Abstract:

Objective.

To measure HPV vaccine acceptance in diverse Mexican adult popula­tions, taking into account HIV status.

Materials and methods:

A total of 1 329 men and women, with and without HIV, participated in one of three intervention studies, offering HPV vaccination, carried out in the states of Morelos, Tlaxcala and Mexico City; either the bivalent (Morelos n=103, Tlaxcala n=127) or quadrivalent HPV-vaccine (Mexico City n=1 099) was offered.

Results:

HPV vaccine was accepted by 80.3% of participants; acceptance was higher in people living with HIV than those without (84.4 vs. 78%, p=0.004). Women had greater HPV infection knowledge (p<0.0001) than men and slightly higher (p=0.4) vaccine acceptance. The main reason for vaccine non-acceptance among HIV-positive participants was their doctor recommended they not get vaccinated.

Conclusion:

Acceptance of HPV-vaccine was high in men and women regardless of HIV status. Even higher rates of acceptability may be achieved by educating healthcare providers to recommend HPV vaccine to their patients.

Keywords:
HPV vaccine; acceptability; people living with HIV; women; male

Resumen:

Objetivo.

Medir la aceptación de la vacuna de VPH en una muestra diversa de población adulta mexicana, teniendo en cuenta su estado de VIH.

Material y métodos:

1 329 hombres y mujeres con y sin VIH participaron en tres estudios de intervención, realizados en los estados de Morelos, Tlaxcala y Ciudad de México. Se ofreció la vacuna bivalente (Morelos n=103, Tlaxcala n=127) o la cuadrivalente (Ciudad de México n=1 099) contra VPH.

Resultados:

La vacuna fue aceptada por 80.3% de los participantes; la aceptación fue mayor en personas que viven con VIH que en aquéllas que no (84.4 vs. 78%, p=0.004). Las mujeres (p<0.0001) tenían mayor conocimientos sobre VPH que los hombres y una aceptación de la vacuna ligeramente mayor (p=0.4). El motivo principal de la no aceptación de la vacuna entre personas con VIH fue que su médico recomendó que no se vacunaran.

Conclusión:

La aceptación de la vacuna contra el VPH fue alta en hombres y mujeres, independientemente del estado de VIH. Se pueden lograr mayores tasas de aceptabilidad educando a los proveedores de atención médica para que recomienden la vacuna contra el VPH a sus pacientes.

Palabras clave:
vacuna contra HPV; aceptabilidad; personas viviendo con VIH: hombres; mujeres

Introduction

HPV infection is the most common sexually transmitted infection among men and women worldwide.¹1. Burchell AN, Winer RL, de Sanjosé S, Franco EL. Chapter 6: Epidemiology and transmission dynamics of genital HPV infection. Vaccine. 2006;24(suppl 3):S3/52-61. https://doi.org/10.1016/j.vaccine.2006.05.031
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https://doi.org/10.1177/2051013613496946... HPV 16/18 are responsible for 70% of invasive cervical cancer cases and 84.3% of anal cancer cases.⁴4. De Vuyst H, Clifford GM, Nascimento MC, Madeleine MM, Franceschi S. Prevalence and type distribution of human papillomavirus in carcinoma and intraepithelial neoplasia of the vulva, vagina and anus: a meta-analysis. Int J Cancer. 2009;124(7):1626-36. https://doi.org/10.1002/ijc.24116
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Prevalence and incidence of HPV8 and occurrence of HPV-associate cervical intraepithelial neoplasia (CIN) and anal intraepithelial neoplasia (AIN) are high in people living with HIV, even with the introduction of antiretroviral therapy.⁸8. Palefsky J. Human papillomavirus-related disease in people with HIV. Curr Opin HIV AIDS. 2009;4(1):52-6. https://doi.org/10.1097/COH.0b013e32831a7246
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HPV vaccines are a strategic tool for efficient prevention of chronic HPV infection, genital warts¹²12. Tejada RA, Vargas KG, Benites-Zapata V, Mezones-Holguín E, Bolaños-Díaz R, Hernandez AV. Human papillomavirus vaccine efficacy in the prevention of anogenital warts: systematic review and meta-analysis. Salud Publica Mex . 2017;59(1):84-94 . https://doi.org/10.7910/DVN/HCMDYJ
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https://doi.org/10.1158/1940-6207.CAPR-0... In some studies, per protocol efficacy of preventing anal intraepithelial neoplasia (AIN) grades 1-3 reaches 77.5%.¹⁷17. Centers for Disease Control and Prevention (CDC). Recommendations on the use of quadrivalent human papillomavirus vaccine in males--Advisory Committee on Immunization Practices (ACIP), 2011 . MMWR Morb Mortal Wkly Rep. 2011;60(50):1705-8. Importantly, HPV vaccines can be used in people living with HIV/AIDS as well as those without HIV, given their high safety and immunogenicity profile.¹⁶16. Kjaer SK, Sigurdsson K, Iversen OE, Hernández-Avila M, Wheeler CM, Perez G, et al. A pooled analysis of continued prophylactic efficacy of quadrivalent human papillomavirus (Types 6/11/16/18) vaccine against high-grade cervical and external genital lesions. Cancer Prev Res (Phila). 2009;2(10):868-78. https://doi.org/10.1158/1940-6207.CAPR-09-0031
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https://doi.org/10.1016/j.vaccine.2006.0... HPV vaccines have been approved in the US²⁴24. U.s. Food & Drug Administation. Gardasil. Available from: https://www.fda.gov/BiologicsBloodVaccines/Vaccines/ApprovedProducts/ucm094042.htm https://www.fda.gov/BiologicsBloodVaccine s/Vaccine s/ApprovedProducts/ucm094042.htm
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Studies show acceptability of the HPV vaccine in both men and women in higher-income countries is high, ranging from 66 to 86%.²⁶26. Donders GG, Gabrovska M, Bellen G, Van KJ, Van Den BT, Riphagen I, et al. Knowledge of cervix cancer, human papilloma virus (HPV) and HPV vaccination at the moment of introduction of the vaccine in women in Belgium. Arch Gynecol Obstet. 2008; 277:291-8. https://doi.org/10.1007/s00404-007-0487-1
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https://doi.org/10.1016/j.ypmed.2014.08.... Health education and vaccine promotion that is considered understandable, pertinent and that addresses rumors or incorrect information as well as social mobilization supporting HPV vaccine implementation are important factors related to HPV vaccine acceptability in low and middle-income countries.³⁸38. Degarege A, Krupp K, Fennie K, Srinivas V, Li T, Stephens DP, et al. Human Papillomavirus Vaccine acceptability among parents of adolescent girls in a rural area, Mysore, India. J Pediatr Adolesc Gynecol. 2018. 31(6):583-91. https://doi.org/ 10.1016/j.jpag.2018.07.008
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https://doi.org/10.1016/S0188-4409(01)00... Worldwide, healthcare provider recommendation is one of the most important facilitators of HPV vaccine acceptability and uptake.⁴²42. Perez S, Zimet GD, Tatar O, Stupiansky NW, Fisher WA, Rosberger Z. Human Papillomavirus Vaccines: Successes and Future Challenges. Drugs. 2018;78(14):1385-96. https://doi.org/10.1007/s40265-018-0975-6
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https://doi.org/10.1080/07853890.2018.14... Also important are healthcare user attitudes towards the HPV vaccine, including perceptions of vaccine efficacy⁴⁶46. Sadlier C, Lynam A, O’Dea S, Delamere S, Quinlan M, Clarke S, et al. HPV vaccine acceptability in HIV-infected and HIV negative men who have sex with men (MSM) in Ireland. Hum Vaccin Immunother . 2016;12(6):1536-41. https://doi.org/10.1080/21645515.2016.1151588
https://doi.org/10.1080/21645515.2016.11... and beliefs in the benefits of getting vaccinated.⁴⁷47. Wheldon CW, Daley EM, Walsh-Buhi ER, Baldwin JA, Nyitray AG, Giuliano AR. An integrative theoretical framework for HPV Vaccine promotion among male sexual minorities. Am J Mens Health. 2018;12(5):1409-20. https://doi.org/10.1177/1557988316652937
https://doi.org/10.1177/1557988316652937... Studies on acceptability provide evidence on barriers and facilitators to vaccination in different populations that can be used to improve HPV vaccine policy development and implementation, such as designing vaccine promotion materials and providing healthcare providers with information about what they can say when having conversations with patients about the HPV vaccine.³⁶36. Gamaoun R. Knowledge, awareness and acceptability of anti-HPV vaccine in the Arab states of the Middle East and North Africa Region: a systematic review. East Mediterr Health J. 2018;24(6):538-48. https://doi.org/10.26719/2018.24.6.538
https://doi.org/10.26719/2018.24.6.538... In the current analysis, our objective was to measure HPV vaccine acceptance in diverse Mexican adult populations, taking into account HIV status.

Materials and methods

This analysis is based on three intervention studies that focused on HPV vaccination and related issues in the states of Morelos, Tlaxcala and Mexico City, in Mexico. All three studies were approved by the Ethics, Biosecurity and Research committees of the National Institute of Public Health of Mexico; additional approval was obtained by the state Ministry of Health in Morelos and Tlaxcala, and by the Specialized Condesa-Iztapalapa Clinics in Mexico City. The study was presented to the healthcare providers from the clinics involved prior to recruitment, as was information about the effectiveness and safety of HPV vaccines for adults with and without HIV. Written informed consent was obtained for all participants in all states, including signatures by two witnesses.

Participants and data collection

In Morelos and Tlaxcala, healthcare users of the local Ambulatory Care Centers for Prevention and Treatment of AIDS and Sexually Transmitted Infections (CAPASITS, by its acronym in Spanish) were recruited. Men and women living with HIV age 18 to 45 were asked to complete paper questionnaires and were offered the bivalent HPV vaccine as part of a voluntary study (separate from their normal clinical care), in 2016. In Mexico City, men and women (including transgender women) 18 to 45 years old, including individuals with and without HIV, were recruited at the Specialized Condesa-Iztapalapa Clinic in 2018; they completed questionnaires using computer-assisted personal interviewing and were offered the quadrivalent HPV vaccine, also as part of a voluntary study that was not part of their clinical care. All questionnaires collected socio-demographic data (age, years of education, sex assigned at birth; table I). The questionnaires applied in Morelos and Tlaxcala also included items about HPV-related knowledge and attitudes (with yes/no answers; table II). The questionnaire applied in Mexico City did not collect data on HPV-related knowledge or attitudes but did ask about which gender the person currently identified with. After completing the questionnaires, study participants were provided with information about the association between HPV and cervical and anal cancer, information about HPV vaccine, and any questions they had were answered.

Analysis

The survey data were entered (single data entry for paper questionnaires) into an excel worksheet or transferred from the file created by the computer-assisted personal interviewing program and analyzed using STATA v.13 statistical software. We used t-test for age and Chi square test for categorical variables. Descriptive statistics were used to examine age, education, gender and HPV knowledge and attitudes. HPV vaccine acceptability was defined as receiving the first dose of the vaccine. Comparisons were done using Chi square test for categorical variables, to assess variable association with vaccine reception and refusal.

Results

In all, 1 329 men and women were included in this analysis, with 103 men and women living with HIV in Morelos, 127 women living with HIV in Tlaxcala, and 1 099 people (789 men and 310 women, including 108 transgender women, of whom in all 275 were people living with HIV and 824 without), at the Condesa and Condesa-Iztapalapa clinics (table I). Of the total sample, 65% were men and 35% women, with older average ages in Morelos and Tlaxcala and younger average age for participants from Mexico City. More women had only an elementary or junior high school education as compared to men, and more men had at least some college education, or graduate studies than women. All these differences are statistically significant.

For most questions on HPV-related knowledge, correct responses ranged from 65 to 92% (table II). Among the respondents who were asked questions about HPV-related knowledge (all of whom were people living with HIV), there were relatively high levels of knowledge about HPV being sexually transmitted, that HPV causes anal and cervical cancer and that an anti-HPV vaccine exists with somewhat fewer people reporting that the HPV vaccine can be applied to both men and women and only a fifth of participants (mostly women) knowing HPV can disappear without treatment. Women living with HIV had greater knowledge in all areas than men living with HIV, and also had much higher risk perception about acquiring HPV (78% for women versus 20% for men). All these differences were statistically significant (table II).

Vaccine acceptance (agreeing to -including providing signed, informed consent- and getting the application of the first dose of the HPV vaccine) was 80.3% in the total sample (table III). Acceptance was 96.8% in women from Tlaxcala (the sample included only women living with HIV), 84.5% in people from Morelos (including men and women living with HIV), and 78% in Mexico City (including men and women with and without HIV). These differences were statistically significant. Acceptance of the vaccine was slightly higher in women compared to men (81.5 and 80% respectively, but this difference was not statistically significant). Similar proportions of cisgender^** Cisgender is a term used to refer to people whose gender identity and the gender assigned at birth agree (people who were labeled as female at birth and identify as women or who were labeled as male at birth and identify as men). That is, people who are not transgender. and transgender women living in Mexico City accepted the HPV vaccine (data not shown). More people living with HIV accepted the vaccine as compared to those without HIV (84.4 vs. 78.0%) and this difference was statistically significant. Among study participants living with HIV and receiving treatment at CAPASITS in Morelos and Tlaxcala, those who decided not to receive the vaccine gave as their principal reason for doing so that their physician recommended they not get vaccinated (data not shown).

Discussion

Among adult residents of three states in Mexico, acceptance of the HPV vaccine in general is high, without significant differences due to sex/gender (between cisgender men and women or between cisgender women and transgender women) or HIV status. In the study populations included in this analysis, a high level of acceptance of the HPV vaccine was observed among people living with HIV, as has been found in other studies.²⁸28. Kahn JA, Rosenthal SL, Jin Y, Huang B, Namakydoust A, Zimet GD. Rates of human papillomavirus vaccination, attitudes about vaccination, and human papillomavirus prevalence in young women. Obstet Gynecol. 2008;111:1103-10. https://doi.org/10.1097/AOG.0b013e31817051fa
https://doi.org/10.1097/AOG.0b013e318170... ^,2929. Marshall H, Ryan P, Roberton D, Baghurst P. A cross-sectional survey to assess community attitudes to introduction of Human Papillomavirus vaccine. Aust NZJ Public Health. 2007;31:325-42. https://doi.org/10.1111/j.1467-842X.2007.00054.x
https://doi.org/10.1111/j.1467-842X.2007... ^,3030. Woodhall SC, Lehtinen M, Verho T, Huhtala H, Hokkanen M, Kosunen E. Anticipated acceptance of HPV vaccination at the baseline of implementation: A survey of parental and adolescent knowledge and attitudes in Finland. J Adolesc Health. 2007;40:466-9. https://doi.org/10.1016/j.jadohealth.2007.01.005
https://doi.org/10.1016/j.jadohealth.200... ^,3131. Friedman AL, Shepeard H. Exploring the knowledge, attitudes, beliefs, and communication preferences of the general public regarding HPV: findings from CDC focus group research and implications for practice. Health Educ Behav. 2007;34(3):471-85. https://doi.org/10.1177/1090198106292022
https://doi.org/10.1177/1090198106292022... ^,3232. Sauvageau C, Duval B, Gilca V, Lavoie F, Ouakki M. Human papilloma virus vaccine and cervical cancer screening acceptability among adults in Quebec, Canada. BMC Public Health. 2007;7:304. https://doi.org/10.1186/1471-2458-7-304
https://doi.org/10.1186/1471-2458-7-304... ^,3333. Tian T, Wang D, Papamichael C, Yan Z, Guoyao S, Zhanlin Z, et al. HPV vaccination acceptability among men who have sex with men in Urumqi, China. Hum Vaccin Immunother. 2018. https://doi.org/10.1080/21645515.2018.1520591
https://doi.org/10.1080/21645515.2018.15... ^,3434. Poole DN, Tracy JK, Levitz L, Rochas M, Sangare K, Yekta S, et al. A cross-sectional study to assess HPV knowledge and HPV vaccine acceptability in Mali. PLoS One. 2013;8(2):e56402. https://doi.org/10.1371/journal.pone.0056402
https://doi.org/10.1371/journal.pone.005... ^,3535. Godoy-Verdugo MK, Zonana-Nacach A, Anzaldo-Campos MC. Aceptación de la vacuna contra el virus del papiloma humano por parte de madres de hijas entre 9 y 13 años de edad. Ginecol Obstet Mex. 2013;81(11):645-51.^,3636. Gamaoun R. Knowledge, awareness and acceptability of anti-HPV vaccine in the Arab states of the Middle East and North Africa Region: a systematic review. East Mediterr Health J. 2018;24(6):538-48. https://doi.org/10.26719/2018.24.6.538
https://doi.org/10.26719/2018.24.6.538... ^,3737. Cunningham MS, Davison C, Aronson KJ. HPV vaccine acceptability in Africa: a systematic review. Prev Med. 2014;69:274-9. https://doi.org/10.1016/j.ypmed.2014.08.035
https://doi.org/10.1016/j.ypmed.2014.08.... ^,3838. Degarege A, Krupp K, Fennie K, Srinivas V, Li T, Stephens DP, et al. Human Papillomavirus Vaccine acceptability among parents of adolescent girls in a rural area, Mysore, India. J Pediatr Adolesc Gynecol. 2018. 31(6):583-91. https://doi.org/ 10.1016/j.jpag.2018.07.008
https://doi.org/10.1016/j.jpag.2018.07.0... ^,3939. Vermandere H, van Stam MA, Naanyu V, Michielsen K, Degomme O, Oort F. Uptake of the human papillomavirus vaccine in Kenya: testing the health belief model through pathway modeling on cohort data. Global Health. 2016;12(1):72. https://doi.org/10.1186/s12992-016-0211-7
https://doi.org/10.1186/s12992-016-0211-... A number of studies have also found that high HPV vaccine acceptability in men who have sex with men (with or without HIV) was 75%.³³33. Tian T, Wang D, Papamichael C, Yan Z, Guoyao S, Zhanlin Z, et al. HPV vaccination acceptability among men who have sex with men in Urumqi, China. Hum Vaccin Immunother. 2018. https://doi.org/10.1080/21645515.2018.1520591
https://doi.org/10.1080/21645515.2018.15... ^,4646. Sadlier C, Lynam A, O’Dea S, Delamere S, Quinlan M, Clarke S, et al. HPV vaccine acceptability in HIV-infected and HIV negative men who have sex with men (MSM) in Ireland. Hum Vaccin Immunother . 2016;12(6):1536-41. https://doi.org/10.1080/21645515.2016.1151588
https://doi.org/10.1080/21645515.2016.11... As for women, in a cohort of young female sex workers living with HIV, 100% agreed to apply the first dose of vaccine, while 79% completed the 3-dose schedule.⁴⁸48. Wadhera P, Evans JL, Stein E, Gandhi M, Couture MC, Sansothy N, et al. HPV knowledge, vaccine acceptance, and vaccine series completion among female entertainment and sex workers in Phnom Penh, Cambodia: the Young Women’s Health Study. Int J STD AIDS . 2015;26(12):893-902. https://doi.org/10.1177/0956462414563626
https://doi.org/10.1177/0956462414563626... Our results therefore suggest that it would be feasible to introduce a vaccination program against HPV between adults in Mexico, including among people living with HIV, who are at high-risk of developing HPV-associated cancers.²2. Giuliano AR, Lazcano-Ponce E, Villa LL, Flores R, Salmeron J, Lee JH, et al. The human papillomavirus infection in men study: human papillomavirus prevalence and type distribution among men residing in Brazil, Mexico, and the United States. Cancer Epidemiol Biomarkers Prev. 2008;17(8):2036-43. https://doi.org/10.1158/1055-9965.EPI-08-0151
https://doi.org/10.1158/1055-9965.EPI-08... ^,88. Palefsky J. Human papillomavirus-related disease in people with HIV. Curr Opin HIV AIDS. 2009;4(1):52-6. https://doi.org/10.1097/COH.0b013e32831a7246
https://doi.org/10.1097/COH.0b013e32831a...

Women and men living with HIV are disproportionately affected by HPV infection and associated diseases.⁴⁹49. Chin-Hong PV, Palefsky JM. Natural history and clinical management of anal human papillomavirus disease in men and women infected with human immunodeficiency virus. Clin Infec Dis. 2002;35(9):1127-34. https://doi.org/10.1086/344057
https://doi.org/10.1086/344057... ^,5050. Sun XW, Kuhn L, Ellerbrock TV, Chiasson MA, Bush TJ, Wright TC Jr. Human papillomavirus infection in women infected with the human immunodeficiency virus. New Engl J Med. 1997;337(19):1343-9. https://doi.org/10.1056/NEJM199711063371903
https://doi.org/10.1056/NEJM199711063371... In their vaccination recommendations, the Centers for Disease Control and Prevention (CDC) have proposed the introduction of the HPV vaccine for people living with HIV, irrespective of the CD4 lymphocyte count.⁵¹51. Markowitz LE, Dunne EF, Saraiya M, Chesson HW, Curtis CR, Gee J, et al. Human papillomavirus vaccination: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2014;63(RR-05):1-30. In Mexico, the National Center for the Prevention and Control of HIV and AIDS (Censida, by its acronym in Spanish) is studying the possibility of universal introduction of vaccination against HPV in people living with HIV. In order to make this public policy decision, it is essential to consider acceptability of the vaccine among healthcare users,²⁹29. Marshall H, Ryan P, Roberton D, Baghurst P. A cross-sectional survey to assess community attitudes to introduction of Human Papillomavirus vaccine. Aust NZJ Public Health. 2007;31:325-42. https://doi.org/10.1111/j.1467-842X.2007.00054.x
https://doi.org/10.1111/j.1467-842X.2007... ^,3434. Poole DN, Tracy JK, Levitz L, Rochas M, Sangare K, Yekta S, et al. A cross-sectional study to assess HPV knowledge and HPV vaccine acceptability in Mali. PLoS One. 2013;8(2):e56402. https://doi.org/10.1371/journal.pone.0056402
https://doi.org/10.1371/journal.pone.005... ^,3535. Godoy-Verdugo MK, Zonana-Nacach A, Anzaldo-Campos MC. Aceptación de la vacuna contra el virus del papiloma humano por parte de madres de hijas entre 9 y 13 años de edad. Ginecol Obstet Mex. 2013;81(11):645-51.^,3838. Degarege A, Krupp K, Fennie K, Srinivas V, Li T, Stephens DP, et al. Human Papillomavirus Vaccine acceptability among parents of adolescent girls in a rural area, Mysore, India. J Pediatr Adolesc Gynecol. 2018. 31(6):583-91. https://doi.org/ 10.1016/j.jpag.2018.07.008
https://doi.org/10.1016/j.jpag.2018.07.0... ^,3939. Vermandere H, van Stam MA, Naanyu V, Michielsen K, Degomme O, Oort F. Uptake of the human papillomavirus vaccine in Kenya: testing the health belief model through pathway modeling on cohort data. Global Health. 2016;12(1):72. https://doi.org/10.1186/s12992-016-0211-7
https://doi.org/10.1186/s12992-016-0211-... ^,4848. Wadhera P, Evans JL, Stein E, Gandhi M, Couture MC, Sansothy N, et al. HPV knowledge, vaccine acceptance, and vaccine series completion among female entertainment and sex workers in Phnom Penh, Cambodia: the Young Women’s Health Study. Int J STD AIDS . 2015;26(12):893-902. https://doi.org/10.1177/0956462414563626
https://doi.org/10.1177/0956462414563626... logistical aspects of vaccine implementation⁴²42. Perez S, Zimet GD, Tatar O, Stupiansky NW, Fisher WA, Rosberger Z. Human Papillomavirus Vaccines: Successes and Future Challenges. Drugs. 2018;78(14):1385-96. https://doi.org/10.1007/s40265-018-0975-6
https://doi.org/10.1007/s40265-018-0975-... ^,5252. Gilca V, Salmerón-Castro J, Sauvageau C, Ogilvie G, Landry M, Naus M, Lazcano-Ponce E. Early use of the HPV 2-dose vaccination schedule: Leveraging evidence to support policy for accelerated impact. Vaccine . 2018;36(32 Pt A):4800-5. https://doi.org/10.1016/j.vaccine.2018.02.004
https://doi.org/10.1016/j.vaccine.2018.0... ^,5353. Wallace L, Kapirir L. How are new vaccines prioritized in low-income countries? A case study of human papilloma virus vaccine and pneumococcal conjugate vaccine in Uganda. Int J Health Policy Manag. 2017;6(12):707-20. https://doi.org/10.15171/ijhpm.2017.37
https://doi.org/10.15171/ijhpm.2017.37... ^,5454. Patel H, Wilson E, Vizzotti C, Parston G, Prestt J, Darzi A. Argentina’s successful implementation of a national human papillomavirus vaccination program. Health Aff (Millwood). 2016;35(2):301-8. https://doi.org/10.1377/hlthaff.2015.1416
https://doi.org/10.1377/hlthaff.2015.141... as well as the need for providing current, accurate information to healthcare professionals about the safety and efficacy of HPV vaccination among adults in general and specifically those living with HIV.⁵⁵55. Wheldon CW, Sutton SK, Fontenot HB, Quinn GP, Giuliano AR, Vadaparampil ST. Physician communication practices as a barrier to risk-based HPV Vaccine uptake among men who have sex with men. J Cancer Educ. 2018;33(5):1126-31. https://doi.org/10.1007/s13187-017-1223-6
https://doi.org/10.1007/s13187-017-1223-... ^,5656. Crann SE, Barata PC, Mitchell R, Mawhinney L, Thistle P, Chirenje ZM, Stewart DE. Healthcare providers’ perspectives on the acceptability and uptake of HPV vaccines in Zimbabwe. J Psychosom Obstet Gynaecol. 2016;37(4):147-55. https://doi.org/10.1080/0167482X.2016.1199544
https://doi.org/10.1080/0167482X.2016.11... ^,5757. Garbutt JM, Dodd S, Walling E, Lee AA, Kulka K, Lobb R. Barriers and facilitators to HPV vaccination in primary care practices: a mixed methods study using the Consolidated Framework for Implementation Research. BMC Fam Pract. 2018;19(1):53. https://doi.org/10.1186/s12875-018-0750-5
https://doi.org/10.1186/s12875-018-0750-... ^,5858. Malo TL, Hall ME, Brewer NT, Lathren CR, Gilkey MB. Why is announcement training more effective than conversation training for introducing HPV vaccination? A theory-based investigation. Implement Sci. 2018;13(1):57. https://doi.org/10.1186/s13012-018-0743-8
https://doi.org/10.1186/s13012-018-0743-... Although our findings must be interpreted with care given the cross-sectional design, they indicate, as other studies have shown, that healthcare provider recommendation is an extremely important factor for encouraging HPV vaccination among people living with or without HIV.⁴⁵45. Attia AC, Wolf J, Núñez AE. On surmounting the barriers to HPV vaccination: we can do better. Ann Med. 2018;50(3):209-25. https://doi.org/10.1080/07853890.2018.1426875
https://doi.org/10.1080/07853890.2018.14... ^,5353. Wallace L, Kapirir L. How are new vaccines prioritized in low-income countries? A case study of human papilloma virus vaccine and pneumococcal conjugate vaccine in Uganda. Int J Health Policy Manag. 2017;6(12):707-20. https://doi.org/10.15171/ijhpm.2017.37
https://doi.org/10.15171/ijhpm.2017.37... ^,5555. Wheldon CW, Sutton SK, Fontenot HB, Quinn GP, Giuliano AR, Vadaparampil ST. Physician communication practices as a barrier to risk-based HPV Vaccine uptake among men who have sex with men. J Cancer Educ. 2018;33(5):1126-31. https://doi.org/10.1007/s13187-017-1223-6
https://doi.org/10.1007/s13187-017-1223-... ^,5656. Crann SE, Barata PC, Mitchell R, Mawhinney L, Thistle P, Chirenje ZM, Stewart DE. Healthcare providers’ perspectives on the acceptability and uptake of HPV vaccines in Zimbabwe. J Psychosom Obstet Gynaecol. 2016;37(4):147-55. https://doi.org/10.1080/0167482X.2016.1199544
https://doi.org/10.1080/0167482X.2016.11... This is especially important if healthcare providers are to support such public policies by recommending the HPV vaccine to their patients.⁴⁵45. Attia AC, Wolf J, Núñez AE. On surmounting the barriers to HPV vaccination: we can do better. Ann Med. 2018;50(3):209-25. https://doi.org/10.1080/07853890.2018.1426875
https://doi.org/10.1080/07853890.2018.14... ^,5353. Wallace L, Kapirir L. How are new vaccines prioritized in low-income countries? A case study of human papilloma virus vaccine and pneumococcal conjugate vaccine in Uganda. Int J Health Policy Manag. 2017;6(12):707-20. https://doi.org/10.15171/ijhpm.2017.37
https://doi.org/10.15171/ijhpm.2017.37... ^,5555. Wheldon CW, Sutton SK, Fontenot HB, Quinn GP, Giuliano AR, Vadaparampil ST. Physician communication practices as a barrier to risk-based HPV Vaccine uptake among men who have sex with men. J Cancer Educ. 2018;33(5):1126-31. https://doi.org/10.1007/s13187-017-1223-6
https://doi.org/10.1007/s13187-017-1223-... ^,5656. Crann SE, Barata PC, Mitchell R, Mawhinney L, Thistle P, Chirenje ZM, Stewart DE. Healthcare providers’ perspectives on the acceptability and uptake of HPV vaccines in Zimbabwe. J Psychosom Obstet Gynaecol. 2016;37(4):147-55. https://doi.org/10.1080/0167482X.2016.1199544
https://doi.org/10.1080/0167482X.2016.11...

Knowledge about HPV was high; in our study, 84% of participants knew that HPV can cause cancer, which compares favorably to another study of women living with HIV where only 50% knew about this association.⁵⁹59. Wigfall LT, Bynum SA, Brandt HM, Hébert JR. HPV vaccine awareness and knowledge among women living with HIV. J Cancer Educ . 2016;31(1):187-90. https://doi.org/10.1007/s13187-015-0943-8
https://doi.org/10.1007/s13187-015-0943-... The Mexican men in this study also had more knowledge than that observed in others, such a study of heterosexual, gay and bisexual men, which found that among those who had heard of HPV, less than a third correctly responded that HPV can cause oral, anal and penile cancers.³⁴34. Poole DN, Tracy JK, Levitz L, Rochas M, Sangare K, Yekta S, et al. A cross-sectional study to assess HPV knowledge and HPV vaccine acceptability in Mali. PLoS One. 2013;8(2):e56402. https://doi.org/10.1371/journal.pone.0056402
https://doi.org/10.1371/journal.pone.005... In addition, knowledge about HPV was higher among women than men, even though women had significantly lower levels of formal education. This seems to indicate that women have acquired their knowledge about HPV through interaction with healthcare providers, in spite of a lack of formal education. These findings support the need for providing healthcare personnel with the resources they need in order to promote HPV knowledge and especially to recommend HPV vaccination among their patients.⁵³53. Wallace L, Kapirir L. How are new vaccines prioritized in low-income countries? A case study of human papilloma virus vaccine and pneumococcal conjugate vaccine in Uganda. Int J Health Policy Manag. 2017;6(12):707-20. https://doi.org/10.15171/ijhpm.2017.37
https://doi.org/10.15171/ijhpm.2017.37... ^,5454. Patel H, Wilson E, Vizzotti C, Parston G, Prestt J, Darzi A. Argentina’s successful implementation of a national human papillomavirus vaccination program. Health Aff (Millwood). 2016;35(2):301-8. https://doi.org/10.1377/hlthaff.2015.1416
https://doi.org/10.1377/hlthaff.2015.141... ^,5555. Wheldon CW, Sutton SK, Fontenot HB, Quinn GP, Giuliano AR, Vadaparampil ST. Physician communication practices as a barrier to risk-based HPV Vaccine uptake among men who have sex with men. J Cancer Educ. 2018;33(5):1126-31. https://doi.org/10.1007/s13187-017-1223-6
https://doi.org/10.1007/s13187-017-1223-... ^,5656. Crann SE, Barata PC, Mitchell R, Mawhinney L, Thistle P, Chirenje ZM, Stewart DE. Healthcare providers’ perspectives on the acceptability and uptake of HPV vaccines in Zimbabwe. J Psychosom Obstet Gynaecol. 2016;37(4):147-55. https://doi.org/10.1080/0167482X.2016.1199544
https://doi.org/10.1080/0167482X.2016.11...

A limitation of this analysis is that given that data on knowledge and attitudes regarding vaccination against HPV were not collected among participants from Mexico City, the analysis cannot provide a complete view on the relationship between these aspects and the acceptance of the first dose of HPV vaccine, even for this study population. Also, information was not collected from healthcare users about whether their healthcare providers recommended they get the HPV vaccine, nor was data collected from the healthcare providers themselves. Data are only available for the application of the first dose of vaccine but not for subsequent doses, although more than one vaccine dose was applied in some of the study locations. In addition, the results of this study are not generalizable because they are based on non-representative samples.

Acceptance of the HPV vaccine was high among adult men and women in Mexico with and without HIV. Even higher rates of acceptability can most likely be achieved by providing healthcare workers with a variety of resources so they can be proficient at recommending the HPV vaccine to their adult patients irrespective of HIV status. Healthcare personnel should be provided with educational experiences that support them in developing greater knowledge, self-efficacy and readiness for change in relation to recommending HPV vaccination as well as specific resources for providing patient counseling and education about HPV vaccination.⁵⁸58. Malo TL, Hall ME, Brewer NT, Lathren CR, Gilkey MB. Why is announcement training more effective than conversation training for introducing HPV vaccination? A theory-based investigation. Implement Sci. 2018;13(1):57. https://doi.org/10.1186/s13012-018-0743-8
https://doi.org/10.1186/s13012-018-0743-... ^,5959. Wigfall LT, Bynum SA, Brandt HM, Hébert JR. HPV vaccine awareness and knowledge among women living with HIV. J Cancer Educ . 2016;31(1):187-90. https://doi.org/10.1007/s13187-015-0943-8
https://doi.org/10.1007/s13187-015-0943-...

Acknowledgements

We would like to thank the study participants who made this possible, and also the healthcare and research personnel at the Cuernavaca and Tlaxcala CAPASITS and the Condesa and Condesa-Iztapalapa Clinics. The study at the CAPASITS was carried out thanks to funding provided by Censida, Mexico’s National AIDS Prevention and Control Program. The study at the Condesa and Condesa-Iztapalapa Clinics was funded by the Ministry of Science, Technology and Innovation (Secretaría de Ciencia, Tecnología e Innovación; Seciti) of Mexico City under the grant SECITI/094/2017, as part of the project, “Prevention and control of HPV-related neoplasia in high risk groups in Mexico City: An intervention with a social dimension”.

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