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| ORIGINAL ARTICLE |
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| Year : 2023 | Volume
: 3
| Issue : 1 | Page : 2 |
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High burden of extended spectrum β–lactamase (ESBL)–encoding genes in third–generation cephalosporin–resistant Escherichia coli recovered from frequently contacted surfaces and wastewater of selected healthcare institutions in Nigeria
Omowunmi Abosede Banjo1, Abimbola Olumide Adekanmbi2, Sodiq Abiola Abolade1
1 Department of Microbiology, Olabisi Onabanjo University, Ago-Iwoye, Nigeria
2 Environmental Microbiology and Biotechnology Laboratory; Molecular Biology and Biotechnology Laboratory, Department of Microbiology, University of Ibadan, Ibadan, Nigeria
| Date of Submission | 12-Sep-2022 |
| Date of Decision | 24-Nov-2022 |
| Date of Acceptance | 29-Nov-2022 |
| Date of Web Publication | 05-Jan-2023 |
Correspondence Address:
Abimbola Olumide Adekanmbi
Environmental Microbiology and Biotechnology Laboratory; Molecular Biology and Biotechnology Laboratory, Department of Microbiology, University of Ibadan, Ibadan
Nigeria
 Source of Support: None, Conflict of Interest: None
DOI: 10.4103/2773-0344.363564
Objective: This study aimed to determine the carriage of extended spectrum β-lactamase (ESBL) genes in third-generation cephalosporin-resistant (3GCR) Escherichia (E.) coli from frequently contacted surfaces, wastewater and disinfectant-cleaning solutions of selected healthcare institutions in South-western Nigeria.
Methods: Samples were collected over three months for the isolation of 3GCR E. coli on MacConkey agar containing 6 μg/mL of cefotaxime. 3GCR E. coli isolates were identified by detection of uidA gene and susceptibility to selected antibiotics was performed using disc-diffusion method. Detection of ESBL genes was done using primer-specific PCR.
Results: A total of 22 ESBL-producing E. coli (11 each from the frequently contacted surfaces and wastewater) were obtained from the pool of 3GCR isolates in this study. No isolate was recovered from the disinfectant-cleaning solution. All the ESBL-producing E. coli obtained from the frequently contacted surfaces and wastewater were multidrug resistant, with complete resistance observed to ampicillin, cefotaxime, cefpodoxime, tetracycline and ertapenem. The ESBL genotyping showed that 54.5% carried blaCTX-M, 63.6% carried blaTEM and 9.1% carried blaSHV in isolates from the frequently contacted surfaces, while 63.6%, 9.1% and 18.2% carried blaCTX-M, blaTEM and blaSHV, respectively, in the isolates obtained from the wastewater.
Conclusions: This study showed a high burden of multidrug resistance E. coli on frequently contacted surfaces and wastewater of the studied healthcare institutions, indicating the need for good hygiene and proper mitigation measures to prevent potential public health and environmental challenges. Keywords: Multi-drug resistance; Wastewater; ESBL-producing E. coli; blaSHV; blaTEM; blaCTX-M
How to cite this article:
Banjo OA, Adekanmbi AO, Abolade SA. High burden of extended spectrum β–lactamase (ESBL)–encoding genes in third–generation cephalosporin–resistant Escherichia coli recovered from frequently contacted surfaces and wastewater of selected healthcare institutions in Nigeria. One Health Bull 2023;3:2 |
How to cite this URL:
Banjo OA, Adekanmbi AO, Abolade SA. High burden of extended spectrum β–lactamase (ESBL)–encoding genes in third–generation cephalosporin–resistant Escherichia coli recovered from frequently contacted surfaces and wastewater of selected healthcare institutions in Nigeria. One Health Bull [serial online] 2023 [cited 2023 May 31];3:2. Available from: http://www.johb.info/text.asp?2023/3/1/2/363564 |
| 1. Introduction | |  |
The physical environment of healthcare facilities serves as a major reservoir of microorganisms. The presence of multiple drug resistant bacteria in the environment is an important contributing factor to healthcare-associated infections. Studies on hospital environments played an important role to characterize the dissemination of resistance determinants, which in some cases extended far beyond patients primary colonized areas [1],[2].
The reality of hospital surfaces’ contribution to extended spectrum β-lactamase (ESBL) spread was not fully appreciated until the emergence of molecular evidence-based outcomes linking environmental isolates with isolates from hospital surfaces and those from the patients themselves[3]. The last decade especially, have witnessed mounting reports on the contributions of hospital surfaces to the spread of resistant bacteria carrying resistant genes.
Studies have reported the reservoir nature of hospital environmental surfaces and their propensity to breed and disseminate several hospital-acquired pathogens, of which the enteric bacteria are notable candidates[4],[5]. Bacteria expressing extended spectrum β-lactamases are important group of pathogens linked to nosocomial outbreaks in the hospital settings[2],[6]. Most bacteria residing on inanimate hospital surfaces owe the ability to survive for long outside their primary niche from few days to months, due to the innate resilience they possess[7]. Most hospitals use traditional disinfection as standard recommended practice to control these surface pathogens[7]. It has been reported that in many cases, especially in developing countries, gaps in disinfection procedure and processes have led to sub-optimal cleaning, which has contributed significantly to the colonization and spread of multidrug resistant bacteria carrying resistance genes in hospitals[7],[8]. In addition to the contribution of hospital surfaces to the expansion of ESBLs, untreated hospital wastewater is another important contributor to antibiotic resistance in the environment[9],[10]. What makes it more daunting is that many healthcare facilities are sited in close proximity to residential buildings in Nigeria. Previous studies reported the practice of discharging untreated wastewater directly into municipal drain or directly into the ground which extended the impact farther beyond the hospital to the community and the wider environment[11],[12],[13]. There are continuing concerns over ESBL-producing bacteria due to the rapid increase of variants and transferability between and within bacterial species as a result of the plasmid-borne nature of the ESBL genes. In multiple studies, the incidence and spread of Escherichia (E.) coli strains producing different variants of the ESBL genes have been associated with the hospital environment[14],[15].
Although some studies have been done on the spread of ESBL-producing bacteria and their carriage of ESBL genes in Nigeria gaps still exist owing to the rapid increase and evolution of ESBLs[9],[10],[12],[13]. The few existing literatures available on hospital surfaces are mostly limited to the assessment of microbial loads and phenotypic screening for antibiotic resistance[16],[17]. In Nigeria, inadequate research on hospital surfaces has led to their under-appreciation as potential sources for the spread of ESBL-producing bacteria. This study assessed the occurrence of ESBL-producing bacteria on selected high-touch hospital surfaces and provided more enlightenment on the contribution of these surfaces to the growing reservoirs of ESBL-producing bacteria in the hospital environment, as well as the carriage of ESBL determinants by E. coli isolated from the wastewater of the selected healthcare institutions, with a view to contributing to existing reports on the subject.
| 2. Materials and Methods | | |
2.1. Study design
The study was carried out in two Local Government areas in Ogun state (Ijebu North and Ijebu-Ode) located in Southwest Nigeria. Five healthcare institutions comprising three privately-owned hospitals coded as MPH, VSH and BPH, one state government-owned hospital (SGH) and a clinic located in an institution of higher education (OCC), were used for the collection of samples.
2.2. Collection of samples
Over the sampling course of three-month (April-June, 2021), samples (12 each) were taken from the hospital surfaces (bedside rails, bedside chairs, kidney dishes, ward sinks, overbed tables) using sterile swab sticks, which had been moistened in sterilized saline solution. A defined portion of the surfaces (3 cm × 3 cm) were sampled for consistency. Personnel (cleaners) were encouraged to follow the usual cleaning and disinfecting practice to erase any form of bias and the samples were taken 45-60 minutes after disinfection. Samples (12 each) of the disinfectant-cleaning solution and wastewater were collected into sterile sample bottles from the final wastewater disposal outlet of each institution. Samples were transported on ice to the microbiology laboratory for analysis within two hours of collection.
2.3. Enrichment of samples for the selective isolation of third-generation cephalosporin-resistant E. coli
Swabs from the frequently contacted surfaces, aliquots of the disinfecting solution and wastewater were each inoculated into Luria Bertani broth containing 6 μg/mL cefotaxime and incubated overnight at 35±2 °C. This was done using the cefotaxime breakpoint of ⩾ 4 μg/mL according to Clinical and Laboratory Standards Institute[18]. The streak plate method was used for the isolation of E. coli from the incubated broth cultures on Mac Conkey agar (Oxoid, UK). Morphologically distinct presumptive isolates were selected and further subcultured and stored. Isolates were initially characterised using conventional methods, and also by targeting the housekeeping uid A gene[19]. The details of the uid A primer are shown in [Table 1].
2.4. Antibiotic susceptibility testing and phenotypic detection of ESBL production
The disc diffusion method was employed in determining the antibiogram of the isolates to nine selected antibiotics (ampicillin, ciprofloxacin, gentamicin, cefotaxime, cefpodoxime, amoxicillin-clavulanate, sulfamethoxazole-trimethoprim, tetracycline and ertapenem), while the detection of ESBL production in the isolates was done using the double disc synergy test[18]. Isolates were designated as sensitive, intermediate or resistant using the zone of inhibition interpretation[18]. The multiple antibiotic resistance index (MARI) of each isolate was calculated as the number of antibiotics resisted by each isolate divided by the total number of antibiotics tested against the isolate.
2.5. Detection of blaTEM, blaSHV and blaCTX-M in the ESBL-producing E. coli
Duplex PCR was used for the detection of blaTEM and blaSHV following the procedures of Maynard et al.[20], while detection of blaCTX-M was done using a monoplex PCR following the methods of Mendonça et al[21]. The primer sequences of the genes are shown in [Table 1].
| 3. Results | | |
3.1. Frequency and Distribution of ESBL-producing E. coli obtained from the samples
A total of 22 confirmed ESBL-producing E. coli isolates were detected from the samples, accounting for 62.85% of 35 strains of third-generation cephalosporin-resistant E. coli obtained. Of the 22 isolates, eleven were from the frequently contacted surfaces and the remaining eleven were from the wastewater samples. No ESBL-producing E. coli was obtained from the disinfecting solutions being used at the healthcare institutions.
[Figure 1] shows the distribution of ESBL-producing E. coli obtained based on the healthcare institutions sampled. VSH and MPH had four isolates each from the frequently contacted surfaces, while SGH had two isolates and one from BPH. No ESBL producer was recovered from OCC. From the wastewater, three isolates were obtained respectively from VSH, SGH and OCC, two isolates from MPH and none from BPH. | Figure 1: Distribution of the ESBL-producing E. coli in the healthcare institutions.
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3.2. Resistance of the ESBL-producing E. coli to selected antibiotics
The resistance of the ESBL-producing E. coli obtained from the frequently contacted surfaces and wastewater to the panel of antibiotics is shown in [Figure 2]. All the isolates obtained from the surfaces and wastewater showed complete resistance to ampicillin, cefotaxime, cefpodoxime, tetracycline and ertapenem. The gentamicin resistance among the isolates from frequently contacted surfaces and wastewater was 27.3% and 45.5% respectively, which was the lowest in this study. The resistance to ciprofloxacin was 72.7% for isolates from the frequently contacted surfaces and 63.6% for isolates obtained from wastewater. The resistance to amoxicillin-clavulanate for isolates from wastewater was higher (90.9%) than that from the frequently contacted surfaces (81.8%), while there was complete resistance to sulfamethoxazole-trimethoprim by the isolates from wastewater as against 81.8% resistance observed in the isolates from the frequently contacted surfaces to the same antibiotic. | Figure 2: Resistance of the ESBL-producing E. coli from frequently contacted surfaces and wastewater to selected antibiotics. augmentin: amoxicillinclavulanate; SMZ-TMP: sulfamethoxazole-trimethoprim.
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3.3. Resistance phenotypes and ESBL gene profile of the ESBL-producing E. coli
The resistance phenotypes and gene profile of isolates obtained from the frequently contacted surfaces and wastewater is shown in [Table 2] and [Table 3]. The MARI of the isolates to the antibiotics ranged from 0.55 to 1.00 in isolates from the frequently contacted surfaces and 0.77 to 1.00 for isolates recovered from wastewater. The data suggested a high risk of antibiotic resistance from the samples studied. There were three isolates from the frequently contacted surfaces showing complete resistance to the panel of nine antibiotics, while two isolates from the wastewater showed 100% resistance to all the antibiotics tested. | Table 2: Resistance phenotypes and ESBL gene profile of the ESBL-producing E. coli isolated from frequently contacted surfaces.
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 | Table 3: Resistance phenotypes and ESBL gene profile of the ESBL-producing E. coli isolated from hospital wastewater
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3.4. Frequency of ESBL genes obtained in the ESBL-producing E. coli from frequently contacted surfaces and wastewater
The frequency of occurrence of ESBL genes in the isolates obtained from the frequently contacted surfaces and wastewater is shown in [Table 4]. The most predominant ESBL gene in the E. coli isolated from the frequently contacted surfaces was blaTEM (63.6%) whereas blaCTX-M (63.6%) was the most predominant in the wastewater. Six isolates (54.5%) from the frequently contacted surfaces carried blaCTX-M, while only one isolate carried blaSHV. Two isolates (18.2%) and one isolate (9.1%) respectively carried blaSHV and blaTEM from the wastewater generated by the healthcare institutions. Overall, the percentage occurrence of ESBL genes in isolates from both frequently contacted surfaces and wastewater was 59.1% (blaCTX-M), 36.4% (blaTEM) and 13.6% (blaSHV). | Table 4: Occurrence (%) of ESBL genes in E. coli from frequently contacted surfaces and wastewater.
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| 4. Discussion | | |
Hospitals were considered as a high-risk environment carrying several resistance genes in numerous studies. Wastewater generated from the operations of healthcare institutions contain antibiotic residues which could trigger the development of resistance in resident bacteria, as a result of adaptation and other mechanisms[22]. Grundmann et al.[23] and Baquero et al.[24] in their respective studies opined that high concentration of antibiotic residues in wastewater from healthcare institutions could select for bacteria showing resistance to different classes of antibiotics, thus further confirming the role of wastewater from healthcare institution as an important contributor to the increasing incidence of antibiotic resistance in bacteria.
In this study, eleven ESBL-producing E. coli isolates were obtained from wastewater generated by five healthcare institutions in two local government areas of Ogun State, South-west Nigeria. All the isolates obtained were resistant to more than three antibiotics (multidrug resistant), with MARI ranging from 0.77-1.00. Several other studies have reported the isolation of multidrug resistant E. coli in hospital wastewater and clinical origins. In a study by Ogbolu et al.[25], high resistance to antibiotics was reported in some clinical Gram-negative bacteria, same as Adekanmbi et al.[13],[26], with a reported case of multidrug resistance in E. coli recovered from wastewater of a University sickbay and a tertiary hospital in Ibadan, Nigeria. Gundogdu et al.[27] reported the same trend in E. coli from the hospital environment.
The frequency of ESBL (blaCTX-M, blaTEM and blaSHV) genes were detected in the isolates obtained from the wastewater of the healthcare institutions. The carriage of these genes by E. coli obtained from hospital wastewater has been reported in several studies conducted in different parts of the world. In this study, 63.6% of the total ESBL-producing E. coli obtained from the hospital wastewater carried blaCTX-M. This could be linked to the diversity and known significant clinical impact of the CTX-M, and the occurrence of many phylogenetic groups of the gene, in comparism with other ESBL genes[28]. Adekanmbi et al.[13] reported the predominance of blaCTX-M in their study, which corroborates the observation in this study. The same authors in another closely-related study also reported blaCTX-M as the most prominent ESBL gene in E. coli associated with wastewater and sludge of a healthcare institution in South-west Nigeria[26]. Other notable studies have reported a high frequency of blaCTX-M in bacteria from hospital wastewater and other samples of clinical origin[29],[30],[31],[32].
The ability to resist first-generation cephalosporins, ampicillin and penicillin in ESBL-producing bacteria is encoded by blaTEM. The relative carriage of blaTEM gene (9.1%) in the isolates obtained from wastewater in this study was very low, as it was detected in only one isolate. The low frequency of blaTEM is contrary to the results obtained in some other studies on ESBL-producing bacteria from hospital wastewater and the clinical settings generally. Lien et al.[33] reported the predominance of blaTEM in E. coli from hospital wastewater in Vietnam, while the high carriage of the same gene was reported by Varela et al.[34]. The blaSHV gene was initially associated with infection-causing members of the Enterobacterales and has normally been domiciled in the hospital settings. Some studies have reported a worrisome scenario on the spread of the gene into the environment[35],[36],[37]. In comparison with other ESBL genes, the frequency of blaSHV is generally very low[11],[38].
The carriage of bacteria especially the multidrug resistant ones on inanimate objects in hospitals may have been on the rise partly due to some unhygienic practices in our healthcare facilities. Several studies have reported the contamination of inanimate surfaces by multidrug resistant bacteria notably E. coli, Klebsiella spp. and Staphylococcus spp. Getachew et al.[39] reported the occurrence of bacterial contaminants on inanimate surfaces at a referral hospital in Ethiopia, while Olowokere et al.[l7], Dziri et al.[40], and Matthew et al.[41] all reported the occurrence of different genera of bacteria on inanimate surfaces within the hospital environment. In this study, a total of eleven ESBL-producing E. coli were isolated from inanimate surfaces and equipment of the five selected healthcare institutions. The unabating incidence of ESBL-producing E. coli in hospital environment could be largely due to several factors including the cross transmission of strains from the hospital environment to patients, patients to patients and the transfer of resistance through mobile genetic elements[14],[42],[43],[44].
All the isolates obtained from the surfaces were multidrug resistant which showing a high level of resistance to eight of the tested nine antibiotics, with the only exception being gentamicin. The occurrence of bacteria showing elevated resistance to most commonly used antibiotics has been reported in several studies and the hospital environment has been identified by several studies as a ‘hotspot’ for the spread of multidrug resistant bacteria, especially ESBL-producing enteric bacteria[45].
Of the eleven ESBL producers obtained from frequently contacted surfaces in this study, blaSHV was detected in one isolate (E. coli S62), six isolates (54.5%) carried blaCTX-M, while seven of the isolates (63.6%) carried blaTEM, making it the predominant ESBL gene. In contrast however to the report of Dziri et al.[40], the percentage carriage of the three target ESBL genes in this study was higher, although the increased number of healthcare institutions sampled in this study could be a major factor contributing to this. This observation has further confirmed the assertion in many other studies of the contribution of frequently contacted surfaces in hospitals and other healthcare facilities to the ever-increasing incidence of antibiotic resistance globally.
| 5. Conclusions | | |
ESBL-producing E. coli with multiple resistance to antibiotics and harboring genes encoding ESBL production were obtained from the frequently contacted surfaces and wastewater in this study. This is very alarming as people especially hospital patients and other personnel have constant interaction with these surfaces, which could eventually lead to the spread and transmission of potentially infectious agents. Another thing of note is the discharge of wastewater from the healthcare institutions to the environment without any treatment, thus exposing receiving aquatic bodies to antibiotic resistant organisms. This study calls for concerted efforts by relevant agencies to enforce the treatment of wastewater from healthcare settings before discharge and the effective disinfection of surfaces in hospitals to prevent a potential public health challenge.
Conflict of interest statement
The authors declare that they have no conflict of interest.
Acknowledgements
The authors are grateful to the healthcare institutions for granting access for sample collection and Mrs Adedolapo Victoria Idowu (nee Olaposi) for assisting with the typesetting and formatting of the manuscript.
Funding
The study received no extramural funding.
Authors’ contributions
Banjo OA and Adekanmbi AO developed the original idea and the protocols. All authors performed the experiments, and were involved in the collection of data. Banjo OA and Adekanmbi AO wrote the preliminary draft and analyzed the data. All authors read, revised and approved the manuscript for publication.
| References | | |
| 1. | Koganti S, Alhmidi H, Tomas ME, Cadnum JL, Jencson A, Donskey CJ. Evaluation of hospital floors as a potential source of pathogen dissemination using a nonpathogenic virus as a surrogate marker. Infect Control Hosp Epidemiol 2016; 37(11): 1374-1377.  |
| 2. | Flores-Carrero A, Labrador I, Paniz-Mondolfi A, Peaper DR, Towle D, Araque M. Nosocomial outbreak of extended-spectrum ß-lactamase-producing Enterobacter ludwigii co-harbouring CTX-M-8, SHV-12 and TEM-15 in a neonatal intensive care unit in Venezuela. J Glob Antimicrob Resist 2016; 7: 114-118. |
| 3. | Freeman S, Eddy SL, McDonough M, Smith MK, Okoroafor N, Jordt H, et al. Active learning increases student performance in science, engineering, and mathematics. Proc Natl Acad Sci U S A 2014; 111(23): 8410-8415. |
| 4. | Kramer S, Dibbern D, Moll J, Huenninghaus M, Koller R, Krueger D, et al. Resource partitioning between bacteria, fungi, and protists in the detritusphere of an agricultural soil. Front Microbiol. 2016; 7: 1524. |
| 5. | Dziri O, Dziri R, Salabi AAE, Chouchani C. Carbapenemase producing Gram-negative bacteria in Tunisia: History of thirteen years of challenge. Infect Drug Resist 2020; 13: 4177—4191. |
| 6. | Paluchowska P, Skalkowska M, Spelak A, Budak A. Occurrence of alert pathogens in hospital environment, Part I. ESBL-producing Enterobacteriaceae strains. Med Dosw Mikrobiol 2012; 64(1): 35-43. |
| 7. | Dancer SJ, Kirkpatrick P, Corcoran DS, Christison F, Farmer D, Robertson C. Approaching zero: Temporal effects of a restrictive antibiotic policy on hospital-acquired clostridium difficile, extended-spectrum ß-lactamase-producing coliforms and meticillin-resistant staphylococcus aureus. Int J Antimicrob Agents 2013; 41(2): 137-142. |
| 8. | |
| 9. | Adelowo OO, Ikhimiukor OO, Knecht C, Vollmers J, Bhatia M, Kaster AK. A survey of extended-spectrum beta-lactamase-producing Enterobacteriaceae in urban wetlands in southwestern Nigeria as a step towards generating prevalence maps of antimicrobial resistance. PLoS One 2020; 15(3): 22-29. |
| 10. | Zhang SC, Huang JQ, Zhao ZC, Cao YP, Li B. Hospital wastewater as a reservoir for antibiotic resistance genes: A meta-analysis. Front Pubi Health 2020; 8: 57-68. doi: 10.3389/fpubh.2020.574968. |
| 11. | Adelowo OO, Caucci S, Banjo OA, Nnanna OC, Awotipe EO, Peters FB. Extended spectrum beta-lactamase (ESBL)-producing bacteria isolated from hospital wastewaters, rivers and aquaculture sources in Nigeria. Environ Sci Pollut Res 2018; 25(3): 2744—2755. |
| 12. | Banjo OA, Adekanmbi AO, Oyelade AA. Occurrence of CTX-M, SHV and TEM ß-lactamase genes in extended spectrum beta-lactamase (ESBL)-producing bacteria recovered from wastewater of a privately-owned hospital in Nigeria and a hand-dug well within its vicinity. Gene Rep 2020; 21(1): 61-70. |
| 13. | Adekanmbi AO, Akinpelu MO, Olaposi AV, Oyelade AA. Extended spectrum beta-lactamase encoding gene-fingerprints in multidrug resistant Escherichia coli isolated from wastewater and sludge of a hospital treatment plant in Nigeria. Int J Environ Stud 2020; 78(1): 140-150. |
| 14. | Guet-Revillet H, Monnier AL, Breton N, Descamps P, Lecuyer H, Alaabouche I. Environmental contamination with extended-spectrum ß-lactamases: Is there any difference between Escherichia coli and Klebsiella spp? Am J Infect Control 2012; 40(9): 845-848. |
| 15. | Ogunsola FT, Mehtar S. Challenges regarding the control of environmental sources of contamination in healthcare settings in low-and middle-income countries-a narrative review. Antimicrob Resist Infect Control 2020; 9(1): 81. |
| 16. | Oluwagbemiga AO, Akinsete SJ, Ana GR. Building conditions and the risk of nosocomial infection from microbial contamination of hospital appliances in a health care facility. Int J Environ Health Res 2017; 27(4): 264-275. |
| 17. | Olowo-okere A, Ibrahim YKE, Babandina MM, Olayinka B. Multidrng resistant bacterial pathogens in the indoor air and floors of surgical wards in a university hospital. J Microbiol Infect Dis 2018; 8(3): 108-113. |
| 18. | |
| 19. | Janezic KJ, Ferry B, Hendricks EW, Janiga BA, Johnson T, Murphy S, et al. Phenotypic and genotypic characterization of Escherichia coli isolated from untreated surface waters. Open Microbiol J 2013; 7: 9-19. |
| 20. | Maynard C, Bekal S, Sanschagrin F, Levesque RC, Brousseau R, Masson L, et al. Heterogeneity among virulence and antimicrobial resistance gene profiles of extraintestinal Escherichia coli Isolates of animal and human origin. J Clin Microbiol 2004; 42(12): 5444-5452. |
| 21. | Mendonça N, Leitao J, Manageiro V, Ferreira E, Caniça M. Spread of extended-spectrum β-Lactamase CTX-M-producing Escherichia coli clinical isolates in community and nosocomial environments in Portugal, Antimicrob Agents Chemother 2007; 51(6): 1946-1955. |
| 22. | Kummerer K. Resistance in the environment. J Antimicrob Chemother 2004;54:311-320. |
| 23. | Grundmann H, Aires-de-Sousa M, Boyce T, Tiemersma JE. Emergence and resurgence of methicillin-resistant staphylococcus aureus as a public-health threat. Lancet 2006; 368(9538): 874-885. |
| 24. | Baquero F, Martinez JL, Canto'n R. Antibiotics and antibiotic resistance in water environments. Curr Opin Biotechnol 2008; 19(3): 260-265. |
| 25. | Ogbolu DO, Daini OA, Ogunledun A, Alli AO, Webber M A. High levels of multidrug resistance in clinical isolates of Gram-negative pathogens from Nigeria. Int J Antimicrob Agents 2011; 37(1): 62-66. |
| 26. | Adekanmbi AO, Akinpelu MO, Olaposi AV, Oyelade AA. Diversity of extended spectrum beta-lactamase (ESBL) genes in Escherichia coli isolated from wastewater generated by a sick bay located in a university health care facility. Gene Rep 2020; 20: 10-22. doi: 10.1016/j.genrep.2020.100738. |
| 27. | Gündo du A, Jennison AV, Smith HV, Stratton H, Katouli M. Extended-spectrum β-lactamase producing Escherichia coli in hospital wastewaters and sewage treatment plants in Queensland, Australia. Can J Microbiol 2013; 59(11): 737-745. |
| 28. | Zhao WH, Hu ZQ. Epidemiology and genetics of CTX-M extended-spectrum β-lactamases in Gram-negative bacteria. Crit Rev Microbiol 2013; 39(1): 79-101. |
| 29. | Mugnaioli C, Luzzaro F, Luca FD, Brigante G, Perilli M, Amicosante G, et al. CTX-M-type extended-spectrum β-Lactamases in Italy: Molecular epidemiology of an emerging countrywide problem. Antimicrob Agents Chemother 2006; 50(8): 2700-2706. |
| 30. | Diwan V, Chandran SP, Tamhankar AJ, Lundborg CS, Macaden R. Identification of extended-spectrum-beta lactamase and quinolone resistance genes in Escherichia coli isolated from hospital wastewater from central India. J Antimicrob Chemother 2012; 67(4): 857-859. |
| 31. | Chandran SP, Diwan V, Tamhankar AJ, Joseph BV, Rosales-Klintz S, Mundayoor S, et al. Detection of carbapenem resistance genes and cephalosporin, and quinolone resistance genes along with oqxAB gene in Escherichia coli in hospital wastewater: A matter of concern. J Appl Microbiol 2014; 117(4): 984-995. |
| 32. | Robin F, Beyrouthy R, Bonacorsi S, Aissa N, Bret L, Brieu N, et al. Inventory of extended spectrum-β-lactamase producing Enterobacteriaceae in France as assessed by a multicenter study. Antimicrob Agents Chemother 2017; 61(3): 1911-1916. |
| 33. | Lien LTQ, Lan PT, Chuc NTK, Hoa NQ, Nhung PH, Thoa NTM, et al. Antibiotic resistance and antibiotic resistance genes in Escherichia coli isolates from hospital wastewater in Vietnam. Int J Environ Res Public Health 2017; 14(7): 699. |
| 34. | Varela AR, Macedo GN, Nunes OC, Manaia CM, Genetic characterization of fluoroquinolone resistant Escherichia coli from urban streams and municipal and hospital effluents. FEMS Microbiol Ecol 2015; 91(5): fiv015. |
| 35. | Pouget JG, Coutinho FJ, Reid-Smith RJ, Boerlin P. Characterization of blaSHV genes on plasmids from Escherichia coli and Salmonella enterica isolates from Canadian food animals (2006-2007). Appl Environ Microbiol 2013; 79(12): 3864-3866. |
| 36. | Zurfluh K, Hachler H, Nuesch-Inderbinen M, Stephan R. Characteristics of extended-spectrum beta-lactamase and carbapenemase-producing Enterobacteriaceae isolates from rivers and lakes in Switzerland. Appi Environ Microbiol 2013; 79(9): 3021-3026. |
| 37. | Maravic A, Skocibusic M, Cvjetan S, Samanic I, Fredotovic Z, Puizina J. Prevalence and diversity of extended spectrum-beta-lactamase-producing Enterobacteriaceae from marine beach waters. Mar Pollut Bull 2015; 90(1-2): 60-67. |
| 38. | Sana T, Rami K, Racha B, Fouad D, Marcel A, Hassan M, et al. Detection of genes TEM, OXA, SHV and CTX-M in 73 clinical isolates of Escherichia coli producers of extended spectrum Beta-lactamases and determination of their susceptibility to antibiotics. Int Arabic J Antimicrob Agents 2011; 1(1): 1-6. |
| 39. | Getachew A, Guadu T, Tadie A, Gizaw Z, Gebrehiwot M, Cherkos DH, et al. Diarrhea prevalence and sociodemographic factors among under-five children in rural areas of North Gondar Zone, Northwest Ethiopia. Int J Pediatr 2018. doi: 10.1155/2018/6031594. eCollection 2018. |
| 40. | Dziri R, Klibi N, Alonso CA , Jouini A, Said LB, Chairat S, et al. Detection of CTX-M-15-producing Escherichia coli isolates of Lineages ST131-B2 and ST167-A in environmental samples of a Tunisian hospital. Microb Drug Resist 2016; 22(5): 399-403. |
| 41. | Matthew D, Dadah AJ, Mohammed SSD, Bacterial contamination of operating theatres: A case study of a hospital in Northern Nigeria. Sci World J 2020; 15 (2): 83-89. |
| 42. | Carattoli A, Miriagou V, Bertini A, Loli A, Colinon C, Villa L, et al. Replicon typing of plasmids encoding resistance to newer β-lactams. Emerg Infect Dis 2006; 12(7): 1145-1148. |
| 43. | Carattoli A. Resistance plasmid families in Enterobacteriaceae. Antimicrob Agents Chemother 2009; 53(6): 2227-2238. |
| 44. | Canton R, Gonzalez-Alba JM, Gala'n JC. CTX-M enzymes: Origin and diffusion. Front Microbiol 2012; 3: 110. |
| 45. | Hota B. Contamination, disinfection, and cross-colonization: Are hospital surfaces reservoirs for nosocomial infection? Clin Infect Dis 2004; 39(8): 1182-1189. |
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[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4]
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