Occurrence of vanA/vanM-positive vancomycin-resistant Enterococcus faecium in hospital wastewater associated with clinical infections in Guangzhou, China: A genomic epidemiological study

Background: The emerging ST80 vancomycin-resistant Enterococcus faecium (VREfm) lineage, linked to the increases of clinical infections in China and Japan, raises concerns about environmental transmission. Hospital wastewater systems are recognized reservoirs for antimicrobial-resistant bacteria, bu...

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Main Authors: Liling Zhang, Minxuan Su, Shaowei Meng, Xuan Zhang, Hao Wu, Meina Wu, Xiaojun Ao, Xiaoyue Zhang, Jiehao Lin, Shijia Yu, Yuqi Hong, Xiucheng Zeng, Shuyi Huang, Yuxin Zhang, Bangjie Yang, Ni Zhang, Yueting Jiang, Lingqing Xu, Zhongde Zhang, Cha Chen, Cong Shen
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:International Journal of Medical Microbiology
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Online Access:http://www.sciencedirect.com/science/article/pii/S1438422125000141
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author Liling Zhang
Minxuan Su
Shaowei Meng
Xuan Zhang
Hao Wu
Meina Wu
Xiaojun Ao
Xiaoyue Zhang
Jiehao Lin
Shijia Yu
Yuqi Hong
Xiucheng Zeng
Shuyi Huang
Yuxin Zhang
Bangjie Yang
Ni Zhang
Yueting Jiang
Lingqing Xu
Zhongde Zhang
Cha Chen
Cong Shen
author_facet Liling Zhang
Minxuan Su
Shaowei Meng
Xuan Zhang
Hao Wu
Meina Wu
Xiaojun Ao
Xiaoyue Zhang
Jiehao Lin
Shijia Yu
Yuqi Hong
Xiucheng Zeng
Shuyi Huang
Yuxin Zhang
Bangjie Yang
Ni Zhang
Yueting Jiang
Lingqing Xu
Zhongde Zhang
Cha Chen
Cong Shen
author_sort Liling Zhang
collection DOAJ
description Background: The emerging ST80 vancomycin-resistant Enterococcus faecium (VREfm) lineage, linked to the increases of clinical infections in China and Japan, raises concerns about environmental transmission. Hospital wastewater systems are recognized reservoirs for antimicrobial-resistant bacteria, but their role in disseminating ST80 VREfm remains unclear. This study investigates VREfm prevalence in hospital wastewater and genomic links between patients and hospital wastewater. Methods: From December 2023 to May 2024, a total of 262 wastewater samples were collected from three hospitals in Guangzhou, China. VREfm was identified using vancomycin-supplemented media. Antimicrobial susceptibility was assessed using the broth dilution method. Ninety-five patient-derived VREfm genomes in the same hospitals were included. Whole-genome sequencing and bioinformatic analysis were performed to reveal genomic characterizations and genetic transmission links. Results: VREfm was detected in 54.6 % (143/262) of samples. All isolates carried vanA, with 25.9 % (37/143) co-harboring vanA and vanM. The dominant ST80 lineage (43.4 %, n = 62) was linked to recent regional prevalence. A novel sequence type ST2460, belonging to CC17, emerged as the second most prevalent (27.2 %, n = 39). ST80 isolates exhibited enriched antimicrobial resistance genes, correlating with multidrug resistance phenotypes and high resistance rates. Genomic analysis revealed that 95.7 % (132/138) of ST80 isolates from wastewater and patients exhibited close genetic relatedness (median of SNP = 19, IQR: 14–23) and were linked within cross-source transmission networks, supported by the high similarity of a shared p23VRE019-like plasmid. Conclusions: Hospital wastewater is a critical reservoir for high-risk VREfm clones, particularly the outbreak-associated ST80 lineage. The persistence of VREfm in effluents and evidence of cross-source transmission underscores the urgent need for enhanced environmental surveillance. Integrated strategies addressing environmental reservoirs are essential to combat the growing threat of VREfm.
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spelling doaj-art-7190ac1b6878499cb4fd8a942f5daf102025-08-20T03:45:30ZengElsevierInternational Journal of Medical Microbiology1438-42212025-06-0131915165810.1016/j.ijmm.2025.151658Occurrence of vanA/vanM-positive vancomycin-resistant Enterococcus faecium in hospital wastewater associated with clinical infections in Guangzhou, China: A genomic epidemiological studyLiling Zhang0Minxuan Su1Shaowei Meng2Xuan Zhang3Hao Wu4Meina Wu5Xiaojun Ao6Xiaoyue Zhang7Jiehao Lin8Shijia Yu9Yuqi Hong10Xiucheng Zeng11Shuyi Huang12Yuxin Zhang13Bangjie Yang14Ni Zhang15Yueting Jiang16Lingqing Xu17Zhongde Zhang18Cha Chen19Cong Shen20The Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, China; State Key Laboratory of Dampness Syndrome of Chinese Medicine/Clinical Laboratory, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, China; Guangdong Provincial Key Laboratory of Research on Emergency in TCM, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, China; State Key Laboratory of Dampness Syndrome of Chinese Medicine/Clinical Laboratory, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, China; State Key Laboratory of Dampness Syndrome of Chinese Medicine/Clinical Laboratory, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaDepartment of Otolaryngology, Hospital of Honghe State Affiliated to Kunming Medical University, Southern Central Hospital of Yunnan Province, Mengzi, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaClinical Laboratory, Guangdong Provincial People's Hospital/Guangdong Academy of Medical Sciences, Southern Medical University, Guangzhou, ChinaClinical Laboratory, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou, ChinaThe Sixth Affiliated Hospital of Guangzhou Medical University, Qingyuan People's Hospital, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, ChinaThe Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, China; Correspondence to: State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Neihuanxi Road, Guangzhou 510080, China.The Second Clinical Medical College, Guangzhou University of Chinese Medicine, State Key Laboratory of Traditional Chinese Medicine Syndrome, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, China; State Key Laboratory of Dampness Syndrome of Chinese Medicine/Clinical Laboratory, Guangdong Provincial Hospital of Chinese Medicine, Guangzhou, China; Guangdong Provincial Key Laboratory of Research on Emergency in TCM, Guangzhou, China; Correspondence to: State Key Laboratory of Dampness Syndrome of Chinese Medicine, The Second Clinical Medical College, Guangzhou University of Chinese Medicine, Dade Road, Guangzhou 510080, China.Background: The emerging ST80 vancomycin-resistant Enterococcus faecium (VREfm) lineage, linked to the increases of clinical infections in China and Japan, raises concerns about environmental transmission. Hospital wastewater systems are recognized reservoirs for antimicrobial-resistant bacteria, but their role in disseminating ST80 VREfm remains unclear. This study investigates VREfm prevalence in hospital wastewater and genomic links between patients and hospital wastewater. Methods: From December 2023 to May 2024, a total of 262 wastewater samples were collected from three hospitals in Guangzhou, China. VREfm was identified using vancomycin-supplemented media. Antimicrobial susceptibility was assessed using the broth dilution method. Ninety-five patient-derived VREfm genomes in the same hospitals were included. Whole-genome sequencing and bioinformatic analysis were performed to reveal genomic characterizations and genetic transmission links. Results: VREfm was detected in 54.6 % (143/262) of samples. All isolates carried vanA, with 25.9 % (37/143) co-harboring vanA and vanM. The dominant ST80 lineage (43.4 %, n = 62) was linked to recent regional prevalence. A novel sequence type ST2460, belonging to CC17, emerged as the second most prevalent (27.2 %, n = 39). ST80 isolates exhibited enriched antimicrobial resistance genes, correlating with multidrug resistance phenotypes and high resistance rates. Genomic analysis revealed that 95.7 % (132/138) of ST80 isolates from wastewater and patients exhibited close genetic relatedness (median of SNP = 19, IQR: 14–23) and were linked within cross-source transmission networks, supported by the high similarity of a shared p23VRE019-like plasmid. Conclusions: Hospital wastewater is a critical reservoir for high-risk VREfm clones, particularly the outbreak-associated ST80 lineage. The persistence of VREfm in effluents and evidence of cross-source transmission underscores the urgent need for enhanced environmental surveillance. Integrated strategies addressing environmental reservoirs are essential to combat the growing threat of VREfm.http://www.sciencedirect.com/science/article/pii/S1438422125000141Enterococcus faeciumVancomycinHospital wastewaterMolecular epidemiologyWhole-genome sequencingTransmission
spellingShingle Liling Zhang
Minxuan Su
Shaowei Meng
Xuan Zhang
Hao Wu
Meina Wu
Xiaojun Ao
Xiaoyue Zhang
Jiehao Lin
Shijia Yu
Yuqi Hong
Xiucheng Zeng
Shuyi Huang
Yuxin Zhang
Bangjie Yang
Ni Zhang
Yueting Jiang
Lingqing Xu
Zhongde Zhang
Cha Chen
Cong Shen
Occurrence of vanA/vanM-positive vancomycin-resistant Enterococcus faecium in hospital wastewater associated with clinical infections in Guangzhou, China: A genomic epidemiological study
International Journal of Medical Microbiology
Enterococcus faecium
Vancomycin
Hospital wastewater
Molecular epidemiology
Whole-genome sequencing
Transmission
title Occurrence of vanA/vanM-positive vancomycin-resistant Enterococcus faecium in hospital wastewater associated with clinical infections in Guangzhou, China: A genomic epidemiological study
title_full Occurrence of vanA/vanM-positive vancomycin-resistant Enterococcus faecium in hospital wastewater associated with clinical infections in Guangzhou, China: A genomic epidemiological study
title_fullStr Occurrence of vanA/vanM-positive vancomycin-resistant Enterococcus faecium in hospital wastewater associated with clinical infections in Guangzhou, China: A genomic epidemiological study
title_full_unstemmed Occurrence of vanA/vanM-positive vancomycin-resistant Enterococcus faecium in hospital wastewater associated with clinical infections in Guangzhou, China: A genomic epidemiological study
title_short Occurrence of vanA/vanM-positive vancomycin-resistant Enterococcus faecium in hospital wastewater associated with clinical infections in Guangzhou, China: A genomic epidemiological study
title_sort occurrence of vana vanm positive vancomycin resistant enterococcus faecium in hospital wastewater associated with clinical infections in guangzhou china a genomic epidemiological study
topic Enterococcus faecium
Vancomycin
Hospital wastewater
Molecular epidemiology
Whole-genome sequencing
Transmission
url http://www.sciencedirect.com/science/article/pii/S1438422125000141
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