Changes in perceptions of antibiotic stewardship among neonatal intensive care unit providers over the course of a learning collaborative: a prospective, multisite, mixed-methods evaluation

Participants

Pre-OASCN, we interviewed site leaders from 30 NICUs; 26 (87%) of whom also completed the post-OASCN interview. The pre-OASCN survey was sent to 349 eligible prescribers across the units, of whom 256 (73%) responded. In the post-OASCN survey, we received 194 (63%) responses among the 309 fielded surveys. A total of 297 individuals participated in either the pre- or post-OASCN survey. For any individual NICU, we received responses from at least 50% of associated prescribers at a given site in the pre-OASCN survey (between 2 and 24 prescribers per site) and 40% in the post-OASCN survey (between 2 and 17 prescribers per site). Table 1 describes the 297 individuals who completed either the pre- or post-OASCN survey, and those that completed both surveys i.e., the longitudinal cohort (N = 166, 65% of the cohort that took the pre-survey). The majority of participants were neonatologists, followed by neonatal fellows, hospitalists/pediatricians, and advanced practice providers (nurse practitioner or physician assistant). Additionally, the majority of respondents had at least 10 years of experience in their roles (excluding fellows), with a plurality spending most of that time at their current site. The longitudinal cohort was similar to the entire sampled cohorts in the distribution of these characteristics (Table 1).

Table 1 Sample characteristics of respondents to the OASCN prescriber survey (pre- and post-intervention).Perceptions of current antibiotic practice

Within the longitudinal cohort overall, >76% of prescribers characterized their units’ antibiotic use practice as having “little” or “very little” inappropriate prescribing, which did not vary significantly pre- versus post-OASCN (Table 2). Looking by collaborative role, site leaders at the pre-OASCN time point reported significantly higher perceived appropriate antibiotic use than other prescriber participants (92% v 73%, 3.62 v. 3.13, p = 0.01; Table 3), however this difference between groups was no longer significant by the post-OASCN survey. Perceptions of appropriate prescribing also did not vary significantly by participation in OASCN Learning Sessions (Table 4), nor by clinical role (neonatologists versus other prescribers), time in clinical role, or time at NICU site (Table 4, and Appendix Tables A.1, and A.2, respectively).

Table 2 Survey responses of the longitudinal cohort, pre- versus post-OASCN intervention.Table 3 Survey responses of the longitudinal cohort, by collaborative role (site leaders versus other prescriber participants).Table 4 Survey responses of longitudinal cohort, by participation in OASCN learning sessions (participated versus did not participate).

In qualitative interviews, site leaders were asked to assess the general appropriateness of antibiotic use in their NICUs before the OASCN Collaborative. Overall, 16/30 (53%) reported having overall appropriate antibiotic prescribing practices, 9 (30%) having overall inappropriate practice overall, and 5 (17%) discussing areas that were appropriate and other areas that were inappropriate. We also queried appropriateness within specific areas of AS (i.e., drug choice, starting or stopping antibiotics, and drug choice and duration). No site leaders reported issues with appropriateness of drug or dose. However, among the 14 site leaders who reported having some inappropriate prescribing practices, 9 (30% overall, 64% of those reporting inappropriate prescribing) noted inappropriate practices around starting antibiotics, and 10 (33% overall, 71% of those reporting inappropriate prescribing) reported inappropriate practices around stopping antibiotics. Major drivers associated with starting antibiotics included fear of a bad outcome, empiric use prior to culture results becoming available, and in some, infants already being on antibiotics before admission to the NICU, and provider reluctance to change long-standing practices:

“I don’t know what it’s going to take to do that, but there are certain concerns that infection in babies is a rare event, and so they’re very worried about missing that one baby [who] should have been on antibiotics and wasn’t.” – Urban setting NICU in Southern California

“So now that we’re taking care of the smaller, younger babies, like I said, I already can tell there’s some kneejerk reactions to putting her on antibiotics, when maybe she didn’t need that, at least for like… 48 hours and see how she does type thing, which is like a very common NICU practice.” – Urban setting NICU in Southern California

Perceptions of AS importance

In the longitudinal cohort, prescribers reported high levels of importance of AS to self, lower levels of importance from other clinicians, higher levels from their NICU leadership, and lower levels from hospital leaders, though all differences from pre- to post-OASCN surveys were not statistically significant except for those of other (non-neonatologist) clinicians (Table 2). Of note, many prescribers (48/166, 29%) reported not knowing how their hospital leadership perceived the importance of AS. There were also few significant differences by provider type, though neonatologists generally viewed AS as more important and active in their units compared to others (Appendix Table A.3). As noted in Table A.1, post-OASCN, those who had spent ≥10 years in their role reported significantly higher levels of AS importance among themselves, other clinicians, NICU leadership, and hospital leadership, compared to those with less experience.

Site leaders reported being highly motivated to participate in the collaborative and improve AS. When asked about other resources for AS, most site leaders did not think there was a strong connection to hospital leadership or hospital-wide AS efforts.

“I don’t think we’re the only one [NICU] where a NICU in a very large, adult-focused hospital, we’re kind of tucked away in a corner a lot of the times, and as long as our metrics are good then they just support us with administrative type of resources, for example, maintaining a team of nurses to look at data.” – Urban setting NICU in Northern California

“[In the NICU,] we tend to be kind of isolated. We’re like our own functioning, tiny, mini hospital.” – Urban setting NICU in Northern California

NICUs may be perceived as a different entity and there may be a reluctance to engage fully with NICUs on wider hospital efforts. Site leaders noted that even though they function separately from the hospital, hospital leadership is still supportive of participation in AS efforts.

“…Administration and everyone else… they don’t know NICU, they don’t know NICU care, and it kind of worries them and scares them so they usually stay out and they don’t— there’s really not a lot of support for it.” – Urban setting NICU in Southern California

One pharmacist involved in AS noted that the pharmacy needs of the NICU are also distinct from the wider hospital. Given the scope of antibiotic needs throughout the hospital, individuals involved in stewardship focus on the adult side and leave the NICU to work on its own.

“…because [antibiotic stewardship responsibility is on] one person for the whole hospital, I focus mainly on adults because that’s where my training is. And NICU is always just kind of run independently” – Urban setting NICU in Southern California

Perceptions of AS activity

Prescribers reported “very” or “extremely” high levels of stewardship activity in the pre- and post-OASCN periods, and with a statistically significant increase over time (67% v. 87%, 3.84 v 4.32, p < 0.001), similar to site leaders alone (Table 3). This increase was more pronounced among those who participated in at least one Learning Session (Table 4) or had ≥10 years in their role (Appendix Table A.1). The overall pre-post trends by provider type were similar to the overall trends, but neonatologists reported significantly larger activity levels in the post-collaborative survey than those with other roles (92% v 79%, 4.45 v. 4.07, p = 0.003; Appendix, Table A.3).

The pre- to post-OASCN increase in AS activity is larger and significant for small sized (68% v 89%, 3.89 v. 4.34, p = 0.048; Appendix, Table A.4) and medium-sized (69% v 93%, 3.91 v. 4.44, p < 0.001) NICUs, but not for the larger NICUs. There was also a significant difference in perceived hospital-wide activity reported by those with ≥10 years in role (3.69 v. 4.05, p < 0.001; Appendix Table A.1), although many (59/166, 36%) reported not knowing the level of activity related to AS in the hospital. Other prescribers, but not site leaders, also reported an increased perception of hospital-wide AS activity during OASCN (3.94 v. 3.70, p = 0.03; Table 3).

In qualitative interviews, over the course of the collaborative, all site leaders reported improvements to activity to improve AS. Site leaders revealed several activities related to AS that were implemented in the NICU during the collaborative, including updating antibiotic use guidelines (18/30, 60%); implementing more standardized rule out sepsis protocols (9/30, 30%), hard antibiotic stops at 48 and 36-h (8/30, 27%), antibiotic timeouts (2/30, 7%); and adding sepsis calculators into their electronic medical record (2/30, 7%). Sites implemented between one and six changes to improve AS, with sites implementing a median of 4 changes. Site leaders reported that clinicians did make progress towards more consistently appropriate prescribing practices over the course of the collaborative as a consequence of these implemented activities.

Perceptions of AS capacity

Prescribers were asked two items in the pre-OASCN survey about the capacity to reduce antibiotic use (openness to and difficulty in reducing antibiotics), and one item in the post-collaborative survey (openness to reducing antibiotics). Prescribers reported high levels of openness in the pre- and post-OASCN surveys and a statistically significant improvement over time (59% pre-OASCN as “very” or extremely” open versus 70% post-OASCN; Table 2). In the pre-OASCN survey, almost all prescribers reported that it would be a little to somewhat difficult to reduce antibiotic use safely (4.3% reported very or extremely difficult to reducing antibiotic use safely).

In the pre-OASCN survey, neonatologists reported significantly higher levels of openness to changing practice than those in other roles (3.85 v. 3.41, p = 0.007; Appendix Table A.3), though this gap shrank in the post-survey despite remaining significantly different. It was also moderated by time in role and site, with those with ≥10 years in their role reporting increased levels of openness in the post-OASCN survey, relative to more junior peers who did not report a significant increase. This was driven by the larger NICUs (Table A.4). Respondents that participated in at least one Learning Session had greater gains in their perception of openness to change during OASCN than those that did not participate (Table 4).

Key barriers to implementing AS practices reported by site leaders included difficulty engaging providers and getting their buy-in. Among the most cited concerns were fear of a bad clinical outcome from withholding antibiotics, stopping antibiotics too early (particularly for preterm babies), the interest of maintaining existing long-standing practice (that often use more antibiotics than is recommended), and the desire to treat culture-negative sepsis and early-onset sepsis.

“The biggest barrier is what we’ve done for 20 or 30 years. We have some older physicians in our practice who have practiced a certain way and given antibiotics at certain times for a really long time.” – Urban setting NICU in Northern California

A consequence of participating in the OASCN collaborative, however, was once there was some buy-in to reduce their antibiotic use, providers did not observe a rise in adverse outcomes and were therefore more open to continued decreases.

“But once we got the buy-in and they saw that there were no adverse outcomes in these babies that weren’t started on antibiotics, I think that that helped a lot. It helped be more smooth for the rest of the year.” – Urban setting NICU in Southern California

We performed analyses on certain subgroups. In 2016–17, 10 (33%) of the OASCN sites participated in a less intensive AS collaborative [24]. Analyses of this group, in comparison to the entire OASCN cohort, did not reveal substantial differences in the perceptions of prescribing appropriateness, importance of AS, AS activity, or capacity. Prior collaborative participants did, however, report a higher perceived level of appropriate prescribing practices before the OASCN collaborative which was no longer significant post-OASCN (data not shown). Lastly, considering the entire cohort of 297 participants (compared to the longitudinal cohort), there were no statistically significant pre-to post-OASCN increases in responses for any question (Appendix Table A.5).

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