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Relationship of Necrotizing Enterocolitis Rates to Adoption of Prevention Practices in US Neonatal Intensive Care Units

Gephart, Sheila M. PhD, RN; Quinn, Megan C. BSN, RN

Section Editor(s): Dowling, Donna PhD, RN; ; Thibeau, Shelley PhD, RNC-NIC;

doi: 10.1097/ANC.0000000000000592
Original Research
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Background: Applying quality improvement methods has reduced necrotizing enterocolitis (NEC) in some neonatal intensive care units (NICUs) by 40% to 90%.

Purpose: This study was conducted to (1) examine relationships between adoption of prevention practices using the NEC-Zero adherence score and NEC rates, and (2) describe implementation strategies NICUs use to prevent NEC.

Methods: A descriptive cross-sectional correlational study was completed among US quality improvement–focused NICUs. Relationships of the NEC-Zero adherence score to NEC rates were examined. Subgroup analyses explored relationships of a human milk adherence subscore and differences between high NEC rate (≥8%) and low NEC rate (≤2%) NICUs.

Results: NICUs (N = 76) ranged in size from 18 to 114 beds. The mean adherence score was 7.3 (standard deviation = 1.7; range, 3-10). The 10-point adherence score was not related to the NEC rate. The human milk subscore related to lower NEC rates (Rho = −0.26, P = .049), as was colostrum for oral care (Rho = −0.27, P = .032). The units that used a feeding protocol showed higher NEC rates (Rho = 0.27, P = .03), although very few addressed the use of effective implementation strategies to track adherence or to ensure consistency among clinicians. The units that used colostrum for oral care were more likely to adopt strategies to limit inappropriate antibiotic exposure (Rho = 0.34, P = .003).

Implications for Practice: Broader use of evidence-based implementation strategies could bolster delivery of NEC prevention practices. Maternal lactation support is paramount.

Implications for Research: Future studies are needed to identify how individual clinicians deliver prevention practices, to find the extent to which this relates to overall delivery of prevention, and to study effects of bundles on NEC outcomes.

Community and Health Systems Science Division, College of Nursing, The University of Arizona, Tucson (Dr Gephart and Ms Quinn); and Cardon Children's Medical Center, Banner Health Network Neonatal Intensive Care Unit, Mesa, Arizona (Ms Quinn).

Correspondence: Sheila M. Gephart, PhD, RN, Community and Health Systems Science Division, College of Nursing, The University of Arizona, PO Box 210203, Tucson, AZ 85721 (gepharts@email.arizona.edu).

Dr Gephart acknowledges that this project was funded by the Robert Wood Johnson Foundation Nurse Faculty Scholars Program (72114). She also received training support from the Agency for Healthcare Research and Quality (K08HS022908) and the Pacific Southwest Region of the National Network of Libraries of Medicine. The authors thank the NEC-Zero study team, including Ms Christina Wyles, Mr Anthony Tolentino, Mr Scott Robert Johnson, and Ms Caroline Porter, for their role in the larger NEC-Zero project and for reviewing the manuscript.

The content is solely the responsibility of the authors and does not necessarily represent the official views of the Robert Wood Johnson Foundation, Agency for Healthcare Research and Quality, or the National Network of Libraries of Medicine.

Dr Gephart is a member of the Editorial Board of Advances in Neonatal Care and was not involved in the review or decision for the manuscript. The other authors declare no conflicts of interest.

Necrotizing enterocolitis (NEC) is a gastrointestinal disease that affects predominantly premature infants and is a major cause of emergent surgery in the neonatal intensive care unit (NICU).1,2 A diagnosis of NEC necessitates many invasive interventions, requires longer stays in the NICU, and heightens the risk for potentially chronic serious complications and death.3–5 While uncommon and occurring in 2% to 12% of very low birth-weight infants, NEC is serious, with up to 30% needing surgery to treat it.6,7 Of those requiring surgical treatment, mortality is as high as 50%.8 For NEC surgery survivors, many will need to stay in the NICU for months and may become dependent on parenteral nutrition in the long term. Lifelong impacts can include delayed neurodevelopment, high infection risk, or liver, intestinal, or kidney failure.

Risk factors for NEC are often attributed to being born early, but multiple factors contribute to the likelihood that an infant will develop NEC.9 In a comprehensive review of NEC risk, Samuels and team3 identified 43 nonmodifiable NEC risk items across neonatal studies. At highest risk were infants born small for gestation and those who required assisted ventilation, experienced hypotension or sepsis, or were born after premature rupture of membranes or outside of the care hospital (ie, “outborn”).3 Black or Hispanic infants have higher rates of NEC than non-Hispanic white infants.10,11 Modifying NEC risk can be driven by promoting mother's own milk (MOM), especially in the first 28 days of life,12–14 adopting standardized feeding guidelines,15,16 and minimizing exposures to unnecessary antibiotics and histamine-2 antagonist blockers. Many add probiotic treatment to the list of protective treatments to avoid NEC, although there remains controversy that stalls implementation in US clinical practice.

In a study by our team in 2014, we tested and determined the relative contribution of different factors to predict NEC (ie, in a score called GutCheckNEC). One of the major risk factors was the variation in practices and NEC rates between NICUs. Revealing strong variations in NEC rates across 284 NICUs, ultimately this pointed to how much the practices within an NICU heavily contribute to the likelihood that an infant would develop the disease in that NICU.11 Other cohorts confirm broad variation in NEC occurrence, although the exact mechanisms for differences are unclear.17–19

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IMPORTANT COMPONENTS OF NEC PREVENTION QUALITY IMPROVEMENT

Feeding high proportions of MOM, especially in the first 14 days of life, is protective against NEC, although it is not a panacea.12 Adoption and consistent use of standardized feeding protocols (SFPs) can reduce risk,15,16 and the prolonged antibiotic exposure or administration of histamine-2 antagonists can increase risk.16 Indeed, prioritizing the delivery of prevention evidence through quality improvement (QI) methods has decreased NEC rates in some units. Tracking improvement across NICUs from 2005 to 2014, the Vermont-Oxford Network showed that 75% of the lowest-performing NICUs engaged in improvement work could reduce NEC but the pace of improvement took 5 to 8 years.20 Quality improvement for NEC prevention has been shown to decrease NEC rates by 41%–92% (Table 1).13,18,21–24

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What This Study Adds

  • Among quality-focused NICUs, the 10-point NEC-Zero adherence score did not relate to reported NEC rates but the human milk subscore did.
  • Across participating US NICUs, general adoption of NEC prevention practices is widespread but the use of evidence-based implementation strategies is less common.
  • Variance in timing for holding feeding during transfusion was widespread. There was no consistency in the interval for feeding cessation, and there were unclear criteria for restarting.
TABLE 1

TABLE 1

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NEC-ZERO DESCRIPTION

In 2015, a multidisciplinary group of clinical and research experts addressed the current scientific and practice-based evidence about NEC prevention and strategies to promote timely recognition. Different from a systematic review, their “scoping review” focused on using the existing literature to answer key clinical questions about evidence that was ready for implementation and potential strategies used to do so.16 The initiative is called NEC-Zero to reflect a common goal to move NEC to “zero incidence.” Informed by a theoretical framework from implementation science, Titler's25–27Translating Research into Practice framework, NEC-Zero aimed to influence adoption of prevention practices by leveraging communication strategies to users who work within a social system and through a simple, noncontroversial, bundled intervention.16 NEC-Zero applies ready-to-implement, evidence-supported, and minimally controversial practices that do not require extra equipment or additional prescriptions. Four essential components comprise the bundle and are informed by the state of the science: (1) human milk feeding that prioritizes mother's milk beginning with colostrum for oral care; (2) use of a unit-approved feeding protocol (sufficiently described and formalized so that one can “take a picture” of it); (3) minimizing exposure to prolonged empiric antibiotics (ie, <4 days when initial blood cultures are negative directly after birth) and avoidance of histamine-2 antagonist blockers; and (4) specifying an approach to risk awareness and timely recognition (eg, using an NEC risk tool such as GutCheckNEC combined with a focused communication tool for when symptoms arise). The NEC-Zero team elected to exclude 2 potentially beneficial practices: use of probiotics (ie, requires a prescription, is not regulated by the Food and Drug Administration, and to some may be controversial) and the choice of donor human milk (DHM)–derived fortifiers (due to cost). While all NEC-Zero practices are evidence based, it was not entirely clear whether certain practices confer greater benefit than others.

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NEC-ZERO ADHERENCE SCORE

In 2016, a consensus-building approach using an electronic Delphi process was conducted to identify, among experts not affiliated with NEC-Zero, how well the recommendations fit current knowledge and beliefs and to “weight” in a 10-point score.28 Still focused on implementation, the NEC-Zero team aimed to use the 10-point score as one strategy in an audit and feedback intervention. Via audit and feedback, the score could be a quick way to indicate how adherent to the prevention bundle the care had been. The Delphi process ended after 2 rounds once consensus was achieved to weight the score. Components in the final NEC-Zero adherence score included prioritized human milk feeding (5 points—3 points for dose of human milk, 1 point for oral colostrum care, and 1 point for DHM availability), SFP (3 points), medication stewardship (1 point), and a unit-specified approach to foster timely recognition (1 point).28 During the Delphi process, holding feeding during packed red blood cell (PRBC) transfusion was determined to be controversial, so it was dropped from the score. We asked participants about it to identify the prevalence of the practice in this study. It was not known whether the 10-point NEC-Zero score relates to actual NEC rates or nuances for implementation could be made consistent. In a review of evidence in 2018 in PubMed and the Cochrane Database of Systematic Reviews using “necrotizing enterocolitis,” “implementation strategies,” and “prevention,” only the NEC-Zero scoping review was identified. No studies were found to describe the broad state of adoption of NEC prevention practices in US NICUs.

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PURPOSE

This study was conducted to (1) examine relationships between adoption of prevention practices using the NEC-Zero adherence score and NEC rates, and (2) describe implementation strategies NICUs use to prevent NEC. The following research questions were explored:

  1. To what extent does the adoption of NEC prevention practices (via the NEC-Zero adherence score) relate to NEC rates?
  2. How are NICUs implementing NEC prevention?
  3. To what extent are there differences between the adoption of NEC prevention practices in NICUs with low NEC rates (≤2%) and those with high NEC rates (≥8%)?

We hypothesized that units with higher adoption of NEC prevention practices would report lower rates of NEC.

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METHODS

Design

A descriptive cross-sectional correlational study was completed using an investigator-developed questionnaire to explore adoption of NEC prevention practices and their relationship to NEC rates in US NICUs. The questionnaire was composed of closed-ended and open-ended questions. Relationships of the NEC-Zero adherence score to NEC rates were explored.

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Survey Item Development

Items for the survey were developed with insight from the previous 2 steps of the process (ie, recommendations from the NEC-Zero group and the Delphi study). Questions were phrased as yes/no or open-response options to query whether their NICU had implemented the following: (1) prioritized human milk feeding; (2) colostrum for oral care; (3) SFPs; (4) a unit-based approach to timely recognition of NEC; (5) restriction of feeding during PRBC transfusion; and (6) restricting the initial course of antibiotics to less than 5 days if blood cultures were negative. Self-reported NEC rates were collected such that the NICU representative used their Vermont-Oxford Network data (with definition for NEC) to report their 2014 rate and their 5-year rate (2009-2014). Open-ended questions explored approaches used in their NICU to implement the following: (1) strategies for the promotion of an exclusive human milk diet; (2) monitoring compliance to SFPs; (3) strategies for communication to foster NEC timely recognition; (4) teamwork across the disciplines; (5) practices to alter enteral feeding around PRBC transfusion; and (6) strategies used to reduce prolonged empiric antibiotic therapy.

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Procedures

All study procedures occurred online using convenience sampling with direct e-mail and snowball recruitment. One unit participant (the nursing leader, quality director, or medical director) was recruited to complete the survey. Only participants from the United States were eligible. Recruitment targeted NICU nursing leadership quality listservs, attendees at QI meetings, Children's Hospital Research Network listservs, and directly NICUs identified from e-mail lists. Once invited, participants viewed a disclosure document about the study and proceeded to the survey delivered via the Qualtrics platform (Provo, Utah). The questionnaire was open for 10 days, and reminders were sent 48 hours before it closed. The institutional review board at the University of Arizona approved this study as exempt and provided oversight for the protection of human subjects.

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Assignment of Adherence Score

The adherence score for each NICU was calculated by giving a numbered score for each category of NEC prevention practice asked about in the survey (see scoring criteria in Table 2). The scores for having a unit-derived SFP and for encouraging intake of MOM were weighted more heavily based on results of the previous Delphi study. NICUs received points for indicating adoption of each adherence score item. For MOM availability, NICUs received 3 points for indicating that more than 75% infants' enteral intake was from MOM administration, 2 points for 50% to 74%, 1 point for 25% to 49%, and 0 points for less than 25%. For DHM availability and oral colostrum administration, they received 1 point for the adoption of each practice and 0 points for not adopting the practice. If an NICU indicated that it had adopted a feeding protocol, it was given 3 points and 0 points if it did not use one. For the practice of antibiotic stewardship, NICUs were given 1 point if they described some type of measure to monitor or limit the length of the initial empiric antibiotic course. Examples that enabled 1 point to be issued included if they specified that they used pharmacist oversight, automatic stop dates on medication orders, auditing, or for active participation in an antibiotic stewardship initiative. If no approach was specified or if they said they relied solely on clinical memory, 0 points were given. Finally, NICUs were given 1 point for standardized timely recognition practices if they described a tangible process (ie, you could take a picture of it or it involved a structured group process) to enhance timely recognition of NEC and 0 points if they did not. Examples of tangible approaches to timely recognition addressed advanced monitoring systems (eg, heart rate vulnerability monitors), specialized tools for communication, or applying intentional risk awareness via use of risk tools (eg, GutCheckNEC, NeoNEEDS, or eNEC). Total adherence scores represented the sum of these items (10 points maximum). The human milk subscore (5 points maximum) represented the sum of the values for MOM, DHM, and oral colostrum administration. Because of findings from the earlier Delphi study, no points were given for enteral feeding around the time of PRBC transfusion because of inconsistent evidence for the practice, although we did ask to determine the prevalence of altering feeding around transfusion.

TABLE 2

TABLE 2

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Data Analysis

Quantitative data (ie, adherence score and the NICU NEC rate) were described using descriptive statistics. Relationships between the adherence score and the NICU NEC rate were analyzed using the Spearman correlation coefficients. Nonparametric analyses using the Mann-Whitney U test were used to identify whether there were differences in adherence score between units with low (≤2%) and high (≥8%) NEC rates. Content analysis was applied to the open-ended responses after counts of practices were collected about the different implementation strategies that NICUs used to prevent NEC in their own words. Coding categories were identified by question, using both conventional and directed methods focused on identifying actionable implementation strategies.29–31

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RESULTS

NICU Characteristics

Unique responses from 76 NICUs located in the United States were obtained (see sample characteristics in Table 3). NICUs ranged in size from 18 to 114 beds, but most were moderate (47%) to high (29%) volume and cared for the sickest neonates (46% American Academy of Pediatrics designated level III and 51% level IV). All were active in some QI collaborative. Participants reported annual NEC rates from 0% to 12.6% (mean = 4.6, standard deviation [SD] = 3). Four NICUs reported rates of 0%.

TABLE 3

TABLE 3

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Relationship of Adherence Score to NEC Rates

Adoption of components of prevention evidence ranged from 11% of NICUs that identified a strategy for timely recognition to 87% of NICUs that had adopted a standardized feeding guideline (Figure 1). Adherence scores ranged from 3 to 10. The mean adherence score was 7.3 (SD = 1.7). The 10-point adherence score was not related to the NEC rate across the sample. When a human milk subscore was computed, it was related to lower NEC rates (Rho = −0.26, P = .049). Using colostrum for oral care was related to lower NEC rates (Rho = −0.27, P = .032). The units that used a feeding protocol showed higher NEC rates (Rho = 0.27, P = .03). The units that used colostrum for oral care were also more likely to adopt strategies to limit inappropriate antibiotic exposure (Rho = 0.34, P = .003).

FIGURE 1

FIGURE 1

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Human Milk Feeding Practices

The most consistently adopted prevention practice was to promote human milk, specifically MOM for feeding, with most units reporting use of multiple strategies in place. The most frequently reported strategies promoting human milk were the use of DHM (n = 66; 86.8%) and the use of mother's colostrum for oral care (n = 57; 75%). When asked about strategies to promote human milk feeding, however, only 55% of clinicians who reported using DHM and 8.8% of clinicians who reported using oral colostrum identified these 2 practices as strategies to promote the use of human milk in their institutions. Two other common practices involved educating parents (n = 33; 43%) about the importance of human milk, especially MOM, and having lactation specialists to support mothers in providing milk for their infants (n = 28; 36.8%). Some clinicians also reported promoting early initiation of milk expression (n = 12; 15.7%) and skin-to-skin holding (n = 11; 14.5%) as practices to increase a mother's milk production. Institution-based initiatives such as Baby Friendly Hospital designation were mentioned by some participants as facilitators to promoting breastfeeding and the use of human milk. Implementing peer lactation support was rarely used.

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Standardized Feeding Protocol Practices

Most respondents reported using SFPs (n = 67; 88%). The details of these SFPs regarding advancement, weight variations, time to fortification, and time to full feeding volume were not explored in this study. Importantly, participants revealed that how well they monitored compliance to the protocol was highly variable and largely infrequent. The most common compliance practice was to audit use (n = 31; 45.5%), but only 9 of those 31 (13.2% of total responding NICUs) reported auditing at regular intervals. A fraction (12 units, 18% of all NICUs) incorporated accountability to ancillary staff members such as nutritionists, dieticians, and developmental specialists into their SFP implementation plans. Other strategies to ensure consistent SFP use included using a standard order set for the protocol and using visual cues such as reminder cards where clinicians placed orders (Table 4). Ten NICUs identified that SFP compliance was supported by “habit,” “peer pressure,” or group “buy-in.” Overall, there was very high “implementation” of SFPs but given the complexity of SFPs, the need for consistent delivery, and the opportunity for fragmented care, we are concerned that actual use of SFPs may be much lower than participants reported.

TABLE 4

TABLE 4

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Feeding Practices During PRBC Transfusion

There was wide variance in practice to withhold or administer enteral feeding during and around the time of PRBC transfusions (Figure 2). Specifically, 48 (63%) clinicians reported that they held feedings before, during, and/or after transfusion and 17 (22%) clinicians reported that they did not. Of those who continued feedings, some made other adjustment such as reverting to trophic feedings (10 mL/kg/d; n = 4) or reducing feeding volume in half. Responses relating to length of time feedings were held varied among clinicians who reported holding feedings. Intervals ranged from 12 hours before transfusion to 24 hours after transfusion and most commonly included holding feedings before, during, and after transfusion. Only 2 reported holding feedings only during the transfusion. Twenty-eight respondents reported a single time (ie, 4 hours, 4-6 hours) rather than indicating the time in relation to the transfusion (ie, 4 hours before, during, and after transfusion). Some of these respondents also indicated variation in their or their colleagues' practice (ie, 6-12 hours) but did not include rationale for this variance. The most common interval reported was 3 hours before, during, and 3 hours after transfusion (n = 8; 10.5%), although few used such an interval.

FIGURE 2

FIGURE 2

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Timely Recognition Practices

The question regarding communication during timely recognition of NEC revealed interesting and varied results. Very few actually addressed communication, and the majority did not have a standardized process to quantify NEC risk, recognize and communicate NEC warning signs, and ensure prompt treatment when NEC was suspected. For the purpose of quantitative analysis, if a participant described a timely recognition strategy that you could take a picture of, it was counted as a systematic unit-centered strategy. If it relied on individual memory or use alone (and was not codified as a printed policy), it was coded as “no timely recognition practice.” Most responses addressed assessment and diagnostic strategies, such as abdominal assessments, abdominal radiographs, and laboratory testing (n = 23). Some participants noted the use of special tools and monitors to help recognize potentially critical illness in early stages, such as the HeRO monitor, pediatric early warning score, and feeding tolerance algorithms. No clinicians mentioned using specific tools to improve communication (eg, SBAR), risk scores (eg, GutCheckNEC, NeoNEEDS, or eNEC), or strategies to engage parents in early warning or risk awareness.

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Antibiotic Stewardship Practices

Respondents gave the fewest responses (n = 48; 63%) for strategies related to antibiotic stewardship (Table 5). Of these, 27% reported that they did not have a process to practice antibiotic stewardship. Of those who did have a process, the most common response was that a 48-hour rule-out period at birth was simply a “routine practice” that relied on the provider to remember to discontinue the antibiotics. Some used the electronic health record to automatically cancel the antibiotic after a rule-out period (17%) or relied on laboratory data to cancel antibiotics (16.7%). Rarely, respondents participated in a dedicated antibiotic stewardship program through their institution or health system (12.5%). Avoiding routine antibiotic administration on admission and working with pharmacists to monitor appropriate use were also described infrequently.

TABLE 5

TABLE 5

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Comparison of High Rate NICUs and Low Rate NICUs

We next evaluated practices in NICUs with very low rates of NEC (ie, <2%) to see whether they differed from NICUs with very high rates of NEC (ie, >8%; Table 6). On average, low NEC rate NICUs were more likely to be a lower acuity or level and have lower bed capacity than high NEC rate NICUs. NICUs from the Western and Midwestern United States were more represented in the low NEC rate group, and NICUs from the Southern and Northeastern United States were more represented in the high NEC rate group. The mean adherence score was similar between both groups, but the mean adherence score for combined human milk elements of the score was a full point higher in the low NEC rate group. Neither the total adherence score nor the human milk subscore significantly differed between high rate and low rate NICUs.

TABLE 6

TABLE 6

The data demonstrated 5 areas in which NICUs with low rates of NEC differed from NICUs with high rates of NEC (Table 7). NICUs with low rates of NEC adopted all practices promoting a human milk diet more often (43.7%), especially the use of colostrum for oral care (75%). These NICUs also described more practices of antibiotic stewardship (68.7%) than the NICUs with high rates of NEC (55.6%). Alternatively, NICUs with high rates of NEC demonstrated better adoption of standard feeding protocols (100%), though whether providers were monitored regarding adherence to these protocols was unclear. High rate NICUs also demonstrated more adoption of standard practices for timely recognition of NEC, but the rates of adherence for timely recognition were low overall.

TABLE 7

TABLE 7

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DISCUSSION

This study surveyed a diverse group of NICU clinicians representing many different geographic regions in the United States, types of institutions, and levels of awareness about NEC prevention. Clinicians of varying roles (RN quality managers, nursing managers, medical directors, and physicians) responded to the survey, contributing to the breadth of perspectives elicited. Although the comprehensive 10-point NEC-Zero adherence score did not relate to lower NEC rates, the human milk adherence subscore comprised of total use of human milk, donor milk use, and use of colostrum for oral care did. The only single component of the adherence score that was individually correlated with a lower NEC rate was the use of colostrum for oral care. Across the units, adoption of feeding protocols was common, although monitoring adherence and ensuring they used consistent strategies were rare.

This study highlights the wide variety of practices used in NICUs to prevent NEC. Strategies to promote a human milk diet were the most prevalent, with many units having multiple strategies to support mothers in lactation to provide human milk to infants. The practice of administering colostrum during oral care may help encourage mothers to provide milk in early postpartum days, but it may be beneficial independent of this support. This practice has been increasingly adopted since 2011 based on theoretical evidence that colostrum applied to the buccal mucosa and absorbed by the lymph tissue boosts immune system growth and decreases inflammatory response.32,33 Respondents did not describe their specific approach to administer colostrum for oral care (eg, using nonabsorbent swabs vs small-volume syringes; administration by parents or by staff). QI practices to bolster use of human milk have shown decreases in NEC, including the human milk bundle used in California18 and the comprehensive program used in Canada.23 Both programs prioritized lactation support, early milk expression, and monitoring of human milk volumes.

Variation in NEC prevention practices was demonstrated despite each NICU's active involvement in QI. Arguably, the fact that all respondents were active in some QI collaborative limits the generalizability of our findings and may overestimate the prevalence of NEC prevention in the United States, although respondents were not necessarily focusing their QI efforts on NEC prevention or reduction. Horbar and colleagues20 estimated the general pace of improvement for NEC as around 8 years that it would take for the lowest performing to achieve rates typical of the best performing, highlighting the wide variation from NICU to NICU. Respondents indicated that actual practice may be sporadic and is often provider dependent. Our findings reveal that implementation strategies for antibiotic stewardship and timely recognition were plagued by clinical uncertainty. Low awareness was made clear by some respondents who questioned the appropriateness of antibiotic stewardship or timely recognition in an NEC-related survey.

The comparison of low and high rate NICUs did not demonstrate clear differences in the adoption of most NEC prevention practices, although their application of implementation strategies could be arguably different. The percentage of low NEC rate NICUs with the highest adoption of human milk practices, however, was double the percentage of those from high rate NICUs and approached statistical significance. Practices more common in units with very low rates of NEC (ie, ≤2%) compared with very high rates (ie, ≥8%) included high human milk use, use of colostrum for oral care, and a practice in place to avoid prolonged antibiotics. Support to help parents provide skin-to-skin care, receive help from NICU-focused lactation specialists, or for providing information about the value of human milk varied.

Likely the most surprising and contradictory finding of this study was the association we showed between high use of feeding protocols and higher NEC rates. This study was limited in that we did not ask details of their protocol or require them to have certain features to ensure they used it consistently. We did ask about implementation strategies that left many immediate opportunities for improvement. The association of feeding protocols with higher NEC rates contradicts meta-analyses that show feeding protocols decrease NEC risk by approximately 67% in very low birth-weight infants (9 studies, N = 4755 infants),16 and by nearly 80% among infants born with weight less than 2500 g (15 studies, N = 18,160 infants).15 With that in mind, the recommendation to use a feeding protocol is unchanged despite the unexpected association in this self-report, survey-based study. Ultimately, the most important thing to remember is that when using a feeding protocol, implementation strategies to make its adoption consistently should be considered (eg, integration into standard order sets, use of audit and feedback, making other team members part of the implementation, and adherence tracking). It is also essential to adopt an algorithm and a definition for feeding intolerance to determine when infants in the unit using the protocol should have their feeding interrupted. Readers may find the experience of Patel and colleagues13 with NEC QI and their feeding protocol modifications made along the way informative.

This study revealed that the practice of holding feedings during and around PRBC transfusions was widely adopted, but there was a wide variation in the length of time feedings were held. The evidence to support this practice is somewhat contradictory and controversial.34–36 Some cases of NEC cluster in the period within 24 to 48 hours after a PRBC transfusion, especially in the anemic infant.37 Yet, the overall quality of the evidence linking transfusion to NEC is “very low” when systematically assessed using the GRADE criteria.38 Our findings showed that it was common to hold, alter, or significantly reduce feedings before, during, and after transfusions. Respondents cited this uncertainty as their reasons for either not holding feedings or the variation in their practice for feeding during transfusions.

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Limitations

While this study contributes better description of the state of NEC prevention practice adoption in US NICUs, it has important limitations. All data were self-reported by participants and may over- or underestimate actual care. The NEC rate reporting was based on the standard definition for NEC used by the Vermont-Oxford Network, which some argue may overestimate actual NEC.39 We did not identify whether radiological or medical reviews were conducted to affirm the diagnosis of NEC within the units reporting. While open-ended response options followed direct and specific questions, participants may not have answered the questions in a way that would thoroughly describe their practices. One indication of this was the noted mismatch between responses to these questions and responses to direct questions (eg, Do you use donor human milk?). While these response options allowed providers to elucidate specific practices or variations on practices within their unit, these responses were occasionally contradictory with other responses or were completely unrelated to the question. However, we managed this limitation by using the closed-ended responses only for calculating the adherence score. Finally, because we included quality-focused NICUs, our results have limited generalizability to others. Our respondents may have been more aware of current evidence-based practices, regularly share clinical practices within their community of practice, or be more readily engaged in measuring their processes and NEC outcomes. We revealed high adoption of feeding protocols but did not systematically ask about its details that enabled better characterization of them. This may have influenced our finding that feeding protocols were related to higher NEC, which contrasts sharply with meta-analyses that consistently show NEC reductions.15,16 There were also very few responses from level II NICUs. While these units may not care for infants at highest risk for NEC, they do care for late-preterm infants who may develop NEC.

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Implications for Practice

An encouraging finding from this study is that most NICUs prioritized human milk, especially MOM. Participants indicated most often that promoting MOM was their first-line intervention to prevent NEC. Empowering mothers to provide milk requires consistent messaging from clinicians about its benefits and providing lactation support. While respondents indicated a commitment to promote human milk feeding, studies have shown wide disparities in how consistently lactation support is offered.40,41 Supporting availability of donor milk if MOM is not available will require changes to organizational policies and making stronger connections with milk banks. Reimbursement for donor milk varies widely, although some states require its insurance reimbursement (Texas, California, Missouri, Kansas, and New York).42 At least one study showed that when donor milk was available, the use of MOM improved.43 The high adoption of feeding protocols but low adherence monitoring and rare integration into electronic order sets is an opportunity that all NICUs can act on today. Strategies to engage families could strengthen the efforts of the clinical team (see https://www.neczero.nursing.arizona.edu/ for family engagement tools).

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Implications for Research

Future studies are needed to explore the role of an adherence score to change clinicians' behavior and raise awareness about NEC. Testing the multifaceted NEC-Zero bundle on clinical outcomes is needed. Transfusion-associated NEC continues to be a controversial topic for many clinicians, and our study demonstrated that this controversy plays out in a wide variation in practices of feeding during blood transfusions. Recent studies suggest that it is perhaps severe anemia, followed by a blood transfusion, not the transfusion itself that creates a high risk for NEC after a transfusion.44 This controversy and confusion can only be alleviated with more high-quality research examining transfusion-associated NEC and the potential detriment of holding feedings for long periods.

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CONCLUSION

This study showed that adopting the use of colostrum for oral care was associated with lower NEC rates and that units with the lowest rates had practices in place to adopt feeding protocols, minimize antibiotic exposures, promote human milk feeding, and foster team collaboration for timely recognition. While the NEC-Zero adherence score was not related to NEC rate, the results demonstrate a wide variation in NEC prevention practices across US NICUs. Adoption of colostrum for oral care was the only individual prevention practice associated with a lower rate of NEC, though a combination score including the 3 prevention practices relating to use of human milk was also associated with lower NEC rates. SFPs and antibiotic stewardship were common, but monitoring compliance to those protocols or practices was uncommon. Standardized practices for early recognition were not widely reported, and withholding feedings related to blood transfusion has become controversial due to current evidence. More consistent use of evidence-based implementation strategies including clinical decision support systems, standard order sets, and application of audit and feedback could improve delivery of NEC prevention practices in US NICUs. Maternal lactation support is paramount to accomplish this goal.

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References

1. Zhang Y, Ortega G, Camp M, Osen H, Chang DC, Abdullah F. Necrotizing enterocolitis requiring surgery: outcomes by intestinal location of disease in 4371 infants. J Pediatr Surg. 2011;46(8):1475–1481.
2. Hackam D, Caplan M. Necrotizing enterocolitis: pathophysiology from a historical context. Semin Pediatr Surg. 2018;27(1):11–18.
3. Samuels N, van de Graaf RA, de Jonge RCJ, Reiss IKM, Vermeulen MJ. Risk factors for necrotizing enterocolitis in neonates: a systematic review of prognostic studies. BMC Pediatr. 2017;17(1):105.
4. National Institute of Child Health Human Development. How many infants are affected or at risk of necrotizing enterocolitis (NEC)? http://www.nichd.nih.gov. Published 2017. Accessed December 20, 2017.
5. Rose AT, Patel RM. A critical analysis of risk factors for necrotizing enterocolitis. Semin Fetal Neonatal Med. 2018;23(6):374–379.
6. Luig M, Lui K. Epidemiology of necrotizing enterocolitis—part I: changing regional trends in extremely preterm infants over 14 years. J Paediatr Child Health. 2005;41(4):169–173.
7. Rees CM, Eaton S, Pierro A. Trends in infant mortality from necrotising enterocolitis in England and Wales and the USA. Arch Dis Child Fetal Neonatal Ed. 2008;93(5):F395–F396.
8. Guner YS, Chokshi N, Petrosyan M, Upperman JS, Ford HR, Grikscheit TC. Necrotizing enterocolitis—bench to bedside: novel and emerging strategies. Semin Pediatr Surg. 2008;17(4):255–265.
9. Gephart SM, McGrath JM, Effken JA, Halpern MD. Necrotizing enterocolitis risk: state of the science. Adv Neonatal Care. 2012;12(2):77–87; quiz 88-89.
10. Jammeh ML, Adibe OO, Tracy ET, et al Racial/ethnic differences in necrotizing enterocolitis incidence and outcomes in premature very low birth weight infants. J Perinatol. 2018;38(10):1386–1390. doi:10.1038/s41372-018-0184-x.
11. Gephart SM, Spitzer AR, Effken JA, Dodd E, Halpern M, McGrath JM. Discrimination of GutCheck(NEC): a clinical risk index for necrotizing enterocolitis. J Perinatol. 2014;34(6):468–475.
12. Patel AL, Johnson TJ, Engstrom JL, et al Impact of early human milk on sepsis and health-care costs in very low birth weight infants. J Perinatol. 2013;33(7):514–519.
13. Patel AL, Trivedi S, Bhandari NP, et al Reducing necrotizing enterocolitis in very low birth weight infants using quality-improvement methods. J Perinatol. 2014;34(11):850–857.
14. Patra K, Hamilton M, Johnson TJ, et al NICU human milk dose and 20-month neurodevelopmental outcome in very low birth weight infants. Neonatology. 2017;112(4):330–336.
15. Jasani B, Patole S. Standardized feeding regimen for reducing necrotizing enterocolitis in preterm infants: an updated systematic review. J Perinatol. 2017;37(7):827–833.
16. Gephart SM, Hanson C, Wetzel CM, et al NEC-Zero recommendations from scoping review of evidence to prevent and foster timely recognition of necrotizing enterocolitis. Matern Health Neonatol Perinatol. 2017;3:23.
17. Uauy RD, Fanaroff AA, Korones SB, Phillips EA, Phillips JB, Wright LL. Necrotizing enterocolitis in very low birth weight infants: biodemographic and clinical correlates. National Institute of Child Health and Human Development Neonatal Research Network. J Pediatr. 1991;119(4):630–638.
18. Lee HC, Kurtin PS, Wight NE, et al A quality improvement project to increase breast milk use in very low birth weight infants. Pediatrics. 2012;130(6):e1679–e1687.
19. Yee WH, Soraisham AS, Shah VS, et al Incidence and timing of presentation of necrotizing enterocolitis in preterm infants. Pediatrics. 2012;129(2):e298–e304.
20. Horbar JD, Edwards EM, Greenberg LT, et al Variation in performance of neonatal intensive care units in the United States. JAMA Pediatr. 2017;171(3):e164396.
21. Ellsbury DL, Clark RH, Ursprung R, Handler DL, Dodd ED, Spitzer AR. A multifaceted approach to improving outcomes in the NICU: the Pediatrix 100 000 Babies Campaign. Pediatrics. 2016;137(4). doi:10.1542/peds.2015-0389.
22. Benjamin J, Chong E, Reynolds J, Gordon PV, Smith JR. Detailed analysis of NEC risks across a decade in a low incidence NICU: can we drive the incidence of NEC toward zero? e-J Neonatol Res. 2012;2(4):181–190.
23. Alshaikh B, Kostecky L, Blachly N, Yee W. Effect of a quality improvement project to use exclusive mother's own milk on rate of necrotizing enterocolitis in preterm infants. Breastfeed Med. 2015;10(7):355–361.
24. Talavera MM, Bixler G, Cozzi C, et al Quality improvement initiative to reduce the necrotizing enterocolitis rate in premature infants. Pediatrics. 2016;137(5). doi:10.1542/peds.2015-1119.
25. Titler MG, Everett LQ. Translating research into practice. Considerations for critical care investigators. Crit Care Nurs Clin North Am. 2001;13(4):587–604.
26. Titler MG, Herr K, Schilling ML, et al Acute pain treatment for older adults hospitalized with hip fracture: current nursing practices and perceived barriers. Appl Nurs Res. 2003;16(4):211–227.
27. Titler MG, Herr K, Brooks JM, et al Translating research into practice intervention improves management of acute pain in older hip fracture patients. Health Serv Res. 2009;44(1):264–287.
28. Gephart SM, Wyles C, Canvasser J. Expert consensus to weight an adherence score for audit and feedback of practices that prevent necrotizing enterocolitis in very low birth weight infants. Appl Nurs Res. 2018;39:182–188.
29. Elo S, Kyngas H. The qualitative content analysis process. J Adv Nurs. 2008;62(1):107–115.
30. Sandstrom B, Willman A, Svensson B, Borglin G. Perceptions of national guidelines and their (non) implementation in mental healthcare: a deductive and inductive content analysis. Implement Sci. 2015;10:43.
31. Phillippi J, Lauderdale J. A guide to field notes for qualitative research: context and conversation. Qual Health Res. 2018;28(3):381–388.
32. Rodriguez NA, Meier PP, Groer MW, Zeller JM. Oropharyngeal administration of colostrum to extremely low birth weight infants: theoretical perspectives. J Perinatol. 2009;29(1):1–7.
33. Rodriguez NA, Meier PP, Groer MW, Zeller JM, Engstrom JL, Fogg L. A pilot study to determine the safety and feasibility of oropharyngeal administration of own mother's colostrum to extremely low-birth-weight infants. Adv Neonatal Care. 2010;10(4):206–212.
34. El-Dib M, Narang S, Lee E, Massaro AN, Aly H. Red blood cell transfusion, feeding and necrotizing enterocolitis in preterm infants. J Perinatol. 2011;31(3):183–187.
35. Wallenstein MB, Arain YH, Birnie KL, et al Red blood cell transfusion is not associated with necrotizing enterocolitis: a review of consecutive transfusions in a tertiary neonatal intensive care unit. J Pediatr. 2014;165(4):678–682.
36. Sood BG, Rambhatla A, Thomas R, Chen X. Decreased hazard of necrotizing enterocolitis in preterm neonates receiving red cell transfusions. J Matern Fetal Neonatal Med. 2016:29(5):737–744.
37. Maheshwari A, Patel RM, Christensen RD. Anemia, red blood cell transfusions, and necrotizing enterocolitis. Semin Pediatr Surg. 2018;27(1):47–51.
38. Hay S, Zupancic JA, Flannery DD, Kirpalani H, Dukhovny D. Should we believe in transfusion-associated enterocolitis? Applying a GRADE to the literature. Semin Perinatol. 2017;41(1):80–91.
39. Gephart SM, Gordon PV, Penn AH, et al Changing the paradigm of defining, detecting, and diagnosing NEC: perspectives on Bell's stages and biomarkers for NEC. Semin Pediatr Surg. 2018;27(1):3–10.
40. Lake ET, Staiger D, Horbar J, Kenny MJ, Patrick T, Rogowski JA. Disparities in perinatal quality outcomes for very low birth weight infants in neonatal intensive care. Health Serv Res. 2015;50(2):374–397.
41. Lake ET, Staiger D, Edwards EM, Smith JG, Rogowski JA. Nursing care disparities in neonatal intensive care units. Health Serv Res. 2018;53(suppl 1):3007–3026.
42. Committee on Nutrition, Section on Breastfeeding, Committee on Fetus and Newborn. Donor human milk for the high-risk infant: preparation, safety, and usage options in the United States. Pediatrics. 2017;139(1). doi:10.1542/peds.2016-3440.
43. Parker MG, Burnham L, Mao W, Philipp BL, Merewood A. Implementation of a donor milk program is associated with greater consumption of mothers' own milk among VLBW infants in a US, level 3 NICU. J Hum Lact. 2016;32(2):221–228.
44. Patel RM, Knezevic A, Shenvi N, et al Association of red blood cell transfusion, anemia, and necrotizing enterocolitis in very low-birth-weight infants. JAMA. 2016;315(9):889–897.
Keywords:

adherence score; breastfeeding; human milk; human milk expression; implementation strategy; necrotizing enterocolitis; NEC-Zero; quality improvement; variations; very low birth-weight infant

© 2019 by The National Association of Neonatal Nurses