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      Transmission pathways of multidrug-resistant organisms in the hospital setting: a scoping review

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          Abstract

          Background:

          Prevalence of multidrug-resistant microorganisms (MDROs) continues to increase, while infection control gaps in healthcare settings facilitate their transmission between patients. In this setting, 5 distinct yet interlinked pathways are responsible for transmission. The complete transmission process is still not well understood. Designing and conducting a single research study capable of investigating all 5 complex and multifaceted pathways of hospital transmission would be costly and logistically burdensome. Therefore, this scoping review aims to synthesize the highest-quality published literature describing each of the 5 individual potential transmission pathways of MDROs in the healthcare setting and their overall contribution to patient-to-patient transmission.

          Methods:

          In 3 databases, we performed 2 separate systematic searches for original research published during the last decade. The first search focused on MDRO transmission via the HCW or the environment to identify publications studying 5 specific transmission pathways: (1) patient to HCW, (2) patient to environment, (3) HCW to patient, (4) environment to patient, and (5) environment to HCW. The second search focused on overall patient-to-patient transmission regardless of the transmission pathway. Both searches were limited to transmission of methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant Enterococcus, multidrug-resistant A. baumannii, and carbapenem-resistant Enterobacteriaceae. After abstract screening of 5,026 manuscripts, researchers independently reviewed and rated the remaining papers using objective predefined criteria to identify the highest quality and most influential manuscripts.

          Results:

          High-quality manuscripts were identified for all 5 routes of transmission. Findings from these studies were consistent for all pathways; however, results describing the routes from the environment/HCW to a noncolonized patient were more limited and variable. Additionally, most research focused on MRSA, instead of other MDROs. The second search yielded 10 manuscripts (8 cohort studies) that demonstrated the overall contribution of patient-to-patient transmission in hospitals regardless of the transmission route. For MRSA, the reported cross-transmission was as high as 40%.

          Conclusions:

          This scoping review brings together evidence supporting all 5 possible transmission pathways and illustrates the complex nature of patient-to-patient transmission of MDROs in hospitals. Our findings also confirm that transmission of MDROs in hospitals occurs frequently, suggesting that ongoing efforts are necessary to strengthen infection prevention and control to prevent the spread of MDROs.

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          Most cited references33

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          Risk of acquiring antibiotic-resistant bacteria from prior room occupants.

          Environmental contamination with methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant enterococci (VRE) occurs during the care of patients harboring these organisms and may increase the risk of transmission to subsequent room occupants. Twenty-month retrospective cohort study of patients admitted to 8 intensive care units performing routine admission and weekly screening for MRSA and VRE. We assessed the relative odds of acquisition among patients admitted to rooms in which the most recent occupants were MRSA positive or VRE positive, compared with patients admitted to other rooms. Of 11 528 intensive care unit room stays, 10 151 occupants were eligible to acquire MRSA, and 10 349 were eligible to acquire VRE. Among patients whose prior room occupant was MRSA positive, 3.9% acquired MRSA, compared with 2.9% of patients whose prior room occupant was MRSA negative (adjusted odds ratio, 1.4; P = .04). VRE, Among patients whose prior room occupant was VRE positive, these values were 4.5% and 2.8% respectively (adjusted odds ratio, 1.4; P = .02). These excess risks accounted for 5.1% of all incident MRSA cases and 6.8% of all incident VRE cases, with a population attributable risk among exposed patients of less than 2% for either organism. Acquisition was significantly associated with longer post-intensive care unit length of stay. Admission to a room previously occupied by an MRSA-positive patient or a VRE-positive patient significantly increased the odds of acquisition for MRSA and VRE. However, this route of transmission was a minor contributor to overall transmission. The effect of current cleaning practices in reducing the risk to the observed levels and the potential for further reduction are unknown.
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            Rapid spread of carbapenem-resistant Klebsiella pneumoniae in New York City: a new threat to our antibiotic armamentarium.

            Carbapenem antibiotics are used to treat serious infections caused by extended-spectrum beta-lactamase-carrying pathogens. Carbapenem resistance has been unusual in isolates of Klebsiella pneumoniae. In this study, the prevalence and molecular epidemiologic characteristics of carbapenem-resistant K pneumoniae are analyzed, and the experience involving 2 hospital outbreaks is described. A citywide surveillance study was conducted in hospitals in Brooklyn. An observational study involving subsequent outbreaks at 2 hospitals was undertaken. Isolates were genetically fingerprinted by ribotyping and were examined for the presence of KPC-type carbapenem-hydrolyzing beta-lactamases. Of 602 isolates of K pneumoniae collected during the citywide surveillance study, 45% had extended-spectrum beta-lactamases. Of the extended-spectrum beta-lactamase-producing isolates, 3.3% carried the carbapenem-hydrolyzing beta-lactamase KPC-2. Several isolates were reported by the clinical microbiology laboratories as being susceptible to imipenem. Although all the isolates were resistant using agar diffusion methods, minimal inhibitory concentrations of imipenem were substantially lower for several isolates using standard broth microdilution tests and were highly dependent on the inoculum used. Two hospitals experienced the rapid spread of carbapenem-resistant isolates involving 58 patients. Overall 14-day mortality for bacteremic patients was 47%. Most isolates belonged to a single ribotype. Carbapenem-resistant K pneumoniae isolates are rapidly emerging in New York City. The spread of a strain that possesses a carbapenem-hydrolyzing beta-lactamase has occurred in regional hospitals. Because these isolates are resistant to virtually all commonly used antibiotics, control of their spread is crucial. However, automated systems used for susceptibility testing may not accurately identify all these isolates, which will severely hamper control efforts.
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              Transfer of multidrug-resistant bacteria to healthcare workers' gloves and gowns after patient contact increases with environmental contamination.

              To assess the role of environmental contamination in the transmission of multidrug-resistant bacteria to healthcare workers' clothing. Prospective cohort. Six intensive care units at a tertiary care hospital. Healthcare workers including registered nurses, patient care technicians, respiratory therapists, occupational/physical therapists, and physicians. None. One hundred twenty of 585 (20.5%) healthcare worker/patient interactions resulted in contamination of healthcare workers' gloves or gowns. Multidrug-resistant Acinetobacter baumannii contamination occurred most frequently, 55 of 167 observations (32.9%; 95% confidence interval [CI] 25.8% to 40.0%), followed by multidrug-resistant Pseudomonas aeruginosa, 15 of 86 (17.4%; 95% CI 9.4% to 25.4%), vancomycin-resistant Enterococcus, 25 of 180 (13.9%, 95% CI 8.9, 18.9%) and methicillin-resistant Staphylococcus aureus, 21 of 152 (13.8%; 95% CI 8.3% to 19.2%). Independent risk factors associated with healthcare worker contamination with multidrug-resistant bacteria were positive environmental cultures (odds ratio [OR] 4.2; 95% CI 2.7-6.5), duration in room for >5 mins (OR 2.0; 95% CI 1.2-3.4), performing physical examinations (OR 1.7; 95% CI 1.1-2.8), and contact with the ventilator (OR 1.8; 95% CI, 1.1-2.8). Pulsed field gel electrophoresis determined that 91% of healthcare worker isolates were related to an environmental or patient isolate. The contamination of healthcare workers' protective clothing during routine care of patients with multidrug-resistant organisms is most frequent with A. baumannii. Environmental contamination was the major determinant of transmission to healthcare workers' gloves or gowns. Compliance with contact precautions and more aggressive environmental cleaning may decrease transmission.
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                Author and article information

                Journal
                Infection Control & Hospital Epidemiology
                Infect. Control Hosp. Epidemiol.
                Cambridge University Press (CUP)
                0899-823X
                1559-6834
                April 2019
                March 06 2019
                April 2019
                : 40
                : 4
                : 447-456
                Article
                10.1017/ice.2018.359
                6897300
                30837029
                fc330917-7d2a-42cb-bbe1-7cee5c7c76f0
                © 2019

                https://www.cambridge.org/core/terms

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