Role of Hospital Environmental Microbiome in the Transmission of Multidrug-Resistant Organisms and Its Clinical Impact on Patient Outcomes in Critical Care Settings

Abstract

Background: The hospital environment in intensive care units is not a passive backdrop to care but a dynamic microbial ecosystem shaped by patient shedding,
staff movement, antibiotic exposure, humidity, water systems, and cleaning practices. Its role in the transmission of multidrug-resistant organisms (MDROs) in
critical care remains an important area of investigation.
Objective: This systematic review and meta-analysis evaluated whether the hospital environmental microbiome contributes to transmission of multidrugresistant organisms in critical care settings and whether such transmission is associated with clinically important patient outcomes.
Methods: A protocol-driven review framework was used, with prespecified searches of PubMed, Embase, Scopus, Web of Science, PsycINFO, Cochrane
CENTRAL, and grey literature sources through 18 March 2026. Eligible studies enrolled adult or mixed adult intensive care populations, examined an
environmental exposure or intervention related to the hospital microbiome, and reported patient acquisition, colonization, infection, or downstream clinical
outcomes. Double screening, double data extraction, risk-of-bias assessment, and random-effects meta-analysis were prespecified.
Results: Quantitative synthesis was feasible for studies evaluating prior-room-occupant or prior-environment exposure and subsequent acquisition of the same
multidrug-resistant organism or pathogen. Nine organism-specific effect sizes from seven observational studies were pooled. The main random-effects model
yielded an odds ratio of 2.09 (95% confidence interval [CI]: 1.64-2.67), indicating that exposure to a room previously occupied by a colonized or infected patient
approximately doubled the odds of acquisition. Heterogeneity was substantial but acceptable for ecological hospital data (I²=62.96%; tau²=0.0779). The
association was stronger for Gram-negative organisms (odds ratio 2.65, 95% CI: 1.87-3.75) than for Gram-positive or spore-forming organisms (odds ratio 1.84,
95% CI: 1.36-2.49). Sensitivity analyses using restricted maximum likelihood estimation were concordant.Narrative synthesis showed convergent evidence that
enhanced terminal disinfection, bundled cleaning programs, water-safe strategies, sink removal, and single-room design may reduce transmission opportunities.
However, direct causal evidence linking environmental exposure to mortality, length of stay, or organ failure remains limited and methodologically
heterogeneous.
Conclusions: Overall, the evidence supports the hospital environmental microbiome as a clinically relevant reservoir and transmission interface for multidrugresistant organisms in critical care. Environmental hygiene, water-system management, and design-based infection prevention should therefore be considered
core components of antimicrobial resistance control in the ICU.