Impacting Delayed Pediatric Influenza Vaccination A Randomized Controlled Trial of Text Message Reminders Annika M. Hofstetter, MD, PhD, MPH, Celibell Y. Vargas, MD, Stewin Camargo, MS, Stephen Holleran, BA, David K. Vawdrey, PhD, Elyse Olshen Kharbanda, MD, MPH, Melissa S. Stockwell, MD, MPH This activity is available for CME credit. See page A3 for information.

Background: Influenza vaccination coverage is low, especially among low-income populations. Most doses are generally administered early in the influenza season, yet sustained vaccination efforts are crucial for achieving optimal coverage. The impact of text message influenza vaccination reminders was recently demonstrated in a low-income population. Little is known about their effect on children with delayed influenza vaccination or the most effective message type.

Purpose: To determine the impact of educational plus interactive text message reminders on influenza vaccination of urban low-income children unvaccinated by late fall. Design: Randomized controlled trial. Setting/participants: Parents of 5,462 children aged 6 months–17 years from four academically affiliated pediatric clinics who were unvaccinated by mid-November 2011. Intervention: Eligible parents were stratified by their child’s age and pediatric clinic site and randomized using a 1:1:1 allocation to educational plus interactive text message reminders, educational-only text message reminders, or usual care. Using an immunization registry-linked text messaging system, parents of intervention children received up to seven weekly text message reminders. One of the messages sent to parents in the educational plus interactive text message arm allowed selection of more information about influenza and influenza vaccination.

Main outcome measures: Influenza vaccination by March 31, 2012. Data were collected and analyzed between 2012 and 2014. Results: Most children were publicly insured and Spanish speaking. Baseline demographics were similar between groups. More children of parents in the educational plus interactive text message arm were vaccinated (38.5%) versus those in the educational-only text message (35.3%; difference¼3.3%, 95% CI¼0.02%, 6.5%; relative risk ratio (RRR)¼1.09, 95% CI¼1.002, 1.19) and usual care (34.8%; difference¼3.8%, 95% CI¼0.6%, 7.0%; RRR¼1.11, 95% CI¼1.02-1.21) arms.

Conclusions: Text message reminders with embedded educational information and options for interactivity have a small positive effect on influenza vaccination of urban, low-income, minority children who remain unvaccinated by late fall. (Am J Prev Med 2015;48(4):392–401) & 2015 American Journal of Preventive Medicine

From the Departments of Pediatrics (Hofstetter, Vargas, Camargo, Holleran, Stockwell), Biomedical Informatics (Vawdrey), and Population and Family Health (Stockwell), Columbia University Medical Center; NewYork-Presbyterian Hospital (Hofstetter, Vawdrey, Stockwell), New York, New York; and HealthPartners Institute for Education and Research (Olshen Kharbanda), Minneapolis, Minnesota

392 Am J Prev Med 2015;48(4):392–401

Address correspondence to: Melissa S. Stockwell, MD, MPH, Departments of Pediatrics and Population and Family Health, Columbia University, 622 W. 168th Street, VC 417, New York NY 10032. E-mail: [email protected]. 0749-3797/$36.00 http://dx.doi.org/10.1016/j.amepre.2014.10.023

& 2015 American Journal of Preventive Medicine

 Published by Elsevier Inc.

Hofstetter et al / Am J Prev Med 2015;48(4):392–401

Introduction

I

nfluenza infection is associated with high morbidity and mortality, especially among high-risk groups such as infants, young children, and patients with chronic medical conditions.1 Influenza vaccination is an effective strategy for preventing infection,2 and this protection also may benefit others within the household and community.3–6 The Advisory Committee on Immunization Practices (ACIP)1 recommends influenza vaccination for all individuals aged Z6 months, ideally in the early fall before virus circulation, but continuing throughout the season. Despite these recommendations, influenza vaccination coverage remains low nationally. It is estimated that 51.5% of children aged 6 months–17 years were vaccinated during the 2011–2012 influenza season.7 Most vaccinated individuals receive their doses early in the season (i.e., by early November).8–13 However, in order to achieve the Healthy People 2020 goal of 70% influenza vaccination coverage for children aged 6 months–17 years14 and achieve herd immunity at the population level, it is necessary to develop interventions that are effective for individuals who delay or defer influenza vaccination. For these patients, strategies promoting more timely vaccination are critical for optimizing protection. This may be especially important for urban low-income minority populations, who are at high risk of influenza transmission and associated complications.15–18 Text message reminder/recall for influenza vaccination is a promising strategy for improving vaccination coverage, particularly in low-income minority populations for whom traditional reminder/recall approaches have been less effective.19–21 It was recently demonstrated that children and adolescents whose parents received a text message influenza vaccination reminder had greater coverage than those receiving usual care.22 It remains unclear if this strategy would impact influenza vaccination among harder-to-reach populations, including those still unvaccinated in late fall. Further questions regarding the use of text message–based influenza vaccination reminders remain. First, a recent survey23 found that 83% of parents were interested in interactivity with a text message reminder/recall system, enabling them to request additional information that could facilitate their decision-making process. However, the effect of such interactivity has yet to be studied. Second, text message influenza vaccination reminder/recall interventions may also benefit other household children who are not the target of the reminder/recall. Few, if any, studies have investigated this potential. This study’s primary aim was to assess the impact of text message reminders, particularly those with interactive capabilities, on influenza vaccination of children who April 2015

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are unvaccinated by late fall. Secondary aims were to examine the intervention effect on influenza vaccination timeliness and influenza vaccination of other household children.

Methods This RCT examined the impact of educational plus interactive text message reminders versus educational-only text message reminders versus usual care on influenza vaccination during the 2011–2012 season among urban, low-income, minority children who remained unvaccinated in the late fall. The study was approved by the Columbia University Medical Center IRB. The study was conducted in four community-based pediatric practices that are part of an ambulatory care network affiliated with a large academic medical center in New York City. These practices are staffed by one pediatric group practice using a common electronic health record (EHR). Patients at these sites are primarily Latino and publicly insured, and the majority are eligible to receive free vaccines through the Vaccines for Children (VFC) Program. During the 2011–2012 influenza season, three sites implemented walk-in hours for influenza vaccination, whereas the fourth site scheduled influenza vaccination–only appointments. Parents were eligible for participation if they had (1) a child aged 6 months–17 years with a visit to one of the study sites in the 12 months prior to September 1, 2011, and (2) a cell phone number listed in the child’s record in the hospital registration system. This system includes all patients who have visited the hospital or an affiliated clinic, including the four study sites, in their lifetime. There were no racial or gender biases in participant selection. When more than one child in the household (as determined by a matching telephone number in the registration system) fulfilled the age and visit criteria, only the youngest child was selected. The remaining children were included in the analytic sample used to examine the intervention effect on other children in the household.

Study Procedures Of the 13,210 parents with a child who fulfilled age and visit criteria, 8,620 remained eligible for participation (Figure 1). All of these parents were sent an initial text message allowing them to “stop” future health messages or switch the message language. Those with undeliverable messages (n¼477) or “stop” replies (n¼137) or who already had been vaccinated in the season (n¼2,544) were excluded from further study. The remaining parents (n¼5,462) were stratified by their child’s age (6–23 months, 24–59 months, and 5–17 years, based upon previously published age categories and age-based expansion of the ACIP recommendations7,24–26) and clinic site and randomized with 1:1:1 allocation to: (1) educational plus interactive text messages; (2) educational-only text messages; or (3) usual care arms using a random sample algorithm generator in SPSS, version 19.0. With this sample size (n=5,462), randomized with equal allocation, and an estimated baseline coverage of 51%,8 there was 80% power to detect a 5% difference in influenza vaccination coverage by March 31, 2012, for each pairwise comparison with α¼0.05 as well as adjusted for multiple comparisons (α¼0.02). The study analysts were blinded to the group assignments. All arms received usual

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Hofstetter et al / Am J Prev Med 2015;48(4):392–401 parents to bring “other children” in for influenza vaccination. All messages were sent in either English or Spanish based upon the parent’s primary language specified in the registration system; this information, along with other demographics, is routinely updated during visits to the hospital and affiliated clinics. The messages were discontinued once the child was vaccinated, as determined by weekly abstractions from the EzVac registry.

Outcome Measures

Figure 1. Study flow diagram. care, which included telephone appointment reminders and general information about influenza vaccination procedures provided in the clinic. Text messages were generated by a customized text messaging platform integrated with the hospital immunization registry, EzVac. EzVac contains active records for all children seen at the hospital’s affiliated clinics. An EzVac record is automatically started when a patient is registered for the first time in the hospital system. The EzVac registry then receives vaccine administration information directly from the network’s EHR, allowing automatic capture of all doses given at the study sites.27 It also synchronizes with the provider-mandated New York City Immunization Registry (CIR), which includes an estimated 93% of doses administered through the VFC Program.28 Thus, influenza vaccine doses given at participating sites and other sites in New York City during the 2011–2012 season should be included in the final study data (collected mid-April 2012 to capture any CIR doses with delayed reporting). Parents (i.e., not children or adolescents) in both text messaging arms were sent five weekly automated text message influenza vaccination reminders in November–December and two booster text messages in January. The messages were sent during the daytime on weekdays based upon practical considerations and parental preferences.23 These messages were o160 characters and included educational content, such as why influenza vaccination is needed, used in a previous study.22 For those in the educational plus interactive text message arm, one of these messages allowed parents to request additional information (Appendix Table 1). At the time of sending that message, those in the educational-only arm instead received a general reminder to bring their child to the clinic for a “flu shot.” In cases where there was more than one child in the household fulfilling the age and visit criteria, one was selected as outlined previously, but messages also encouraged

The primary pre-specified outcome measure of interest was influenza vaccination by March 31, 2012. Secondary outcomes included timeliness of influenza vaccination, missed opportunities for influenza vaccination, and influenza vaccination of other household children by March 31, 2012. Missed opportunities were defined as any clinic visit between the start of the intervention and March 31, 2012, where an unvaccinated child failed to receive influenza vaccine. For children requiring two doses in a given season, all analyses focused on their first dose only.

Statistical Analysis All analyses used the individual child as the unit of analysis. In the primary analysis, 158 children were excluded because they received influenza vaccine between randomization and the intervention start date (November 14, 2011) or had delayed reporting of vaccine received before the intervention start date. Influenza vaccine receipt was compared between the three arms using Pearson chisquared tests. A sensitivity analysis (i.e., intention-to-treat analysis) including randomized children who were vaccinated before the intervention start date was conducted. An additional analysis was performed excluding those with one or more undeliverable message. Analyses were corrected for multiple comparisons using po0.02 to indicate significance. Timeliness of influenza vaccination was first examined using Kaplan–Meier analysis.29 Individuals who remained unvaccinated were censored at March 31, 2012. Factors associated with time to vaccination were then identified using Cox proportional hazards models. An adjusted hazard ratio (aHR) o1 signified a lower likelihood of early vaccination. Additionally, visit type (e.g., preventive care, acute care, vaccination-only)—as determined by type of health care encounter note—at influenza vaccination or a missed vaccination opportunity was compared between groups. Influenza vaccination of other household children was also assessed by comparing coverage levels between arms using Pearson chi-squared test and describing concordance in influenza vaccination status between the www.ajpmonline.org

Hofstetter et al / Am J Prev Med 2015;48(4):392–401 “primary target” and other household children. All data were collected in 2012–2013. Analyses were performed in 2013–2014 using SAS, version 9.3.

Results Of the 5,462 children of parents who were randomized, 5,304 (97.1%) were included in the primary analyses, and 158 (2.9%) were excluded because they were vaccinated before intervention initiation (Figure 1). Groups varied by gender in the primary analytic sample; no other baseline demographic differences were observed (Table 1). The parents in the text messaging arms (n¼3,540) included 325 (9.2%) who had undeliverable messages, 71 (2.0%) who stopped further messages, and five (0.1%) who requested to switch the message language. There were no differences in child gender, age, or insurance as well as parent language between those with and without undeliverable messages or stop replies. Of parents in the educational plus interactive text message arm (n¼1,780), 17 (1.0%) replied to the interactive message. Parents most commonly requested more information about the “yearly shot” (n¼9, 52.9%), followed by the “child’s flu risk” (n¼5, 29.4%). The median number of text messages sent before influenza vaccination of a child in either text messaging arm was five (interquartile range¼2–7); there were no differences by text messaging arm or child age. More children of parents in the educational plus interactive text message arm underwent influenza vaccination by March 31, 2012 (38.5%) than those in the educational-only text message arm (35.3%; difference¼3.3%, 95% CI¼0.02%, 6.5%; relative risk ratio [RRR]¼1.09, 95% CI¼1.00, 1.19; p¼0.04) and usual care arm (34.8%; difference¼3.8%, 95% CI¼0.6%, 7.0%; RRR¼1.11, 95% CI¼1.02, 1.21; po0.02) (Table 2). No difference in influenza vaccination was noted between the educational-only and usual care arms (p¼0.74). After adjusting for gender, age, and clinic site, children of parents in the educational plus interactive text message arm remained more likely to be vaccinated by March 31, 2012, compared to those in the educational-only (adjusted RR [aRR]¼1.10, 95% CI¼1.01, 1.20) and usual care (aRR¼1.11, 95% CI¼1.02, 1.21) arms. In the multivariable models, there were no interactions between intervention and clinic site (p¼0.68) or intervention and age category (6–23 months, 24–59 months, or 5–17 years) (p¼0.17). Among all randomized subjects, influenza vaccination coverage by March 31, 2012, differed, although not significantly, between the text messaging arms (p¼0.12): 39.9% in the educational plus interactive text message arm versus 37.5% in the educational-only text April 2015

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message arm versus 36.8% in the usual care arm. However, 158 of these were previously vaccinated; thus, the 102 in the text messaging arms could not have been impacted by the intended intervention. In a sensitivity analysis excluding 325 children for whom one or more text message was undeliverable, influenza vaccination coverage by March 31, 2012, was not materially different from that in the primary analyses (39.0% in the educational plus interactive text message arm, 36.0% in the educational-only text message arm, and 34.8% in the usual care arm; po0.05). Timeliness of influenza vaccination differed by study arm, child age, and visit type (Figure 2). In a proportional hazards regression model including study arm, age, and gender, the educational-only text message and usual care arms were associated with a longer time to vaccination compared to the educational plus interactive text message arm (aHR¼0.90, 95% CI¼0.81, 1.00, and aHR¼0.88, 95% CI¼0.79, 0.98, respectively). Similarly, older children were less likely than those aged 6–23 months to undergo timely vaccination (24–59-montholds, aHR¼0.84, 95% CI¼0.74, 0.95; 5–17-year-olds, aHR¼0.60, 95% CI¼0.52, 0.68). Influenza vaccination also was less timely among those vaccinated at scheduled preventive care and acute care visits than at vaccinationonly visits after adjusting for study arm, age, and gender (aHR¼0.38, 95% CI¼0.32, 0.46, and aHR¼0.54, 95% CI¼0.43, 0.68, respectively). Among vaccinated children, most (77.6%) received a vaccine at a scheduled preventive care visit as opposed to acute care visit (11.5%) or vaccination-only visit (8.5%). The proportion of children vaccinated at a vaccinationonly visit differed by study arm (po0.01): educational plus interactive text message arm, 7.5%; educational-only text message arm, 11.5%; and usual care arm, 6.5%. It also differed by age (po0.01): 3.5% of 6–23-month-olds, 8.0% of 24–59-month-olds, and 10.6% of 5–17-year-olds. The proportion of 5–17-year-olds with vaccination-only visits varied non-significantly by study arm (p¼0.08): educational plus interactive text message arm, 9.9%; educational-only text message arm, 14.1%; and usual care arm, 7.8%. Some vaccinated children (n¼300) did not have a healthcare encounter note generated at the time of vaccination. Of these, 30.7% had a visit within 7 days of vaccination, likely returning for a vaccinationonly visit with a nurse (i.e., vaccine ordered by provider at earlier appointment). The remaining 69.3% were vaccinated either during a vaccination-only visit (vaccine ordered 47 days before vaccination) (most likely) or at an outside clinic in New York City (less likely). Of all vaccinated children, 13.9% had one or more missed vaccination opportunity before actual influenza vaccination.

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Table 1. Study Population Characteristics, % (n) Unless Otherwise Noted Total samplea

Characteristic Total (n)

Primary analytic samplea

Educational þ interactive text messages

Educational-only text messages

Usual care

1,821

1,821

1,820

Educational-only text messages

Usual care

1,780

1,760

1,764

0.07

0.04

Female

47.7 (869)

50.8 (926)

47.4 (862)

47.5 (845)

51.0 (897)

47.0 (829)

Male

52.3 (952)

49.2 (895)

52.6 (958)

52.5 (935)

49.0 (863)

53.0 (935)

Age

0.93

0.99

6–23 months

14.2 (258)

13.5 (246)

14.5 (263)

13.7 (244)

13.2 (232)

13.7 (242)

24–59 months

34.7 (631)

35.3 (643)

34.4 (626)

34.7 (618)

35.2 (619)

34.7 (612)

5–17 years

51.1 (932)

51.2 (932)

51.1 (931)

51.6 (918)

51.6 (909)

51.6 (910)

Language

0.81

0.69

Spanish

57.3 (1,043)

57.1 (1,039)

58.6 (1,067)

57.2 (1,018)

57.1 (1,005)

58.7 (1,035)

English

39.9 (726)

39.9 (727)

37.9 (690)

40.0 (712)

40.1 (706)

37.9 (668)

Other

0.8 (15)

1.0 (18)

1.1 (20)

0.8 (15)

0.8 (14)

1.1 (20)

Unknown

2.0 (37)

2.0 (37)

2.4 (43)

2.0 (35)

2.0 (35)

2.3 (41)

Insurance

0.16

Public

89.6 (1,632)

88.3 (1,607)

87.6 (1,594)

Private

5.6 (101)

6.3 (115)

5.8 (106)

Uninsured

4.8 (88)

5.4 (99)

6.6 (120)

p-value

0.15 89.6 (1,595)

88.1 (1,551)

87.4 (1,542)

5.5 (98)

6.4 (113)

6.0 (105)

4.9 (87)

5.5 (96)

6.6 (117)

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Note: Boldface indicates statistical significance (po0.05). a Total sample includes the 5,462 children who were randomized. The primary analytic sample (n¼5,304) excludes the 158 children who were randomized, but received influenza vaccine prior to the intervention start.

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Gender

p-value

Educational þ interactive text messages

April 2015

3.2% (–1.1%, 7.6%)

1.11 (0.97, 1.28)

Among unvaccinated children, 27.6% had one or more clinic visit between the intervention initiation and March 31, 2012, and, thus, one or more missed opportunity for influenza vaccination; one-third had more than one missed opportunity. Of these missed opportunities, the majority occurred at acute care visits (52.5%), followed by scheduled preventive care visits (38.8%); few occurred at vaccination-only visits (0.9%). The proportion of unvaccinated subjects with missed opportunities did not differ across groups (educational plus interactive text message arm, 27.5%; educational-only arm, 29.1%; usual care, 26.2%; p¼0.30). However, it did vary by age (po0.05): 6–23-month-olds, 25.4%; 24–59-month-olds, 30.3%; 5–17-year-olds, 26.5%. There were 1,193 other children in the study households who were unvaccinated at the start of the intervention (404 household children of parents in the educational plus interactive text message arm, 414 in educational-only text message arm, and 375 in usual care arm). As of March 31, 2012, influenza vaccination coverage of these household children did not differ significantly based upon the intervention arm of the parent (educational plus interactive text message arm, 36.1%; educational-only text message arm, 35.3%; usual care arm, 30.4%; p¼0.19), although it tended to be higher if the parent was in either text messaging arm versus usual care arm (35.7% vs 30.4%, p¼0.07). Concordance in influenza vaccination status by March 31, 2012, between the target child and other household children was high (80.0%), especially among household children with the parent in either text messaging arm compared to usual care arm (82.5% vs 74.4%, po0.01).

0.1% (–4.3%, 4.5%) 28.7 (261)

1.00 (0.88, 1.15)

1.14 (0.99, 1.30) 5.3% (–0.4%, 10.9%) 5.2% (–0.4%, 10.9%) 38.7 (237)

1.14 (0.99, 1.30)

1.04 (0.87, 1.25) 2.1% (–7.2%, 11.4%) 9.9% (0.6%, 19.2%) 47.5 (115)

1.25 (1.02, 1.53)

1.11 (1.02, 1.21) 3.8% (0.6%, 7.0%) 3.3% (0.02%, 6.5%) 34.8 (613)

1.09 (1.00, 1.19)

RRR (95% CI) Difference, % (95% CI) RRR (95% CI) Difference, % (95% CI) % (n)

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RRR, relative risk ratio; TMs, text message reminders.

31.8 (289) 31.9 (293) 5–17 years

38.8 (240) 44.0 (272) 24–59 months

39.7 (92) 49.6 (121) 6–23 months

35.3 (621) 38.5 (686) All ages

% (n)

% (n)

Discussion

Age

Educationalþinteractive versus educational-only TMs Usual care (n¼1,764) Educational-only TMs (n¼1,760) Educationalþ interactive TMs (n¼1,780)

Table 2. Influenza Vaccination Coverage by March 31, 2012 (primary analytic sample)

Educationalþinteractive TMs versus usual care

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This study demonstrated the positive impact of text messaging on children who remained unvaccinated by mid-November 2011, which is beyond the typical peak of influenza vaccine administrations.8 National data indicate that most vaccinations occur in the fall, as recommended.9–13 Thus, there may be opportunities to significantly improve vaccination coverage levels by identifying and contacting parents of those children not yet vaccinated by late fall. Text messaging may be a valuable tool for reaching this population. Moreover, these findings suggest that text message vaccination reminders targeting individuals may positively affect vaccination of other household members. Nonetheless, the fact remains that only approximately one third of all patients in this study were ultimately vaccinated, highlighting the need for additional interventions aimed at improving influenza vaccination of this high-risk population.

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Figure 2. Timeliness of influenza vaccination, 2011–2012 season Kaplan-Meier survival curves illustrating the cumulative proportion of children who received their first influenza vaccine dose of the 2011–2012 season between November 14, 2011 (day of intervention initiation), and March 31, 2012 (140 days after intervention initiation), as compared by (a) study arm (p¼0.06); (b) child age (po0.001); and (c) visit type at vaccine administration (among vaccinated children only) (po0.001). TM, text message reminders.

This study found that educational plus interactive text message reminders increased influenza vaccination, whereas educational-only text message reminders had no effect on uptake in this population of high-risk children who remained unvaccinated by mid-November. These findings indicate that there may be particular benefit to having an educational message with an interactive option, as the one interactive message was the only difference between the two text messaging arms. Although very few parents (1%) elected to use this modality, interactive choices were crafted to provide an educational overview (i.e., “shot can’t cause flu,” “flu not just bad cold,” “yearly shot”). Thus, parents simply reading these options would have received additional important information about influenza vaccination, including reinforcement of its importance. Moreover, it is possible that the process of deciding whether or not to interact with the system engaged them actively rather than passively, resulting in greater attention being placed on the education-embedded

choices. A previous study found that interrogative, rather than declarative, questioning about a future action may spur behavioral changes.30 Although that study focused on intentions, the principles may also apply here. “Introspective self-talk” may result from reading the interactive options in the text message and lead to “adoption of behavior” (i.e., influenza vaccination). In support of this, another study demonstrated that healthcare workers who completed a questionnaire about influenza vaccination were more likely to be vaccinated.31 Furthermore, because lower levels of activation in one’s health and health care may exist among minorities and those of low SES,32,33 interventions that better prepare and empower these families may result in greater communication and action in the primary care setting.34 Further investigation of exactly how interactive text messages increase influenza vaccination, including whether they engage and activate recipients in a different manner than those receiving information in a non-interactive form, is needed. The fact www.ajpmonline.org

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that the educational-only text message reminders failed to demonstrate a beneficial effect on coverage levels, which has been shown in the general pediatric population in these practices,22 may indicate that high-risk families who are not vaccinated early in the season as recommended may require more or different information or alternative delivery methods of that information to make a vaccination decision. Enhanced understanding of these informational needs and optimal delivery methods is critical for designing effective interventions targeting this population. In this study, the majority of vaccinated patients received their doses at scheduled visits in the mid-tolate influenza season, in accordance with ACIP recommendations to vaccinate throughout the season.1 The finding that those in the educational plus interactive text message arm received their influenza vaccine dose earlier could be explained by the fact that more of these patients, especially older ones, ultimately received their doses at vaccination-only visits. Indeed, among vaccinated subjects, those with vaccination-only visits were more likely to be vaccinated earlier. Text messages represent “cues to action”; thus, they may be particularly effective when individuals are able to act on them immediately (i.e., go directly to the clinic for vaccination) rather than face routine delays in scheduling preventive care visits. These findings demonstrate the potential of text message reminders to impact timely influenza vaccination of high-risk populations, especially when vaccination-only visits are available in the practice and among older children. Reminders were less effective among children aged 6–23 months who had higher coverage and more timely uptake overall, possibly because of their more frequent preventive care visits and greater provider emphasis on vaccinating these younger patients. Nonetheless, it is important to mention that certain younger children aged 6 months–8 years require two doses in a season; thus, promoting timely vaccination of these patients is critical for optimizing protection.8,35 Many individuals with clinic visits remained unvaccinated by the end of the season. Thus, strategies also should be employed to reduce such missed vaccination opportunities, especially at acute care visits (i.e., most common visit type for missed opportunities) when appropriate and among children aged 24–59 months (i.e., most common age group for missed opportunities). Clinician decision support in the EHR, particularly when integrated with an immunization registry, is one promising approach. These registry-linked electronic reminders could alert the provider when influenza vaccination is due and offer educational talking points for them to use,36,37 potentially closing information gaps that may lead to such missed opportunities. April 2015

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There was strong concordance in influenza vaccination status between the “primary target” child and other children in the household. Although the study detected no significant impact of text message reminders on influenza vaccination of other household members, there was a tendency toward greater coverage among household children of parents in the text messaging arms, indicating that a “spillover effect” may be apparent. One of the biggest benefits of text message vaccination reminder/ recall, particularly when linked with EHRs and immunization registries, is the potential to quickly identify and reach a large target population, during an influenza epidemic, for example. The spread of the intervention to individuals not specifically targeted could enhance considerably the overall impact at the population level. This spillover effect warrants further study and almost certainly has important public health implications. Other studies have demonstrated that enhancing vaccination coverage of children has the potential to benefit others within the household and community.3–6,38 The study had several limitations. First, it included only families with a cell phone number in the registration system. These families may differ from those without a cell phone number,39–42 although recent studies found that the vast majority of Americans have cell phones43 and 89% of parents in these practices have text message– enabled phones.23 Second, some parents who received the messages may have been unable to read them owing to low literacy levels, although all messages were no more than a fourth-grade reading level, per the Flesch–Kincaid readability test. Third, the use of telephone numbers to identify other household children could have resulted in misclassification of some subjects, although telephone numbers may be more stable contact information than home addresses44 and thus a more accurate way to identify these children with the available data. Fourth, under-reporting of influenza vaccination may have occurred, although is unlikely given the automated data extractions from the EHR and mandated reporting for those aged r18 years to the city immunization registry. However, delayed entry of some vaccine administrations did occur, with the result that some subjects were randomized after influenza vaccination and thus removed from the primary analytic sample. Fifth, this study was unable to assess reasons for missed vaccination opportunities with the available data, including possible contraindications to vaccination, particularly during acute care visits, or parental refusals. Missed opportunities also may vary by provider type; this was not assessed here because nearly all providers in this study were pediatricians. Future studies should explore these reasons for missed opportunities further. Moreover, for a small number of patients, the type of visit during which vaccine was administered was not available

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(i.e., no healthcare encounter note was generated); the majority of these were likely vaccination-only visits. Finally, the conduct of the study in one ambulatory care network in an urban low-income community may have affected its generalizability. Thus, this work should be replicated in other populations, practices, and communities. In conclusion, this study found that text message reminders with embedded educational information and options for interactivity had a small positive impact on influenza vaccination of high-risk children who remained unvaccinated in the late fall. It also illustrates other potential benefits of text message reminders that require further investigation (i.e., their impact on influenza vaccination timeliness and influenza vaccination coverage of other household members) and the need to reduce missed vaccination opportunities. We would like to thank the EzVac immunization registry team and the Ambulatory Care Network of New York-Presbyterian Hospital. We would also like to thank Sekhar Ramakrishnan for his statistical assistance. This study was supported by Grant No. R40MC17169 from the Maternal and Child Health Bureau (Title V, Social Security Act), Health Resources and Services Administration, USDHHS. Dr. Hofstetter receives research support for unrelated investigator-initiated studies from Merck Sharp & Dohme Corp and the Pfizer Medical Education Group. Dr. Stockwell is an unfunded co-investigator on the latter grant. The other authors have no financial disclosures to report. Trial Registration Name: TextFluenza: Using Technology To Promote Flu Vaccination In Underserved Maternal And Child Populations. Trial Registration Number: NCT01146912. Date of Registration: June 16, 2010.

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Appendix Supplementary data Supplementary data associated with this article can be found at http://dx.doi.org/10.1016/j.amepre.2014.10.023.