Vaccine 33 (2015) 1748–1755
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Vaccine journal homepage: www.elsevier.com/locate/vaccine
Vaccine hesitancy among parents of adolescents and its association with vaccine uptake James R. Roberts a,∗ , David Thompson b , Brianna Rogacki b , Jessica J. Hale b , Robert M. Jacobson c , Douglas J. Opel d , Paul M. Darden b a
Medical University of South Carolina, Department of Pediatrics, 135 Rutledge Ave, MSC 561, Charleston, SC 29425, USA University of Oklahoma Health Sciences Center, Department of Pediatrics, Section of General and Community Pediatrics, 1200 Children’s Avenue, OUCPB Suite 12400, Oklahoma City, OK 73104, USA c Department of Pediatric and Adolescent Medicine, Mayo Clinic, Desk Ba3b, 200 First St SW, Rochester, MN 55905-0001, USA d Seattle Children’s Research Institute, JMB—6 Clinical and Translational Research, 1900 9th Ave, Seattle, WA 98101, USA b
a r t i c l e
i n f o
Article history: Received 4 September 2014 Received in revised form 21 January 2015 Accepted 27 January 2015 Available online 7 February 2015 Keywords: Vaccine Immunization Adolescent Hesitancy Parent
a b s t r a c t Background: Addressing parental vaccine hesitancy may increase adolescent vaccination acceptance. However, no validated measure exists to identify parents hesitant toward adolescent vaccines. Objective: To determine if a modified version of the Parent Attitudes about Childhood Vaccines (PACV) survey, a previously validated tool to identify parental hesitancy toward vaccines in infants, predicts adolescent vaccine uptake at office visits. Methods: We modified the PACV for use in the adolescent setting and distributed it to a convenience sample of parents of adolescents aged 11 to 17 presenting for care at a diverse group of six pediatric practices in Oklahoma and South Carolina. We determined the vaccination status of the parents’ adolescents for 3 vaccines (Tetanus–diphtheria–acellular pertussis [Tdap], meningococcal conjugate [MCV4], and human papillomavirus [HPV] vaccines). We used Fisher’s exact tests to compare vaccination status with each survey item and with an overall general hesitancy scale that we constructed. Results: We analyzed 363 surveys. At the time of the visit, vaccination coverage was 84% for Tdap, 73% for MCV, and 45% for any dose of HPV. Thirty-nine percent of parents expressed concern about vaccine efficacy and 41% expressed concern about side effects. Forty-five percent of parents disagreed with the statement that “teens can get all of the vaccines that are due at a single visit.” Two individual items were associated with not receiving a dose of HPV vaccine that was due. The overall modified PACV score failed to predict adolescent vaccine uptake at an office visit. Conclusion: Several individual items were associated with vaccine uptake. The cumulative modified PACV, a general measure of vaccine hesitancy, was not associated with vaccination status despite illuminating parental hesitancy. We need to better understand vaccine-specific concerns for the adolescent population. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction The Advisory Committee on Immunization Practices (ACIP) recommends that all adolescents between the ages of 11 and 18 years of age receive 2 doses of meningococcal conjugate (MCV4) vaccine, 1 dose of the adult/adolescent formulation of tetanus–diphtheria–acellular pertussis (Tdap), 3 doses of human papillomavirus (HPV) vaccine, a yearly dose of influenza vaccine, any needed catchup vaccines, and those vaccines indicated for
∗ Corresponding author. Tel.: +1 843 876 8512. E-mail address: [email protected] (J.R. Roberts). http://dx.doi.org/10.1016/j.vaccine.2015.01.068 0264-410X/© 2015 Elsevier Ltd. All rights reserved.
adolescents with high-risk conditions [1–3]. According to the National Immunization Survey-Teen (NIS-Teen), the vaccination coverage of 13–17 year olds increased from 2011 to 2013 for both MCV4 and Tdap. Between 2012 and 2013, 74.0–77.8% of teens received MCV4 and 84.6–86.0% received Tdap [4,5]. For the threedose HPV vaccine series, the rates did not improve from 2011 to 2012 with only 33.4% of females receiving all three doses of HPV in 2012 [4], but slightly increased for 2013 to 37.6% [5]. Vaccination rates for Tdap exceed the Healthy People 2020 goal, but the MCV4 and HPV vaccine coverage rates remained below their goals. Barriers to adolescent vaccination include the lack of central registries that permit clinicians to track individual patients, fewer visits to health care providers, limited and often incorrect parental
J.R. Roberts et al. / Vaccine 33 (2015) 1748–1755
and adolescent knowledge and understanding about vaccines and vaccine safety, and missed opportunities at well or sick visits and parental attitudes [6–13]. Our recent study of NIS-Teen data reveals other barriers to vaccination, some of which are HPV vaccine specific. Notably, among parents not intending to vaccinate with HPV in the next year, the percentage of parents citing safety concerns/side effects with respect to HPV increased from 4.5% in 2008 to 16.4% in 2010, while safety concern/side effects for MCV and Tdap never reached 1%. Parents also reported additional reasons for not giving the HPV vaccine including their teen being “not sexually active” and “not an appropriate age” [14]. Clinician recommendation increases immunization delivery across ages and vaccines. Parents who are generally hesitant about vaccines may be positively influenced by a recommendation from their children’s clinicians to accept immunizations [15,16]. We were interested in evaluating an instrument to measure parental hesitancy regarding adolescent vaccine delivery. In the absence of an adolescent- specific scale, we selected the Parent Attitudes about Childhood Vaccines Survey (PACV) by Opel et al. In evaluations of the PACV, Opel et al. have demonstrated both construct and predictive validity by associating parental PACV scores with immunization status at 19 months of age [17,18]. This study’s purpose is to determine if a modified version of the PACV for use in parents of adolescents aged 11–17 years predicts adolescent vaccine uptake. 2. Methods 2.1. Survey development The initial tested PACV contained 18 items, but this was reduced to 15 items after evaluating its validity [18]. Since we were modifying the PACV for use with a different population, we decided to begin with all 18 original PACV items. The items were modified to reflect our target population of parents of adolescents by substituting the word “teen” for the word “child” and by modifying the language to be read directly by either the parent or the teen. We piloted the English language questions for clarity with five parents of adolescents each in South Carolina and Oklahoma using in-person cognitive interviews. We revised the wording of some questions based on their feedback. Specific changes included replacing the word “shot” with “vaccine” to clarify the type of shots we were referring to. We reworded the PACV question “I trust the information I receive about shots” to read “I trust the information I receive from my teen’s doctor about vaccines.” Lastly, we included several socio-demographic items, such as the relationship of the accompanying adult to the adolescent as well as the age, race/ethnicity, marital status and educational level of the accompanying adult. When the English language survey was finalized, we used an IRB-approved Spanish language translation service to translate the survey into Spanish. We piloted the Spanish language survey with 5 parents using in-person cognitive interviews and made minor modifications for clarity to the items. 2.2. Setting/sample This study took place in three practices in each of two pediatric practice research networks—the Oklahoma Child Health Research Network (OCHRN) and the South Carolina Pediatric Practice Research Network (SCPPRN). The OCHRN practices included a community-based practice serving a predominantly Hispanic population, a primary care clinic staffed by pediatric faculty, and a resident continuity clinic. The SCPPRN practices included a resident continuity clinic, a private practice serving predominantly white and privately insured families, and a rural health clinic.
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We selected practices within each pediatric research network that ensured broad demographic representation and that had consistent vaccine delivery characteristics. In particular, all 6 practices routinely assessed immunization status and administered vaccines at all visits, including sick visits. In addition, all 6 participating practices routinely recommend receipt of the HPV vaccine beginning at age 11 for both males and females. To maintain consistency in the implementation of the study, the research staff developed a protocol that all practices followed. This document described the recruitment and survey distribution strategies, determined which variables would be collected from each source, and ensured that the data were collected systematically and uniformly. 2.3. Recruitment/survey distribution From October 2011 to March 2012, we collected survey data using the modified PACV in a convenience sample of parents or other adults accompanying adolescents 11 to 17 years of age who came to a participating practice for any visit type. We collected a minimum of 60 surveys in each of 6 practices. We obtained verbal parental permission and adolescent assent at the time of intake or triage. In the event that the parent brought two adolescents on the same day, research staff asked the parent to take the survey with the younger patient in mind, as this one was more likely to require vaccines at this visit. Surveys were distributed on each day of the week to the parent and adolescent while they were in the waiting room or exam room before the physician entered the room. All parents completed the survey before the physician entered the room. 2.4. Medical record review and vaccination status Research staff reviewed adolescents’ medical records to determine their vaccination status, age, and gender. Trained study personnel reviewed medical records using a standardized data collection sheet. The research assistants recorded the date each vaccine was received and indicated whether the adolescent was due or not due for vaccines at the completion of the visit. To assess the study’s primary outcome, we determined whether each adolescent remained due or not due for Tdap, MCV4 or HPV vaccines after the visit was completed. Thus for Tdap, participants were considered “not due” if they received Tdap at the study encounter or had received one or more doses of Tdap vaccine since age 10 years. For the MCV4 vaccine, participants between 11 and 15 years were “not due” if they received MCV4 during the study encounter or had ever received at least one dose of MCV4. Those who were 16 and 17 years of age were considered “not due” if they received MCV4 at the visit or had ever received an MCV4 dose on or after their 16th birthday. For the HPV vaccine, the ACIP recommendation for adolescents is to complete the 3 dose series by the time they are 13 years old using intervals of 1–2 months for dose 2 after dose 1, and 6 months for dose 3 after dose 1 [3]. Therefore, participants were considered “not due” if, at the conclusion of the visit, they had either: (1) received three doses of HPV vaccine, (2) received two doses of HPV vaccine and it was less than 6 months from the first dose or less than 3 months from the 2nd dose of HPV vaccine, or (3) received one dose of HPV vaccine less than two months from the visit. Otherwise the adolescent was considered due for HPV vaccine. Thus a study encounter in which an adolescent was due for a vaccine at the end of the visit represented an adolescent who not fully up to date on vaccines. Survey data were entered into a designed QualtricsTM (Provo, UT) database by trained data entry personnel. Quality of data entry was confirmed with 10% duplicated data entry. This database was moved to SAS 9.3 for analysis.
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2.5. Data analysis We used descriptive statistics to summarize participant sociodemographics and vaccination status. We calculated frequency distributions of all survey items. Four of the 18 items requested responses in a “yes”/“no”/“I don’t know” format. Twelve other items requested responses on a 5-point Likert-type scale and two items involved an 11-point (0–10) scale. To understand patterns of association and independence among survey items, we recoded some items so that high scores consistently denoted hesitancy and low scores denoted non-hesitancy for all items. After this reordering, we used SAS PROC FACTOR to perform an exploratory factor analysis, employing a principal components strategy to extract underlying factors or constructs connected with vaccine hesitancy. We also established a cumulative vaccine hesitancy scale in a manner similar to Opel et al. [17,18]. Opel et al. created the cumulative hesitancy score by using raw item scores, summing all raw item scores to obtain a total raw score, and then converting the total raw score to a 0–100 scale. To create our scale, we rescored each item’s values so they ranged from 0 to 10 (“three level” items were scored 0, 5, and 10; “five level” items were scored 2, 4, 6, 8, and 10) where higher scores signified greater hesitancy. We summed the itemspecific scores and then rescaled the sum so that the maximum possible cumulative hesitancy score was 100. We examined associations between vaccination status [due vs. not due] and individual PACV items after establishing categories for some items based on the raw response’s empirical distributions.
We collapsed the items with 5-point Likert-type response categories into 3 groups with the two affirmative responses grouped together, the middle response maintained separately, and the two negative responses grouped together. The two questions that used an 11-point scale (0–10) were grouped as in Opel et al.’s study with categories of 0–5, 6–7, and 8–10 [17,18]. We summarized vaccination status by research network site. We compared the hesitancy score for the modified PACV (using both the original 18-item PACV scale and the revised version consisting of the 15 items retained by Opel et al.) between those who were due and those who were not due for each of the 3 vaccines using permutation tests on cumulative scores using SAS PROC NPAR1WAY. We used Fisher’s exact tests to determine whether responses to individual hesitancy questions were associated with whether adolescents were due for vaccination. The Institutional Review Boards for Human Research at the Medical University of South Carolina and the University of Oklahoma Health Sciences Center both reviewed and approved the study protocol. 3. Results A total of 363 parent surveys were collected. Approximately 91.5% of the 363 adults who accompanied adolescents to the clinic were parents. The remainder included grandparents and legal guardians. As shown in Table 1, our sample consisted of a broad distribution of race/ethnicity and age as well as more males than females. The percentage of adolescents who were due for HPV at
Table 1 Demographic characteristics of adolescents and their parents or other accompanying adults. Characteristic
Age of adolescentˆ 11 12 13 14 15 16 17
Total sample (N = 363)
Oklahoma (N = 182)
N
N
%
South Carolina (N = 181) %
N
%
86 68 60 42 45 40 22
23.7 18.7 16.5 11.6 12.4 11.0 6.1
51 31 26 23 23 17 11
28.0 17.0 14.3 12.6 12.6 9.3 6.0
35 37 34 19 22 23 11
19.3 20.4 18.8 10.5 12.2 12.7 6.1
Gender of adolescent F M
160 203
44.1 55.9
91 91
50.0 50.0
69 112
38.1 61.9
Relationship of adult to adolescent# Mother Father Grandparent Guardian Other relative Other Missing
295 29 12 10 5 3 9
83.3 8.2 3.4 2.8 1.4 0.9
146 12 6 5 3 2 8
83.9 6.9 3.5 2.9 1.7 1.2
149 17 6 5 2 1 1
82.8 9.4 3.3 2.8 1.1 0.6
Accompanying adult’s age# 21–30 31–40 41–50 51–60 61–70 71—99 Missing
23 159 122 31 10 2 16
6.6 45.8 35.2 8.9 2.9 0.5
15 102 43 12 7 0 3
8.4 57.0 24.0 6.7 3.9 0.0
8 57 79 19 3 2 13
4.8 33.9 47.0 11.3 1.8 1.2
Race/ethnicity of accompanying adult# American Indian/Alaska Native Asian Black Native Hawaiian or other Pacific Islander White Hispanic Multi-Racial Missing
3 1 130 0 130 85 7 7
0.8 0.3 36.5 0.0 36.5 23.9 2.0
3 1 39 0 48 82 7 2
1.7 0.6 21.7 0.0 26.7 45.6 3.9
0 0 91 0 82 3 0 5
0.0 0.0 51.7 0.0 46.6 1.7 0.0
J.R. Roberts et al. / Vaccine 33 (2015) 1748–1755
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Table 1 (Continued) Characteristic
Accompanying adult’s marital status# Single Dual parent Missing
Total sample (N = 363)
Oklahoma (N = 182)
N
%
N
163 192 8
45.9 54.1
86 95 1
47.5 52.5
77 97 7
44.3 55.7
70 97 92 98 6
19.6 27.2 25.8 27.5
55 54 44 26 3
30.7 30.2 24.6 14.5
15 43 48 72 3
8.4 24.2 27.0 40.4
Accompanying adult’s education# Less than high school High school graduate Some college College graduate or beyond Missing ˆ
South Carolina (N = 181) %
N
%
This variable is from the vaccine information form. # Variable is from the Parent Survey. These tables are based on the PARENT survey responders—363.
Table 2 Percentage of teens in the practices of each research network site who were not due by vaccine (Tdap, MCV, and HPV). Site
All sites Oklahoma South Carolina
Not due named vaccine at conclusion of visit Tdap/Td (%)
MCV (%)
HPV (%)
84.0 83.5 84.5
72.7 72.0 73.5
44.9 52.2 37.6
N = 363.
the end of the encounter was considerably higher compared to the other vaccines (Table 2). Factor analysis identified two underlying constructs that accounted for 83% of the variability in responses among the survey’s 18 items. Table 3 shows that 11 of the survey’s 18 items loaded positively on a single construct that we identified to be “safety and concerns.” A second underlying factor was linked to a positive loading from one additional item, and to negative loadings with two of the 11 items we associated with the first factor. Responses to these two items, correlated with one another (r = 0.63). Table 4 reports the parents’ (or other accompanying adults’) responses to each of the 18 hesitancy questions and how they were associated with adolescents’ vaccination status. Parents’ responses to a number of survey items expressed considerable hesitancy. Overall, 39% of adults expressed concern about preventing disease and 41% expressed concern about serious side effects. Forty-six percent of adults disagreed with the statement that “teens can get all of
the vaccines that are due at a single visit.” Nearly all adults agreed with the statement that “It is my role as a parent to question vaccines.” Of note, 25% responded “unsure” when asked “Overall, how unsure about vaccines for teens would you consider yourself to be?” While these responses document vaccine hesitance among parents of adolescents, we found no association between cumulative hesitancy score for parents and adolescent’s vaccination status for Tdap (P = 0.59, 0.46 (15-item and 18-item scales, respectively), MCV (P = 0.84, 0.75) or HPV (P = 0.92, 0.69). However, several individual survey items discriminated between those who were due or not due for specific vaccines (Table 4). More parents who had adolescents who were “due” for HPV answered “yes” (hesitant response) to “Have you ever delayed a vaccine for reasons other than illness or allergy” compared to those who were “not due”, (8.7% vs. 5.0%, P = 0.048). Parents whose adolescents were due for HPV more often disagreed with the statement “I am able to openly discuss concerns about vaccines with my teen’s doctor” compared to those who were “not due”, (6.0% vs. 1.2%, P = 0.046). Two additional items were associated with vaccination status, but not in the hypothesized direction (Table 4). Parents whose adolescents were due for Tdap and MCV expressed hesitancy less often by stating they were “concerned that a vaccine might not prevent the disease” than did parents of adolescents who were not due for those vaccines. Parents whose adolescents were due for Tdap expressed hesitancy less often by disagreeing with the statement “it is better for my teen to develop immunity by getting sick than by getting a vaccine” than did parents of adolescents who were not due.
Table 3 Results of exploratory factor analysis: factor loadings (≥0.350) for accompanying adult’s survey responses. Survey item Have you ever DELAYED a vaccine for this teen for reasons other than illness or allergy? Have you ever SKIPPED a vaccine for this teen for reasons other than illness or allergy? How sure are you that following the doctor’s recommended shot schedule is a good idea for your teen? It is my role as a parent to question vaccines Teens get more vaccines than are good for them I believe that many of the illnesses that vaccines prevent are severe It is better for my teenager to develop immunity (protection from disease) by getting sick than by getting a vaccine Are you concerned that a vaccine might not prevent the disease? I trust the information I receive from my teen’s doctor about vaccines Are you concerned that your teen might have a serious side effect from a vaccine? I think teens can get all of the vaccines that are due at a single visit Are you concerned that one of the vaccines for teens might not be safe? Do you know of anyone who has had a bad reaction to a vaccine? The ONLY reason I have my teenager get vaccines is so they can attend school If you had another teen today, would you want that teen to get all the vaccines that the doctor recommends? Overall, how unsure about vaccines for teens would you consider yourself to be? I am able to openly discuss my concerns about vaccines with my teen’s doctor All things considered, how much do you trust your teen’s doctor? 1
Factor 1 safety and concerns1
Factor 22
0.551 0.374 0.415 0.360 0.576 0.608 0.608
−0.435
0.637
−0.386
0.383 0.492 0.489 0.593
Factor 1 accounted for 64.5% of the variability in responses among the survey’s 18 items. 2 Factors 1 and 2 together account for 83.3% of the variability.
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Table 4 Parent or other accompanying adult’s survey responses and their association with vaccinations due at the encounter. Tdap/Td
All N Parent question
%
Response1
N
%
N
Not due
%
P
MCV
P N
%
N
Not due
Due
%
N
Due
P
HPV %
N
Not due
% Due
Yes No I don’t know
25 318 12
7.0 89.6 3.4
23 265 10
7.7 88.9 3.4
2 53 2
3.5 93.0 3.5
0.5
19 233 8
7.3 89.6 3.1
6 85 4
6.3 89.5 4.2
0.8
8 142 9
5.0 89.3 5.7
17 176 3
8.7 89.8 1.5
0.05
Have you ever SKIPPED a vaccine for this teen for reasons other than illness or allergy?
Yes No I don’t know
19 333 9
5.3 92.2 2.5
15 281 8
4.9 92.4 2.6
4 52 1
7.0 91.2 1.8
0.8
11 245 8
4.2 92.8 3
8 88 1
8.2 90.7 1.0
0.2
8 152 3
4.9 93.3 1.8
11 181 6
5.6 91.4 3.0
0.7
How sure are you that following the doctor’s recommended shot schedule is a good idea for your teen?
0–5 6–7 8–10
29 27 274
8.8 8.2 83.0
22 23 237
7.8 8.2 84
7 4 37
14.6 8.3 77.1
0.3
20 19 205
8.2 7.8 84
9 8 69
10.5 9.3 80.2
0.7
12 12 126
8.0 8.0 84.0
17 15 148
9.4 8.3 82.2
0.9
It is my role as a parent to question vaccines
Agree Disagree Not sure
336 11 8
94.6 3.1 2.3
283 9 6
95 3 2
53 2 2
93.0 3.5 3.5
0.8
245 9 6
94.2 3.5 2.3
91 2 2
95.8 2.1 2.1
0.8
149 7 3
93.7 4.4 1.9
187 4 5
95.4 2.0 2.6
0.4
Teens get more vaccines than are good for them
Agree Disagree Not sure
92 151 115
25.7 42.2 32.1
77 131 92
25.7 43.7 30.7
15 20 23
25.9 34.5 39.7
0.3
68 114 78
26.2 43.8 30
24 37 37
24.5 37.8 37.8
0.4
49 69 43
30.4 42.9 26.7
43 82 72
21.8 41.6 36.5
0.07
I believe that many of the illnesses that vaccines prevent are severe
Agree Disagree Not sure
292 21 47
81.1 5.8 13.1
241 19 42
79.8 6.3 13.9
51 2 5
87.9 3.4 8.6
0.4
207 18 37
79 6.9 14.1
85 3 10
86.7 3.1 10.2
0.2
129 13 18
80.6 8.1 11.3
163 8 29
81.5 4.0 14.5
0.2
It is better for my teenager to develop immunity (protection from disease) by getting sick than by getting a vaccine
Agree Disagree Not sure
58 246 51
16.3 69.3 14.4
50 212 37
16.7 70.9 12.4
8 34 14
14.3 60.7 25.0
0.05
44 177 38
17 68.3 14.7
14 69 13
14.6 71.9 13.5
0.8
32 103 26
19.9 64.0 16.1
26 143 25
13.4 73.7 12.9
0.1
Are you concerned that a vaccine might not prevent the disease?
Not concerned Concerned Not sure
179 141 38
50.0 39.4 10.6
150 126 26
49.7 41.7 8.6
29 15 12
51.8 26.8 21.4
0.007 132 110 21
50.2 41.8 8
47 31 17
49.5 32.6 17.9
0.02
80 64 16
50.0 40.0 10.0
99 77 22
50.0 38.9 11.1
0.9
I trust the information I receive from my teen’s doctor about vaccines
Agree Disagree Not sure
332 16 10
92.7 4.5 2.8
279 13 8
93 4.3 2.7
53 3 2
91.4 5.2 3.4
0.9
240 14 6
92.3 5.4 2.3
92 2 4
93.9 2.0 4.1
0.3
143 8 7
90.5 5.1 4.4
189 8 3
94.5 4.0 1.5
0.2
Are you concerned that your teen might have a serious side effect from a vaccine?
Not concerned Concerned Not sure
182 148 29
50.7 41.2 8.1
150 126 26
49.7 41.7 8.6
32 22 3
56.1 387.6 5.3
0.6
133 107 22
50.8 40.8 8.4
49 41 7
50.5 42.3 7.2
0.9
82 62 16
51.3 38.8 10.0
100 86 13
50.3 43.2 6.5
0.4
I think teens can get all of the vaccines that are due at a single visit
Agree Disagree Not sure
86 163 110
24.0 45.4 30.6
73 140 88
24.3 46.5 29.2
13 23 22
22.4 39.7 37.9
0.4
64 123 74
24.5 47.1 28.4
22 40 36
22.4 40.8 36.7
0.3
37 69 54
23.1 43.1 33.8
49 94 56
24.6 47.2 28.1
0.5
Are you concerned that one of the vaccines for teens might not be safe?
Not concerned Concerned Not sure
153 152 52
42.9 42.6 14.6
131 125 46
43.4 41.4 15.2
22 27 6
40.0 49.1 10.9
0.5
116 105 40
44.4 40.2 15.3
37 47 12
38.5 49.0 12.5
0.3
73 65 23
45.3 40.4 14.3
80 87 29
40.8 44.4 14.8
0.7
Do you know of anyone who has had a bad reaction to a vaccine?
Yes No I don’t know
48 292 20
13.3 81.1 5.6
35 250 17
11.6 82.8 5.6
13 42 3
22.4 72.4 5.2
0.09
33 218 11
12.6 83.2 4.2
15 74 9
15.3 75.5 9.2
0.1
18 135 8
11.2 83.9 5.0
30 157 12
15.1 78.9 6.0
0.5
J.R. Roberts et al. / Vaccine 33 (2015) 1748–1755
Have you ever DELAYED a vaccine for this teen for reasons other than illness or allergy?
Agree Disagree I don’t know
47 310 4
13.0 85.9 1.1
37 262 4
12.2 86.5 1.3
10 48 0
17.2 82.8 0
0.4
33 226 4
12.5 85.9 1.5
14 84 0
14.3 85.7 0
0.4
21 137 4
13.0 84.6 2.5
26 173 0
13.1 86.9 0
0.08
If you had another teen today, would you want that teen to get all the vaccines that the doctor recommends?
Yes No I don’t know
319 13 28
88.6 3.6 7.8
272 9 21
90.1 3 7
47 4 7
81.0 6.9 12.1
0.1
237 8 17
90.5 3.1 6.5
82 5 11
83.7 5.1 11.2
0.2
144 5 11
90.0 3.1 6.9
175 8 17
87.5 4.0 8.5
0.8
Overall, how unsure about vaccines for teens would you consider yourself to be?
Sure Unsure Don’t know
232 88 33
65.7 24.9 9.3
195 73 28
65.9 24.7 9.5
37 15 5
64.9 26.3 8.8
0.9
166 63 28
64.6 24.5 10.9
66 25 5
68.8 26.0 5.2
0.3
103 38 16
65.6 24.2 10.2
129 50 17
65.8 25.5 8.7
0.9
I am able to openly discuss my concerns about vaccines with my teen’s doctor
Agree Disagree Not sure
344 14 4
95.0 3.9 1.1
291 11 2
95.7 3.6 0.7
53 3 2
91.4 5.2 3.4
0.2
249 13 2
94.3 4.9 0.8
95 1 2
96.9 1.0 2.0
0.1
159 2 1
98.1 1.2 0.6
185 12 3
92.5 6.0 1.5
0.05
All things considered, how much do you trust your teen’s doctor?
0–5 6–7 8–10
18 20 319
5.0 5.6 89.4
16 17 268
5.3 5.6 89
2 3 51
3.6 5.4 91.1
0.9
13 15 235
4.9 5.7 89.4
5 5 84
5.3 5.3 89.4
0.9
9 12 138
5.7 7.5 86.8
9 8 181
4.5 4.0 91.4
0.3
Notes: P values are calculated using Fishers Exact Test. For Question on scale of 1–10, 1 equals ‘not sure’ or ‘do not trust’ and 10 ‘completely sure’ or ‘completely trust’. This scale applies only to the third and last survey items in the table. 1 Shaded response for each item reflects ‘relative hesitancy’.
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The ONLY reason I have my teenager get vaccines is so they can attend school
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4. Discussion We found that although the PACV was successful in predicting vaccine delays in childhood immunizations, the version we modified for adolescents failed to predict vaccination status at the end of adolescent visits. Two individual items did correlate well, and in an expected manner, with HPV vaccine status. There were significantly more adolescents who remained due than not due for HPV after a clinical encounter if their parents indicated they previously delayed their adolescents’ vaccines for reasons other than illness or allergy. Similarly, there were significantly more adolescents who remained due than not due for HPV if their parents indicated they were not able to openly discuss their concerns about vaccines with their adolescents’ doctor. Consistent with national data [4,5], adolescents’ vaccination status in 6 practices of 2 pediatric practice research networks was considerably lower for HPV than for MCV4 or Tdap. Exactly why this is occurring is unclear. There is the possibility that practices may not have offered the HPV vaccine at all visits or the recommendation for HPV vaccine may have been separated from that for Tdap and MCV. Alternatively, the parent may have refused. The two individual survey items that were associated with poor vaccine uptake tends to support the idea of some degree of safety concerns, trust, and hesitancy. In addition, 25% of respondents were unsure about giving vaccines to teens. This implies that a level of hesitancy toward adolescent vaccines exists, yet is perhaps currently not high enough to influence vaccination behavior. Our factor analysis findings also deserve comment. Our original intention for doing factor analysis was to determine whether similar constructs for vaccine hesitancy as were found in the childhood context by Opel et al. also existed in the adolescent context. The three factors in Opel et al.’s study were “safety and efficacy”, “general attitudes”, and “behavior” [17,18]. We found most factors loaded on one factor, which we originally labeled “safety and concerns”, although an alternate label could also be a combination of the general attitudes and safety concerns. These findings suggest that the PACV, as designed for the childhood vaccine context, may either be too one-dimensional for the adolescent context or, does not adequately capture additional relevant hesitancy constructs salient to the adolescent context. Gilkey et al. explored a subset of 11,754 parents who completed the Parental Attitudes Module as part of the NIS-Teen. They found that 8 items loaded onto 3 factors, labeled “harms”, “benefits”, and “trust” [19]. An additional barrier is the newness of the HPV vaccine and parents desire for more vaccine-specific information before giving it to their child, neither of which is captured in the current PACV [20]. We found it intriguing that the hesitant response to two survey items was significantly associated with an increase in vaccine uptake. Among parents who acknowledged that they were “concerned that a vaccine might not prevent the disease”, more had adolescents who were up-to-date for both Tdap and MCV. Similarly, among parents who agreed with the statement “It is better for my teenager to develop immunity by getting sick than by getting a vaccine”, more had adolescents who up-to-date for Tdap. The rationale for these unexpected associations is unclear. One possible explanation is the concern of the associated diseases with Tdap and MCV is sufficient for parents to opt for the vaccines regardless of their concerns about efficacy. For parents who agree that it is better for their child to develop immunity by getting sick than by getting the vaccine, it is interesting to note that the main differences in responses were related to the percent of responses that were unsure, rather than the hesitancy response. It is also possible that one or more of these results may be due to having made multiple comparisons in this exploratory study. There also may be additional nuances in attitudes and beliefs among parent of adolescents regarding individual adolescent
vaccines that the modified PACV did not capture. Darden showed that parents report reasons for not vaccinating their adolescents against HPV that are unique to that vaccine, such as safety and absence of sexual activity [14]. Therefore, tools to measure vaccine hesitancy with adolescent vaccines likely require measurement of different attitudes and beliefs than those that are relevant to childhood vaccines and may even require domains that are vaccinespecific. Several other factors may explain why we found no association between cumulate hesitancy scores on the modified PACV and adolescent vaccination status, unlike the studies by Opel et al. using childhood vaccination status [17,18]. First, our dichotomous measure of immunization status was less granular than the measure of days under-immunized which Opel et al. used and which accounted for the period of time during which infants were overdue for vaccines. Rather than using a time period of days over-due for individual vaccines we used due versus not-due. All doses of vaccine are recommended during the same age period (11 to 12 years or, for MCV4, 16 years of age) rather than at months of age as is the case for younger children. Because vaccination delay in adolescents is measured in months or years, not days, this study could not achieve the same precision of measurement. Second, vaccine policy and the vaccine delivery system in the adolescent vaccine context is different than that in the childhood vaccine context, and the factors underlying this difference may simply eclipse any effect parental vaccine hesitancy might have on adolescent vaccine uptake. For instance, in the childhood vaccine context in which the PACV was validated [17], vaccine policy and the delivery system are oriented in ways that facilitate vaccine uptake with numerous health supervision visits in the first 4 years of life and laws requiring childhood vaccines for school-entry. Conversely, adolescents generally have fewer physician visits (health supervision or other visits) than do young children. Moreover, SC and OK schools do not require the MCV4 and HPV vaccines in adolescents for school entry. There is currently a school requirement for Tdap for students entering the 7th grade. This requirement was in place at the time of the study in Oklahoma, but not for South Carolina. Third, the study population enrolled in Opel et al.’s studies differs demographically from those in Oklahoma and South Carolina on factors that may affect parental hesitancy. The population in Opel et al.’s study was well educated (91% some college or beyond), predominately white (80%), and married (83.5%). In addition, Opel et al.’s studies were conducted in Washington State, where vaccine hesitancy may well be higher than in either Oklahoma or South Carolina. Fourth, we could not determine whether an adolescent who remained due for a vaccine at the end of a visit was due because their parent refused the vaccine or the provider did not offer or recommend the vaccine. Although each practice in the study routinely offers the adolescent vaccines at all visits as mentioned earlier, it is likely that this did not happen at every study visit. Therefore, an adolescent remaining due at the end of the visit is an imperfect marker of parental attitudes and beliefs toward that vaccine. Our study has some additional limitations. The study population represented a convenience sample, and therefore our results are prone to selection bias. Patients who scheduled visits and then agreed to participate in the study may have been less likely than members of the general clinic population to be due for vaccines, which could underestimate the proportion is due for vaccines. The survey could have acted independently as a prompting intervention for needed vaccines. Conversely, the act of completing the survey may have induced negative feelings about vaccines and caused the parent to opt out of the vaccine. We were also unable to collect data on non-respondents, and this may have represented a source of bias in the sample. We did not collect reasons why adolescents
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did not receive a vaccine, so we are unable to distinguish between instances where parents refused or when the provider didn’t offer the vaccine. There may be some limits of generalizability, as vaccination varies by practice and by state. We have attempted to have a wide variation of practice types. In conclusion, vaccine coverage for HPV was much lower than for MCV4 and Tdap. The modified PACV scale did not predict vaccine uptake in adolescents despite finding a moderate degree of vaccine hesitancy in this population. Further investigation can refine measurement tools that will predict the vaccination status and capture the vaccine-specific concerns of this population. Contributors’ statement James R. Roberts: Dr. Roberts conceptualized and designed the study, drafted the initial manuscript, critically reviewed and edited the manuscript, and approved the final manuscript as submitted. Jessica J. Hale, David Thompson: Ms. Hale and Dr. Thompson carried out the initial analyses, reviewed and revised the manuscript, and approved the final manuscript as submitted. Robert M. Jacobson, Douglas J. Opel, and Paul M. Darden: Drs. Jacobson, Opel, and Darden assisted in the conceptualization and design of the study, critically reviewed and edited the manuscript, and approved the final manuscript as submitted. Funding source This study is funded by grant R40 MC 21522 through the U.S. Department of Health and Human Services, Health Resources and Services Administration, Maternal and Child Health Research Program Clinical trial registration Not applicable. Financial disclosures Dr. Darden has the following disclosures to report: He is a member of the US HPV Advisory Board for Merck. Dr. Jacobson reports the following: He is a member of a safety review committee, for a Phase IV safety study conducted by Merck & Co. in males receiving HPV4 and a member of a data monitoring committee for a series of Phase III pneumococcal vaccine trials also conducted by Merck & Co. Conflict of interest statement The remaining authors have no financial relationships or conflicts of interest relevant to this article to disclose. References [1] Bilukha OO, Rosenstein N, National Center for Infectious Diseases CfDC, Prevention. Prevention and control of meningococcal disease. Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 2005;54(RR–7):1–21 (PubMed PMID: 15917737, Centers for Disease Control).
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[2] Broder KR, Cortese MM, Iskander JK, Kretsinger K, Slade BA, Brown KH, et al. Preventing tetanus, diphtheria, and pertussis among adolescents: use of tetanus toxoid, reduced diphtheria toxoid and acellular pertussis vaccines recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 2006;55(RR-3):1–34 (PubMed PMID: 16557217, Centers for Disease Control). [3] Markowitz LE, Dunne EF, Saraiya M, Lawson HW, Chesson H, Unger ER, et al. Quadrivalent human papillomavirus vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 2007;56(RR-2):1–24 (PubMed PMID: 17380109, Centers for Disease Control). [4] Centers for Disease Control and Prevention. National and state vaccination coverage among adolescents aged 13–17 years—United States, 2012. MMWR Morb Mortal Wkly Rep 2013;62(34):685–93 (Epub 2013/08/30. PubMed PMID: 23985496). [5] Elam-Evans LD, Yankey D, Jeyarajah J, Singleton JA, Curtis RC, MacNeil J, et al. National, regional, state, and selected local area vaccination coverage among adolescents aged 13–17 years—United States, 2013. MMWR Morb Mortal Wkly Rep 2014;63(29):625–33 (Epub 2014/07/24. PubMed PMID: 25055186). [6] Brabin L, Greenberg DP, Hessel L, Hyer R, Ivanoff B, Van Damme P. Current issues in adolescent immunization. Vaccine 2008;26(33):4120–34. [7] Chao C, Slezak JM, Coleman KJ, Jacobsen SJ. Papanicolaou screening behavior in mothers and human papillomavirus vaccine uptake in adolescent girls. Am J Public Health 2009;99(6):1137–42, http://dx.doi.org/10.2105/ajph. 2008.147876. [8] Daley MF, Curtis CR, Pyrzanowski J, Barrow J, Benton K, Abrams L, et al. Adolescent immunization delivery in school-based health centers: a national survey. J Adolesc Health 2009;45(5):445–52. [9] Kempe A, Beaty BL, Steiner JF, Pearson KA, Lowery NE, Daley MF, et al. The regional immunization registry as a public health tool for improving clinical practice and guiding immunization delivery policy. Am J Public Health 2004;94(6):967–72 (Epub 2004/07/14. PubMed PMID: 15249300; PubMed Central PMCID: PMC1448374). [10] Sanford RK. Adolescent vaccination: physician challenges and solutions. J Adolesc Health 2010;46(2 (Suppl 2)):S16–23. [11] Oster NV, McPhillips-Tangum CA, Averhoff F, Howell K. Barriers to adolescent immunization: a survey of family physicians and pediatricians. J Am Board Fam Pract 2005;18(1):13–9 (Epub 2005/02/15. PubMed PMID: 15709059). [12] Schaffer SJ, Humiston SG, Shone LP, Averhoff FM, Szilagyi PG. Adolescent immunization practices: a national survey of US physicians. Arch Pediatr Adolesc Med 2001;155(5):566–71 (Epub 2001/05/18. PubMed PMID: 11343499). [13] Stretch R, Roberts SA, McCann R, Baxter D, Chambers G, Kitchener H, et al. Parental attitudes and information needs in an adolescent HPV vaccination programme. Br J Cancer 2008;99(11):1908–11, http://dx.doi.org/10.1038/ sj.bjc.6604766 (Epub 2008/11/06. PubMed PMID: 18985038; PubMed Central PMCID: PMC2600705). [14] Darden PM, Thompson DM, Roberts JR, Hale JJ, Pope C, Naifeh M, et al. Reasons for not vaccinating adolescents: National Immunization Survey of Teens, 2008–2010. Pediatrics 2013;131(4):645–51, http://dx.doi.org/10.1542/ peds.2012-2384 (Epub 2013/03/20. PubMed PMID: 23509163). [15] Gust DA, Darling N, Kennedy A, Schwartz B. Parents with doubts about vaccines: which vaccines and reasons why. Pediatrics 2008;122(4):718–25, http://dx.doi.org/10.1542/peds.2007-0538 (Epub 2008/10/03, PubMed PMID: 18829793). [16] Darden PM, Jacobson RM. Impact of a physician recommendation. Hum Vaccin Immunother 2014;10(9) (Epub 2014/05/09. PubMed PMID: 24810597). [17] Opel DJ, Mangione-Smith R, Taylor JA, Korfiatis C, Wiese C, Catz S, et al. Development of a survey to identify vaccine-hesitant parents: the parent attitudes about childhood vaccines survey. Hum Vaccin 2011;7(4):419–25 (Epub 2011/03/11. PubMed PMID: 21389777; PubMed Central PMCID: PMC3360071). [18] Opel DJ, Taylor JA, Mangione-Smith R, Solomon C, Zhao C, Catz S, et al. Validity and reliability of a survey to identify vaccine-hesitant parents. Vaccine 2011;29(38):6598–605, http://dx.doi.org/10.1016/j.vaccine.2011.06.115 (Epub 2011/07/19. PubMed PMID: 21763384). [19] Gilkey MB, Magnus BE, Reiter PL, McRee AL, Dempsey AF, Brewer NT. The vaccination confidence scale: a brief measure of parents’ vaccination beliefs. Vaccine 2014;32(47):6259–65, http://dx.doi.org/10.1016/j.Vaccine.2014.09.007 (Epub 2014/09/27. PubMed PMID: 25258098). [20] Holman DM, Benard V, Roland KB, Watson M, Liddon N, Stokley S. Barriers to human papillomavirus vaccination among US adolescents: a systematic review of the literature. JAMA Pediatr 2014;168(1):76–82, http://dx.doi.org/10.1001/ jamapediatrics.2013.2752 (PubMed PMID: 24276343).
Contents lists available at ScienceDirect
Vaccine journal homepage: www.elsevier.com/locate/vaccine
Vaccine hesitancy among parents of adolescents and its association with vaccine uptake James R. Roberts a,∗ , David Thompson b , Brianna Rogacki b , Jessica J. Hale b , Robert M. Jacobson c , Douglas J. Opel d , Paul M. Darden b a
Medical University of South Carolina, Department of Pediatrics, 135 Rutledge Ave, MSC 561, Charleston, SC 29425, USA University of Oklahoma Health Sciences Center, Department of Pediatrics, Section of General and Community Pediatrics, 1200 Children’s Avenue, OUCPB Suite 12400, Oklahoma City, OK 73104, USA c Department of Pediatric and Adolescent Medicine, Mayo Clinic, Desk Ba3b, 200 First St SW, Rochester, MN 55905-0001, USA d Seattle Children’s Research Institute, JMB—6 Clinical and Translational Research, 1900 9th Ave, Seattle, WA 98101, USA b
a r t i c l e
i n f o
Article history: Received 4 September 2014 Received in revised form 21 January 2015 Accepted 27 January 2015 Available online 7 February 2015 Keywords: Vaccine Immunization Adolescent Hesitancy Parent
a b s t r a c t Background: Addressing parental vaccine hesitancy may increase adolescent vaccination acceptance. However, no validated measure exists to identify parents hesitant toward adolescent vaccines. Objective: To determine if a modified version of the Parent Attitudes about Childhood Vaccines (PACV) survey, a previously validated tool to identify parental hesitancy toward vaccines in infants, predicts adolescent vaccine uptake at office visits. Methods: We modified the PACV for use in the adolescent setting and distributed it to a convenience sample of parents of adolescents aged 11 to 17 presenting for care at a diverse group of six pediatric practices in Oklahoma and South Carolina. We determined the vaccination status of the parents’ adolescents for 3 vaccines (Tetanus–diphtheria–acellular pertussis [Tdap], meningococcal conjugate [MCV4], and human papillomavirus [HPV] vaccines). We used Fisher’s exact tests to compare vaccination status with each survey item and with an overall general hesitancy scale that we constructed. Results: We analyzed 363 surveys. At the time of the visit, vaccination coverage was 84% for Tdap, 73% for MCV, and 45% for any dose of HPV. Thirty-nine percent of parents expressed concern about vaccine efficacy and 41% expressed concern about side effects. Forty-five percent of parents disagreed with the statement that “teens can get all of the vaccines that are due at a single visit.” Two individual items were associated with not receiving a dose of HPV vaccine that was due. The overall modified PACV score failed to predict adolescent vaccine uptake at an office visit. Conclusion: Several individual items were associated with vaccine uptake. The cumulative modified PACV, a general measure of vaccine hesitancy, was not associated with vaccination status despite illuminating parental hesitancy. We need to better understand vaccine-specific concerns for the adolescent population. © 2015 Elsevier Ltd. All rights reserved.
1. Introduction The Advisory Committee on Immunization Practices (ACIP) recommends that all adolescents between the ages of 11 and 18 years of age receive 2 doses of meningococcal conjugate (MCV4) vaccine, 1 dose of the adult/adolescent formulation of tetanus–diphtheria–acellular pertussis (Tdap), 3 doses of human papillomavirus (HPV) vaccine, a yearly dose of influenza vaccine, any needed catchup vaccines, and those vaccines indicated for
∗ Corresponding author. Tel.: +1 843 876 8512. E-mail address: [email protected] (J.R. Roberts). http://dx.doi.org/10.1016/j.vaccine.2015.01.068 0264-410X/© 2015 Elsevier Ltd. All rights reserved.
adolescents with high-risk conditions [1–3]. According to the National Immunization Survey-Teen (NIS-Teen), the vaccination coverage of 13–17 year olds increased from 2011 to 2013 for both MCV4 and Tdap. Between 2012 and 2013, 74.0–77.8% of teens received MCV4 and 84.6–86.0% received Tdap [4,5]. For the threedose HPV vaccine series, the rates did not improve from 2011 to 2012 with only 33.4% of females receiving all three doses of HPV in 2012 [4], but slightly increased for 2013 to 37.6% [5]. Vaccination rates for Tdap exceed the Healthy People 2020 goal, but the MCV4 and HPV vaccine coverage rates remained below their goals. Barriers to adolescent vaccination include the lack of central registries that permit clinicians to track individual patients, fewer visits to health care providers, limited and often incorrect parental
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and adolescent knowledge and understanding about vaccines and vaccine safety, and missed opportunities at well or sick visits and parental attitudes [6–13]. Our recent study of NIS-Teen data reveals other barriers to vaccination, some of which are HPV vaccine specific. Notably, among parents not intending to vaccinate with HPV in the next year, the percentage of parents citing safety concerns/side effects with respect to HPV increased from 4.5% in 2008 to 16.4% in 2010, while safety concern/side effects for MCV and Tdap never reached 1%. Parents also reported additional reasons for not giving the HPV vaccine including their teen being “not sexually active” and “not an appropriate age” [14]. Clinician recommendation increases immunization delivery across ages and vaccines. Parents who are generally hesitant about vaccines may be positively influenced by a recommendation from their children’s clinicians to accept immunizations [15,16]. We were interested in evaluating an instrument to measure parental hesitancy regarding adolescent vaccine delivery. In the absence of an adolescent- specific scale, we selected the Parent Attitudes about Childhood Vaccines Survey (PACV) by Opel et al. In evaluations of the PACV, Opel et al. have demonstrated both construct and predictive validity by associating parental PACV scores with immunization status at 19 months of age [17,18]. This study’s purpose is to determine if a modified version of the PACV for use in parents of adolescents aged 11–17 years predicts adolescent vaccine uptake. 2. Methods 2.1. Survey development The initial tested PACV contained 18 items, but this was reduced to 15 items after evaluating its validity [18]. Since we were modifying the PACV for use with a different population, we decided to begin with all 18 original PACV items. The items were modified to reflect our target population of parents of adolescents by substituting the word “teen” for the word “child” and by modifying the language to be read directly by either the parent or the teen. We piloted the English language questions for clarity with five parents of adolescents each in South Carolina and Oklahoma using in-person cognitive interviews. We revised the wording of some questions based on their feedback. Specific changes included replacing the word “shot” with “vaccine” to clarify the type of shots we were referring to. We reworded the PACV question “I trust the information I receive about shots” to read “I trust the information I receive from my teen’s doctor about vaccines.” Lastly, we included several socio-demographic items, such as the relationship of the accompanying adult to the adolescent as well as the age, race/ethnicity, marital status and educational level of the accompanying adult. When the English language survey was finalized, we used an IRB-approved Spanish language translation service to translate the survey into Spanish. We piloted the Spanish language survey with 5 parents using in-person cognitive interviews and made minor modifications for clarity to the items. 2.2. Setting/sample This study took place in three practices in each of two pediatric practice research networks—the Oklahoma Child Health Research Network (OCHRN) and the South Carolina Pediatric Practice Research Network (SCPPRN). The OCHRN practices included a community-based practice serving a predominantly Hispanic population, a primary care clinic staffed by pediatric faculty, and a resident continuity clinic. The SCPPRN practices included a resident continuity clinic, a private practice serving predominantly white and privately insured families, and a rural health clinic.
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We selected practices within each pediatric research network that ensured broad demographic representation and that had consistent vaccine delivery characteristics. In particular, all 6 practices routinely assessed immunization status and administered vaccines at all visits, including sick visits. In addition, all 6 participating practices routinely recommend receipt of the HPV vaccine beginning at age 11 for both males and females. To maintain consistency in the implementation of the study, the research staff developed a protocol that all practices followed. This document described the recruitment and survey distribution strategies, determined which variables would be collected from each source, and ensured that the data were collected systematically and uniformly. 2.3. Recruitment/survey distribution From October 2011 to March 2012, we collected survey data using the modified PACV in a convenience sample of parents or other adults accompanying adolescents 11 to 17 years of age who came to a participating practice for any visit type. We collected a minimum of 60 surveys in each of 6 practices. We obtained verbal parental permission and adolescent assent at the time of intake or triage. In the event that the parent brought two adolescents on the same day, research staff asked the parent to take the survey with the younger patient in mind, as this one was more likely to require vaccines at this visit. Surveys were distributed on each day of the week to the parent and adolescent while they were in the waiting room or exam room before the physician entered the room. All parents completed the survey before the physician entered the room. 2.4. Medical record review and vaccination status Research staff reviewed adolescents’ medical records to determine their vaccination status, age, and gender. Trained study personnel reviewed medical records using a standardized data collection sheet. The research assistants recorded the date each vaccine was received and indicated whether the adolescent was due or not due for vaccines at the completion of the visit. To assess the study’s primary outcome, we determined whether each adolescent remained due or not due for Tdap, MCV4 or HPV vaccines after the visit was completed. Thus for Tdap, participants were considered “not due” if they received Tdap at the study encounter or had received one or more doses of Tdap vaccine since age 10 years. For the MCV4 vaccine, participants between 11 and 15 years were “not due” if they received MCV4 during the study encounter or had ever received at least one dose of MCV4. Those who were 16 and 17 years of age were considered “not due” if they received MCV4 at the visit or had ever received an MCV4 dose on or after their 16th birthday. For the HPV vaccine, the ACIP recommendation for adolescents is to complete the 3 dose series by the time they are 13 years old using intervals of 1–2 months for dose 2 after dose 1, and 6 months for dose 3 after dose 1 [3]. Therefore, participants were considered “not due” if, at the conclusion of the visit, they had either: (1) received three doses of HPV vaccine, (2) received two doses of HPV vaccine and it was less than 6 months from the first dose or less than 3 months from the 2nd dose of HPV vaccine, or (3) received one dose of HPV vaccine less than two months from the visit. Otherwise the adolescent was considered due for HPV vaccine. Thus a study encounter in which an adolescent was due for a vaccine at the end of the visit represented an adolescent who not fully up to date on vaccines. Survey data were entered into a designed QualtricsTM (Provo, UT) database by trained data entry personnel. Quality of data entry was confirmed with 10% duplicated data entry. This database was moved to SAS 9.3 for analysis.
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2.5. Data analysis We used descriptive statistics to summarize participant sociodemographics and vaccination status. We calculated frequency distributions of all survey items. Four of the 18 items requested responses in a “yes”/“no”/“I don’t know” format. Twelve other items requested responses on a 5-point Likert-type scale and two items involved an 11-point (0–10) scale. To understand patterns of association and independence among survey items, we recoded some items so that high scores consistently denoted hesitancy and low scores denoted non-hesitancy for all items. After this reordering, we used SAS PROC FACTOR to perform an exploratory factor analysis, employing a principal components strategy to extract underlying factors or constructs connected with vaccine hesitancy. We also established a cumulative vaccine hesitancy scale in a manner similar to Opel et al. [17,18]. Opel et al. created the cumulative hesitancy score by using raw item scores, summing all raw item scores to obtain a total raw score, and then converting the total raw score to a 0–100 scale. To create our scale, we rescored each item’s values so they ranged from 0 to 10 (“three level” items were scored 0, 5, and 10; “five level” items were scored 2, 4, 6, 8, and 10) where higher scores signified greater hesitancy. We summed the itemspecific scores and then rescaled the sum so that the maximum possible cumulative hesitancy score was 100. We examined associations between vaccination status [due vs. not due] and individual PACV items after establishing categories for some items based on the raw response’s empirical distributions.
We collapsed the items with 5-point Likert-type response categories into 3 groups with the two affirmative responses grouped together, the middle response maintained separately, and the two negative responses grouped together. The two questions that used an 11-point scale (0–10) were grouped as in Opel et al.’s study with categories of 0–5, 6–7, and 8–10 [17,18]. We summarized vaccination status by research network site. We compared the hesitancy score for the modified PACV (using both the original 18-item PACV scale and the revised version consisting of the 15 items retained by Opel et al.) between those who were due and those who were not due for each of the 3 vaccines using permutation tests on cumulative scores using SAS PROC NPAR1WAY. We used Fisher’s exact tests to determine whether responses to individual hesitancy questions were associated with whether adolescents were due for vaccination. The Institutional Review Boards for Human Research at the Medical University of South Carolina and the University of Oklahoma Health Sciences Center both reviewed and approved the study protocol. 3. Results A total of 363 parent surveys were collected. Approximately 91.5% of the 363 adults who accompanied adolescents to the clinic were parents. The remainder included grandparents and legal guardians. As shown in Table 1, our sample consisted of a broad distribution of race/ethnicity and age as well as more males than females. The percentage of adolescents who were due for HPV at
Table 1 Demographic characteristics of adolescents and their parents or other accompanying adults. Characteristic
Age of adolescentˆ 11 12 13 14 15 16 17
Total sample (N = 363)
Oklahoma (N = 182)
N
N
%
South Carolina (N = 181) %
N
%
86 68 60 42 45 40 22
23.7 18.7 16.5 11.6 12.4 11.0 6.1
51 31 26 23 23 17 11
28.0 17.0 14.3 12.6 12.6 9.3 6.0
35 37 34 19 22 23 11
19.3 20.4 18.8 10.5 12.2 12.7 6.1
Gender of adolescent F M
160 203
44.1 55.9
91 91
50.0 50.0
69 112
38.1 61.9
Relationship of adult to adolescent# Mother Father Grandparent Guardian Other relative Other Missing
295 29 12 10 5 3 9
83.3 8.2 3.4 2.8 1.4 0.9
146 12 6 5 3 2 8
83.9 6.9 3.5 2.9 1.7 1.2
149 17 6 5 2 1 1
82.8 9.4 3.3 2.8 1.1 0.6
Accompanying adult’s age# 21–30 31–40 41–50 51–60 61–70 71—99 Missing
23 159 122 31 10 2 16
6.6 45.8 35.2 8.9 2.9 0.5
15 102 43 12 7 0 3
8.4 57.0 24.0 6.7 3.9 0.0
8 57 79 19 3 2 13
4.8 33.9 47.0 11.3 1.8 1.2
Race/ethnicity of accompanying adult# American Indian/Alaska Native Asian Black Native Hawaiian or other Pacific Islander White Hispanic Multi-Racial Missing
3 1 130 0 130 85 7 7
0.8 0.3 36.5 0.0 36.5 23.9 2.0
3 1 39 0 48 82 7 2
1.7 0.6 21.7 0.0 26.7 45.6 3.9
0 0 91 0 82 3 0 5
0.0 0.0 51.7 0.0 46.6 1.7 0.0
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Table 1 (Continued) Characteristic
Accompanying adult’s marital status# Single Dual parent Missing
Total sample (N = 363)
Oklahoma (N = 182)
N
%
N
163 192 8
45.9 54.1
86 95 1
47.5 52.5
77 97 7
44.3 55.7
70 97 92 98 6
19.6 27.2 25.8 27.5
55 54 44 26 3
30.7 30.2 24.6 14.5
15 43 48 72 3
8.4 24.2 27.0 40.4
Accompanying adult’s education# Less than high school High school graduate Some college College graduate or beyond Missing ˆ
South Carolina (N = 181) %
N
%
This variable is from the vaccine information form. # Variable is from the Parent Survey. These tables are based on the PARENT survey responders—363.
Table 2 Percentage of teens in the practices of each research network site who were not due by vaccine (Tdap, MCV, and HPV). Site
All sites Oklahoma South Carolina
Not due named vaccine at conclusion of visit Tdap/Td (%)
MCV (%)
HPV (%)
84.0 83.5 84.5
72.7 72.0 73.5
44.9 52.2 37.6
N = 363.
the end of the encounter was considerably higher compared to the other vaccines (Table 2). Factor analysis identified two underlying constructs that accounted for 83% of the variability in responses among the survey’s 18 items. Table 3 shows that 11 of the survey’s 18 items loaded positively on a single construct that we identified to be “safety and concerns.” A second underlying factor was linked to a positive loading from one additional item, and to negative loadings with two of the 11 items we associated with the first factor. Responses to these two items, correlated with one another (r = 0.63). Table 4 reports the parents’ (or other accompanying adults’) responses to each of the 18 hesitancy questions and how they were associated with adolescents’ vaccination status. Parents’ responses to a number of survey items expressed considerable hesitancy. Overall, 39% of adults expressed concern about preventing disease and 41% expressed concern about serious side effects. Forty-six percent of adults disagreed with the statement that “teens can get all of
the vaccines that are due at a single visit.” Nearly all adults agreed with the statement that “It is my role as a parent to question vaccines.” Of note, 25% responded “unsure” when asked “Overall, how unsure about vaccines for teens would you consider yourself to be?” While these responses document vaccine hesitance among parents of adolescents, we found no association between cumulative hesitancy score for parents and adolescent’s vaccination status for Tdap (P = 0.59, 0.46 (15-item and 18-item scales, respectively), MCV (P = 0.84, 0.75) or HPV (P = 0.92, 0.69). However, several individual survey items discriminated between those who were due or not due for specific vaccines (Table 4). More parents who had adolescents who were “due” for HPV answered “yes” (hesitant response) to “Have you ever delayed a vaccine for reasons other than illness or allergy” compared to those who were “not due”, (8.7% vs. 5.0%, P = 0.048). Parents whose adolescents were due for HPV more often disagreed with the statement “I am able to openly discuss concerns about vaccines with my teen’s doctor” compared to those who were “not due”, (6.0% vs. 1.2%, P = 0.046). Two additional items were associated with vaccination status, but not in the hypothesized direction (Table 4). Parents whose adolescents were due for Tdap and MCV expressed hesitancy less often by stating they were “concerned that a vaccine might not prevent the disease” than did parents of adolescents who were not due for those vaccines. Parents whose adolescents were due for Tdap expressed hesitancy less often by disagreeing with the statement “it is better for my teen to develop immunity by getting sick than by getting a vaccine” than did parents of adolescents who were not due.
Table 3 Results of exploratory factor analysis: factor loadings (≥0.350) for accompanying adult’s survey responses. Survey item Have you ever DELAYED a vaccine for this teen for reasons other than illness or allergy? Have you ever SKIPPED a vaccine for this teen for reasons other than illness or allergy? How sure are you that following the doctor’s recommended shot schedule is a good idea for your teen? It is my role as a parent to question vaccines Teens get more vaccines than are good for them I believe that many of the illnesses that vaccines prevent are severe It is better for my teenager to develop immunity (protection from disease) by getting sick than by getting a vaccine Are you concerned that a vaccine might not prevent the disease? I trust the information I receive from my teen’s doctor about vaccines Are you concerned that your teen might have a serious side effect from a vaccine? I think teens can get all of the vaccines that are due at a single visit Are you concerned that one of the vaccines for teens might not be safe? Do you know of anyone who has had a bad reaction to a vaccine? The ONLY reason I have my teenager get vaccines is so they can attend school If you had another teen today, would you want that teen to get all the vaccines that the doctor recommends? Overall, how unsure about vaccines for teens would you consider yourself to be? I am able to openly discuss my concerns about vaccines with my teen’s doctor All things considered, how much do you trust your teen’s doctor? 1
Factor 1 safety and concerns1
Factor 22
0.551 0.374 0.415 0.360 0.576 0.608 0.608
−0.435
0.637
−0.386
0.383 0.492 0.489 0.593
Factor 1 accounted for 64.5% of the variability in responses among the survey’s 18 items. 2 Factors 1 and 2 together account for 83.3% of the variability.
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Table 4 Parent or other accompanying adult’s survey responses and their association with vaccinations due at the encounter. Tdap/Td
All N Parent question
%
Response1
N
%
N
Not due
%
P
MCV
P N
%
N
Not due
Due
%
N
Due
P
HPV %
N
Not due
% Due
Yes No I don’t know
25 318 12
7.0 89.6 3.4
23 265 10
7.7 88.9 3.4
2 53 2
3.5 93.0 3.5
0.5
19 233 8
7.3 89.6 3.1
6 85 4
6.3 89.5 4.2
0.8
8 142 9
5.0 89.3 5.7
17 176 3
8.7 89.8 1.5
0.05
Have you ever SKIPPED a vaccine for this teen for reasons other than illness or allergy?
Yes No I don’t know
19 333 9
5.3 92.2 2.5
15 281 8
4.9 92.4 2.6
4 52 1
7.0 91.2 1.8
0.8
11 245 8
4.2 92.8 3
8 88 1
8.2 90.7 1.0
0.2
8 152 3
4.9 93.3 1.8
11 181 6
5.6 91.4 3.0
0.7
How sure are you that following the doctor’s recommended shot schedule is a good idea for your teen?
0–5 6–7 8–10
29 27 274
8.8 8.2 83.0
22 23 237
7.8 8.2 84
7 4 37
14.6 8.3 77.1
0.3
20 19 205
8.2 7.8 84
9 8 69
10.5 9.3 80.2
0.7
12 12 126
8.0 8.0 84.0
17 15 148
9.4 8.3 82.2
0.9
It is my role as a parent to question vaccines
Agree Disagree Not sure
336 11 8
94.6 3.1 2.3
283 9 6
95 3 2
53 2 2
93.0 3.5 3.5
0.8
245 9 6
94.2 3.5 2.3
91 2 2
95.8 2.1 2.1
0.8
149 7 3
93.7 4.4 1.9
187 4 5
95.4 2.0 2.6
0.4
Teens get more vaccines than are good for them
Agree Disagree Not sure
92 151 115
25.7 42.2 32.1
77 131 92
25.7 43.7 30.7
15 20 23
25.9 34.5 39.7
0.3
68 114 78
26.2 43.8 30
24 37 37
24.5 37.8 37.8
0.4
49 69 43
30.4 42.9 26.7
43 82 72
21.8 41.6 36.5
0.07
I believe that many of the illnesses that vaccines prevent are severe
Agree Disagree Not sure
292 21 47
81.1 5.8 13.1
241 19 42
79.8 6.3 13.9
51 2 5
87.9 3.4 8.6
0.4
207 18 37
79 6.9 14.1
85 3 10
86.7 3.1 10.2
0.2
129 13 18
80.6 8.1 11.3
163 8 29
81.5 4.0 14.5
0.2
It is better for my teenager to develop immunity (protection from disease) by getting sick than by getting a vaccine
Agree Disagree Not sure
58 246 51
16.3 69.3 14.4
50 212 37
16.7 70.9 12.4
8 34 14
14.3 60.7 25.0
0.05
44 177 38
17 68.3 14.7
14 69 13
14.6 71.9 13.5
0.8
32 103 26
19.9 64.0 16.1
26 143 25
13.4 73.7 12.9
0.1
Are you concerned that a vaccine might not prevent the disease?
Not concerned Concerned Not sure
179 141 38
50.0 39.4 10.6
150 126 26
49.7 41.7 8.6
29 15 12
51.8 26.8 21.4
0.007 132 110 21
50.2 41.8 8
47 31 17
49.5 32.6 17.9
0.02
80 64 16
50.0 40.0 10.0
99 77 22
50.0 38.9 11.1
0.9
I trust the information I receive from my teen’s doctor about vaccines
Agree Disagree Not sure
332 16 10
92.7 4.5 2.8
279 13 8
93 4.3 2.7
53 3 2
91.4 5.2 3.4
0.9
240 14 6
92.3 5.4 2.3
92 2 4
93.9 2.0 4.1
0.3
143 8 7
90.5 5.1 4.4
189 8 3
94.5 4.0 1.5
0.2
Are you concerned that your teen might have a serious side effect from a vaccine?
Not concerned Concerned Not sure
182 148 29
50.7 41.2 8.1
150 126 26
49.7 41.7 8.6
32 22 3
56.1 387.6 5.3
0.6
133 107 22
50.8 40.8 8.4
49 41 7
50.5 42.3 7.2
0.9
82 62 16
51.3 38.8 10.0
100 86 13
50.3 43.2 6.5
0.4
I think teens can get all of the vaccines that are due at a single visit
Agree Disagree Not sure
86 163 110
24.0 45.4 30.6
73 140 88
24.3 46.5 29.2
13 23 22
22.4 39.7 37.9
0.4
64 123 74
24.5 47.1 28.4
22 40 36
22.4 40.8 36.7
0.3
37 69 54
23.1 43.1 33.8
49 94 56
24.6 47.2 28.1
0.5
Are you concerned that one of the vaccines for teens might not be safe?
Not concerned Concerned Not sure
153 152 52
42.9 42.6 14.6
131 125 46
43.4 41.4 15.2
22 27 6
40.0 49.1 10.9
0.5
116 105 40
44.4 40.2 15.3
37 47 12
38.5 49.0 12.5
0.3
73 65 23
45.3 40.4 14.3
80 87 29
40.8 44.4 14.8
0.7
Do you know of anyone who has had a bad reaction to a vaccine?
Yes No I don’t know
48 292 20
13.3 81.1 5.6
35 250 17
11.6 82.8 5.6
13 42 3
22.4 72.4 5.2
0.09
33 218 11
12.6 83.2 4.2
15 74 9
15.3 75.5 9.2
0.1
18 135 8
11.2 83.9 5.0
30 157 12
15.1 78.9 6.0
0.5
J.R. Roberts et al. / Vaccine 33 (2015) 1748–1755
Have you ever DELAYED a vaccine for this teen for reasons other than illness or allergy?
Agree Disagree I don’t know
47 310 4
13.0 85.9 1.1
37 262 4
12.2 86.5 1.3
10 48 0
17.2 82.8 0
0.4
33 226 4
12.5 85.9 1.5
14 84 0
14.3 85.7 0
0.4
21 137 4
13.0 84.6 2.5
26 173 0
13.1 86.9 0
0.08
If you had another teen today, would you want that teen to get all the vaccines that the doctor recommends?
Yes No I don’t know
319 13 28
88.6 3.6 7.8
272 9 21
90.1 3 7
47 4 7
81.0 6.9 12.1
0.1
237 8 17
90.5 3.1 6.5
82 5 11
83.7 5.1 11.2
0.2
144 5 11
90.0 3.1 6.9
175 8 17
87.5 4.0 8.5
0.8
Overall, how unsure about vaccines for teens would you consider yourself to be?
Sure Unsure Don’t know
232 88 33
65.7 24.9 9.3
195 73 28
65.9 24.7 9.5
37 15 5
64.9 26.3 8.8
0.9
166 63 28
64.6 24.5 10.9
66 25 5
68.8 26.0 5.2
0.3
103 38 16
65.6 24.2 10.2
129 50 17
65.8 25.5 8.7
0.9
I am able to openly discuss my concerns about vaccines with my teen’s doctor
Agree Disagree Not sure
344 14 4
95.0 3.9 1.1
291 11 2
95.7 3.6 0.7
53 3 2
91.4 5.2 3.4
0.2
249 13 2
94.3 4.9 0.8
95 1 2
96.9 1.0 2.0
0.1
159 2 1
98.1 1.2 0.6
185 12 3
92.5 6.0 1.5
0.05
All things considered, how much do you trust your teen’s doctor?
0–5 6–7 8–10
18 20 319
5.0 5.6 89.4
16 17 268
5.3 5.6 89
2 3 51
3.6 5.4 91.1
0.9
13 15 235
4.9 5.7 89.4
5 5 84
5.3 5.3 89.4
0.9
9 12 138
5.7 7.5 86.8
9 8 181
4.5 4.0 91.4
0.3
Notes: P values are calculated using Fishers Exact Test. For Question on scale of 1–10, 1 equals ‘not sure’ or ‘do not trust’ and 10 ‘completely sure’ or ‘completely trust’. This scale applies only to the third and last survey items in the table. 1 Shaded response for each item reflects ‘relative hesitancy’.
J.R. Roberts et al. / Vaccine 33 (2015) 1748–1755
The ONLY reason I have my teenager get vaccines is so they can attend school
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4. Discussion We found that although the PACV was successful in predicting vaccine delays in childhood immunizations, the version we modified for adolescents failed to predict vaccination status at the end of adolescent visits. Two individual items did correlate well, and in an expected manner, with HPV vaccine status. There were significantly more adolescents who remained due than not due for HPV after a clinical encounter if their parents indicated they previously delayed their adolescents’ vaccines for reasons other than illness or allergy. Similarly, there were significantly more adolescents who remained due than not due for HPV if their parents indicated they were not able to openly discuss their concerns about vaccines with their adolescents’ doctor. Consistent with national data [4,5], adolescents’ vaccination status in 6 practices of 2 pediatric practice research networks was considerably lower for HPV than for MCV4 or Tdap. Exactly why this is occurring is unclear. There is the possibility that practices may not have offered the HPV vaccine at all visits or the recommendation for HPV vaccine may have been separated from that for Tdap and MCV. Alternatively, the parent may have refused. The two individual survey items that were associated with poor vaccine uptake tends to support the idea of some degree of safety concerns, trust, and hesitancy. In addition, 25% of respondents were unsure about giving vaccines to teens. This implies that a level of hesitancy toward adolescent vaccines exists, yet is perhaps currently not high enough to influence vaccination behavior. Our factor analysis findings also deserve comment. Our original intention for doing factor analysis was to determine whether similar constructs for vaccine hesitancy as were found in the childhood context by Opel et al. also existed in the adolescent context. The three factors in Opel et al.’s study were “safety and efficacy”, “general attitudes”, and “behavior” [17,18]. We found most factors loaded on one factor, which we originally labeled “safety and concerns”, although an alternate label could also be a combination of the general attitudes and safety concerns. These findings suggest that the PACV, as designed for the childhood vaccine context, may either be too one-dimensional for the adolescent context or, does not adequately capture additional relevant hesitancy constructs salient to the adolescent context. Gilkey et al. explored a subset of 11,754 parents who completed the Parental Attitudes Module as part of the NIS-Teen. They found that 8 items loaded onto 3 factors, labeled “harms”, “benefits”, and “trust” [19]. An additional barrier is the newness of the HPV vaccine and parents desire for more vaccine-specific information before giving it to their child, neither of which is captured in the current PACV [20]. We found it intriguing that the hesitant response to two survey items was significantly associated with an increase in vaccine uptake. Among parents who acknowledged that they were “concerned that a vaccine might not prevent the disease”, more had adolescents who were up-to-date for both Tdap and MCV. Similarly, among parents who agreed with the statement “It is better for my teenager to develop immunity by getting sick than by getting a vaccine”, more had adolescents who up-to-date for Tdap. The rationale for these unexpected associations is unclear. One possible explanation is the concern of the associated diseases with Tdap and MCV is sufficient for parents to opt for the vaccines regardless of their concerns about efficacy. For parents who agree that it is better for their child to develop immunity by getting sick than by getting the vaccine, it is interesting to note that the main differences in responses were related to the percent of responses that were unsure, rather than the hesitancy response. It is also possible that one or more of these results may be due to having made multiple comparisons in this exploratory study. There also may be additional nuances in attitudes and beliefs among parent of adolescents regarding individual adolescent
vaccines that the modified PACV did not capture. Darden showed that parents report reasons for not vaccinating their adolescents against HPV that are unique to that vaccine, such as safety and absence of sexual activity [14]. Therefore, tools to measure vaccine hesitancy with adolescent vaccines likely require measurement of different attitudes and beliefs than those that are relevant to childhood vaccines and may even require domains that are vaccinespecific. Several other factors may explain why we found no association between cumulate hesitancy scores on the modified PACV and adolescent vaccination status, unlike the studies by Opel et al. using childhood vaccination status [17,18]. First, our dichotomous measure of immunization status was less granular than the measure of days under-immunized which Opel et al. used and which accounted for the period of time during which infants were overdue for vaccines. Rather than using a time period of days over-due for individual vaccines we used due versus not-due. All doses of vaccine are recommended during the same age period (11 to 12 years or, for MCV4, 16 years of age) rather than at months of age as is the case for younger children. Because vaccination delay in adolescents is measured in months or years, not days, this study could not achieve the same precision of measurement. Second, vaccine policy and the vaccine delivery system in the adolescent vaccine context is different than that in the childhood vaccine context, and the factors underlying this difference may simply eclipse any effect parental vaccine hesitancy might have on adolescent vaccine uptake. For instance, in the childhood vaccine context in which the PACV was validated [17], vaccine policy and the delivery system are oriented in ways that facilitate vaccine uptake with numerous health supervision visits in the first 4 years of life and laws requiring childhood vaccines for school-entry. Conversely, adolescents generally have fewer physician visits (health supervision or other visits) than do young children. Moreover, SC and OK schools do not require the MCV4 and HPV vaccines in adolescents for school entry. There is currently a school requirement for Tdap for students entering the 7th grade. This requirement was in place at the time of the study in Oklahoma, but not for South Carolina. Third, the study population enrolled in Opel et al.’s studies differs demographically from those in Oklahoma and South Carolina on factors that may affect parental hesitancy. The population in Opel et al.’s study was well educated (91% some college or beyond), predominately white (80%), and married (83.5%). In addition, Opel et al.’s studies were conducted in Washington State, where vaccine hesitancy may well be higher than in either Oklahoma or South Carolina. Fourth, we could not determine whether an adolescent who remained due for a vaccine at the end of a visit was due because their parent refused the vaccine or the provider did not offer or recommend the vaccine. Although each practice in the study routinely offers the adolescent vaccines at all visits as mentioned earlier, it is likely that this did not happen at every study visit. Therefore, an adolescent remaining due at the end of the visit is an imperfect marker of parental attitudes and beliefs toward that vaccine. Our study has some additional limitations. The study population represented a convenience sample, and therefore our results are prone to selection bias. Patients who scheduled visits and then agreed to participate in the study may have been less likely than members of the general clinic population to be due for vaccines, which could underestimate the proportion is due for vaccines. The survey could have acted independently as a prompting intervention for needed vaccines. Conversely, the act of completing the survey may have induced negative feelings about vaccines and caused the parent to opt out of the vaccine. We were also unable to collect data on non-respondents, and this may have represented a source of bias in the sample. We did not collect reasons why adolescents
J.R. Roberts et al. / Vaccine 33 (2015) 1748–1755
did not receive a vaccine, so we are unable to distinguish between instances where parents refused or when the provider didn’t offer the vaccine. There may be some limits of generalizability, as vaccination varies by practice and by state. We have attempted to have a wide variation of practice types. In conclusion, vaccine coverage for HPV was much lower than for MCV4 and Tdap. The modified PACV scale did not predict vaccine uptake in adolescents despite finding a moderate degree of vaccine hesitancy in this population. Further investigation can refine measurement tools that will predict the vaccination status and capture the vaccine-specific concerns of this population. Contributors’ statement James R. Roberts: Dr. Roberts conceptualized and designed the study, drafted the initial manuscript, critically reviewed and edited the manuscript, and approved the final manuscript as submitted. Jessica J. Hale, David Thompson: Ms. Hale and Dr. Thompson carried out the initial analyses, reviewed and revised the manuscript, and approved the final manuscript as submitted. Robert M. Jacobson, Douglas J. Opel, and Paul M. Darden: Drs. Jacobson, Opel, and Darden assisted in the conceptualization and design of the study, critically reviewed and edited the manuscript, and approved the final manuscript as submitted. Funding source This study is funded by grant R40 MC 21522 through the U.S. Department of Health and Human Services, Health Resources and Services Administration, Maternal and Child Health Research Program Clinical trial registration Not applicable. Financial disclosures Dr. Darden has the following disclosures to report: He is a member of the US HPV Advisory Board for Merck. Dr. Jacobson reports the following: He is a member of a safety review committee, for a Phase IV safety study conducted by Merck & Co. in males receiving HPV4 and a member of a data monitoring committee for a series of Phase III pneumococcal vaccine trials also conducted by Merck & Co. Conflict of interest statement The remaining authors have no financial relationships or conflicts of interest relevant to this article to disclose. References [1] Bilukha OO, Rosenstein N, National Center for Infectious Diseases CfDC, Prevention. Prevention and control of meningococcal disease. Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep 2005;54(RR–7):1–21 (PubMed PMID: 15917737, Centers for Disease Control).
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