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      Reducing healthcare-associated infections incidence by a probiotic-based sanitation system: A multicentre, prospective, intervention study

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          Abstract

          Healthcare Associated Infections (HAI) are a global concern, further threatened by the increasing drug resistance of HAI-associated pathogens. On the other hand, persistent contamination of hospital surfaces contributes to HAI transmission, and it is not efficiently controlled by conventional cleaning, which does not prevent recontamination, has a high environmental impact and can favour selection of drug-resistant microbial strains. In the search for effective approaches, an eco-sustainable probiotic-based cleaning system (Probiotic Cleaning Hygiene System, PCHS) was recently shown to stably abate surface pathogens, without selecting antibiotic-resistant species. The aim of this study was to determine whether PCHS application could impact on HAI incidence. A multicentre, pre-post interventional study was performed for 18 months in the Internal Medicine wards of six Italian public hospitals (January 1 st 2016—June 30 th 2017). The intervention consisted of the substitution of conventional sanitation with PCHS, maintaining unaltered any other procedure influencing HAI control. HAI incidence in the pre and post-intervention period was the main outcome measure. Surface bioburden was also analyzed in parallel. Globally, 11,842 patients and 24,875 environmental samples were surveyed. PCHS was associated with a significant decrease of HAI cumulative incidence from a global 4.8% (284 patients with HAI over 5,930 total patients) to 2.3% (128 patients with HAI over 5,531 total patients) (OR = 0.44, CI 95% 0.35–0.54) (P<0.0001). Concurrently, PCHS was associated with a stable decrease of surface pathogens, compared to conventional sanitation (mean decrease 83%, range 70–96.3%), accompanied by a concurrent up to 2 Log drop of surface microbiota drug-resistance genes ( P<0.0001; P c = 0.008). Our study provides findings which support the impact of a sanitation procedure on HAI incidence, showing that the use of a probiotic-based environmental intervention can be associated with a significant decrease of the risk to contract a HAI during hospitalization. Once confirmed in larger experiences and other target populations, this eco-sustainable approach might be considered as a part of infection control and prevention (IPC) strategies.

          Trial registration—ISRCTN International Clinical Trials Registry, ISRCTN58986947.

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          Role of hospital surfaces in the transmission of emerging health care-associated pathogens: norovirus, Clostridium difficile, and Acinetobacter species.

          Health care-associated infections (HAI) remain a major cause of patient morbidity and mortality. Although the main source of nosocomial pathogens is likely the patient's endogenous flora, an estimated 20% to 40% of HAI have been attributed to cross infection via the hands of health care personnel, who have become contaminated from direct contact with the patient or indirectly by touching contaminated environmental surfaces. Multiple studies strongly suggest that environmental contamination plays an important role in the transmission of methicillin-resistant Staphylococcus aureus and vancomycin-resistant Enterococcus spp. More recently, evidence suggests that environmental contamination also plays a role in the nosocomial transmission of norovirus, Clostridium difficile, and Acinetobacter spp. All 3 pathogens survive for prolonged periods of time in the environment, and infections have been associated with frequent surface contamination in hospital rooms and health care worker hands. In some cases, the extent of patient-to-patient transmission has been found to be directly proportional to the level of environmental contamination. Improved cleaning/disinfection of environmental surfaces and hand hygiene have been shown to reduce the spread of all of these pathogens. Importantly, norovirus and C difficile are relatively resistant to the most common surface disinfectants and waterless alcohol-based antiseptics. Current hand hygiene guidelines and recommendations for surface cleaning/disinfection should be followed in managing outbreaks because of these emerging pathogens. (c) 2010 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Mosby, Inc. All rights reserved.
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            Controlling hospital-acquired infection: focus on the role of the environment and new technologies for decontamination.

            There is increasing interest in the role of cleaning for managing hospital-acquired infections (HAI). Pathogens such as vancomycin-resistant enterococci (VRE), methicillin-resistant Staphylococcus aureus (MRSA), multiresistant Gram-negative bacilli, norovirus, and Clostridium difficile persist in the health care environment for days. Both detergent- and disinfectant-based cleaning can help control these pathogens, although difficulties with measuring cleanliness have compromised the quality of published evidence. Traditional cleaning methods are notoriously inefficient for decontamination, and new approaches have been proposed, including disinfectants, steam, automated dispersal systems, and antimicrobial surfaces. These methods are difficult to evaluate for cost-effectiveness because environmental data are not usually modeled against patient outcome. Recent studies have reported the value of physically removing soil using detergent, compared with more expensive (and toxic) disinfectants. Simple cleaning methods should be evaluated against nonmanual disinfection using standardized sampling and surveillance. Given worldwide concern over escalating antimicrobial resistance, it is clear that more studies on health care decontamination are required. Cleaning schedules should be adapted to reflect clinical risk, location, type of site, and hand touch frequency and should be evaluated for cost versus benefit for both routine and outbreak situations. Forthcoming evidence on the role of antimicrobial surfaces could supplement infection prevention strategies for health care environments, including those targeting multidrug-resistant pathogens.
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              The role played by contaminated surfaces in the transmission of nosocomial pathogens.

              Studies in the 1970s and 1980s suggested that environmental surface contamination played a negligible role in the endemic transmission of healthcare-associated infections. However, recent studies have demonstrated that several major nosocomial pathogens are shed by patients and contaminate hospital surfaces at concentrations sufficient for transmission, survive for extended periods, persist despite attempts to disinfect or remove them, and can be transferred to the hands of healthcare workers. Evidence is accumulating that contaminated surfaces make an important contribution to the epidemic and endemic transmission of Clostridium difficile, vancomycin-resistant enterococci, methicillin-resistant Staphylococcus aureus, Acinetobacter baumannii, Pseudomonas aeruginosa, and norovirus and that improved environmental decontamination contributes to the control of outbreaks. Efforts to improve environmental hygiene should include enhancing the efficacy of cleaning and disinfection and reducing the shedding of pathogens. Further high-quality studies are needed to clarify the role played by surfaces in nosocomial transmission and to determine the effectiveness of different interventions in reducing associated infection rates.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: Project administrationRole: ResourcesRole: SoftwareRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Project administrationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                12 July 2018
                2018
                : 13
                : 7
                : e0199616
                Affiliations
                [1 ] Section of Microbiology and Medical Genetics, Department of Medical Sciences, University of Ferrara, Ferrara, Italy
                [2 ] CIAS Interdepartmental Research Centre, Departments of Medical Sciences and Architecture, University of Ferrara, Ferrara, Italy
                [3 ] Department of Medicine, University of Udine, Udine, Italy
                [4 ] Fondazione Policlinico Universitario Agostino Gemelli, Roma, Italy
                [5 ] Department of Infection Prevention Control and Risk Management, S. Anna University Hospital, Ferrara, Italy
                [6 ] Centre for Research on Health and Social Care Management (CERGAS), Department of Policy Analysis and Public Management, Bocconi University, Milan, Italy
                [7 ] Department of Public Health, Experimental and Forensic Medicine, University of Pavia, Pavia, Italy
                [8 ] Azienda USL di Ferrara, Ferrara, Italy
                [9 ] Department of Biomedical Sciences and Dental and Functional Images, University of Messina, Messina, Italy
                [10 ] Ospedale di Santa Maria del Prato, Feltre (Belluno), Italy
                [11 ] Azienda Ospedaliera Universitaria Ospedali Riuniti di Foggia, Foggia, Italy
                [12 ] Ospedale Sant’Antonio Abate, Tolmezzo (Udine), Italy
                University of Calgary, CANADA
                Author notes

                Competing Interests: The authors declare that they received unrestricted funds by Copma scrl (Ferrara, Italy), but the funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. This does not alter the authors' adherence to PLOS ONE policies on sharing data and materials.

                ¶ The complete membership of the author group can be found in the Acknowledgements

                Author information
                http://orcid.org/0000-0001-6048-9141
                http://orcid.org/0000-0002-1257-3434
                http://orcid.org/0000-0002-2009-9357
                http://orcid.org/0000-0003-2572-6556
                http://orcid.org/0000-0002-5293-402X
                http://orcid.org/0000-0002-9018-7600
                Article
                PONE-D-18-02642
                10.1371/journal.pone.0199616
                6042698
                30001345
                5483415f-a0cf-4e67-9f48-917a43f22c21
                © 2018 Caselli et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 8 February 2018
                : 11 June 2018
                Page count
                Figures: 4, Tables: 5, Pages: 17
                Funding
                Funded by: COPMA scrl
                The authors declare that they received unrestricted funding from Copma Scrl (via Veneziani 32, 44124 Ferrara, Italy). However, this does not influenced in any way the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.
                Categories
                Research Article
                Medicine and Health Sciences
                Infectious Diseases
                Nosocomial Infections
                Medicine and Health Sciences
                Hematology
                Bloodstream Infections
                Medicine and Health Sciences
                Urology
                Urinary Tract Infections
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbiome
                Biology and Life Sciences
                Genetics
                Genomics
                Microbial Genomics
                Microbiome
                Biology and Life Sciences
                Microbiology
                Microbial Genomics
                Microbiome
                Medicine and Health Sciences
                Health Care
                Environmental Health
                Sanitation
                Medicine and Health Sciences
                Public and Occupational Health
                Environmental Health
                Sanitation
                Medicine and Health Sciences
                Gastroenterology and Hepatology
                Gastrointestinal Infections
                Medicine and Health Sciences
                Infectious Diseases
                Soft Tissue Infections
                Medicine and Health Sciences
                Pulmonology
                Respiratory Infections
                Lower Respiratory Tract Infections
                Custom metadata
                All relevant data are within the paper and its Supporting Information files, including data held in the public repository BioStudies ( https://www.ebi.ac.uk/biostudies/), Accession No. S-BSST75.

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                Uncategorized

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