Prevalence of anal high-risk human papillomavirus (HR-HPV) types in people living with HIV and a history of cancer
Salim A. Barquet-Muñoz
Dysplasia Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorRoxana A. López-Morales
Laboratory of Virus and Cancer, Unidad de Investigación Biomédica en Cáncer, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México & Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorElizabeth A. Stier
Department of Obstetrics and Gynecology, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts, USA
Search for more papers by this authorEmmanuel Mejorada-Pulido
Dysplasia Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorDiego Solís-Ramírez
Dysplasia Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorNaomi Jay
Anal Neoplasia Clinic, Research, and Education Center, University of California San Francisco, San Francisco, California, USA
Search for more papers by this authorPaulina Moctezuma
Dysplasia Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorMariel Morales-Aguirre
Dysplasia Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorAlejandro García-Carrancá
Laboratory of Virus and Cancer, Unidad de Investigación Biomédica en Cáncer, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México & Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorRocío Méndez-Martínez
Basic Research Unit, Virus, and Cancer Laboratory, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorAlexandra Martin-Onraët
Infectious Diseases Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorDelia Pérez-Montiel
Department of Surgical Pathology, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorMaría José Mendoza-Palacios
Infectious Diseases Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorCorresponding Author
Patricia Volkow
Infectious Diseases Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Correspondence
Patricia Volkow, Infectious Diseases Department. Instituto Nacional de Cancerología, Av. San Fernando No. 22, Col. Belisario Domínguez, Sección XVI, Tlalpan, 14080 CDMX, México City, México.
Email: [email protected]
Search for more papers by this authorSalim A. Barquet-Muñoz
Dysplasia Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorRoxana A. López-Morales
Laboratory of Virus and Cancer, Unidad de Investigación Biomédica en Cáncer, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México & Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorElizabeth A. Stier
Department of Obstetrics and Gynecology, Boston University Chobanian and Avedisian School of Medicine, Boston, Massachusetts, USA
Search for more papers by this authorEmmanuel Mejorada-Pulido
Dysplasia Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorDiego Solís-Ramírez
Dysplasia Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorNaomi Jay
Anal Neoplasia Clinic, Research, and Education Center, University of California San Francisco, San Francisco, California, USA
Search for more papers by this authorPaulina Moctezuma
Dysplasia Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorMariel Morales-Aguirre
Dysplasia Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorAlejandro García-Carrancá
Laboratory of Virus and Cancer, Unidad de Investigación Biomédica en Cáncer, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México & Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorRocío Méndez-Martínez
Basic Research Unit, Virus, and Cancer Laboratory, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorAlexandra Martin-Onraët
Infectious Diseases Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorDelia Pérez-Montiel
Department of Surgical Pathology, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorMaría José Mendoza-Palacios
Infectious Diseases Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Search for more papers by this authorCorresponding Author
Patricia Volkow
Infectious Diseases Department, Instituto Nacional de Cancerología, Mexico City, Mexico
Correspondence
Patricia Volkow, Infectious Diseases Department. Instituto Nacional de Cancerología, Av. San Fernando No. 22, Col. Belisario Domínguez, Sección XVI, Tlalpan, 14080 CDMX, México City, México.
Email: [email protected]
Search for more papers by this authorAll the authors contributed equally to the work.
Abstract
This study aimed to describe the prevalence of high-risk human papillomavirus (HR-HPV) types in the anal canal in a cohort of people living with HIV (PLWHIV) with a history of malignancy.
Setting
Referral tertiary care hospital for adult patients with cancer.
Methods
We reviewed data of patients from the AIDS Cancer Clinic on antiretroviral therapy in chronic control who were consecutively referred for high-resolution anoscopy (HRA), where they underwent anal evaluation, collection of specimens for anal cytology and anal human papillomavirus (HPV) followed by HRA with directed biopsy if needed.
Results
A total of 155 patients were included; 149 (96.1%) were men, all of them men who have sex with men (MSM); the median age was 39 (IQR 32-47) years; 105 (67.7%) with Kaposi sarcoma, 40 (25.8%) with non-Hodgkin lymphoma and 10 (6.4%) with other neoplasms; only 7 (4.5%) had active cancer. The prevalence of HR-HPV infection was 89% (n=138) (95% CI 83–93) with at least one HR-HPV infection, and 62% (96) had coinfection with at least two types; the median HR-HPV types of coinfection were 3 (IQR 2–4). The number of patients infected with HPV 16 was 64 (41.3%, 95% CI 33.8–49.3), HPV 18 was 74 (47.7%, 95% CI 39.9–55.7) and with both 35 (22.6%). Some 59 patients (38%) had high-grade squamous intraepithelial lesions (HSIL) and 49 (31.6%) had low-grade squamous intraepithelial lesions (LSIL). The prevalence of HR-HPV and HSIL among patients aged ≤35 and >35 years was the same.
Conclusions
In this cohort of PLWHIV with a history of malignancy we found a high prevalence of HR-HPV 16 and 18 and anal HSIL, even in persons aged ≤35 years. These data highlight the importance of anal cancer screening in PLWHIV and history of malignancy.
CONFLICT OF INTEREST STATEMENT
None of the authors have any conflicts of interest to declare.
Supporting Information
Filename | Description |
---|---|
hiv13684-sup-0001-FigureS1.docxWord 2007 document , 17.4 KB | Figure S1.. Prevalence of human papillomavirus (HPV) subtypes in people living with HIV (PLWHIV) with history of malignancy by gender (N = 155). HPV 52 with a statistically significant difference (male 16.1% vs. female 50.0%, p = 0.03). |
hiv13684-sup-0002-FigureS2.docxWord 2007 document , 42.2 KB | Figure S2. Distribution by the number of any human papillomavirus (HPV) present simultaneously in the anal canal in PLWHIV with a malignancy diagnosis. |
hiv13684-sup-0003-FigureS3.docxWord 2007 document , 17.8 KB | Figure S3. Prevalence of all subtypes of human papillomavirus (HPV) by neoplasia (N = 155). The most frequent was HPV 11 for Kaposi sarcoma (p = 0.033) and HPV 43 for other malignancies (p = 0.046). |
hiv13684-sup-0004-TableS1.docxWord 2007 document , 59 KB | Table S1. Prevalence of subtype human papillomavirus (HPV) by type of anal lesion in people living with HIV (PLWHIV) with history of malignancy (N = 155). |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Jin F, Vajdic CM, Law M, et al. Incidence and time trends of anal cancer among people living with HIV in Australia. AIDS. 2019; 33(8): 1361-1368. doi:10.1097/QAD.0000000000002218
- 2Clifford GM, Georges D, Shiels MS, et al. A meta-analysis of anal cancer incidence by risk group: toward a unified anal cancer risk scale. Int J Cancer. 2021; 148(1): 38-47. doi:10.1002/ijc.33185
- 3de Martel C, Plummer M, Vignat J, Franceschi S. Worldwide burden of cancer attributable to HPV by site, country and HPV type. Int J Cancer. 2017; 141(4): 664-670. doi:10.1002/ijc.30716
- 4Hernandez AL, Karthik R, Sivasubramanian M, et al. Prevalence of anal HPV infection among HIV-positive men who have sex with men in India. J Acquir Immune Defic Syndr. 2016; 71(4): 437-443. doi:10.1097/QAI.0000000000000855
- 5Supindham T, Chariyalertsak S, Utaipat U, et al. High prevalence and genotype diversity of anal HPV infection among MSM in northern Thailand. Lama JR, ed. PLoS One. 2015; 10(5):e0124499. doi:10.1371/journal.pone.0124499
- 6Somia IKA, Teeratakulpisarn N, Jeo WS, et al. Prevalence of and risk factors for anal high-risk HPV among HIV-negative and HIV-positive MSM and transgender women in three countries at South-East Asia. Medicine (Baltimore). 2018; 97(10):e9898. doi:10.1097/MD.0000000000009898
- 7Eng C, Ciombor KK, Cho M, et al. Anal cancer: emerging standards in a rare disease. J Clin Oncol. 2022; 40(24): 2774-2788. doi:10.1200/JCO.21.02566
- 8Shmakova A, Germini D, Vassetzky Y. HIV-1, HAART and cancer: a complex relationship. Int J Cancer. 2020; 146(10): 2666-2679. doi:10.1002/ijc.32730
- 9Crum-Cianflone N, Hullsiek KH, Marconi V, et al. Trends in the incidence of cancers among HIV-infected persons and the impact of antiretroviral therapy: a 20-year cohort study. AIDS. 2009; 23(1): 41-50. doi:10.1097/QAD.0b013e328317cc2d
- 10Steinau M, Unger ER, Hernandez BY, et al. Human papillomavirus prevalence in invasive anal cancers in the United States before vaccine introduction. J Low Genit Tract Dis. 2013; 17(4): 397-403. doi:10.1097/LGT.0b013e31827ed372
- 11Wang C-CJ, Sparano J, Palefsky JM. Human immunodeficiency virus/AIDS, human papillomavirus, and anal cancer. Surg Oncol Clin N Am. 2017; 26(1): 17-31. doi:10.1016/j.soc.2016.07.010
- 12Albuquerque A, Nathan M, Cappello C, Dinis-Ribeiro M. Anal cancer and precancerous lesions: a call for improvement. Lancet Gastroenterol Hepatol. 2021; 6(4): 327-334. doi:10.1016/S2468-1253(20)30304-6
- 13 IARC. IA for R on CWHO. In: IARC. IA for R on CWHO, ed. ed. WHO Classification of Tumours Editorial Board: Female Genital Tumours. 5th ed. International Agency for Research in Cancer (IARC); 2022.
- 14Berry JM, Jay N, Cranston RD, et al. Progression of anal high-grade squamous intraepithelial lesions to invasive anal cancer among HIV-infected men who have sex with men. Int J Cancer. 2014; 134(5): 1147-1155. doi:10.1002/ijc.28431
- 15Choi Y, Loutfy M, Remis RS, et al. HPV genotyping and risk factors for anal high-risk HPV infection in men who have sex with men from Toronto, Canada. Sci Rep. 2021; 11(1): 4779. doi:10.1038/s41598-021-84079-y
- 16LoSchiavo C, D'Avanzo PA, Emmert C, et al. Predictors of anal high-risk HPV infection across time in a cohort of young adult sexual minority men and transgender women in New York City, 2015–2020. Am J Mens Health. 2022; 16(4):15579883221119084. doi:10.1177/15579883221119084
- 17Torres-Ibarra L, Conde-Glez CJ, Salmerón J, et al. Risk factors for anal HPV-16/18 infection in Mexican HIV-infected men who have sex with men. Prev Med. 2014; 69: 157-164. doi:10.1016/j.ypmed.2014.09.011
- 18Wei F, Gaisa MM, D'Souza G, et al. Epidemiology of anal human papillomavirus infection and high-grade squamous intraepithelial lesions in 29 900 men according to HIV status, sexuality, and age: a collaborative pooled analysis of 64 studies. Lancet HIV. 2021; 8(9): e531-e543. doi:10.1016/S2352-3018(21)00108-9
- 19Fink VI, Jenkins CA, Castilho JL, et al. Survival after cancer diagnosis in a cohort of HIV-positive individuals in Latin America. Infect Agent Cancer. 2018; 13(1): 16. doi:10.1186/s13027-018-0188-3
- 20Belaunzarán-Zamudio PF, Caro-Vega YN, Shepherd BE, et al. The population impact of late presentation with advanced HIV disease and delayed antiretroviral therapy in adults receiving HIV Care in Latin America. Am J Epidemiol. 2020; 189(6): 564-572. doi:10.1093/aje/kwz252
- 21Bruzzesi E, Galli L, Poli A, et al. Prevalence and risk factors of anal HPV infection in MSM living with HIV: identifying the target groups to prioritize for immunization. J Acquir Immune Defic Syndr. 2022; 91(2): 226-231. doi:10.1097/QAI.0000000000003057
- 22Ji Y, Lu H. Malignancies in HIV-infected and AIDS patients. Adv Exp Med Biol. 2017; 1018: 167-179. doi:10.1007/978-981-10-5765-6_10
- 23 Centro Nacional para la Salud de la Infancia y la Adolescencia. Actualización de esquema de vacunación contra Virus del Papiloma Humano (VPH) en niñas/adolescentes femeninas y en la población de mujeres cis y trans que viven con VIH. 2022. https://www.gob.mx/salud/censia/articulos/actualizacion-de-esquema-de-vacunacion-contra-virus-del-papiloma-humano-vph-319938
- 24Alarcón-Romero LDC, Organista-Nava J, Gómez-Gómez Y, et al. Prevalence and distribution of human papillomavirus genotypes (1997–2019) and their association with cervical cancer and precursor lesions in women from southern Mexico. Cancer Control. 2022; 29:10732748221103332. doi:10.1177/10732748221103331
- 25Luna-Aguirre CM, Reyes-Cortés LM, Torres-Grimaldo AA, et al. Prevalence of human papillomavirus types in north and central regions of Mexico. Epidemiol Infect. 2018; 146(13): 1724-1730. doi:10.1017/S0950268818001747
- 26Hoots BE, Palefsky JM, Pimenta JM, Smith JS. Human papillomavirus type distribution in anal cancer and anal intraepithelial lesions. Int J Cancer. 2009; 124(10): 2375-2383. doi:10.1002/ijc.24215
- 27Garbuglia AR, Gentile M, Del Nonno F, et al. An anal cancer screening program for MSM in Italy: prevalence of multiple HPV types and vaccine-targeted infections. J Clin Virol. 2015; 72: 49-54. doi:10.1016/j.jcv.2015.09.001
- 28Cachay ER, Gilbert T, Deiss R, Mathews WC. Shared decision-making concerning anal cancer screening in persons with human immunodeficiency virus. Clin Infect Dis. 2023; 76(4): 582-591. doi:10.1093/cid/ciac491
- 29 Censida. Boletin Dia Munidal. Del Sida; 2022. https://www.gob.mx/censida/articulos/boletin-de-diagnostico-y-tratamiento-antirretroviral-censida
- 30Stier EA, Clarke MA, Deshmukh AA, et al. International Anal Neoplasia Society's consensus guidelines for anal cancer screening. Int J Cancer. 2024; 154(10): 1694-1702. doi:10.1002/ijc.34850
- 31Palefsky JM, Lee JY, Jay N, et al. ANCHOR Investigators Group. Treatment of anal high-grade squamous intraepithelial lesions to prevent anal cancer. N Engl J Med. 2022; 386(24): 2273-2282. doi:10.1056/NEJMoa2201048