Human Papillomavirus Knowledge, Vaccination Status, and Barriers to Vaccination in an Urban Transgender Clinic Population

Abstract

Introduction: This study aimed to better understand patient-reported human papillomavirus (HPV) vaccination rates and barriers to vaccination among transgender patients receiving care at a gender- affirming clinic in urban New York. Methods: All patients with arrived appointments at the Center for Transgender Care at Northwell Health from 1 January 2020 through 14 July 2021, aged 14 and up, were invited to participate. Participants were sent an online consent form followed by a survey that assessed HPV knowledge, personal vaccination history, and reasons for or against vaccination. Data were collected in RedCap and analyzed using descriptive and basic inferential statistics. We received 79 completed consent forms and 70 completed surveys. Results: At least 68 of the 70 participants identified as transgender or gender diverse. Only 61.4% (43/70) of participants reported ever being offered the HPV vaccine and 55.7% (39/70) reported ever receiving at least one dose. Common reasons in favor of vaccination included doctor recommendation and decreasing cancer risk. Common reasons mentioned against HPV vaccination included sexual inactivity, concern over side effects, and assumption of low-risk HPV status. Of unvaccinated participants, 58.1% (18/31) reported they were more likely to get vaccinated after completing the survey. Conclusions: The HPV vaccination rate in this study was higher than the rates seen in previous studies involving sexual and gender minority participants. Provider recommendation was found to be important in promoting vaccination.

Introduction

Human papillomavirus (HPV) is the most common sexually transmitted infection (STI) in the United States (US).[1] Approximately 85% of US individuals will acquire an HPV infection at some point in their lives.[1] HPV is spread during 1vaginal, anal, or oral sex or by close skin-to-skin touching during sex. The virus can cause benign genital warts as well as various cancers, including oropharyngeal, cervical, vulvar, vaginal, anal, and penile cancer. [1]

Vaccination against HPV became available in the US in 2006 in the form of a quadrivalent vaccine (HPV4).[2,3,4] This vaccine protected against HPV types 6 and 11 (responsible for 90% of genital warts) and 16 and 18 (responsible for most HPV-related cancers).[2,3,4] HPV4 was initially only approved for routine use in individuals assigned female sex at birth (AFAB).[3,5] In 2011, the recommendation was extended to include individuals assigned male sex at birth (AMAB), with the specific mention of men who have sex with men.[3,5] The nine-valent HPV vaccine (9vHPV or Gardasil 9) became available for individuals both AFAB and AMAB in 2015 and protects against HPV types 31, 33, 45, 52, and 58 in addition to the original four types 6, 11, 16, and 18.[6]

Since late 2016, 9vHPV has been the only HPV vaccine used in the US. [7] The recommendation by the Centers for Disease Control and Prevention (CDC) at this time was for routine HPV vaccination in all individuals, regardless of sex assigned at birth, at ages 11-12 years (or as young as 9 years), and for those ages 13-26 years who did not yet start or complete the vaccine series.[7] In 2019, the vaccine was approved for up to age 45 years.[8] The CDC Advisory Committee on Immunization Practices (ACIP) recommends shared decision-making on the benefits of vaccination for those ages 27-45 years.[8]

The efficacy of the HPV vaccine is well-established. The HPV vaccine has the potential to prevent greater than 90% of all cancers attributed to HPV.[7] Since it was first introduced to the public in 2006 for use in individuals AFAB only, there has been an 81-88% decrease in infection with HPV types that cause most cancers and genital warts among teens and young adults AFAB.[7] Despite its proven benefits, HPV vaccination rates among adolescents have lagged behind the rates of other vaccines routinely recommended for this age group.[3,9] In 2022 in the US, 76% of adolescents ages 13-17 years had received at least one dose of the HPV vaccine and 62.6% had completed the series.[9] For adults ages 18-26 years, only 47.4% reported receiving at least one dose of the vaccine.[10] An objective of Healthy People 2030 is to ‘increase the proportion of adolescents who get recommended doses of the HPV vaccine’.[11]

Transgender individuals were first mentioned as a special population for whom routine HPV vaccination was recommended in late 2016.[4] Transgender persons identify as a gender that is different from their assigned sex at birth. Women AMAB are known as transgender women or trans women. Men AFAB are known as transgender men or trans men. Individuals who identify outside of or who move between the gender binary may describe their identity as agender, non-binary, genderqueer, or genderfluid. These individuals are part of the gender minority and occasionally collectively referred to as gender diverse.

There are limited data on HPV vaccination rates and perspectives in lesbian, gay, and bisexual individuals, and even less data on the transgender population.[12] A 2022 integrative review of HPV vaccination among transgender and gender-diverse individuals in the US included only seven quantitative studies from 1985 to 2020 and all seven included cisgender participants as well.[12] Five of the seven studies had cisgender individuals making up more than 90% of the study population.[12] The transgender population is underrepresented in research overall.[12,13,14,15] Among all lesbian, gay, bisexual, and transgender (LGBT)-related projects funded by the National Institutes of Health (NIH) between 1989 and 2011, only 6.8% of them studied transgender individuals.[16]

There are high rates of stigma and numerous barriers to health care for transgender individuals.[17] Barriers include but are not limited to medical provider lack of knowledge and/or cultural sensitivity, negative attitudes towards the patient population, patient discomfort with medical examinations, patient discomfort with gendered services, outright discrimination or fear of discrimination, lack of insurance coverage, and outright denial of services.[14,17,18] These barriers lead to decreased usage of healthcare services, including preventive care such as vaccination.[12,17] This results in disproportionately poor health outcomes among transgender individuals, including high rates of HPV infection and HPV-associated cancers.[12,13,18,19]

Limited data reveal lower rates of HPV vaccination among transgender individuals when compared to their cisgender counterparts.[12,14,18,19] A survey of 155 college students belonging to a primarily LGBT organization at the University of South Florida reported an approximately 33% HPV vaccination rate.[20] Another study that surveyed young men who have sex with men and transgender women in Los Angeles and Chicago found that 14% of the responding population received one or more dose of the vaccine and less than 5% received three doses.[21] Most available literature examining the HPV vaccination rate and barriers to/facilitators of vaccination does not separate sexual minority and gender minority individuals when reporting results. This is a hindrance in better understanding the transgender community specifically and their healthcare experiences.

As stated by the authors of the integrative review of HPV vaccination among transgender and gender-diverse (TGD) individuals in the US, “[there is] a gap in the literature regarding HPV vaccination among TGD people”.[12] And, more importantly, “this dearth of knowledge is concerning as evidence suggests that TGD people have increased risk for HPV infection and HPV-associated cancer than cisgender people”.[12] It is for this reason that we outline the following objectives for this study (1) to assess baseline knowledge about HPV and the HPV vaccine in a transgender population; (2) to better understand the patient-reported barriers to HPV vaccination at the patient, provider, and system levels; (3) to explore how patient demographics correlate with reported HPV vaccination status; and (4) to compare the above findings in our Center for Transgender Care patient population to existing literature on other LGBTQI (lesbian, gay, bisexual, transgender, queer or questioning, intersex) populations.

Methods

Participants and procedures

This cross-sectional study was approved by the Northwell Health Institutional Review Board (IRB). All patients with arrived appointments at the Center for Transgender Care at Northwell Health from January 1, 2020 through July 14, 2021, aged 14 and up, regardless of sex assigned at birth or gender identity, were invited to participate. This totaled 529 patients. These patients were sent an email containing a link to an online consent form. Once consent was obtained, individuals were redirected to the online RedCap survey. Participants were told to anticipate 15 minutes for completion of the survey. After survey completion, they had the chance to enter their email address to win a $100 gift card. One winner was selected. A waiver of parental permission was granted by the Northwell IRB for patients less than 18 years old.

Survey instrument and measures

Participants were asked about their HPV knowledge, HPV vaccination history, reasons for or against vaccination, demographic information, and sexual history. Pertinent questions and responses from the survey are described here. Please refer to Supplementary Appendix SA1 for the full survey. HPV knowledge questions included, “Have you ever heard of HPV?” and “Which of the following types of cancer do you believe HPV can cause?” with the following answer choices: vulvar, vaginal, cervical, uterine, ovarian, penile, testicular, anal, mouth/throat, and none of the above. A subsequent true/false section of the survey included the following statements: “You can always tell when someone has HPV”, “HPV can cause abnormal Pap smears”, “HPV can cause herpes”, “HPV can cause genital warts”, “Most HPV infections clear on their own”, “The HPV vaccine protects against all HPV infections”, “Some typical symptoms of HPV include painful sores and discharge”, and “Only females can get vaccinated against HPV”.

The survey then assessed knowledge of the HPV vaccine and personal vaccination history. Questions in this section included, “Have you ever heard of the HPV vaccine?”, “Have you been offered the HPV vaccine before?”, and “Have you received at least one dose of the HPV vaccine?”.

Participant HPV vaccination perspectives were assessed using a 4-point Likert scale with response options: not at all, somewhat, moderately, and strongly. Participants were provided the following list of common reasons for vaccination and asked how strongly these attitudes influenced their decision about vaccination: “I wanted to decrease my risk for cancer”, “It was recommended by my doctor”, “It was recommended by my parent/guardian”, “It was recommended by a friend”, and “It was recommended by a sexual partner”.

The following list of common reasons against vaccination was provided and participants were again asked to select how strongly these attitudes influenced their decision about vaccination on the same 4-point Likert scale: “I was concerned about possible side effects”, “I do not believe in vaccination”, “I thought I had a low risk of getting HPV in my lifetime”, “I had already tested positive for HPV”, “I was afraid of the injection”, “I was hesitant for religious reasons”, “I wasn’t sexually active yet”, “I felt that my provider did not spend enough time discussing the vaccine with me”, “I did not want to talk about it with my parents/guardian because HPV is sexually transmitted”, and “My parent/guardian did not want me to get the vaccine”.

Demographic information was then collected, including gender identity, sex assigned at birth, and sexual identity. Participants were specifically asked, “How would you best describe your gender?” and provided the following response options: female, male, transgender female, transgender male, non-binary, other (text box provided), and choose not to answer. They were asked, “What was your assigned sex at birth?” and provided the following response options: male, female, and intersex. Lastly, participants were asked, “How would you describe your sexual identity?” and provided the following response options: bisexual, gay or lesbian, heterosexual, pansexual, queer, questioning or unsure, other (text box provided), and choose not to answer.

Finally, participants were asked to reflect on the survey. Using a 5-point Likert scale with response options of significantly more likely, somewhat more likely, unchanged, somewhat less likely, and significantly less likely, they were asked, “After completing the survey, how much more or less likely are you to receive the HPV vaccine?” Another 5-point Likert scale assessed patient comfort with answering survey questions.

Data analysis

Data were collected in RedCap and analyzed using descriptive and basic inferential statistics. There were 82 individuals who started the consent form, 79 who completed the consent form, and 69 who completed both the consent form and the survey. One participant left their survey status as “incomplete” upon submission but responded to every question except for reporting their age. Due to the small sample size overall, this individual’s survey was deemed complete, and 70 participants were included in analysis. Due to the wide age range of participants and the different HPV vaccines and recommended number of doses available over many years, patients who received at least one dose of the HPV vaccine were considered “vaccinated” for the purposes of this study. Those who had not received any doses were considered “unvaccinated”.

Results

There was a 13.2% (70/529) response rate. Participant demographics are listed in

Table 1. Participant demographics and human papillomavirus (HPV) vaccination status.

	Total n (%)	Vaccinated n (%)	Unvaccinated n (%)	p-value, χ2(df)
Race (n=70)				p=0.503 χ2(5)=4.330
Asian	5 (7.1)	1 (20.0)	4 (80.0)
Black/African	2 (2.9)	1 (50.0)	1 (50.0)
Caucasian	44 (62.9)	26 (59.1)	18 (40.9)
Hispanic/Latinx	6 (8.6)	3 (50.0)	3 (50.0)
Other	10 (14.3)	7 (70.0)	3 (30.0)
Choose not to answer	3 (4.3)	1 (33.3)	2 (66.7)
Religion (n=70)				p=0.748 χ2(8)=5.090
Agnostic	11 (15.7)	6 (54.6)	5 (45.4)
Buddhist	2 (2.9)	1 (50.0)	1 (50.0)
Catholic	3 (4.3)	2 (66.7)	1 (33.3)
Christian – other type not listed	5 (7.1)	3 (60.0)	2 (40.0)
Jewish	7 (10.0)	4 (57.1)	3 (42.9)
Protestant	2 (2.9)	0 (0.0)	2 (100)
Not religious	26 (37.1)	13 (50.0)	13 (50.0)
Other	8 (11.4)	5 (62.5)	3 (37.5)
Choose not to answer	6 (8.6)	5 (83.3)	1 (16.7)
Highest level of education (n=70)				p=0.233 χ2(4)=5.574
Grade school	3 (4.3)	1 (33.3)	2 (66.7)
High school	28 (40.0)	13 (46.4)	15 (53.6)
College	24 (34.3)	16 (66.7)	8 (33.3)
Graduate school	11 (15.7)	8 (72.7)	3 (27.3)
Choose not to answer	4 (5.7)	1 (25.0)	3 (75.0)
Annual household income (n=70)				p=0.165 χ2(6)=9.153
Less than $20,000	11 (15.7)	3 (27.3)	8 (72.7)
$20,000 to $34,999	4 (5.7)	3 (75.0)	1 (25.0)
$35,000 to $49,999	7 (10.0)	3 (42.9)	4 (57.1)
$50,000 to $74,999	8 (11.4)	6 (75.0)	2 (25.0)
$75,000 to $99,999	4 (5.7)	4 (100)	0 (0.0)
Over $100,000	17 (24.3)	9 (52.9)	8 (47.1)
Choose not to answer	19 (27.1)	11 (57.9)	8 (42.1)
Gender (n=70)				p=0.130 χ2(6)=9.884
Female	2 (2.9)	2 (100)	0 (0.0)
Male	5 (7.1)	4 (80.0)	1 (20.0)
Transgender female	18 (25.7)	7 (38.9)	11 (61.1)
Transgender male	31 (44.3)	19 (61.3)	12 (38.7)
Non-binary	10 (14.3)	6 (60.0)	4 (40.0)
Other	3 (4.3)	0 (0.0)	3 (100)
Choose not to answer	1 (1.5)	1 (100)	0 (0.0)
Sex assigned at birth (n=70)				p=0.144 χ2(2)=3.869
Male	23 (32.9)	11 (47.8)	12 (52.2)
Female	45 (64.3)	28 (62.2)	17 (37.8)
Intersex	2 (2.9)	0 (0.0)	2 (100)
Sexual identity (n=70)				p=0.422 χ2(7)=7.062
Bisexual	14 (20.0)	7 (50.0)	7 (50.0)
Gay or lesbian	8 (11.4)	5 (62.5)	3 (37.5)
Heterosexual	6 (8.6)	3 (50.0)	3 (50.0)
Pansexual	12 (17.1)	7 (58.3)	5 (41.7)
Queer	17 (24.3)	13 (76.5)	4 (23.5)
Questioning or unsure	2 (2.9)	1 (50.0)	1 (50.0)
Other	7 (10.0)	2 (28.6)	5 (71.4)
Choose not to answer	4 (5.7)	1 (25.0)	3 (75.0)

χ² – chi-square; df – degrees of freedom.

. The average participant age was 26.9 (range 16 to 50 years old). The population was composed of mostly Caucasian, non-religious, at least high school educated, high-income individuals. When describing their gender, 49 participants identified as transgender. Seven individuals identified as strictly male or female and, of them, only one person identified with the sex assigned to them at birth. Ten participants described themselves as non-binary. Three participants selected “other” and free-texted their identity with each of these falling outside of the gender binary. One participant selected “choose not to answer”. Thus, at least 68 of the 70 participants included in our study identified as a gender minority. The single participant who identified with their sex assigned at birth was included in the analysis as the Center for Transgender Care treats patients at all stages of the transitioning process.[22]

Participant HPV knowledge is outlined in

Table 2. HPV knowledge and HPV vaccination status.

	Total	Vaccinated	Unvaccinated	p-value, χ2(df)
	n (%)	n (%)	n (%)
Which types of cancer can HPV cause? (n=70)
Vulvar	38 (54.3)	21 (55.3)	17 (44.7)	p=0.934, χ2(1)=0.007
Vaginal	42 (60.0)	27 (64.3)	15 (35.7)	p=0.077, χ2(1)=3.127
Cervical	52 (74.3)	35 (67.3)	17 (32.7)	p=0.001, χ2(1)=11.016
Uterine	29 (41.4)	19 (65.5)	10 (34.5)	p=0.165, χ2(1)=1.928
Ovarian	27 (38.6)	19 (70.4)	8 (29.6)	p=0.050, χ2(1)=3.827
Penile	34 (48.6)	19 (55.9)	15 (44.1)	p=0.978, χ2(1)=0.001
Testicular	30 (42.8)	18 (60.0)	12 (40.0)	p=0.532, χ2(1)=0.391
Anal	38 (54.3)	24 (63.2)	14 (36.8)	p=0.172, χ2(1)=1.867
Mouth/throat	31 (44.3)	19 (61.3)	12 (38.7)	p=0.402, χ2(1)=0.701
None of the above	7 (10.0)	1 (14.3)	6 (85.7)	p=0.020, χ2(1)=5.410
Most HPV infections clear on their own (n=70)				**
True	4 (5.7)	3 (75.0)	1 (25.0)
False	44 (62.9)	20 (45.5)	24 (54.5)
Not sure	22 (31.4)	16 (72.7)	6 (27.3)
HPV can cause herpes (n=70)				p=0.938, χ2(2)=0.128
True	11 (15.7)	6 (54.6)	5 (45.4)
False	28 (40.0)	15 (53.6)	13 (46.4)
Not sure	31 (44.3)	18 (58.1)	13 (41.9)
Some typical symptoms of HPV include painful sores and discharge (n=70)				**
True	45 (64.3)	26 (57.8)	19 (42.2)
False	5 (7.1)	5 (100)	0 (0.0)
Not sure	20 (28.6)	8 (40.0)	12 (60.0)

^**Chi-square test may not be valid since 33% of cells have expected counts less than 5. HPV – human papillomavirus; χ² – chi-square; df – degrees of freedom.

. A total of 90.0% (63/70) of study participants had heard of HPV. Among multiple-choice options, cervical cancer was the most commonly recognized HPV-related cancer. It was also the only cancer type for which a statistically significant difference in correct identification was observed between vaccinated and unvaccinated participants. Of the 52 participants who correctly identified cervical cancer as HPV-related, 35 were vaccinated and 17 were unvaccinated (p=0.001, degrees of freedom (df)=1, chi-square=11.016). Less than half of participants recognized that HPV could cause vulvar, penile, and oropharyngeal cancer. There was no statistically significant difference in correct identification between vaccinated and unvaccinated participants for these three cancers.

A total of 72.9% (51/70) of study participants had heard of the HPV vaccine but only 61.4% (43/70) reported being offered the vaccine prior to completing the survey. Of the 70 participants, 39 (55.7%) reported ever receiving at least one dose of the HPV vaccine. There was no evidence supporting a statistically significant difference in vaccination status by demographics, as seen in Table 1.

Among participants who shared their HPV vaccination perspectives using the 4-point Likert scale, the most common reasons in favor of vaccination that factored into their decision making were as follows: “It was recommended by my doctor” (41/43, 95.3%) and “I wanted to decrease my risk for cancer” (38/43, 88.4%). Conversely, the most common reasons against vaccination were as follows: “I wasn’t sexually active yet” (22/43, 51.2%), “I was concerned about possible side effects” (16/43, 37.2%), and “I thought I had a low risk of getting HPV in my lifetime” (16/43, 37.2%).

Of unvaccinated participants, 58.1% (18/31) reported they were more likely to get vaccinated after completing the survey. The remainder of unvaccinated participants reported their likelihood of vaccination was unchanged. No participants reported being less likely to get vaccinated or complete their vaccine series. Notably, 94.3% (66/70) of participants felt comfortable or neutral taking the survey. There was no difference in comfort level based on HPV vaccination status at the time of survey completion (p=0.729, df=3, chi-square=1.301).

Discussion

Our data provide insight into the knowledge of HPV and the HPV vaccine as well as vaccination status in a largely transgender population. More than half of study participants (39/70, 55.7%) received at least one dose of the HPV vaccine. This is below the 76% HPV vaccination rate of US adolescents (ages 13-17) but similar to the 47.4% vaccination rate of young adults (ages 18-26) in the US overall.[9,10] This is also higher than the previously discussed 14-33% rate of HPV vaccination in existing studies that focus on gender and sexual minority participants.[20,21]

We must consider, however, whether the HPV vaccination rates from our survey can be extrapolated to represent other transgender and gender-diverse populations. Our sample is made up of mostly white, college-educated, high-income patients who have already established care at a gender-affirming healthcare facility. Given known barriers to care among the transgender population, such as patient lack of insurance coverage and provider lack of knowledge or cultural sensitivity, it may be reasonable to conclude that our rate of vaccination is higher than what may be seen in the transgender community. Future research could examine participants’ perceived provider cultural competence and medical and/or institutional trust, as these may largely affect vaccination rates.

A prospective study of HPV vaccination rates in two Northwell Health Obstetrics and Gynecology clinics in the same geographic location as our study reveals an HPV vaccination rate of 38.1%.[23] The participants in this study were also most commonly white (39.8%) and at least high school educated (92.9%), but their gender and sexual identities are not known.[23] Although both studies include individuals from the same healthcare system and geographic region, there are enough population differences to alter the HPV vaccination rate, with a higher rate among participants from the Center for Transgender Care.[23] Given previous literature revealing lower HPV vaccination rates among transgender individuals when compared to their cisgender counterparts, this finding may also speak to the importance of gender-affirming care in increasing vaccination rates in this population.12,14,18,19

The most common reason against HPV vaccination among study participants was that they were not yet sexually active. The most common reason in favor of vaccination was recommendation by a doctor. Similarly, a study of more than 900 adults in Texas in 2018 found that lack of knowledge of the HPV vaccine and lack of provider recommendation were the most common reasons against vaccination.[24] This highlights the importance of provider recommendation of the HPV vaccine.

A strength of our study is that it adds to the limited body of research focusing on the transgender community. This study sought to capture perspectives and opinions of transgender individuals specifically. Transgender and gender-diverse participants make up at least 97.1% (68/70) of our study population. An objective of Healthy People 2030 is to improve the health of the LGBT population through increasing data collection on these individuals’ health and well-being.[25] This study seeks to do exactly that. Another strength of this study is that individuals overwhelmingly felt comfortable or neutral participating in the survey and that participation alone was enough to increase willingness to get vaccinated or complete the series.

Our study is limited by self-selection bias introduced by the nature of a voluntary survey. It is also limited by a low response rate and, therefore, a small sample size. This could be due to the sensitive nature of survey content or the fact that the survey was possibly confusing or time consuming. Piloting the survey could have helped improve response rates. Another limitation of this study is that the participants are mostly white, college-educated, and high-income, and that they are already receiving care at a gender-affirming clinic. This limits the generalizability of our findings. We also did not confirm patient HPV vaccination status or number of doses received via medical records. Therefore, recall bias may have affected our results. Lastly, we did not follow-up to see if participant self-reported intentions to get vaccinated or complete the series were achieved. A follow-up study could be performed using medical records to a) confirm HPV vaccine status at the time of survey completion and b) identify changes in HPV vaccination rates following survey completion.

Conclusions

Our data suggest that HPV vaccination rates among a transgender clinic population are higher than HPV vaccination rates seen in previous studies involving sexual and gender minority participants. Importantly, these findings must be interpreted in the context of a voluntary survey and a mostly white, college-educated group of participants who have already established care at a gender-affirming clinic. This study highlights the importance of provider recommendation in increasing vaccination rates. If may also emphasize the importance of a gender-affirming healthcare center in increasing vaccination rates, which is an area of potential further study. Most importantly, this study works towards two Healthy People 2030 objectives by contributing to the body of research on the transgender population and working to increase HPV vaccination among adolescents.