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Published in: BMC Infectious Diseases 1/2020

01-12-2020 | Human Papillomavirus | Research article

Comorbidities associated with HPV infection among people living with HIV-1 in the southeastern US: a retrospective clinical cohort study

Authors: Yuanfan Ye, Greer A. Burkholder, Howard W. Wiener, Russell Griffin, Stella Aslibekyan, Karen Fry, Ashraf Khan, Sadeep Shrestha

Published in: BMC Infectious Diseases | Issue 1/2020

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Abstract

Background

The southeastern US is an epicenter for incident HIV in the US with high prevalence of human papillomavirus (HPV) co-infections. However, epidemiologies of HPV-associated clinical conditions (CC) among people living with HIV-1 infection (PLWH) are not fully known.

Methods

Electronic medical records (EMR) of PLWH attending one of the leading HIV clinics in the southeastern US between 2006 and 2018 were reviewed and analyzed. The retrospective study was nested within the University of Alabama at Birmingham HIV clinical cohort, which has electronically collected over 7000 PLWH’s clinical and sociobehavioral data since 1999. Incidence rates of HPV-related CC including anogenital warts, penile, anal, cervical, and vaginal/vulvar low- and high-grade squamous intraepithelial lesions (LSIL and HSIL) were estimated per 10,000 person years. Joinpoint regressions were performed to examine temporal changes in the trends of incident CC. All rates and trends were stratified by gender and race.

Results

Of the 4484 PLWH included in the study (3429 men, 1031 women, and 24 transgender), we observed 1038 patients with HPV-related CC. The median nadir CD4 count (cells/uL) was higher in the HPV-condition free group than the case groups (P < 0.0001). Anogenital warts, anal LSIL, HSIL, and cancer were more likely to be diagnosed among HIV-infected men than women. White men presented more frequently with anal LSIL and anal and penile cancers than black men (P < 0.03). White women were also more likely to be diagnosed with cervical HSIL (P = 0.023) and cancer (P = 0.037) than black women.

Conclusions

There were significant differences between gender and race with incidence of HPV-related CC among HIV patients. EMR-based studies provide insights on understudied HPV-related anogenital conditions in PLWH; however, large-scale studies in other regions are needed to generalize current findings and draw public health attention to co-infection induced non-AIDS defining comorbidities among PLWH.
Literature
1.
go back to reference Poljak M, Sterbenc A, Lunar MM. Prevention of human papillomavirus (HPV)-related tumors in people living with human immunodeficiency virus (HIV). Expert Rev Anti Infect Ther. 2017;15(11):987–99.CrossRef Poljak M, Sterbenc A, Lunar MM. Prevention of human papillomavirus (HPV)-related tumors in people living with human immunodeficiency virus (HIV). Expert Rev Anti Infect Ther. 2017;15(11):987–99.CrossRef
2.
go back to reference Centers for Disease Control and Prevention. Human papillomavirus (HPV). Atlanta: Department of Health and Human Services; 2020. Centers for Disease Control and Prevention. Human papillomavirus (HPV). Atlanta: Department of Health and Human Services; 2020.
3.
go back to reference zur Hausen H. Papillomavirus Infections – a major cause of human cancers. Biochim Biophys Acta. 1996;1288(2):F55–78.PubMed zur Hausen H. Papillomavirus Infections – a major cause of human cancers. Biochim Biophys Acta. 1996;1288(2):F55–78.PubMed
4.
go back to reference McQuillan G, Kruszon-Moran D, Markowitz LE, Unger ER, Paulose-Ram R. Prevalence of HPV in adults aged 18–69: United States, 2011–2014. NCHS data brief, no 280. Hyattsville: National Center for Health Statistics; 2017. McQuillan G, Kruszon-Moran D, Markowitz LE, Unger ER, Paulose-Ram R. Prevalence of HPV in adults aged 18–69: United States, 2011–2014. NCHS data brief, no 280. Hyattsville: National Center for Health Statistics; 2017.
5.
go back to reference Liu G, Sharma M, Barnabas RV. HIV-positive women have higher risk of human papilloma virus infection, precancerous lesions, and cervical cancer. AIDS. 2018;32(6):795–808.CrossRef Liu G, Sharma M, Barnabas RV. HIV-positive women have higher risk of human papilloma virus infection, precancerous lesions, and cervical cancer. AIDS. 2018;32(6):795–808.CrossRef
6.
go back to reference Bruni L, Diaz M, Castellsagué X, Ferrer E, Bosch FX, de Sanjosé S. Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis. 2010; 202:1789–99.CrossRef Bruni L, Diaz M, Castellsagué X, Ferrer E, Bosch FX, de Sanjosé S. Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis. 2010; 202:1789–99.CrossRef
7.
go back to reference Clifford GM, Tully S, Franceschi S. Carcinogenicity of Human Papillomavirus (HPV) Types in HIV-Positive Women: A Meta-Analysis from HPV Infection to Cervical Cancer Clinical Infectious Diseases. 2017;1228–35.CrossRef Clifford GM, Tully S, Franceschi S. Carcinogenicity of Human Papillomavirus (HPV) Types in HIV-Positive Women: A Meta-Analysis from HPV Infection to Cervical Cancer Clinical Infectious Diseases. 2017;1228–35.CrossRef
8.
go back to reference Holly EA, Ralston ML, Darragh TM, Greenblatt RM, Jay N, Palefsky JM. Prevalence and Risk Factors for Anal Squamous Intraepithelial Lesions in Women. JNCI Journal of the National Cancer Institute. 2001;93:843–9.CrossRef Holly EA, Ralston ML, Darragh TM, Greenblatt RM, Jay N, Palefsky JM. Prevalence and Risk Factors for Anal Squamous Intraepithelial Lesions in Women. JNCI Journal of the National Cancer Institute. 2001;93:843–9.CrossRef
9.
go back to reference Palefsky JM, Holly EA, Hogeboom CJ, Ralston ML, DaCosta MM, Botts R, et al. Virologic, Immunologic, and Clinical Parameters in the Incidence and Progression of Anal Squamous Intraepithelial Lesions in HIV-Positive and HIV-Negative Homosexual Men. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology. 1998;17:314–9.CrossRef Palefsky JM, Holly EA, Hogeboom CJ, Ralston ML, DaCosta MM, Botts R, et al. Virologic, Immunologic, and Clinical Parameters in the Incidence and Progression of Anal Squamous Intraepithelial Lesions in HIV-Positive and HIV-Negative Homosexual Men. Journal of Acquired Immune Deficiency Syndromes and Human Retrovirology. 1998;17:314–9.CrossRef
10.
go back to reference Palefsky JM, Holly EA, Ralston ML, Jay N, Michael Berry J, Darragh TM. High incidence of anal high-grade squamous intra-epithelial lesions among HIV-positive and HIV-negative homosexual and bisexual men. AIDS. 1998;12:495–503.CrossRef Palefsky JM, Holly EA, Ralston ML, Jay N, Michael Berry J, Darragh TM. High incidence of anal high-grade squamous intra-epithelial lesions among HIV-positive and HIV-negative homosexual and bisexual men. AIDS. 1998;12:495–503.CrossRef
11.
go back to reference Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, Snijders PJ, Meijer CJ. International Agency for Research on Cancer Multicenter Cervical Cancer Study Group. Epidemiologic classification of human papillomavirus types associated with cervical cancer. New Engl J Med. 2003;348(6):518–27.CrossRef Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, Snijders PJ, Meijer CJ. International Agency for Research on Cancer Multicenter Cervical Cancer Study Group. Epidemiologic classification of human papillomavirus types associated with cervical cancer. New Engl J Med. 2003;348(6):518–27.CrossRef
12.
go back to reference Schiffman M, Wentzensen N. Human papillomavirus (HPV) infection and the multi-stage carcinogenesis of cervical cancer. Schiffman M, Wentzensen N. Human papillomavirus infection and the multistage carcinogenesis of cervical cancer. Cancer Epidemiol Biomarkers Prev. 2013;22(4):553–60. Schiffman M, Wentzensen N. Human papillomavirus (HPV) infection and the multi-stage carcinogenesis of cervical cancer. Schiffman M, Wentzensen N. Human papillomavirus infection and the multistage carcinogenesis of cervical cancer. Cancer Epidemiol Biomarkers Prev. 2013;22(4):553–60.
13.
go back to reference Ramírez-Fort MK, Khan F, Rady PL, Tyring SK. Human Papillomavirus: Bench to Bedside. Curr Probl Dermatol. Basel, Karger, 2014, vol 45, pp I-VIII Ramírez-Fort MK, Khan F, Rady PL, Tyring SK. Human Papillomavirus: Bench to Bedside. Curr Probl Dermatol. Basel, Karger, 2014, vol 45, pp I-VIII
14.
go back to reference Saraiya M, Unger ER, Thompson TD, Lynch CF, Hernandez BY, Lyu Cw, Steinau M, Watson M, Wilkinson EJ, Hopenhayn C, Copeland G, Cozen W, Peters ES, Huang Y, Saber MS, Altekruse S, Goodman MT, HPV Typing of Cancers Workgroup. US assessment of HPV types in cancers: implications for current and 9-valent HPV vaccines. J Natl Cancer Inst. 2015;107(6):djv086. Saraiya M, Unger ER, Thompson TD, Lynch CF, Hernandez BY, Lyu Cw, Steinau M, Watson M, Wilkinson EJ, Hopenhayn C, Copeland G, Cozen W, Peters ES, Huang Y, Saber MS, Altekruse S, Goodman MT, HPV Typing of Cancers Workgroup. US assessment of HPV types in cancers: implications for current and 9-valent HPV vaccines. J Natl Cancer Inst. 2015;107(6):djv086.
16.
go back to reference Willig JH, Aban I, Nevin CR, Ye J, Raper JL, McKinnel JA, Delaitsch LL, Mrus JM, De La Rosa GR, Mugavero MJ, Saag MS. Darunavir outcomes study: Comparative effectiveness of virologic suppression, regimen durability, and discontinuation reasons for three-class experienced patients at 48 weeks. AIDS Res Hum Retroviruses. 2010;26:1279–85.CrossRef Willig JH, Aban I, Nevin CR, Ye J, Raper JL, McKinnel JA, Delaitsch LL, Mrus JM, De La Rosa GR, Mugavero MJ, Saag MS. Darunavir outcomes study: Comparative effectiveness of virologic suppression, regimen durability, and discontinuation reasons for three-class experienced patients at 48 weeks. AIDS Res Hum Retroviruses. 2010;26:1279–85.CrossRef
17.
go back to reference National Cancer Institute. Joinpoint Regression Program. Version 4.3.1.0. The Institute; 2016. National Cancer Institute. Joinpoint Regression Program. Version 4.3.1.0. The Institute; 2016.
18.
go back to reference Kim HJ, Fay MP, Feuer EJ, Midthune, DN. Permutation Tests for Joinpoint Regression with Applications to Cancer Rates", Statistics in Medicine 19. 2000;335–51.CrossRef Kim HJ, Fay MP, Feuer EJ, Midthune, DN. Permutation Tests for Joinpoint Regression with Applications to Cancer Rates", Statistics in Medicine 19. 2000;335–51.CrossRef
19.
go back to reference Clegg L, Hankey B, Tiwari R, Feuer E, Edwards B. Estimating average annual percent change in trend analysis. Stat Med. 2009;28(29):3670–8.CrossRef Clegg L, Hankey B, Tiwari R, Feuer E, Edwards B. Estimating average annual percent change in trend analysis. Stat Med. 2009;28(29):3670–8.CrossRef
20.
go back to reference Kim HJ, Luo J, Chen HS, Green D, Buckman D, Byrne J, Feuer EJ. Improved confidence interval for average annual percent change in trend analysis. Statistics in medicine vol. 36, 19 (2017): 3059–74.CrossRef Kim HJ, Luo J, Chen HS, Green D, Buckman D, Byrne J, Feuer EJ. Improved confidence interval for average annual percent change in trend analysis. Statistics in medicine vol. 36, 19 (2017): 3059–74.CrossRef
21.
go back to reference Park HS, Lloyd S, Decker RH, Wilson LD, Yu JB. Overview of the Surveillance, Epidemiology, and End Results database: evolution, data variables, and quality assurance. Curr Probl Cancer. 2012;36:183–190.CrossRef Park HS, Lloyd S, Decker RH, Wilson LD, Yu JB. Overview of the Surveillance, Epidemiology, and End Results database: evolution, data variables, and quality assurance. Curr Probl Cancer. 2012;36:183–190.CrossRef
22.
go back to reference Palefsky JM. Human Papillomavirus-Related Disease in Men: Not Just a Women’s Issue. Journal of Adolescent Health. 2010;46:S12–9.CrossRef Palefsky JM. Human Papillomavirus-Related Disease in Men: Not Just a Women’s Issue. Journal of Adolescent Health. 2010;46:S12–9.CrossRef
24.
go back to reference Schim van der Loeff MF, Mooij SH, Richel O, de Vries HJC, Prins JM. HPV and anal cancer in HIV-infected individuals: a review. Curr HIV/AIDS Rep. 2014;11:250–62.CrossRef Schim van der Loeff MF, Mooij SH, Richel O, de Vries HJC, Prins JM. HPV and anal cancer in HIV-infected individuals: a review. Curr HIV/AIDS Rep. 2014;11:250–62.CrossRef
25.
go back to reference D’Souza G, Wiley DJ, Li X, Chmiel JS, Margolick JB, Cranston RD, et al. Incidence and epidemiology of anal cancer in the multicenter AIDS cohort study. J Acquir Immune Defic Syndr. 2008;48:491–9. D’Souza G, Wiley DJ, Li X, Chmiel JS, Margolick JB, Cranston RD, et al. Incidence and epidemiology of anal cancer in the multicenter AIDS cohort study. J Acquir Immune Defic Syndr. 2008;48:491–9.
26.
go back to reference Watson M, Johnson SD, Zhang T, Oster AM. Characteristics of and Trends in HIV Diagnoses in the Deep South Region of the United States, 2012-2017. AIDS Behav. 2019;23(Suppl 3):224–32.CrossRef Watson M, Johnson SD, Zhang T, Oster AM. Characteristics of and Trends in HIV Diagnoses in the Deep South Region of the United States, 2012-2017. AIDS Behav. 2019;23(Suppl 3):224–32.CrossRef
Metadata
Title
Comorbidities associated with HPV infection among people living with HIV-1 in the southeastern US: a retrospective clinical cohort study
Authors
Yuanfan Ye
Greer A. Burkholder
Howard W. Wiener
Russell Griffin
Stella Aslibekyan
Karen Fry
Ashraf Khan
Sadeep Shrestha
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2020
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-020-4822-5

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