Volume 12, Issue 2 (6-2024)                   JoMMID 2024, 12(2): 110-120 | Back to browse issues page

XML Print

Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
AGBO O, Momoh M, Odimegwu D, Adonu C. Colistin Resistance in WHO-Designated Global Priority Pathogens Isolated from Wastewater Effluents of Two Hospitals in Enugu Metropolis, South East Nigeria. JoMMID 2024; 12 (2) :110-120
URL: http://jommid.pasteur.ac.ir/article-1-659-en.html
Colistin Resistance in WHO-Designated Global Priority Pathogens Isolated from Wastewater Effluents of Two Hospitals in Enugu Metropolis, South East Nigeria
Oluchi AGBO * , Mumuni Momoh , Damian Odimegwu , Cyril Adonu
Department of Pharmaceutics, University of Nigeria, Nsukka, PMB 410001, Enugu State, Nigeria
Abstract:   (237 Views)
Introduction: Hospitals are breeding grounds for multidrug-resistant (MDR) bacteria, posing treatment challenges and increasing the risk of spreading "superbugs." This study investigates the prevalence of colistin-resistant bacteria, a last-resort antibiotic, in wastewater from tertiary hospitals in Enugu, Nigeria. Methods: Twenty wastewater samples were collected over three months from two tertiary hospitals in Enugu. A standardized protocol by the American Public Health Association (APHA) was followed. Samples were collected aseptically from key drainage points and transported to the lab within 2 hours. Bacteria were isolated using the pour-plate method and characterized by morphological and biochemical tests, including Catalase, Oxidase, and Glucose Fermentation. Antibiotic susceptibility was assessed using Kirby-Bauer disc diffusion, and colistin resistance was confirmed via broth microdilution. Multiplex PCR detected mcr genes indicating plasmid-mediated resistance. Data were analyzed using SPSS version 23 with Chi-Square and ANOVA tests at a significance level of P < 0.05. Results: Gram-negative bacteria were isolated from 63.1% of samples, with Klebsiella spp. being the most prevalent, accounting for 24.6%. Colistin resistance was phenotypically observed in E. coli (83%), Klebsiella spp. (75%), and Pseudomonas aeruginosa (100%). Genotypically, E. coli harbored mcr-1 (17%) and mcr-3 (83%), while all Klebsiella and Pseudomonas isolates carried multiple mcr genes. Additionally, these bacteria showed resistance to multiple antibiotics, including Septrin, Gentamycin, and Ceftriaxone. Conclusion: The significant presence of colistin-resistant bacteria, especially E. coli and Klebsiella, poses a public health concern, potentially leading to treatment failures and spreading resistance genes. Stricter monitoring of hospital wastewater is necessary to identify emerging resistance trends and improve antibiotic practices in hospitals.
Keywords: Colistin resistance, Antibiotic resistance, Enterobacteriaceae, Hospital wastewater, mcr-1 gene, mcr-2 gene, mcr-3 gene, Multidrug resistance, Nigeria
Full-Text [PDF 1202 kb]   (59 Downloads)    
Type of Study: Original article | Subject: Anti-microbial agents, resistance and treatment protocols
Received: 2024/04/6 | Accepted: 2024/09/20 | Published: 2024/09/18
References
1. Sabri NA, Schmitt H, Van der Zaan B, Gerritsen HW, Zuidema T, Rijnaarts HHM, et al. Prevalence of antibiotics and antibiotic resistance genes in a wastewater effluent-receiving river in the Netherlands. J Environ Chem Eng. 2018; 8 (1). [DOI:10.1016/j.jece.2018.03.004]
2. Kamaruzzaman NF, Tan LP, Hamdan RH, Choong SS, Wong WK, Gibson AJ, et al. Antimicrobial Polymers: The Potential Replacement of Existing Antibiotics? Int J Mol Sci 2019; 20 (11): 2747. [DOI:10.3390/ijms20112747]
3. Murray CJ, Ikuta KS, Sharara F, Swetschinski L, Aguilar GR, Gray A, et al. Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. Lancet. 2022; 399 (10325): 629- 55. [DOI:10.1016/S0140-6736(21)02724-0]
4. Sakkas H, Bozidis P, Ilia A, Mpekoulis G. Antimicrobial Resistance in Bacterial Pathogens and Detection of Carbapenemases in Klebsiella pneumoniae Isolates from Hospital Wastewater. Antibiotics. 2019; 8 (85): 85. [DOI:10.3390/antibiotics8030085]
5. Bhagirath A, Yangi L, Patidar R, Yerex K, Ma X, Kumar A, et al. Two Component Regulatory Systems and Antibiotic Resistance in Gram-Negative Pathogens. Int J Mol Sci. 2019; 20 (7): 1781. [DOI:10.3390/ijms20071781]
6. Parvez S, Khan A. 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. 2018; 51: 82-8. [DOI:10.1016/j.ijantimicag.2017.08.032]
7. Galvin S, Boyle F, Hickey P, Vellinga A, Morris D, Cormican M. Enumeration and characterization of antimicrobial-resistant Escherichia coli bacteria in effluent from municipal, hospital, and secondary treatment facility sources. Appl Environ Microbiol. 2010; 76 (14): 4772-9. [DOI:10.1128/AEM.02898-09]
8. Picão RC, Cardoso JP, Campana EH, Nicoletti AG, Petrolini FVB, Assis DM, et al. The route of antimicrobial resistance from the hospital effluent to the environment: Focus on the occurrence of KPC-producing Aeromonas spp.. and Enterobacteriaceae in sewage. Diagn Microbiol Infect Dis. 2013; 76 (1): 80-5. [DOI:10.1016/j.diagmicrobio.2013.02.001]
9. World Health Organization. AWARE Classification antibiotics. Available At: https://www.who.int/news/item/01-10-2019-who-releases-the-2019-aware- classification-antibiotics (accessed March 2024).
10. Sib E, Lenz-plet F, Barabasch V, Savin M, Hembach N, Schallenberg A, et al. Bacteria isolated from hospital, municipal and slaughterhouse wastewaters show characteristic, different resistance profiles. Sci Total Environ. 2020; 746: 140894. [DOI:10.1016/j.scitotenv.2020.140894]
11. WHO. Critically important antimicrobials for human medicine, 6th revision. Available from https://www.who.int/foodsafety/publications/antimicrobials-sixth/en/. 2019 (accessed March 2024)
12. Jovcic B, Novovic K, Dekic S, Hrenovic J. Colistin Resistance in Environmental Isolates of Acinetobacter baumannii. Microb Drug Resist. 2021; 27 (3): 328-36. [DOI:10.1089/mdr.2020.0188]
13. Falagas ME, Kasiakou SK. Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clin Infect Dis. 2005; 40 (9): 1333-41. [DOI:10.1086/429323]
14. Bialvaei ZA, Kafil SH. Colistin, mechanisms and prevalence of resistance. Curr Med Res Opin. 2015; 31 (4): 707-21. [DOI:10.1185/03007995.2015.1018989]
15. Sun J, Zhang H, Liu YH, Feng Y. Towards understanding MCR-like colistin resistance. Trends Microbiol. 2018; 26 (9): 794-808. [DOI:10.1016/j.tim.2018.02.006]
16. Deris ZZ, Akter J, Sivanesan S, Roberts KD, Thompson PE, Nation RL, et al. A secondary mode of action of polymyxins against Gram-negative bacteria involves the inhibition of NADH-quinone oxidoreductase activity. J Antibiot (Tokyo). 2014; 67 (2): 147-51. [DOI:10.1038/ja.2013.111]
17. Abavisani M, Bostanghadiri N, Ghahramanpour H, Kodori M, Akrami F, Fathizadeh H, et al. Colistin resistance mechanisms in Gram-negative bacteria: A Focus on Escherichia coli. Letters Appl Microbiol. 2023; 76 (2): ovad023. [DOI:10.1093/lambio/ovad023]
18. Cheesbrough M. District Laboratory Practice in Tropical Countries. Part 2. 2nd ed. Cambridge: Cambridge University Press; 2000. p. 157-9.
19. Oli AN, Ogbuagu VI, Ejikeugwu CP, Iroha IR, Ugwu MC, Ofomata CM, et al. Multi-Antibiotic Resistance and Factors Affecting Carriage of Extended Spectrum β -Lactamase-Producing Enterobacteriaceae in Pediatric Population of Enugu Metropolis, Nigeria. Med Sci. 2019; 7: 104-16. [DOI:10.3390/medsci7110104]
20. Mangal S, Park H, Zeng L, Yu HH, Lin YW, Velkov T, et al. Composite particle formulations of colistin and meropenem with improved in-vitro bacterial killing and aerosolization for inhalation. Int J Pharm. 2018; 548 (1): 443-53. [DOI:10.1016/j.ijpharm.2018.07.010]
21. Hedges AJ. Estimating the precision of serial dilutions and viable bacterial counts. Int J Food Microbiol. 2002; 76 (3): 207-14. [DOI:10.1016/S0168-1605(02)00022-3]
22. Fawole M, Oso B. Characterization of bacteria: In: Laboratory Manual of Microbiology. Spectrum Book Ltd, Ibadan, Nigeria. 2004; 24-45.
23. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testing, 27th ed.; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2017.
24. European Committee on Antimicrobial Susceptibility Testing (EUCAST) breakpoint tables for interpretation of MICs and zone diameters, 2020; version 10.0.
25. Aldous WK, Pounder JI, Cloud JL, Woods GL. Comparison of six methods of extracting Mycobacterium tuberculosis DNA from processed sputum for testing by quantitative real-time PCR. J Clin Microbiol, 2005; 43 (5): 2471-3. [DOI:10.1128/JCM.43.5.2471-2473.2005]
26. Rebelo AR, Bortolaia V, Kjeldgaard JS, Pedersen SK, Leekitcharoenphon P, Hansen IM, et al. Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Euro Surveill. 2018; 23 (6): 17-00672. [DOI:10.2807/1560-7917.ES.2018.23.6.17-00672]
27. Ma F, Shen C, Zheng X, Liu Y, Chen H, Zhong L, et al. Identification of a novel plasmid carrying mcr-4.3 in an Acinetobacter baumannii strain in China. Antimicrob Agents Chemother. 2019; 63 (6): e00133-19. [DOI:10.1128/AAC.00133-19]
28. Mcgann P, Snesrud E, Maybank R, Corey B, Ong AC, Clifford R, et al. Escherichia coli Harboring mcr-1 and bla CTX-M on a Novel IncF Plasmid: First Report of mcr-1 in the United States. Antimicrob Agents Chemother. 2016, 60 (7): 4420-1. [DOI:10.1128/AAC.01103-16]
29. Villar HE, Baserni MN, Jugo MB. Faecal contamination of recreational freshwaters in Buenos Aires, Argentina. Water Sci Technol, 2018; 48: 233-8.
30. Li B, Zhang Y, Wei J, Shao D, Liu K, Shi Y, et al. Characterization of a novel small plasmid carrying the florfenicol resistance gene floR in Haemophilus parasuis. J Antimicrob Chemother. 2015; 70 (11): 3159-61. [DOI:10.1093/jac/dkv230]
31. Savin M, Bierbaum G, Hammerl JA, Heinemann C, Parcina M, Sib E. Antibiotic-resistant bacteria and antimicrobial residues in wastewater and process water from German pig slaughterhouses and their receiving municipal wastewater treatment plants. Sci Total Environ. 2020; 727: 138788. [DOI:10.1016/j.scitotenv.2020.138788]
32. Manges AR, Geum HM, Guo A, Edens TJ, Fibke CD, Pitout JDD. Global Extraintestinal Pathogenic Escherichia coli (ExPEC) Lineages. Clin Microbiol Rev. 2019; 32 (3): e00135-18. [DOI:10.1128/CMR.00135-18]
33. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev. 2015; 28 (3): 603-61. [DOI:10.1128/CMR.00134-14]
34. Berendonk TU, Manaia CM, Merlin C, Kassinos DF, Cytryn E, Walsh F, et al. Tackling antibiotic resistance: the environmental framework. Nat Rev Microbiol, 2015; 13 (5): 310-7. [DOI:10.1038/nrmicro3439]
35. Olaitan AO, Morand S, Rolain JM. Mechanisms of polymyxin resistance: acquired and intrinsic resistance in bacteria. Front Microbiol. 2014; 5: 643. [DOI:10.3389/fmicb.2014.00643]
36. Rice LB. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE. J Infect Dis. 2008; 197 (8): 1079-81. [DOI:10.1086/533452]
37. Tacconelli E, Carrara E, Savoldi A. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis. 2018; 18 (3): 318-27. [DOI:10.1016/S1473-3099(17)30753-3]
38. Yang P, Chen Y, Jiang S, Shen P, Lu X, Xiao Y. Association between the rate of fluoroquinolones-resistant gram-negative bacteria and antibiotic consumption from China based on 145 tertiary hospitals data in 2014. BMC Infect Dis. 2020; 20 (1): 269. [DOI:10.1186/s12879-020-04981-0]
39. Du H, Chen L, Tang YW, Kreiswirth BN. The emergence of the mcr-1 colistin resistance gene in carbapenem-resistant Enterobacteriaceae. Lancet Infect Dis. 2016; 18 (3): 287-8. [DOI:10.1016/S1473-3099(16)00056-6]
40. Fernandes MR, McCulloch JA, Vianello MA, Moura Q, Pérez-Chaparro PJ, Esposito F. First report of the globally disseminated IncX4 plasmid carrying the mcr-1 gene in a colistin-resistant Escherichia coli sequence type 101 isolate from a human infection in Brazil. Antimicrob Agents Chemother. 2016; 60 (10): 6415-7. [DOI:10.1128/AAC.01325-16]
Add your comments about this article : Your username or Email:
CAPTCHA
Send email to the article author

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.