Recovery and genetic characterization of clinically-relevant ST2 carbapenem-resistant Acinetobacter baumannii isolates from untreated hospital sewage in Zhejiang Province, China

Danxia Gu; Yuchen Wu; Kaichao Chen; Yanyan Zhang; Xiaoyang Ju; Zelin Yan; Miaomiao Xie; Edward Wai Chi Chan; Sheng Chen; Zhi Ruan; Rong Zhang; Jun Zhang

doi:10.1016/j.scitotenv.2024.170058

Recovery and genetic characterization of clinically-relevant ST2 carbapenem-resistant Acinetobacter baumannii isolates from untreated hospital sewage in Zhejiang Province, China

Sci Total Environ. 2024 Mar 15:916:170058. doi: 10.1016/j.scitotenv.2024.170058. Epub 2024 Jan 12.

Authors

Danxia Gu¹, Yuchen Wu², Kaichao Chen³, Yanyan Zhang², Xiaoyang Ju², Zelin Yan², Miaomiao Xie³, Edward Wai Chi Chan³, Sheng Chen³, Zhi Ruan⁴, Rong Zhang⁵, Jun Zhang⁶

Affiliations

¹ Department of Clinical Laboratory, The Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, China; Laboratory Medicine Center, Department of Clinical Laboratory, Zhejiang Provincial People's Hospital (Affiliated People's Hospital), Hangzhou Medical College, Hangzhou, Zhejiang, China.
² Department of Clinical Laboratory, The Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, China.
³ Department of Food Science and Nutrition, Faculty of Science, The Hong Kong Polytechnic University, Kowloon, Hong Kong.
⁴ Department of Clinical Laboratory, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China; Key Laboratory of Precision Medicine in Diagnosis and Monitoring Research of Zhejiang Province, Hangzhou, China.
⁵ Department of Clinical Laboratory, The Second Affiliated Hospital of Zhejiang University, School of Medicine, Hangzhou, China. Electronic address: zhang-rong@zju.edu.cn.
⁶ Department of Clinical Laboratory, Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China; Key Laboratory of Precision Medicine in Diagnosis and Monitoring Research of Zhejiang Province, Hangzhou, China. Electronic address: jameszhang2000@zju.edu.cn.

PMID: 38218490
DOI: 10.1016/j.scitotenv.2024.170058

Abstract

The global transmission of carbapenem-resistant Acinetobacter baumannii (CRAB) poses a significant and grave threat to human health. To investigate the potential relationship between hospital sewage and the transmission of CRAB within healthcare facilities, isolates of Acinetobacter spp. obtained from untreated hospital sewage samples were subjected to antimicrobial susceptibility tests, genome sequencing, and bioinformatic and phylogenetic tree analysis, and that data were matched with those of the clinical isolates. Among the 70 Acinetobacter spp. sewage isolates tested, A. baumannii was the most prevalent and detectable in 5 hospitals, followed by A. nosocomialis and A. gerneri. Worryingly, 57.14 % (40/70) of the isolates were MDR, with 25.71 % (18/70) being resistant to carbapenem. When utilizing the Pasteur scheme, ST2 was the predominant type among these CRAB isolates, with Tn2006 (ΔISAba1-bla_OXA-23-ATPase-yeeB-yeeA-_ΔISAba1) and Tn2009 (_ΔISAba1-bla_OXA-23-ATPase-hp-parA-yeeC-hp-yeeB-_ΔISAba1) being the key mobile genetic elements that encode carbapenem resistance. Seven A. gerneri isolates which harbored Tn2008 (ISAba1-bla_OXA-23 -ATPase) and the bla_PER-1 gene were also identified. Besides, an A. soil isolate was found to exhibit high-level of meropenem resistance (MIC ≥128 mg/L) and harbor a bla_NDM-1 gene located in a core genetic structure of ISAba125-bla_NDM-1-ble-trpF-dsbC-cutA. To investigate the genetic relatedness between isolates recovered from hospital sewage and those collected from ICUs, a phylogenetic tree was constructed for 242 clinical isolates and 9 sewage isolates. The results revealed the presence of two evolutionary clades, each containing isolates from both ICU and sewage water, suggesting that CRAB isolates in untreated sewage water were also the transmission clones or closely related evolutionary isolates recoverable in hospital settings. Findings in this work confirm that hospital sewage is a potential reservoir of CRAB.

Keywords: Carbapenem; Dissemination; Resistance; Wastewater.

MeSH terms

Acinetobacter Infections* / drug therapy
Acinetobacter baumannii* / genetics
Adenosine Triphosphatases / genetics
Adenosine Triphosphatases / therapeutic use
Anti-Bacterial Agents / pharmacology
Bacterial Proteins / genetics
Carbapenems / pharmacology
Hospitals
Humans
Interleukin-1 Receptor-Like 1 Protein / genetics
Microbial Sensitivity Tests
Phylogeny
Sewage
Water
beta-Lactamases / genetics

Substances

Anti-Bacterial Agents
Bacterial Proteins
beta-Lactamases
Interleukin-1 Receptor-Like 1 Protein
Sewage
Carbapenems
Adenosine Triphosphatases
Water