Factors associated with human papillomavirus vaccine-series initiation and healthcare provider recommendation in US adolescent females: 2007 National Survey of Children's Health

Vaccine 30 (2012) 3112–3118

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Factors associated with human papillomavirus vaccine-series initiation and healthcare provider recommendation in US adolescent females: 2007 National Survey of Children’s Health夽 May Lau a,b,∗ , Hua Lin a , Glenn Flores a,b a b

Division of General Pediatrics, Department of Pediatrics, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390-9063, United States Children’s Medical Center Dallas, 1935 Medical District Drive, Dallas, TX 75235, United States

a r t i c l e

i n f o

Article history: Received 29 December 2011 Received in revised form 12 February 2012 Accepted 13 February 2012 Available online 15 March 2012 Keywords: HPV Vaccination Adolescents Healthcare provider Recommendation

a b s t r a c t Objective: To identify factors associated with initiation of the human papillomavirus vaccine series and parental report of a healthcare provider recommendation of the human papillomavirus vaccine in adolescent females. Design: Cross-sectional analysis of 2007 National Survey of Children’s Health. Participants: Parents of 12–17 year-old US adolescent females. Main outcome measures: Associations of sociodemographic and healthcare factors with initiation of the human papillomavirus vaccine series and parental report of a healthcare provider recommendation of the human papillomavirus vaccine. Results: Data were analyzed for 16,139 adolescent females. Almost 20% of adolescent females initiated the HPV vaccine series. Significantly higher proportions of adolescent females who initiated the human papillomavirus vaccine series vs. those who did not initiate the human papillomavirus vaccine series had a parental report of their healthcare provider recommending the human papillomavirus vaccine (84% vs. 20%). In multivariable analyses, adolescent females who were American Indian/Alaska Native, were multiracial, received the meningococcal vaccine, received the tetanus/tetanus–diphtheria/tetanus–diphtheria–acellular pertussis vaccine, or were poor had higher adjusted odds of initiating the human papillomavirus vaccine series; parental report of a healthcare provider recommendation of the human papillomavirus vaccine was associated with about 18 times the adjusted odds of initiating the human papillomavirus vaccine series. In separate multivariable analyses, adolescent females who were African-American and uninsured had lower adjusted odds of a parental report of a healthcare provider recommendation of the human papillomavirus vaccine. Conclusion: Parental report of a healthcare provider recommendation is significantly associated with human papillomavirus vaccine-series initiation. African-American race/ethnicity and uninsurance were associated with lower odds of a parental report of a healthcare provider recommendation of the human papillomavirus vaccine. Routine healthcare provider recommendation of human papillomavirus vaccination might improve adolescent females’ human papillomavirus vaccination rates. © 2012 Elsevier Ltd. All rights reserved.

Abbreviations: AI/AN, American Indian/Alaska Native; API, Asian/Pacific Islander; CDC, Center for Disease Control; HCP, healthcare provider; HPV, human papillomavirus; NSCH, National Survey of Children’s Health; TD, tetanus–diphtheria; Tdap, tetanus–diphtheria–acellular pertussis. 夽 Presented in part as a platform presentation at the annual meeting of the Pediatric Academic Societies, May 2, 2010, Vancouver, BC; at the AcademyHealth Annual Research Meeting, June 27, 2010, Boston, MA; and at the American Public Health Association Annual Meeting, November 10, 2010, Denver, CO; and as a poster presentation at the Society for Adolescent Health and Medicine Annual Meeting, March 30, 2011, Seattle, WA. ∗ Corresponding author at: Division of General Pediatrics, Department of Pediatrics, University of Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390-9063, United States. Tel.: +1 214 648 2842; fax: +1 214 648 3220. E-mail addresses: [email protected] (M. Lau), [email protected] (H. Lin), glenn.fl[email protected] (G. Flores). 0264-410X/$ – see front matter © 2012 Elsevier Ltd. All rights reserved. doi:10.1016/j.vaccine.2012.02.034

M. Lau et al. / Vaccine 30 (2012) 3112–3118

1. Introduction In June 2006, the three-dose quadrivalent human papillomavirus (HPV) vaccine was approved for licensure for adolescent females 9–26 years old [1]. After the initial dose of the HPV vaccine, the second and third dose are given at two and six months subsequently [1]. Less than half of adolescent females 13–17 years old had received at least one dose of the HPV vaccine in 2010 [2]. Published analyses have identified selected factors associated with HPV vaccine-series initiation, including race/ethnicity, insurance type, geographic region, parental educational attainment, having a preventive health visit, receipt of other vaccines, and parental or adolescent female report of a healthcare provider (HCP) recommendation of the vaccine [3–9]. Most of these studies examined HPV vaccine-series initiation in adolescent females from limited geographic areas, with a certain type of insurance coverage, or from managed care organizations or university-based health settings [4–7,10]. Few nationally representative studies exist on the HPV vaccine series [2,8,9,11] or the impact of HCP recommendation of the HPV vaccine in adolescent females according to parental report [9,11,12]. One study examined HCP recommendation of the HPV vaccine in adolescent females, as reported by the adolescent female [8]. Most of these studies only examined adolescents 13–17 years old [2,8,11,12]. Only one study included adolescent females younger than 13 years old [9]. The Center for Disease Control and Prevention (CDC) recommends HPV vaccine-series initiation at 11–12 years old [13]. To ensure a thorough understanding of factors associated with HPV vaccine-series initiation and parental report of an HCP recommendation of the vaccine, nationally representative studies including adolescent females younger than 13 years old are needed. Furthermore, no studies have examined factors associated with parental report of a HCP recommendation of the HPV vaccine in a nationally representative sample of US adolescent females. The study aim, therefore, was to examine factors associated with HPV vaccine-series initiation and HCP recommendation in a nationally representative sample of US adolescent females 12–17 years old.

2. Methods 2.1. Data source The 2007 National Survey of Children’s Health (NSCH) was a cross-sectional, random-digit-dial household telephone survey conducted by the CDC’s National Center for Health Statistics [14]. The 2007 NSCH was the most up-to-date dataset available at the time of this analysis. The NSCH was designed to produce national and state estimates of various physical, emotional, and behavioral health indicators for children 0–17 years old. A total of 91,642 childlevel interviews were completed between April 2007 and July 2008. Survey respondents were parents or guardians (hereafter referred to as parents) who were most knowledgeable about the health and healthcare of children in the household. The respondent was the mother or father for 94% of the sampled children. The index child for the survey was randomly selected from the household. All interviews were conducted in English, Spanish, or one of four Asian languages: Mandarin, Cantonese, Korean, or Vietnamese. The Spanish and Asian language questionnaires were translated from the English version by experienced translators in each of the respective languages and reviewed for accuracy and cultural appropriateness [14]. All questionnaires were administered by experienced bilingual interviewers. There were 688 households with age-eligible children in which the NSCH interview was not completed because the household did not speak English, Spanish, or one of the four Asian languages [14]. Use of NSCH sample weights permits generalization of findings to the noninstitutionalized US population of

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children 0–17 years old [14]. Households without a landline were not selected to participate in the NSCH, so additional weight was given to interviews from sporadic telephone-service households, given that these households are similar to no telephone-service households [14]. Additional details of the survey have been previously described [14]. This was a secondary database analysis without personal identifiers, so this study was exempt from institutional review board approval. 2.2. Definitions and variables There were two dependent variables of interest: HPV vaccineseries initiation, and parental report of HCP recommendation of the HPV vaccine. HPV vaccine-series initiation was assessed by asking the respondent, “Has [subject child] ever received any HPV shots?” Parental report of HCP recommendation of the HPV vaccine was assessed by asking the respondent, “Did a doctor or health care provider recommend that [subject child] receive HPV shots?” Race/ethnicity was classified according to parental report [White, African-American, Asian/Pacific Islander (API), Latino, American Indian/Alaska Native (AI/AN), or multiracial]. Any report of Latino ethnicity was classified as Latino, regardless of race. 2.3. Analyses All analyses were performed using SAS 9.1 to account for the complex sample design of NSCH and to produce national weighted estimates [15]. The sample was limited to parents of adolescent females 12–17 years old, given that the question regarding HPV vaccination was only asked of adolescent females 12–17 years old. Age was analyzed as a continuous variable. Twelve sociodemographic characteristics of adolescents and their households who initiated or did not initiate the HPV vaccine series were compared, followed by bivariate analyses to identify associations between access-to-care and use-of-service variables and HPV vaccine-series initiation. Multivariable stepwise logistic regression analyses were performed to examine adjusted associations of independent variables with HPV vaccine-series initiation and with HCP recommendation of the HPV vaccine. Independent variables in the HPV vaccine-series initiation model included the adolescent’s age, race/ethnicity, receipt of tetanus/tetanus–diphtheria (TD)/tetanus–diphtheria–acellular pertussis (Tdap) vaccine and meningococcal vaccine, receipt of preventive medical care in the past 12 months, parental report of HCP recommendation of the HPV vaccine, insurance status (at time of survey), US region, and poverty level (using the federal poverty threshold for a family of four at the time of the survey). Poverty was dichotomized as <100% of federal poverty threshold vs. ≥100% of federal poverty threshold. Independent variables analyzed for associations with parental report of HCP recommendation of HPV vaccination included race/ethnicity, highest parental educational attainment, the primary language spoken at home, the number of children in the household, US region, health insurance coverage, having a usual source of care (defined as a place where the child usually goes for well child care and when sick), having a personal doctor or nurse (defined as someone who knows the child and their history well), receipt of preventive medical care in past 12 months, and receipt of the tetanus/TD/Tdap vaccine and meningococcal vaccines. The usual source of care and having a personal doctor or nurse variables were both included, given that it is possible to have a usual source of care but not have a personal doctor or nurse. The initial alpha-to-enter was 0.15, and the final alpha-to-enter was 0.05. Relative risk was calculated only for parental report of HCP recommendation of the HPV vaccine, given that this variable had a high prevalence in the study population [16].

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Table 1 Sociodemographic characteristics of US female adolescents 12–17 years old who have and have not initiated the HPV vaccine series. Characteristic

Mean age (years) Race/ethnicity (%) White Latino African-American Asian/Pacific Islander American Indian/Alaska Native Multiracial No. of children in household (%) 1 2 ≥3 Highest educational attainment of household (%) Not a high-school graduate High-school graduate At least some college Primary language spoken at home not English (%) Mother’s age (yrs) Mother born in US (%) Child born in US (%) Parents employed full time (%) Parents married/cohabit (%) Combined family income: % of federal poverty threshold (%) <100% 100–199% 200–299% 300–399% ≥400% Unknown Region (%) Northeast Midwest South West

Mean (S.E.) or proportion

P

HPV vaccine-series non-initiators (n = 13,112)

HPV vaccine-series initiators (n = 3350)

14.5 (0.04)

14.5 (0.08)

59 18 17 3 1 3

61 16 15 3 1 5

29 37 34

29 38 33

11 28 61 9 43.0 (0.15) 83 94 88 75

11 22 67 8 43.1 (0.34) 84 95 91 73

14 21 18 13 28 8

14 14 13 14 38 7

16 24 36 24

24 21 34 22

.80 .17

.46

.06

.56 .80 .84 .19 .03 .29 <.01

<.01

3. Results 3.1. Sociodemographics A total of 16,462 interviews were analyzed for US adolescent females 12–17 years old. Almost 20% of adolescent females initiated the HPV vaccine series. The mean age of adolescent females who did and did not initiate the HPV vaccine series did not differ (Table 1). Parents whose daughters initiated the HPV vaccine series were more likely to be employed full time. Adolescent females who initiated the HPV vaccine series were more likely to be poor and live in the Northeast, compared with adolescent females not initiating the HPV vaccine series. No differences were noted in any of the other eight sociodemographic variables.

3.2. HPV vaccine-series initiation and access to care and use of services Close to 10% of adolescent females who did not initiate the HPV vaccine series were uninsured, compared with only about 6% of those who initiated the HPV vaccine series (Table 2). Over 95% of adolescent females who initiated the HPV vaccine series had a personal doctor or nurse, vs. only 92% of those who did not initiate the HPV vaccine series. Compared with adolescent females who did not initiate the HPV vaccine series, higher percentages of adolescent females who initiated the HPV vaccine series had a usual source of care. Almost 20% of adolescent females who did not initiate the HPV vaccine series did not have a preventive medical care in the past 12 months, triple the proportion for adolescent females who initiated the HPV vaccine series. Adolescent females who initiated the HPV vaccine series were significantly more likely to have received the

tetanus/TD/Tdap and meningococcal vaccine. Over 80% of adolescent females who initiated the HPV vaccine series had a parental report of HCP recommendation for the HPV vaccine vs. only 20% of adolescent females who did not initiate the HPV vaccine series. 4. Multivariable analyses 4.1. HPV vaccine-series initiation Parental report of HCP recommendation of the HPV vaccine was associated with almost 18 times the odds and 11 times the relative risk of HPV vaccine-series initiation (Table 3). Meningococcal vaccine receipt was associated with triple the odds of HPV vaccine-series initiation. Although the association was not significant in bivariate analyses, AI/AN and multiracial adolescents had almost three times the adjusted odds of HPV vaccine-series initiation, compared with white adolescents. Adolescent females from poor families and those who received the tetanus/Td/Tdap vaccine had 1.5 the odds of HPV vaccine-series initiation. Lack of preventive medical care in the past 12 months was associated with about half the odds of HPV vaccine-series initiation. 4.2. Parental report of HCP recommendation of the HPV vaccine Tetanus/TD/Tdap vaccine receipt was associated with almost triple the odds and meningococcal vaccine receipt with double the odds of a parental report of HCP recommendation of the HPV vaccine (Table 4). Adolescent females who had a personal doctor/nurse had over twice the odds of a parental report of HCP recommendation of the HPV vaccine. Adolescent females who did not have preventive medical care in the past 12 months, were living in the

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Table 2 Bivariate analyses of factors associated with HPV vaccine-series initiation in US adolescent females. Characteristic

No health insurance (%) Has personal doctor/nurse (%) Has usual source of care (%) No preventive medical care in past 12 mos (%) Received tetanus booster/TD/Tdap vaccine (%) Received meningococcal vaccine (%) Parental report of a healthcare provider recommendation of the HPV vaccine series (%)

Proportion

P

HPV vaccine-series non-initiators (n = 13,112)

HPV vaccine-series initiators (n = 3350)

9 92 93 19

6 95 96 6

.01 <.01 <.01 <.01

82

94

<.01

31 20

65 83

<.01 <.01

Table 3 Multivariable analysis of factors associated with HPV vaccine-series initiation in US adolescent femalesa . Characteristic

Odds ratio (95% CI) of HPV vaccine-series initiation

Parental report of a health care provider recommendation of the HPV vaccine series Received meningococcal vaccine Race/ethnicity American Indian/Alaska Native Multiracial African-American Asian/Pacific Islander Latino Combined family income: % of federal poverty threshold (%) <100% poverty level Received tetanus booster/TD/Tdap vaccine No preventive medical care past 12 mos

17.8 (13.7, 23.2) 2.84 (2.23, 3.61) 2.51 (1.38, 4.57) 2.43 (1.32, 4.47) 1.07(0.72, 1.6) 1.05(0.49, 2.22) 1.3(0.84, 2.01) 1.49 (1.01, 2.21) 1.48 (1.03, 2.11) 0.55 (0.31, 0.98)

Significant results are bolded. a Adjusted for adolescent’s age, insurance status, and US region.

southern, midwest, and western regions of the United State, were uninsured, were of African-American race/ethnicity, and had parents whose highest education attainment was a high-school degree or less had lower odds of a parental report of HCP recommendation of the HPV vaccine.

Table 4 Multivariable analysis of factors associated with parental report of a healthcare provider’s recommendation of the HPV vaccine in US adolescent females.a Characteristic

Odds ratio (95% CI) of parental report of HCP recommendation of the HPV vaccine

Received tetanus booster/TD/Tdap vaccine Received meningococcal vaccine Has personal doctor or nurse No preventive medical care past 12 mos Region South Midwest West No health insurance Highest educational attainment of household: high school graduate or lower Race/ethnicity African-American Latino Asian/Pacific Islander American Indian/Alaska Native Multiracial

2.48 (1.9, 3.25) 2.2 (1.81, 2.67) 1.8 (1.07,3.04) 0.36 (0.25,0.52)

0.58 (0.46, 0.74) 0.59 (0.48, 0.73) 0.63 (0.45, 0.89) 0.64 (0.43, 0.96) 0.73 (0.59, 0.91)

0.65 (0.48, 0.87) 0.71 (0.47, 1.07) 0.86 (0.40, 1.83) 0.86 (0.44, 1.68) 0.86 (0.59, 1.26)

Significant results are bolded. a Adjusted for the primary language spoken at home, the number of children in household, and having a usual source of care.

5. Discussion The study findings reveal that parental report of HCP recommendation is associated with a significantly higher odds and relative risk of HPV vaccine-series initiation in a nationally representative study of adolescent females 12–17 years old from all five racial/ethnic groups and multiracial youth. This is the highest published magnitude, to our knowledge, for this association in adolescent females. Two other national studies examining factors associated with HPV vaccine-series initiation in adolescent females demonstrated that parental report of HCP recommendation was associated with 2.5 times and five times the odds of HPV vaccine-series initiation [8,11]. In contrast, there is one nationally representative study which demonstrated almost half of parents choosing not to vaccinate their 9–17 year-old daughter would not do so even after physician recommendation of the HPV vaccine [12]. Smaller regional studies of adolescents and young women also have demonstrated parental report of HCP recommendation is associated with HPV vaccine-series initiation [6,17–19]. One study in Los Angeles demonstrated parental report of HCP recommendation of the HPV vaccine was associated with 48.5 the odds of HPV vaccine-series initiation in Latino and African-American adolescent females 11–18 years old [6]. In two North Carolina studies, parental report of HCP recommendation of the HPV vaccine was associated with double the relative risk and 12 times the odds of HPV vaccine-series initiation, respectively [17,18]. Physician discussion and recommendation of the HPV vaccine was associated with 94 times the odds of HPV vaccine-series initiation in a sample of insured young women 19–26 years old from a US health plan [19]. Analogous to findings for the HPV vaccine series, parental report of HCP recommendation of the influenza and meningococcal vaccines also have been associated with higher rates of influenza and meningococcal vaccination in children [20,21]. Of concern, in two separate studies, only one in three parents reported a physician

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recommendation of the HPV vaccine for their daughter, possibly indicating missed opportunities for HCP recommendation of the HPV vaccine [6,17]. The findings of these multiple studies, taken together with our study results, suggest that routine HCP recommendation of the HPV vaccine might result in higher adolescent female HPV vaccination rates. Receipt of other adolescent vaccines was found to be associated with significantly higher odds of HPV vaccine-series initiation. Specifically, receipt of the tetanus booster/TD/Tdap and meningococcal vaccines was associated with increased odds of HPV vaccine-series initiation. Receipt of the meningococcal and influenza vaccines has previously been shown to be associated with HPV vaccine-series initiation in regional studies [3,7], but our study demonstrates an association of receipt of the tetanus/TD/Tdap vaccine with HPV vaccine-series initiation. States with tetanuscontaining vaccine mandates have been shown to have higher HPV vaccine rates [22]. The CDC recommends that the HPV vaccine series be initiated at the same age as the Tdap and meningococcal vaccine [13]. It is possible that an adolescent visit for vaccine administration may provide HCPs an opportunity to discuss the HPV vaccine, thereby, enhancing the likelihood of initiating the HPV vaccine series. Although parental report of HCP recommendation of the HPV vaccine was strongly associated with HPV vaccine-series initiation, not all adolescent females received such a recommendation. African-American adolescent females were significantly less likely to have a parental report of HCP recommendation of the HPV vaccine. In separate multivariable stepwise logistic analyses (data not shown), African-American adolescent females who had received the tetanus/TD/Tdap or the meningococcal vaccines had double the odds of parental report of HCP recommendation of the HPV vaccine. African-American females who were uninsured, had no preventive medical care in the past 12 months, and had parents whose highest educational attainment was a high-school degree or less had lower odds of a parental report of HCP recommendation of the HPV vaccine. There are conflicting studies regarding African-American female HPV vaccine-series initiation rates, compared with whites [23,24]. Nevertheless, African-American females have the highest cervical-cancer mortality rate of all race/ethnicities [25]. Analogous disparities in HCP recommendation for preventive measures for African-Americans also have been noted for colorectal screening [26–28]. Given that a parental report of HCP recommendation of the HPV vaccine is associated with substantially higher odds of HPV vaccine-series initiation, routine HCP recommendation of the HPV vaccine to African-American adolescent females might have the potential to reduce or eliminate disparities in HPV vaccine-series initiation and completion, and cervical cancer mortality. Uninsured adolescents were less likely to have a parental report of HCP recommendation of the HPV vaccine. Uninsurance also has been documented to be associated with lack of a HCP recommendation for colorectal screening and mammography in adults [29,30]. Uninsured adolescents are less likely to have a primary healthcare provider [31,32], which could account for the lower odds of a parental report of HCP recommendation of the HPV vaccine. Research has previously demonstrated that uninsured adolescents and young women have lower odds of HPV vaccine-series initiation [4,33]. The Affordable Care Act may make insurance more affordable for the uninsured [34], thereby potentially increasing access to HCP recommendations and vaccines. Lack of a preventive medical care in the past 12 months was associated with no parental report of HCP recommendation of the HPV vaccine. Adolescents have the lowest rates of adherence to well-child visits and higher rates of non-preventive medical visits [35,36]. Research demonstrates that most adolescent vaccines are provided during preventive medical care visits [37], and adolescents who do not seek preventive care are more likely to be

delayed in receiving vaccines such as the Td vaccine [38]. A preventive medical care visit in the past 12 months has been shown to be associated with HPV vaccine-series initiation [7]. HCPs may need to recommend vaccines during any healthcare visit, whether for preventive or sick care. Although one study suggests that parents prefer doctor’s offices for vaccinations, other healthcare sites in which parents would accept vaccinations for their adolescents include, in order of preference, public-health clinics, school-health clinics, obstetrics/gynecology clinics (for females), and emergency departments [39]. A pediatric emergency room-based influenza vaccination program successfully increased influenza vaccination rates of children and their families [40]. HCPs in healthcare sites other than a pediatrician’s office, thus could serve as potentially important sources for increasing HPV vaccination rates by recommending the HPV vaccine. Certain study limitations should be noted. The 2007 NSCH is a cross-sectional study. Although NSCH data are almost five years old, this was the latest dataset available when this analysis was performed. The 2011 NSCH currently is still in progress, and is scheduled to end in March 2012 [41]. All information was obtained via parental report, not medical records, so the prevalence of HPV vaccine-series initiation and parental report of HCP recommendation of the HPV vaccine may not necessarily be accurate, due to recall bias, although a recent study demonstrated that parents had one of the lowest rates of incorrectly recalling their daughter’s HPV vaccine-series status, compared with other vaccines [42]. Although directionality cannot be determined from a cross-sectional study, it is possible that parents whose daughters received the HPV vaccine may be more likely to remember an HCP recommendation for the vaccine. As in other studies examining the association of HCP recommendation of the HPV vaccine with HPV vaccine-series initiation [9,11,12], the assumption was that parents whose adolescent daughters did and did not initiate the HPV vaccine series were able to recall if an HCP recommended the HPV vaccine. It is possible that parents may not report an HCP recommendation for the HPV vaccine due to access-to-care issues, lack of a medical home, or receiving care from HCPs not recommending or having the HPV vaccine. Having a personal doctor or nurse and usual source of care, therefore, were adjusted in multivariable analyses of factors associated with parental report of HCP recommendation for the HPV vaccine. Completion of the full HPV vaccine series could not be examined, given that there were insufficient numbers of adolescent females who had completed the entire HPV vaccine series at the time the 2007 NSCH was conducted. HPV vaccine-series completion rates have been shown to be lower than HPV vaccine-series initiation rates [2,4,5,24,43,44]. Analyses of HPV vaccine-series initiation and parental report of HCP recommendation of the HPV vaccine could not be stratified by age, due to insufficient sample sizes. Information on religious affiliation and the adolescents’ history of sexual activity is not available in the NSCH. HPV vaccineseries initiation and HCP recommendation of the HPV vaccine in adolescent males were not examined, given that Food and Drug Administration approval of the HPV vaccine for adolescent males was not granted until 2009 [45]. Compared with pediatricians, family practice practitioners are less likely to recommend that children receive all vaccines, but information on physician specialty is not available in the NSCH [46]. The NSCH does not provide information on API subgroups such as Chinese, Filipino, Asian Indian, and AI/AN tribal groups. Specific study strengths also should be noted. NSCH is one of the largest and most diverse national datasets that contains information on all five major US racial/ethnic groups and multiracial adolescents. This study examined factors associated with HPV vaccine-series initiation in a nationally representative sample of US adolescents 12–17 years old from all five major US racial/ethnic groups and multiracial adolescents using the latest NSCH data

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available and shortly after the Advisory Committee on Immunization Practices recommended the HPV vaccine series in March 2007 [1]. Other nationally representative studies have examined fewer racial/ethnic groups, did not examine multiracial youth, and included only adolescents ≥13 years old [2,8,9,11]. These studies also examined fewer sociodemographic factors, or did not include other variables that potentially could be associated with HPV vaccine series-initiation, such as the number of children living at home, the primary language spoken at home, the mother’s and adolescent female’s birthplace, parents’ employment status, and parents’ marital status. Furthermore, this is the first nationally representative study to examine factors associated with parental report of HCP recommendation of the HPV vaccine for 12–17 year olds for all five major US racial/ethnic groups and multiracial adolescents, with additional information on factors associated with a parental report of HCP recommendation of the HPV vaccine in African-American adolescents. The study findings have several research, practice, and policy implications for improving HPV vaccine-series rates. Increasing HCP recommendation of the HPV vaccine might require HCP reminders. Use of HCP vaccination reminders via electronic medical records or office protocols has been shown to improve pediatric vaccination rates [47]. To improve HPV vaccine-series rates, HCP providers may need to initiate the HPV vaccine series with administration of other adolescent vaccines. Simultaneous administration of adolescent vaccines has been documented to improve vaccine receipt [47]. In one university-based healthcare system, half of eligible adolescent females concurrently received another adolescent vaccine with the initial HPV vaccine [4]. Encouraging healthcare providers to recommend the HPV vaccine to all vaccine-eligible adolescents, regardless of race/ethnicity and insurance status, could help reduce HPV vaccine receipt disparities. One recent survey, for example, revealed that only about half of physicians recommend the HPV vaccine to adolescent female patients [48]. HCPs, therefore, might consider any healthcare visit as an opportunity to recommend the HPV vaccine series for unimmunized, vaccine-eligible adolescent females. Author contributions Dr. Lau has had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Lau and Flores. Acquisition of data: Lau, Lin, and Flores. Analysis and interpretation of data: Lau, Lin, and Flores. Drafting of the manuscript: Lau, Lin, and Flores. Critical revision of the manuscript for important intellectual content: Lau and Flores. Statistical analysis: Lau, Lin, and Flores. Administrative, technical, and material support: Lau and Flores. Study supervision: Lau and Flores. All authors approved the final version of the submitted manuscript. Financial disclosure None reported. References [1] Markowitz LE, Dunne EF, Saraiya M, Lawson HW, Chesson H, Unger E, et al. Quadrivalent human papillomavirus vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2007;56(RR-2):1–24. [2] Center for Disease Control. National and state, vaccination coverage among adolescents aged 13–17 years – United States, 2010. MMWR Morb Mortal Wkly Rep 2010;60(33):1117–23. [3] Chao C, Velicer C, Slezak JM, Jacobsen SJ. Correlates for human papillomavirus vaccination of adolescent girls and young women in managed care organization. Am J Epidemiol 2010;171(3):357–67. [4] Dempsey A, Cohn L, Dalton V, Ruffin M. Patient and clinic factors associated with adolescent human papillomavirus vaccine utilization within a university-based health system. Vaccine 2010;28(4):989–95.

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[5] Cook RL, Zhang J, Mullins J, Kauf T, Brumback B, Steingraber H, et al. Factors associated with initiation and completion of human papillomavirus vaccine series among young women enrolled in Medicaid. J Adolesc Health 2010;47(6):596–9. [6] Guerry SL, De Rosa CJ, Markowitz LE, Walker S, Liddon N, Kerndt PR, et al. Human papillomavirus vaccine initiation among adolescent girls in high-risk communities. Vaccine 2011;29(12):2235–41. [7] Reiter PL, Cates JR, McRee A, Gottlieb SL, Shafer A, Smith JS, et al. Statewide HPV vaccine initiation among adolescent females in North Carolina. Sex Transm Dis 2010;37(9):549–56. [8] Caskey R, Lindau ST, Alexander GC. Knowledge and early adoption of the HPV vaccine among girls and young women: results of a national survey. J Adolesc Health 2009;45(5):453–62. [9] Wong CA, Berkowitz A, Dorell CG, Anhang Price R, Lee J, Saraiya M. Human papillomavirus vaccine uptake among 9–17 year old girls. Cancer 2011, doi:10.1002/cncr.26246 [Epub ahead of print]. [10] Staras SAS, Vadaparampil ST, Haderxhanaj LT, Shenkman EA. Disparities in human papillomavirus vaccine series initiation among adolescent girls enrolled in Florida Medicaid programs, 2006–2008. J Adolesc Health 2010;47(4): 381–8. [11] Dorell CG, Yankey D, Santibanez TA, Markowitz LE. Human papillomavirus vaccination series initiation and completion, 2008–2009. Pediatrics 2011;128(5):830–9. [12] Dorell C, Yankey D, Strasser D. Parent-reported reasons for nonreceipt of recommended adolescent vaccinations, National Immunization Survey-Teen, 2009. Clin Pediatr 2011;50(12):1116–24. [13] Center for Disease Control. Recommended immunization schedule for persons aged 7 through 18 years, United States. Available at: http://aapredbook.aappublications.org/resources/IZSchedule7-18yrs.pdf; 2011 [accessed 30.06.11]. [14] Blumberg SJ, Foster EB, Fraiser AM, Satorius J, Skalland BJ, Nysse-Carris KL, et al. Design and operation of the National Survey of Children’s Health. Available at: ftp://ftp.cdc.gov/pub/Health Statistics/NCHS/slaits/nsch07/2 Methodology Report/NSCH Design and Operations 052109.pdf; 2007 [accessed 27.06.11]. [15] SAS. SAS software, Release 9.1. Cary, NC: SAS Institute Inc.; 2008. [16] Kleinman LC, Norton EC. What the risk? A simple approach for estimating adjusted risk measures from nonlinear models including logistic regression. Health Serv Res 2009;44(1):288–302. [17] Brewer NT, Gottlieb SL, Reiter PL, McRee A, Liddon N, Markowitz L, et al. Longitudinal predictors of human papillomavirus vaccine initiation among adolescent girls in a high-risk geographic area. Sex Transm Dis 2011;38(3): 197–204. [18] Gottlieb SL, Brewer NT, Sternberg MR, Smith JS, Ziarnowski K, Liddon N, et al. Human papillomavirus initiation in an area with elevated rates of cervical cancer. J Adolesc Health 2009;45(5):430–7. [19] Rosenthal SL, Weiss TW, Zimet GD, Ma L, Good MB, Vichnin MD. Predictors of HPV vaccine uptake among women aged 19–26: importance of a physician’s recommendation. Vaccine 2011;29:890–5. [20] Daley MF, Crane LA, Chandramouli V, Beaty BL, Barrow J, Allred N, et al. Influenza among healthy young children: changes in parental attitude and predictors of immunization during the 2003 to 2004 influenza season. Pediatrics 2006;117(2):e268–77. [21] Lu PJ, Jain N, Cohn AC. Meningococcal conjugate vaccination among adolescents aged 13–17 years, United States, 2007. Vaccine 2010;28(11):2350–5. [22] Dempsey AF, Schaffer SE. Human papillomavirus vaccination rates and state mandates for tetanus-containing vaccines. Prev Med 2011;52:268–9. [23] Bednarczyk RA, Birkhead GS, Morse DL, Dolevres H, McNutt LA. Human papillomavirus vaccine uptake and barriers: association with perceived risk, actual risk, and race/ethnicity among female students at a New York university, 2010. Vaccine 2011;29(17):3138–43. [24] Schluterman NH, Terplan M, Lydecker AD, Tracy JK. Human papillomavirus (HPV) vaccine uptake and completion at an urban hospital. Vaccine 2011;29(21):3767–72. [25] Watson M, Saraiya M, Benard V, Coughlin SS, Flowers L, Cokkinides V, et al. Burden of cervical cancer in the United States, 1998–2003. Cancer 2008;113(Suppl. 10):2855–64. [26] Coughlin SS, Thompson T. Physician recommendation for colorectal screening by race/ethnicity, and health insurance status among men and women in the United States, 2000. Health Promot Pract 2005;6(4):369–78. [27] James TM, Greiner KA, Ellerbeck EF, Feng C, Ahluwalia JS. Disparities in colorectal cancer screening: a guideline-based analysis. Ethn Dis 2006;16:228–33. [28] Rich SE, Kuyateh FM, Dwyer DM, Groves C, Steinberger EK. Trends in selfreported health care provider recommendations for colorectal cancer screening by race. Prev Med 2011;53(1–2):70–5. [29] Matthews BA, Andeson RC, Nattinger AB. Colorectal screening behavior and health insurance status (United States). Cancer Causes Control 2005;16(6):735–42. [30] Bhosle M, Samuel S, Vosuri V, Paskett E, Balkrishnan R. Physician and patient characteristics associated with outpatient breast cancer screening recommendations in the United States: analysis of the National Ambulatory Medical Care Survey Data 1996–2004. Breast Cancer Res Treat 2007;103(1):53–9. [31] Lawrence RS, Gootman JA, Sim LJ., eds. Adolescent health services: missing opportunities. Washington, DC: The National Academies Press; 2009. [32] DeVoe JE, Tillotson CJ, Wallace LS. Children’s receipt of health care services and family health insurance patterns. Ann Fam Med 2009;7:406–13. [33] Price RA, Tiro JA, Saraiya M, Meissner H, Breen N. Use of human papillomavirus vaccine among young adult women in the United States: an analysis of the

3118

[34]

[35] [36]

[37]

[38] [39]

[40]

[41]

M. Lau et al. / Vaccine 30 (2012) 3112–3118

2008 National Health Interview Survey. Cancer 2011, doi:10.1002/cncr.26244 [Epub ahead of print]. Kaiser Family Foundation. Summary of coverage provisions in the Patient Protection and Affordable Care Act. April 14, 2011, Available at http://www.kff.org/healthreform/upload/8023-R.pdf [accessed 08.08.11]. Nordin JD, Solberg LI, Parker ED. Adolescent primary care patterns. Ann Fam Med 2010;8(6):511–6. Selden TM. Compliance with well-child visit recommendations: evidence from the Medical Expenditure Panel Survey, 2000–2002. Pediatrics 2006;118(6):e1766–78. Rand CM, Shone LP, Albertin C, Auinger P, Klein JD, Szilagyi PG. National health care visit patterns of adolescents: implications for delivery of new adolescent vaccines. Arch Pediatr Adolesc Med 2007;161(3):252–9. Lee GM, Lorick SA, Pfoh E, Kleinman K, Fishbein D. Adolescent immunizations: missed opportunities for prevention. Pediatrics 2008;122(4):711–7. Clevenger L, Pyrzanowski J, Curtis CR, Bull S, Crane LA, Barrow JC, et al. Parents’ acceptance of adolescent immunizations outside of the traditional medical home. J Adolesc Health 2011;49:133–40. Pappano D, Humiston S, Goepp J. Efficacy of a pediatric emergency department-based influenza vaccination program. Arch Pediatr Adolesc Med 2004;158(11):1077–83. Centers for Disease Control and Prevention. State and local area integrated telephone survey. National Survey of Children’s Health. Available at: http://www.cdc.gov/nchs/slaits/nsch.htm; 2011 [accessed 30.01.12].

[42] Dorell CG, Jain N, Yankey D. Validity of parent-reported vaccination status for adolescents aged 13–17 years: National Immunization Survey-Teen, 2008. Public Health Rep 2011;126(Suppl. 2):60–9. [43] Tan W, Vierea AJ, Rowe-West B, Grimshaw A, Quinn B, Walter EB. The HPV vaccine: are dosing recommendations being followed? Vaccine 2011;29(14):2548–54. [44] Dempsey A, Cohn L, Dalton V, Ruffin M. Worsening disparities in HPV vaccine utilization among 19–26 year old women. Vaccine 2011;29(3): 528–34. [45] Centers for Disease Control. FDA licensure of quadrivalent human papillomavirus (HPV4 Gardasil) for use in males and guidance from the Advisory Committee on Immunization Practices. MMWR Morb Mortal Wkly Rep 2010;59(20):630–2. [46] Gust D, Weber D, Weintraub E, Kennedy A, Soud F, Burns A. Physicians who do and do not recommend children get all vaccinations. J Health Commun 2008;13(6):573–82. [47] Briss PA, Rodewald LE, Hinman AR, Shefer AM, Strikas RA, Bernier RR, et al. Reviews of the evidence regarding interventions to improve vaccination coverage in children, adolescents, and adults. Am J Prev Med 2000;18(Suppl. 1):97–140. [48] Vadaparampil ST, Kahn JA, Salmon D, Lee J, Quinn GP, Roetzheim R, et al. Missed clinical opportunities: provider recommendations for HPV vaccination for 11–12 year olds girls are limited. Vaccine 2011 [Epub ahead of print].