Multidrug-resistant pathogens contaminate river water used in irrigation in disenfranchised communities

Marwan Osman; Dina Daaboul; Anahita Ghorbani Tajani; Khaled El Omari; Bledar Bisha; Jouman Hassan; Casey L Cazer; Kathryn J Fiorella; Nabil Karah; Aula Abbara; Monzer Hamze; Kevin J Cummings; Thierry Naas; Issmat I Kassem

doi:10.1016/j.jgar.2023.12.016

Multidrug-resistant pathogens contaminate river water used in irrigation in disenfranchised communities

J Glob Antimicrob Resist. 2024 Mar:36:175-180. doi: 10.1016/j.jgar.2023.12.016. Epub 2023 Dec 27.

Authors

Affiliations

¹ Department of Neurosurgery, Yale University School of Medicine, New Haven, Connecticut; Cornell Atkinson Center for Sustainability, Cornell University, Ithaca, New York; Department of Public and Ecosystem Health, College of Veterinary Medicine, Cornell University, Ithaca, New York. Electronic address: marwan.osman@yale.edu.
² Laboratoire Microbiologie Santé et Environnement (LMSE), Doctoral School of Sciences and Technology, Faculty of Public Health, Lebanese University, Tripoli, Lebanon; Team 'Resist' UMR1184, 'Immunology of Viral, Auto-Immune, Hematological and Bacterial diseases (IMVA-HB', INSERM, Université Paris-Saclay, CEA, LabEx LERMIT, Faculty of Medicine, Le Kremlin-Bicêtre, France.
³ Department of Animal Science, University of Wyoming, Laramie, Wyoming.
⁴ Laboratoire Microbiologie Santé et Environnement (LMSE), Doctoral School of Sciences and Technology, Faculty of Public Health, Lebanese University, Tripoli, Lebanon; Quality Control Center Laboratories at the Chamber of Commerce, Industry & Agriculture of Tripoli & North Lebanon, Tripoli, Lebanon.
⁵ Center for Food Safety and Department of Food Science and Technology, University of Georgia, Griffin, Georgia.
⁶ Department of Public and Ecosystem Health, College of Veterinary Medicine, Cornell University, Ithaca, New York; Department of Population Medicine & Diagnostic Sciences, Cornell University College of Veterinary Medicine, Ithaca, New York.
⁷ Department of Public and Ecosystem Health, College of Veterinary Medicine, Cornell University, Ithaca, New York.
⁸ Department of Molecular Biology and Umeå Centre for Microbial Research, Umeå University, Umeå, Sweden.
⁹ Department of Infection, Imperial College, St Marys Hospital, London, Syria Public Health Network, London, United Kingdom.
¹⁰ Laboratoire Microbiologie Santé et Environnement (LMSE), Doctoral School of Sciences and Technology, Faculty of Public Health, Lebanese University, Tripoli, Lebanon.
¹¹ Team 'Resist' UMR1184, 'Immunology of Viral, Auto-Immune, Hematological and Bacterial diseases (IMVA-HB', INSERM, Université Paris-Saclay, CEA, LabEx LERMIT, Faculty of Medicine, Le Kremlin-Bicêtre, France; Bacteriology-Hygiene Unit, Assistance Publique-Hôpitaux de Paris, AP-HP Paris-Saclay, Bicêtre Hospital Le Kremlin-Bicêtre, France; Associated French National Reference Center for Antibiotic Resistance: Carbapenemase-Producing Enterobacteriaceae, Le Kremlin-Bicêtre, France.

PMID: 38154747
DOI: 10.1016/j.jgar.2023.12.016

Abstract

Objectives: The contamination of fresh surface waters poses a significant burden on human health and prosperity, especially in marginalized communities with limited resources and inadequate infrastructure. Here, we performed in-depth genomic analyses of multidrug-resistant bacteria (MDR-B) isolated from Al-Oueik river water that is used for irrigation of agricultural fields in a disenfranchised area that also hosts a makeshift Syrian refugee camp.

Methods: A composite freshwater sample was filtered. Faecal coliforms were counted and extended spectrum cephalosporins and/or ertapenem resistant bacteria were screened. Isolates were identified using MALDI-TOF-MS and analysed using whole-genome sequencing (WGS) to identify the resistome, sequence types, plasmid types, and virulence genes.

Results: Approximately 10⁶ CFU/100 mL of faecal coliforms were detected in the water. Four drug-resistant Gram-negative bacteria were identified, namely Escherichia coli, Klebsiella pneumoniae, Enterobacter hormaechei, and Pseudomonas otitidis. Notably, the E. coli isolate harboured bla_NDM-5 and a YRIN-inserted PBP3, representing an emerging public health challenge. The K. pneumoniae isolate carried bla_SHV-187 as well as mutations in the gene encoding the OmpK37 porin. Enterobacter hormaechei and P. otitidis harboured bla_ACT-16 and bla_POM-1, respectively.

Conclusion: This report provides comprehensive genomic analyses of MDR-B in irrigation water in Lebanon. Our results further support that irrigation water contaminated with faecal material can be a reservoir of important MDR-B, which can spread to adjacent agricultural fields and other water bodies, posing both public health and food safety issues. Therefore, there is an urgent need to implement effective water quality monitoring and management programs to control the proliferation of antibiotic-resistant pathogens in irrigation water in Lebanon.

Keywords: Antimicrobial resistance; NDM-5; One Health; Refugee; River; Water quality.

MeSH terms

Enterobacter / genetics
Escherichia coli* / genetics
Gram-Negative Bacteria
Humans
Klebsiella pneumoniae / genetics
Plasmids / genetics
Rivers* / microbiology

Supplementary concepts

Enterobacter hormaechei