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Multidrug-Resistant Enterobacteriaceae in Coastal Water

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Multidrug-Resistant Enterobacteriaceae in Coastal Water Cohen et al. Antimicrob Resist Infect Control (2020) 9:169 https://doi.org/10.1186/s13756-020-00826-2 RESEARCH Open Access Multidrug-resistant enterobacteriaceae in coastal water: an emerging threat Regev Cohen1,2* , Svetlana Paikin1, Assaf Rokney3, Maxim Rubin‑Blum4 and Peleg Astrahan5 Abstract Background: The environmental role of carbapenemase‑producing Enterobacteriaceae (CPE) acquisition and infec‑ tion in human disease has been described but not thoroughly investigated. We aimed to assess the occurrence of CPE in nearshore aquatic bodies. Methods: Enterobacteriaceae were cultured from coastal and estuary water near Netanya, Israel in June and July of 2018. Bacteria were identifed by VITEK2® and their antimicrobial susceptibility was tested according to the CLSI guidelines. Enterobacteriaceae genomes were sequenced to elucidate their resistome and carbapenemase types. Results: Among other clinically relevant bacteria, four CPE (three Enterobacter spp and one Escherichia coli isolate) were isolated from two river estuaries (Poleg and Alexander Rivers) and coastal water at a popular recreational beach (Beit Yanai). Molecular analysis and genome sequencing revealed the persistent presence of rare beta‑lactamase resistance genes, including blaIMI‑2 and a previously unknown blaIMI‑20 allele, which were not found among the local epidemiological strains. Genome comparisons revealed the high identity of riverine and marine CPE that were culti‑ vated one month apart. Conclusions: We show that CPE contamination was widespread in nearshore marine and riverine habitats. The high genome‑level similarity of riverine and marine CPEs, isolated one month apart, hints at the common source of infec‑ tion. We discuss the clinical implications of these fndings and stress the urgent need to assess the role of the aquatic environment in CPE epidemiology. Keyword: Carbapenemase producing enterobacteriaceae (CPE), Seawater, Estuary, Israel, Public health, Enterobacter spp. Background transmission of these bacteria to humans outside of Carbapenem-resistant Enterobacteriaceae (CRE), in healthcare facilities following exposure to wildlife, live- particular, carbapenemase- and extended-spectrum stock and pet animals have been reported [3]. Te envi- β-lactamase-producing Enterobacteriaceae (CPE and ronmental routes of CRE infection may play a role in ESBL-PE) endanger global health, as they have spread causing human disease and spreading it globally, how- worldwide during the last two decades. Te risk factors ever, they have not been thoroughly investigated yet. In for the acquisition of these multidrug-resistant organ- particular, little is known about the epidemiology of CRE isms (MDROs) are usually associated with healthcare [1] in the aquatic environment. and overseas travel [2]. Potential modes of environmental Recent studies show that CRE may contaminate aquatic environments such as marine surface water [4–7], rivers *Correspondence: [email protected]; [email protected] [5, 8–17], estuaries [18] and polluted drinking water [19]. 1 Head of Infectious Diseases and Infection Control Units, Sanz Medical Riverine CRE often harbor several carbapenemase types Center, Laniado Hospital, 16 Divrei Haim St, Kiryat Sanz, 42150 Netnaya, Israel [8, 10, 11, 15]. A case of blaIMI-2 CP-Enterobacter asbur- Full list of author information is available at the end of the article iae bacteremia following a river near-drowning accident © The Author(s) 2020. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Cohen et al. Antimicrob Resist Infect Control (2020) 9:169 Page 2 of 9 was described, and the infecting pathogen was isolated Sampling and bacterial isolation from the river one month later [16]. In two studies that On two occasions (June, July 2018), water samples were reported the isolation of CPE from seawater, Entero- collected with sterile-glass containers (pre-combusted at bacter spp. was prominent and comprised of 69–76% of 500 °C) and delivered to the laboratory at room tempera- the Enterobacteriaceae isolated [6, 7]. Assessing the link ture. 200–1300 ml of freshwater or seawater was fltered, between the clinical and aquatic epidemiology of CRE is using a vacuum pump, through a 0.2 µm sterile cellulose often challenging. While some studies showed that clini- acetate membrane (Sartorius Stedim®). Distinct volumes cal strains may be found in aquatic bodies [7, 9, 16], none of water were fltered at each site (Table 1), due to difer- such link was demonstrated in others [17, 20]. ences in turbidity and membrane clogging. Control mem- CRE may reach aquatic bodies as a result of organic branes were obtained by fltering room air for the same contamination from multiple sources [21], including duration. Te membranes were soaked in an enrichment hospital efuents [22–24], wastewater treatment plants medium (thioglycolate broth (Novamed®)), that served as (WWTPs) [24–26], discharge of livestock farms and agri- the source of cultures: frst after overnight incubation at culture [3, 27], seepage water [28] as well as others [21]. room temperature, and after 24 h of incubation at 37 °C. Once mixed with the aquatic body, these efuents may Te media were cultured on TSBA + Blood/Chocolate introduce not only foreign MDROs, but also high doses agar, MacConkey agar, CNA agar, Chromagar Orienta- of antibiotics, which likely trigger resistance propagation tion, Chromagar MSupercarba and Streptococci Select [29]. In Israel, the main sources of aquatic contamina- medium plates (all from HyLabs®). Colonies were picked, tion comprise of regional councils that are not connected isolated and then identifed using VITEK2® (bioMérieux). to WWTPs, controlled discharges from fsh farms and Antimicrobial susceptibility testing was performed by WWTPs [30] and untreated sewage from the Palestinian VITEK2® (bioMérieux) and Etest (bioMérieux) on Muel- Authority [31]. Israeli governmental programs that moni- ler–Hinton agar according to the Clinical & Laboratory tor the quality of coastal seawater and rivers report coli- Standards Institute (CLSI) guidelines. Enterobacteriaceae form concentrations, but not the presence of MDROs. growing on CRE plates were subjected to the modifed MDRO infection, however, poses a real threat to those Hodge test or CARBA NP hydrolysis. Following species engaged in recreational water activities. isolation and identifcation, the carbapenemase type was ® A young patient who sufered a near-drowning expe- identifed using Cepheid GeneXpert Carba-R for blaKPC, rience in one of Netanya’s beaches was admitted to the blaNDM, blaVIM, blaIMP, blaOXA-48 genes. Te blaIMI was Laniado medical center, Netanya, Israel, in June 2014. identifed using the polymerase chain reaction (PCR) Bacterial screening upon his admission to the intensive [32]. care unit found he was a carrier of two CPE species: We repeated the sampling from the same sites 3 weeks Enterobacter cloacae and Klebsiella oxytoca, both carry- later. During the second sampling session, we mainly ing blaKPC. We assumed that seawater ingestion and aspi- attempted to identify CREs, and used 60 ml of sterile ration led to this infection, as no other risk factors could media as a negative control. explain the high rates of CPE colonization. We hypoth- esized that these CPEs originated from rivers supply- Genome sequencing, assembly and bioinformatics ing water to the shoreline in the vicinity of Netanya. To DNA was extracted from three Enterobacter isolates: test this hypothesis, we aimed to identify CPE in coastal nEC133, nEC134 and nEC135 using the Presto Mini waters and two river estuaries in the Sharon district. gDNA Bacteria kit (GeneAid). DNA libraries were pre- pared using the Illumina Nextera XT kit (Illumina). Material and methods Sequencing was performed using the Illumina MiSeq Sampling sites platform with 2 × 250 bp paired-end reads aiming Two river estuaries were sampled in the vicin- at > 100 × coverage, MiSeq Reagent Kit v2. ity of the Laniado hospital: Poleg (32°16′11.7"N 34°49′55.7"E) ~ 13 Km south to Laniado hospital and Bioinformatic analyses ′ ′ the Alexander River (32°23 46.7"N 34°51 57.0"E) ~ 5 Km Sequencing was performed using the Illumina MiSeq north to the hospital. Two popular public recreational platform with 2 × 250 bp paired-end reads aiming beaches along the coastline were also sampled: Beit Yanai at > 100 coverage, MiSeq Reagent Kit v2. Genomes ′ ′ × (32°23 15.7"N 34°51 48.3"E) ~ 4.6 Km north of the hospi- were de-novo assembled with SPAdes V3.12 [33] and tal and 1 Km south of the Alexander river estuary; and their quality was estimated with checkM [34]. Te ′ ′ Sironit (32°19 51.4"N 34°50 53.8"E) 1.7 Km south of the whole-genome multilocus sequence typing (wgMLST hospital and 6.5 Km north of the Poleg River estuary [35]) for Enterobacter cloacae complex was performed (Fig. 1). Cohen et al. Antimicrob Resist Infect Control (2020) 9:169 Page 3 of 9 Haifa Mediterranean Sea Netanya Tel Aviv Ashdod The city of Nablus, the Palesnian Authority Nablus river WWTP • Netanya Yad Hana •Tul- Karem Authorized treated waste water, dumping site (32.24999, 34.87761) • Raanana 1 Km Fig.
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