{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,23]],"date-time":"2026-06-23T07:47:17Z","timestamp":1782200837006,"version":"3.54.5"},"reference-count":50,"publisher":"MDPI AG","issue":"1","license":[{"start":{"date-parts":[[2024,1,10]],"date-time":"2024-01-10T00:00:00Z","timestamp":1704844800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Italian Ministry of University and Research","award":["2022FZL92A"],"award-info":[{"award-number":["2022FZL92A"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Antimicrobial resistance (AMR) poses several issues concerning the management of hospital-acquired infections, leading to increasing morbidity and mortality rates and higher costs of care. Multidrug-resistant (MDR) bacteria can spread in the healthcare setting by different ways. The most important are direct contact transmission occurring when an individual comes into physical contact with an infected or colonized patient (which can involve healthcare workers, patients, or visitors) and indirect contact transmission occurring when a person touches contaminated objects or surfaces in the hospital environment. Furthermore, in recent years, toilets in hospital settings have been increasingly recognised as a hidden source of MDR bacteria. Different sites in restrooms, from toilets and hoppers to drains and siphons, can become contaminated with MDR bacteria that can persist there for long time periods. Therefore, shared toilets may play an important role in the transmission of nosocomial infections since they could represent a reservoir for MDR bacteria. Such pathogens can be further disseminated by bioaerosol and\/or droplets potentially produced during toilet use or flushing and be transmitted by inhalation and contact with contaminated fomites. In this review, we summarize available evidence regarding the molecular features of MDR bacteria contaminating toilets of healthcare environments, with a particular focus on plumbing components and sanitary installation. The presence of bacteria with specific molecular traits in different toilet sites should be considered when adopting effective managing and containing interventions against nosocomial infections potentially due to environmental contamination. Finally, here we provide an overview of traditional and new approaches to reduce the spreading of such infections.<\/jats:p>","DOI":"10.3390\/microorganisms12010136","type":"journal-article","created":{"date-parts":[[2024,1,10]],"date-time":"2024-01-10T05:47:21Z","timestamp":1704865641000},"page":"136","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":19,"title":["Multidrug-Resistant Bacteria Contaminating Plumbing Components and Sanitary Installations of Hospital Restrooms"],"prefix":"10.3390","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7638-1538","authenticated-orcid":false,"given":"Felice","family":"Valzano","sequence":"first","affiliation":[{"name":"Department of Clinical and Experimental Medicine, University of Foggia, Via Napoli 20, 71122 Foggia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna Rita Daniela","family":"Coda","sequence":"additional","affiliation":[{"name":"Department of Medical and Surgical Sciences, University of Foggia, Via Napoli 20, 71122 Foggia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5638-227X","authenticated-orcid":false,"given":"Arcangelo","family":"Liso","sequence":"additional","affiliation":[{"name":"Department of Medical and Surgical Sciences, University of Foggia, Via Napoli 20, 71122 Foggia, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabio","family":"Arena","sequence":"additional","affiliation":[{"name":"Department of Clinical and Experimental Medicine, University of Foggia, Via Napoli 20, 71122 Foggia, Italy"},{"name":"IRCCS Don Carlo Gnocchi Foundation, Via di Scandicci 269, 50143 Florence, Italy"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,1,10]]},"reference":[{"key":"ref_1","unstructured":"World Health Organization (WHO) (2023, November 10). Antimicrobial Resistance: Global Report on Surveillance, Geneva. Available online: https:\/\/iris.who.int\/bitstream\/handle\/10665\/112642\/9789241564748_eng.pdf;jsessionid=831AB5113EE962A27DA6BBAD68754A76?sequence=1."},{"key":"ref_2","unstructured":"Centers for Disease Control and Prevention (CDC) (2023, November 10). Antibiotic Resistance Threats in the United States, Available online: https:\/\/stacks.cdc.gov\/view\/cdc\/82532."},{"key":"ref_3","unstructured":"European Centre for Disease Prevention and Control (ECDC) (2023, November 10). Assessing the Health Burden of Infections with Antibiotic-Resistant Bacteria in the EU\/EEA, 2016\u20132020. Available online: https:\/\/www.ecdc.europa.eu\/en\/publications-data\/health-burden-infections-antibiotic-resistant-bacteria-2016-2020."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"010407","DOI":"10.7189\/jogh.09.010407","article-title":"Global Burden of Clostridium Difficile Infections: A Systematic Review and Meta-Analysis","volume":"9","author":"Balsells","year":"2019","journal-title":"J. Glob. Health"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1539","DOI":"10.1056\/NEJMra1403772","article-title":"Clostridium Difficile Infection","volume":"372","author":"Leffler","year":"2015","journal-title":"N. Engl. J. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1017\/ice.2018.359","article-title":"Transmission Pathways of Multidrug-Resistant Organisms in the Hospital Setting: A Scoping Review","volume":"40","author":"Blanco","year":"2019","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1016\/j.molmed.2015.03.005","article-title":"Hospital-Associated Microbiota and Implications for Nosocomial Infections","volume":"21","author":"Lax","year":"2015","journal-title":"Trends Mol. Med."},{"key":"ref_8","unstructured":"Centers for Disease Control and Prevention (CDC) (2023, November 10). Reduce Risk from Water, Available online: https:\/\/www.cdc.gov\/hai\/prevent\/environment\/water.html."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e01715","DOI":"10.1128\/AEM.01715-20","article-title":"Risk Factors Associated with Carbapenemase-Producing Enterobacterales (CPE) Positivity in the Hospital Wastewater Environment","volume":"86","author":"Park","year":"2020","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1435","DOI":"10.1093\/cid\/cix132","article-title":"The Hospital Water Environment as a Reservoir for Carbapenem-Resistant Organisms Causing Hospital-Acquired Infections-A Systematic Review of the Literature","volume":"64","author":"Mathers","year":"2017","journal-title":"Clin. Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1016\/j.jhin.2016.01.010","article-title":"What Happens in Hospitals Does Not Stay in Hospitals: Antibiotic-Resistant Bacteria in Hospital Wastewater Systems","volume":"93","author":"Hocquet","year":"2016","journal-title":"J. Hosp. Infect."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1128\/am.30.2.229-237.1975","article-title":"Microbiological Hazards of Household Toilets: Droplet Production and the Fate of Residual Organisms","volume":"30","author":"Gerba","year":"1975","journal-title":"Appl. Microbiol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1080\/09603123.2015.1135312","article-title":"Presence of Human Noroviruses on Bathroom Surfaces: A Review of the Literature","volume":"26","author":"Leone","year":"2016","journal-title":"Int. J. Environ. Health Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1329","DOI":"10.1017\/ice.2017.216","article-title":"Provider Role in Transmission of Carbapenem-Resistant Enterobacteriaceae","volume":"38","author":"Grabowski","year":"2017","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"614","DOI":"10.1111\/j.1365-2672.2012.05234.x","article-title":"A Model of the Transmission of Micro-Organisms in a Public Setting and Its Correlation to Pathogen Infection Risks","volume":"112","author":"Gerhardts","year":"2012","journal-title":"J. Appl. Microbiol."},{"key":"ref_16","unstructured":"Jessen, C.U. (1955). Airborne Microorganisms: Occurrance and Control, G.E.C. Gads Forlag."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1186\/s13756-018-0301-9","article-title":"CDC Epicenters Program Bioaerosol Concentrations Generated from Toilet Flushing in a Hospital-Based Patient Care Setting","volume":"7","author":"Knowlton","year":"2018","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"065107","DOI":"10.1063\/5.0013318","article-title":"Can a Toilet Promote Virus Transmission? From a Fluid Dynamics Perspective","volume":"32","author":"Li","year":"2020","journal-title":"Phys. Fluids"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"580","DOI":"10.1016\/S1473-3099(19)30230-0","article-title":"New Environmental Reservoir of CPE in Hospitals","volume":"19","author":"Smismans","year":"2019","journal-title":"Lancet Infect. Dis."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"2000118","DOI":"10.2807\/1560-7917.ES.2021.26.21.2000118","article-title":"Outbreak of OXA-48-Producing Enterobacterales in a Haematological Ward Associated with an Uncommon Environmental Reservoir, France, 2016 to 2019","volume":"26","author":"Jolivet","year":"2021","journal-title":"Eurosurveillance"},{"key":"ref_21","unstructured":"European Centre for Disease Prevention and Control (ECDC) (2023, November 10). Antimicrobial Resistance Surveillance in Europe 2023: 2021 Data. Available online: https:\/\/op.europa.eu\/en\/publication-detail\/-\/publication\/97ee4ab5-0994-11ee-b12e-01aa75ed71a1\/language-en."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.jhin.2021.01.029","article-title":"Risk Factors for the Environmental Spread of Different Multidrug-Resistant Organisms: A Prospective Cohort Study","volume":"111","author":"Saliba","year":"2021","journal-title":"J. Hosp. Infect."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/S0195-6701(98)90141-4","article-title":"The Toilet as a Transmission Vector of Vancomycin-Resistant Enterococci","volume":"40","author":"Noble","year":"1998","journal-title":"J. Hosp. Infect."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1007\/BF02601862","article-title":"Contamination of a Hospital Environment by Clostridium Difficile","volume":"3","author":"Rolfe","year":"1979","journal-title":"Curr. Microbiol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"102204","DOI":"10.1016\/j.anaerobe.2020.102204","article-title":"Role of Clostridioides Difficile in Hospital Environment and Healthcare Workers","volume":"63","author":"Reigadas","year":"2020","journal-title":"Anaerobe"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1515","DOI":"10.1007\/s10096-015-2380-3","article-title":"Spanish Clostridium difficile Study Group Impact of Clinical Awareness and Diagnostic Tests on the Underdiagnosis of Clostridium Difficile Infection","volume":"34","author":"Reigadas","year":"2015","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"655","DOI":"10.1016\/j.ijheh.2019.03.006","article-title":"Antibiotic Resistant Bacteria and Resistance Genes in Biofilms in Clinical Wastewater Networks","volume":"222","author":"Sib","year":"2019","journal-title":"Int. J. Hyg. Environ. Health"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1186\/s13756-023-01261-9","article-title":"Sanitary Installations and Wastewater Plumbing as Reservoir for the Long-Term Circulation and Transmission of Carbapenemase Producing Citrobacter Freundii Clones in a Hospital Setting","volume":"12","author":"Hamerlinck","year":"2023","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_29","first-page":"E34","article-title":"Microbial Competition in Environmental Nosocomial Reservoirs and Diffusion Capacity of OXA48-Klebsiella Pneumoniae: Potential Impact on Patients and Possible Control Methods","volume":"58","author":"Herruzo","year":"2017","journal-title":"J. Prev. Med. Hyg."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1016\/j.jhin.2020.07.017","article-title":"Toilet Drain Water as a Potential Source of Hospital Room-to-Room Transmission of Carbapenemase-Producing Klebsiella Pneumoniae","volume":"106","author":"Heireman","year":"2020","journal-title":"J. Hosp. Infect."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.ajic.2018.06.021","article-title":"The Relevance of Sink Proximity to Toilets on the Detection of Klebsiella Pneumoniae Carbapenemase inside Sink Drains","volume":"47","author":"Buchan","year":"2019","journal-title":"Am. J. Infect. Control"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1016\/j.idh.2019.08.005","article-title":"Two Carbapenemase-Producing Enterobacteriaceae Outbreaks Detected Retrospectively by Whole-Genome Sequencing at an Australian Tertiary Hospital","volume":"25","author":"Marmor","year":"2020","journal-title":"Infect. Dis. Health"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.jhin.2012.06.007","article-title":"Multidrug-Resistant Pseudomonas Aeruginosa Outbreaks in Two Hospitals: Association with Contaminated Hospital Waste-Water Systems","volume":"82","author":"Breathnach","year":"2012","journal-title":"J. Hosp. Infect."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1016\/j.jhin.2016.05.009","article-title":"Acetic Acid as a Decontamination Method for Sink Drains in a Nosocomial Outbreak of Metallo-\u03b2-Lactamase-Producing Pseudomonas Aeruginosa","volume":"94","author":"Melander","year":"2016","journal-title":"J. Hosp. Infect."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2705","DOI":"10.1111\/jam.15121","article-title":"Toilet Hygiene-Review and Research Needs","volume":"131","author":"Abney","year":"2021","journal-title":"J. Appl. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"20493","DOI":"10.1038\/s41598-022-24686-5","article-title":"Commercial Toilets Emit Energetic and Rapidly Spreading Aerosol Plumes","volume":"12","author":"Crimaldi","year":"2022","journal-title":"Sci. Rep."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1093\/cid\/ciy052","article-title":"Intensive Care Unit Wastewater Interventions to Prevent Transmission of Multispecies Klebsiella Pneumoniae Carbapenemase-Producing Organisms","volume":"67","author":"Mathers","year":"2018","journal-title":"Clin. Infect. Dis."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jhin.2011.08.010","article-title":"Potential for Aerosolization of Clostridium Difficile after Flushing Toilets: The Role of Toilet Lids in Reducing Environmental Contamination Risk","volume":"80","author":"Best","year":"2012","journal-title":"J. Hosp. Infect."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1017\/ice.2020.11","article-title":"CDC Prevention Epicenter Program Bioaerosols Generated from Toilet Flushing in Rooms of Patients with Clostridioides Difficile Infection","volume":"41","author":"Wilson","year":"2020","journal-title":"Infect. Control Hosp. Epidemiol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1069","DOI":"10.1016\/S1473-3099(19)30262-2","article-title":"Contact Precautions in Single-Bed or Multiple-Bed Rooms for Patients with Extended-Spectrum \u03b2-Lactamase-Producing Enterobacteriaceae in Dutch Hospitals: A Cluster-Randomised, Crossover, Non-Inferiority Study","volume":"19","author":"Buiting","year":"2019","journal-title":"Lancet Infect. Dis."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1016\/S1473-3099(19)30626-7","article-title":"Contact Isolation versus Standard Precautions to Decrease Acquisition of Extended-Spectrum \u03b2-Lactamase-Producing Enterobacterales in Non-Critical Care Wards: A Cluster-Randomised Crossover Trial","volume":"20","author":"Maechler","year":"2020","journal-title":"Lancet Infect. Dis."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1016\/j.ajic.2017.11.005","article-title":"Evaluation of Hospital-Grade Disinfectants on Viral Deposition on Surfaces after Toilet Flushing","volume":"46","author":"Sassi","year":"2018","journal-title":"Am. J. Infect. Control"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.envint.2015.10.015","article-title":"Concentrations of Antibiotics Predicted to Select for Resistant Bacteria: Proposed Limits for Environmental Regulation","volume":"86","author":"Larsson","year":"2016","journal-title":"Environ. Int."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2718","DOI":"10.1093\/jac\/dkt281","article-title":"Current and Emergent Strategies for Disinfection of Hospital Environments","volume":"68","author":"Abreu","year":"2013","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1692","DOI":"10.1016\/j.ajic.2016.07.004","article-title":"Efficacy of an Automated Ultraviolet C Device in a Shared Hospital Bathroom","volume":"44","author":"Cooper","year":"2016","journal-title":"Am. J. Infect. Control"},{"key":"ref_46","unstructured":"(2023, November 10). Flush Down Automatic Toilet Seat. Available online: https:\/\/flushdown.myshopify.com\/."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"033320","DOI":"10.1063\/5.0040310","article-title":"Aerosol Generation in Public Restrooms","volume":"33","author":"Schreck","year":"2021","journal-title":"Phys. Fluids"},{"key":"ref_48","unstructured":"Cicchetti, A. (2024, January 07). Studio Di Fattibilit\u00e0 Del Nuovo Dispositivo Medico Toil\u00e9 Di Planus Spa. Available online: https:\/\/www.planus.eu\/up_file\/Report_Altems-VR.pdf."},{"key":"ref_49","unstructured":"(2023, November 10). SplaShh\u2014Shop Foaming Toilet Powder \u201cTake Control of Your Bathroom\u201d. Available online: https:\/\/splashhpowder.com\/."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1186\/s13756-021-01023-5","article-title":"Droplets Generated from Toilets during Urination as a Possible Vehicle of Carbapenem-Resistant Klebsiella Pneumoniae","volume":"10","author":"Arena","year":"2021","journal-title":"Antimicrob. Resist. Infect. Control"}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/1\/136\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T13:43:32Z","timestamp":1760103812000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/12\/1\/136"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,1,10]]},"references-count":50,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,1]]}},"alternative-id":["microorganisms12010136"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms12010136","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,1,10]]}}}