Introduction
Patients undergoing chronic hemodialysis have multiple risk factors for Staphylococcus aureus infections. Over a third of patients undergoing dialysis carry S. aureus in their nares, which increases their risk of access-related S. aureus bloodstream infections (BSI) by almost four-fold. Reference Saxena, Panhotra and Venkateshappa1 In fact, their risk for methicillin-resistant S. aureus infections is 100 times that of the average person. Reference Rha, See and Dunham2 The nares are the primary reservoir for S. aureus and from there they can contaminate patients’ skin Reference Boelaert, Van Landuyt, Gordts, De Baere, Messer and Herwaldt3 and be spread between patients in a hemodialysis unit through contaminated furniture, equipment, or healthcare professionals’ (HCP) hands. Reference Grothe, Taminato, Belasco, Sesso and Barbosa4
The Society for Healthcare Epidemiology of America, Infectious Diseases Society of America, and Association for Professionals in Infection Control and Epidemiology recently recommended that dialysis units consider targeted or universal decolonization of patients on hemodialysis. Reference Popovich, Aureden and Ham5 Intranasal mupirocin decolonizes S. aureus carriage and can reduce infection rates for patients undergoing chronic hemodialysis. Reference Boelaert, Van Landuyt, Gordts, De Baere, Messer and Herwaldt3,Reference Nair, Perencevich, Blevins, Goto, Nelson and Schweizer6–Reference Vasquez, Walker, Franzus, Overbay, Reagan and Sarubbi10 However, mupirocin decolonization can be difficult to implement and routine use may lead to mupirocin resistance. Reference Fisher, Golestaneh, Allon, Abreo and Mokrzycki7,Reference Tacconelli, Carmeli, Aizer, Ferreira, Foreman and D’Agata8,Reference Vasquez, Walker, Franzus, Overbay, Reagan and Sarubbi10,Reference Smith and Herwaldt11 Intranasal povidone iodine (PVI) has been used to suppress S. aureus and to prevent infections in surgical settings and nursing homes. Reference Miller, McKinnell and Singh12–Reference Monstrey, Govaers, Lejuste, Lepelletier and Ribeiro de Oliveira16 Compared with mupirocin, nasal PVI may be preferred given its price, patient preferences, and mechanism of action, which makes PVI resistance unlikely. Reference Phillips, Rosenberg and Shopsin14–Reference Maslow, Hutzler, Cuff, Rosenberg, Phillips and Bosco17
We evaluated the implementation of nasal PVI in the novel setting of outpatient hemodialysis units during a pragmatic multicenter stepped-wedge cluster randomized trial that studied both PVI’s effectiveness and PVI implementation strategies. We previously described the study protocol. Reference Racila, O’Shea and Nair18 We aimed to evaluate HCP’s satisfaction with PVI decolonization and identify practical strategies that facilitate PVI decolonization in outpatient hemodialysis units.
Methods
We conducted a qualitative descriptive study and evaluation to identify factors affecting implementation of PVI nasal decolonization during our trial (conducted from June 1, 2020 to May 31, 2023). We conducted interviews and performed thematic analysis on transcripts.
Settings and processes
During this stepped-wedge trial, we implemented nasal PVI decolonization at 16 outpatient hemodialysis units affiliated with 5 US academic medical centers in 3 geographic regions. Reference Racila, O’Shea and Nair18 Participating units served a range of patient populations and included small rural units, mid-size urban and suburban units, and large urban units. The population of patients receiving dialysis in participating units ranged from 14 (two smallest units) to 203 (largest unit). Five units were operated by external hemodialysis providers contracted by the academic medical center. We translated patient-facing material into Spanish, French, and Mandarin Chinese. We asked patients to apply PVI to their nares before each hemodialysis session, at the unit, or at home.
Data collection
The research team developed and piloted in-depth, semi-structured interview guides. We invited all research coordinators and staff at all hemodialysis units to participate. To increase participation, we also conducted site visits to seven hemodialysis units affiliated with three of the five partner universities. Qualitative experts conducted single and group interviews on virtual platforms, by phone, or in person. Interviewees included nurses, hemodialysis technicians, research coordinators, and other clinical and non-clinical personnel. We audio-recorded and transcribed interviews, and then imported transcripts into MAXQDA software. 19
Data analysis
We conducted thematic analysis of transcripts concurrent with data collection. The experienced qualitative team (KCD, SHS, AMR) collaboratively developed a thematic codebook that incorporated both a priori codes identified in the study’s design and inductive codes that emerged from interview data. First, we independently read a subset of transcripts (n = 4) to identify potential inductive codes, then met weekly using consensus to create and modify the codebook. To ensure coding fidelity given the variety of participant types, we coded seven transcripts using consensus, or negotiated, coding methodology. Reference Garrison, Cleveland-Innes, Koole and Kappelman20,Reference Kuckartz21 Subsequently we divided coding responsibilities and met weekly to resolve any coding ambiguities, and systematically documented discussions and rationales for codebook modifications. We periodically asked the principal investigator and site leaders to help us interpret emerging findings.
For this manuscript, we organized findings into four categories: trial context, patient-related factors, HCP-related factors, and strategies and tools to facilitate engagement of patients and HCPs. We chose to report trial-related barriers and facilitating factors to briefly provide context on PVI decolonization during the trial. We decided to present thematic findings about acceptability and engagement and perceptions of infection risk within sections divided by patient and HCP factors, because we wanted to identify elements common across trial units that could assist hemodialysis unit leaders interested in planning to implement PVI decolonization in their units.
The University of Iowa Institutional Review Board approved the study for three academic medical centers. The Institutional Review Boards at Emory University and University of Illinois Chicago approved the study for their sites.
Results
We interviewed sixty-six participants. All interviewees worked in participating units or as research team members assisting participating units. No patients were interviewed. We report interviewee roles in Table 1. We provide exemplar quotes in Table 2.
Table 1. Summary of interviewees by role
Table 2. Selected exemplar quotes illuminating themes
Note. HCP, healthcare personnel; RP, research personnel.
Trial context: summary of barriers and facilitating factors
Interviewees reported that hemodialysis units had varied success in recruiting patients and ensuring PVI was available to patients. Factors facilitating PVI use included educating patients and HCPs on infection risk; tailoring communication for specific patients; engaging unit staff, including non-clinical staff (eg, education specialists); ensuring that patients had access to PVI supplies and helping them apply PVI as needed; planning how to facilitate PVI use within available clinical space, and creating and using patient-friendly tools and strategies. Conversely, significant barriers included limited staffing, poor staff engagement, and perceived limited knowledge of patients’ infection risk among patients and some HCPs.
Interviewees identified important barriers to engaging HCP in PVI implementation during the trial, including high staff turnover, increased workload, and new infection-prevention protocols to prevent spread of SARS-CoV-2. Demonstrating these obstacles, interviewees at some sites reported staffing challenges that reduced their capacity to support the study. Interviewees also noted that clinical duties had increased, which reduced time for staff education. Consequently, some staff felt uninformed about PVI, and occasionally interviewees reported that they had actually learned about the PVI trial from participating patients. Additionally, interviewees perceived that PVI application was an add-on rather than an integral part of patient care. A further burden for staff was the variation in patient participation. Since patients could opt in or out of the study multiple times, HCP felt they did not have time to figure out patient participation while they were focusing on other tasks.
Trial context: COVID-related barriers and infection-prevention fatigue
Interviewees reported that during the trial, the COVID-19 pandemic radically affected outpatient hemodialysis units, increasing HCP’s workload and stress. They pointed out that newly instituted infection-prevention practices—social distancing, universal masking, staggered patient arrivals, and waiting room restrictions—complicated both staff members’ workflow and their ability to integrate PVI application into their workflow. Consequently, both HCPs and patients experienced “infection prevention fatigue.” Furthermore, according to interviewees, both HCP and patients perceived that masking and social distancing could protect patients from other infections, which may have reduced their interest in or commitment to further infection-prevention activities like PVI decolonization.
Patient-related factors
Throughout this section, we provide perspectives from interviewees (HCP and trial coordinators), who reported their own perceptions of patient attitudes and practices.
Acceptability and engagement
Interviewees reported that patients who used PVI generally found it acceptable. Interviewees did not report witnessing any major adverse or side effects and they noted that most patients were able to apply the PVI without assistance. However, interviewees described that some patients were unwilling to participate in research or were worried about iodine allergies. Study materials were available in four languages but some interviewees noted that the lack of other languages was a potential obstacle to engaging or educating patients about PVI use. Interviewees described patient-level challenges to PVI use. They reported that a small number of patients needed help applying PVI due to visual impairments or difficulty opening PVI bottles or applying PVI with the one hand they could use during dialysis. Interviewees also reported that some patients were too overwhelmed by health or life issues to add another task. Other patient-level barriers included depression, memory issues, lack of social support, and living situations that did not facilitate infection-prevention measures. Interviewees also reported that some patients expressed to them that nothing they did would improve their health and, thus, were unwilling to add infection-prevention practices. Some patients who used PVI at home told interviewees that using a calendar and incorporating PVI into their daily routines (eg, applying PVI when they did other personal hygiene activities like tooth brushing) was helpful.
Perceptions of infection risk
Interviewees reported that patients’ perceptions of their own infection risk could be either a facilitating factor or a barrier. For example, interviewees stated that patients who regularly used PVI (3 times per week) often noted their high infection risk and said they used PVI because they perceived direct benefits to themselves. Moreover, some patients told interviewees that they used PVI on non-dialysis days (eg, when shopping) and some requested access to PVI after the study ended. Conversely, interviewees reported that some patients were unaware of or unconcerned about their infection risk or were unaware that other patients had acquired serious infections and, thus, were unwilling to implement routine infection-prevention practices (eg, washing access sites). Some interviewees suggested that patient-centered conversations with trusted HCPs could improve patients’ understanding of their infection risk and the need for prevention measures, which could foster patients’ interest in using PVI.
HCP-related factors
Acceptability and engagement
Interviewees generally found the PVI-related activities acceptable but did not feel the activities fit into their clinical workflow if they needed to first ascertain whether individual patients had consented. Clear communication about PVI’s potential benefit to patients and leadership support were reported to facilitate HCP engagement. According to interviewees, the level of intervention support varied across hemodialysis units, including some within the same academic institution. At some units, local clinical leaders (eg, nephrologists) strengthened implementation by expressing explicit support in staff meetings or discussing the trial directly with patients. However, interviewees at a few units reported that unit leaders were minimally involved in the study and that staff and patients who lacked knowledge about the intervention were not engaged.
Interviewees perceived that implementing PVI could be feasible and acceptable, particularly if integrated into routine practices for all patients and if HCPs were persuaded that PVI could help protect their patients from serious infections. Nevertheless, several interviewees identified workflow as a potential obstacle for some units and suggested that an alternative might be implementing PVI decolonization only for patients most at risk for access-related BSI.
Perceptions of infection risk
Interviewees noted that some HCPs thought their patients seldom had BSIs, and thus additional infection-prevention activities were unnecessary. Some interviewees suggested that they or their peers could also benefit from clear, evidence-based, recurring education about patients’ risks for access-related BSIs and potential benefits of PVI decolonization.
HCPs identified themselves as important advocates for infection prevention and appropriate, trusted partners in conversations with patients about infection risk and prevention. Some interviewees suggested that dietitians, education specialists, social workers, and clinic receptionists could encourage patients to use PVI or answer their questions and that dietitians and educators particularly could help patients develop strategies to integrate PVI into their routines.
Strategies and tools to facilitate engagement of patients and HCP
Interviewees identified the following facilitating factors for PVI use on the unit, both during the trial or for wider clinical implementation: a designated accessible space where patients picked up their own PVI bottles and swabs or PVI delivery to patients at their chairs, and individual trash cans near patients’ chairs in which to dispose of used PVI and packaging. To support engagement of both patients and HCP, interviewees reported leadership support of PVI use, clear communication about infection risk and the potential role of decolonization, and deliberate and repeated messaging about PVI to HCP and patients in staff meetings, one-on-one discussions, and through videos and flyers.
Tools used during the study (Table 3) included signs and flyers; three-dimensional plastic noses to use while demonstrating PVI application; “take home” bags containing a month’s supply of PVI, tracking materials (eg, calendar or checklist), and instructions for PVI use; and instructive videos and flyers. Interviewees found study material acceptable. However, they recommended tailoring materials for different patient populations in the future. For example, interviewees also recommended any new educational material aimed at either HCPs or patients use simple, direct language; translation or interpretation; multiple formats; and images that reflected the unit’s patient population, specifically with respect to race and/or ethnicity. They also suggested developing additional videos or infographics discussing patients’ infection risk or sharing personal stories of patients who acquired serious infections.
Table 3. Tools used and purposes.
Note. HCP, healthcare professionals; PVI, povidone-iodine
Discussion
Our interviews with staff in outpatient hemodialysis units suggest that PVI nasal decolonization to prevent S. aureus BSI among patients on hemodialysis could be feasible. However, we also identified numerous barriers to engaging HCPs and patients in our trial. Our interviewees reported that many patients found nasal PVI acceptable. Similarly, HCP felt that nasal PVI could be incorporated into clinical practice if hemodialysis units decided that routine S. aureus decolonization was a patient-safety goal.
Nevertheless, engaging patients in novel infection-prevention practices is difficult. Patients undergoing hemodialysis have high rates of depression and anxiety, Reference Khan, Khan, Adnan, Sulaiman and Mushtaq22–Reference Jones, Harvey, Harris, Butler and Vaux25 which can reduce adherence. Reference Alosaimi, Asiri and Alsuwayt26,Reference Cukor, Rosenthal, Jindal, Brown and Kimmel27 Jones et al found that hemodialysis processes create multiple stresses and that patients’ cognitive and physical well-being can fluctuate across the dialysis cycle. Reference Jones, Harvey, Harris, Butler and Vaux25 The interviewees in our study noted that obstacles included the overall high health burden for patients, depression, and cognitive issues. Units could consider how to support patients in integrating PVI decolonization into their routines to minimize patient burden.
Patient perspectives might also facilitate implementation. A scoping review of patient involvement in infection prevention and control concluded that HCPs and patients should collaborate to improve implementation of guidelines and associated interventions. Reference Fernandes Agreli, Murphy, Creedon, Ni Bhuachalla, O’Brien and Gould28 More specific to the hemodialysis setting, several groups have found that patients undergoing hemodialysis have crucial perspectives on infection-prevention practices and their own roles. Reference Kim and Lee29–Reference Gray, Toy, Dalla-Bona, Broom and Gray33 We did not interview patients. Future work should investigate what patients know about their infection risks and what they are willing to do for prevention. We should also test the efficacy of various engagement and educational strategies in different populations of patients on hemodialysis to help us develop more effective strategies for engaging patients in novel infection-prevention activities such as PVI nasal decolonization.
Similarly, HCPs also experience barriers to engaging in new infection-prevention practices. A large needs assessment conducted by Fitzgerald et al identified barriers to implementing infection prevention and control practices in hemodialysis units, including HCPs’ time constraints/high patient volumes, lack of motivation and knowledge, and low patient engagement. Reference Fitzgerald, Tyner, Drake, Beach, Rupp and Schwedhelm34 Our interviewees identified similar barriers in their units. Over the past 30 years, HCPs in dialysis units have reported experiencing stress and burnout. Reference Böhmert, Kuhnert and Nienhaus35 This has been exacerbated during the COVID-19 pandemic. Reference Pawłowicz-Szlarska, Forycka and Harendarz36 Our study also found HCPs’ work stress reduced their capacity to take an active role in the trial, and thus work stress may impede implementation of new infection-prevention measures. However, McAlearney et al found that nurses’ perspectives and action could improve implementation of a central-line-associated BSI prevention initiative. Reference McAlearney and Hefner37 This suggests that infection-prevention staff who wish to implement intranasal PVI to decrease S. aureus infections in hemodialysis settings must understand work processes in dialysis units and must work directly with unit staff to develop a protocol that works for staff and patients.
Multiple studies have shown that patients undergoing hemodialysis are at high risk for S. aureus infections. Reference Saxena, Panhotra and Venkateshappa1,Reference Rha, See and Dunham2 A study by Rha et al found that the risk of S. aureus BSI is also higher for non-Hispanic Black or African American patients and Hispanic or Latino patients than for white patients. Reference Rha, See and Dunham2 Nevertheless, Pedersen et al recently found that most HCPs working in an academic medical center who responded to a survey were unaware that healthcare associated infection (HAI) rates vary by race and ethnicity. Reference Pedersen, Pryor and Bearman38 Interviewees in our study also did not discuss racial or ethnic differences in infection risk, suggesting there is an opportunity to improve understanding and develop interventions to reduce those disparities. In addition, interviewees reported that patients and some HCPs underestimated patients’ infection risk in general. In fact, some HCPs felt their patients were unlikely to acquire BSIs. This misunderstanding was a major barrier to implementing intranasal PVI decolonization. Thus, an early step in the integration of infection-prevention interventions like intranasal PVI into clinical practice, would be to increase HCPs’ and patients’ awareness of the patients’ infection risk in order to increase their willingness to adopt preventive measures.
This study has limitations. We implemented PVI decolonization as part of an implementation-effectiveness clinical trial testing whether it would reduce BSIs; however, the COVID-19 pandemic not only reduced hemodialysis units’ ability to actively implement the intervention but also increased other infection mitigation practices. While the 16 participating hemodialysis units included a wide range of patients and units, all were located in the US and other countries might experience different barriers. Additionally, implementation of a practice as part of a study can differ from implementation as clinical practice. In our trial, patients could consent or decline to participate, and HCPs were not required to deliver the intervention. Given the units’ challenges, research staff facilitated implementation. Thus, we may have missed some barriers or facilitating factors to implementing PVI decolonization as part of routine practice. We had limited access to HCP at some units and thus needed to elicit the local context from research coordinators, and we did not interview patients directly. Thus, assumption bias may affect our findings. Nevertheless, our findings were consistent across units.
While engaging HCP was difficult during the clinical trial, the results from our qualitative study suggest that both HCPs and patients would find PVI decolonization acceptable. Our results suggest that implementation of PVI decolonization could be feasible for outpatient hemodialysis units if it is supported by clinical leaders, HCPs are engaged, HCPs and patients understand the risk of infection and the role of decolonization in preventing infection, and PVI application is integrated into routine clinical care.
Financial support
This project was funded by grant number R01HS026724 from the Agency for Healthcare Research and Quality (AHRQ) within the U.S. Department of Health and Human Services (HHS). Povidone-iodine product was donated by 3M (funding number ISR74). The authors of this manuscript are responsible for its content. Statements in the manuscript do not necessarily represent the official views of, or imply endorsement by, AHRQ or HHS.
Competing interests
The authors have no declarations of interest.
Clinical trial information
ClinicalTrials.gov Identifier: NCT04210505, https://clinicaltrials.gov/.
Open access
