Limited influence of hospital wastewater on the microbiome and resistome of wastewater in a community sewerage system

Buelow, Elena; Bayjanov, Jumamurat R.; Majoor, Eline; Willems, Rob J. L.; Bonten, Marc J. M.; Schmitt, Heike; Schaik, Willem van

doi:10.1093/femsec/fiy087

Cited by 92 publications

(69 citation statements)

References 66 publications

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“…By comparison, the residential wastewater of South Korea and Kuwait had abundances of clinically-relevant variants ranging from 478 to 933 RPKM and 200 to 850 RPKM, respectively (Figure 2). Previous studies implicating hospital wastewater as a major source of environmental antibiotic resistance have largely compared hospital wastewater with environments further downstream such as wastewater treatment plants or surface water (Buelow et al, 2018; Ng et al, 2017; Rodriguez-Mozaz et al, 2015; Rowe et al, 2017). Our results thus challenge the prevailing hypothesis that hospital effluent represents the most concerning source of environmental antibiotic resistance genes and suggests that all upstream wastewater may serve as important reservoirs of clinically-relevant genes.…”

Section: Resultsmentioning

confidence: 99%

“…Hospital wastewater has also been proposed as an important source of environmental antibiotic resistance due to the high levels of antibiotic use and resistant bacteria amongst hospital patients (Harris et al, 2014; Wellcome Trust et al, 2018). Abundances of ARGs in hospital effluents have been found to be higher than in downstream environments such as WWTPs and surface water (Buelow et al, 2018; Ng et al, 2017; Rodriguez-Mozaz et al, 2015; Rowe et al, 2017). However, hospitals contribute less than 1% of the total amount of municipal wastewater at WWTPs and have been found to have little influence on the levels of antibiotic resistance observed at WWTPs (Buelow et al, 2018; Harris et al, 2014; Kümmerer, 2004; Varela et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

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Multi-site sampling and risk prioritization reveals the public health relevance of antibiotic resistance genes found in wastewater environments

Duvallet

et al. 2019

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24The spread of bacterial antibiotic resistance across human and environmental habitats is a global 25 public health challenge. Wastewater has been implicated as a major source of antibiotic 26 resistance in the environment, as it carries resistant bacteria and resistance genes from humans 27 into natural ecosystems. However, different wastewater environments and antibiotic resistance 28 genes in wastewater do not all present the same level of risk to human health. In this study, we 29 investigate the public health relevance of antibiotic resistance found in wastewater by combining 30 metagenomic sequencing with risk prioritization of resistance genes, analyzing samples across 31 urban sewage system environments in multiple countries. We find that many of the resistance 32 genes commonly found in wastewater are not readily present in humans. Ranking antibiotic 33 resistance genes based on their potential pathogenicity and mobility reveals that most of the 34 resistance genes in wastewater are not clinically relevant. Additionally, we show that residential 35 wastewater resistomes pose greater risk to human health than those in wastewater treatment plant 36 samples, and that residential wastewater can be as risky as hospital effluent. Across countries, 37 differences in antibiotic resistance in residential wastewater can, in some cases, reflect 38 differences in antibiotic drug consumption. Finally, we find that the flow of antibiotic resistance 39 genes is influenced by geographical distance and environmental selection. Taken together, we 40 demonstrate how different analytical approaches can provide greater insights into the public 41 health relevance of antibiotic resistance in wastewater.42 43

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Multi-site sampling and risk prioritization reveals the public health relevance of antibiotic resistance genes found in wastewater environments

Duvallet

et al. 2019

Preprint

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“…This is because unstable lactam rings increase susceptibility of β-lactam antibiotics to hydrolysis immediately after excretion [94,95]. Hospital sewage tanks containing a large amount of residual antibiotics [96] may change the composition of tank ora and further promote the development of AMR by high selective pressure on bacteria [20,97,98]. Antibiotics exert selective pressure in favor of the growth resistant bacteria, even at very low concentrations [99][100][101].…”

Section: Concentration Of Residual Antimicrobial Agents In Hospital Smentioning

confidence: 99%

Metagenomic survey and whole genome sequencing of antimicrobial resistant bacteria in the sewage of a Japanese hospital

Katagiri

Kuroda

Sekizuka

et al. 2020

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Background The dissemination of antimicrobial-resistant bacteria (ARB) and the transfer of antimicrobial resistance genes (ARGs) are a threat to public health. Antibiotics are indispensable therapeutic agents essential for the treatment of infectious diseases; however, inappropriate use of antibiotics leads to the emergence of ARB. It is established that hospitals are closely involved in the spread of antimicrobial resistance (AMR), which impedes antibiotic treatment and subsequently increases mortality. In addition, excrement of patients or healthy carriers of ARB are discharged from the hospital sewage through the wastewater treatment plant (WWTP) into the rivers, causing an AMR burden on the environment.Method Metagenomic analysis was performed on the hospital sewage samples, followed by whole genome sequencing of the extended spectrum β-lactamase (ESBL)-producing organisms (EPOs). A comparative genome analysis was also performed between EPO isolates from sewage and clinical isolates.Results Metagenomic analysis showed that the hospital sewage tanks had bacterial flora corresponding to the human gut. During the study period, the hospital was relocated to a newly constructed building with new sewage tanks; however, the presence of ARB/ARGs in the new hospital sewage tanks became markedly equivalent to that of the old hospital within one month. The ESBL blaCTX−M and carbapenemase blaIMP genes were not much detected in the original hospital sewage samples by metagenome analysis, but selection on CHROMagar ESBL increased the sensitivity to detect those β-lactamase genes. Comparative genome analysis between sewage and clinical EPO isolates revealed partial similarity; however, most EPO isolates exhibited a notable difference (≥ 50) in single nucleotide variations based on core-genome phylogeny. This result suggests that only some of the sewage EPO isolates were originated from the clinical patient. Therapeutic agents in the hospital sewage were analyzed and the concentration of levofloxacin and clarithromycin was 0.0325 and 0.0135 µg/mL, respectively.Conclusions Whole genome analysis between sewage and clinical isolates suggested that healthy or asymptomatic carriers may be involved in the contamination of hospital sewage. Moreover, the hospital sewage tank may serve as a hotspot for the horizontal transfer of ARGs under the selective pressure of antimicrobial agents. Therefore, ARB monitoring in hospital sewage is expected to detect the presence of carriers prior to nosocomial ARB outbreaks. In addition, hospital wastewater should be treated suitably to bring ARB below detectable levels to reduce the environmental AMR burden.

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“…Figure 7). However, their overall contribution to the resistance load at WWTPs has been shown to be small (Buelow et al, 2018). So, to fine-tune the risk assessment, we would propose to include the fecal content in to the analysis to be able to determine possible selection or dissemination scenarios.…”

Section: Estimated Resistance Risk Correlates With Fecal Pollution Lementioning

confidence: 99%

Fecal pollution explains antibiotic resistance gene abundances in anthropogenically impacted environments

Karkman

Pärnänen

Larsson

2018

Preprint

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Discharge of treated sewage leads to release of antibiotic resistant bacteria, resistance genes and antibiotic residues to the environment. Such pollution can directly contribute to increased morbidity caused by the transmission of resistant fecal pathogens. Residual antibiotics in wastewaters have been speculated to select for resistant bacteria and thereby promote the evolution and emergence of new resistance factors. Increased abundance of antibiotic resistance genes in sewage and sewage-impacted environments may, however, simply be a result of fecal contamination with resistant bacteria rather than caused by an on-site selection pressure. In this study we have disentangled these two alternative scenarios by relating the relative resistance gene abundance to the accompanying extent of fecal pollution in publicly available metagenomic data. This was possible by analyzing the abundance of a newly discovered phage which is exceptionally abundant in, and specific to, human feces. The presence of resistance genes could largely be explained by fecal pollution, with no clear signs of selection in the environment, the only exception being environments polluted by very high levels of antibiotics from manufacturing where selection is evident. Our results demonstrate the necessity to take in to account the fecal pollution levels to avoid making erroneous assumptions regarding environmental selection of antibiotic resistance. The presence or absence of selection pressure has major implications for what the risk scenarios are (transmission versus evolution) and for what mitigations (reducing pathogenic bacteria or selective agents) should be prioritized to reduce health risks related to antibiotic resistance in the environment.

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Limited influence of hospital wastewater on the microbiome and resistome of wastewater in a community sewerage system

Cited by 92 publications

References 66 publications

Multi-site sampling and risk prioritization reveals the public health relevance of antibiotic resistance genes found in wastewater environments

Multi-site sampling and risk prioritization reveals the public health relevance of antibiotic resistance genes found in wastewater environments

Metagenomic survey and whole genome sequencing of antimicrobial resistant bacteria in the sewage of a Japanese hospital

Fecal pollution explains antibiotic resistance gene abundances in anthropogenically impacted environments

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