‘Does human papillomavirus (HPV) cause cancer?’ – A cross-sectional study of HPV awareness among sexual minority men in Nigeria
Connor R. Volpi
A , John Chama B , Natalia Blanco C , Ruxton Adebiyi B , Kareshma Mohanty D , Ayuba Doroh B , Jumoke A. Aigoro B , Christiana Katu B , Uche Ononaku B , John Maigida B , Abayomi Aka E , Ashley Shutt C , Patrick Dakum B , Man Charurat C , Sylvia Adebajo B C and Rebecca G. Nowak C *
A
B
C
D
E
Abstract
Human papillomavirus (HPV)-associated cancers are a global concern, particularly for sexual minority men (SMM). Understanding awareness and the determinants of these beliefs is crucial for developing educational programs to reduce HPV-associated cancers. This study explored awareness and determinants of beliefs about HPV’s carcinogenicity among SMM living with and without HIV in Nigeria.
Participants were recruited through secure social media platforms in Abuja, Nigeria. REDCap surveys captured demographics, sexual practices and participants’ beliefs regarding HPV’s role in cancer. Multivariable logistic regression modeling was used to estimate adjusted odds ratios (aOR) and 95% confidence intervals (CI) for the relationships between individual characteristics and belief levels stratified by those living with and without HIV.
Of 982 participants, the median age was 29 years (interquartile range: 26–34); 64.1% were living with HIV, and 9.7% believed HPV causes cancer. Awareness was highest for anal (82.1%) and penile cancers (15.8%) and less so for oropharyngeal and female HPV-associated cancers (range: 3–7%). Anogenital warts increased the odds of awareness for SMM living with HIV (aOR: 6.4, CI: 3.0–13.6) and for individuals without HIV (aOR: 4.8, CI: 1.6–14.2). Living with HIV for over 6 years was independently associated with a two-fold increased knowledge about HPV’s carcinogenicity (aOR: 2.1, CI: 1.1–4.1).
Awareness of HPV’s carcinogenicity was low; however, those who were aware were more likely to identify male HPV-associated cancers relevant to their own cancer risk. Formalizing targeted education in HIV care settings may promote knowledge and advocacy for prevention strategies.
Keywords: cancer, health literacy, HIV, HPV vaccine, human papillomavirus, lower- and middle-income countries, MSM, SSA.
Introduction
Cancers associated with human papillomavirus (HPV) are emerging as a significant global public health concern given their increasing prevalence and impact on morbidity and mortality worldwide.1 Anal cancer, specifically, has been of interest given its increase in incidence,2 with recent work highlighting upward trends in mortality.3 However, mortality trends have seldom included data from lower- and middle-income countries (LMIC),4 which possess fewer resources to prevent such cancers and are suspected of having an increasing prevalence of HPV-associated cancers.1
As the most populous country in Africa, Nigeria represents an important LMIC in which to examine this issue. Nigerian sexual minority men (SMM) living with HIV have an 86% prevalence of anal high-risk (hr)-HPV,5,6 compared with the worldwide estimate of 74%.7 High prevalences of anal hr-HPV,7,8 both within SMM living with HIV and in the broader population,9 combined with the hesitancy to access healthcare services because of anti-homosexuality laws may contribute to future trends in cancer morbidity and mortality.10 Moreover, a recent cross-sectional study across six states in Nigeria highlighted low levels of knowledge about HPV.11 Understanding the levels of awareness and the determinants of these beliefs is crucial for developing targeted educational programs on prevention strategies,12,13 especially given the growing risk of HPV-associated cancers.
The objective of this study, therefore, is to assess awareness of HPV and its causal link to cancer among Nigerian SMM living with and without HIV. We will explore independent demographic and clinical factors associated with individuals who believe HPV causes cancer.
Methods
Study design and population
For this cross-sectional study, participants were recruited by community outreach efforts and announcements made on secure social media platforms catering to SMM from 4 July to 18 October 2023 in Abuja, Nigeria. Eligibility criteria included aged ≥18 years, assigned male sex at birth, having engaged in anal and oral intercourse with another male partner, and provided informed consent. Participant data were collected via trained interviewers using REDCap electronic surveys, and participants were compensated for transport and time with 3000 Naira (approximately USD3.50).14
Statistical analyses
Our primary outcome was participants’ responses to the question, ‘Does HPV cause cancer?’, dichotomized as ‘Yes’ or ‘No/Unsure’. The following variables were dichotomized as ‘Yes or No’: prior engagement with the clinic, living with HIV, knowledge of cancers caused by HPV, history of anogenital warts, and oral sex in the past 6 months. Binary variables included age, split at the median as 18–30 or >30 years; gender, split as male or other; and years living with HIV, split as <6 or ≥6 years. A priori independent risk factors for knowledge of HPV’s oncogenicity were resident state (FCT or outside of FCT), preferred sexual position (top, bottom, and versatile), antiretroviral (ART) adherence (reported taking <95% of pills classified as not very good, ≥95% of pills as very good), and smoking status (never, former, and current).
Descriptive analyses examined covariate distributions using Pearson χ2 or Fisher’s exact tests. Logistic regression estimated unadjusted and adjusted odds ratios (aOR) with 95% confidence intervals (CIs), separately for SMM living with and without HIV. Noncollinear variables that were statistically significant in bivariate analysis (P < 0.05) and changed the beta coefficients by more than 10% were retained in the final models. All statistical analyses were performed using STATA 16 (College Station, TX, USA).
Ethics approval
This study was reviewed and approved by the Federal Capital Territory (FCT) Health Research Ethics Committee (FHREC/2023/01/109/27-06-23) and the University of Maryland Baltimore IRB (HP-00106266). All participants provided a summary of their comprehension of the study before providing written informed consent.
Results
Of the 982 participants enrolled, 59% were 18–30 years of age, 64% were living with HIV, and of those with HIV, 82% were adherent to their antiretroviral therapy (ART). Sixty-four percent engaged in receptive anal intercourse, and 69% had engaged in oral sex in the past 6 months. Only 10% positively confirmed that HPV causes cancer. SMM who were >30 years of age (15% vs 6%; P < 0.01) and those who had a history of anogenital warts (37% vs 9%; P < 0.01) believed HPV causes cancer. However, level of knowledge about HPV’s oncogenicity was similar regardless of HIV status (both 10%; P = 0.97). Among SMM living with HIV, those living with HIV for ≥6 years were more likely to believe that HPV causes cancer than those living with HIV for <6 years (15% vs 6%, P < 0.01) (Table 1).
| Characteristics | Total (n = 982) | Does HPV cause cancer? | P-valueA | ||
|---|---|---|---|---|---|
| No/unsure (n = 887) | Yes (n = 95) | ||||
| n (col %) | n (row %) | n (row %) | |||
| Age (years) | <0.01 | ||||
| 18–30 | 575 (58.5) | 539 (93.7) | 36 (6.3) | ||
| >30 | 407 (41.5) | 348 (85.5) | 59 (14.5) | ||
| Gender | 0.20 | ||||
| Male | 972 (99.1) | 879 (90.4) | 93 (9.6) | ||
| Other | 9 (0.9) | 7 (77.8) | 2 (22.2) | ||
| Resident state | 0.03 | ||||
| Federal Capital Territory (Abuja) | 847 (86.2) | 772 (91.2) | 75 (8.8) | ||
| Outside of Federal Capital Territory | 135 (13.8) | 115 (85.2) | 20 (14.8) | ||
| Preferred sexual position | 0.23 | ||||
| Top | 355 (36.3) | 324 (91.3) | 31 (8.7) | ||
| Bottom | 283 (28.9) | 258 (91.2) | 25 (8.8) | ||
| Versatile | 340 (34.8) | 301 (88.5) | 39 (11.5) | ||
| Oral sex in the past 6 months? | 0.03 | ||||
| No | 245 (26.2) | 46 (95.8) | 2 (4.2) | ||
| Yes | 644 (68.7) | 234 (95.5) | 11 (4.5) | ||
| Don’t know | 48 (5.1) | 564 (87.6) | 80 (12.4) | ||
| Receive care at TRUST? | 0.56 | ||||
| No | 856 (87.2) | 775 (90.5) | 91 (9.5) | ||
| Yes | 126 (12.8) | 112 (88.9) | 14 (11.1) | ||
| Living with HIV | 0.97 | ||||
| No | 341 (34.7) | 307 (90.0) | 34 (10.0) | ||
| Yes | 629 (64.1) | 569 (90.5) | 60 (9.5) | ||
| Don’t know | 12 (1.2) | 11 (91.7) | 1 (8.3) | ||
| Years living with HIVB | <0.01 | ||||
| <6 | 374 (59.5) | 353 (94.4) | 21 (5.6) | ||
| ≥6 | 255 (40.5) | 216 (84.7) | 39 (15.3) | ||
| Self-categorized antiretroviral adherenceC | 0.52 | ||||
| Not very good | 76 (12.5) | 67 (88.2) | 9 (11.8) | ||
| Very good | 500 (82.1) | 451 (90.2) | 49 (9.8) | ||
| Don’t know | 33 (5.4) | 31 (93.9) | 2 (6.1) | ||
| Smoking status?D | 0.71 | ||||
| Never | 344 (35.3) | 310 (90.1) | 34 (9.9) | ||
| Former | 252 (25.9) | 232 (92.1) | 20 (7.9) | ||
| Current | 375 (38.5) | 335 (89.3) | 40 (10.7) | ||
| Don’t know | 3 (0.3) | 2 (66.7) | 1 (33.3) | ||
| History of anogenital warts?E | <0.01 | ||||
| No | 829 (93.4) | 758 (91.4) | 71 (8.6) | ||
| Yes | 59 (6.6) | 37 (62.7) | 22 (37.3) | ||
TRUST, a SMM-community based HIV care clinic.
When asked which cancers were caused by HPV, among those knowledgeable about the link to cancer (n = 95), SMM were more likely to report that HPV caused anal cancer (82%) or penile cancer (16%). They were less likely to associate HPV with oropharyngeal (3%), cervical (7%), vaginal (6%) or vulvar (0%) cancers (Table 2).
| HPV-specific cancers | Does HPV cause cancer? | P-valueA | ||
|---|---|---|---|---|
| No/unsure (n = 887) | Yes (n = 95) | |||
| n (col %) | n (col %) | |||
| Cervical cancer? | <0.01 | |||
| No | 887 (100.0) | 88 (92.6) | ||
| Yes | 0 (0.0) | 7 (7.4) | ||
| Vaginal cancer? | <0.01 | |||
| No | 887 (100.0) | 89 (62.1) | ||
| Yes | 0 (0.0) | 6 (6.3) | ||
| Vulvar cancer? | – | |||
| No | 887 (100.0) | 95 (100.0) | ||
| Yes | 0 (0.0) | 0 (0.0) | ||
| Anal cancer? | <0.01 | |||
| No | 886 (99.8) | 17 (17.9) | ||
| Yes | 1 (0.2) | 78 (82.1) | ||
| Penile cancer? | <0.01 | |||
| No | 887 (100.0) | 80 (84.2) | ||
| Yes | 0 (0.0) | 15 (15.8) | ||
| Oropharyngeal cancer? | <0.01 | |||
| No | 887 (100.0) | 92 (96.8) | ||
| Yes | 0 (0.0) | 3 (3.2) | ||
Regardless of the participant’s HIV status, anogenital warts remained an independent risk factor for knowing that HPV causes cancer (living with HIV aOR: 6.35, 95% CI: 3.55–11.35; without HIV aOR: 4.66, 95% CI: 1.62–13.38). Living with HIV for ≥6 years was associated with 2-fold higher odds of believing that HPV causes cancer when compared with SMM living with HIV for <6 years after adjusting for age and history of anogenital warts (aOR: 2.24, 95% CI: 1.06–4.73). Older age initially was associated with 3-fold higher odds of believing that HPV causes cancer, but this was no longer significant in the multivariable models (Table 3).
| Characteristics | Living with HIV (n = 569) | HIV-negative (n = 307) | |||
|---|---|---|---|---|---|
| Unadjusted OR (95% CI) | Adjusted OR (95% CI) | Unadjusted OR (95% CI) | Adjusted OR (95% CI) | ||
| Age (years) | |||||
| 18–30 | Ref. | Ref. | Ref. | Ref. | |
| >30 | 2.53 (1.64–3.93) | 1.62 (0.85–3.05) | 2.96 (1.43–6.10) | 1.62 (0.86–3.05) | |
| Resident state | |||||
| Federal Capital Territory (Abuja) | Ref. | Ref. | Ref. | Ref. | |
| Outside of Federal Capital Territory | 1.79 (1.05–3.04) | 1.46 (0.64–3.34) | 0.96 (0.38–2.43) | 1.47 (0.64–3.36) | |
| Years living with HIV | |||||
| <6 | Ref. | Ref. | – | – | |
| ≥6 | 3.04 (1.74–5.30) | 2.14 (1.13–4.07) | – | – | |
| History of anogenital warts? | |||||
| No | Ref. | Ref. | Ref. | Ref. | |
| Yes | 6.35 (3.55–11.35) | 6.35 (2.96–13.6) | 4.66 (1.62–13.38) | 4.77 (1.60–14.23) | |
Bolded indicates P < 0.05.
Discussion
The findings of our study highlight the awareness and beliefs surrounding HPV and its link to cancer among a large sample of SMM from a community clinic in Abuja, Nigeria. Our investigation revealed a low level of awareness regarding the link between HPV and cancer, with most clients reporting ‘no or unsure’. Interestingly, participants who reported a history of anogenital warts were more likely to believe in HPV’s carcinogenicity. The finding aligns with other research highlighting that individuals who reported treatment for genital warts were more likely to have heard of HPV.15 This underscores the influence of personal health experiences and health literacy on perceptions of HPV-related health risks. Efforts to improve awareness and education about HPV and its association with cancer, particularly among SMM living with HIV given their high risk of cancer,16 are crucial for enhancing early detection and prevention efforts.12,13
Furthermore, our study identified that living longer with HIV was associated with increased awareness of the carcinogenic potential of HPV. Because SMM living longer with HIV are engaged with healthcare settings, they may have a greater awareness of co-infections such as HPV as they continue to age.17 Age also emerged as a potential factor influencing beliefs, with older individuals exhibiting a higher likelihood of attributing cancer to HPV, although this association was no longer significant in the final models. This observation suggests a potential age-related difference in knowledge and awareness of HPV-related health that supports research related to health literacy among older populations.18
Strengths of this study include a robust sample size and a focused examination of HPV awareness in a population that is often underrepresented in research. However, limitations include the cross-sectional design, which restricts causal inferences, and potential biases in self-reported knowledge. Education levels, a key potential confounder, were not recorded in this study. Nonetheless, our findings provide crucial insights into factors that shape HPV and cancer knowledge among SMM in Nigeria. By identifying demographic and clinical factors associated with awareness, this research highlights specific groups for whom educational interventions can be tailored to address knowledge gaps. Targeted outreach for at-risk populations may enhance awareness of HPV-related health risks and prevention strategies.12,13 The findings also inform the need for education campaigns to inform SMM about vaccines available to prevent HPV.13 Future research should actively engage with SMM in LMICs, such as Nigeria, to develop and implement culturally tailored strategies that effectively disseminate knowledge about HPV-related health risks. This approach can foster informed decision-making, promote health-seeking behaviors, and strengthen community-driven advocacy efforts.
Data availability
The data used to support the findings of this study are available to share upon completion of a data transfer and use agreement, coordinated by the corresponding author on behalf of the TRUST/RV368 Study team.
Declaration of funding
The research reported in this publication was supported by the National Cancer Institute (1K07CA225403, 5T32CA009314-40); Maryland Department of Health’s Cigarette Restitution Fund Program (CH-649-CRF), and the President’s Emergency Plan for AIDS Relief through a cooperative agreement between the Department of Health and Human Services/Centers for Disease Control and Prevention, Global AIDS Program, and the Institute for Human Virology-Nigeria (NU2GGH002099). None of the funders had a specific role in the conceptualization, design, data collection, analysis, decision to publish, or preparation of the manuscript.
Acknowledgements
The authors would like to thank the study participants and staff of TRUST/RV368 for allowing this work to be possible.
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