Update on the Resistance of Escherichia coli Isolated from Urine Specimens in a Moroccan Hospital: A Review of a 7-Year Period
by
Elmostafa Benaissa
1,*, 
Nadia Elmrimar
1,
Elmehdi Belouad
1,
Youness Mechal
2,
Mohammed Ghazouani
2,
Fatna Bsaibiss
2,
Yassine Benlahlou
1,
Mariama Chadli
2,
Nadia Touil
3,
Abdelhay Lemnaouer
1,
Adil Maleb
4 and
Mostafa Elouennass
1 1
Department of Clinical Bacteriology, Mohammed V Military Teaching Hospital, Research Team of Epidemiology and Bacterial Resistance, Faculty of Medicine and Pharmacy of Rabat, Mohammed V University, Avenue Mohamed Belarbi El Alaoui, Rabat B.P. 6203, Morocco
2
Department of Clinical Bacteriology, Mohammed V Military Teaching Hospital, Faculty of Medicine and Pharmacy of Rabat, Mohammed V University, Avenue Mohamed Belarbi El Alaoui, Rabat B.P. 6203, Morocco
3
Research and Biosafety Laboratory, Mohammed V Military Teaching Hospital/Faculty of Medicine and Pharmacy, Mohammed V University, Avenue Mohamed Belarbi El Alaoui, Rabat B.P. 6203, Morocco
4
Department of Clinical Bacteriology, Mohammed VI Hospital, Research Team of Epidemiology and Bacterial Resistance, Faculty of Medicine and Pharmacy of Rabat, Mohammed V University, Avenue Mohamed Belarbi El Alaoui, Rabat B.P. 6203, Morocco
*
Author to whom correspondence should be addressed.
GERMS 2021, 11(2), 189-198; https://doi.org/10.18683/germs.2021.1256
Submission received: 30 December 2020
/
Revised: 10 April 2021
/
Accepted: 19 April 2021
/
Published: 2 June 2021
Abstract
Introduction: Escherichia coli is the most commonly isolated species in both community and healthcare-associated infections. Our study's purpose was to determine the rates of antibiotic resistance of E. coli isolates in hospital and community populations, track the kinetics of resistance rates of E. coli isolates to major antibiotics, particularly those prescribed for urinary tract infections and study the occurrence and evolution of multi-resistant phenotypes. Methods: We conducted a retrospective study at the Bacteriological Department of the Mohammed V Military Hospital of Instruction, over a period of 7 years. All isolates of E. coli from inpatients and outpatients were included. Identification of bacterial isolates was based on culture, morphological and biochemical identification characteristics. Antibiotic susceptibility was studied using the Mueller Hilton agar diffusion method by using OXOID® type antibiotic discs and interpreted according to the recommendations of EUCAST/CA-SFM 2019. Results: The rate of resistance of E. coli isolates to 3rd generation cephalosporins, imipenem and fluoroquinolones was 12%, 1% and 34%, respectively. The difference between the resistance rates of inpatient and outpatient E. coli isolates was statistically significant for most antibiotics (p < 0.05). The rate of extended-spectrum beta-lactamase phenotype (ESBL) was 6.73%. The carbapenemase phenotype was 1.25%. The ESBL phenotype rate increased from 3% in 2012 to 11.16% in 2018. Conclusions: The progression of the ESBL phenotype in both hospital and community settings, due to the increase in the resistance rate to 3rd generation cephalosporin, is prompting a review of the strategy for the therapeutic management of urinary tract infections with these molecules as probabilistic treatment.
Introduction
Escherichia coli is a commensal bacterium of the digestive tract of humans and animals. It represents 80% of the facultative aero-anaerobic human digestive flora.[1] E. coli is the most 1commonly isolated species in both community and healthcare-associated infections. It is also the most commonly isolated species from urinary tract infections (50-80%).[2]
Increasing rates of E. coli resistance to antibiotics represent a national and international public health problem. These rates vary by region and sampling site.
The genetic determinism of these resistance mechanisms can be either chromosomal or plasmidic. The latter is the most dangerous due to its ease of dissemination.[3]
At national level, little to no data are available on the evolution of E. coli resistance to antibiotics, outside of some single-center studies reporting variable rates of E. coli with an extended-spectrum beta-lactamase phenotype (ESBL) ranging from 1.3% to 12.4%.[4,5] This diffusion of multi-resistant E. coli strains has an impact on the use of critical antibiotics (carbapenems, 3rd generation cephalosporins, 4th generation cephalosporins and fluroquinolones), with the emergence and spread of carbapenemase-producing strains among others. Indeed, different data report carbapenem resistance rates ranging from 2.4% to 4% for ertapenem.[5,6] The purpose of our study was to determine the rates of antibiotic resistance of E. coli isolates in hospital and community populations, track the kinetics of resistance rates of E. coli isolates to major antibiotics, particularly those prescribed for urinary tract infections, and study the occurrence and evolution of multi-resistant phenotypes.
Methods
We conducted a retrospective study at the Bacteriological Department of Mohammed V Military Hospital of Instruction, over a period of 7 years from 01 January 2012 to 31 December 2018.
All isolates of E. coli from the prescribed urine cytobacteriological examination (UCE) from inpatients and outpatients were included.
Identification of bacterial isolates was based on culture, morphological and biochemical identification characteristics. Biochemical identification was performed using API20E ready-to-use galleries (bioMérieux SA, France).
Antibiotic susceptibility was studied using the Mueller Hilton agar diffusion method by using OXOID® type antibiotic discs and interpreted according to the recommendations of EUCAST/CA-SFM 2019.[7] The interpretation was performed using the ADAGIO® automated system (Bio-Rad Laboratories, France). Quality control of the antibiotic susceptibility test was performed with the E. coli strain ATCC 25922.
The fluoroquinolones, the sulfamethoxazole-trimethoprim, the 3rd generation cephalosporins and the carbapenems used in the study were: norfloxacin, cotrimoxazole, ceftriaxone and ertapenem and imipenem, respectively.
The detection of ESBLs was performed by a phenotypic method based on synergy detection between the amoxicillin-clavulanic acid disc and three third-generation cephalosporin discs: cefotaxime, ceftazidime and cefepime.[8]
Carbapenemases detection was performed using the Carba-test®. This test is based on a color change of a chromogenic substrate in the presence of a carbapenemase-producing strain. Testing is conducted directly in micro-tubes with freshly isolated Enterobacteriaceae colonies and the reading should be taken within 30 minutes.[9]
Data extraction was performed using the epidemiological model of the ADAGIO® automated system antibiotic susceptibility testing system and the Laboratory Information System (LIS). Duplicates were excluded.
Moroccan legislation does not require ethical approval for retrospective studies based on laboratory data.
Statistical analysis
Strains categorized as "intermediate" were counted as resistant. Statistical analysis was performed using Excel and SPSS 2020 software. Comparison of the resistance rate between inpatients and outpatients was performed using the Chi-square test. A p value of less than 0.05 was considered statistically significant.
Results
We collected 10324 isolates of E. coli during the study period, including 3485 isolates from ambulatory patients (33.8%) and 6839 isolates from hospitalized patients (66.2%). The sex ratio (M/F) was 0.5. The average age was 47 years with extremes between 0 and 96 years.
Antibiotic susceptibility study of all E. coli isolates showed resistance rates to ampicillin, amoxicillin-clavulanic acid, 3rd generation cephalosporin, imipenem, norfloxacin, gentamicin, amikacin, mecillinam, fosfomycin and nitrofurans of 64%, 36%, 12%, 1%, 34%, 10%, 3%, 9%, 2% and 2%, respectively – Figure 1.
Comparison of antibiotic resistance rates of E. coli isolates in the two populations (inpatients and outpatients) showed a statistically significant difference for ampicillin (p<0.001), amoxicillin-clavulanic acid (p<0.001), 3rd generation cephalosporin (p<0.001), ertapenem (p=0.002), norfloxacin (p<0.001), gentamicin (p=0.007), amikacin (p=0,004), sulfamethoxazole-trimethoprim (p<0.001), but not for imipenem (p=0.432), fosfomycin (p=0.678) and nitrofurans (p=0.293) – Table 1.
The rate of ESBL phenotype was 6.73% (695/10324) for all E. coli isolates. This rate was 4.1% (144/3485) for outpatients and 8.05% (551/6839) for inpatients. The carbapenemase phenotype was 1.25% (129/10324) for all E. coli isolates. The carbapenemase phenotype was 1.03% (36/3485) for outpatients and 1.36% (93/6839) inpatients.
The resistance rate of E. coli ESBL isolates to fosfomycin, nitrofurans, mecillinam, ertapenem and amikacin in inpatients versus outpatients was 2% versus 1%, 2% versus 2%, 9% versus 11%, 8% versus 7% and 9% versus 10%, respectively. The difference between the rates of E. coli isolates with ESBL phenotype for inpatients and outpatients was not statistically significant for amoxicillin-clavulanic acid (p=0.890), 3rd generation cephalosporin (p=0.774), ertapenem (p=0.767), norfloxacin (p=0.725), gentamicin (p=0.949), amikacin (p=0.805), sulfamethoxazole-trimethoprim (p=0.095), imipenem (p=0.442), fosfomycin (p=0.788) and nitrofurans (p=0.755), but it was significant for ampicillin (p<0.001) – Table 2.
Table 3 shows the distribution of the ESBL phenotype per year. The ESBL phenotype rate increased from 3% in 2012 to 11.16% in 2018.
Figure 2 shows the progression of beta-lactam resistance. The resistance rate of ampicillin increased from 56% in 2012 to 66% in 2018 and that of amoxicillin-clavulanic acid has decreased from 36% in 2012 to 34% in 2018. The resistance rate to 3rd generation cephalosporins increased from 7% in 2012 to 13% in 2018, while the carbapenem resistance rate remained relatively stable and low during the study period.
Figure 3 shows the evolution of E. coli resistance to norfloxacin, cotrimoxazole, gentamicin and amikacin. The resistance rate of E. coli to norfloxacin increased from 36% in 2012 to 47% in 2016 and the rate for cotrimoxazole increased from 30% in 2012 to 43% in 2016. The resistance rate of E. coli to gentamicin decreased from 11% in 2012 to 8% in 2018 and that of amikacin increased from 1% in 2012 to 5% in 2017.
E. coli resistance to fosfomycin and nitrofurans remained stable and low during our study period (< 5%) – Figure 4.
Discussion
Surveillance of local epidemiology and its evolution remains essential for appropriate and effective first-line antibiotic therapy. In our research, the study of antibiotic resistance in hospital and community E. coli uropathogen isolates showed variable rates of resistance depending on the antibiotic tested. Resistance rates of E. coli isolates to ampicillin and amoxicillin-clavulanic acid were 64% and 36%, respectively – Figure 1. Nationally, different studies report varying resistance rates ranging from 61.2% to 70.1% for ampicillin and 38.8% to 66% for amoxicillin-clavulanic acid. In analyzing the kinetics curve, we found an increase in the resistance rate of E. coli isolates to ampicillin ranging from 56% in 2012 to 66% in 2018, while the rate for amoxicillin-clavulanic acid experienced fluctuations from 36% in 2012 to 34% in 2018 with peaks in 2013 and 2014 reaching 43% and 39% respectively – Figure 2. These rates are comparable to national and European data and some African studies,[6,10,11] but the rates are higher in the pediatric population.[12,13] These figures are sometimes well over 10%, making it difficult to consider these molecules in the empirical treatment of urinary tract infections.
The rate of resistance to 3rd generation cephalosporins showed an increase from 7% in 2012 to 13% in 2018 – Figure 2. These data are higher than those reported by various national studies, which reported 3rd generation cephalosporins resistance rates ranging from 4.5% in 2014 to 5.6% in 2015 in the adult population and lower in the infant population with rates varying from 21% in 2014 to 16.38% in 2018.[5,6,12] At the international level, our data are lower than those published by the European Antimicrobial Resistance Surveillance Network (EARS-Net), which reported rates ranging from 14.6% in 2015 to 15.1% in 2018 and higher than those published by the French surveillance network (ONERBA) which reported 3rd generation cephalosporins resistance rates ranging from 2.2% in 2008 to 4% in 2017.[14,15] In Tunisia, the rate of resistance to 3rd generation cephalosporins in enterobacteria increased from 8% in 2002 to 16.3% in 2014.[16] In our study, this high rate of resistance to 3rd generation cephalosporins is explained by the production of ESBL with plasmid determinism type CTX-M-15, epidemic in our regions. This finding has been confirmed by national genotypic studies.[3,4] The rate of E. coli isolates with an ESBL phenotype increased from 3% in 2012 to 11.6% in 2018, i.e., a 30% increase – Table 3. This increase is verified at the national level and is more pronounced in the pediatric population.[6,12,13] The progression of the ESBL phenotype is a worldwide phenomenon reported by various studies. In Senegal, the ESBL rate increased from 3.3% in 2003 to 14.2% in 2013 in the community. In France, the rate varied from 1.8% to 5.1% in 2016 depending on the region and from 1% in 2007 to 4.73% in 2015 in the community.[17,18] These E. coli ESBL isolates are often associated with other resistance mechanisms and this was well illustrated in our study. This multi-resistance is explained by the fact that ESBL genes, generally carried by plasmids, are often associated with antibiotic resistance genes, notably to aminoglycosides and fluoroquinolones.[19]
Faced with multi-resistance, the pressure to prescribe carbapenems contributes to the emergence of carbapenemases. Carbapenemases are a heterogeneous group of enzymes whose common feature is to hydrolyze at least one of the carbapenems. The most frequent are KPC (Ambler class A), VIM, NDM (class B), OXA-48 (class D). The latter is one of the most recently described carbapenemases and is mainly identified in Mediterranean countries.[20] In our study, the resistance rate to imipenem rose from 0% in 2012 to around 1% in 2018 – Figure 2. These data are similar to those reported at the national level.[5,6] Resistance to carbapenems is mainly due to the production of carbapenemase and also to other mechanisms such as the combination of two resistance mechanisms ESBL and/or cephalosporinase associated with loss of membrane permeability in Enterobacteriaceae.[20]
Resistance to fluoroquinolones has been growing for several years and is now a global problem. During our study period, the rate of resistance to fluoroquinolones increased from 30% in 2012 to 42% in 2017 – Figure 3. These data are higher than those reported by various local studies, which showed variable rates ranging from 27% in 2010 to 29.1% in 2015.[5,6,21] On the other hand, these rates are low in the pediatric population and this is due to the prescription of these molecules in this population because of their joint toxicity. According to a study conducted in Senegal on the evolution of antibiotic resistance in community-based uropathogenic E. coli, the rate of resistance to ciprofloxacin rose from 22.1% in 2003 to 29.8% in 2013.[11] EARS-Net reported resistance rates ranging from 24.8% in 2015 to 25.3% in 2018.[15] The increase in the resistance rate to fluoroquinolones is explained by the predominance of endemic plasmid-supported resistance. This has been confirmed by national genotypic studies.[22]
During the study period, resistance to sulfamethoxazole-trimethoprim combination increased from 36% in 2012 to 40% in 2018 – Figure 3. This increase was reported by national studies and some African studies.[11,12] This high rate of resistance to the sulfamethoxazole-trimethoprim combination is explained by the massive and irrational prescription of this molecule and also by the plasmid resistance which is mediated by 2 drug-resistant DHPS enzymes encoded by sul1 or sul2 genes.[23] In view of these high rates of resistance to fluoroquinolones and cotrimoxazole, these molecules will not be recommended in the probabilistic treatment of urinary tract infections in our region.
Resistance to gentamicin and amikacin was 10% and 3%, respectively – Figure 1. These rates are similar to national data and some African studies.[5,24] These molecules still maintain a good sensitivity against uropathogenic E. coli isolates, hence the interest in using them in dual therapy for the probabilistic treatment of severe urinary tract infections.
The resistance rate of E. coli isolates to fosfomycin, mecillinam and nitrofurans was 2%, 9% and 2%, respectively – Figure 1. These rates are close to those reported in national studies.[5,6] These molecules showed resistance rates below 10% and therefore can be used as probabilistic treatment in simple cystitis. E. coli ESBL isolates showed a sensitivity rate of more than 89% to these molecules for both patient categories (outpatients and inpatients) – Table 2. In light of these data, these antibiotics have shown the benefit of their use in the probabilistic treatment of simple E. coli ESBL urinary tract infections.
Conclusions
The progression of the ESBL phenotype in both hospital and community settings, due to the increase in the resistance rate to 3rd generation cephalosporins, is prompting a review of the strategy for the therapeutic management of urinary tract infections with these molecules as probabilistic treatment.
Alongside the emergence of the ESBL phenotype, we are witnessing an alarming increase in the resistance rate to fluoroquinolones, which, together with the 3rd generation cephalosporins, constitute an important therapeutic class in the management of serious urinary tract infections.
Faced with this multi-resistance, the pressure to prescribe carbapenems contributes to the emergence of carbapenemases.
A sound therapeutic strategy is essential, based on the implementation of a national plan to combat antibiotic resistance in order to preserve the therapeutic arsenal at a time when the prospects for bringing new molecules to the market are virtually absent.
Author Contributions
All authors have made substantial contributions. ME conceived, determined and designed the study. EB, NE, YM, FB, MG, MC, ELB and YB acquired clinical and biological data. EB, NT, AL, AM and ME analysed the data. EB, YM and ME presented and interpreted graphical data. EB and ME drafted, corrected and edited the manuscript. AM, AL and NT performed the linguistic review and critically revised the manuscript. All authors read and approved the final version of the manuscript.
Funding
None to declare.
Institutional Review Board Statement
This study does not constitute human research requiring Institutional Review Board approval according to Moroccan legislation.
Data Availability Statement
The datasets used and analyzed during the current study are available from the corresponding author on reasonable request.
Acknowledgments
The authors would like to thank all the technicians of the Bacteriology Laboratory of the Mohammed V Military Hospital in Rabat for their contribution to the achievement of this study.
Conflicts of Interest
All authors – none to declare.
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Figure 1.
Antibiotic resistance rate of E. coli (n=10324). R – resistant; I – intermediate; AMP – ampicillin; AMC – amoxicillin-clavulanic acid; C1G – first generation cephalosporins; FOX – cefoxitin; ERT – ertapenem; C3G – 3rd generation cephalosporins; IMP – imipenem; CN – gentamicin; AK – amikacin; NOR – norfloxacin; SXT – sulfamethoxazole-trimethoprim; NT – nitrofuran; FOS – fosfomycin; MEC – mecillinam.
Figure 1.
Antibiotic resistance rate of E. coli (n=10324). R – resistant; I – intermediate; AMP – ampicillin; AMC – amoxicillin-clavulanic acid; C1G – first generation cephalosporins; FOX – cefoxitin; ERT – ertapenem; C3G – 3rd generation cephalosporins; IMP – imipenem; CN – gentamicin; AK – amikacin; NOR – norfloxacin; SXT – sulfamethoxazole-trimethoprim; NT – nitrofuran; FOS – fosfomycin; MEC – mecillinam.
Figure 2.
The evolution of E. coli resistance rate to beta-lactams.
Figure 3.
The evolution of E. coli resistance to norfloxacin, cotrimoxazol, gentamicin and amikacin.
Figure 3.
The evolution of E. coli resistance to norfloxacin, cotrimoxazol, gentamicin and amikacin.
Figure 4.
The evolution of E. coli resistance to fosfomycin and furans.
Table 1.
Antibiotic resistance rates of E. coli isolates from inpatients and outpatients.
| Outpatients | Inpatients | P value | Chi-square | df value | Contingency coefficient | |||||
|---|---|---|---|---|---|---|---|---|---|---|
| Isolates | R+I | % | Isolates | R+I | % | |||||
| AMP | 3452 | 2075 | 60.11% | 6664 | 4412 | 66.21% | p<0.001 | 36.475 | 1 | 0.0599 |
| AMC | 3482 | 1135 | 32.57% | 6842 | 2599 | 37.97% | p<0.001 | 29.011 | 1 | 0.0529 |
| TZP | 1285 | 167 | 13.00% | 3841 | 763 | 19.86% | p<0.001 | 30.126 | 1 | 0.0764 |
| C1G | 2570 | 578 | 22.49% | 3640 | 1270 | 34.89% | p<0.001 | 110.215 | 1 | 0.132 |
| FOX | 3221 | 66 | 2.05% | 6451 | 214 | 3.32% | p<0.001 | 11.845 | 1 | 0.035 |
| C3G | 3511 | 239 | 6.81% | 6813 | 1027 | 15.07% | p<0.001 | 146.41 | 1 | 0.118 |
| CFM | 1173 | 120 | 10.23% | 3624 | 673 | 18.57% | p<0.001 | 44.073 | 1 | 0.0954 |
| ERT | 3247 | 75 | 2.31% | 6455 | 224 | 3.47% | p=0.002 | 9.354 | 1 | 0.031 |
| IMP | 113 | 2 | 1.77% | 414 | 2 | 0.48% | p=0.432 | 0.617 | 1 | 0.0342 |
| CN | 2983 | 252 | 8.45% | 6125 | 628 | 10.25% | p=0.007 | 7.284 | 1 | 0.0283 |
| AK | 3303 | 73 | 2.21% | 6545 | 213 | 3.25% | p=0.004 | 7.992 | 1 | 0.0285 |
| NOR | 3284 | 881 | 26.83% | 6600 | 2515 | 38.11% | p<0.001 | 123.193 | 1 | 0.111 |
| SXT | 3227 | 1156 | 35.82% | 6141 | 2640 | 42.99% | p<0.001 | 44.787 | 1 | 0.069 |
| FOS | 2490 | 37 | 1.49% | 4989 | 82 | 1.64% | p=0.678 | 0.173 | 1 | 0.0048 |
| NT | 2337 | 35 | 1.50% | 4627 | 87 | 1.88% | p=0.293 | 1.108 | 1 | 0.0126 |
| MEC | 1079 | 75 | 6.95% | 3169 | 315 | 9.94% | p=0.004 | 8.271 | 1 | 0.0441 |
E. coli antibiotic resistance rates were compared between outpatients and inpatients using the Chi-square test. AMP – ampicillin; AMC – amoxicillin-clavulanic acid; TZP – piperacillin-tazobactam; C1G – first generation cephalosporins; FOX – cefoxitin; C3G – 3rd generation cephalosporins; CFM – cefixime; ERT – ertapenem; IMP – imipenem; CN – gentamicin; AK – amikacin; NOR – norfloxacin; SXT – sulfamethoxazole-trimethoprim; NT – nitrofuran; FOS – fosfomycin; MEC – mecillinam.
Table 2.
Resistance rates of E. coli isolates with an ESBL phenotype from inpatients and outpatients.
Table 2.
Resistance rates of E. coli isolates with an ESBL phenotype from inpatients and outpatients.
| Inpatients | Outpatients | P value | Chi-square | df value | Contingency coefficient | |||||
|---|---|---|---|---|---|---|---|---|---|---|
| ESBL isolates | R+I | % | ESBL isolates | R+I | % | |||||
| AMP | 534 | 534 | 100% | 133 | 133 | 100% | p<0.001 | 239.88 | 1 | 0.514 |
| AMC | 551 | 452 | 82% | 141 | 117 | 83% | p=0.890 | 0.0193 | 1 | 0.00528 |
| TZP | 430 | 200 | 47% | 109 | 48 | 44% | p=0.722 | 0.126 | 1 | 0.0153 |
| C1G | 210 | 206 | 98% | 65 | 64 | 98% | p=0.735 | 0.0207 | 1 | 0.0204 |
| FOX | 515 | 57 | 11% | 125 | 19 | 15% | p=0.260 | 1.27 | 1 | 0.0445 |
| C3G | 558 | 551 | 99% | 144 | 142 | 99% | p=0.774 | 0.0827 | 1 | 0.0109 |
| CFM | 402 | 399 | 99% | 98 | 95 | 97% | p=0.171 | 1.877 | 1 | 0.0611 |
| ERT | 509 | 42 | 8% | 116 | 8 | 7% | p=0.767 | 0.0875 | 1 | 0.0118 |
| IMP | 49 | 1 | 2% | 12 | 0 | 0% | p=0.442 | 0.592 | 1 | 0.098 |
| CN | 491 | 145 | 30% | 115 | 33 | 29% | p=0.949 | 0.00402 | 1 | 0.00258 |
| AK | 520 | 47 | 9% | 127 | 13 | 10% | p=0.805 | 0.0608 | 1 | 0.00969 |
| NOR | 502 | 447 | 89% | 118 | 107 | 91% | p=0.725 | 0.124 | 1 | 0.0141 |
| SXT | 479 | 342 | 71% | 119 | 75 | 63% | p=0.095 | 6.016 | 1 | 0.0941 |
| FOS | 410 | 8 | 2% | 104 | 1 | 1% | p=0.788 | 457.4 | 1 | 0.686 |
| NT | 357 | 8 | 2% | 95 | 2 | 2% | p=0.755 | 392.808 | 1 | 0.681 |
| MEC | 371 | 35 | 9% | 89 | 10 | 11% | p=0.753 | 256.383 | 1 | 0.594 |
E. coli ESBL antibiotic resistance rates were compared between outpatients and inpatients using the Chi-square test. AMP – ampicillin; AMC – amoxicillin-clavulanic acid; TZP – piperacillin-tazobactam; C1G – first generation cephalosporins; FOX – cefoxitin; C3G – 3rd generation cephalosporins; CFM – cefixime; ERT – ertapenem; IMP – imipenem; CN – gentamicin; AK – amikacin; NOR – norfloxacin; SXT – sulfamethoxazole-trimethoprim; NT – nitrofuran; FOS – fosfomycin; MEC – mecillinam; ESBL – extended-spectrum beta-lactamase.
Table 3.
The distribution of the ESBL phenotype per year.
| Years | Isolates of E coli | Number of ESBL isolates | ESBL (%) |
|---|---|---|---|
| 2012 | 797 | 24 | 3% |
| 2013 | 1716 | 47 | 2.7% |
| 2014 | 1607 | 37 | 2.30% |
| 2015 | 848 | 37 | 4.36% |
| 2016 | 1166 | 88 | 7.55% |
| 2017 | 2031 | 221 | 10.88% |
| 2018 | 2159 | 241 | 11.16% |
ESBL – extended-spectrum beta-lactamase.
© GERMS 2021.
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MDPI and ACS Style
Benaissa, E.; Elmrimar, N.; Belouad, E.; Mechal, Y.; Ghazouani, M.; Bsaibiss, F.; Benlahlou, Y.; Chadli, M.; Touil, N.; Lemnaouer, A.; et al. Update on the Resistance of Escherichia coli Isolated from Urine Specimens in a Moroccan Hospital: A Review of a 7-Year Period. GERMS 2021, 11, 189-198. https://doi.org/10.18683/germs.2021.1256
AMA Style
Benaissa E, Elmrimar N, Belouad E, Mechal Y, Ghazouani M, Bsaibiss F, Benlahlou Y, Chadli M, Touil N, Lemnaouer A, et al. Update on the Resistance of Escherichia coli Isolated from Urine Specimens in a Moroccan Hospital: A Review of a 7-Year Period. GERMS. 2021; 11(2):189-198. https://doi.org/10.18683/germs.2021.1256
Chicago/Turabian StyleBenaissa, Elmostafa, Nadia Elmrimar, Elmehdi Belouad, Youness Mechal, Mohammed Ghazouani, Fatna Bsaibiss, Yassine Benlahlou, Mariama Chadli, Nadia Touil, Abdelhay Lemnaouer, and et al. 2021. "Update on the Resistance of Escherichia coli Isolated from Urine Specimens in a Moroccan Hospital: A Review of a 7-Year Period" GERMS 11, no. 2: 189-198. https://doi.org/10.18683/germs.2021.1256
APA StyleBenaissa, E., Elmrimar, N., Belouad, E., Mechal, Y., Ghazouani, M., Bsaibiss, F., Benlahlou, Y., Chadli, M., Touil, N., Lemnaouer, A., Maleb, A., & Elouennass, M. (2021). Update on the Resistance of Escherichia coli Isolated from Urine Specimens in a Moroccan Hospital: A Review of a 7-Year Period. GERMS, 11(2), 189-198. https://doi.org/10.18683/germs.2021.1256
