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Topic: HPV vaccination in adol

Topic: HPV vaccination in adolescence

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Journal of Community Health (2020) 45:702–711 https://doi.org/10.1007/s10900-019-00784-w

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O R I G I N A L PA P E R

Misinformation, Gendered Perceptions, and Low Healthcare Provider Communication Around HPV and the HPV Vaccine Among Young Sexual Minority Men in New York City: The P18 Cohort Study

Jessica Jaiswal1,2,3 · Caleb LoSchiavo2,4 · Anthony Maiolatesi2,3,5 · Farzana Kapadia2,6,7 · Perry N. Halkitis2,4

Published online: 4 February 2020 © Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Human papillomavirus (HPV) is the most common sexually transmitted infection among adults in the United States, and can cause several types of cancer. This is of particular concern for sexual minority men, as their increased risk of HIV acquisi- tion increases risk for HPV and HPV-associated cancers, particularly when coupled with low rates of HPV vaccination. As part of a larger study of the syndemic of HIV, substance use, and mental health among young sexual minority men in New York City, we sought to explore what sexual minority men know about HPV and the HPV vaccine, along with their experi- ences have been communicating about the virus and vaccine. We interviewed 38 young sexual minority men with diverse sociodemographic characteristics and identified three main themes: low knowledge about HPV infection and vaccination, highly gendered misconceptions about HPV only affecting women, and lack of communication from healthcare providers about HPV. The prevalence of incorrect HPV knowledge, coupled with inadequate education and vaccination in healthcare settings, indicates a missed opportunity for HPV prevention in a high-risk and high-need population.

Keywords Human papillomavirus · HPV · Health communication · Sexual minority men

Introduction

Human papillomavirus (HPV) remains the most common sexually transmitted infection (STI) in the United States, despite the availability of the 9-valent HPV (9vHPV) vac- cine [1–4]. Conservative population estimates project that genital HPV infection is the most common, affecting nearly 50% of women and 75% of men [3, 4]. This high prevalence of HPV in the US has staggering public health implications [1, 2, 5–7]. Thirty high-risk HPV types are implicated in the etiology of several cancers [8, 9]. HPV types 16 and 18 cause an estimated 72% of anogenital cancers, 55% of vaginal cancers, and 33% of vulvar cancers [6, 7], while low- risk, non-oncogenic HPV types 6 and 11 cause anogenital warts [10].

Routine HPV vaccination was originally recommended starting at age 11–12, allowing for the three-dose series to be completed prior to sexual debut [11]. The historic age parameters for HPV vaccination—11–26 for cisgender women, 13–21 for cisgender men, and 13–26 for sexual minority men (SMM) and transgender women [11]—were recently extended by the US Food and Drug Administration (FDA) to include ages 27–45 [12]. Across age and gender,

* Jessica Jaiswal [email protected]

1 Department of Health Science, University of Alabama, 470 Russell Hall, Tuscaloosa, AL 35487, USA

2 Center for Health, Identity, Behavior & Prevention Studies, School of Public Health, Rutgers University, 1 Riverfront Plaza, Suite 1020, Newark, NJ 07102, USA

3 Center for Interdisciplinary Research on AIDS, Yale University, 135 College Street, New Haven, CT 06510, USA

4 School of Public Health, Rutgers University, 683 Hoes Lane West, Piscataway, NJ 08854, USA

5 School of Public Health, Yale University, 60 College Street, New Haven, CT 06510, USA

6 College of Global Public Health, New York University, 726 Broadway, New York, NY 10012, USA

7 School of Medicine, New York University, 550 1st Avenue, New York, NY 10016, USA

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HPV vaccine uptake remains low, with men initiating and completing the three doses at lower proportions than women [13–15]. HPV infection and low vaccine uptake dispropor- tionately affect SMM, with studies finding that only 13–21% have received at least one of the three doses [16–26]. Low HPV vaccine uptake in SMM is a critical public health con- cern, as HPV infection has been documented to facilitate HIV acquisition and transmission [27–31]. Further, comor- bid HPV/HIV infection increases probability of HPV-related illnesses developing [32–34].

HPV vaccination and vaccine acceptability among SMM are influenced by HPV knowledge, healthcare utilization and engagement, and vaccine recommendation from providers [16–18, 35, 36]. These factors may, in turn, explain sub- standard vaccine coverage in this community. HPV knowl- edge among SMM is low, with less than half knowing that HPV can cause genital, oral, and anal cancers [37]. While provider recommendation is a well-documented predictor of HPV vaccination [18, 24, 38], along with utilization of and sexual orientation disclosure in healthcare services [35, 36], the ability of SMM to engage in healthcare is inhibited by stigma, medical mistrust, and inaccessibility [23, 39, 40]. Barriers to health care are compounded further for those with intersecting marginalized identities [41–43]. Addition- ally, cultural competency among providers and affirming health care have been associated with higher rates of HPV vaccine uptake in SMM [24], though adequate training to provide such care is lacking [44–46]. Collectively, these barriers perpetuate a preventable public health crisis where SMM are disproportionally exposed to and affected by HPV despite the availability of the 9vHPV vaccine.

The objective of this study was to elucidate the nature and depth of (a) HPV and HPV vaccine knowledge and (b) provider communication about HPV vaccine, in a diverse sample of young urban SMM. Further, our questions spe- cific to the HPV vaccine sought to illuminate barriers and facilitators to vaccination, the degree of vaccine literacy, and sources of vaccine knowledge in SMM.

Methods

Study Sample

From April–June 2018, 38 semi-structured interviews were conducted with a sample of racially and ethnically diverse SMM. Participants were randomly selected, strati- fied by race/ethnicity, from a larger cohort study of emerg- ing adult SMM and transgender women in New York City [47, 48]. Participants who were randomly selected for par- ticipation were contacted by email or text message, or in person following completion of a visit for the parent study, with an invitation to participate. The parent study recruited

individuals who, at baseline of Wave 2, were 22–23 years old, were assigned male at birth, had sex with a man in the previous 6 months, reported a negative or unknown HIV serostatus, and lived in the New York City metropolitan region. The qualitative interviews were part of a longitu- dinal sub-study within the parent study, which included brief quantitative surveys as well as biological testing for human papillomavirus (HPV) and herpes simplex virus (HSV); baseline quantitative results have been published elsewhere [25]. The [Rutgers University and New York University] Institutional Review Boards approved all study activities, and all participants provided informed consent.

Data Collection

The research team developed a semi-structured interview guide to examine knowledge and communication regard- ing HPV and the HPV vaccine. Topics included questions about HPV knowledge, vaccine knowledge, experience with and motivations for vaccination, sources of HPV and vaccine knowledge, and experiences with communi- cation about HPV and the vaccine. The interview guide was divided into two sections discussing the vaccine and virus separately, though topics naturally overlapped dur- ing interviews. Additional probes were provided for each question, to ensure that all areas of interest were covered. Interviews lasted, on average, approximately 30 min, with some variation depending on participants’ knowledge and experiences with HPV.

Data Analysis

Interviews were audio-recorded by trained research assis- tants, transcribed by research interns, and checked for accu- racy by two additional interns. Participant names and other potentially identifying information were redacted while transcribing, so that participants were anonymous during analysis; pseudonyms are used to identify participants in the manuscript. The research team utilized a multi-step approach to identify and analyze salient themes from the interview transcripts. This included open coding, application of codes to transcripts, and rigorous review of transcripts and codes to identify themes and patterns. Once coding was complete, quotations were extracted and organized by codes and sub-codes into larger themes, based on patterns revealed throughout analysis. All analyses were reviewed closely by the first two authors, to address occasional differ- ences in interpretation and to discern relationships among established codes Qualitative data were coded and organ- ized using Dedoose v8.0.35, and quantitative data on sample characteristics were analyzed using R v3.6.1.

704 Journal of Community Health (2020) 45:702–711

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Results

Sociodemographic Characteristics

The sample of SMM (n = 38) was diverse in terms of race/ ethnicity, income, education, and sexual identity (Table 1). At the point of the interview, the average age was about 26 years old (M = 25.82, SD 0.95) and ranged 24–27 years. Enrollment was stratified such that near-equal proportions identified as Hispanic/Latinx (n = 10, 26.3%), Black (n = 10, 26.3%), Asian (n = 9, 23.7%), and White (n = 9, 23.7%).

At the study baseline, the majority of interviewees were HIV-negative (n = 35, 92.1%). About half identified as exclu- sively homosexual (55.3%, n = 21). One-fifth had a high school degree or less (n = 8), 34.2% had some college educa- tion, including those with an associate’s degree and current undergraduate students (n = 13), and 44.7% had a bachelor’s or graduate degree (n = 17). Most of the sample was low income, with a total annual income below $5000 (n = 13, 34.2%) or $5000–24,999 (n = 13, 34.2%). Those who par- ticipated in the qualitative interview did not significantly differ from the overall sample of P18 participants, based on these characteristics.

Qualitative Results

Three main themes emerged from the qualitative data: (1) knowledge about HPV and the vaccine is generally low; (2) SMM think only cisgender women are vulnerable to HPV; and (3) under-communication with healthcare pro- viders around HPV and the vaccine is common.

Regarding the first theme, participant knowledge about HPV and the vaccine widely varied, but was most often incorrect. Misinformation and lack of knowledge pertained to several domains related to HPV, including conflation of HPV with other STIs, confusion about transmission, symptoms and outcomes of HPV, and a pervasive lack of knowledge regarding vaccination, testing and treatment. In many cases, participants shared incorrect information with elements of correct information, suggesting that some public health messaging around HIV and STIs has been effective, but HPV has not been sufficiently addressed.

Theme 1: Low HPV Knowledge and Conflation with Other STIs, Especially HIV

Virtually all participants shared incorrect information about HPV and the vaccine. Participants frequently con- fused HPV with other STIs, and often conflated transmis- sion routes with those of HIV. Although the conflation suggests that participants were well aware of HIV trans- mission routes, this finding also suggests that medical and public health messaging around HPV has been extremely inadequate, too often defining SMM’s healthcare solely by HIV.

Most participants shared incorrect knowledge around HPV. In most cases, participants shared mostly incorrect knowledge, but correctly identified some elements:

I know that it’s not curable. I know that it is man- ageable, so I know that the difference is that it, you know, there’s no like, you can’t take, like, antibiotics and make it go away ‘cause it’s not, it’s a virus, it’s not a bacterial infection, and I know that you can manage it in terms of, like, oh, you know, like if you have, like, a wart or something, you can maybe put on a cream or something just to help manage it, but other than that you really are just relying on your immune system to either clear it up or not clear it up. [Josh, 25, Asian]

Above, Josh is correct that the immune system often clears the HPV infection and that antibiotics will not treat HPV, but later reported incorrect information about HPV transmission and vaccination. Similarly, Marc, quoted below, understood there are multiple strains of HPV with different outcomes, but was unclear about the specific details:

Table 1 Sociodemographic characteristics of qualitative interview participants (n = 38)

a Indicates measure taken from baseline P18 assessment

n %

Age (M, SD) 25.82 0.95 Race  Hispanic/Latinx 10 26.3

 Black non-Hispanic 10 26.3  Asian non-Hispanic 9 23.7  White non-Hispanic 9 23.7 Sexual identitya

 Not exclusively homosexual 17 44.7  Exclusively homosexual 21 55.3 Educationa

 High school/GED or less 8 21.0  Some college 13 34.2  Bachelor’s or graduate degree 17 44.7 Total annual incomea

 < $5000 13 34.2  $5000–24,999 13 34.2  $25,000+ 11 28.9 Refuse to answer 1 2.6 HIV statusa

 Negative 35 92.1  Positive 2 5.3  Not tested 1 2.6

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I believe there are like… I believe there are differ- ent ‘strands.’ I am not sure how many. I believe it was 4 last time I went to go to get checked out… I believe the different strands, come out to different symptoms… I believe the different strands can be stronger than others. I am not completely 100% sure [laughs]. [Marc, 27, Latinx]

Trevor thought HPV could be prevented by using con- doms, which is false. However, it is correct that HPV can be transmitted via skin contact:

From what I know [HPV transmission is] genital to skin contact, so you can get oral HPV and you can get vaginal, anal HPV. It’s just without using con- doms. [Trevor, 26, Black]

I mean I think the most common thing is that we would think of as a preventing, as a presenting symp- tom would be warts, I think as with any kind of virus, I’m sure when you have uptake, depending on the severity, you could have general symptoms of virus from being a temperature, or cramps, or aches, or things like that, maybe chills, I don’t know. [Jeremy, 25, White]

The pervasive lack of knowledge around HPV also extended to issues related to vaccination. Below, Evan explains his understanding of HPV vaccine efficacy, fram- ing it in terms of the age guidelines:

The vaccine, it works best when you’re between, I guess fourteen and twenty-six. Or twenty-four. Yeah. But when you’re past that, it doesn’t really work anymore, and it could cause some adverse reactions. [Evan, 26, Asian]

The conf lation of vaccine age recommendations— which were expanded several months after our data col- lection period—also speaks to the failure of messaging around the HPV vaccine to young men.

Participants often conflated HPV with other STIs, par- ticularly herpes and HIV. This finding suggests that while other sexual health messaging has reached this population, there has been inadequate messaging around HPV.

… I think I had the strain–oh god I don’t remember the number, cause it was like strain [pause] I know there was a 2 in it. There was a 2 in it. So like, it was a certain strain and I looked it up and it was like, it’s one of the least, you know, it doesn’t really do anything. So I was like, “Oh okay.” Kinda similar to like herpes. Everybody got it but, we don’t get the feelings of it, so…Yeah, you can have [HPV] and everybody kind of like, you know, [has] cold sores, whatever, you know, [like] we all have, kind of have

a strain of it but, it doesn’t affect you day to day but I guess if it does get more, you get the little lumps and the bumps, so.

I: Anything you know about ways that HPV is trans- mitted? Or ways that you can give or get HPV?

P: Well I’m sure it’s vaginal, anal, oral. I’m sure there’s, yeah, like open wounds. Pretty sure it’s simi- lar to like HIV… I know with HIV it’s through blood, vaginal, anally, breast milk, and there’s one more but I’m missing that. [Julian, 26, Latinx]

Bio-transmission. So, usually that means we’re con- cerned about exchange of bodily fluids…do I get to assume it’s the same as the risk for HIV? Um blood, so certainly if you have open sores, like being careful about that. Semen as well as, I guess, pre-cum, some- thing to kind of like be on the lookout for, breast milk is the one I always forget … and then vaginal fluids. So just kind of like as a general rule, I’m thinking about like, if I am trying to avoid [HPV] transmis- sion, it means use of condoms, if I’m gonna be having penetrative sex. And that there is a lower, although not zero, risk with oral sex, assuming that’s-that there aren’t open sores within the mouth. Also not some- thing that’s applicable within my life, but like nee- dles…Don’t share them. [Ricardo, 27, Latinx]

Theme 2: Belief that Only Cisgender Women are Vulnerable to HPV

The vast majority of participants had not discussed HPV with family, although some recall HPV coming up in fam- ily discussions but only in regard to female siblings. This appeared to lead to many participants perceiving that the vaccine was only for cisgender women. Additionally, for most participants, HPV commercials were the primary way in which they heard any information about HPV or the vac- cine. This targeted media messaging also left participants with the impression that only women are affected by HPV (e.g., Gardasil commercials depicting adolescent girls).

Many participants were under the impression that HPV was only experienced by women, suggesting a widespread perception that boys and men are not affected by it. Very few participants discussed HPV with their family. For those that did, HPV most often came up in the context of a sister’s vaccination. For example, Trevor explained:

I know that for my sister it had come up more because girl and my parents declined to have her go on Gardasil because at the time there were stories in the news espe- cially on Fox News that they watched religiously, that

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it was causing terrible side effects. … I think it was generally thought to be something that would really only affect my sister. And wouldn’t affect me. [Trevor, 26, Black]

P: I think the vaccine is for woman… I heard it’s only, the vaccine…no no, the virus only target woman, even if the man got it, it wouldn’t affect them. But he would be the carrier of that [virus], he might transmit that [virus] to his partner who is a female.

I: Do you think you ever would get vaccinated in the future?

P: [pause] No… It’s not as … I guess that virus is not contagious like HIV or other STD, and even you have it, even if you have it, you’re a woman, and it turns [to] cancer, it takes long time to turn to cancer. So I guess that’s why I’m not getting it… ‘cause from the day you have it to cancer, it might take like 10 or 20 years. Or I guess like it’s not life threaten[ing] situation? [Mike, 26, Asian]

P: From what I think I know, it’s unbiased to gender. I think that it’s more prevalent in women, I wanna say like cervical cancer, but again I’m not too knowledged on it.

I: Talk a little bit more about cervical cancer.

P: So, in my head, I believe that it’s women who get HPV that are untreated, it turns into cervical cancer or it can lead into cervical cancer, but that’s just a hypoth- esis that I can’t really [check].

I: And any other types of cancer or is it just cervical cancer?

P: I don’t really know too much about women, I’m gay, but, that’s what I’ve heard.

I: Cool. Anything you’ve heard about cancer in men?

P: Yes there’s the, the rectal cancer I don’t think that’s the word but anal cancer, I think that’s it but again, don’t know too much about that. [Trevor, 26, Black]

Gardasil commercials led participants to believe that only cisgender women are affected by HPV. Many partici- pants reported learning about HPV from media messaging, specifically the Gardasil commercials. Again, this wide- spread messaging appeared to give participants the impres- sion that HPV was an STI that affects women, and likewise that the vaccine was only for women:

I: Do you remember the first time that you were aware of HPV?

P: I’ve, it was the commercial. I’ll be completely hon- est. It was that commercial. And I it stands out to me so much because I remember “HPV can lead to cervi- cal cancer.” And I just remember hearing it and it stuck in my brain forever, and I just remember being like “Thank god I don’t have ovaries.” (I: Mhm.) But then I googled it one day cause I got, I was like “What if I get it one day” and I was like, “wait it can affect me too?” [Julian, 26, Latinx]

Similarly, Robby, quoted below, recalled seeing Gardasil commercials that only recently expanded gender representa- tion to include men, though too late for the young men in our sample to be vaccinated at an appropriate age prior to sexual debut. These commercials also contributed to participants perceiving that a person must be a young child to be vaccine eligible.

I just vaguely remember [women] being like the tar- get audience like earlier on. I would, yeah there was like a, a commercial, I don’t know for, for, it might’ve been for the vaccine but that’s just the impression I had, and that, like the risk for males, like males can contract the virus but the risk for like actual cancer, I guess it would be ovarian cancer but, like the risk for actual cancer wouldn’t, be anything for that because they don’t have ovaries. [Robby, 27, Asian]

Theme 3: Healthcare Providers Under‑Communicate About HPV and Vaccination

Finally, participants overwhelmingly reported inadequate HPV-related communication with their healthcare provid- ers. Although some were offered the vaccine, their clinicians rarely explained the importance of the vaccine or facilitated discussion. For participants that did initiate the series, healthcare providers did not facilitate vaccine completion. Overall, the data strongly suggest that young SMM are not receiving messaging around HPV or the vaccine.

Healthcare providers did not adequately explain the importance of the HPV vaccine. Most participants reported minimal, if any, HPV-related communication with health- care providers. While some participants were offered the vaccine by a provider, there was scant communication about HPV, the vaccine, or the importance of HPV prevention:

I only remember specifically having screening it like talking about it once with my doctor but that was pretty much ‘You should get this’ and I was just like ‘Ok’, not anything more specific or like, in depth than that. [Kyle, 24, Black]

When I was 17 or something, my doctor was like “Oh it’s on your shot list!” And I was like “Okay.” Beyond that, not really… it was just like a annual

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checkup thing. It’s like “Oh okay you also need your flu shot as well,” so I probably got that. [David, 25, Asian]

I did bring up when [my HPV test] came out positive, here, at [research center]. I told my primary [care pro- vider] and I was like “What can I do?”… And I was like “Okay I came out with this [positive result for HPV], and this was the strand. Uh, the strain.” And he was just like “You’ll be fine. Just, you’re good.” And I was like “Hm oh okay.” That was it. It was very quick, simple- he brushed over like it was nothing…he said “Don’t worry about it, you’ll be fine.” And that was it. [Julian, 26, Latinx]

I: So have you ever talked to a healthcare provider about HPV?

P: Honestly, no. Most healthcare providers I’ve spoken to rarely spoke on anything other than HIV and preg- nancy. [James, 25, Black]

P: No doctor has ever brought [HPV] up to me. And I’ve always had to advocate for this. I remember when it came out, and it was just women getting it, I read somewhere like gay men need to get this because you can get anal cancer, so I went to my doctor, and she was like “Oh I guess that’s technically correct,” and I was like “Okay so vaccinate me,” and she was like “Well, your insurance isn’t gonna cover it.” So I ended up getting it, but I had to pay for it out of pocket, and this was like 2009. I mean now it’s all covered, but I remember like cussing out the insurance company people on the phone. But really, like, no doctor has ever asked about this, which kills me because I work in sexual health.

I: So when you did bring [HPV] up to your doctor, did she talk to you at all about the virus?

P: No, not at all…She was like “I guess you’re sexu- ally active, like you can get it if you want it.” …I think this was before I was sexually active, because this was like my annual physical freshman year of college, and I brought it up and I’m like “This is something I read I needed,” and she didn’t talk about side effects, she didn’t talk about what can come with it, it was like me advocating for myself and she was like “You can get it if you want but like you’re gonna have to pay out of pocket.” [Chris, 27, White]

I: Do you remember [the HPV vaccine] being offered?

P: I think a couple of times, but I didn’t really know much about it so I said no…I mean he probably explained it, but I don’t remember like exactly how the conversation was.

I: Anything specific about the conversation stick with you? No? And then, you said you decided not to get it ‘cause you didn’t know that much about it? (P: Yeah). Tell me a little more about that, about the decision not to get something that you don’t know that much about.

P: Well I’m not just gonna do something if I don’t know, anything about it like I didn’t. It’s really just hard for me to remember, like the conversation, but I know like I wouldn’t just, do something or take something if it’s offered to me if don’t like know, like know about it, espe- cially like medication and stuff.. it’s just like I could be putting anything into my body and not know what I’m doing. [Gabe, 24, Black]

The healthcare system does not adequately follow up with patients to encourage vaccine completion. Even when young SMM initiate the HPV vaccine, healthcare providers are not adequately following up with their patients to ensure completion:

P: I remember getting one shot…And I know that it’s supposed to be more I just don’t know if I ever got the other ones

I: Is there any reason you didn’t get the other [two] doses?

P: I think it was just timing, [pause] I don’t know… I usually see my doctor every like, June, and then just something keeps happening, I guess, I just said it doesn’t work out, [pause] or like it just never comes up again cause I’m there like to get a physical, or something else and I just never really got back to it…it wasn’t a priority … I don’t think it’s an issue of time I just think that it’s an issue of priority like, in subsequent, in subsequent like visits that it just didn’t end up happening. [Kyle, 24, Black]

I remember one of the [research center] surveys about HPV, and we talk about vaccine. And that’s why actu- ally, I believe, isn’t the vaccine- is like three time[s]? … Yeah I mean I just wanna make sure because I feel like I heard about it, and I talk to my doctor about it, for the vaccine, and I probably took like the first two, but I never actually went for the third one because I didn’t have time to so yeah. … Yeah, I took the first two, and then …

,

Article

Understanding How Adolescents Think about the HPV Vaccine

Robyn A. Pennella, Katherine A. Ayers * and Heather M. Brandt

St. Jude Children’s Research Hospital, 262 Danny Thomas Pl, Memphis, TN 38105, USA; [email protected] (R.A.P.); [email protected] (H.M.B.) * Correspondence: [email protected]; Tel.: +19-(01)-3025555

Received: 11 September 2020; Accepted: 13 November 2020; Published: 18 November 2020 �����������������

Abstract: Despite educational efforts, Tennessee human papillomavirus (HPV) vaccination rates are 43%, among the lowest in the United States. This study examined how adolescents think about the HPV vaccine to identify patterns and misconceptions to enhance educational efforts. Adolescents (ages 11–12) (N = 168) responded to open-ended questions regarding their thinking about the HPV vaccine. Data were analyzed and interpreted using qualitative thematic analysis. Three domains of themes emerged from response

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