Assessment of well water as a reservoir for extended-spectrum β-lactamases (ESBL) and carbapenem resistant Enterobacteriaceae from Iwo, Osun state, Nigeria
-
Omowumi Temitayo Akinola
,
Faustina Uloma Onyeaghasiri
,
Olayinka Oluyemi Oluranti
,
Olayinka Oladapo Elutade
Abstract
Background and Objectives: Unsafe water supplies are of public health concern, especially in developing countries. This article aims to investigate the microbiological quality of water from eight Wells in Iwo and to explore for the extended-spectrum β-lactamase (ESBL) and carbapenemase genes contained in isolated enteric bacteria from in the water samples.
Materials and Methods: Bacterial isolation and identification were done using standard conventional methods. Antibiotic susceptibility testing was conducted using the Kirby–Bauer method. Ten phenotypically carbapenem-resistant isolates were further subjected to genotypic analysis (PCR amplification) for the detection of ESBL and carbapenemase gene.
Results: A total of 148 Enterobacteriaceae isolates belonging to seven (7) genera were isolated and identified which included E. coli, Enterobacter spp., Klebsiella spp., Salmonella, Citrobacter sp, Proteus, and Shigella. Results showed that 55% of isolates were resistant to tetracycline, 28% to cefepime, the least resistance was shown in moxifloxacin and gentamicin which had 6% and 9%, respectively, of the total isolates. For the two carbapenems used, results showed meropenem and imipenem had resistant values of 14% each, respectively. Two isolates carried the blaCTX-M gene while the carbapenemase gene (blaKPC, blaNDM, and blaOXA) was not detected in all the ten isolates.
Conclusion: There was also negative chromosomal detection of carbapenemase in MDR isolates from well waters in Iwo town. Consequently, resistance to carbapenem antibiotics in these isolates may not be mediated by carbapenemase but by the production of extended-spectrum β-lactamases and through other mechanisms of resistance.
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4. Khan N, Hussain ST, Saboor A. Physiochemical investigation of the drinking water sources from mardan, khyber Pakhtunkhwa, Pakistan. Int J Phys Sci 2013; 8: 1661-1671.
5. Stange C, Sidhu JPS, Tiehm A, Toze S. Antibiotic resistance and virulence genes in coliform water isolates. Int J Hyg Environ Health 2016; 219:823-831.
6. Adegoke AA, Madu CE, Aiyegoro OA, Stenström TA, Okoh AI. Antibiogram and beta-lactamase genes among cefotaxime resistant E. coli from wastewater treatment plant. Antimicrob Resist Infect Control 2020; 9: 46.
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9. Bengtsson-Palme J, Kristiansson E, Larsson DGJ. Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiol Rev 2018; 42:fux053.
10. Hana XM, Hub HW, Chenc QL, Yanga LY, Lia HL, Zhuc YG, et al. Antibiotic resistance genes and associated bacterial communities in agricultural soils amended with different sources of animal manures. Soil Biol Biochem 2018; 126: 91-102.
11. Read AF, Woods RJ. Antibiotic resistance management. Evol Med Public Health 2014; 2014: 147.
12. Purohit MR, Chandran S, Shah H, Olwan V, Jamhankar AJ, Lundborg CS. Antibiotic resistance in an Indian rural community: A 'One-Health' observational study on commensal coliform from humans, animals, and water. Int J Environ Res Public Health 2017; 14: 386.
13. Parvez S, Khan AU. Hospital sewage water: A reservoir for variants of New Delhi metallo-β-lactamase (NDM)-and extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae. Int J Antimicrob Agents 2017; 51: 82-88.
14. Khan AU, Nordmann P. Spread of carbapenemase NDM-1 producers: The situation in India and what may be proposed. Scand J Infect Dis 2012; 44: 531-535.
15. Marathe NP, Pal C, Gaikwad SS, Jonsson V, Kristiansson E, Larsson DGJ. Untreated urban waste contaminates Indian river sediments with resistance genes to last resort antibiotics. Water Res 2017; 124: 388-397.
16. Ogbolu DO, Webber MA. High level and novel mechanisms of carbapenem resistance in gram negative bacteria from tertiary hospitals in Nigeria. Int J Antimicrob Agents 2014; 43: 412-417.
17. Diab M, Hamze M, Bonnet R, Saras E, Madec JY, Haenni M. Extended-spectrum beta-lactamase (ESBL)- and carbapenemase-producing Enterobacteriaceae in water sources in Lebanon. Vet Microbiol 2018; 217: 97-103.
18. De Oliveira DMP, Forde BM, Kidd TJ, Harris PNA, Schembri MA, Beatson SA, et al. Antimicrobial resistance in ESKAPE pathogens. Clin Microbiol Rev 2020; 33(3): e00181-19.
19. Khan AU, Maryam L, Zarrilli R. Structure, genetics and worldwide spread of New Delhi metallo-β-lactamase (NDM): A threat to public health. BMC Microbiol 2017; 17: 101.
20. Cheesbrough M (1984). Medical manual for tropical countries. 2nd ed. Cambridge University Press. UK.
21. Haberecht HB, Nealon NJ, Gilliland JR, Holder AV, Runyan C, Oppel RC, et al. Antimicrobial-resistant Escherichia coli from environmental waters in northern Colorado. J Environ Public Health 2019: 2019:3862949.
22. Queipo-Ortuño MI, De Dios Colmenero J, Macias M, Bravo MJ, Morata P. Preparation of bacterial DNA template by boiling and effect of immunoglobulin G as an inhibitor in real-time PCR for serum sample from patients with Brucellosis. Clin Vaccine Immunol 2008; 15: 293-296.
23. Paterson DL, Hujer KM, Hujer AM, Yeiser B, Bonomo MD, Rice LB, et al. Extended-spectrum beta-lactamases in Klebsiella pneumoniae bloodstream isolates from seven countries: dominance and widespread prevalence of SHV- and CTX-M-type beta-lactamases. Antimicrob Agents Chemother 2003; 47: 3554-3560.
24. Edelstein M, Pimkin M, Palagin I, Edelstein I, Stratchounski L. Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals. Antimicrob Agents Chemother 2003; 47: 3724-3732.
25. Hujer KM, Hujer AM, Hulten EA, Bajaksouzian S, Adams JM, Donskey CJ, et al. Analysis of antibiotic resistance genes in multidrug-resistant Acinetobacter sp. isolates from military and civilian patients treated at the Walter reed army medical center. Antimicrob Agents Chemother 2006; 50: 4114-4123.
26. Hindiyeh M, Smollen G, Grossman Z, Ram D, Davidson Y, Mileguir F, et al. Rapid detection of blaKPC carbapenemase genes by real-time PCR. J Clin Microbiol 2008; 46: 2879-2883.
27. Abednego MM, Mbaruk AS, John NM, John MM. Water-borne bacterial pathogens in surface waters of Nairobi river and health implication to communities downstream Athi river. Int J Life Sci Pharma Res 2013; 3: L4-L10.
28. Thani TS, Symekher SM, Boga H, Oundo J. Isolation and characterization of Escherichia coli pathotypes and factors associated with well and boreholes water contamination in Mombasa County. Pan Afr Med J 2016; 23: 12.
29. Adesakin TA, Oyewale AT, Bayero U, Mohammed AN, Aduwo IA, Ahmed PZ, Abubakar ND, Barje IB. Assessment of bacteriological quality and physico-chemical parameters of domestic water sources in Samaru community, Zaria, Northwest Nigeria. Heliyon 2020; 6(8): e04773.
30. Farooq S, Hashmi I, Qazi IA, Qaiser S, Rasheed S. Monitoring of coliforms and chlorine residual in water distribution network of Rawalpindi, Pakistan. Environ Monit Assess 2008; 140: 339-347.
31. Cole D, Griffin PM, Fullerton KE, Ayers T, Smith K, Ingram LA, et al. Attributing sporadic and outbreak associated infections to sources: blending epidemiological data. Epidemiol Infect 2014; 142: 295-302.
32. Chalmer RM, Aird, H, Bolton FJ. Waterborne Escherichia coli 0157. Symp Ser Soc Appl Microbiol 2000; (29): 124S-132S.
33. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004; 2: 123-140.
34. Odonkor ST, Addo KK. Prevalence of Multidrug-Resistant Escherichia coli isolated from drinking water sources. Int J Microbiol 2018; 2018:7204013.
35. Jiang ZD, Lowe B, Verenkar MP, Ashley D, Steffen R, Tornieporth N. Prevalence of enteric pathogens among international travellers with diarrhea acquired in Kenya (Mombasa), India (Goa), or Jamaica (Montego Bay). J Infec Dis 2002; 185: 497-502.
36. Paterson DL. Resistance in gram-negative bacteria: Enterobacteriaceae. Am J Med 2006; 119(6 Suppl 1): S20-8; discussion S62-70.
37. Chamosa LS, Álvarez VE, Nardelli M, Quiroga MP, Cassini, MH, Centrón D. Lateral antimicrobial resistance genetic transfer is active in the open environment. Sci Rep 2017; 7: 513.
38. Hamelin K, Bruant G, El-Shaarawi A, Hill S, Edge TA, Bekal S, et al. Virulence and antimicrobial resistance DNA microarray detects a high frequency of virulence genes in Escherichia coli from Great Lakes recreational waters. Appl Environ Microbiol 2006; 72: 4200-4206.
39. Bonomo RA, Szabo D. Mechanisms of multidrug resistance in Acinetobacter species and Pseudomonas aeruginosa. Clin Infect Dis 2006; 43 Suppl 2: S49-56.
40. Mahmoud NE, Altayb HN, Gurashi RM. Detection of Carbapenem-Resistant genes in Escherichia coli isolated from drinking water in Khartoum, Sudan. J Environ Public Health 2020; 2020: 2571293.
41. Harmon DE, Miranda OA, McCarley A, Eshaghia M, Carlson N, Ruiz C. Prevalence and characterization of carbapenem-resistant bacteria in water bodies in the Los Angeles- Southern California area. Microbiologyopen 2019; 8(4): e00692.
42. Bonomo RA, Burd EM, Conly J, Limbago BM, Poirel L, Segre JA, et al. Carbapenemase-producing organisms: A global scourge. Clin Infect Dis 2018; 66: 1290-1297.
43. Rizek C, Fu L, Dos Santos LC, Leite G, Ramos J, Rossi F, et al. Characterization of carbapenem-resistant Pseudomonas aeruginosa clinical isolates, carrying multiple genes coding for this antibiotic resistance. Ann Clin Microbiol Antimicrob 2014; 13: 43.
44. Papp-Wallace, KM, Endimiani, A, Taracila, MA, Bonomo, RA Carbapenems: Past, present and future. Antimicrob Agents Chemother 2011; 55: 4943-4960.
45. de Oliveira Garcia D, Doi Y, Szabo D, Adams-Haduch JM, Vaz TM, Leite D, et al. Multiclonal outbreak of Klebsiella pneumoniae producing extended-spectrum β‐lactamase CTX‐M‐2 and novel variant CTX‐M‐59 in a neonatal intensive care unit in Brazil. Antimicrob Agents Chemother 2008; 52: 1790-1793.
46. Olowo-okere A, Ibrahim YKE, Olayinka BO, Ehinmidu, JO, Mohammed Y, Nabti LZ, et al. Phenotypic and genotypic characterization of clinical carbapenem-resistant Enterobacteriaceae isolates from Sokoto, northwest Nigeria. New Microbes New Infect 2020; 37: 100727.
47. Kinney CA, Heuvel BV. Translocation of pharmaceuticals and personal care products after land application of biosolids. Curr Opin Environ Sci Health 2020; 14: 23-30.
48. Koch N, Islam NF, Sonowal S, Prasad R, Sarma H. Environmental antibiotics and resistance genes as emerging contaminants: Methods of detection and bioremediation. Curr Res Microb Sci 2021; 2: 100027.
49. Bartrons, M, Peñuelas J. Pharmaceuticals and personal-care products in plants. Trends Plant Sci 2017; 22: 194-203.
50. Riaz L, Mahmood T, Khalid A, Rashid A, Ahmed Siddique MB, Kamal A, et al. Fluoroquinolones (FQs) in the environment: A review on their abundance, sorption and toxicity in soil. Chemosphere 2018; 191: 704-720.
51. Bengtsson-Palme J, Jonsson V, Heß S. What is the role of the environment in the emergence of novel antibiotic resistance genes? A modeling approach. Environ Sci Technol 2021; 55: 15734-15743.
2. WHO. European Strategic Workshop on Water Safety Planning: Key Outcomes, Berlin, Germany 2014. Berlin WSP workshop report_ FINAL (umweltbundesamt.de) Accessed date: 15 March 2020.
3. Pawari MJ, Gawande S. Ground water pollution and its consequence. Int J Eng Res Gen Sci 2015; 3: 773-776.
4. Khan N, Hussain ST, Saboor A. Physiochemical investigation of the drinking water sources from mardan, khyber Pakhtunkhwa, Pakistan. Int J Phys Sci 2013; 8: 1661-1671.
5. Stange C, Sidhu JPS, Tiehm A, Toze S. Antibiotic resistance and virulence genes in coliform water isolates. Int J Hyg Environ Health 2016; 219:823-831.
6. Adegoke AA, Madu CE, Aiyegoro OA, Stenström TA, Okoh AI. Antibiogram and beta-lactamase genes among cefotaxime resistant E. coli from wastewater treatment plant. Antimicrob Resist Infect Control 2020; 9: 46.
7. Momtaz H, Dehkordi FS, Hosseini MJ, Sarshar M, Heidari M. Serogroups, virulence genes and antibiotic resistance in Shiga toxin-producing Escherichia coli isolated from diarrheic and non-diarrheic pediatric patients in Iran. Gut Pathog 2013; 5: 39.
8. Adzitey F. Incidence and antimicrobial susceptibility of Escherichia coli isolated from beef (meat muscle, liver and kidney) samples in Wa Abattoir, Ghana. Cogent Food Agric 2020; 6: 1718269.
9. Bengtsson-Palme J, Kristiansson E, Larsson DGJ. Environmental factors influencing the development and spread of antibiotic resistance. FEMS Microbiol Rev 2018; 42:fux053.
10. Hana XM, Hub HW, Chenc QL, Yanga LY, Lia HL, Zhuc YG, et al. Antibiotic resistance genes and associated bacterial communities in agricultural soils amended with different sources of animal manures. Soil Biol Biochem 2018; 126: 91-102.
11. Read AF, Woods RJ. Antibiotic resistance management. Evol Med Public Health 2014; 2014: 147.
12. Purohit MR, Chandran S, Shah H, Olwan V, Jamhankar AJ, Lundborg CS. Antibiotic resistance in an Indian rural community: A 'One-Health' observational study on commensal coliform from humans, animals, and water. Int J Environ Res Public Health 2017; 14: 386.
13. Parvez S, Khan AU. Hospital sewage water: A reservoir for variants of New Delhi metallo-β-lactamase (NDM)-and extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae. Int J Antimicrob Agents 2017; 51: 82-88.
14. Khan AU, Nordmann P. Spread of carbapenemase NDM-1 producers: The situation in India and what may be proposed. Scand J Infect Dis 2012; 44: 531-535.
15. Marathe NP, Pal C, Gaikwad SS, Jonsson V, Kristiansson E, Larsson DGJ. Untreated urban waste contaminates Indian river sediments with resistance genes to last resort antibiotics. Water Res 2017; 124: 388-397.
16. Ogbolu DO, Webber MA. High level and novel mechanisms of carbapenem resistance in gram negative bacteria from tertiary hospitals in Nigeria. Int J Antimicrob Agents 2014; 43: 412-417.
17. Diab M, Hamze M, Bonnet R, Saras E, Madec JY, Haenni M. Extended-spectrum beta-lactamase (ESBL)- and carbapenemase-producing Enterobacteriaceae in water sources in Lebanon. Vet Microbiol 2018; 217: 97-103.
18. De Oliveira DMP, Forde BM, Kidd TJ, Harris PNA, Schembri MA, Beatson SA, et al. Antimicrobial resistance in ESKAPE pathogens. Clin Microbiol Rev 2020; 33(3): e00181-19.
19. Khan AU, Maryam L, Zarrilli R. Structure, genetics and worldwide spread of New Delhi metallo-β-lactamase (NDM): A threat to public health. BMC Microbiol 2017; 17: 101.
20. Cheesbrough M (1984). Medical manual for tropical countries. 2nd ed. Cambridge University Press. UK.
21. Haberecht HB, Nealon NJ, Gilliland JR, Holder AV, Runyan C, Oppel RC, et al. Antimicrobial-resistant Escherichia coli from environmental waters in northern Colorado. J Environ Public Health 2019: 2019:3862949.
22. Queipo-Ortuño MI, De Dios Colmenero J, Macias M, Bravo MJ, Morata P. Preparation of bacterial DNA template by boiling and effect of immunoglobulin G as an inhibitor in real-time PCR for serum sample from patients with Brucellosis. Clin Vaccine Immunol 2008; 15: 293-296.
23. Paterson DL, Hujer KM, Hujer AM, Yeiser B, Bonomo MD, Rice LB, et al. Extended-spectrum beta-lactamases in Klebsiella pneumoniae bloodstream isolates from seven countries: dominance and widespread prevalence of SHV- and CTX-M-type beta-lactamases. Antimicrob Agents Chemother 2003; 47: 3554-3560.
24. Edelstein M, Pimkin M, Palagin I, Edelstein I, Stratchounski L. Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals. Antimicrob Agents Chemother 2003; 47: 3724-3732.
25. Hujer KM, Hujer AM, Hulten EA, Bajaksouzian S, Adams JM, Donskey CJ, et al. Analysis of antibiotic resistance genes in multidrug-resistant Acinetobacter sp. isolates from military and civilian patients treated at the Walter reed army medical center. Antimicrob Agents Chemother 2006; 50: 4114-4123.
26. Hindiyeh M, Smollen G, Grossman Z, Ram D, Davidson Y, Mileguir F, et al. Rapid detection of blaKPC carbapenemase genes by real-time PCR. J Clin Microbiol 2008; 46: 2879-2883.
27. Abednego MM, Mbaruk AS, John NM, John MM. Water-borne bacterial pathogens in surface waters of Nairobi river and health implication to communities downstream Athi river. Int J Life Sci Pharma Res 2013; 3: L4-L10.
28. Thani TS, Symekher SM, Boga H, Oundo J. Isolation and characterization of Escherichia coli pathotypes and factors associated with well and boreholes water contamination in Mombasa County. Pan Afr Med J 2016; 23: 12.
29. Adesakin TA, Oyewale AT, Bayero U, Mohammed AN, Aduwo IA, Ahmed PZ, Abubakar ND, Barje IB. Assessment of bacteriological quality and physico-chemical parameters of domestic water sources in Samaru community, Zaria, Northwest Nigeria. Heliyon 2020; 6(8): e04773.
30. Farooq S, Hashmi I, Qazi IA, Qaiser S, Rasheed S. Monitoring of coliforms and chlorine residual in water distribution network of Rawalpindi, Pakistan. Environ Monit Assess 2008; 140: 339-347.
31. Cole D, Griffin PM, Fullerton KE, Ayers T, Smith K, Ingram LA, et al. Attributing sporadic and outbreak associated infections to sources: blending epidemiological data. Epidemiol Infect 2014; 142: 295-302.
32. Chalmer RM, Aird, H, Bolton FJ. Waterborne Escherichia coli 0157. Symp Ser Soc Appl Microbiol 2000; (29): 124S-132S.
33. Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol 2004; 2: 123-140.
34. Odonkor ST, Addo KK. Prevalence of Multidrug-Resistant Escherichia coli isolated from drinking water sources. Int J Microbiol 2018; 2018:7204013.
35. Jiang ZD, Lowe B, Verenkar MP, Ashley D, Steffen R, Tornieporth N. Prevalence of enteric pathogens among international travellers with diarrhea acquired in Kenya (Mombasa), India (Goa), or Jamaica (Montego Bay). J Infec Dis 2002; 185: 497-502.
36. Paterson DL. Resistance in gram-negative bacteria: Enterobacteriaceae. Am J Med 2006; 119(6 Suppl 1): S20-8; discussion S62-70.
37. Chamosa LS, Álvarez VE, Nardelli M, Quiroga MP, Cassini, MH, Centrón D. Lateral antimicrobial resistance genetic transfer is active in the open environment. Sci Rep 2017; 7: 513.
38. Hamelin K, Bruant G, El-Shaarawi A, Hill S, Edge TA, Bekal S, et al. Virulence and antimicrobial resistance DNA microarray detects a high frequency of virulence genes in Escherichia coli from Great Lakes recreational waters. Appl Environ Microbiol 2006; 72: 4200-4206.
39. Bonomo RA, Szabo D. Mechanisms of multidrug resistance in Acinetobacter species and Pseudomonas aeruginosa. Clin Infect Dis 2006; 43 Suppl 2: S49-56.
40. Mahmoud NE, Altayb HN, Gurashi RM. Detection of Carbapenem-Resistant genes in Escherichia coli isolated from drinking water in Khartoum, Sudan. J Environ Public Health 2020; 2020: 2571293.
41. Harmon DE, Miranda OA, McCarley A, Eshaghia M, Carlson N, Ruiz C. Prevalence and characterization of carbapenem-resistant bacteria in water bodies in the Los Angeles- Southern California area. Microbiologyopen 2019; 8(4): e00692.
42. Bonomo RA, Burd EM, Conly J, Limbago BM, Poirel L, Segre JA, et al. Carbapenemase-producing organisms: A global scourge. Clin Infect Dis 2018; 66: 1290-1297.
43. Rizek C, Fu L, Dos Santos LC, Leite G, Ramos J, Rossi F, et al. Characterization of carbapenem-resistant Pseudomonas aeruginosa clinical isolates, carrying multiple genes coding for this antibiotic resistance. Ann Clin Microbiol Antimicrob 2014; 13: 43.
44. Papp-Wallace, KM, Endimiani, A, Taracila, MA, Bonomo, RA Carbapenems: Past, present and future. Antimicrob Agents Chemother 2011; 55: 4943-4960.
45. de Oliveira Garcia D, Doi Y, Szabo D, Adams-Haduch JM, Vaz TM, Leite D, et al. Multiclonal outbreak of Klebsiella pneumoniae producing extended-spectrum β‐lactamase CTX‐M‐2 and novel variant CTX‐M‐59 in a neonatal intensive care unit in Brazil. Antimicrob Agents Chemother 2008; 52: 1790-1793.
46. Olowo-okere A, Ibrahim YKE, Olayinka BO, Ehinmidu, JO, Mohammed Y, Nabti LZ, et al. Phenotypic and genotypic characterization of clinical carbapenem-resistant Enterobacteriaceae isolates from Sokoto, northwest Nigeria. New Microbes New Infect 2020; 37: 100727.
47. Kinney CA, Heuvel BV. Translocation of pharmaceuticals and personal care products after land application of biosolids. Curr Opin Environ Sci Health 2020; 14: 23-30.
48. Koch N, Islam NF, Sonowal S, Prasad R, Sarma H. Environmental antibiotics and resistance genes as emerging contaminants: Methods of detection and bioremediation. Curr Res Microb Sci 2021; 2: 100027.
49. Bartrons, M, Peñuelas J. Pharmaceuticals and personal-care products in plants. Trends Plant Sci 2017; 22: 194-203.
50. Riaz L, Mahmood T, Khalid A, Rashid A, Ahmed Siddique MB, Kamal A, et al. Fluoroquinolones (FQs) in the environment: A review on their abundance, sorption and toxicity in soil. Chemosphere 2018; 191: 704-720.
51. Bengtsson-Palme J, Jonsson V, Heß S. What is the role of the environment in the emergence of novel antibiotic resistance genes? A modeling approach. Environ Sci Technol 2021; 55: 15734-15743.
| Files | ||
| Issue | Vol 14 No 3 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i3.9772 | |
| Keywords | ||
| Antibiotic resistance; Carbapenem; Enterobacteriaceae; Extended-spectrum β-lactamases; Nigeria; Water quality | ||
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How to Cite
1.
Akinola O, Onyeaghasiri F, Oluranti O, Elutade O. Assessment of well water as a reservoir for extended-spectrum β-lactamases (ESBL) and carbapenem resistant Enterobacteriaceae from Iwo, Osun state, Nigeria. Iran J Microbiol. 2022;14(3):351-361.
