Staphylococcus aureus colonization is common in hospitalized infants. Reference Nurjadi, Eichel and Tabatabai1–Reference Zervou, Zacharioudakis, Ziakas and Mylonakis3 Persistent S. aureus colonization poses risk for the development of infections, Reference Nurjadi, Eichel and Tabatabai1,Reference Zervou, Zacharioudakis, Ziakas and Mylonakis3,Reference Schuetz, Hogan and Reich4 including skin and soft-tissue infections (SSTIs), respiratory tract infections, bacteremia, and musculoskeletal infections. Reference Nelson and Gallagher5 These infections are associated with increased mortality, Reference Ericson, Popoola and Brian Smith6–Reference de Kraker, Davey and Grundmann8 morbidity, Reference Ericson, Popoola and Brian Smith6,Reference Verstraete, Boelens and De7,Reference Weeks, Garcia Prats and Baker9–Reference Boghossian, Page and Bell11 and hospital length of stay, Reference de Kraker, Davey and Grundmann8 and they impose a significant cost burden for families and hospitals. Reference Song, Perencevich, Campos, Short and Singh12
Given the risks associated with S. aureus colonization in neonates, infection prevention (IP) strategies, including contact precautions and hand hygiene measures, are frequently implemented by healthcare workers (HCWs). Reference Akinboyo, Zangwill, Berg, Cantey, Huizinga and Milstone13,Reference Milstone, Elward and Brady14 Although consensus about when active surveillance and decolonization for S. aureus should be performed in the NICU is lacking, Reference Hocevar, Lessa, Gallagher, Conover, Gorwitz and Iwamoto15,Reference Milstone, Song, Coffin and Elward16 these IP measures have traditionally been instituted to prevent methicillin-resistant S. aureus (MRSA) transmission in the neonatal intensive care unit (NICU). However, most S. aureus infections are caused by methicillin-susceptible S. aureus (MSSA), with similar risk for morbidity and mortality as MRSA. Reference Ericson, Popoola and Brian Smith6,Reference Shane, Hansen and Stoll10,Reference Graham, Morel and Zhou17–Reference Popoola, Colantuoni and Suwantarat20 Thus, some centers have implemented IP measures to reduce the risk of MSSA infection. Reference Shahbaz21 Gaps remain in the literature characterizing how NICU HCWs conceptualize their role in the transmission and prevention of S. aureus. We sought to understand HCW perceptions surrounding S. aureus transmission and prevention in the NICU using a qualitative approach. This information can guide future S. aureus prevention interventions, educational initiatives, and research in the NICU.
Methods
Setting and participants
From July to October 2021, we conducted semistructured focus groups with HCWs practicing in the St. Louis Children’s Hospital (SLCH) NICU. This level IV, 150-bed NICU has ∼1,500 admissions annually and has mostly private rooms, with some patient beds in an open-bay layout. Purposive sampling was conducted to include a variety of professions represented in the clinical setting. Clinicians were stratified based on their role: bedside nurses, nurse managers, therapy services personnel (respiratory and occupational therapists), advanced practice nurses, clinical fellows in neonatology, and attending neonatologists. To address and minimize the effect of power differentials on participant dialogue, separate focus groups were conducted for attending neonatologists, neonatology fellows, bedside nurses, and nursing leadership plus advanced practice nurses. Each focus group was conducted by nonhealthcare professionals (S.P. and S.M.) to allow for candid discussion. Focus groups were conducted in person and virtually via Microsoft Teams (Microsoft, Redmond, WA). This study was approved by the Washington University Institutional Review Board. Informed consent was obtained from all participants.
Recruitment
Individuals were recruited through a combination of strategies that are standard for qualitative research in healthcare settings, including flyers posted in the NICU and staff lounge, in-person canvassing of HCWs in the NICU (by S.P. and G.I.), unit-wide emails, and announcements during provider meetings. Reference Webber-Ritchey, Aquino and Ponder22 We conducted focus groups until we reached appropriate diversity in the sample as well as thematic saturation. Reference Guest, Namey and Chen23
Infection prevention procedures at SLCH
Active surveillance for MRSA has been conducted since 2004, wherein all NICU infants are screened for nasal MRSA colonization at admission and weekly thereafter until hospital discharge. MRSA-colonized infants are placed in contact precautions (requiring all HCWs to wear isolation gowns and gloves when entering the patients’ rooms), and they undergo a decolonization regimen (Table 1). In June 2020, active surveillance for MSSA colonization, and decolonization of infants detected to be MSSA colonized, was implemented. The 7-day decolonization regimen includes twice-daily application of mupirocin to the nares, periumbilical, and perianal regions. Infants whose postmenstrual age is >30 weeks receive 3 chlorhexidine baths (on days 1, 3, and 7). On day 4, additional measures include enhanced cleaning and replacement of patient bed, linens, suction tubing and canister, and nasal cannula tubing or ventilator circuit and tubing.
Table 1. Staphylococcus aureus Infection Prevention Policies and Protocols at SLCH Level IV NICU
Note. NICU, neonatal intensive care unit; MRSA, methicillin-resistant Staphylococcus aureus; MSSA, methicillin-susceptible S. aureus; IP, infection prevention; CHG, chlorhexidine gluconate.
Data collection
A semistructured interview guide was created using input from a multiprofessional team with expertise in neonatology, infectious diseases, IP, and qualitative methods. The questions addressed HCW perceptions and practices regarding the clinical significance of MRSA and MSSA colonization, transmission dynamics, challenges to IP, and potential interventions to reduce transmission.
Data analysis
Interviews were recorded and transcribed using Microsoft Teams software (Redmond, WA). The transcripts were deidentified and reviewed (S.P.) to ensure accuracy. Deductive coding was used in this analysis, and 3 authors (S.P., S.M., and S.F.) developed the original code book based on prior literature comprising infection prevention in the healthcare setting. The code book was updated, including the addition of 1 code, and updates were made to definitional clarity and examples after the 2 coders met to discuss coding discrepancies. The final code book is provided in the Supplementary Materials (online). Transcripts were double-coded by 2 independent authors (S.P. and S.M.) using NVivo software. Discrepancies between the coders were discussed until consensus was reached, and disputes were settled by a third coder (S.F.). Following coding, we conducted thematic analysis to understand the patterns and recurrences in the coded transcripts.
Results
We conducted 10 semistructured focus groups with 38 NICU HCWs. Participants included 6 attending neonatologists, 3 neonatology fellows, 3 therapists, 10 bedside nurses, 15 nurse leaders or educators, and 1 advanced practice nurse. There was 100% participation by all consented HCWs. Focus groups lasted 40–90 minutes, and each was comprised of 1–12 participants. Four themes emerged: (1) MRSA and MSSA are inconsistently described as high risk. (2) IP interventions are burdensome. (3) Multiple sources of transmission are recognized. (4) opportunities exist to advance IP. In Table 2, we present nonexhaustive, example quotes to illustrate the findings within each theme. Reference Eldh, Årestedt and Berterö24 Additional example quotes are provided in the Supplementary Table (online).
Table 2. Nonexhaustive, Example Quotes Within Each Coding Theme to Illustrate Findings
MRSA and MSSA are inconsistently described as high risk
Participants discussed the risk of MRSA in 3 ways: risk to patients, risk to themselves, and risk compared to MSSA. Clinicians did not communicate great concern about the development of infection in infants colonized with either MRSA or MSSA. Those expressing less concern often cited their perception of a low frequency of invasive S. aureus infections in their NICU to support their belief. Many who expressed great concern attributed their risk perception to either a memorable personal experience caring for an extremely ill patient or recognized specific patient risk factors that pose increased infection vulnerability (Table 2, quote 1.1).
Physician focus groups viewed MSSA as less clinically relevant than MRSA, whereas nursing groups were less certain about the clinical differences between MSSA and MRSA (Table 2, quote 1.2). All groups expressed the perception that MSSA decolonization was often less successful than MRSA decolonization (ie, patients remained persistently colonized with MSSA or frequently reacquired colonization after a period of eradication).
Overall, HCWs were not worried about their personal risk for S. aureus infection. However, several communicated concern about bringing pathogens from the hospital to their children at home. Participants commonly expressed that working in healthcare would be extremely difficult if they constantly worried about personal infection risk.
Infection prevention interventions are burdensome
HCWs described how IP interventions, including contact precautions, patient screening, patient decolonization, and environmental cleaning, placed burden on patients, families, and clinicians. Clinicians were primarily concerned about the physical and emotional burden on families. HCWs emphasized that patients on isolation were stigmatized, resulting in less interaction by HCWs and potentially resulting in delayed social development. When discussing colonization status and subsequent interventions, clinicians described communication strategies in which they attempted to minimize the blame and burden placed on families by framing MRSA as a common nosocomial disease (Table 2, quote 2.1).
HCWs identified contact precautions and environmental cleaning as substantial burdens. Clinicians described challenges when trying to follow contact precautions and often cited these challenges to explain drifts in practice. These barriers fell into 4 broad categories: general workflow interruptions, emergent scenarios, quick events, and confusion about patient isolation status.
Participants reported that contact precautions disturbed their normal workflow. Gowns were described as hot and uncomfortable, which limited the amount of time individuals stayed in rooms of patients requiring contact precautions. Physician groups described how isolation requirements changed the order of their examinations before rounds, as well as how often and how long they spoke with families in these rooms (Table 2, quote 2.2).
All clinicians expressed that it was difficult to adhere to contact precautions when a patient was clinically decompensating. They described a prioritization of the immediate clinical needs of the patient over any potential infection risk posed by not wearing a gown when entering the patient’s room. However, HCWs also identified nonemergent scenarios, such as turning off a feeding pump or silencing an alarm, which would lead to a drift in practice. Some HCWs expressed the perception that they were not contributing to S. aureus transmission if they quickly went into a room and did not touch the patient. Physicians recognized unique barriers for teams not based in the NICU (eg, consulting services), citing that these groups may be unfamiliar with the signage indicating infants requiring contact precautions. Focus groups with nursing leadership also recognized that policies to discontinue contact precautions (Table 1) are confusing for staff members (Table 2, quote 2.3).
Clinicians also described a large work burden associated with required environmental cleaning. Nurses described time constraints that made it difficult at the beginning of each shift to follow environmental cleaning protocols that are completed in all patient rooms. In addition to daily cleaning, a large cleaning effort on day 4 of the decolonization protocol (Table 1) was perceived to be a uniquely heavy, albeit necessary, burden. Many nurses also expressed frustrations about systemic barriers to environmental cleaning such as inadequate availability of cleaning supplies.
Recognition of multiple sources of transmission
HCWs described their impressions of how people and environmental surfaces could be sources of transmission. Nearly every focus group perceived families as the main source of S. aureus in the NICU. Common explanations for this perception included families being less educated about IP and hand hygiene and the fact that families are not required to follow contact precautions (Table 2, quote 3.1). Participants acknowledged that HCWs could be a source of transmission, although they discussed that they were unaware of robust supporting data.
HCWs recognized how hospital surfaces act as sources of transmission and described how people, including themselves, may spread S. aureus from these surfaces to patients via physical contact (Table 2, quote 3.2). Often, participants pointed to the burden and challenges faced with contact precautions and other protective equipment to explain the drift in practice that would lead to HCWs transmitting S. aureus from the environment to patients. In addition to hospital surfaces, HCWs frequently discussed how families might introduce S. aureus into the NICU through their personal belongings, especially cell phones.
Opportunities to advance IP
HCWs identified several areas for future IP, including interventions targeting families, scrub sinks, and ultraviolet technology. Participants expressed interest in families playing a larger part in IP. They described possible interventions surrounding education, hand hygiene, family screening, and family decolonization. In line with their approach to minimize blame and stigma when communicating to families about S. aureus, HCWs expressed more favorable views toward interventions that focused on empowering or educating families (Table 2, quote 4.1). To this end, HCWs hesitated to offer decolonization immediately after the patient’s first positive colonization screening test and instead were in favor of offering families decolonization the second time that a patient tested positive.
Other potential interventions were also shared frequently across all focus groups. There was a high level of interest in bringing back scrub sinks and increasing the use of ultraviolet technology to decontaminate personal belongings and hospital equipment. Although these interventions were often discussed favorably, HCWs strongly expressed that they wanted to assess the evidence surrounding any intervention before implementation. To understand HCW perceptions, we specifically queried participants about 2 MRSA IP practices that have previously been implemented during outbreak settings: periodic HCW worker screening and periodic HCW decolonization without screening. Reference Milstone, Budd and Shepard25–Reference Albrich and Harbarth27 Overall, there was a lack of interest for either intervention due to concerns about stigma from patients’ families, altered work schedules due to testing positive, and the further development of antibiotic-resistant bacteria.
Discussion
Few studies have characterized how HCWs conceptualize infectious disease transmission and prevention in acute-care settings. We assessed NICU HCW perceptions regarding S. aureus disease severity, sources of transmission, challenges to IP, and opportunities for future interventions within a NICU that practices active surveillance for S. aureus colonization, contact precautions, and decolonization. The findings from this study illuminate areas for future education and research and highlight the need to re-evaluate or redesign current IP strategies.
During our focus groups, in general, HCWs did not express a high level of concern regarding S. aureus colonization among NICU patients, or the risk colonization poses for subsequent infection. Reference Rycroft-Malone, Seers, Titchen, Harvey, Kitson and McCormack28 However, there was variability in individual HCW perceptions; those with personal experience caring for critically ill neonates with S. aureus infection voiced concern about S. aureus colonization and infection risk. The lack of concern regarding colonization was even more pronounced for MSSA, which HCWs believed to be less clinically relevant than MRSA. In turn, the utility of MSSA screening and decolonization was questioned. Multiple studies have demonstrated that S. aureus colonization, with either MRSA or MSSA, indeed poses increased risk, by up to 24-fold, for the development of invasive infection in neonates. Reference Nurjadi, Eichel and Tabatabai1,Reference Zervou, Zacharioudakis, Ziakas and Mylonakis3,Reference Schuetz, Hogan and Reich4,Reference Ericson, Popoola and Brian Smith6,Reference Popoola, Colantuoni and Suwantarat20,Reference Milstone, Voskertchian and Koontz29 Nationally, the incidence of MSSA invasive infection exceeds MRSA invasive infection by 2.5-fold, with similar risk for morbidity and mortality. Reference Ericson, Popoola and Brian Smith6,Reference Shane, Hansen and Stoll10,Reference Graham, Morel and Zhou17–Reference Popoola, Colantuoni and Suwantarat20 Additionally, implementation of MSSA surveillance and decolonization in the NICU setting has been associated with a sustained reduction in MSSA infections. Reference Popoola, Colantuoni and Suwantarat20,Reference Voskertchian, Akinboyo, Colantuoni, Johnson and Milstone30 Hence, our focus groups revealed an opportunity to educate HCWs with both local and national data demonstrating the substantial risk of infection associated with S. aureus colonization (MRSA and MSSA), the morbidity and mortality associated with these infections, and the reduction in infection incidence with decolonization and other IP measures.
HCWs perceived initiatives to prevent S. aureus acquisition and transmission, particularly personal protective equipment and environmental cleaning, to be a substantial burden. Inconsistencies in adhering to contact precautions were identified, and efforts to decontaminate environmental surfaces were felt to be difficult in the context of performing patient care. However, environmental surfaces are important reservoirs for S. aureus, and enhanced cleaning has been demonstrated to reduce MRSA transmission and acquisition in these settings. Reference Huang, Datta and Platt31–Reference Datta, Platt, Yokoe and Huang33 Further compounding these challenges, consensus regarding optimal IP practices is lacking. For example, institutions vary regarding practices such as surveillance, decolonization, and universal gloving. Reference Hocevar, Lessa, Gallagher, Conover, Gorwitz and Iwamoto15,Reference Milstone, Song, Coffin and Elward16,Reference Nist, Pickler and Harrison34 This inconsistency underscores the need for future studies that incorporate the realities of these complex settings to ultimately devise effective, yet minimally burdensome, IP measures.
HCWs overwhelmingly attributed families as the primary source of S. aureus transmission to NICU infants. A study conducted at Johns Hopkins University demonstrated that, among NICU patients who acquired S. aureus colonization during their hospitalization, approximately half became colonized with a strain that was also recovered from their parents, while the remaining half became colonized with a non–parental-concordant strain. However, infant acquisition of nonparental S. aureus strains was also identified. Reference Milstone, Voskertchian and Koontz29 These data suggest that although parents play a role in S. aureus transmission, other sources, including HCWs and environmental reservoirs, may be important contributors as well. Reference Stein, Navon-Venezia and Chmelnitsky35–Reference Geva, Wright, Baldini, Smallcomb, Safran and Gray37
Our data reveal specific IP opportunities with variable buy-in from HCWs. HCWs favored initiatives focused on family education compared with those that targeted HCWs or that restricted families through mandatory policies. HCWs also responded favorably to offering families the option to perform decolonization. Given the success of parental decolonization in reducing the prevalence of S. aureus colonization in neonates in one study, Reference Milstone, Voskertchian and Koontz29 this may be a viable route to pursue. Their support of these family-focused initiatives may be consistent with their belief that families were the primary source of transmission. On the other hand, HCW screening and decolonization initiatives were viewed less favorably by HCWs due to concerns about confidentiality, altered work schedules, and antibiotic resistance. Thus, while the efficacy of screening and decolonizing HCWs may be indicated in specific scenarios, the threshold for implementation is high.
An important strength of this study is the cumulative knowledge derived from the engagement of diverse cohorts of frontline clinicians engaged in the delivery of critical care. This study had several limitations. First, we used a variety of recruitment strategies to obtain this sample, which resulted in a lack of ability to track overall response rate. Moreover, this sample represents individuals who self-selected to participate. This study was conducted at a single site and may not be generalizable to other settings, especially since reported HCW attitudes may be influenced by institutional practices, including active surveillance and decolonization, which vary among institutions. Lastly, data were collected through focus groups; this setting may have led participants to alter or limit their responses. Similar research that employs individual interviews or even anonymous surveys could further explore this topic.
In conclusion, using focus groups, we characterized HCW attitudes surrounding S. aureus in the NICU. We illuminated HCW perceptions regarding the risk posed by S. aureus colonization, particularly MSSA, which in turn may contribute to drifts in IP practices and perceived burdens associated with IP procedures. Our data highlight the importance of educating HCWs about mechanisms of transmission, infection risk, and the rationale for IP practices. Sharing local and published data may increase adherence to infection control practices. Moreover, addressing systemic challenges to reduce work burden is also essential. Enhancing HCW knowledge and relieving work burden could improve IP efforts and mitigate S. aureus in NICU settings.
Supplementary material
To view supplementary material for this article, please visit https://doi.org/10.1017/ice.2023.86
Acknowledgments
We thank Jessica Britton (assistant nursing manager) and Colette Penaloza (assistant nursing manager) for their assistance with study recruitment.
Financial support
This work was supported by the Children’s Discovery Institute of Washington University and St. Louis Children’s Hospital through the Pediatric Student Research Program.
Competing interest
All authors report no conflict of interest in publishing this material.
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