OBJECTIVES. The objective of this study was to test the hypothesis that clinical alerts for routine pediatric vaccinations within an electronic health record would reduce missed opportunities for vaccination and improve immunization rates for young children in an inner-city population.
METHODS. A 1-year intervention study (September 1, 2004, to August 31, 2005) with historical controls was conducted in 4 urban primary care centers affiliated with an academic medical center. All children who were younger than 24 months were enrolled. Electronic health record–based clinical reminders for routine childhood vaccinations were programmed to appear prominently at every patient encounter with vaccines due. The main outcome measures were rates of captured immunization opportunities and overall immunization rates at 24 months of age.
RESULTS. Immunization alerts appeared at 15928 visits during the intervention. Alert implementation was associated with increases in captured immunization opportunities from 78.2% to 90.3% at well visits and from 11.3% to 32.0% at sick visits. Adjusted up-to-date immunization rates at 24 months of age increased from 81.7% to 90.1% from the control to intervention period. Children in the intervention group also became up-to-date earlier than control patients. Patient characteristics were stable throughout the study.
CONCLUSIONS. An electronic health record–based clinical alert intervention was associated with increases in captured opportunities for vaccination at both sick and well visits and significant improvements in immunization rates at 2 years of age. As electronic health records become more common in medical practice, such systems may transform immunization delivery to children.
Improving the quality of health care has increasingly become a national priority.1,2 Despite a recognized lack of quality measures for children,3 immunization rates have been designated as 1 of the 10 leading health indicators for the nation by Healthy People 20104 and have been found to be responsive to quality improvement initiatives.5 Immunization rates are a particularly useful measure of the quality of pediatric care because immunization schedules are clearly delineated, standardized nationally, and structured to protect children from life-threatening illness. Even with this focus, levels of vaccination for 19- to 35-month-olds in many areas remain below goals of 90% coverage.6 Among the >4000000 children born annually in the United States alone who require routine immunizations, minority children continue to have the lowest rates of up-to-date vaccination.7
The persistence of overall immunization rates below national targets and continuing differences across racial and ethnic groups indicate the need for novel strategies to improve immunization delivery. These approaches may be directed at increasing demand for vaccines and enhancing access to care for parents and their children or may focus on providers and their ability to vaccinate children in their practices effectively through such strategies as preventing missed opportunities for immunization.8,9 Sparked by the 2001 publication of Crossing the Quality Chasm: A New Health System for the 21st Century,2 health care providers have increasingly focused attention on improving outcomes using computer systems.10
These systems have been implemented in both pediatric and adult settings. Among adults, computer systems have been used to improve influenza vaccination rates by generating mailed reminders11 and identifying at-risk hospitalized12 and primary care patients.13 For children, electronic systems have reduced inaccuracies in the charting of vaccines14 and have generated reminders for families through autodialer calls and automated letters based on computerized registries.15–17 However, research has demonstrated limitations of registry-based reminders in the inner city, including incomplete records, inaccurate contact information, patient missed visits, and provider missed opportunities.18–21 Overall, the importance of electronic systems for determining immunizations that are due at pediatric health care visits is even greater than in other areas given the complexity of the immunization schedule,22–26 frequent changes in immunization recommendations, and the prevalence of invalid doses such as those given too early, which may be erroneously counted toward up-to-date status.27,28
The combination of electronic health records (EHRs) with alerts delivered to clinicians at the point of care represents a particularly promising strategy to improve routine vaccination rates in pediatric practice.29 EHR systems have been shown to be reliable and are capable of identifying children with immunization delay.18 Current estimates indicate that >20% of all primary care pediatric practices use EHRs and that rates of adoption exceed 30% for larger practices and near 50% for practice networks.30 As the adoption of EHRs continues to expand, clinical alerts can become a key strategy in improving immunization rates and, ultimately, the health of children. Therefore, this formal evaluation tests the hypothesis that clinical alerts for routine pediatric vaccinations increase the proportion of immunization opportunities captured at health care visits, improve overall immunization rates for children at 24 months of age, and decrease the age when children become up-to-date.
Setting and EHR
The Children's Hospital of Philadelphia (CHOP) Primary Care Network consists of 4 urban Philadelphia practices with a combined total of >72000 annual visits. Fewer than 25% of patients in the practices have private insurance, and >80% are minorities. Nearly 45 pediatricians and 5 nurse practitioners provide care at the 4 sites. In addition, these practices serve as the continuity clinics for ∼120 pediatric residents. Immunization rates in this population historically closely match those rates for Philadelphia published in the National Immunization Survey.31 The ambulatory EHR, EpicCare (Verona, WI), was implemented in each practice between June 2001 and June 2002.
Study Design and Patient Population
We performed a 1-year intervention study beginning in September 2004. The visit-level analysis included all sick or well office visits by children who were younger than 24 months and had at least 1 study vaccine due in the 1-year control or intervention period. For the main patient-level analysis, all children who reached 24 months of age between September 1, 2004, and August 31, 2005, were included in the intervention group, and historical control subjects included children who reached 24 months of age in the year before the intervention (September 1, 2003, to August 31, 2004). In addition, intervention and control patients were required to have at least 1 visit during the intervention or control period, respectively. This ensured that intervention patients had an opportunity to be exposed to the immunization alerts.
EHR-based clinical reminders for routine childhood vaccinations were programmed to appear prominently whenever any patient encounter was opened within the EHR for a child who was younger than 2 years. The alerts appeared for all clinical staff who interacted with the system during both office visits and telephone care. Because alerts are most effective when they support existing workflows, no function was developed to force adherence to or review of the alerts.32 Vaccines considered in the EHR decision support system included diphtheria, tetanus, acellular pertussis (DTaP); Haemophilus influenzae type b (Hib); inactivated poliovirus (IPV); measles-mumps-and rubella (MMR); hepatitis B (Hep B); pneumococcal conjugate vaccine (PCV); and varicella. Prompted by an incomplete immunization record within the EHR, the alerts used a multistep process to advise users of the specific vaccines due when they opened a patient chart. First, invalid vaccine doses, those given at too young an age or too close to a previous dose, were excluded. Next, considering the child's age, the timing of previous doses, and the interval since their administration, the system determined which antigens were due. The system accounted for such details as the need for only 2 Hib vaccine doses for children who were immunized starting at 12 months and only 1 dose for those who were vaccinated beginning at 15 months of age. To increase the proportion of immunization opportunities captured among patients who were known to be at high risk for immunization delay, we programmed alerts to appear at or near the earliest point allowed according to the Advisory Committee on Immunization Practices (ACIP) guidelines (Table 1). 23–25 Subsequently, the system checked whether any combination vaccine products were available to minimize the number of shots a child received and then presented recommendations to the provider. For simplification of interpretation of the alerts, the dates of any vaccines that were considered invalid were presented along with the immunization record in the patient summary screen, known as the snapshot, within the EHR. The entire process of presenting the alerts resulted in no perceptible delay in accessing the patient chart.
Alerts included direct links to immunization order sets to facilitate the administration of due vaccines. At office visits with pediatricians or nurse practitioners, the provider ultimately decided whether due vaccines were administered and had the opportunity to defer vaccination if contraindications were recognized or the family declined. The clinician chose whether to document the reason that vaccines were not given. The implementation of the alerts did not change the office workflow for nurse visits.
Because the alerts were developed within the context of a quality improvement initiative designed to improve immunization rates, the implementation of the clinical alerts was accompanied by provider, nurse, and office staff education. Provider training, conducted in the months surrounding alert implementation, began in June 2004 and included a discussion of baseline immunization rates and barriers to timely immunization. The study team held 2 telephone conferences with physicians, nurses, and administrators to discuss office workflows and answer specific questions about alerts. In addition, designated on-site physician and nurse leaders or the study team answered ongoing questions from the treating clinicians.
During the control period, no vaccine alerts existed, but providers and nurses always were able to review the immunization record within the EHR and decide which vaccines were due. Immunizations could be readily ordered and charted with the EHR, but a direct link to immunization orders was not presented. In addition, before the intervention, there was no consensus regarding the strategy of immunizing at the earliest possible opportunity per ACIP guidelines. Vaccine-related education that was conducted by attending physicians and nurses and focused on immunization guidelines did occur before and during the control period, often in the context of resident teaching.
This study was designed to test the effect of immunization alerts on 2 main outcomes: (1) rates of captured opportunities for vaccination (visit-level analysis) and (2) overall immunization rates at 2 years of age (patient-level analysis). The impact of the intervention on the age when children became up-to-date was also investigated. Rates of captured vaccine opportunities were assessed at the visit level and measured the proportion of all sick or well visits at which at least 1 study vaccine was given if due. Additional analysis addressed only the subset of these visits with at least 1 delayed (past due) vaccine per ACIP guidelines. As an additional end point, the proportion of all sick or well visits at which all due vaccines were given was considered. All study vaccines were included in the main analysis of captured opportunities. However, a sensitivity analysis that excluded the pneumococcal vaccine because of shortages was conducted. In addition, the sensitivity analysis accounted for a change in practice regarding the fourth dose of DTaP. Before the intervention, this dose generally was administered beginning at 15 months of age. In contrast, because the population was recognized as high risk, alerts for this dose during the intervention began at 12 months of age.24,25 To address this change, the main analysis included all visits with DTaP 4 due between 12 and 15 months as immunization opportunities, whereas the sensitivity analysis excluded these opportunities from consideration.
The patient-level analysis considered up-to-date immunization rates at 24 months of age for 4 DTaP, 3 IPV, 1 MMR, 3 Hib, 3 Hep B, and 1 varicella (4:3:1:3:3:1). As a secondary analysis, immunization rates were calculated excluding invalid doses. PCV was not included in the patient-level analysis because of prolonged shortages during the study period.
Covariates were chosen to assess the stability of patient characteristics between the control and intervention periods. These include patient race, gender, insurance status, and the practice site where patients received care. Like these measures, the proportion of children with chronic medical conditions is an important indicator of practice stability. The chronic medical problems considered in this study were derived from a previously published list and include multiple conditions that may require increased use of health services.33 The conditions included diabetes, sickle cell anemia, cerebral palsy, seizures, asthma, congenital heart disease, trisomy 21, cancer, immunocompromise, autoimmune disease, major organ disease such as cystic fibrosis, developmental delays, and congenital anomalies.
The proportion of covariates present among intervention versus control patients were compared by χ2 tests, and P values were reported. P ≤ .05 was considered significant. The central analysis was performed using Stata 9 (College Station, TX).
For the main visit-level analysis, the proportion of sick or well visits that had vaccines due and at which at least 1 due vaccine was given during the intervention and control periods was calculated. This analysis was repeated including only visits with at least 1 delayed vaccination. In addition, the proportion of immunization opportunities captured was calculated for visits at which all due vaccines were given. In each case, the risk difference with 95% confidence interval (CI) between the proportion of immunization opportunities captured in the intervention versus control period was determined. Results were confirmed by sensitivity analyses that excluded visits with only PCV due or only the fourth dose of DTaP due among those who were younger than 15 months.
For the patient-level analysis, up-to-date rates for patients at 24 months of age for the study vaccines were compared between the intervention and control periods. Risk differences were standardized to the characteristics of all children in the sample so that comparisons would not be confounded by chance differences in children's characteristics or providers' behavior over time.34 Bias-corrected CIs were estimated using 999 bootstrap resamplings. We implemented this marginal standardization using Sudaan 9 (RTI International, Research Triangle Park, NC). These methods accounted for the clustering of observations within clinician in estimating variances and all CIs. Thus, all estimates assume that some clinicians were more likely to follow alerts than others.
To illustrate the impact of this intervention on the age when children became up-to-date for all study vaccines, we conducted a survival analysis and generated Kaplan-Meier survival curves. The P value adjusted for patient-level covariates for the difference in the time to up-to-date between the intervention and control patients was obtained by Cox regression. The institutional review board of CHOP approved the study.
For the analysis of up-to-date rates at 24 months of age, 1669 intervention and 1548 control patients and were included (Table 2). Overall, the 2 groups were similar. Among the chronic medical problems in this inner-city population, asthma was the most common condition followed by developmental delays.
During the control period, 19909 (11772 well and 8137 sick) visits occurred with immunizations due. Immunization alerts among children who were younger than 24 months appeared at 15928 (10318 well and 5610 sick) visits during the intervention period.
The implementation of EHR alerts was associated with significant increases in captured immunization opportunities at all visits (Table 3, Fig 1). The proportion of well visits with at least 1 immunization given if any vaccine was due increased from 78.2% to 90.3% (risk difference 12.2 percentage points; 95% CI: 11.2%–13.1%). Immunization opportunities captured at sick visits increased from 11.3% to 32.0% from the control to intervention year (risk difference 20.7 percentage points; 95% CI: 19.3%–22.1%). For sick visits, the proportion of captured immunization opportunities each month of the intervention was higher than during any month of the control period. The proportion of captured well-visit opportunities for the last 10 months of the intervention exceeded any month of the control period.
Alerts also improved immunization delivery at visits by children with vaccine delay (Table 3). Furthermore, the alert system was associated with an increase in the proportion of visits at which all due vaccines were given. In all analyses, significant improvements during the intervention persisted when correcting for PCV shortages and changes in the timing of DTaP 4. Total immunization opportunities decreased from the control to the intervention period and in the corrected analysis (Table 3).
Unadjusted up-to-date immunization rates at 24 months of age increased from 81.8% in the control period to 90.1% in the intervention period (risk difference: 8.3 percentage points; 95% CI: 5.9%–10.7%). After adjustment for all covariates and clustering by provider, the large improvement in immunization rates at 24 months persisted. Rates increased 8.4% (95% CI: 5.8%–10.6%) in this analysis from 81.7% to 90.1%.
Immunization rates were also measured excluding invalid doses. Unadjusted rates were 79.5% in the control versus 88.2% in the intervention period (P < .001). With this correction, a total of 36 control patients and 31 intervention patients were no longer up-to-date at 24 months. These numbers represent 2.3% of control and 1.9% of intervention patients. Adjusting for all covariates, children in the intervention group also became up-to-date earlier than control patients (P < .001; Fig 2).
Alerts for routine pediatric vaccines in this study were associated with an immediate and significant increase in immunization rates. Captured immunization opportunities at well visits increased >10% and those at sick visits increased threefold after implementation of the EHR-based alert system. With this 1-year intervention, immunization rates rose >8% among patients who were exposed to the intervention, and the age at which children became up-to-date decreased.
Because failure to capture every opportunity to vaccinate has been found to cause 13% of incomplete vaccination in suburban practices, 27% in the clinic setting, and 40% in other practices,35 a successful alert system for routine pediatric immunizations depends on increasing the proportion of opportunities for immunization that result in vaccination. For this reason, alerts appeared at or near the earliest recommended age according to ACIP guidelines.36 Because missed opportunities to vaccinate most often occur at sick visits despite the willingness of parents to accept immunization in this setting37,38 and a lack of true contraindications,39 the substantial improvement in captured opportunities to vaccinate at sick visits confirms the effectiveness of the alerts.
This intervention also addressed another significant source of missed opportunities: failure to give all due vaccines.39 Alerts were associated with a greater increase in the proportion of children who received all due vaccines than received at least 1 due vaccine. Even accounting for PCV shortages and changes in the administration of the fourth DTaP dose, these increases persisted at both well and sick visits.
The success of this project involved using an EHR-based strategy as a part of a broader quality improvement initiative. For development of the immunization alert system, it was necessary to standardize the immunization schedule. As part of this process, the decision was made to activate the alerts at the earliest possible opportunity per ACIP guidelines. This change in approach may have contributed to the observed improvement in immunization practice. In addition, as Fig 1 demonstrates, rates of captured immunization opportunities began to rise at both sick and well visits with provider and practice education. However, reflecting the impact of the EHR-based system, the implementation of the alerts was associated with an additional improvement in rates of captured immunization opportunities at both sick and well visits, which was sustained throughout the intervention year. This finding is consistent with the immunization literature, which suggests that multicomponent interventions that include education are often effective and that education alone, particularly when of limited intensity, is of uncertain benefit.8
The effectiveness of this intervention likely depended on the design of the immunization alert system according to published guidelines for effective clinical decision support.32,40 The alerts appeared at the point of care, offered a specific recommendation, and then facilitated compliance with that recommendation. In addition, discussion was fostered through nurse and physician leaders at each site to develop a consensus around the established approach for the alerts: immunize at the earliest possible opportunity per established guidelines.36 Furthermore, the system met a known need. Invalid doses are commonly administered by providers at all levels,27 and important deficiencies exist in providers' knowledge of immunization schedules and contraindications.41
The approach used in this study has several limitations. By using historical control subjects, this study is potentially subject to bias from vaccine shortages. However, in the practices considered, the PCV was the only one affected by persistent supply problems and controlling for shortages did not reduce the study's effect. Through the use of historical control subjects, this study is also potentially vulnerable to confounding by trends in immunization practice. However, given the dramatic and immediate change in vaccination behavior and the 8% improvement in immunization rates at 24 months of age that accompanied the activation of the clinical alerts, we do not believe that the findings are biased by secular trends. Additional suggesting that secular trends do not explain the observed pattern, rates for 4 DTaP, 3 IPV, and 1 MMR actually decreased slightly from the control to intervention period for nonstudy sites according to the Philadelphia Kids Immunization Database/Tracking System, the city's immunization registry (C. Victor Spain, DVM, PhD, written communication, 2007).
Although this intervention was associated with significant improvements in immunization delivery, rates of captured immunization opportunities did not reach 100% for well visits or exceed 45% for sick visits. At well visits, children with precautions, contraindications, or families who refused vaccine administration might have contributed to the continuing pool of missed opportunities. At sick visits, additional education for providers and patients regarding precautions and true contraindications might ultimately be needed to improve adherence to immunization guidelines. The lack of information on why shots were not given at individual visits limits definitive interpretation of these results.
The provider-focused approach used in this study relies on patients' having access to and visiting a physician office as opposed to alternative patient-focused strategies to improve vaccination rates that actively encourage families to come for medical visits. On a population level, reminder/recall interventions including those with postcards, letters, and telephone or autodialer calls have been effective in improving rates between 5 and 20 percentage points in multiple practice settings.9,42 When combined with outreach, such systems have been able to reduce racial and ethnic disparities in immunization delay.43 Individually tailored calendars kept by families have also shown promise in improving immunization rates in the urban setting.44 Combining patient-focused reminder/recall interventions with provider-focused EHR-based alerts to reduce missed opportunities may ultimately prove more effective than either strategy alone in improving immunization rates.
To our knowledge, this trial represents the first use of EHR-based alerts for routine pediatric immunizations as a centerpiece of an in-office quality improvement initiative designed to improve immunization rates for routine pediatric vaccinations in a highly vulnerable population: urban children who are younger than 24 months. Once patients reached the office, this system greatly increased the likelihood that immunizations were delivered, and patients who were exposed to the intervention had significantly improved vaccination rates. Unlike reminder, recall, and outreach, which have been slow to be adopted in many settings,45 the success of the alert system over time does not require the ongoing investment of resources at the practice level and need only be adjusted for changes in the immunization schedule. As a result, improvements might be more easily sustained and more widely disseminated. More broadly, as occurred in this study, immunization alerts within EHRs might increasingly move routine pediatric immunization out of well-child care to the first visit of any kind when children are due. The system might also support the administration of vaccines to children by nurses through the use of standing orders. As a result, highly trained physicians and nurse practitioners might benefit from more time to manage chronic illness and address patients' specific concerns.
A Young Investigator's Grant from the Ambulatory Pediatric Association supported this work.
We thank Anthony Luberti, MD, Jonathan Crossette, MPH, Jodi Cohen, MD, Colette Desrochers, MD, Blaze Gusic, MD, Cheryl Hausman, MD, Jennifer Joslin, MD, Margaret Laigaie, RN, Dorothy Novick, MD, and Noel Rosales, MD, for helpful comments and technical insights during the course of this research. We extend particular thanks to the Primary Care Centers of CHOP for participation. In addition, we recognize C. Victor Spain, Liyuan Ma, and Barbara Watson, MD, for assistance in providing immunization rates for Philadelphia and Lelisha Rios for administrative support.
- Accepted April 26, 2007.
- Address correspondence to Alexander G. Fiks, MD, Pediatric Generalist Research Group, Children's Hospital of Philadelphia, 3535 Market St, Room 1546, Philadelphia, PA 19104. E-mail:
The authors have indicated they have no financial relationships relevant to this article to disclose.
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