A global multinational survey of cefotaxime-resistant coliforms in urban wastewater treatment plants

Marano, Roberto B. M.; Fernandes, Telma; Manaia, Célia M.; Nunes, Olga C.; Morrison, Donald A.; Berendonk, Thomas U.; Kreuzinger, Norbert; Telson, Tanel; Corno, Gianluca; Fatta‐Kassinos, Despo; Merlin, Christophe; Topp, Edward; Jurkevitch, Édouard; Henn, Leonie; Scott, Andrew; Heß, Stefanie; Slipko, Katarzyna; Laht, Mailis; Kisand, Veljo; Cesare, Andrea Di; Karaolia, Popi; Michael, Stella G.; Petre, Alice L.; Rosal, Roberto; Pruden, Amy; Riquelme, Virginia; Agüera, Ana; Esteban, Belén; Łuczkiewicz, Aneta; Kalinowska, Agnieszka; Leonard, Anne Frances Clare; Gaze, William H.; Adegoke, Agbabiaka Lukman; Stenström, Thor Axel; Pollice, Alfieri; Salerno, Carlo; Schwermer, Carsten Ulrich; Krzemiński, Paweł; Guilloteau, Hélène; Donner, Erica; Drigo, Barbara; Libralato, Giovanni; Guida, Marco; Bürgmann, Helmut; Beck, Karin; Garelick, Hemda; Tacão, Marta; Henriques, Isabel; Martínez‐Alcalá, Isabel; Guillén-Navarro, José Manuel; Popowska, Magdalena; Piotrowska, Monika Joanna; Quintela-Baluja, Marcos; Bunce, Joshua T.; Polo-López, María Inmaculada; Nahim–Granados, Samira; Pons, Marie‐Noëlle; Milaković, Milena; Udikovic-Kolic, Nikolina; Ory, Jérôme; Ousmane, Traore; Caballero, Pilar Calvo; Oliver, A. J.; Rodríguez-Mozaz, Sara; Balcázar, José Luís; Jäger, Thomas; Schwartz, Thomas; Yang, Ying; Zou, Shichun; Lee, Yunho; Yoon, Younggun; Herzog, Bastian; Mayrhofer, Heidrun; Prakash, Om; Nimonkar, Yogesh; Heath, Ester; Baraniak, Anna; Abreu-Silva, Joana; Choudhury, Manika; Muñoz, Leonardo Pantoja; Križanović, Stela; Brunetti, Gianluca; Maile-Moskowitz, Ayella; Brown, Connor

doi:10.1016/j.envint.2020.106035

Cited by 68 publications

(42 citation statements)

References 47 publications

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“…As such many countries are now implementing national surveillance programs, which cover both clinical and veterinary settings. However, few such schemes appear to exist for monitoring AMR in environmental or aquatic settings (Marano et al ., 2020). The WHO have developed and recommended the Tricycle Programme as a mechanism to collect harmonised data on prevalence of ESBL producing E. coli from different sectors, including the environment (Matheu et al ., 2017).…”

Section: Discussionmentioning

confidence: 99%

Establishing a marine monitoring programme to assess antibiotic resistance: a case study from the Gulf Cooperation Council (GCC) region

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et al. 2022

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The World Health Organization considers antimicrobial resistance as one of the most pressing global issues which poses a fundamental threat to human health, development, and security. Due to demographic and environmental factors, the marine environment of the Gulf Cooperation Council (GCC) region may be particularly susceptible to the threat of antimicrobial resistance. However, there is currently little information on the presence of AMR in the GCC marine environment to inform the design of appropriate targeted surveillance activities. The objective of this study was to develop, implement and conduct a rapid regional baseline monitoring survey of the presence of AMR in the GCC marine environment, through the analysis of seawater collected from high-risk areas across four GCC states: (Bahrain, Oman, Kuwait, and the United Arab Emirates). 560 Escherichia coli strains were analysed as part of this monitoring programme between December 2018 and May 2019. Multi-drug resistance (resistance to three or more structural classes of antimicrobials) was observed in 32.5% of tested isolates. High levels of reduced susceptibility to ampicillin (29.6%), nalidixic acid (27.9%), tetracycline (27.5%), sulfamethoxazole (22.5%) and trimethoprim (22.5%) were observed. Reduced susceptibility to the high priority critically important antimicrobials: azithromycin (9.3%), ceftazidime (12.7%), cefotaxime (12.7%), ciprofloxacin (44.6%), gentamicin (2.7%) and tigecycline (0.5%), was also noted. A subset of 173 isolates was whole genome sequenced, and high carriage rates of qnrS1 (60/173) and blaCTX-M-15 (45/173) were observed, correlating with reduced susceptibility to the fluoroquinolones and third generation cephalosporins, respectively. This study is important because of the resistance patterns observed, the demonstrated utility in applying genomic-based approaches to routine microbiological monitoring, and the overall establishment of a transnational AMR surveillance framework focussed on coastal and marine environments.

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Section: Discussionmentioning

confidence: 99%

Establishing a marine monitoring programme to assess antibiotic resistance: a case study from the Gulf Cooperation Council (GCC) region

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Baker‐Austin

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et al. 2022

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“…Escherichia stood out in this study both as having the most ARG connections on assembled contigs in common with local antibiogram data and tending to increase in relative abundance in the effluent. Extended-spectrum beta-lactamase producing E. coli are regularly isolated from treated wastewater effluent globally and are being considered by the World Health Organization (2021) and others as a standardized monitoring target for antibiotic resistance in wastewater ( Diallo et al, 2013 ; Bréchet et al, 2014 ; Li et al, 2019 ; Marano et al, 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Evaluation of Metagenomic-Enabled Antibiotic Resistance Surveillance at a Conventional Wastewater Treatment Plant

et al. 2021

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Wastewater treatment plants (WWTPs) receive a confluence of sewage containing antimicrobials, antibiotic resistant bacteria, antibiotic resistance genes (ARGs), and pathogens and thus are a key point of interest for antibiotic resistance surveillance. WWTP monitoring has the potential to inform with respect to the antibiotic resistance status of the community served as well as the potential for ARGs to escape treatment. However, there is lack of agreement regarding suitable sampling frequencies and monitoring targets to facilitate comparison within and among individual WWTPs. The objective of this study was to comprehensively evaluate patterns in metagenomic-derived indicators of antibiotic resistance through various stages of treatment at a conventional WWTP for the purpose of informing local monitoring approaches that are also informative for global comparison. Relative abundance of total ARGs decreased by ∼50% from the influent to the effluent, with each sampling location defined by a unique resistome (i.e., total ARG) composition. However, 90% of the ARGs found in the effluent were also detected in the influent, while the effluent ARG-pathogen taxonomic linkage patterns identified in assembled metagenomes were more similar to patterns in regional clinical surveillance data than the patterns identified in the influent. Analysis of core and discriminatory resistomes and general ARG trends across the eight sampling events (i.e., tendency to be removed, increase, decrease, or be found in the effluent only), along with quantification of ARGs of clinical concern, aided in identifying candidate ARGs for surveillance. Relative resistome risk characterization further provided a comprehensive metric for predicting the relative mobility of ARGs and likelihood of being carried in pathogens and can help to prioritize where to focus future monitoring and mitigation. Most antibiotics that were subject to regional resistance testing were also found in the WWTP, with the total antibiotic load decreasing by ∼40–50%, but no strong correlations were found between antibiotics and corresponding ARGs. Overall, this study provides insight into how metagenomic data can be collected and analyzed for surveillance of antibiotic resistance at WWTPs, suggesting that effluent is a beneficial monitoring point with relevance both to the local clinical condition and for assessing efficacy of wastewater treatment in reducing risk of disseminating antibiotic resistance.

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“…The final treated wastewater is discharged into Lake Michigan within the Milwaukee Bay area (43.02329162715021, −87.89408612678749). Similar to a global analysis of disinfected WW effluents [ 22 ], no CTX-resistant E. coli isolates were identified in post-chlorinated WW effluents. The 69 E. coli isolates were tested for resistance against twelve different antibiotics.…”

Section: Resultsmentioning

confidence: 68%

Similarities in Virulence and Extended Spectrum Beta-Lactamase Gene Profiles among Cefotaxime-Resistant Escherichia coli Wastewater and Clinical Isolates

et al. 2022

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The World Health Organization has identified antibiotic resistance as one of the largest threats to human health and food security. In this study, we compared antibiotic resistance patterns between ESBL-producing Escherichia coli from human clinical diseases and cefotaxime-resistant environmental strains, as well as their potential to be pathogenic. Antibiotic susceptibility was tested amongst clinical isolates (n = 11), hospital wastewater (n = 22), and urban wastewater (n = 36, both influent and treated effluents). Multi-drug resistance predominated (>70%) among hospitalwastewater and urban wastewater influent isolates. Interestingly, isolates from clinical and urban treated effluents showed similar multi-drug resistance rates (~50%). Most hospital wastewater isolates were Phylogroup A, while clinical isolates were predominately B2, with a more diverse phylogroup population in urban wastewater. ESBL characterization of cefotaxime-resistant populations identified blaCTX-M-1 subgroup as the most common, whereby blaKPC was more associated with ceftazidime and ertapenem resistance. Whole-genome sequencing of a carbapenemase-producing hospital wastewater E. coli strain revealed plasmid-mediated blaKPC-2. Among cefotaxime-resistant populations, over 60% of clinical and 30% of treated effluent E. coli encoded three or more virulence genes exhibiting a pathogenic potential. Together, the similarity among treated effluent E. coli populations and clinical strains suggest effluents could serve as a reservoir for future multi-drug resistant E. coli clinical infections.

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A global multinational survey of cefotaxime-resistant coliforms in urban wastewater treatment plants

Cited by 68 publications

References 47 publications

Establishing a marine monitoring programme to assess antibiotic resistance: a case study from the Gulf Cooperation Council (GCC) region

Establishing a marine monitoring programme to assess antibiotic resistance: a case study from the Gulf Cooperation Council (GCC) region

Evaluation of Metagenomic-Enabled Antibiotic Resistance Surveillance at a Conventional Wastewater Treatment Plant

Similarities in Virulence and Extended Spectrum Beta-Lactamase Gene Profiles among Cefotaxime-Resistant Escherichia coli Wastewater and Clinical Isolates

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