Edited by: Patricia Matthews-Juarez, Meharry Medical College, United States
Reviewed by: Jiping Yue, University of Chicago, United States; Martha Jane Felini, University of North Texas Health Science Center, United States
This article was submitted to Cancer Epidemiology and Prevention, a section of the journal Frontiers in Oncology
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Human papillomavirus (HPV) is the most common sexually transmitted infection worldwide (
Because of their increased risk for developing cervical cancer, HIV-positive women are screened more regularly than HIV-negative women (at least until a history of three consecutive normal Pap test results has been established) (
Data from HPV vaccine clinical trials supports the benefits of HPV vaccination among at-risk populations disproportionately affected by HPV-related diseases and cancers, such as HIV-positive women and MSM, in light of minimal risks (e.g., adverse events such as syncope) and decreased effectiveness for those already exposed to some HPV types. Yet, HPV vaccine coverage remains suboptimal among MSM (
Increasing HPV vaccination coverage and adherence to cervical cancer screening guidelines are both
In May-June 2016, 30 staff were recruited from three ASOs located in the South US Census region. The principal investigator (LTW) emailed a description of the research study to leaders at four ASOs located in South Carolina (SC). The three ASO leaders that responded were asked to invite eligible staff to participate. Eligibility criteria included being an employee, volunteer, or community partner who provided HIV/sexually transmitted disease (STD) risk-reduction counseling to PLWH or high-risk HIV-negative men (including MSM) or women.
The HINTS is a population-based mail survey that was used to obtain a subsample of respondents that resided in the same U.S. Census Region (South) and Division (South Atlantic) as our study participants (
Participants in our ASO study completed a 30-min, self-administered, 118-item paper and pencil survey that included questions about HPV and HPV vaccine awareness, knowledge, and attitudes/beliefs drawn heavily from the HINTs survey. For this analysis, we are only focusing on these domains (i.e., awareness, knowledge, and attitudes/beliefs). The principal investigator (LTW) conducted the survey in a group setting and was able to provide oversight to ensure that the respondents did not get help answering the knowledge questions from either from the Internet or their colleagues.
Both samples were asked if they had ever heard of HPV and the HPV vaccine. We used an adapted version of the HINTS HPV vaccine awareness question to ask our ASO sample if they had heard of specific HPV vaccines (i.e., Cervarix®, Gardasil®, Gardasil-9®) and cancer screening tests (i.e., anal Pap test, HPV test). Response options were yes/no.
Both samples were asked about knowledge that HPV can cause anal, cervical, oral, and penile cancers; is a sexually transmitted disease; and will usually clear (i.e., go away on its own without treatment). We used an adapted version of the HPV knowledge question to assess the ASO sample's knowledge that HPV causes more health problems for PLWH and other types of cancers (i.e., vaginal, vulvar). Questions from older HINTS iterations and existing surveys were adapted to assess the ASO sample's HPV vaccine knowledge about the following: main purpose is to prevent HPV infection, 3-doses recommended for females and males (including PLWH) through 26 years old, not recommended for persons older than 26 years old, cervical cancer screening is still needed (
In both samples, beliefs about the HPV vaccine's cervical cancer prevention effectiveness was assessed. We adapted the HINTS HPV vaccine effectiveness question to include other HPV-related cancers (i.e., anal, oral, penile, vaginal, and vulvar). A similar question from an older HINTS iteration was used to assess ASO staff's beliefs that the Pap test was effective at detecting cervical cancer in its earliest stages when treatment is more effective. Response options were: not at all successful, a little successful, pretty successful, very successful, and don't know. We dichotomized this variable as successful or not at all successful/don't know.
We also adapted the HINTS question about cervical cancer being preventable to include other HPV-related cancers (i.e., anal, oral, penile, vaginal, and vulvar). ASO staff who worked with female clients were asked how much they agreed/disagreed that anal, cervical, oral, vaginal, and vulvar cancers were preventable. Similarly, ASO staff who worked with MSM clients were asked if anal, oral, and penile cancers were preventable. Response options were: strongly agree, agree, disagree, strongly disagree: We dichotomized these questions as agree or disagree.
We used a single item to assess ASO staff's perceptions of barriers that their clients might encounter when trying to access the HPV vaccine, cervical cancer screening tests (i.e., Pap test, HPV test), and/or follow-up treatment or diagnostic tests if their Pap test result was unclear or abnormal. Response options included patient (i.e., childcare), provider (i.e., HIV stigma, HPV stigma), and system-level (i.e., clinic hours, cost, health insurance, transportation, travel distance) barriers. An open-ended response option was used to assess other barriers.
Stata/SE 14.2 (College Station, Texas, USA) was used to perform all data analyses. We restricted our HINTS data analyses to the subpopulation of US adults who lived in the South Atlantic division of the South US Census division and had no missing observations for any of our covariates (H4C4:
ASO staff were younger (mean age: 47.7 ± 12.5 years; H4C4: 49.5 ± 15.7,
Characteristics of ASO staff compared to US adults
Age, years | 47.7 ± 12.5 |
49.5 ± 15.7 |
50.8 ± 15.3 |
≥50 | 12 (43) | 192 (53) |
173 (54) |
Male | 16 (53) | 116 (32) |
108 (33) |
Non-Hispanic Black or African American | 25 (83) | 97 (27) |
61 (19) |
Married | 11 (37) | 195 (53) |
198 (61) |
College graduate or more | 23 (77) | 212 (58) |
200 (62) |
≥50,000 | 12 (40) | 224 (61) |
212 (66) |
Heard of HPV | 30 (100) | 365 (100) |
323 (100) |
Heard of the HPV vaccine | 23 (77) | 316 (87) |
278 (86) |
HPV can cause anal cancer | 20 (67) | 100 (27) |
113 (35) |
…cervical cancer | 30 (100) | 293 (80) |
271 (84) |
…oral cancer | 11 (38) | 118 (32) |
122 (38) |
…penile cancer | 17 (59) | 110 (30) |
126 (39) |
…vaginal cancer | 25 (83) | – | – |
…vulvar cancer | 14 (48) | – | – |
HPV is a sexually transmitted disease | 24 (80) | 235 (64) |
231 (72) |
HPV will usually go away on its own | 24 (80) | 33 (9) |
32 (10) |
HPV vaccine can prevent anal cancer | 10 (33) | – | – |
…cervical cancer | 14 (47) | 147 (40) |
137 (43) |
…oral cancer | 11 (48) | – | – |
…penile cancer | 9 (30) | – | – |
…vaginal cancer | 11 (48) | – | – |
…vulvar cancer | 11 (48) | – | – |
Other characteristics of ASO staff (
#Years worked with PLWH | 11.4 ± 7.7 |
#Years worked at ASO ( |
8.5 ± 7.1 |
#Clients served, total ( |
89.0 ± 85.2 |
Heterosexual, female | 12 (40) |
Heterosexual, male | 6 (20) |
Lesbian or gay | 12 (40) |
Employed full time at ASO | 23 (76) |
Worked with HIV-positive women (or HIV-negative women engaging in HIV risk behaviors) |
28 (93) |
Worked with MSM (HIV-positive and HIV-negative) | 29 (97) |
Worked with clients ≤ 26 years old | 23 (100) |
Clients have talked to them about the HPV vaccine | 7 (30) |
Worked with clients who had initiated the 3-dose HPV vaccine series | 7 (30) |
Worked with clients who had completed the 3-dose HPV vaccine series | 4 (17) |
Worked with clients who had been diagnosed with an HPV-related disease or cancer | 18 (60) |
Heard of Cervarix® | 12 (52) |
… Gardasil® | 8 (35) |
… Gardasil-9® | 18 (78) |
Heard of the HPV test | 24 (80) |
Heard of an anal Pap test | 19 (66) |
HPV causes more health problems for PLWH | 24 (80) |
Main purpose of the HPV vaccine is to prevent HPV infection | 19 (83) |
Three doses of the HPV vaccine are recommended |
9 (39) |
HPV vaccine is recommended for females and males ≤ 26 years old | 19 (83) |
HPV vaccine is recommended for PLWH 9-26 years old | 16 (70) |
HPV vaccine is not recommended for people >26 years old | 6 (26) |
Females who have gotten the HPV vaccine still need to get screened for cervical cancer | 21 (91) |
HPV vaccine is safe | 12 (52) |
HPV vaccine is effective | 10 (43) |
Pap test can detect cervical cancer in its earliest stages | 26 (87) |
There's not much a woman can do to lower her chances of getting anal cancer | 1 (3) |
… cervical cancer | 1 (3) |
… oral cancer | 2 (7) |
… vaginal cancer | 13 (43) |
… vulvar cancer | 1 (3) |
There's not much a man can do to lower his chances of getting anal cancer | 1 (3) |
… oral cancer | 1 (3) |
… penile cancer | 13 (45) |
Childcare | 8 (27) |
HPV stigma | 19 (63) |
HIV stigma | 8 (27) |
Clinic hours | 23 (77) |
Cost | 18 (60) |
Health insurance | 15 (50) |
Transportation | 15 (50) |
Travel distance | 14 (47) |
Other | 10 (33) |
In the ASO staff and both HINTS samples, all had heard of HPV. Compared to US adults residing in the South Atlantic division, all ASO staff knew that HPV can cause cervical cancer (H4C4: 80%,
A smaller percentage (77%) of ASO staff (
Almost all ASO staff (91%) knew that vaccinated females still needed to be screened for cervical cancer. The HINTS 3 (2008) iteration is the last time that this survey question was assessed. Comparatively 94% of US adults at that time knew that vaccinated females still needed to be screened for cervical cancer (
Compared to US adults residing in the South Atlantic region (H4C4: 85%; H5C1: 83%), 77% of ASO staff had heard of the HPV vaccine. Almost half (47%) of ASO staff thought that the HPV vaccine can prevent cervical cancer, which was a statistically significant higher than the proportion of US adults residing in the South Atlantic region (H4C4: 40%,
All ASO staff were willing to encourage their female and MSM clients to talk to their healthcare providers about the HPV vaccine. A larger percentage of ASO staff who worked with MSM clients (95%) were willing to encourage these males to get the HPV vaccine, compared to ASO staff who worked with female clients (91%;
ASO staff's attitudes toward human papillomavirus (HPV) vaccine | Notes:
Eighty-seven percent of ASO staff thought the Pap test was effective at detecting cervical cancer in its earliest stages. (Table
All ASO staff who worked with female clients were willing to ask these females when did they had their most recent Pap test, encourage unscreened/underscreened females to talk to their health care provider about getting a Pap test, and if applicable, also encourage these females to follow up with their health care provider if abnormal follow-up care was needed. Almost all ASO staff who worked with female clients were willing to ask them if their most recent Pap test result was normal, unclear, or abnormal (96%), and were also willing to help these females better understand their Pap test results (93%; Table
Attitudes towards cervical cancer screening among 28 ASO staff who worked with HIV-positive (or at-risk HIV-negative) female clients.
Pap test | |
Willing to ask female clients, |
28 (100) |
27 (96) | |
Willing to encourage unscreened/underscreened female clients to talk to their health care provider about getting a Pap test | 28 (100) |
Willing to help female clients better understand their Pap test results | 26 (93) |
Willing to encourage females clients to follow up with their health care provider if abnormal follow-up care was needed | 28 (100) |
Willing to encourage their female clients to talk to their health care provider about getting an HPV test if applicable | 28 (100) |
Willing to help female clients find free or low-cost cervical cancer screening tests (i.e., Pap test, HPV DNA test) | 27 (96) |
Most ASO staff had heard of the HPV DNA test (80%; Table
Many ASO staff had heard of the anal Pap test (66%; Table
ASO staff's attitudes toward anal Pap test|Notes:
Only 27% of ASO staff identified childcare as a barrier for their clients. While 63% thought HPV stigma was a barrier, only 27% thought HIV stigma was a barrier for their clients. Beyond HPV stigma, most of the barriers were related to healthcare access and included the following: 77% clinic hours, 60% cost, 50% health insurance, 50% transportation, 47% travel distance. An open-ended response options was included to capture other barriers, of which 33% of ASO staff identified: “
Community-based ASOs provide PLWH, MSM, and other vulnerable populations with valuable resources such as health education, patient navigation, and social support. Some of the ASO staff that we recruited for our research study had high levels of awareness and knowledge about HPV and some effective HPV-related cancer prevention (i.e., HPV vaccination) and screening (i.e., HPV test) tools. This may be attributed to the disproportionate burden of HPV-related diseases and cancers among their clients. That said, the lower level of awareness about the anal Pap test raised some concern given the high proportion of ASO staff that participated in our research study who work with MSM clients and the high burden of anal diseases and cancers among MSM (which is further exacerbated by HIV infection). ASO staff's lack of knowledge about anal Pap tests could be attributed (at least in part) to the fact that in contrast to cervical cancer, there are no recommended screening guidelines for anal cancer. However, the general sense is that for high-risk populations such as MSM (and especially HIV-positive MSM), the potential for improving HPV-related cancer outcomes outweigh the potential harm. In this regard, the potential for ASO staff to help their clients overcome barriers and enable them to make informed (or at a minimum shared) decisions about cancer screening with their health care providers becomes increasingly important (
Although some ASO staff may not share the same positive attitudes and beliefs about HPV vaccination and anal and/or cervical cancer screening, almost all of the ASO staff in our research study were willing to promote patient-provider communication and provide patient navigation support to their clients. Studies have shown that ASO clients' health outcomes are positively associated with how effectively ASOs can integrate various services (
This study is one of only a few that have compared the US population-based HINTS sample to a special subpopulation of US adults (
The main limitation of our study is its small sample size. However, it should be noted that our study was a sample of provider-level participants, and not a population-level sample. Further, our sample of provider-level participants served a vulnerable subgroup of the population (i.e., PLWH, MSM, and other vulnerable populations). Although we were able to ask more specific questions, this limited our ability to make additional comparisons between our sample and the HINTS sample. Our study findings may not be generalizable to other ASO staff in other locales. Another limitation is that we did not assess gay stigma as a potential healthcare access barrier.
HPV vaccination can reduce the burden of HPV vaccine preventable diseases and cancers. Future research to assess what ASO staff's beliefs are about the HPV vaccine specifically for special populations such as PLWH and MSM is warranted, especially since most knew that the HPV vaccine was recommended for PLWH, but only about half (or fewer) thought that the HPV vaccine was safe and effective. Similarly, early detection of precancerous cells can improve health outcomes. Because ASO play an important role in improving health outcomes for their clients (
Data collection activities for this research study were carried out in accordance with the recommendations of the University of South Carolina's Office of Research Compliance with verbal informed consent from all subjects that participated in our needs assessment survey. All participants gave verbal informed consent in accordance with the Declaration of Helsinki. The protocol was approved by the institutional review board of the University of South Carolina's Office of Research Compliance.
LW conceptualized the research project and HB (along with LW's other K01 mentors contributed to the study design). LW conducted the literature review that informed the development of the survey, which LW developed and HB and SB contributed to expert review and content validity. LW conducted the research study (which included all aspects of data acquisition). LW lead data analysis with assistance from NS. All authors (LW, SB, NS, HB, and MO) have all contributed to the interpretation of the findings. LW provided the initial draft of the findings, and all authors (LW, SB, NS, HB, and MO) assisted with revising subsequent drafts for important intellectual content. All authors (LW, SB, NS, HB, and MO) read and provided approval for publication of the final draft of the manuscript that was submitted. LW along with her K01 mentors (HB and MO) agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work were appropriately investigated and resolved.
HB was and still is a member of the United States HPV Advisory Board of Merck. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors are grateful to the organizational leaders, staff, volunteers, and community partners at AID Upstate, the Joseph H. Neal Wellness Center, and Palmetto AIDS Life Support Services for their willingness to participate in and valuable contributions made to our research study. We are also grateful to Dr. Richard P. Moser (Training Director and Research Methods Coordinator, Behavioral Research Program, Office of the Associate Director, Division of Cancer Control and Population Sciences, National Cancer Institute) for his time and valuable input on the data analysis of the HINTS sample that was included in this research study.