Population-level surveillance of antibiotic resistance in Escherichia coli through sewage analysis

Hutinel, Marion; Huijbers, P.M.C.; Fick, Jerker; Åhrén, Christina; Larsson, D. G. Joakim; Flach, Carl-Fredrik

doi:10.2807/1560-7917.es.2019.24.37.1800497

Cited by 87 publications

(72 citation statements)

References 35 publications

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“…Traditionally, microbiological water quality is assessed based on coliforms analyses, a method still used widely throughout the world [25,26,27]. Coliforms are thus a target of interest for standardized antibiotic resistance monitoring (Marano et al, in preparation; [28]). Major advantages include feasibility of implementation, low technical requirements, and potential for global data comparability.…”

Section: Introductionmentioning

confidence: 99%

Comparison of Culture- and Quantitative PCR-Based Indicators of Antibiotic Resistance in Wastewater, Recycled Water, and Tap Water

Rocha

Fernandes

Riquelme

et al. 2019

IJERPH

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Standardized methods are needed to support monitoring of antibiotic resistance in environmental samples. Culture-based methods target species of human-health relevance, while the direct quantification of antibiotic resistance genes (ARGs) measures the antibiotic resistance potential in the microbial community. This study compared measurements of tetracycline-, sulphonamide-, and cefotaxime-resistant presumptive total and fecal coliforms and presumptive enterococci versus a suite of ARGs quantified by quantitative polymerase chain reaction (qPCR) across waste-, recycled-, tap-, and freshwater. Cross-laboratory comparison of results involved measurements on samples collected and analysed in the US and Portugal. The same DNA extracts analysed in the US and Portugal produced comparable qPCR results (variation <28%), except for blaOXA-1 gene (0%–57%). Presumptive total and fecal coliforms and cefotaxime-resistant total coliforms strongly correlated with blaCTX-M and intI1 (0.725 ≤ R2 ≤ 0.762; p < 0.0001). Further, presumptive total and fecal coliforms correlated with the Escherichia coli-specific biomarkers, gadAB, and uidA, suggesting that both methods captured fecal-sourced bacteria. The genes encoding resistance to sulphonamides (sul1 and sul2) were the most abundant, followed by genes encoding resistance to tetracyclines (tet(A) and tet(O)) and β-lactams (blaOXA-1 and, blaCTX-M), which was in agreement with the culture-based enumerations. The findings can help inform future application of methods being considered for international antibiotic resistance surveillance in the environment.

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Section: Introductionmentioning

confidence: 99%

Comparison of Culture- and Quantitative PCR-Based Indicators of Antibiotic Resistance in Wastewater, Recycled Water, and Tap Water

Rocha

Fernandes

Riquelme

et al. 2019

IJERPH

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“…The same associations and high levels of FIB, AMR bacteria, and ARGs were not observed in municipal wastewater absent of hospital waste [103]. Similarly, in a study of Swedish sewage samples, Hutinel et al [107] reported a higher variability in resistance rates in hospital sewage than in municipal sewage, indicating that antibiotics in hospital sewage might reach concentrations capable of selecting for resistant bacteria in sewer pipes.…”

Section: Medical Wastementioning

confidence: 69%

“…(1) treated by municipal WWTPs (i.e., hospital is an indirect discharger) [101,102]; (2) treated by onsite treatment systems [97,103]; and (3) with no treatment at all prior to discharge (i.e., direct discharger) to surface water [24,97,102]. Antibiotics and antibiotic residues can enter municipal wastewater influent through pharmaceutical disposal, urine and feces from patients treated with pharmaceuticals and from antimicrobials used for cleaning surfaces or washing hands or clothes [104][105][106][107]. Raw sewage may be blended with pre-treated and/or raw medical waste, creating a hotspot for the transfer of ARGs [40].…”

Section: Medical Wastementioning

confidence: 99%

Antibiotic Resistance in Recreational Waters: State of the Science

Nappier

Liguori

Ichida

et al. 2020

IJERPH

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Ambient recreational waters can act as both recipients and natural reservoirs for antimicrobial resistant (AMR) bacteria and antimicrobial resistant genes (ARGs), where they may persist and replicate. Contact with AMR bacteria and ARGs potentially puts recreators at risk, which can thus decrease their ability to fight infections. A variety of point and nonpoint sources, including contaminated wastewater effluents, runoff from animal feeding operations, and sewer overflow events, can contribute to environmental loading of AMR bacteria and ARGs. The overall goal of this article is to provide the state of the science related to recreational exposure and AMR, which has been an area of increasing interest. Specific objectives of the review include (1) a description of potential sources of antibiotics, AMR bacteria, and ARGs in recreational waters, as documented in the available literature; (2) a discussion of what is known about human recreational exposures to AMR bacteria and ARGs, using findings from health studies and exposure assessments; and (3) identification of knowledge gaps and future research needs. To better understand the dynamics related to AMR and associated recreational water risks, future research should focus on source contribution, fate and transport—across treatment and in the environment; human health risk assessment; and standardized methods.

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“…For culture-based studies the evaluation of overlap between wastewater and human isolates is limited to comparisons of phenotypic AMR profiles, which may reflect significant differences in underlying genotypes, particularly for Gram-negative organisms such as Enterobacterales. Most studies 25,28,32,34,35 showed AMR prevalence in wastewater was lower, but common AMR phenotypes were frequently shared, indicating culture/phenotype-based surveillance of wastewater may be useful for low-resolution monitoring of AMR in clinical isolates. Targeted culture-based approaches could also pick up relevant high-risk drugresistant clones (MRSA, VRE, CRE, MDR-Salmonella Typhimurium DT104) 26,27,29,35 .…”

Section: Discussionmentioning

confidence: 99%

Wastewater Surveillance of Antimicrobial Resistance in Human Populations: A Systematic Review

Chau¹,

Barker²,

Sims³

et al. 2020

Preprint

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Wastewater-based surveillance of antimicrobial resistance (AMR) may facilitate convenient monitoring of population-level AMR prevalence without the healthcare-associated bias and data collection restrictions inherent to clinically oriented systems. However, differences in study design and methodology likely contribute to differences in outcomes and interpretation, limiting reproducibility, reliability and meta-analysis. We therefore systematically reviewed studies using wastewater for AMR surveillance in human populations to identify optimal practices to detect wastewater-human AMR correlations. We evaluated 7,063 records and 174 full-text methods in a two-stage screen; 20 studies were included. Risk of bias assessment divided studies into high-risk (n=3), low-risk (n=3) and unclear-risk (n=14). Most studies detected wastewater-human AMR correlations (n=15) but only six studies identified statistically significant associations, most via culture-independent approaches (n=5). Genomic approaches also facilitated higher-resolution AMR monitoring whereas culture-based studies primarily undertook observational comparisons of specific organisms and phenotypic AMR profiles. Studies identifying wastewater-human AMR correlations were consistently associated with sampling wastewater influent irrespective of other methodological approaches. For longitudinal studies, a timeframe of >=6 months was similarly associated. Most influent studies identifying wastewater-human AMR correlations used composite (n=5) or flow-proportional wastewater sampling methods (n=4); however, grab sampling was commonest overall (n=6) and generally appeared similarly effective.Wastewater-based surveillance of AMR in human populations appears relatively robust, with most included studies reporting a correlation despite high diversity in study design and methodology. Our review supports sampling of wastewater influent using composite sampling (at a minimum) as a standard. Impacts of other methodological approaches are less clear; however, a minimum timeframe of six months for longitudinal studies, and increased sampling coverage for culture-independent studies to enable adequate biostatistical analyses appear sensible. As this relatively new field grows, more studies with clear wastewater-based population-level AMR surveillance aims are needed to better determine the impact of confounding features and validate comprehensive “best practice” protocols.

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Population-level surveillance of antibiotic resistance in Escherichia coli through sewage analysis

Cited by 87 publications

References 35 publications

Comparison of Culture- and Quantitative PCR-Based Indicators of Antibiotic Resistance in Wastewater, Recycled Water, and Tap Water

Comparison of Culture- and Quantitative PCR-Based Indicators of Antibiotic Resistance in Wastewater, Recycled Water, and Tap Water

Antibiotic Resistance in Recreational Waters: State of the Science

Wastewater Surveillance of Antimicrobial Resistance in Human Populations: A Systematic Review

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