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Toward a Model of HPV Vaccine Series Completion in Adolescent Hispanic Males

Identifying Mothers' Salient Behavioral, Normative, and Control Beliefs

Roncancio, Angelica M., PhD; Carmack, Chakema C., PhD; Ward, Kristy K., MD; Vernon, Sally W., PhD; Muñoz, Becky T., PhD; Cano, Miguel A., PhD; Cribbs, Felicity L., BA

doi: 10.1097/FCH.0000000000000221
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Human papillomavirus (HPV) vaccine series completion among adolescent Hispanic males (35%) is lower than the Healthy People 2020 80% goal. This directed qualitative content analysis identified mothers' beliefs about their sons completing the series. We found that mothers (N = 19) (1) express positive feelings; (2) believe the vaccine has positive effects; (3) identify the father and doctors as supporters and friends as nonsupporters; (4) list health insurance, transportation, and clinic reminders as facilitators; and (5) mention affordability as a barrier to vaccine completion. Results provide guidance for interventions. Increasing HPV vaccination among boys will decrease the overall incidence of HPV in this population.

Department of Social Sciences, University of Houston-Downtown, Texas (Dr Roncancio); Psychological Health and Learning Sciences, University of Houston, Texas (Dr Carmack); Texas Oncology, Sugar Land (Dr Ward); Center for Health Promotion and Prevention Research, The University of Texas School of Public Health, Houston (Dr Vernon and Ms Cribbs); Department of Psychology, Mount St Mary's University, Emmitsburg, Maryland (Dr Muñoz); and Department of Epidemiology, Florida International University, Miami (Dr Cano).

Correspondence: Angelica M. Roncancio, PhD, Department of Social Sciences, University of Houston-Downtown, One Main St, Houston, TX 77002 (amroncancio@gmail.com).

Research for this publication was supported by NIH/NCI grant K01CA181437 and NIH/NIAAA grant K01AA025992.

The authors declare no conflict of interest.

CERTAIN HUMAN PAPILLOMAVIRUS (HPV) types can cause penile, anal, and oropharyngeal cancer in males. This includes types 16 and 18, which cause the majority of HPV-associated cancers (∼63%) and types 31, 33, 45, 52, and 58 that are responsible for an additional 4%.1–6 As compared with females, the prevalence of high-risk oral and genital HPV is higher among males.7 Other HPV types (6 and 11) are responsible for an estimated 90% of cases of genital warts.6 Fortunately, the introduction of the HPV vaccine series has greatly increased our ability to prevent cancers caused by these HPV types.8–10

Vaccinating all eligible males is especially important given the rise in the incidence of HPV-caused oropharyngeal cancer in the United States and the fact that the incidence of this type of cancer is higher among males.11,12 In 2009, the Food and Drug Administration approved the HPV vaccine for use in males between the ages of 9 and 26 years.6 In 2011, the Advisory Committee on Immunization Practices recommended vaccination with the Gardasil vaccine.6 The Healthy People 2020 goal is an 80% HPV vaccine completion rate among all adolescents.13 However, according to the 2015 National Immunization Survey, the vaccine initiation rate among Hispanic males between the ages of 13 and 17 years was an estimated 58.9% and the completion rate was 35%.14 Given the low rate of vaccine series completion, it is clear that we need to increase our efforts to raise HPV vaccine series completion among adolescent Hispanic males.

Research on HPV vaccine uptake among adolescent Hispanic males indicates that a doctor's recommendation, a doctor's visit in the last year, older age, awareness of the vaccine, and lower income predict vaccine uptake.15,16 Furthermore, among foreign-born parents, those born in Mexico (compared with other countries) are less likely to have had a son who initiated the HPV vaccine series and less acculturated parents were less likely to vaccinate due to a lack of awareness about the vaccine.17 However, there is less research examining the factors that influence HPV vaccine series completion among this population. Some studies have found that clinic reminders, awareness that males can be vaccinated against HPV, and having vaccine information might increase vaccine completion.18,19 It is necessary to continue to identify factors that are specifically related to completion because researchers have found that factors influencing uptake and completion, at least in females, differ.20

The first step toward developing an effective intervention is to build a theory-based behavioral model. The Integrative Model of Behavioral Prediction (IM)21,22 proposes that engaging in any given behavior can be predicted by an individual's intention to engage in that behavior, possession of the necessary skills and abilities to engage in that behavior, and a lack of environmental constraints to engaging in the behavior. According to the IM, behavior change is achieved through identifying the most salient beliefs associated with a behavior and developing intervention messages that target those beliefs. The 3 belief constructs include behavioral, normative, and control beliefs. Behavioral beliefs are composed of experiential attitudes (ie, perceived positive and negative feelings about the behavior) and instrumental attitudes (ie, perceived positive and negative effects of the behavior). Normative beliefs encompass perceived supporters and nonsupporters of the behavior in question. That is, those are perceived to agree or disagree that the individual should engage in the behavior. Control beliefs are perceived behavioral facilitators and barriers. Beliefs vary by culture and should be identified by conducting elicitation interviews with the population of interest.23 Therefore, the purpose of this study is to identify the salient beliefs Hispanic mothers hold about having their sons complete the HPV vaccine series.

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METHODS

Participants

From May 2014 through January 2015, we conducted in-depth elicitation interviews with Hispanic mothers of adolescent boys between the ages of 11 and 17 years. Participants were recruited from community sites including community centers and clinics in Houston, Texas. Eligibility criteria included identifying as Hispanic or Latino, Spanish as the primary language, and having a son between 11 and 17 years of age who had received at least one dose of the HPV vaccine. Experts suggest conducting elicitation interviews with a sample composed of participants who have and have not engaged in the target behavior.23 We achieved data saturation at 19 interviews. Our sample consisted of 6 mothers of boys who had received 1 dose of the HPV vaccine, 5 mothers of boys who had received 2 doses of the HPV vaccine, and 8 mothers of boys who had received 3 doses.

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Procedure

Potential participants were approached at the community sites in Spanish, and provided with a brief description of the study. We explained the purpose of the study, eligibility criteria, the length of the interview, and the incentive amount. Women who met the eligibility criteria and were interested in participating provided written informed consent. The majority of the participants were interviewed at the recruitment sites, but when that was not possible, research staff conducted the interview at the participant's home, in a quiet room that allowed for privacy and where it was quiet enough to allow for audio-recording. The recruitment sites included 3 community centers and 2 clinics. Each of the sites allowed the research team access to a private, quiet room where the interview could be conducted and recorded. Before the interview, participants completed a brief demographic survey that included mother's age, country of birth, marital status, and level of education. The interviews were then conducted and audio-recorded by female research staff. Each interview lasted between 20 and 35 minutes. Participants were compensated $20 for their participation. All procedures were approved by the institutional review board at the University of Texas Health Science Center-Houston (HSC-SPH-13-0594).

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Interview guide and data analysis

The interview guide consisted of a series of open-ended questions. Its development was guided by previous research conducting elicitation interviews to discover underlying beliefs, as described by the IM.24–28 This research provided guidelines and suggestions regarding the wording of the interview questions. As such, our interview guide consisted of questions that identified participants' behavioral, normative, and control beliefs related to having their sons complete the vaccine series (Table 1). Four questions elicited behavioral beliefs associated with vaccine completion. Two of the 4 questions identified experiential attitudes (ie, positive and negative feelings about vaccinating) and the remaining 2 questions elicited instrumental attitudes (ie, positive and negative effects of vaccinating). Two questions elicited normative beliefs (ie, who would support vaccination and who would not support vaccination). The final 2 IM items elicited control beliefs (ie, barriers and facilitators to vaccinating). Additional probes were prepared in case they were needed. However, during the coding process we noted that they were infrequently employed. As suggested,25 we pilot tested the interview guide with 5 mothers from the population of interest to ensure comprehension and clarity of the questions.

TABLE 1

TABLE 1

We followed Middlestadt and colleagues'29 recommendations for collecting and analyzing qualitative interview data. The interviews were transcribed verbatim by a Spanish-speaking transcriptionist. Given that the purpose of the study was to identify mothers' beliefs about having their sons complete the HPV vaccine series, our research design was a content analysis. Specifically, we employed directed qualitative content analysis30 to rank the beliefs mentioned and to select the most salient beliefs. This type of content analysis is appropriate when the goal is to validate an existing theory.30 It is recommended for elicitation interview studies29 and qualitative studies employing the IM and conceptually related theory of planned behavior.25 We employed the framework method31 to analyze these data. The primary author first read through the transcripts and developed a list of codes for positive and negative experiential attitudes (ie, behavioral beliefs), positive and negative instrumental attitudes (ie, behavioral beliefs), behavioral supporters and nonsupporters (ie, normative beliefs), and behavioral facilitators and barriers (ie, control beliefs), respectively. Codes were created by assigning concepts to key words or phrases regarding a particular belief. Similar key words and phrases were then grouped and named with a particular code. After developing the codes, independent coders, including the primary author, examined the text for the predetermined codes. The second and third coders were instructed to note any additional codes that they believed should be considered for inclusion. They marked the quote(s) they believed were associated with any additional codes. Then, the potential codes and their associated quotes were discussed by all 3 coders and a consensus regarding their inclusion was reached. This process resulted in the addition of 1 code “clinic hours,” which was listed as a behavioral facilitator (ie, control belief). As prescribed by the framework method,31 the primary author then developed a spreadsheet with matrices for each interview question in which participants' responses/quotes were entered into the rows and the codes were entered in adjacent columns at the top. Each coder received a copy of the spreadsheet and read each response and marked the cells under each code as appropriate. All discrepancies between the coders' theme counts were examined, discussed, and resolved. The frequencies and percentages for the theme counts were calculated to determine the majority responses for each construct and select the most salient beliefs. As suggested by Francis and colleagues,25,32 the most salient beliefs were defined as, at minimum, the top 75% of beliefs mentioned.

To maintain qualitative rigor, we were guided by the model of trustworthiness' 4 components: credibility, transferability, dependability, and confirmability.33 To establish credibility, we employed a peer examination strategy.34 The coauthor (C.C.C.) carefully reviewed and discussed the coding process with the primary author. We established transferability by employing the same data collection methods to investigate HPV vaccine series completion among Spanish-speaking Hispanic mothers of girls and obtained similar findings.35 In order to establish dependability, we have carefully described the research methods to ensure that our study is auditable.33 Finally, we employed triangulation36 to establish confirmability. More specifically, we employed method triangulation, investigator triangulation, and data source triangulation. We collected quantitative data and confirmed the association of the beliefs with HPV vaccination in this population (ie, method triangulation). The associated manuscript is in preparation. Four of the authors (A.M.R., C.C.C., B.T.M., and F.L.C.) were involved in the study from its inception to provide multiple observations and perspectives (ie, investigator triangulation). We collected data from both mothers who had and mothers who had not yet had their sons complete the HPV vaccine series (ie, data source triangulation). This allowed us to gain insight into the behavior from 2 different perspectives (those who had engaged in the behavior and those who had not).

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RESULTS

Demographics

The mean age of our 19 participants was 42.3 years (standard deviation = 6.0 years), with the majority older than 40 years (Table 2). Most participants were married or living with a partner (68.4%), did not complete high school (73.7%), and were foreign-born (94.8%), with a mean of 19.3 years living in the United States (standard deviation = 9.2 years). Over half (57.9%) had sons between the ages of 13 and 14 years. All of the sons were covered by health insurance, with 89.6% covered by a government-funded/subsidized plan. Approximately 42% of the sons had received all 3 doses of the vaccine, with the remaining having received either 1 or 2 doses (31.6% and 26.3%, respectively).

TABLE 2

TABLE 2

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Behavioral beliefs

Experiential attitudes (positive and negative)

The most often mentioned positive feelings included good (34.8%), happy (17.4%), at ease (13%), and secure (13%). Mothers stated that they would feel good because their sons would have all of the required doses. “I felt good because I said to myself, ‘Now he has all of the vaccines that are required for the series.’” Others stated that they would feel happy because the vaccine series would protect him from HPV. “I will feel happy when I finish the vaccine series because it will help him avoid HPV.” At ease was another positive feeling expressed by mothers and was attributed to the belief that completing the vaccine series would prevent their son from getting HPV. “I felt at ease after completing the vaccine series, because it is best to prevent HPV.” Feeling more secure about their son's future health was the fourth most frequently mentioned positive feeling associated with having him complete the HPV vaccine series. “I felt more secure about his health after he completed the vaccine series.”

Almost 80% of the mothers reported no negative feelings about having their sons complete the vaccine series. Mothers who responded “no negative feelings” elaborated that this was because the vaccine would help ensure good health. “Not one negative feeling. There are no negative feelings if the vaccine keeps him healthy.”

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Instrumental attitudes (positive and negative)

The most frequently mentioned positive effects included for protection (28.6%), for prevention (28.6%), and the vaccine is good for his health (23.8%). Mothers explained that completing the vaccine series would protect their sons from HPV. “Well, I know that by completing the series he will be protected. At least he will be protected from HPV.” Those who responded prevention said that vaccine series would prevent illnesses or cancer: “A positive effect is the prevention of a sexually transmitted illness. Also, the vaccine will prevent him from getting cancer.” Mothers who responded that the vaccine is good for his health often explained that they believed that their son would enjoy better health as a result of the vaccine: “Well, it was the same as when he received the other two doses, I believe that the vaccine is good for his health.”

No negative effects (88.2%) was the most common response when mothers were asked to describe negative effect of vaccinating. “Negative effects? I don't believe that there are any and vaccinating against HPV is something that I will not regret. I will not regret having prevented my son from giving someone else the human papillomavirus or contracting it from someone else.” Mothers often explained that having their sons complete the HPV vaccine series would only have positive health effects.

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Normative beliefs

Supporters

The most salient supporters of HPV vaccine series completion were the son's father (31.4%), the son's mother (28.6%), and the doctor (20%). The son's father was mentioned most frequently as a supporter of completing the vaccine series. “My husband, my child's father, supports completing the vaccine series. As his parents we watch over the health of our child to make sure that he is well and maintains good health.” Mothers often elaborated that it was their responsibility to make the decision to have their sons complete the vaccine series for his health. “I made the decision myself. As the mother, I am the one who makes decisions for my children.” Doctors were mentioned as supporters because they recommended vaccination against HPV. “The doctor. He told me about the vaccine, explained it to me and said that vaccinating my son was a good thing to do.”

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Nonsupporters

Most mothers (73.7%) did not identify any nonsupporters, but a small percentage (15.8%) identified their friends as nonsupporters. This pattern of responses suggests that these mothers did not have anyone discouraging or not supporting vaccination and that it would not matter if someone did. “I believe that no one would discourage me from vaccinating him. Besides, I am the only one who will make that decision for my son.” Some mothers' also mentioned that their friends did not support vaccination because they had inaccurate information about the vaccine. “My friends, the misinformed ones, always say that it could damage him in certain areas of his personal life. But I don't listen to them. I simply tell them that vaccinating is my decision and they must respect it.” Other mothers explained that those friends believed that vaccinating was unnecessary. “Sometimes friends comment, they say ‘No, why would you vaccinate him if he doesn't need the vaccine?’ But once you read the information in the brochures and such ... Perhaps this is what they need. They haven't received information about the vaccine and they feel unsure about vaccinating their sons.”

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Control beliefs

Facilitators

The 4 most salient facilitators to vaccine completion included health insurance (39.3%), transportation (17.9%), scheduling vaccination appointments (10.7%), and vaccine reminders (7.1%). One mother said, “Well, for me it was easy to vaccinate because he has Medicaid. But if he did not have health insurance then it would be difficult to vaccinate him because I do not have the means necessary to pay for that vaccine.” Regarding transportation, one mother stated, “Having a way to get to the clinic makes completing the vaccine series easier.” Transportation as a facilitator was followed by having a scheduled vaccination appointment for the next dose in the series. “Having a scheduled appointment with the doctor to vaccinate him would make it easier to complete the vaccine series.” Finally, receiving clinic reminders about upcoming vaccine doses was the fourth most frequently mentioned facilitator of vaccine series completion. “For me it would be easier if the clinic remind me or sent me a notification message so that I can have it in mind that he needs one more dose of the vaccine to complete the series.”

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Barriers

The top 3 barriers to vaccine completion included nothing (25%), no health insurance (25%), and cost of the vaccine (13%). Several mothers stated that there were no barriers to having their son complete the HPV vaccine series. “No, there was nothing that made vaccinating him difficult.” However, other mothers mentioned that if their son did not have health insurance at the time when the next vaccine dose was due, completing the vaccine series would be difficult. “My son not having health insurance and having to wait until he has health insurance would make it difficult to complete the series.” The majority of responses regarding the cost of the vaccine were related to the mother being unable to cover the cost of the vaccines out-of-pocket. “Well, I say that it is money, not having money that would make it hard to complete the series because then I would have to pay for the HPV vaccine myself.”

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DISCUSSION

This qualitative elicitation study identified the behavioral, normative, and control beliefs held by Hispanic mothers about having their adolescent sons complete the 3-dose HPV vaccine series. Our findings can be used to develop quantitative survey items, which will allow researchers to better understand what factors predict vaccine series completion in this population. In addition, the beliefs we identified add to the literature regarding the types of intervention messages that may help increase vaccine series completion in this population.

Mothers' experiential attitudes (ie, positive and negative feelings) were all positive. Good, the most mentioned feeling, related to complying with the recommendation about the number of doses needed. The remaining positive feelings (ie, happy, at ease, and secure) were associated with the health benefits of the vaccine. These findings support existing research that Hispanic parents are generally accepting of the HPV vaccine.37,38 They also provide guidance for intervention messages and suggest that it is more important to reinforce and increase the positive feelings identified rather than focusing on reducing negative feelings since negative feelings do not appear to be as salient for vaccine series completion in this population. Future research should investigate the relative importance of the feelings identified to determine which should be addressed in interventions.

The most often mentioned instrumental attitudes (ie, positive and negative effects) were all positive. Mothers believe that completing the vaccine series will offer protection from HPV and cancer and that it provides health benefits. Negative effects of vaccination were not salient in this population, suggesting the once the series is initiated, concern about side effects is minimized. Our findings suggest reinforcing the health benefits of completing the HPV vaccine series and incorporating the terms “prevention,” “protection,” and the “vaccine is good for his health” in intervention messages. This is supported by research showing that a focus on vaccine benefits is associated with greater vaccination intentions.39

For Hispanic mothers of adolescent boys, the son's father was the most mentioned supporter of HPV vaccine series completion. The importance of fathers in HPV vaccination decisions is supported by existing research.40 However, this is the first study to show that their support is important for vaccine completion in adolescent boys, as it is for vaccine completion in adolescent girls.35 This suggests that the role fathers play in decision-making should be taken into account. One strategy is to have intervention messages reinforce that fathers do support vaccine series completion. Findings also suggest that intervening with fathers might increase vaccine completion in this population.

Existing literature supports the importance of perceiving that the doctor supports HPV vaccination.16,41 As such, reinforcing the belief that doctors recommend vaccine series completion may increase the likelihood of completion. Also, increasing the mother's belief in her role as a supporter of vaccine series completion may increase her self-efficacy and the likelihood that her son completes the vaccine series.

Mothers' friends were the second most common response when asked about nonsupporters after “no one.” However, mothers often elaborated that their friends' opinions would not change their belief that completing the series was the best thing to do. Existing research among mothers of girls is consistent with our finding of friends as nonsupporters of vaccination.40 Future research should investigate the importance of friends' lack of support for mothers of boys. The current findings suggest that interventions should emphasize likely supporters of vaccination and, to a lesser extent, develop messages to counter the potential influence of friends' perceived lack of support.

Lacking health insurance and having to pay for the vaccine were the second and third most frequently mentioned perceived or potential barriers after “no barriers.” Existing research supports the association between vaccination and vaccine affordability (ie, having health insurance coverage or vaccine availability for free or at a low cost).38 The final 2 facilitators to vaccine series completion were related to the vaccination appointment itself. Mothers mentioned that having a scheduled vaccination appointment and a clinic reminder about the upcoming appointment facilitated vaccine series completion. There is support for the influence of vaccine reminders on vaccination rates.42 However, this is the first study to identify the importance of having a vaccination appointment. Interventions should raise awareness among these mothers that the health insurance covers the cost of the vaccine. Furthermore, even if their child's coverage lapses, programs such as Vaccines For Children cover the cost of the vaccine for eligible uninsured and underinsured children. Interventions should also reinforce the importance of making vaccination appointments and provide mothers with strategies to remember and keep upcoming appointments. In addition, health care providers should be encouraged to send appointment reminders. Finally, as evidenced by our “no barriers” finding, many mothers did not encounter obstacles to vaccination. This suggests a need to further explore the difference between perceived and actual barriers to HPV vaccination.

There are some limitations to the study. First, given that we only interviewed Spanish-speaking Hispanic mothers of boys, our results may not be generalizable to English-speaking Hispanic mothers, mothers with high levels of acculturation, or to non-Hispanic mothers. Mothers whose primary language is English or who are highly acculturated may have different salient beliefs than the mothers we interviewed in the current study. Also, our study participants resided in an urban area; therefore, our results may not reflect the beliefs of mothers who live in rural areas and have more limited transportations or clinic options and thus may experience more barriers to accessing the HPV vaccine. Interviewing fathers was beyond the scope of our study, so our findings may not reflect the beliefs of fathers. Mothers are more likely than fathers to make medical decisions and attend clinic visits with their minor children, so it is possible that their beliefs, attitudes, and experiences differ in significant ways.43–47 These other populations may have different salient beliefs that need to be identified and addressed by future interventions. Also, as with research of this nature, there is the possibility of social desirability bias on the part of the respondent. In order to limit the effects of this bias, interviewers received training on how to engage with participants and conduct the interview in such a way as to ensure that participants felt comfortable sharing their beliefs. Finally, there is the possibility of interviewer bias. To minimize this bias, we employed a structured interview guide and provided interviewers with in-depth training.

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CONCLUSION

This is the first study to examine Spanish-speaking Hispanic mothers' beliefs about having their sons complete the HPV vaccine series using the Integrative Model. We found generally positive feelings toward having their sons complete the HPV vaccine series and a belief that completing the series would positively affect the health of their sons. Fathers and doctors were generally viewed as being supportive of the son completing the series. We also found evidence of having health insurance, transportation, and receiving a clinic reminder as facilitators to vaccine completion. Future research should confirm our results and expand the research scope to identify the salient beliefs fathers hold and explore their role in vaccinating their sons against HPV. It should also examine whether and how beliefs differ depending on whether the mother has a son, daughter, or both and how this influences HPV vaccine series completion. This will facilitate the development of HPV educational interventions for both parents. Our findings provide important guidance for the development of interventions for Spanish-speaking Hispanic mothers of adolescent boys. Ultimately, effective theory-based interventions have the potential to reduce the burden of HPV-associated cancers in the Hispanic population.

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Keywords:

adolescent; cancer vaccines; Hispanic Americans; mothers; papillomavirus vaccines

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