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Misconception: Human Papillomavirus Vaccine and Infertility

Christine L. Schuler, Chassidy J. Hanley and Tamera Coyne-Beasley CLIN PEDIATR 2014 53: 158 originally published online 26 September 2013 DOI: 10.1177/0009922813504026 The online version of this article can be found at: http://cpj.sagepub.com/content/53/2/158

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research-article2013

504026

CPJXXX10.1177/0009922813504026Clinical PediatricsSchuler et al

Article

Misconception: Human Papillomavirus Vaccine and Infertility

Christine L. Schuler, MD, MPH1, Chassidy J. Hanley, MPH1, and Tamera Coyne-Beasley, MD, MPH1

Clinical Pediatrics 165 2014, Vol. 53(2) 158 The Author(s) 2013 Reprints and permissions: sagepub.com/journalsPermissions.nav DOI: 10.1177/0009922813504026 cpj.sagepub.com

Abstract Background. This study sought to determine if parents of males express concerns about vaccine-associated infertility (VAI) with the human papillomavirus (HPV) vaccine and to understand the impact of those concerns. Methods. Parents of sons were surveyed to determine VAI concerns. Logistic regression was used to find if parents worried about VAI had lower knowledge of HPV disease, more concern for side effects, lacked information about vaccination, or had lower intention to vaccinate. Results. In all, 39% of parents were worried about VAI. Parents worried about VAI had similar knowledge of HPV compared with other parents. Parents worried about VAI had twice the odds of agreeing the vaccine may cause side effects and agreeing they did not have enough information compared to their counterparts. Parents worried about VAI less often intended to vaccinate sons than other parents. Conclusions. These findings suggest many parents worry about VAI in sons with HPV vaccine. Keywords HPV vaccine, infertility, parent, HPV, side effects

Introduction
Human papillomavirus (HPV) is a widely prevalent sexually transmitted infection among both males and females.1,2 HPV is associated with genital warts3 and various malignancies, including cervical, penile, anal, and oropharyngeal cancers, among others.4 Within the United States, rates for 2 HPV-related cancers, anal and oropharyngeal cancers, have increased in recent years.5 Currently, 2 vaccines are available that protect against HPV, including bivalent (HPV2) and quadrivalent (HPV4) vaccines.6 HPV4 vaccine was licensed for use in males in 20097 and is currently the only HPV vaccine approved for use in males. HPV4 vaccine protects against HPV types 6 and 11, the types primarily responsible for genital warts, and types 16 and 18, two prevalent oncogenic types.8 Although the Advisory Committee on Immunization Practices recommended permissive vaccination in 2010 and routine vaccination for males aged 11 to 12 years in October 2011, with catch up vaccination for males 13 to 21 years old,8 less than 9% of eligible males have received any doses of HPV vaccine.9 The reasons for low vaccination rates in males are likely multifactorial, but reasons that have been proposed include the initial Advisory Committee on Immunization Practices permissive recommendation for HPV vaccine in males, as

well as low awareness among parents about the vaccines availability for boys.10 Concerns that boys may not see a clear benefit from vaccination,11 or other potential barriers to vaccination, including parents worries about possible side effects,12,13 may also be important to consider in the setting of low vaccination rates. Commonly described side effects of HPV4 vaccine include local skin reactions near injection sites, headache, and fever.14 Syncope has also been reported in association with HPV4 vaccine and has occurred in the context of other adolescent vaccinations as well.15 Among males specifically aged 9 to 26 years, pain at injection site was reported in about 61%, headache reported in about 12%, and fever reported in about 8%.14 Other more serious reactions have been reported with HPV4 vaccine such as thromboembolic events and Guillain Barre syndrome, but further examination of these reports and surveillance data has

 he University of North Carolina at Chapel Hill, Chapel Hill, NC, T USA

Corresponding Author: Tamera Coyne-Beasley, UNC Gillings School of Global Public Health, The University of North Carolina at Chapel Hill, Campus Box 7225, 231 MacNider, Chapel Hill, NC 27599-7225, USA. Email: coybea@med.unc.edu

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Schuler et al not established a causative link with the HPV vaccine and these conditions.15 In addition to recognized side effects, studies have also reported concerns about other potential effects associated with HPV vaccine such as promiscuity,13,16,17 birth defects, miscarriages,18 or vaccine-associated infertility (VAI).17-21 Although HPV vaccine has not been studied in humans specifically with regard to infertility, studies using male and female rat models have shown no adverse effects on fertility, and thus there is currently no evidence to support a link between infertility and HPV4 vaccine.22,23 It is unclear exactly what proportion of parents are concerned about VAI. To our knowledge, concerns for VAI have not been studied specifically in the context of male vaccination, and the relevance of such concerns to the uptake of HPV vaccine is unclear. Qualitative studies among parents of females suggest that fear of the vaccine causing reproductive health issues, especially infertility, may contribute to decision making for those not vaccinated.24,25 In a systematic review, safety concerns were found to be associated womens intent to get vaccinated against HPV in 8 quantitative studies. In this review, 3 of the 5 studies that reported concerns regarding safety and adverse effects of the vaccines specifically cited concerns about vaccination on future fertility.26 Given the importance of exploring barriers to vaccination among males at a time of low vaccination rates, we sought to determine how common concerns for VAI are among parents of boys. We also sought to determine if parents concerned about VAI had lower knowledge of HPV disease, increased concern for unknown side effects, lacked information to decide about HPV vaccine for sons, or had lower intention to vaccinate sons against HPV.

159

Measures
We assessed parents beliefs about VAI through proposing the following statement to parents: I worry about what the HPV vaccine will do to my sons fertility (ability to have children.) Response options included strongly agree, agree, disagree, strongly disagree, and prefer not to answer. We categorized responses into agree (strongly agree and agree) and disagree (disagree, strongly disagree, and prefer not to answer) for analyses. Prefer not to answer was categorized as disagree to bias results toward the null. We determined parent knowledge of HPV disease through 5 individual knowledge items pertaining to the role of HPV in genital warts, cervical cancer, anal cancer, penile cancer, and oropharyngeal cancer. We assessed knowledge of genital warts by proposing the following statement to parents HPV causes genital warts. We provided response options, including true, false, dont know, and prefer not to answer. We considered true to be the correct response and other responses were considered incorrect. We assessed knowledge of HPV-related cancers in the same way. We created a composite variable with 2 categories, high and low knowledge. Low knowledge was defined as 0 to 3 questions correct of 5, and high knowledge was defined as 4 to 5 questions correct of 5. We determined parents concern for side effects by proposing the following statement The HPV vaccine may cause unknown long-term side effects. We determined if parents had adequate information to decide about HPV vaccine for sons by proposing the statement I dont have enough information on the HPV vaccine to decide if my son should get it. For each of these items we offered 4 response options ranging from strongly agree to strongly disagree and also offered a prefer not to answer option. We dichotomized responses for analyses into agree (strongly agree and agree) and disagree (other possible responses). We determined parents intention to vaccinate sons by proposing the following question: How likely is your son to get the [HPV] vaccine next year? We offered response options including definitely will, probably will, probably wont, and definitely wont. We dichotomized responses for analyses into probably will (probably will and definitely will) and probably wont (probably wont and definitely wont).

Methods
We conducted a cross-sectional survey-based study in 2010 of parents with sons aged 9 to 21 years. The survey was created using constructs from the health belief model27 as well as themes that emerged from focus groups with both parents and young men. Recruitment took place at a general and multispecialty hospital-based pediatrics clinic. All parents had at least one son aged 9 to 21 years and surveys were available in English or Spanish. Research staff administered portions of the survey but parents completed most portions independently in the clinic. We offered participants a $20 gift card incentive to take part in the study. We asked parents to complete surveys based on their oldest son aged 9 to 17 years. If they did not have a son in this age range we requested that they complete the survey based on their oldest son aged 18 to 21 years. The Institutional Review Board at the University of North Carolina approved the study.

Analyses
Analyses excluded parents who reported sons had received any doses of HPV vaccine. We used descriptive statistics to determine the proportion of parents concerned about VAI. We used 2 tests and Fishers exact

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160 tests as appropriate to examine associations between parent and child demographics and beliefs in VAI. We compared parents who chose prefer not to answer for the VAI item with those who chose other responses using Fishers exact tests. We investigated the relationship between beliefs in VAI and each of the four outcomes using bivariate and multivariate logistic regression models. Multivariate models adjusted for parent demographics, including age, gender, race, ethnicity, education, marital status, and age of the index son. We performed supplemental analyses excluding all prefer not to answer responses. We used of .05 for all analyses.

Clinical Pediatrics 53(2) greater odds of agreeing they did not have enough information to decide about HPV vaccine compared to parents not worried about VAI (AOR = 2.22, 95% CI = 1.22-4.03). Approximately 63% of parents reported they would probably vaccinate sons against HPV next year. Parents worried about VAI had lower odds of intending to vaccinate sons compared to their counterparts, but this estimate was of borderline statistical significance (AOR = 0.56 95% CI = 0.32-1.01). Supplemental analyses showed that excluding prefer not to answer responses for the VAI item, as well as outcomes, yielded similar results for all outcomes (Table 4).

Results
A total of 290 parents participated in the survey, and excluding 20 parents of vaccinated sons yielded an analytic sample of 270. Approximately half of parents were older than 40 years. Most participants were female (79%) and self-identified as white (51%) or black (41%). The majority of parents were non-Hispanic. Approximately 60% of parents reported having college experience and an additional 14% reported graduate school experience. Most parents completed the survey based on a son aged 13 to 21 years (63%). Many parents (72%) reported they also had a daughter(s). Parent and child demographics were not significantly associated with worry about VAI (Table 1). Approximately 39% (106/270) of parents agreed they worried about VAI in sons (strongly agree 14% [38/270], agree 25% [68/270]). Remaining participants disagreed (38%, 102/270), strongly disagreed (9%, 25/270), or preferred not to answer (14%, 37/270) with regard to worry about VAI in sons. Choosing the prefer not to answer option was significantly associated with parent educational level but not other demographics; parents with less education appeared to choose prefer not to answer more often than parents with more education (Table 2). The distribution of responses for all outcome items is displayed in Table 3. Most parents (88%) had low knowledge of HPV disease. Parents worried about VAI did not differ significantly with respect to knowledge of HPV disease compared with parents not worried about VAI (adjusted odds ratio [AOR] high knowledge = 1.18, 95% confidence interval [CI] = 0.53-2.65). About 46% of parents agreed HPV vaccine may cause unknown, long-term side effects. Parents worried about VAI had approximately twice the odds of agreeing HPV vaccine may cause unknown long-term side effects compared with their counterparts (AOR = 2.29, 95% CI = 1.353.88). More than 70% of parents in our sample agreed they did not have enough information to decide about HPV vaccine for sons. Parents worried about VAI had

Discussion
To our knowledge, this is the first study dedicated to exploring parents concerns for infertility associated with HPV vaccine among males and investigating the consequences of such concerns. A surprising proportion of parents in our sample, almost 40%, agreed they were concerned about VAI in sons associated with HPV vaccine. The implications of this finding are not yet clear, but our results certainly demonstrate that the full range of parents concerns about HPV vaccine in boys, including the concern for VAI, is not well understood. Currently, little research exists that offers insight into reasons parent do or do not vaccinate sons. In one recent study parents often reported sons were unvaccinated because a provider had not recommended HPV vaccine, or they did not know HPV vaccine was available for sons.28 Conversely, concern for side effects was less often cited as a central reason for not vaccinating sons in that study.28 Our findings indicate, however, that the importance of parents concerns about potential side effects like VAI should still be considered seriously. Our estimate for intention to vaccinate among parents concerned about VAI, although not reaching statistical significance, may indicate some degree of hesitation to vaccinate among these parents. This finding, in conjunction with a relatively high prevalence of concern for VAI in our sample, is worrisome. In the setting of low vaccination rates in males, further study in other populations is warranted to determine if concerns for VAI in sons persist and if such concerns truly affect vaccine uptake. Parents concerned for VAI in our study, not surprisingly, had greater concern for unknown, long-term side effects of HPV vaccine than their counterparts who were not concerned about VAI. Likewise, those concerned about VAI often reported not having enough information to decide about HPV vaccine for sons. These findings may indicate a need for clearer parent education on the side-effect profile of HPV vaccine and reasons for use in

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Table 1. Sample Characteristics and Percentage of Parents Worried About Vaccine-Associated Infertility (VAI) by Demographics (n = 270). n Total Parent characteristics Age in years <40 40 Gender Male Female Race White Black Otherc Ethnicity Non-Hispanic Hispanic Educationd High school or less Any college Any graduate school Marital status Married Unmarriede Child characteristics Age in years, index son 9-10 11-12 13-21 Daughter No Yes
a b

161

No. Concerned About VAI

% Concerned About VAI

P .87a .67a .12b 1.00b .57a .10a .50a .82a

270

129 141 57 213 137 110 23 254 16 70 161 39 149 121

48 52 21 79 51 41 9 94 6 26 60 14 55 45

50 56 21 85 46 51 9 100 6 24 67 15 52 54

39 40 37 40 34 46 39 39 38 34 42 38 35 45

52 48 170 76 194

19 18 63 28 72

17 21 68 29 77

33 44 40 38 40

P value derived from 2 test. P value derived from Fishers exact test. c Other race includes multiracial (n = 9), other race and Latino/Hispanic (n = 8), Native American/Alaskan Native (n = 3), and other race unspecified (n = 2), missing (n = 1). d High school education or less category also includes GED. Any college education includes any college experience, bachelors degree, or associates degree. e Unmarried includes single, separated, divorced, or widowed.

males. Clinicians should ask parents if they have concerns about vaccinating sons, review the known potential side effects of HPV vaccine, clarify that infertility is not associated with vaccination, and inform parents that HPV vaccine has been studied with regard to safety specifically in males.14 When necessary, clinicians may also offer parents information about the commonality of side effects in both vaccine and placebo groups, as has been suggested previously; offering this information may help some parents evaluate the risks associated with HPV vaccine.29 Acknowledging that some parents have

voiced concern for VAI may also be useful in broadening the scope of conversations with parents and enable parents to more freely discuss other concerns. Open discussions with parents could be extremely important in situations where parents have not yet decided whether to vaccinate their children or not.29 Apart from discussions in the clinical setting, providers should realize that parents are likely to obtain information from, and be influenced by, a variety of sources when making vaccination decisions. Health care providers are certainly an important source of information for

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Clinical Pediatrics 53(2)

Table 2. Comparison of Parents Who Chose Prefer Not to Answer Versus Other Responses According to Demographics (n = 270). Parents Choosing Prefer Not to Answer, n (%) Total Parent characteristics Age in years <40 40 Gender Male Female Race White Black Otherb Ethnicity Non-Hispanic Hispanic Educationc High school or less Any college Any graduate school Marital status Married Unmarriedd Child characteristics Age in years, index son 9-10 11-12 13-21
a b

Pa 1.00 .83 .27 .25 .02 .15 1.00

37 (14)

18 (14) 19 (13) 7 (12) 30 (14) 15 (11) 17 (15) 5 (22) 33 (13) 4 (25) 17 (24) 17 (11) 3 (8) 16 (11) 21 (17)

7 (13) 6 (13) 24 (14)

P values obtained using Fishers exact test. Other race includes multiracial (n = 9), other race and Latino/Hispanic (n = 8), Native American/Alaskan Native (n = 3), other race unspecified (n = 2), and missing (n = 1). c High school education or less category also includes GED. Any college education includes any college experience, bachelors degree, or associates degree. d Unmarried includes single, separated, divorced, or widowed.

parents,30,31 but many parents may also obtain information from the Internet30 or seek input from their peers or family members.32,33 Although no studies are available that definitively show how parents become concerned about VAI, it is plausible that parents may hear myths about infertility or other vaccine-associated side effects from their peers or family members. Social influences have a role in vaccination decisions in general, and the importance of social norms has been observed with HPV vaccine for females.13,34 Perhaps peer influences also contribute to shaping parents beliefs about vaccine side effects, possibly even concerns about VAI in the setting of HPV vaccine. Concerns for VAI should be studied further particularly in different racial groups. In our sample almost half

of parents who self-identified as black reported concern for VAI in sons, more than parents who self-identified as white or those from other racial groups. Although differences between racial groups did not reach significance, the high proportion of black parents concerned about VAI (46%) is worrisome given the burden of HPV disease in blacks, including HPV disease in black men.5 This finding is also worrisome as black parents have been more likely than white parents to have concerns about vaccines and distrust providers.35 Likewise, concerns have been documented among blacks about obtaining medical care related to sexually transmitted infections.36 Globally, myths surrounding immunization have hindered vaccination efforts. Tetanus immunization was hindered in Mexico, the Philippines, and

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Schuler et al
Table 3. Response Distributions and Recategorizations for All Outcomes. Outcome Knowledge of human papillomavirus (HPV) disease (n = 270) HPV vaccine may cause unknown long-term side effects (n = 267) Not enough information on HPV vaccine to decide if son should get it (n = 270) Intention to vaccinate in next year (n = 246) Response Distribution Low knowledge High knowledge Prefer not to answer Strongly disagree Disagree Agree Strongly agree Prefer not to answer Strongly disagree Disagree Agree Strongly agree Definitely wont Probably wont Probably will Definitely will n (%) 238 (88) 32 (12) 57 (21) 6 (2) 80 (30) 95 (36) 29 (11) 9 (3) 8 (3) 58 (21) 92 (34) 103 (38) 19 (8) 73 (30) 118 (48) 36 (15) Recategorization Not applicable

163

n (%) 143 (54) 124 (46)

Disagree Agree Disagree Agree Probably wont Probably will

75 (28) 195 (72)

92 (37) 154 (63)

Table 4. Unadjusted and Adjusteda Odds Ratios (AOR) for Various Outcomes According to Beliefs in Human Papillomavirus (HPV) VaccineAssociated Infertility (VAI). Worried About VAI; OR (95% CI) 1.23 (0.59-2.60) 2.18 (1.32-3.59) 1.99 (1.11-3.54) 0.71 (0.42-1.20) Worried About VAIa; AOR (95% CI) 1.18 (0.53-2.65) 2.29 (1.35-3.88) 2.22 (1.22-4.03) 0.56 (0.32-1.01) Worried About VAI; Supplemental AORb (95% CI) 0.98 (0.43-2.23)c 2.58 (1.36-4.90)d 2.67 (1.40-5.10)e 0.56 (0.30-1.04)f

Outcome High knowledge of HPV disease (n = 270) Agree HPV vaccine may cause unknown long-term side effects (n = 267) Agree not enough information on HPV vaccine to decide if son should get it (n = 270) Probably will vaccinate (n = 246)
a b

Not Worried About VAI 1 1 1 1

Adjusted analyses account for parent age, gender, race, ethnicity, education, marital status, and age of the index son. Supplemental analyses exclude prefer not to answer responses. c Estimates based on reduced sample, n = 233. d Estimates based on reduced sample, n = 201. e Estimates based on reduced sample, n = 231. f Estimates based on reduced sample, n = 212.

Uganda by rumors that the vaccine was an antifertility vaccine.37 Since the vaccine protects against a sexually transmitted infection it may prompt sociocultural sensitivities more so than other vaccines.37,38 Parents concerns for VAI should also be studied more intensely in parents with less than a college education, among multiple racial groups, and in parents of Hispanic ethnicity. In our study, each of these subgroups had a surprising proportion of parents who chose the prefer not to answer response with regard to concerns for VAI in sons, and some parents may have chosen this

response if they were unsure about infertility in the context of HPV vaccine. Consequently, our estimates for the prevalence of concerns for VAI may not accurately reflect, and likely underestimate, the true prevalence of such concerns. Obtaining more accurate estimates regarding the concern for VAI in these groups may help direct efforts in parent education and could be important to help promote informed decision making about HPV vaccine for sons. This study has both strengths and limitations. Limitations of our study include recruitment of participants from one

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164 geographic area, the cross-sectional nature of our study, and the relatively low proportion of participants of Hispanic ethnicity. Strengths of our study include that it addressed a topic previously unexplored with respect to parents concerns for VAI in males and that it was conducted after licensure of HPV vaccine for males. It is important to note, however, that our study was conducted before the recommendation for routine male vaccination.

Clinical Pediatrics 53(2)

6. Centers for Disease Control, Prevention. FDA licensure of bivalent human papillomavirus vaccine (HPV2, Cervarix) for use in females and updated HPV vaccination recommendations from the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep. 2010;59:626-629. 7. Centers for Disease Control and Prevention. FDA licensure of quadrivalent human papillomavirus vaccine (HPV4, Gardasil) for use in males and guidance from the Advisory Committee on Immunization Practices (ACIP). MMWR Morb Mortal Wkly Rep. 2010;59:630-632. 8. Centers for Disease Control and Prevention. Recommendations on the use of quadrivalent human papillomavirus vaccine in malesAdvisory Committee on Immunization Practices (ACIP), 2011. MMWR Morb Mortal Wkly Rep. 2011;60:1705-1708. 9. Centers for Disease Control and Prevention. National and state vaccination coverage among adolescents aged 13-17 yearsUnited States, 2011. MMWR Morb Mortal Wkly Rep. 2012;61:671-677. 10. Reiter PL, McRee AL, Kadis JA, Brewer NT. HPV vac cine and adolescent males. Vaccine. 2011;29:5595-5602. 11. Liddon N, Hood J, Wynn BA, Markowitz LE. Acceptability of human papillomavirus vaccine for males: a review of the literature. J Adolesc Health. 2010;46:113123. 12. Brewer NT, Fazekas KI. Predictors of HPV vaccine acceptability: a theory-informed, systematic review. Prev Med. 2007;45:107-114. 13. Marlow LA, Waller J, Wardle J. Parental attitudes to pre pubertal HPV vaccination. Vaccine. 2007;25:1945-1952. 14. Highlights of prescribing information: Gardasil, no date, http://www.fda.gov/downloads/BiologicsBloodVaccines/ Vaccines/ApprovedProducts/UCM111263.pdf. Accessed February 7, 2013. 15. Slade BA, Leidel L, Vellozzi C, et al. Postlicensure safety surveillance for quadrivalent human papillomavirus recombinant vaccine. JAMA. 2009;302:750-757. 16. Schuler CL, Reiter PL, Smith JS, Brewer NT. Human papillomavirus vaccine and behavioural disinhibition. Sex Transm Infect. 2011;87:349-353. 17. Forster A, Wardle J, Stephenson J, Waller J. Passport to promiscuity or lifesaver: press coverage of HPV vaccination and risky sexual behavior. J Health Commun. 2010;15:205-217. 18. Watson M, Shaw D, Molchanoff L, McInnes C. Challenges, lessons learned and results following the implementation of a human papilloma virus school vaccination program in South Australia. Aust N Z J Public Health. 2009;33:365-370. 19. Bastani R, Glenn BA, Tsui J, et al. Understanding subop timal human papillomavirus vaccine uptake among ethnic minority girls. Cancer Epidemiol Biomarkers Prev. 2011;20:1463-1472. 20. Bingham A, Drake JK, LaMontagne DS. Sociocultural issues in the introduction of human papillomavirus vaccine in low-resource settings. Arch Pediatr Adolesc Med. 2009;163:455-461.

Conclusion
Our study demonstrates that, as Sturm et al29 suggested, conversations with families about vaccines are of great importance and that offering the vaccine information sheet to parents is not an adequate substitute for openended, candid discussions with parents. Clinicians should remain cognizant that vaccination decisions are likely multifactorial, are often complex, and that many parents may have misconceptions about HPV vaccine. Ensuring parents have accurate information may require concerted efforts to address known potential side effects and benefits of HPV vaccine while also dispelling myths, such as vaccine-associated infertility. Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding
The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: Tamera Coyne-Beasley received a Merck Investigator Initiated Research Grant.

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