Reducing Fluoroquinolone Use and Clostridioides difficile Infections in Community Nursing Homes Through Hospital–Nursing Home Collaboration

JAMDA 21 (2020) 55e61

JAMDA journal homepage: www.jamda.com

Original Study

Reducing Fluoroquinolone Use and Clostridioides difficile Infections in Community Nursing Homes Through HospitaleNursing Home Collaboration Christina B. Felsen MPH a, Elizabeth S. Dodds Ashley MHS, PharmD b, Grant R. Barney BS c, Dallas L. Nelson MD, CMD d, Joseph A. Nicholas MD e, Hongmei Yang PhD f, Marie E. Aydelotte MD g, Alexander Karlic MD h, Nirmala C. Nicholas MD d, Kim K. Petrone MD i, Rena D. Pine MD j, Scott L. Schabel MD k, Annette Medina-Walpole MD d, Ghinwa K. Dumyati MD a, l, * a

Center for Community Health and Prevention, University of Rochester Medical Center, Rochester, NY Division of Infectious Diseases and International Health, Duke Center for Antimicrobial Stewardship and Infection Prevention, Durham, NC c Emerging Infections Program, New York State Department of Health, Albany, NY d Department of Medicine, Geriatrics/Aging University of Rochester Medical Center, Rochester, NY e Department of Medicine and Physical Medicine and Rehabilitation, University of Rochester Medical Center, Rochester, NY f Department of Biostatistics and Computational Biology, University of Rochester Medical Center, Rochester, NY g Jewish Senior Life, Rochester, NY h Unity Living Center and Unity Hospital, Rochester Regional Health, Rochester, NY i St Ann’s Community, Rochester, NY j St John’s Home, Rochester, NY k Division of Long Term Care, Rochester Regional Health, Rochester, NY l Department of Medicine, Division of Infectious Disease, University of Rochester Medical Center, Rochester, NY b

a b s t r a c t Keywords: Antibiotic stewardship nursing homes quality improvement fluoroquinolones C difficile infections

Objective: Nursing homes (NHs) are an important target for antibiotic stewardship (AS). We describe a collaborative model to reduce Clostridioides difficile infections (CDIs) in NHs through optimization of antibiotic use including a reduction in high-risk antibiotics such as fluoroquinolones. Design: Quasi-experimental, pre- and post-intervention study. Setting and participants: Six NHs in Monroe County, NY. Methods: A hospital-based AS expert team assisted NHs in identifying targets for improving antibiotic use. Interventions included (1) collaboration with a medical director advisory group to develop NH consensus guidelines for testing and treatment of 2 syndromes (urinary tract infections and pneumonia) for which fluoroquinolone use is common, (2) provision of multifaceted NH staff education on these guidelines and education of residents and family members on the judicious use of antibiotics, and (3) sharing facility-specific and comparative antibiotic and CDI data. We used Poisson regression to estimate antibiotic use per 1000 resident days (RD) and CDIs per 10,000 RD, pre- and post-intervention. Segmented regression analysis was used to estimate changes in fluoroquinolone and total antibiotic rates over time. Results: Postintervention, the monthly rate of fluoroquinolone days of therapy (DOT) per 1000 RD significantly decreased by 39% [rate ratio (RR) 0.61, 95% confidence interval (CI) 0.59-0.62, P < .001] across all NHs and the total antibiotic DOT decreased by 9% (RR 0.91, 95% CI 0.90-0.92, P < .001). Interrupted time series analysis of fluoroquinolone and total DOT rates confirmed these changes. The quarterly CDI rate decreased by 18% (RR 0.82, 95% CI 0.68-0.99, P ¼ .042). Conclusions and implications: A hospital-NH partnership with a medical director advisory group achieved a significant reduction in total antibiotic and fluoroquinolone use and contributed to a reduction in CDI

This work was supported by a grant from the New York State Department of Health. The Clostridioides difficile infection surveillance was supported by the Centers for Disease Control and Prevention collaborative agreement. The authors declare no conflicts of interest. https://doi.org/10.1016/j.jamda.2019.11.010 1525-8610/Ó 2019 AMDA e The Society for Post-Acute and Long-Term Care Medicine.

* Address correspondence to Ghinwa K. Dumyati, MD, Center for Community Health and Prevention, 46 Prince Street, Rochester, NY 14607. E-mail address: [email protected] (G.K. Dumyati).

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incidence. This approach offers one way for NHs to gain access to AS expertise and resources and to standardize practices within the local community. Ó 2019 AMDA e The Society for Post-Acute and Long-Term Care Medicine.

Antibiotic use is common in nursing homes (NHs), with an annual prevalence ranging from 47% to 79%.1 Antibiotic exposure predisposes NH residents to Clostridioides difficile infections (CDIs) and colonization with multidrug-resistant organisms.2e4 For example, up to 50% of residents are colonized with methicillin-resistant Staphylococcus aureus, and colonization with resistant gram-negative bacilli is increasing.2,5e7 When prescribing patterns are compared to professional society guidelines, NH antibiotic use often appears inappropriate (eg, incorrect drug, dose, duration) or nonindicated (eg, asymptomatic bacteriuria and upper respiratory tract infections).8e15 Use of broad-spectrum antibiotics, such as fluoroquinolones, is also common in NHs.16e18 Fluoroquinolones are associated with a higher risk of CDI,19 and several studies show a reduction of CDI with decreased use of fluoroquinolones and other high-risk antibiotics.20e23 NHs are now required by the Centers for Medicare & Medicaid Services to develop and implement protocols to optimize the treatment of infections, monitor the use of antibiotics, and reduce the risk of antibiotic-associated adverse events including allergic reactions, CDI, and the development of antibiotic-resistant organisms.24,25 Several unique system and population challenges to improving antibiotic prescribing in the NH setting exist. Antibiotics may be overused because of diagnostic uncertainty in frail and cognitively impaired residents, lack of available diagnostic tests at the time of antibiotic prescribing decisions, patient and family members’ expectations, and staffing issues including low nurse to patient ratio and high turnover.13,26,27 Antibiotic stewardship programs (ASPs) in the hospital setting are successful at optimizing antibiotic use and improving patient outcomes.6,19,20,28e31 NHs often lack the antibiotic stewardship (AS) expertise and resources commonly found in acute care. In addition, patients move back and forth between hospitals and NHs, so there is a strong incentive for hospitals to have NHs in their communities with good antibiotic prescribing practices to minimize antibiotic resistance and CDI. Extending acute care AS support to NHs may help NHs achieve their stewardship goals, as well as improve the health of the community served by both the hospital and the NH. We report on a hospital-NH collaborative to reduce CDI incidence by optimizing NH antibiotic use and reducing the use of fluoroquinolones through education, consensus guideline development, and tracking of antibiotic use.

CDI surveillance data from all community NHs were obtained as detailed below. NHs with high CDI rates, and the ability to provide antibiotic use data, were invited to participate; 6 of 33 NHs were enrolled. Facility characteristics at baseline are listed in Supplementary Table 1. The mean NH bed size was 339 (SD ¼ 183). All NHs had a mix of long-term and short-stay (less than 90 days) residents; 2 facilities had long-term ventilator units. Two of the facilities were affiliated with a hospital, with some physicians sharing their time between the 2 settings; however, none of the facilities shared electronic medical records, infection control staff, or pharmacists. The majority of NHs had no elements of AS in place at the time of enrollment. The HBT engaged a voluntary advisory committee initially made up of medical directors of the 6 enrolled NHs and the director of a local geriatric medical group. Over time, additional NH medical directors joined the advisory committee, for a total of 13 members. The advisory committee provided input into the various components of the intervention and met in person at least twice a year. Two medical directors from the committee were asked to provide additional consultation to the HBT and were minimally compensated for their time. Each medical director was responsible for implementing intervention components at their facility. The institutional review board of the University of Rochester Medical Center approved this study. Data Collection The HBT obtained data from the NY Emerging Infections Program (EIP) on the incidence of C difficile infections occurring more than 3 days after NH admission. The EIP conducts active, population and laboratory-based surveillance for incident CDI, defined as a positive C difficile assay on a stool specimen in a county resident with no positive test in the prior 8 weeks. Antibiotic dispenses by resident were obtained from NH dispensing pharmacies. Antibiotic data were often provided in paper or Excel format to be tabulated by the HBT; these methods were described previously.34 Resident days were obtained from the NH or from publicly available NH bed census data.35 CDI incidence and antibiotic use patterns were analyzed at baseline to determine intervention targets; analysis continued on a quarterly basis throughout the project to measure progress. The HBT also obtained total and urinary antibiograms for each NH from local microbiology laboratories to evaluate resistance patterns. Intervention Design

Methods Study Setting and Design Beginning in 2010, we convened a collaborative in Monroe County, NY, aimed at reducing CDI rates in the 4 acute care facilities in the county. As part of this work, representatives from the 4 hospitals formed an AS team, consisting of an infectious diseases physician, stewardship pharmacist, infection preventionist (IP), and project coordinator. After achieving a more than 30% countywide CDI reduction, the team expanded its focus to area NHs, recognizing the NH as a potential reservoir for C difficile and multidrug-resistant organisms.5,32,33 The hospital-based team (HBT) developed a pragmatic, quasi-experimental project to optimize antibiotic use and reduce CDI in community NH using a collaborative model.

The multifaceted, 5-year intervention started in 2014 in 1 NH and moved sequentially to the others based on facility readiness and HBT availability (Supplementary Figure 1). The HBT used the CDC’s core elements for antibiotic stewardship in acute care to guide initial intervention development as the NH core elements were not yet available (Table 1).36,37 Antibiotic data review confirmed that UTI and pneumonia were the most common indications for antibiotic use; fluoroquinolone use was also prevalent (Figure 1). We therefore targeted an improvement in antibiotic use for these indications and antibiotic class. The medical director advisory committee developed consensus testing and treatment guidelines for UTI and pneumonia, promoting improved clinical evaluation to limit overdiagnosis, shortened duration of treatment, and alternatives to fluoroquinolones (Supplementary Material 1).

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Table 1 Details of the Antibiotic Stewardship Intervention in Nursing Homes Core Element

Intervention Details

Leadership commitment

 At each nursing home (NH), the medical director convened a multidisciplinary, introductory meeting to engage key stakeholders including the NH administrator, nursing directors, quality officer, infection preventionist (IP), nurse educator, and if available, the on-site dispensing or consultant pharmacist.  Using a template provided by the hospital-based team (HBT), the medical director and administrator created and signed formal statements to support stewardship efforts in their NH.  Each NH formed a smaller core antibiotic stewardship (AS) team often including the medical director, IP, and in-house pharmacist.  Important stakeholders outside of the team were identified including nurse managers and educators, midlevel providers, and quality staff. Data were shared with these groups by the NH AS team; the AS team also sought input from these groups on the implementation of intervention components.  The HBT team worked with the microbiology lab to develop NH-specific antibiograms and a combined antibiogram for the smaller NHs.  The HBT coached the NH on interpretation of antibiotic data to decide on intervention targets. Guidance on the risks of and alternatives to fluoroquinolones were provided.  The HBT helped the NH to incorporate AS into their daily routine such as developing a method to track and review residents started on antibiotics for urinary tract infection (UTI).  The medical director advisory group and HBT developed community, syndrome-specific guidelines focused on improving testing and treatment for UTI and pneumonia.  The HBT reviewed charts of residents treated for UTI at several NHs to understand the prescribing pathway and provide facility-specific feedback on how testing and treatment for UTI could be improved.  The HBT provided each NH with UTI treatment guidelines based on their specific antibiotic resistance data.  The HBT regularly reviewed antibiotic data to identify other, facility-specific interventions such as improving documentation of antibiotic indication through use of an order sheet and institution of a formal antibiotic time-out process.  The HBT summarized each NH’s antibiotic data and provided feedback during quarterly, face-to-face meetings. Summarized data included the distribution of the most common antibiotics and indications, and antibiotic use rates by days of therapy and number of treated residents for UTI and pneumonia.  Comparative antibiotic and Clostridioides difficile data across NH was also provided.  To transition antibiotic tracking to the NH and promote sustainability, the HBT created antibiotic tracking tools for NH staff to complete.  During face-to-face meetings, the HBT reviewed progress in implementation of the core elements including challenges faced by each NH. HBT provided examples of how other NH overcame these challenges.  The HBT developed several educational modules and materials focused on the community treatment guidelines and general principles of AS. Education consisted of 1. interactive, face-to-face sessions with medical and nursing staff and residents and their family members; 2. printed materials including posters for nursing staff, testing and treatment pocket cards for medical staff, and informational brochures for residents and their families; and 3. regional workshops and invited speaker sessions to share knowledge, tools, and lessons learned from our local project with other NHs.  Education was transitioned over time to the NH staff (medical director, IP, consultant pharmacist).  All educational materials and tools were made available on a public website

Accountability

Drug expertise

Actions to improve use

Tracking and reporting

Education

Fig. 1. Comparison of DOT rate per 1000 resident days by antibiotic class for all nursing homes, pre- and post-intervention. IV, intravenous; PO, oral; TMP-SMX, trimethoprimsulfamethoxazole.

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For each NH, an initial multidisciplinary meeting that included the NH administrator was arranged to ensure leadership support for this project and engage NH staff. The HBT presented comparative baseline CDI data from all participating NHs and highlighted the risk of fluoroquinolones including the risk of CDI. After this meeting, each NH created an AS team, often championed by an IP with a medical director and less often by a consultant pharmacist. These leaders emerged as champions over time, without mandate from senior leadership or additional compensation for their new role. The composition of the other members of the AS teams varied, often including dispensing or consulting pharmacists, nursing leadership, nurse educators, advance practice providers, and the NH administrator. The HBT visited each NH monthly at the start of the project and then transitioned to quarterly visits. At face-to-face meetings, the HBT presented a summary of each NH’s current antibiotic and CDI data, as well as comparison to data from other enrolled NHs. Progress in implementing the core elements was discussed. Additionally, the HBT provided initial face-to-face education to medical and nursing staff on the UTI and pneumonia consensus guidelines. During this education, the HBT interpreted each NH’s antibiogram, highlighting that the most common uropathogen, Escherichia coli, is often resistant to fluoroquinolones. The HBT also reviewed the NH’s emergency box medication inventory and suggested fluoroquinolones alternatives. To disseminate this information, various printed educational materials were created by the HBT, including pocket cards with treatment guidelines, UTI testing guideline posters, and family education pamphlets (Table 1). The HBT also gave presentations to patients and families on the benefit and harm of antibiotics. All educational and data presentations were shared with the medical directors and IPs to adapt to their facility and provide ongoing education. In addition, 5 regional workshops were organized and attended by AS team members from the enrolled NHs and from participants from across the region. Further details of the interventions are in Table 1.

Table 2 Crude Antibiotic Use and Clostridioides difficile Rate Ratios (RRs): Intervention vs Baseline Preintervention Postintervention RR Rate Rate Total DOT 80.5 per 1000 RD Fluoroquinolone 12.3 DOT per 1000 RD C difficile 1.14 infections per 10,000 RD

95% CI

P value

75.3

0.91 0.90, 0.92 <.001

7.5

0.61 0.59, 0.62 <.001

0.93

0.82 0.68, 0.99

.042

18% from 1.14 to 0.93 post-intervention (P ¼ .042, 95% CI 0.68-0.99; Table 2). The downward trend over time of CDI rates across all enrolled NHs is shown in Supplementary Figure 2 (P < .001). We also evaluated the change in total antibiotic and fluoroquinolone use over time, using interrupted time series analysis. For overall antibiotic use, there was a slight trend of increasing use before the educational intervention. Postintervention, the rate declined significantly (level change ¼ 15.48, P ¼ .008; slope change ¼ 1.53, P ¼ .040; Figure 3). For fluoroquinolone use, the rate was decreasing across NHs by 0.13 DOT/1000 RD per month prior to the educational intervention, resulting in an 11.8% decrease. A significant immediate drop in fluoroquinolone use of 2.63 DOT/1000 RD or 20.9% occurred at the time of the intervention (P ¼ .010). Following the intervention, monthly fluoroquinolone use continued to decline by 0.18 DOT/1000 RD (slope change ¼ 0.05; P ¼ .70; Figure 3). Given the low overall rate of CDI in the NHs, we did not achieve power to conduct a segmented regression analysis for CDI. Discussion

Outcomes and Statistical Analysis We used Poisson regression to estimate monthly antibiotic use per 1000 resident days (RD) for fluoroquinolones and total days of antibiotic therapy (DOT), before and after intervention. Quarterly CDI per 10,000 RD was also estimated. The preintervention period for each NH was considered to be 1 year prior to the month of initial education with the exception of NH D, for which only 5 months of preintervention data were available. We report rates, rate ratios (RRs), and the corresponding 95% confidence intervals (CIs). A segmented regression model with first order of autocorrelation was used to assess the extent to which the intervention affected changes in the rates of fluoroquinolone and total antibiotic use per 1000 RD. This method controls for baseline level and trend when estimating expected changes from the intervention. The Durbin-Watson test for data autocorrelation suggests first order of data autocorrelation. Intra-NH correlation was considered when analyzing combined data from all NHs for overall inference. Analyses were conducted using SAS, version 9.4 (SAS Institute, Cary, NC).

Partnership between a hospital-based AS team and an NH medical director advisory group resulted in a significant reduction in total antibiotic and fluoroquinolone use, and contributed to a reduction in CDI incidence across several NHs in Monroe County. This was achieved through implementation of interventions focused on 2 infectious syndromes, UTI and pneumonia, for which antibiotic use is common and often inappropriate. This collaborative approach is a unique model to engage and support NHs that presently do not have the expertise or infrastructure to implement an ASP.

Results Across all NHs, total antibiotic use declined by 9% (P < .001, 95% CI 0.90-0.92), fluoroquinolone use declined by 39% (P < .001, 95% CI 0.590.62) (Table 2), and at least 5 of the 7 core elements were implemented (data not shown). Changes in antibiotic use differed by facility with a decrease in total antibiotic use observed in 4 NHs. A decrease in fluoroquinolone use occurred in all NHs, ranging from 36% in NH C to 77% in NH D (Figure 2). This decrease was seen among all types of fluoroquinolones, including those used for pneumonia and UTI (data not shown). The rate of CDI per 10,000 RD decreased across NHs by

Fig. 2. Percentage change in rates of total antibiotic and fluoroquinolone DOT before and after the intervention by nursing home.

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Fig. 3. Observed rates of total antibiotic and fluoroquinolone DOT before and after the intervention.

We succeeded in significantly reducing fluoroquinolone use by 39%. This was accomplished without a corresponding increase in broad-spectrum antibiotic use postintervention (Figure 1). In fact, overall antibiotic use decreased by 9%. Some specific drugs highlighted in the UTI guidelines decreased (ie, nitrofurantoin), likely due to discontinuing chronic UTI prophylaxis and reducing duration of UTI treatment. We postulate that this change in the prescribing of fluoroquinolones was due to the increasing awareness of NH medical staff to (1) the high prevalence of fluoroquinolone use in their NH through review of facility-specific and comparative antibiotic data, (2) the high resistance of E coli to fluoroquinolones through NH antibiogram reviews, and (3) the risks of fluoroquinolone use, including CDI. The HBT provided regular graphical and tabular data to each NH that was used to engage facilities and monitor progress over time. Deidentified comparison data from other local NHs was shared with the NH AS team and provided to the local quality assurance team at each NH. The HBT also addressed other drivers of antibiotic use in the NHs such as family expectations and the role of front-line staff in the prescribing process38e40 by providing education to nursing staff, residents, and family members through face-to-face meetings, posters, and pamphlets. Although only quarterly for much of the study period, this episodic direct contact was critical to developing and sustaining NH ASP activities. The HBT was able to dedicate significant time to intervention design, including time spent generating data summaries and educational materials because of grant funding to cover this effort. We are currently evaluating the sustainability of these efforts in the absence of external funding and regular HBT involvement. Changing prescribing behavior is challenging.41e43 We surmise that the ability of the enrolled NHs to change their antibiotic prescribing is due primarily to the engagement of the medical directors in collective decision making to establish consensus guidelines that fit the context of the local NHs. Having the NH directors personally own these aspects of infectious syndrome diagnosis and antibiotic selection ensured that the guidelines would be both feasible to implement and sustainable beyond the involvement of the HBT. The importance of this engagement for successful NH AS interventions was previously noted44 and was made evident in our project when 1 NH ASP dissolved upon the medical director’s departure. The inter-NH nature of the collaborative also contributed to the success. The collective data sharing and guideline development fostered a sense of establishing community-wide best practices to combat the community-level problems of CDI and colonization with multidrug-resistant organisms, which even extended to additional local NHs represented on the

advisory team but not directly participating in the collaborative. The collaborative approach also allowed us to use peer comparison to aid in prescribing pattern changes, a behavioral intervention that was successful in other health care settings.45 Education of frontline staff regarding diagnostic stewardship is an important aspect of acute care and NH ASP; however, high turnover of NH staff makes these efforts difficult to sustain. In contrast to the hospital setting, NHs have a limited number of individuals making prescribing decisions. These prescribers also tend to turn over less frequently than frontline nursing staff. It was therefore easier for the HBT to provide consistent education to the NH prescribers and for the medical directors to reinforce this education while onsite at the NH. Champions (often an IP, pharmacist, or medical director) played a vital role in leading or supporting the ASP; this is commonly reported as an important part of quality improvement interventions.46,47 These champions actively collaborated with other team members to monitor antibiotic use data, evaluate treatment appropriateness, and educate providers, staff, residents, and their family members. Additionally, in NHs with an IP champion, regular discussion of treatment or diagnostic issues with the medical director aided in intervention implementation as the medical directors are better able to influence prescribing behavior by providing individual feedback to other prescribers.28 In 1 NH, this feedback was given by a consultant pharmacist champion who focused on all antibiotic orders and provided regular postprescription review to the medical providers. This NH was one of the few enrolled in the project where a reduction in both fluoroquinolone and overall DOT occurred. The pharmacist’s physical presence in the facility on a daily basis, which differs from the monthly availability of most consultant pharmacists, may have played a role in this. Previous efforts have shown that CDI incidence in the NH is complex and related not only to NH antibiotic use, but also to the care residents receive at other locations, including acute care hospitals.32 Downward trends in CDI in NHs in other states were recently reported and postulated to be due to reduced fluoroquinolone use in the acute care setting.48 This may be the case in our current project where CDI decreased by 18% across NHs, but it is difficult to ascertain to what degree this was due to NH factors vs ongoing efforts to combat CDI in our local hospitals.49 As with many infection prevention initiatives, it is likely a combined effect. Our study has several limitations. First, because of the quality improvement nature of the project, we cannot define what aspect of the project was most effective at changing prescribing behavior and

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reducing CDI incidence. Second, we were unable to obtain data on unintended outcomes such as hospitalization or mortality rates. However, the medical directors did not notice any obvious clinical harms from adoption of the guidelines. Third, the ease of data collection varied by NH. Most NHs had an in-house pharmacy to provide dispensing data, but obtaining data from outside pharmacies was more difficult. This may limit the ability to reproduce our work in settings where commercial pharmacies are more prevalent. Fourth, because of the unavailability of antibiotic data with indication prior to the start of our project, we could not measure changes in syndromespecific antibiotic use. We focused only on DOT rather than length of therapy; the latter variable could have added to our assessment of the impact of our treatment guidelines. In addition, we were unable to evaluate how dispensing antibiotic data correlates with antibiotic administration data. Despite these limitations, overall antibiotic use decreased by 9%. Conclusion and Implications

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We report on the collaboration between a hospital-based team with stewardship expertise and a group of NHs in implementing antibiotic stewardship to reduce fluoroquinolone use and C difficile infections. This approach may be 1 way for NHs to gain access to AS expertise and align practices within the local community. Engaging medical leadership at NHs in a consensus-building process for guideline and intervention development aided in ASP implementation. The value of having successful ASP in local NHs needs to be recognized by the broader health care community, which can support dedicated resources to provide education, AS tool development, and data interpretation. Acknowledgments The authors thank staff of all the participating nursing homes, especially the Infection Preventionists and pharmacists; Vince Galetta, MS, RPh, for providing antibiotic dispensing data; Alexandra Yamshchikov, MD, for assistance with the pneumonia consensus guidelines; Brenda Tesini, MD, for her critical review of the manuscript; Travis John, MD, for creating the timeline figure; and Trupti Hatwar, MPH, and Rebecca Tsay, MPH, MLS, for providing Clostridioides difficile infection data.

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43. Fleming A, Bradley C, Cullinan S, et al. Antibiotic prescribing in long-term care facilities: A qualitative, multidisciplinary investigation. BMJ Open 2014;4: e006442. 44. Sloane PD, Zimmerman S, Ward K, et al. A 2-year pragmatic trial of antibiotic stewardship in 27 community nursing homes. J Am Geriatr Soc; 2019 Jul 18 [Epub ahead of print]. 45. Meeker D, Linder JA, Fox CR, et al. Effect of behavioral interventions on inappropriate antibiotic prescribing among primary care practices: A randomized clinical trial. JAMA 2016;315:562e570. 46. Low LF, Fletcher J, Goodenough B, et al. A systematic review of interventions to change staff care practices in order to improve resident outcomes in nursing homes. PLoS One 2015;10:e0140711. 47. Woo K, Milworm G, Dowding D. Characteristics of quality improvement champions in nursing homes: A systematic review with implications for evidence-based practice. Worldviews Evid Based Nurs 2017;14: 440e446. 48. Guh AY, Mu Y, Baggs J, et al. Trends in incidence of long-term-care facility onset Clostridium difficile infections in 10 US geographic locations during 2011-2015. Am J Infect Control 2018;46:840e842. 49. Felsen C, Quinlan G, El-Daher N, et al. City-wide collaboration to reduce Clostridium difficile infections. Open Forum Infect Dis 2015;2:970.

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Supplementary Fig. 1. Timeline of hospital-based team interventions in recruited nursing homes. UTI, urinary tract infection.

Supplementary Fig. 2. Clostridioides difficile infection (CDI) rate per 10,000 resident days in all nursing homes, 2013-2018. Consensus guidelines for testing and treatment of urinary tract infections, Consensus guidelines for testing and treatment of pneumonia.

C.B. Felsen et al. / JAMDA 21 (2020) 55e61

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Supplementary Table 1 Characteristics at Baseline of NHs Included in the Intervention NH

Size*

% of Post-acute Beds

Full-time Medical Director on Site During the Day

Full-Time APP on Site During the Day (No. of APP)

On-Site Pharmacy

EMR

On Call Coverage Provided by In-House Staff

Number of AS Elements in Place

Resident Case Mix Index

Part of Regional Geriatric Group

Date of First Education Session (Baseline)

A B C D E F

Large Medium Large Small Small Large

15 28 5 20 0 .05

Y N Y N N Y

Y Y Y Y Y Y

Y Y Y Y N N

Y N N N Y N

Y Y N Y N Y

0 0 4 0 0 1

1.00 1.30 0.99 1.06 1.03 1.04

N Y Y N Y N

Sep 2014 Feb 2015 Jun 2016 Jun 2015 Nov 2015 Nov 2016

(3-4) (4) (6-7) (2.5) (2) (5)

APP, advanced practice provider; AS, antibiotic stewardship; EMR, electronic medical record. *Nursing home size: small ¼ <200 beds; medium ¼ 200-299 beds; large ¼ >300 beds.