuille E, Decré D, Mahjoub-Messai F, Bidet P, Arlet G, Bingen E. OXA-48 carbapenemase-producing Klebsiella pneumoniae isolated from Libyan patients. Microb Drug Resist. 2013;19(6):491–7.
Leistner R, Denkel LA, Gastmeier P, Werner G, Layer F, Pfeifer Y. Prevalence of MRSA and Gram-negative bacteria with ESBLs and carbapenemases in patients from Northern Africa at a German hospital. J Antimicrob Chemother. 2015;70(11):3161–4.
Mathlouthi N, Al-Bayssari C, El Salabi A, Bakour S, Ben Gwierif S, Zorgani AA, et al. Carbapenemases and extended-spectrum β-lactamases producing enterobacteriaceae isolated from Tunisian and Libyan hospitals. J Infect Dev Ctries. 2016;10(7):718–27.
Mohammed MA, Alnour TMS, Shakurfo OM, Aburass MM. Prevalence and antimicrobial resistance pattern of bacterial strains isolated from patients with urinary tract infection in Messalata Central Hospital. Libya Asian Pac J Trop Med. 2016;9(8):771–6.
Abujnah AA, Zorgani A, Sabri MAM, El-Mohammady H, Khalek RA, Ghenghesh KS. Multidrug resistance and extended-spectrum beta-lactamases genes among Escherichia coli from patients with urinary tract infections in Northwestern Libya. Libyan J Med. 2015;10(1).
Pirš M, Andlovic A, Cerar T, Žohar-Čretnik T, Kobola L, Kolman J, et al. A case of OXA-48 carbapenemase-producing Klebsiella pneumoniae in a patient transferred to Slovenia from Libya, November 2011. Eurosurveillance [Internet]. 2011;16(50):pii=20042. Available from: www.eurosurveillance.orghttp://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20042
Salem MA, Ahmed FA. Bacterial Profile of Urinary Tract Infection and Antimicrobial Susceptibility Pattern Among Patients Attending at Bushra Medical Laboratory, Tripoli. Libya J Gastroenterol Hepatol Res. 2018;7(4):2671–5.
Zorgani A, Abofayed A, Glia A, Albarbar A, Hanish S. Prevalence of device-associated nosocomial infections caused by gram-negative bacteria in a trauma intensive care unit in Libya. Oman Med J. 2015;30(4):270–5.
Zorgani A, Almagatef A, Sufya N, Bashein A, Tubbal A. Detection of CTX-M-15 among uropathogenic Escherichia coli isolated from five major hospitals in Tripoli, Libya. Oman Med J. 2017;32(4):322–7.
Zorgani A, Daw H, Sufya N, Bashein A, Elahmer O, Chouchani C. Co-occurrence of plasmid-mediated AmpC β-lactamase activity among Klebsiella pneumoniae and Escherichia coli. Open Microbiol J. 2017;11(1):195–202.
Ahmed SF, Ali MMM, Mohamed ZK, Moussa TA, Klena JD. Fecal carriage of extended-spectrum beta-lactamases and AmpC-producing Escherichia coli in a Libyan community. Ann Clin Microbiol Antimicrob. 2014;13(22).
Ali IM, Amirthalingam R. Clinical isolates of MEC A, methicillin, vancomycin resistance S. aureus; ESBLs producing K. pneumoniae, E. coli, P. auregenosa from various clinical source and its antimicrobial resistance patterns. Int J Med Res Heal Sci. 2015;4(1):123.
Buzayan MM, El-Garbulli FR. Detection of ESBL and AmpC-lactamases producing in uropathogen Escherichia coli isolates at Benghazi Center of Infectious Diseases and Immunity. Int J Curr Microbiol Appl Sci [Internet]. 2014;3(2):145–53. Available from: http://www.ijcmas.com
Buzayan MM, Tobgi RS, Ibrahim AAT. Detection of extended spectrum β-lactamases among urinary Escherichia coli and Klebsiella pneumoniae from two centres. Jamahiriya Med J. 2010;10(1):10–6.
Carannante N, Pallotto C, Bernardo M, Di Caprio G, Tascini C. Treatment of a Klebsiella pneumoniae KPC cellulitis and gut decolonization with ceftazidime/avibactam in a migrant from Libya. J Chemother. 2018;30(3):183–4.
Dau AA, Tloba S, Daw MA. Characterization of wound infections among patients injured during the 2011 Libyan conflict. East Mediterr Heal J. 2013;19(4):356–61.
Elramalli A, Almshawt N, Ahmed MO. Current problematic and emergence of carbapenemase-producing bacteria: A brief report from a libyan hospital. Pan Afr Med J. 2017;26.
Rakotovao-Ravahatra ZD, Randriatsarafara FM, Rasoanandrasana S, Raverohanta L, Rakotovao AL. Resistant phenotypes of Escherichia coli strains responsible for urinary tract infection in the laboratory of the University Hospital Joseph Raseta Befelatanana, Antananarivo. Pan Afr Med J. 2017;26.
Randrianirina F, Vaillant L, Ramarokoto CE, Rakotoarijaona A, Andriamanarivo ML, Razafimahandry HC, et al. Antimicrobial resistance in pathogens causing nosocomial infections in surgery and intensive care units of two hospitals in Antananarivo, Madagascar. J Infect Dev Ctries. 2010;
Randrianirina F, Vedy S, Rakotovao D, Ramarokoto CE, Ratsitohaina H, Carod JF, et al. Role of contaminated aspiration tubes in nosocomial outbreak of Klebsiella pneumoniae producing SHV-2 and CTX-M-15 extended-spectrum β-lactamases. J Hosp Infect. 2009;72(1):23–9.
Ranosiarisoa ZN, El Harrif S, Andrianirina AZ, Duron S, Simon-Ghediri MJ, Ramparany L, et al. Epidemiology of Early-onset Bacterial Neonatal Infections in Madagascar. Pediatr Infect Dis J. 2019;38(1):76–81.
Rasamiravaka T, Batavisoa E, Ranaivosoa MK, Rasamindrakotroka A. Profile and antimicrobial resistance to newly available drugs of urinary tract pathogens among Malagasy pregnant women. Trop Biomed. 2016;
Rasamiravaka T, Shaista Sheila HSL, Rakotomavojaona T, Rakoto-Alson AO, Rasamindrakotroka A. Changing profile and increasing antimicrobial resistance of uropathogenic bacteria in Madagascar. Med Mal Infect. 2015;
Andriatahina T, Randrianirina F, Hariniana ER, Talarmin A, Raobijaona H, Buisson Y, et al. High prevalence of fecal carriage of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae in a pediatric unit in Madagascar. BMC Infect Dis. 2010;10.
Chereau F, Herindrainy P, Garin B, Huynh BT, Randrianirina F, Padget M, et al. Colonization of extended-spectrum-β-lactamase- and NDM-1-producing Enterobacteriaceae among pregnant women in the community in a low-income country: A potential reservoir for transmission of multiresistant Enterobacteriaceae to neonates. Antimicrob Agents Chemother. 2015;59(6):3652–5.
Herindrainy P, Randrianirina F, Ratovoson R, Hariniana E, Buisson Y, Genel N, et al. Rectal carriage of extended-spectrum beta-lactamase-producing Gram-negative bacilli in community settings in Madagascar. PLoS One. 2011;
Naas T, Cuzon G, Robinson AL, Andrianirina Z, Imbert P, Ratsima E, et al. Neonatal infections with multidrug-resistant ESBL-producing E. cloacae and K. pneumoniae in Neonatal Units of two different Hospitals in Antananarivo, Madagascar. BMC Infect Dis. 2016;16(1).
Gallaher JR, Banda W, Lachiewicz AM, Krysiak R, Cairns BA, Charles AG. Colonization with Multidrug-Resistant Enterobacteriaceae is Associated with Increased Mortality Following Burn Injury in Sub-Saharan Africa. World J Surg. 2018;42(10):3089–96.
Gray KJ, Wilson LK, Phiri A, Corkill JE, French N, Hart CA. Identification and characterization of ceftriaxone resistance and extended-spectrum β-lactamases in Malawian bacteraemic Enterobacteriaceae. J Antimicrob Chemother. 2006;57(4):661–5.
Kumwenda GP, Sugawara Y, Abe R, Akeda Y, Kasambara W, Chizani K, et al. First Identification and genomic characterization of multidrug-resistant carbapenemase-producing Enterobacteriaceae clinical isolates in Malawi. Africa J Med Microbiol. 2019;68(12):1707–15.
Sangare SA, Rondinaud E, Maataoui N, Maiga AI, Guindo I, Maiga A, et al. Very high prevalence of extended-spectrum beta-lactamase-producing Enterobacteriaceae in bacteriemic patients hospitalized in teaching hospitals in Bamako, Mali. PLoS One. 2017;
Tandé D, Boisramé-Gastrin S, Münck MR, Héry-Arnaud G, Gouriou S, Jallot N, et al. Intrafamilial transmission of extended-spectrum-β-lactamase-producing Escherichia coli and Salmonella enterica Babelsberg among the families of internationally adopted children. J Antimicrob Chemother. 2010;65(5):859–65.
Hailaji NSM, Ould Salem ML, Ghaber SM. La sensibilité aux antibiotiques des bactéries uropathogènes dans la ville de Nouakchott – Mauritanie. Prog en Urol. 2016;26(6):346–52.