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Multicenter Study
. 2018 Jul 12;13(7):e0199616.
doi: 10.1371/journal.pone.0199616. eCollection 2018.

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

Elisabetta Caselli  1   2 , Silvio Brusaferro  3 , Maddalena Coccagna  2 , Luca Arnoldo  3 , Filippo Berloco  4 , Paola Antonioli  5 , Rosanna Tarricone  6 , Gabriele Pelissero  7 , Silvano Nola  8 , Vincenza La Fauci  9 , Alessandro Conte  3 , Lorenzo Tognon  10 , Giovanni Villone  11 , Nelso Trua  12 , Sante Mazzacane  2 ; SAN-ICA Study Group
Affiliations
Multicenter Study

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

Elisabetta Caselli et al. PLoS One. .

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 1st 2016-June 30th 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; Pc = 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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Conflict of interest statement

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.

Figures

Fig 1
Fig 1. Study design graphic representation.
Six Italian hospitals from different geographical regions were enrolled in the study (North: Feltre, Tolmezzo, Vigevano; Centre: Rome; South: Foggia, Messina). Five hospitals were randomly allocated in two Intervention groups (I1, I2) and one further hospital represented an external control (extC): I1-group included Roma, Foggia and Feltre hospitals, entering the study on January 1st 2016; I2-group included Vigevano and Tolmezzo hospitals, entering 5-months later, on May 1st 2016; extC hospital was represented by Messina hospital, receiving no intervention and monitored from May 1st 2016. The phases of the study are indicated by colours: orange, 6-months pre-intervention period (pre-PCHS); light green, stabilization period, when PCHS was introduced; green, 6-months post-intervention period (PCHS), when PCHS was routinely applied. Sampling campaigns for microbiological analyses are indicated by circles: conventional microbiological analyses were performed monthly (black circles), and molecular analyses were performed quarterly (red circles) in all enrolled hospitals.
Fig 2
Fig 2. HAI incidence rates in the I1-I2 intervention hospitals.
Results are expressed as bimonthly value of incidence rate per 1,000 patient-days, respectively in the pre-PCHS (red) and PCHS periods (blue). 95% CI intervals are also reported.
Fig 3
Fig 3. Surface contamination in the surveyed hospitals.
(A) Pathogen load on hospital surfaces, expressed as CFU/m2. Six pathogens were measured by direct CFU counting on specific Rodac plates, as described in Methods (Staphylococcal spp., Enterobacteriaceae spp., Acinetobacter spp., Candida spp., Pseudomonas spp., Clostridium spp.). Graphed results represent the sum of the median values obtained for each measured pathogen. Median values (lower part of the box) and Q3 values (upper part of the box, representing the 75% percentile values) are shown for each hospital, and for pre-intervention (pre-PCHS) and intervention (PCHS) phases. Values reported for the external control hospital (Messina), correspond to those detected in the 1st and 2nd 6-month periods of the study. (B) Total bacterial load and PCHS-Bacilli count, respectively measured by a pan-bacterial qPCR (panB) and a specific qPCR for Bacillus genus (spo0A). Results are expressed as genome copy number per 100 ng of tested DNA. The median values ± SD of pre-PCHS and PCHS phases are shown. Values reported for the external control hospital (Messina), correspond to those detected in the 1st and 2nd 6-month periods of the study.
Fig 4
Fig 4. Resistome analysis of PCHS-Bacillus strains.
Antibiotic resistance genes were analyzed by microarray both in the PCHS detergent prior to application, containing a blend of three Bacillus species (Original) and in the Bacillus isolates (Isolates) collected from hospital surfaces in the PCHS phase of I1 and I2 hospital groups. For original PCHS-Bacilli, results are expressed as mean values ± SD of six replicates. For Isolates, results are expressed as the mean value ± SD of 120 Bacillus isolated from hospital surfaces. Both Original and Isolates values were compared to negative control values (NTC). Each Bacillus isolate was identified by PCR and sequencing prior to microarray analysis, as previously described [29].
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Grants and funding

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.

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