BACKGROUND AND OBJECTIVES:

Infants in NICUs are at risk for underimmunization. Adherence to the routine immunization schedule recommended by the Advisory Committee for Immunization Practices minimizes the risk of contracting vaccine-preventable illnesses in this vulnerable population. From January 2015 to June 2017, only 56% (419 of 754) of the infants in our Mayo Clinic level IV NICU were fully up to date for recommended immunizations at the time of discharge or hospital unit transfer. We aimed to increase this rate to 80% within 6 months.

METHODS:

Using the quality improvement methodology of Define, Measure, Analyze, Improve, Control, we analyzed baseline data, including provider and nursing surveys using a fishbone diagram, the 5 Whys, and a Pareto chart. We identified 3 major root causes of the quality gap: lack of provider knowledge of the routine immunization schedule, failure of providers to order vaccines when due, and hesitancy of parents toward vaccination. Using plan-do-study-act cycles, 5 improvement interventions were implemented. These included an intranet resource for NICU providers on the routine immunization schedule, an Excel-based checklist to track when immunizations were due, and provider education on parental vaccine hesitancy and vaccine safety.

RESULTS:

During the 19-month improve and control phases of the project, the fully immunized rate at the time of NICU discharge or transfer rose from a baseline of 56% (419 of 754) to 93% (453 of 488), with a P value <.001.

CONCLUSIONS:

Our NICU significantly improved infant immunization rates with a small number of interventions. These interventions may be generalizable to other NICUs with low infant immunization rates.

Infants cared for in the setting of a NICU represent a vulnerable population with regard to vaccine-preventable illnesses. Many of these infants develop chronic medical conditions, such as chronic lung disease of prematurity, which place them at higher risk of developing serious medical complications from infections. For example, authors of previous studies have found that low birth weight infants have increased risk of contracting pertussis and increased disease severity with pertussis infection.1,2 

Premature and low birth weight infants have adequate immune responses to immunizations using the same routine schedules used in normal birth weight term infants.3  The Advisory Committee on Immunization Practices (ACIP), the American Academy of Pediatrics, the American Academy of Family Physicians, and the American College of Obstetricians and Gynecologists all recommend the same routine vaccine schedule.4,5  These harmonized recommendations call for vaccinations at certain chronological ages, regardless of birth weight or gestational age at birth, with the exception of delayed timing of the first dose of hepatitis B (HepB) vaccination in infants <2 kg at time of birth whose mothers had negative test results for HepB surface antigen during pregnancy.4,5 

Despite this harmonized schedule, infants cared for in NICUs have high rates of under-immunization during their NICU stay, at time of hospital discharge, and in later childhood. Authors of a retrospective cohort study of infants 2 months of age or older at time of discharge found that only 51% were fully up to date with immunizations at NICU discharge.6  Furthermore, this under-immunization may persist for years. Langkamp et al7  demonstrated that very low birth weight infants were more likely to be underimmunized at 12, 24, and 36 months. A recent study of infants cared for in the US military health care system revealed decreased immunization rates at 24 months for former low birth weight infants.8  Similarly, low immunization rates have been reported at 12 months of life for extremely low birth weight infants.9  In contrast, receipt of at least 1 immunization before initial hospital discharge is correlated with higher immunization rates at 24 months.10 

In our NICU, we found that baseline immunization rates were well below the Healthy People 2020 target rates of 90% for the infant vaccine series.11  Between January 1, 2015, and June 30, 2017, only 56% (419 of 754) of infants cared for in our NICU received all doses of routine immunizations recommended by the time of discharge or hospital unit transfer. Our specific aim for this quality improvement (QI) project was to increase our NICU’s fully up-to-date immunization rate at time of discharge or unit transfer from 56% to 80% over a 6-month improvement phase, from October 1, 2017, to March 31, 2018.

We conducted our project at a single-site 26-bed level IV NICU at Mayo Clinic in Rochester, Minnesota. The practice includes 8 neonatologists, 3 neonatal-perinatal medicine fellows, 16 nurse practitioners, and 112 bedside nurses. The practice also has rotating pediatric residents and medical students. More than 350 infants are cared for in the NICU annually, with 18% being very low birth weight. Mayo Clinic sponsored this QI project.

A neonatal-perinatal medicine fellow (R.C.S) led this project with the collaboration of 2 neonatologists (J.L.F. and C.E.C.) and the medical director of the institution’s primary care immunization program (R.M.J). One of the team leaders (J.L.F.) has advanced training in QI methodology. She provided feedback and coaching throughout all phases of the project. The Six Sigma core tool of Define, Measure, Analyze, Improve, Control was used for this QI project. The Mayo Clinic Institutional Review Board considered this project not human subjects research and exempt from its review.

To identify the root causes leading to our quality gap, we used a number of QI tools. Initially, members from our project met with various stakeholders to qualitatively assess potential barriers to on-time vaccination. Stakeholders included neonatologists, neonatal-perinatal fellows, pediatric residents, nurse practitioners, community pediatric and adolescent medicine staff, and pediatric pharmacists. From the information learned from these discussions, we constructed a fishbone diagram and a 5-Whys diagram (Figs 1 and 2).

FIGURE 1

The fishbone diagram analysis of the baseline immunization process in the NICU.

FIGURE 1

The fishbone diagram analysis of the baseline immunization process in the NICU.

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FIGURE 2

Five-Ways analysis of causes of under-immunization in the NICU.

FIGURE 2

Five-Ways analysis of causes of under-immunization in the NICU.

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To better quantify the impact of these barriers, we sent surveys (Research Electronic Data Capture [REDCap] version 7.4.23; Vanderbilt University, Nashville, TN) to stakeholders. Five questions, based on common themes from stakeholder meetings, were included in the survey related to perceived barriers to on-time immunization. The severity of potential barriers to on-time immunization were ranked by using a 5-point Likert scale (1 = not a barrier at all; 5 = significant barrier). We constructed a Pareto chart on the basis of these survey responses to rank the impact of root causes on the quality gap (Fig 3).

FIGURE 3

Pareto chart analysis of factors contributing to under-immunization in the NICU.

FIGURE 3

Pareto chart analysis of factors contributing to under-immunization in the NICU.

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On the basis of this analysis, we identified 3 major root causes of underimmunization in our NICU: (1) providers lacking knowledge of the routine ACIP immunization schedule, (2) providers not ordering immunizations when they were due, and (3) parents expressing hesitancy toward vaccination.

The improve phase of the project lasted for 6 months, from October 1, 2017, through March 31, 2018. The 5 plan-do-study-act (PDSA) cycles are summarized in Table 1. We implemented 3 PDSA cycles in October 2017. Each targeted 1 of the main root causes of underimmunization identified during the analyze phase.

  • For the first PDSA cycle, we addressed the lack of provider knowledge of the ACIP immunization schedule by creating a readily accessible, easy-to-interpret intranet resource for NICU providers that detailed the routine vaccine schedule and minimal dosing intervals. This included a separate flow sheet that addressed the timing of HepB immunizations. This vaccine series is more complex than other vaccines because the provider must take into account maternal HepB surface antigen status and infant birth weight.

  • The second PDSA cycle addressed providers forgetting to order vaccines when they were due. We implemented an Excel-based checklist to track and flag the immunization status of all infants cared for in the NICU (Microsoft Excel, version 14.0.7208.5000; Microsoft Corporation, Redmond, WA). The NICU clinical assistant maintained the checklist. When the Excel-based checklist indicated that a patient was due for an immunization, the NICU clinical assistant notified the provider team. To prevent interval dosing errors, we programmed the checklist to adjust the indicated due date of upcoming immunizations on the basis of the ACIP minimal dosing intervals (Supplemental Table 3).

  • The third PDSA cycle involved creating a separate intranet education resource on counseling parents with hesitancy regarding vaccination of their infant. This resource used Allison Tepper Singer’s Corroborate, About me, Science, Explain/Advise (CASE) approach to vaccine hesitancy.12,13 

  • The fourth PDSA cycle focused on provider education and spanned between November and December 2017. Providers received this education in the form of in-time bedside teaching, e-mail communications, and an intradepartment newsletter. This included reinforcement of interventions implemented in PDSA cycles 1 through 3. Additionally, education was provided on the safety of administering immunizations to infants within the NICU. This included review of literature related to potential adverse events after vaccine administration in premature infants, such as increased apneic events or sepsis evaluations, as well as the limitations of these studies.

  • The fifth PDSA cycle was implemented in December 2017. It focused on improving documentation of parental consent for vaccines within the electronic health record (EHR). These interventions included NICU provider education on the required elements of vaccine consent and creation of shorthand templates for documenting vaccine consent in the EHR.

TABLE 1

PDSA Cycles

DateImprovementLabela
October 2017 Intranet resources including first HepB vaccine timing flow sheet, routine infant vaccine schedule, and vaccine minimal dosing intervals PDSA No. 1 
October 2017 Excel-based checklist to track and flag immunization status of all infants in NICU PDSA No. 2 
October 2017 Intranet resource and education on using CASE approach to discussing vaccines with hesitant parents PDSA No. 3 
November–December 2017 NICU provider education on safety of administering vaccines to infants and reinforcement of previous improvements PDSA No. 4 
December 2017 NICU provider education on documentation of parental consent for vaccine administration and creation of documentation resources within the EHR PDSA No. 5 
DateImprovementLabela
October 2017 Intranet resources including first HepB vaccine timing flow sheet, routine infant vaccine schedule, and vaccine minimal dosing intervals PDSA No. 1 
October 2017 Excel-based checklist to track and flag immunization status of all infants in NICU PDSA No. 2 
October 2017 Intranet resource and education on using CASE approach to discussing vaccines with hesitant parents PDSA No. 3 
November–December 2017 NICU provider education on safety of administering vaccines to infants and reinforcement of previous improvements PDSA No. 4 
December 2017 NICU provider education on documentation of parental consent for vaccine administration and creation of documentation resources within the EHR PDSA No. 5 
a

Labels are used to indicate the timing of interventions in Fig 4.

We assessed the primary outcome measure and impact of the QI interventions using time series analysis with an annotated run chart. For the preintervention period, we used the monthly percentages of infants up to date on their immunizations to calculate the median baseline. During the intervention period, we calculated monthly percentages and plotted them on run and control charts, with the PDSA cycles annotated to indicate the month in which we implemented them. This allowed for temporal insights between the time series data and changes the QI team made to the system.

The QI project began on October 1, 2017, and concluded on April 30, 2019. The baseline preintervention period extended from January 1, 2015, through June 30, 2017. The improve phase took place from October 1, 2017, through March 31, 2018, with the control phase spanning from April 1, 2018, through April 30, 2019. All patients discharged or transferred from the NICU each month were included in the data abstraction.

The primary outcome measure for this QI initiative was the percentage of infants who were up to date on their immunizations at time of NICU discharge or transfer. We ascertained immunization rates by chart review of the EHR for all infants discharged or transferred from the Mayo Clinic NICU during the study period. A single team leader (R.C.S.) reviewed all charts. We counted infants as fully up to date if they had received all immunizations due per the ACIP immunization schedule, with the exception of rotavirus vaccination. We excluded rotavirus vaccination from this assessment because it was our policy not to administer live vaccines within the NICU.

A secondary outcome measure was the delay in immunization for each vaccine (HepB vaccine, pneumococcal conjugate vaccine 13-valent [PCV13], diphtheria-tetanus-acellular pertussis inactivated poliovirus–Haemophilus influenzae type b [DTaP-IPV/Hib]) at each age it was due (birth, 1, 2, 4, 6 months). We counted the delay by subtracting the intended age of each vaccine per the ACIP schedule from the age the vaccine was given. If an eligible infant never received a vaccine during the NICU stay, we tallied the delay until the date of NICU discharge or unit transfer. For example, if an infant with a birth weight <2 kg received the first HepB on day-of-life 41, we counted the delay as 11 days. We tracked the rate of inappropriate immunizations, such as immunizations given too early (ie, violating the minimum age or minimum interval) as a balancing measure.

We determined the effectiveness of the interventions by evaluating an annotated run chart for signal of sustained improvement. Once we noted sustained improvement, we used statistical process control p-charts to monitor for special-cause variation, including performance outside the upper and lower control limits. Excel was used to create the p-chart with control limit formulas as described by Provost and Murray.14  In addition, we used statistical analysis to compare baseline versus postintervention delays for each vaccine. All presented data were analyzed in Excel and GraphPad QuickCalcs Software (La Jolla, CA). Continuous variables were analyzed by using 2-tailed t tests, and categorical variables were analyzed with 2-tailed Fisher’s exact tests. P values of <.05 were considered statistically significant.

Throughout the project period, the NICU discharged or transferred 1242 infants. This included 754 patients in the preintervention period and 488 patients in the postintervention period. We excluded patients from the QI project if they died or were transferred before any immunizations were due. For infants ≥2 kg at birth, this included death or hospital unit transfer within the first 24 hours after birth. For infants <2 kg at birth, this included death or hospital unit transfer within the first 30 days after birth. In the preintervention period, 160 infants were excluded because of death (n = 33) or unit transfer (n = 127) During the postintervention period, we excluded 62 infants because of death (n = 15) or unit transfer (n = 47). Of the 754 infants included in the baseline period, 56% of infants (n = 419) were fully up to date at the time of NICU discharge or unit transfer.

We sent electronic surveys to multiple stakeholders in the NICU to better understand potential root causes of the quality gap before the initiation of any interventions (REDCap). A total of 84 stakeholders completed surveys with a response rate of 48%. Using a 5-point Likert scale, respondents rated the degree to which they felt certain barriers led to the low vaccination rate within the NICU. The Pareto chart (Fig 3) reveals these findings.

At the end of the control phase, we sent a follow-up survey (REDCap) to the same group of stakeholders. A total of 65 individuals completed the follow-up survey for a response rate of 37%. Using 5-point Likert scales, survey respondents indicated a statistically significant increase in their satisfaction with the system used within the NICU for ordering and giving immunizations (P = .01). We found no statistically significant differences in provider-reported comfort level in discussing vaccines with vaccine-hesitant parents, likelihood to recommend other NICUs adopt our system for ordering and giving vaccines, or provider self-reported knowledge of the routine infant immunization schedule.

During the 6-month improve phase, the percentage of infants up to date on their immunizations increased to 93.5% (145 of 155). The rate was similar during the first 13 months of the control phase with 92.5% (308 of 333) of infants up to date. The combined rate of fully immunized infants during the improve and control phases was 92.8%, which was significantly improved from the baseline rate (P < .001). Monthly fully immunized rates are revealed on a p-control chart (Fig 4). The mean number of days immunizations were delayed compared to the intended routine schedule is demonstrated in Table 2. Statistically significant reductions in delays of administration of vaccines were achieved in the improvement and control phases for all vaccines routinely given before 6 months of age. We only had 1 infant older than 6 months of age discharged or transferred during the improve and control phases.

FIGURE 4

Percentage of NICU patients fully up to date for vaccines at discharge or transfer. A p-control chart of monthly rates of infants fully immunized at the time of NICU discharge or transfer is shown.

FIGURE 4

Percentage of NICU patients fully up to date for vaccines at discharge or transfer. A p-control chart of monthly rates of infants fully immunized at the time of NICU discharge or transfer is shown.

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TABLE 2

Pre- Versus Post-QI Mean Days Immunizations Delayed From Intended Routine Schedule

VaccineImmunization Delay, dP
BaselineImprovement and Control Phases
First HepB, if BW <2 kg 13.8 8.1 .007 
First HepB if BW ≥2 kg 8.8 2.3 <.001 
Second Hep B 19.5 5.2 <.001 
Third HepB 16.4 N/A 
First PCV13 8.6 2.9 .005 
Second PCV13 17.1 4.5 .01 
Third PCV13 16.4 N/A 
First DTaP-IPV/Hib 8.6 2.9 .005 
second DTaP-IPV/Hib 17.1 4.5 .01 
Third DTaP-IPV/Hib 16.4 N/A 
VaccineImmunization Delay, dP
BaselineImprovement and Control Phases
First HepB, if BW <2 kg 13.8 8.1 .007 
First HepB if BW ≥2 kg 8.8 2.3 <.001 
Second Hep B 19.5 5.2 <.001 
Third HepB 16.4 N/A 
First PCV13 8.6 2.9 .005 
Second PCV13 17.1 4.5 .01 
Third PCV13 16.4 N/A 
First DTaP-IPV/Hib 8.6 2.9 .005 
second DTaP-IPV/Hib 17.1 4.5 .01 
Third DTaP-IPV/Hib 16.4 N/A 

BW, birth weight; N/A, not applicable.

There was no statistical difference in the balancing measure of immunizations given inappropriately between the baseline measure and the improve and control phases. During the baseline measure, 10 immunizations were inappropriately administered out of 1150 total immunizations given (8.7 per 1000 immunizations). Four immunizations were administered inappropriately during the improve and control phases out of 555 immunizations given (7.2 per 1000 immunizations; P value = .99).

Through the use of Define, Measure, Analyze, Improve, Control QI methodology, we were able to significantly improve the rate of infants fully up to date for immunizations at the time of discharge or transfer from our level IV NICU. We exceeded our original goal and have maintained a fully vaccinated rate of >90% for more than a year. Additionally, we were able to significantly decrease the number of days that immunizations were delayed compared to the routine infant vaccination schedule endorsed by the ACIP and others.

Our low baseline NICU infant immunization rate is in line with other studies of this population.6,10  Authors of a QI effort in an Alabama NICU found similar barriers to on-time immunization of premature infants <29 weeks, including providers not remembering to order vaccines and parental and staff hesitancy to administer vaccinations.15  Systematic tracking of when immunizations are due has been used in other successful NICU infant immunization improvement efforts.15,16  Efforts targeting provider education on immunizations led to improved immunization rates in infants with congenital heart disease cared for in a PICU.17  Immunization rates of infants with chronic lung disease were improved with implementation of regular immunization record review, implementation of rounding tools, and several other small improvement efforts.18 

Our project has limitations. Three of our interventions were introduced simultaneously, which makes it difficult to assess the impact of any single intervention. In other NICUs, factors other than those identified by our single-site QI project may lead to low infant immunization rates. Among these are provider and parental concern of adverse events after routine immunizations within this population. Higher rates of sepsis evaluations and increases in respiratory support have been reported in the days after immunization in premature and extremely low birth weight infants.1921  A limitation of these studies and similar observational approaches is that the days before immunization were used as a baseline, and providers may delay immunizations until times of clinical stability, which may overestimate adverse effects of vaccine administration.22  An argument can also be made that risk of cardiorespiratory events after immunization makes it more important to immunize NICU infants before hospital discharge while they are still under close medical monitoring and care.

Infants treated in NICUs represent a vulnerable population with the potential for high morbidity and mortality from vaccine-preventable infections. Our QI effort, and others, demonstrate that this population is at risk for underimmunization and that immunization rates can be improved with a small number of interventions. We encourage other NICUs to assess their baseline immunization rates of their infants and to undertake QI efforts if needed.

In our NICU, we have implemented a control plan to sustain the improved infant immunization rate, which includes regular monthly audits of the infant immunization rate plotted on a control chart. If the monthly rates deviate from the lower control limit or decrease below our goal rate of 80%, we will perform further root-cause analyses.

We acknowledge the multidisciplinary team whose work made this project a success including Elsa Thompson; Jennifer Brickley, RN; Ole Olson, RPh; Kevin Graner, RPh; and Virginia Schuning, RN.

Dr Stetson conceptualized and designed the quality improvement project, designed survey and data collection instruments, collected and analyzed data, drafted the initial manuscript, and reviewed and revised the manuscript; Drs Fang, Colby, and Jacobson conceptualized and designed the quality improvement project and critically reviewed the manuscript for important intellectual content; and all authors approved the final manuscript as submitted and agree to be accountable for all aspects of the work.

FUNDING: No external funding.

ACIP

Advisory Committee for Immunization Practices

CASE

Corroborate, About me, Science, Explain/Advise

DTaP-IPV/Hib

diphtheria-tetanus-acellular pertussis inactivated poliovirus–Haemophilus influenzae type b

EHR

electronic health record

HepB

hepatitis B

PCV13

Pneumococcal conjugate vaccine 13-valent

PDSA

plan-do-study-act

QI

quality improvement

REDCap

Research Electronic Data Capture

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Competing Interests

POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

FINANCIAL DISCLOSURE: Dr Jacobson serves as a member of 2 safety review committees, 1 for a postlicensure study of the quadrivalent human papillomavirus vaccine in men (funded by Merck) and another postlicensure study of the nonavalent human papillomavirus vaccine in both sexes (also funded by Merck). Dr Jacobson also serves as a member of a data and safety monitoring board for a series of prelicensure studies of adults and infants with a 15-valent pneumococcal conjugate vaccine (also funded by Merck); Drs Stetson, Fang, and Colby have indicated they have no financial relationships relevant to this article to disclose.

Supplementary data