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Multicenter Study
. 2024 May 14;331(18):1544-1557.
doi: 10.1001/jama.2024.2759.

Reducing Hospitalizations and Multidrug-Resistant Organisms via Regional Decolonization in Hospitals and Nursing Homes

Gabrielle M Gussin  1 , James A McKinnell  2 , Raveena D Singh  1 , Loren G Miller  2 , Ken Kleinman  3 , Raheeb Saavedra  1 , Thomas Tjoa  1 , Shruti K Gohil  1 , Tabitha D Catuna  1 , Lauren T Heim  1 , Justin Chang  1 , Marlene Estevez  1 , Jiayi He  1 , Kathleen O'Donnell  4 , Matthew Zahn  5 , Eunjung Lee  1   6 , Chase Berman  1 , Jenny Nguyen  1 , Shalini Agrawal  1 , Isabel Ashbaugh  1 , Christine Nedelcu  1 , Philip A Robinson  7 , Steven Tam  8 , Steven Park  1 , Kaye D Evans  9 , Julie A Shimabukuro  9 , Bruce Y Lee  10 , Emily Fonda  11 , John A Jernigan  12 , Rachel B Slayton  12 , Nimalie D Stone  12 , Lynn Janssen  4 , Robert A Weinstein  13   14 , Mary K Hayden  13 , Michael Y Lin  13 , Ellena M Peterson  15 , Cassiana E Bittencourt  15 , Susan S Huang  1   16 ; CDC Safety and Healthcare Epidemiology Prevention Research Development (SHEPheRD) Program
Affiliations
Multicenter Study

Reducing Hospitalizations and Multidrug-Resistant Organisms via Regional Decolonization in Hospitals and Nursing Homes

Gabrielle M Gussin et al. JAMA. .

Abstract

Importance: Infections due to multidrug-resistant organisms (MDROs) are associated with increased morbidity, mortality, length of hospitalization, and health care costs. Regional interventions may be advantageous in mitigating MDROs and associated infections.

Objective: To evaluate whether implementation of a decolonization collaborative is associated with reduced regional MDRO prevalence, incident clinical cultures, infection-related hospitalizations, costs, and deaths.

Design, setting, and participants: This quality improvement study was conducted from July 1, 2017, to July 31, 2019, across 35 health care facilities in Orange County, California.

Exposures: Chlorhexidine bathing and nasal iodophor antisepsis for residents in long-term care and hospitalized patients in contact precautions (CP).

Main outcomes and measures: Baseline and end of intervention MDRO point prevalence among participating facilities; incident MDRO (nonscreening) clinical cultures among participating and nonparticipating facilities; and infection-related hospitalizations and associated costs and deaths among residents in participating and nonparticipating nursing homes (NHs).

Results: Thirty-five facilities (16 hospitals, 16 NHs, 3 long-term acute care hospitals [LTACHs]) adopted the intervention. Comparing decolonization with baseline periods among participating facilities, the mean (SD) MDRO prevalence decreased from 63.9% (12.2%) to 49.9% (11.3%) among NHs, from 80.0% (7.2%) to 53.3% (13.3%) among LTACHs (odds ratio [OR] for NHs and LTACHs, 0.48; 95% CI, 0.40-0.57), and from 64.1% (8.5%) to 55.4% (13.8%) (OR, 0.75; 95% CI, 0.60-0.93) among hospitalized patients in CP. When comparing decolonization with baseline among NHs, the mean (SD) monthly incident MDRO clinical cultures changed from 2.7 (1.9) to 1.7 (1.1) among participating NHs, from 1.7 (1.4) to 1.5 (1.1) among nonparticipating NHs (group × period interaction reduction, 30.4%; 95% CI, 16.4%-42.1%), from 25.5 (18.6) to 25.0 (15.9) among participating hospitals, from 12.5 (10.1) to 14.3 (10.2) among nonparticipating hospitals (group × period interaction reduction, 12.9%; 95% CI, 3.3%-21.5%), and from 14.8 (8.6) to 8.2 (6.1) among LTACHs (all facilities participating; 22.5% reduction; 95% CI, 4.4%-37.1%). For NHs, the rate of infection-related hospitalizations per 1000 resident-days changed from 2.31 during baseline to 1.94 during intervention among participating NHs, and from 1.90 to 2.03 among nonparticipating NHs (group × period interaction reduction, 26.7%; 95% CI, 19.0%-34.5%). Associated hospitalization costs per 1000 resident-days changed from $64 651 to $55 149 among participating NHs and from $55 151 to $59 327 among nonparticipating NHs (group × period interaction reduction, 26.8%; 95% CI, 26.7%-26.9%). Associated hospitalization deaths per 1000 resident-days changed from 0.29 to 0.25 among participating NHs and from 0.23 to 0.24 among nonparticipating NHs (group × period interaction reduction, 23.7%; 95% CI, 4.5%-43.0%).

Conclusions and relevance: A regional collaborative involving universal decolonization in long-term care facilities and targeted decolonization among hospital patients in CP was associated with lower MDRO carriage, infections, hospitalizations, costs, and deaths.

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Conflict of interest statement

Conflict of Interest Disclosures: Ms Gussin reported grants from Centers for Disease Control and Prevention during the conduct of the study; other from Medline Industries Conducting studies for which participating nursing homes received contributed antiseptic and cleaning products outside the submitted work. Dr McKinnell reported providing infection prevention and antimicrobial stewardship consulting services for long term care facilities with Expert Stewardship, Inc. Dr Miller reported grants from CDC during the conduct of the study; grants from Medline outside the submitted work. Dr Kleinman reported grants from CDC during the conduct of the study; nonfinancial support from Medline Industries conducting studies for which participating nursing homes received contributed antiseptic products and nonfinancial support from Xttrium Laboratories conducting studies for which participating hospital and nursing home patients receive contributed antiseptic products outside the submitted work. Mr Saavedra reported grants from Center for Disease Control and Prevention during the conduct of the study; other from Medline Industries conducting studies for which participating nursing homes received contributed antiseptic and cleaning products and other from Xttrium Laboratories Conducting studies in which participating nursing homes and hospital patients received contributed antiseptic products outside the submitted work. Mr Tjoa reported grants from Centers for Disease Control and Prevention during the conduct of the study. Dr Gohil reported grants from Centers for Disease Control and Prevention during the conduct of the study. Ms Catuna reported grants from Centers for Disease Control and Prevention during the conduct of the study; personal fees from Amgen, Inc for employment not related to submitted work and personal fees from ICON Plc for employment not related to submitted work outside the submitted work. Ms Heim reported grants from Centers for Disease Control and Prevention during the conduct of the study. Dr Chang reported grants from Centers for Disease Control and Prevention during the conduct of the study. Ms Estevez reported grants from Centers for Disease Control and Prevention during the conduct of the study. Ms He reported grants from Centers for Disease Control and Prevention during the conduct of the study. Ms O’Donnell reported grants from CDC during the conduct of the study. Dr E. Lee reported grants from Centers for Disease Control and Prevention during the conduct of the study. Mr Berman reported grants from Centers for Disease Control and Prevention during the conduct of the study; nonfinancial support from Medline conducting studies for which participating nursing homes received contributed antiseptic and cleaning products outside the submitted work. Ms Nguyen reported grants from Centers for Disease Control and Prevention during the conduct of the study. Ms Agrawal reported grants from Centers for Disease Control and Prevention during the conduct of the study. Ms Ashbaugh reported grants from Centers for Disease Control and Prevention during the conduct of the study. Ms Nedelcu reported grants from Centers for Disease Control and Prevention during the conduct of the study. Dr Tam reported grants from Centers for Disease Control and Prevention during the conduct of the study. Dr Park reported grants from Centers for Disease Control and Prevention during the conduct of the study. Ms Evans reported grants from Centers for Disease Control and Prevention during the conduct of the study. Ms Shimabukuro reported grants from Centers for Disease Control and Prevention during the conduct of the study. Dr B. Lee reported grants from Centers for Disease Control and Prevention Developing Healthcare Safety Research (SHEPheRD) task order 2015-05 during the conduct of the study. Dr Hayden reported grants from CDC and personal fees from Sanofi member of a clinical adjudication panel for an investigational COVID-19 vaccine outside the submitted work. Dr Lin reported I have received research support in the form of contributed product from Sage Products (Stryker Corporation). Dr Peterson reported grants from Centers for Disease Control for during the conduct of the study. Dr Bittencourt reported grants from Centers for Disease Control and Prevention during the conduct of the study. Dr Huang reported other from Medline Industries conducting studies for which participating nursing homes received contributed antiseptic and cleaning products and other from Xttrium Laboratories conducting studies for which participating nursing homes and hospital patients received contributed antiseptic products outside the submitted work. No other disclosures were reported.

Figures

Figure 1.
Figure 1.. MDRO Point Prevalence (Screening) Among Facilities Participating in the Regional Decolonization Collaborative, Baseline and End of Intervention
CRE indicates carbapenem resistant Enterobacterales; ESBL, extended spectrum β-lactamase; MDRO, multidrug-resistant organism; MRSA, methicillin-resistant Staphylococcus aureus; and VRE, vancomycin-resistant Enterococci.
Figure 2.
Figure 2.. Multivariable Regression for Factors Associated With MDRO Carriage in NHs and LTACHs (MDRO, MRSA, and VRE)
Gastrointestinal devices include gastronomy, jejunostomy, nasogastric, and rectal tubes. Models adjust for clustering by facility. CRE indicates carbapenem resistant Enterobacterales; ESBL, extended spectrum β-lactamase; LTACH, long-term acute care hospital; MRSA, methicillin-resistant Staphylococcus aureus; NH, nursing homes; and VRE, vancomycin-resistant Enterococci.
Figure 3.
Figure 3.. Multivariable Regression for Factors Associated With MDRO Carriage in NHs and LTACHs (ESBL and CRE)
CRE indicates carbapenem resistant Enterobacterales; ESBL, extended spectrum β-lactamase; LTACH, long-term acute care hospital; MRSA, methicillin-resistant Staphylococcus aureus; NH, nursing homes; and VRE, vancomycin-resistant Enterococci.
Figure 4.
Figure 4.. Incident Cultures in the Intervention vs Baseline Period
Results are based on generalized linear mixed models that accounted for clustering within facilities and adjusted for facility-level annual admissions, mean age, % White race, % Medicaid-insured, and mean Elixhauser comorbidity count. CRE indicates carbapenem resistant Enterobacterales; ESBL, extended spectrum β-lactamase; LTACH, long-term acute care hospitals; MDRO, multidrug-resistant organism; MRSA, methicillin-resistant Staphylococcus aureus; and NH, nursing homes.
Figure 5.
Figure 5.. Monthly Infection-Related Hospitalization Rates Among Nursing Homes Residents in Participating (Decolonization) vs Nonparticipating Nursing Homes
Q indicates quarter.
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