Skip to main content
Top
Published in: Virology Journal 1/2014

Open Access 01-12-2014 | Research

The diversity of human papillomavirus infection among human immunodeficiency virus-infected women in Yunnan, China

Authors: Hong-Yun Zhang, Man-Dong Fei, Yong Jiang, Qiu-Yue Fei, Hong Qian, Lin Xu, Yu-Ni Jin, Cheng-Qin Jiang, Hai-Xia Li, Sarah M Tiggelaar, Jennifer S Smith, Vikrant V Sahasrabuddhe, You-Lin Qiao

Published in: Virology Journal | Issue 1/2014

Login to get access

Abstract

Background

Yunnan has one of the oldest and the most severe human immunodeficiency virus (HIV) epidemics in China. We conducted an observational study to evaluate the human papillomavirus (HPV) genotype distribution in relation to cervical neoplastic disease risk among HIV-infected women in Yunnan.

Methods

We screened 301 HIV-infected non-pregnant women in Mangshi prefecture in Yunnan province. All consenting participants underwent simultaneous and independent assessment by cervical cytology, colposcopy-histopathology, and HPV genotyping. Unadjusted and multivariable-adjusted multinomial logistic regression analysis was conducted to evaluate factors associated with single or multiple carcinogenic HPV genotypes.

Results

HPV genotypes were present in 43.5% (131/301) overall, and carcinogenic HPV genotypes were present in 37.5% (113/301) women. Among women with carcinogenic HPV genotypes, 80 (70.8% of 113) had a single carcinogenic HPV type, while 33 (29.2%) women had multiple (2 or more) carcinogenic HPV types. Overall, the most common carcinogenic HPV types were HPV52 (7.3%), HPV58 (6.6%), HPV18 (6.3%), HPV16 (6.0%), and HPV33 (5.3%). In women with cervical precancerous lesions (i.e., high-grade squamous intraepithelial lesions [HSIL] on cytology or cervical intraepithelial neoplasia grade 2 or worse [CIN2+] detected on colposcopy-histology), the most commonly detected genotypes were HPV16 (28.6%), HPV52 (25.0%), HPV58 (17.9%), HPV18 (10.7%) and HPV31 (10.7%). Increasing age was an independent risk factor associated with presence of single carcinogenic HPV types (adjusted odds ratio: 1.04, 95%CI: 1.01-1.07, p = 0.012) but not with the presence of multiple carcinogenic types in the multivariable-adjusted models.

Conclusions

As HIV-infected women continue to live longer on antiretroviral therapy in China, it will be increasingly important to screen for, and prevent, HPV-associated cervical cancer in this population, especially given the wide diversity and multiplicity of HPV genotypes.
Appendix
Available only for authorised users
Literature
1.
go back to reference GLOBOCAN: Estimated cancer incidence,mortality and prevalence worldwide in 2012. In International Agency for Research on Cancer. 2012. . http://globocan.iarc.fr/ GLOBOCAN: Estimated cancer incidence,mortality and prevalence worldwide in 2012. In International Agency for Research on Cancer. 2012. . GLOBOCAN: Estimated cancer incidence,mortality and prevalence worldwide in 2012. In International Agency for Research on Cancer. 2012. . http://​globocan.​iarc.​fr/​ GLOBOCAN: Estimated cancer incidence,mortality and prevalence worldwide in 2012. In International Agency for Research on Cancer. 2012. .
2.
go back to reference Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V: WHO International Agency for Research on Cancer Monograph Working Group: A review of human carcinogens–Part B: biological agents. Lancet Oncol 2009,10(4):321-322. 10.1016/S1470-2045(09)70096-8PubMedCrossRef Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V: WHO International Agency for Research on Cancer Monograph Working Group: A review of human carcinogens–Part B: biological agents. Lancet Oncol 2009,10(4):321-322. 10.1016/S1470-2045(09)70096-8PubMedCrossRef
3.
go back to reference Clifford GM, Goncalves MA, Franceschi S: Human papillomavirus types among women infected with HIV: a meta-analysis. AIDS 2006,20(18):2337-2344. 10.1097/01.aids.0000253361.63578.14PubMedCrossRef Clifford GM, Goncalves MA, Franceschi S: Human papillomavirus types among women infected with HIV: a meta-analysis. AIDS 2006,20(18):2337-2344. 10.1097/01.aids.0000253361.63578.14PubMedCrossRef
4.
go back to reference Bratcher LF, Sahasrabuddhe VV: The impact of antiretroviral therapy on HPV and cervical intraepithelial neoplasia: current evidence and directions for future research. Infect Agents Canc 2010, 5: 8. 10.1186/1750-9378-5-8CrossRef Bratcher LF, Sahasrabuddhe VV: The impact of antiretroviral therapy on HPV and cervical intraepithelial neoplasia: current evidence and directions for future research. Infect Agents Canc 2010, 5: 8. 10.1186/1750-9378-5-8CrossRef
5.
go back to reference Chaturvedi AK, Madeleine MM, Biggar RJ, Engels EA: Risk of human papillomavirus-associated cancers among persons with AIDS. J Natl Cancer Inst 2009,101(16):1120-1130. 10.1093/jnci/djp205PubMedPubMedCentralCrossRef Chaturvedi AK, Madeleine MM, Biggar RJ, Engels EA: Risk of human papillomavirus-associated cancers among persons with AIDS. J Natl Cancer Inst 2009,101(16):1120-1130. 10.1093/jnci/djp205PubMedPubMedCentralCrossRef
6.
go back to reference Estimates for the HIV/AIDS Epidemic in China. In: 2011. Estimates for the HIV/AIDS Epidemic in China. In: 2011.
7.
go back to reference Comprehensive AIDS/STD Report for Yunnan Province. Prepared for the A2 Analysis & Advocacy Project. In Yunnan Provincial Center for Disease Control and Prevention, United States Agency on International Development, Family Health International. 2007. Comprehensive AIDS/STD Report for Yunnan Province. Prepared for the A2 Analysis & Advocacy Project. In Yunnan Provincial Center for Disease Control and Prevention, United States Agency on International Development, Family Health International. 2007.
8.
go back to reference Zhang HY, Tiggelaar SM, Sahasrabuddhe VV, Smith JS, Jiang CQ, Mei RB, Wang XG, Li ZA, Qiao YL: HPV prevalence and cervical intraepithelial neoplasia among HIV-infected women in Yunnan Province, China: a pilot study. Asian Pac J Canc Prev: APJCP 2012,13(1):91-96. 10.7314/APJCP.2012.13.1.091CrossRef Zhang HY, Tiggelaar SM, Sahasrabuddhe VV, Smith JS, Jiang CQ, Mei RB, Wang XG, Li ZA, Qiao YL: HPV prevalence and cervical intraepithelial neoplasia among HIV-infected women in Yunnan Province, China: a pilot study. Asian Pac J Canc Prev: APJCP 2012,13(1):91-96. 10.7314/APJCP.2012.13.1.091CrossRef
9.
go back to reference Zhang YX, Xiong Y, Gui XE, Rong YP, Cai HB, Ma L: Analysis of cervical HPV infection in HIV positive Chinese women. Zhonghua Chan Ke Za Zhi 2012,47(3):185-190. Zhang YX, Xiong Y, Gui XE, Rong YP, Cai HB, Ma L: Analysis of cervical HPV infection in HIV positive Chinese women. Zhonghua Chan Ke Za Zhi 2012,47(3):185-190.
10.
go back to reference Zhang YX, Xiong Y, Gui XE, Chen SH, Rong YP, Cai HB: Epidemiologic risk profile of human papillomavirus infections in human immunodeficiency virus-positive Chinese women. Jpn J Infect Dis 2011,64(5):411-416.PubMed Zhang YX, Xiong Y, Gui XE, Chen SH, Rong YP, Cai HB: Epidemiologic risk profile of human papillomavirus infections in human immunodeficiency virus-positive Chinese women. Jpn J Infect Dis 2011,64(5):411-416.PubMed
11.
go back to reference Lu L, Jia M, Ma Y, Yang L, Chen Z, Ho DD, Jiang Y, Zhang L: The changing face of HIV in China. Nature 2008,455(7213):609-611.PubMed Lu L, Jia M, Ma Y, Yang L, Chen Z, Ho DD, Jiang Y, Zhang L: The changing face of HIV in China. Nature 2008,455(7213):609-611.PubMed
12.
go back to reference Zhao FH, Lewkowitz AK, Hu SY, Chen F, Li LY, Zhang QM, Wu RF, Li CQ, Wei LH, Xu AD, Zhang WH, Pan QJ, Zhang X, Belinson JL, Sellors JW, Smith JS, Qiao YL, Franceschi S: Prevalence of human papillomavirus and cervical intraepithelial neoplasia in China: a pooled analysis of 17 population-based studies. Int J Canc J Int Canc 2012,131(12):2929-2938. 10.1002/ijc.27571CrossRef Zhao FH, Lewkowitz AK, Hu SY, Chen F, Li LY, Zhang QM, Wu RF, Li CQ, Wei LH, Xu AD, Zhang WH, Pan QJ, Zhang X, Belinson JL, Sellors JW, Smith JS, Qiao YL, Franceschi S: Prevalence of human papillomavirus and cervical intraepithelial neoplasia in China: a pooled analysis of 17 population-based studies. Int J Canc J Int Canc 2012,131(12):2929-2938. 10.1002/ijc.27571CrossRef
13.
go back to reference Mane A, Nirmalkar A, Risbud AR, Vermund SH, Mehendale SM, Sahasrabuddhe VV: HPV genotype distribution in cervical intraepithelial neoplasia among HIV-infected women in Pune. India PloS One 2012,7(6):e38731. 10.1371/journal.pone.0038731PubMedCrossRef Mane A, Nirmalkar A, Risbud AR, Vermund SH, Mehendale SM, Sahasrabuddhe VV: HPV genotype distribution in cervical intraepithelial neoplasia among HIV-infected women in Pune. India PloS One 2012,7(6):e38731. 10.1371/journal.pone.0038731PubMedCrossRef
14.
go back to reference Ghosh I, Ghosh P, Bharti AC, Mandal R, Biswas J, Basu P: Prevalence of human papillomavirus and co-existent sexually transmitted infections among female sex workers, men having sex with men and injectable drug abusers from eastern India. Asian Pac J Canc Prev: APJCP 2012,13(3):799-802. 10.7314/APJCP.2012.13.3.799CrossRef Ghosh I, Ghosh P, Bharti AC, Mandal R, Biswas J, Basu P: Prevalence of human papillomavirus and co-existent sexually transmitted infections among female sex workers, men having sex with men and injectable drug abusers from eastern India. Asian Pac J Canc Prev: APJCP 2012,13(3):799-802. 10.7314/APJCP.2012.13.3.799CrossRef
15.
go back to reference Couture MC, Page K, Stein ES, Sansothy N, Sichan K, Kaldor J, Evans JL, Maher L, Palefsky J: Cervical human papillomavirus infection among young women engaged in sex work in Phnom Penh, Cambodia: prevalence, genotypes, risk factors and association with HIV infection. BMC Infect Dis 2012, 12: 166. 10.1186/1471-2334-12-166PubMedPubMedCentralCrossRef Couture MC, Page K, Stein ES, Sansothy N, Sichan K, Kaldor J, Evans JL, Maher L, Palefsky J: Cervical human papillomavirus infection among young women engaged in sex work in Phnom Penh, Cambodia: prevalence, genotypes, risk factors and association with HIV infection. BMC Infect Dis 2012, 12: 166. 10.1186/1471-2334-12-166PubMedPubMedCentralCrossRef
16.
go back to reference Aggarwal R, Sachdeva RK, Naru J, Suri V, Sharma A, Nijhawan R: HPV genotyping in north Indian women infected with HIV. Int J Gynecol Pathol: Offic J Int Soc Gynecol Pathol 2012,31(5):475-481. 10.1097/PGP.0b013e31824a1d60CrossRef Aggarwal R, Sachdeva RK, Naru J, Suri V, Sharma A, Nijhawan R: HPV genotyping in north Indian women infected with HIV. Int J Gynecol Pathol: Offic J Int Soc Gynecol Pathol 2012,31(5):475-481. 10.1097/PGP.0b013e31824a1d60CrossRef
17.
go back to reference Chen MJ, Wu MY, Yang JH, Chao KH, Yang YS, Ho HN: Increased frequency of genital human papillomavirus infection in human immunodeficiency virus-seropositive Taiwanese women. J Formos Med Assoc Taiwan Yi Zhi 2005,104(1):34-38.PubMed Chen MJ, Wu MY, Yang JH, Chao KH, Yang YS, Ho HN: Increased frequency of genital human papillomavirus infection in human immunodeficiency virus-seropositive Taiwanese women. J Formos Med Assoc Taiwan Yi Zhi 2005,104(1):34-38.PubMed
18.
go back to reference Sirimai K, Chalermchockcharoenkit A, Roongpisuthipong A, Pongprasobchai S: Associated risk factors of human papillomavirus cervical infection among human immunodificiency virus-seropositive women at Siriraj Hospital. J Med Assoc Thailand Chotmaihet Thangphaet 2004,87(3):270-276. Sirimai K, Chalermchockcharoenkit A, Roongpisuthipong A, Pongprasobchai S: Associated risk factors of human papillomavirus cervical infection among human immunodificiency virus-seropositive women at Siriraj Hospital. J Med Assoc Thailand Chotmaihet Thangphaet 2004,87(3):270-276.
19.
go back to reference Strickler HD, Palefsky JM, Burk RD: HPV types present in invasive cervical cancers of HIV-seropositive women. Int J Canc J Int Canc 2008,123(5):1224-1225. 10.1002/ijc.23630CrossRef Strickler HD, Palefsky JM, Burk RD: HPV types present in invasive cervical cancers of HIV-seropositive women. Int J Canc J Int Canc 2008,123(5):1224-1225. 10.1002/ijc.23630CrossRef
20.
go back to reference Strickler HD, Palefsky JM, Shah KV, Anastos K, Klein RS, Minkoff H, Duerr A, Massad LS, Celentano DD, Hall C, Fazzari M, Cu-Uvin S, Bacon M, Schuman P, Levine AM, Durante AJ, Gange S, Melnick S, Burk RD: Human papillomavirus type 16 and immune status in human immunodeficiency virus-seropositive women. J Natl Cancer Inst 2003,95(14):1062-1071. 10.1093/jnci/95.14.1062PubMedCrossRef Strickler HD, Palefsky JM, Shah KV, Anastos K, Klein RS, Minkoff H, Duerr A, Massad LS, Celentano DD, Hall C, Fazzari M, Cu-Uvin S, Bacon M, Schuman P, Levine AM, Durante AJ, Gange S, Melnick S, Burk RD: Human papillomavirus type 16 and immune status in human immunodeficiency virus-seropositive women. J Natl Cancer Inst 2003,95(14):1062-1071. 10.1093/jnci/95.14.1062PubMedCrossRef
21.
go back to reference Vaccarella S, Franceschi S, Snijders PJ, Herrero R, Meijer CJ, Plummer M: Concurrent infection with multiple human papillomavirus types: pooled analysis of the IARC HPV Prevalence Surveys. Canc Epidemiol Biomark Prev: Publ Am Assoc Canc Res Cosponsored Am Soc Prev Oncol 2010,19(2):503-510. 10.1158/1055-9965.EPI-09-0983CrossRef Vaccarella S, Franceschi S, Snijders PJ, Herrero R, Meijer CJ, Plummer M: Concurrent infection with multiple human papillomavirus types: pooled analysis of the IARC HPV Prevalence Surveys. Canc Epidemiol Biomark Prev: Publ Am Assoc Canc Res Cosponsored Am Soc Prev Oncol 2010,19(2):503-510. 10.1158/1055-9965.EPI-09-0983CrossRef
22.
go back to reference Park EK, Cho H, Lee SH, Lee SG, Lee SY, Kim KH, Lee CH, Chung JS, Kwak IS: Human papillomavirus prevalence and genotype distribution among HIV-infected women in Korea. J Korean Med Sci 2014,29(1):32-37. 10.3346/jkms.2014.29.1.32PubMedPubMedCentralCrossRef Park EK, Cho H, Lee SH, Lee SG, Lee SY, Kim KH, Lee CH, Chung JS, Kwak IS: Human papillomavirus prevalence and genotype distribution among HIV-infected women in Korea. J Korean Med Sci 2014,29(1):32-37. 10.3346/jkms.2014.29.1.32PubMedPubMedCentralCrossRef
23.
go back to reference Wu EQ, Liu B, Cui JF, Chen W, Wang JB, Lu L, Niyazi M, Zhao C, Ren SD, Li CQ, Gong XZ, Smith JS, Belinson JL, Liaw KL, Velicer C, Qiao YL: Prevalence of type-specific human papillomavirus and pap results in Chinese women: a multi-center, population-based cross-sectional study. Canc Causes Contr: CCC 2013,24(4):795-803. 10.1007/s10552-013-0162-8CrossRef Wu EQ, Liu B, Cui JF, Chen W, Wang JB, Lu L, Niyazi M, Zhao C, Ren SD, Li CQ, Gong XZ, Smith JS, Belinson JL, Liaw KL, Velicer C, Qiao YL: Prevalence of type-specific human papillomavirus and pap results in Chinese women: a multi-center, population-based cross-sectional study. Canc Causes Contr: CCC 2013,24(4):795-803. 10.1007/s10552-013-0162-8CrossRef
24.
go back to reference Wright TC Jr, Schiffman M: Adding a test for human papillomavirus DNA to cervical-cancer screening. N Engl J Med 2003,348(6):489-490. 10.1056/NEJMp020178PubMedCrossRef Wright TC Jr, Schiffman M: Adding a test for human papillomavirus DNA to cervical-cancer screening. N Engl J Med 2003,348(6):489-490. 10.1056/NEJMp020178PubMedCrossRef
25.
go back to reference Palefsky JM, Gillison ML, Strickler HD: Chapter 16: HPV vaccines in immunocompromised women and men. Vaccine 2006,24(Suppl 3):140-146. 10.1016/j.vaccine.2006.05.120CrossRef Palefsky JM, Gillison ML, Strickler HD: Chapter 16: HPV vaccines in immunocompromised women and men. Vaccine 2006,24(Suppl 3):140-146. 10.1016/j.vaccine.2006.05.120CrossRef
26.
go back to reference Richart RM: Cervical intraepithelial neoplasia. Pathol Annu 1973, 8: 301-328.PubMed Richart RM: Cervical intraepithelial neoplasia. Pathol Annu 1973, 8: 301-328.PubMed
27.
go back to reference Solomon D, Davey D, Kurman R, Moriarty A, O’Connor D, Prey M, Raab S, Sherman M, Wilbur D, Wright T Jr, Young N: Forum Group Members; Bethesda 2001 Workshop: The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA 2002,287(16):2114-2119. 10.1001/jama.287.16.2114PubMedCrossRef Solomon D, Davey D, Kurman R, Moriarty A, O’Connor D, Prey M, Raab S, Sherman M, Wilbur D, Wright T Jr, Young N: Forum Group Members; Bethesda 2001 Workshop: The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA 2002,287(16):2114-2119. 10.1001/jama.287.16.2114PubMedCrossRef
28.
go back to reference Zhu Y, Ding X, Wang Y, Gao J, Shen M, He J: Human papillomavirus infections in women with clinical gynaecological diseases in southwest China. Int J STD AIDS 2012,23(3):e1-e5. 10.1258/ijsa.2009.009015PubMedCrossRef Zhu Y, Ding X, Wang Y, Gao J, Shen M, He J: Human papillomavirus infections in women with clinical gynaecological diseases in southwest China. Int J STD AIDS 2012,23(3):e1-e5. 10.1258/ijsa.2009.009015PubMedCrossRef
Metadata
Title
The diversity of human papillomavirus infection among human immunodeficiency virus-infected women in Yunnan, China
Authors
Hong-Yun Zhang
Man-Dong Fei
Yong Jiang
Qiu-Yue Fei
Hong Qian
Lin Xu
Yu-Ni Jin
Cheng-Qin Jiang
Hai-Xia Li
Sarah M Tiggelaar
Jennifer S Smith
Vikrant V Sahasrabuddhe
You-Lin Qiao
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2014
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-014-0202-3

Other articles of this Issue 1/2014

Virology Journal 1/2014 Go to the issue