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Erschienen in: International Journal of Clinical Oncology 5/2015

01.10.2015 | Original Article

Oncogenic human papillomavirus is not helpful for cytology screening of the precursor lesions of anal cancers in Taiwanese men who are infected with human immunodeficiency virus

verfasst von: Shu-Hsing Cheng, Chi-Chao Wang, Shih-Lung Chang, Fang-Yeh Chu, Yu-Mei Hsueh

Erschienen in: International Journal of Clinical Oncology | Ausgabe 5/2015

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Abstract

Background

Homosexual men infected with human immunodeficiency virus (HIV) are at increased risk of developing anal cancer. The aim of this study was to assess the clinical sensitivity of anal cytology analysis and oncogenic human papillomavirus (HPV) detection for predicting histological anal intraepithelial neoplasia.

Methods

Between March 2011 and December 2013, we enrolled 196 HIV-positive men in Taoyuan General Hospital, Taiwan. We analyzed the results of thin-preparation anal Pap smears, HPV genotyping, and histology of anoscopic biopsy samples.

Results

The mean age (±standard deviation) was 31.43 (±8.74) years. The proportion (95 % confidence interval) with abnormal thin-preparation anal cytology was 36.2 % (29.8–43.2 %): 16.8 % (12.2–22.7 %) atypical squamous cells of undetermined significance, 14.8 % (10.5–20.4 %) low-grade squamous intraepithelial lesions, and 4.6 % (2.4–8.5 %) high-grade squamous intraepithelial lesions. At least one HPV genotype was detected in 90.8 % of subjects, and the mean number of HPV infection types was 4.41 (±3.24).The frequency of histological high-grade anal intraepithelial lesions was 7.14 % (95 % confidence interval 4.3–11.6 %). Anal cytology yielding atypical squamous cells of undetermined significance or higher grades resulted in a sensitivity of 64.3 %, specificity of 65.9 %, positive predictive value of 12.7 %, and negative predictive value of 96 %. Using both oncogenic HPV and cytology did not provide better performance.

Conclusions

Anal cytology yielding atypical squamous cells of undetermined significance or higher grades could detect two-thirds of high-grade anal intraepithelial neoplasias in HIV-infected men and should be promoted for anal cancer prevention.
Literatur
1.
Zurück zum Zitat Diamond C, Taylor TH, Aboumrad T et al (2005) Increased incidence of squamous cell anal cancer among men with AIDS in the era of highly active antiretroviral therapy. Sex Transm Dis 32:314–320CrossRefPubMed Diamond C, Taylor TH, Aboumrad T et al (2005) Increased incidence of squamous cell anal cancer among men with AIDS in the era of highly active antiretroviral therapy. Sex Transm Dis 32:314–320CrossRefPubMed
2.
Zurück zum Zitat Piketty C, Selinger-Leneman H, Grabar S et al (2008) Marked increase in the incidence of invasive anal cancer among HIV-infected patients despite treatment with combination antiretroviral therapy. AIDS 22:1203–1211CrossRefPubMed Piketty C, Selinger-Leneman H, Grabar S et al (2008) Marked increase in the incidence of invasive anal cancer among HIV-infected patients despite treatment with combination antiretroviral therapy. AIDS 22:1203–1211CrossRefPubMed
3.
Zurück zum Zitat Smyczek P, Singh AE, Romanowski B (2013) Anal intraepithelial neoplasia: review and recommendations for screening and management. Int J STD AIDS 24:843–851CrossRefPubMed Smyczek P, Singh AE, Romanowski B (2013) Anal intraepithelial neoplasia: review and recommendations for screening and management. Int J STD AIDS 24:843–851CrossRefPubMed
4.
Zurück zum Zitat Stanley MA, Winder DM, Sterling JC et al (2012) HPV infection, anal intra-epithelial neoplasia (AIN) and anal cancer: current issues. BMC Cancer 12:398PubMedCentralCrossRefPubMed Stanley MA, Winder DM, Sterling JC et al (2012) HPV infection, anal intra-epithelial neoplasia (AIN) and anal cancer: current issues. BMC Cancer 12:398PubMedCentralCrossRefPubMed
5.
Zurück zum Zitat Kreuter A, Reimann G, Esser S et al (2003) Screening and therapy of anal intraepithelial neoplasia (AIN) and anal carcinoma in patients with HIV-infection. Dtsch Med Wochenschr 128:1957–1962CrossRefPubMed Kreuter A, Reimann G, Esser S et al (2003) Screening and therapy of anal intraepithelial neoplasia (AIN) and anal carcinoma in patients with HIV-infection. Dtsch Med Wochenschr 128:1957–1962CrossRefPubMed
6.
Zurück zum Zitat Machalek DA, Poynten M, Jin F et al (2012) Anal human papillomavirus infection and associated neoplastic lesions in men who have sex with men: a systematic review and meta-analysis. Lancet Oncol 13:487–500CrossRefPubMed Machalek DA, Poynten M, Jin F et al (2012) Anal human papillomavirus infection and associated neoplastic lesions in men who have sex with men: a systematic review and meta-analysis. Lancet Oncol 13:487–500CrossRefPubMed
7.
Zurück zum Zitat Zbar AP, Fenger C, Efron J (2002) The pathology and molecular biology of anal intraepithelial neoplasia: comparisons with cervical and vulvar intraepithelial carcinoma. Int J Colorectal Dis 17:203–215CrossRefPubMed Zbar AP, Fenger C, Efron J (2002) The pathology and molecular biology of anal intraepithelial neoplasia: comparisons with cervical and vulvar intraepithelial carcinoma. Int J Colorectal Dis 17:203–215CrossRefPubMed
8.
Zurück zum Zitat Darragh TM, Winkler B (2011) Anal cancer and cervical cancer screening: key differences. Cancer Cytopathol 119:5–19CrossRefPubMed Darragh TM, Winkler B (2011) Anal cancer and cervical cancer screening: key differences. Cancer Cytopathol 119:5–19CrossRefPubMed
9.
Zurück zum Zitat Ho GY, Bierman R, Beardsley L et al (1998) Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 338:423–428CrossRefPubMed Ho GY, Bierman R, Beardsley L et al (1998) Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med 338:423–428CrossRefPubMed
10.
Zurück zum Zitat Patel P, Hanson DL, Sullivan PS et al (2008) Incidence of types of cancer among HIV-infected persons compared with the general population in the United States, 1992–2003. Ann Intern Med 148:728–736CrossRefPubMed Patel P, Hanson DL, Sullivan PS et al (2008) Incidence of types of cancer among HIV-infected persons compared with the general population in the United States, 1992–2003. Ann Intern Med 148:728–736CrossRefPubMed
11.
Zurück zum Zitat Grulich AE, Jin F, Poynten IM et al (2013) 14. Natural history of high-grade squamous intraepithelial lesions (HSIL) in homosexual men: early evidence from the Study of the Prevention of Anal Cancer (SPANC). Sex Health 10:576CrossRef Grulich AE, Jin F, Poynten IM et al (2013) 14. Natural history of high-grade squamous intraepithelial lesions (HSIL) in homosexual men: early evidence from the Study of the Prevention of Anal Cancer (SPANC). Sex Health 10:576CrossRef
12.
Zurück zum Zitat Kreuter A, Potthoff A, Brockmeyer NH et al (2010) Anal carcinoma in human immunodeficiency virus-positive men: results of a prospective study from Germany. Br J Dermatol 162:1269–1277CrossRefPubMed Kreuter A, Potthoff A, Brockmeyer NH et al (2010) Anal carcinoma in human immunodeficiency virus-positive men: results of a prospective study from Germany. Br J Dermatol 162:1269–1277CrossRefPubMed
13.
Zurück zum Zitat Center for Disease Control (2014) Statistics of communicable diseases and surveillance reports in Taiwan area, Dec. 2013. Center for Disease Control, Department of Health and Welfare, Executive Yuan, Taiwan Center for Disease Control (2014) Statistics of communicable diseases and surveillance reports in Taiwan area, Dec. 2013. Center for Disease Control, Department of Health and Welfare, Executive Yuan, Taiwan
14.
Zurück zum Zitat Yu CT, Chao SC, Lee HC et al (2013) High prevalence of anal human papillomavirus infection and associated risky behaviors in men infected with human immunodeficiency virus in Taiwan. AIDS Behav 17:1211–1218CrossRefPubMed Yu CT, Chao SC, Lee HC et al (2013) High prevalence of anal human papillomavirus infection and associated risky behaviors in men infected with human immunodeficiency virus in Taiwan. AIDS Behav 17:1211–1218CrossRefPubMed
15.
Zurück zum Zitat Cheng SH, Chu FY, Wang CC et al (2014) Screening and risk factors for anal cancer precursors in men infected with HIV in Taiwan. J Med Virol 86:193–201CrossRefPubMed Cheng SH, Chu FY, Wang CC et al (2014) Screening and risk factors for anal cancer precursors in men infected with HIV in Taiwan. J Med Virol 86:193–201CrossRefPubMed
16.
Zurück zum Zitat Solomon D, Davey D, Kurman R et al (2002) The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA 287:2114–2119CrossRefPubMed Solomon D, Davey D, Kurman R et al (2002) The 2001 Bethesda System: terminology for reporting results of cervical cytology. JAMA 287:2114–2119CrossRefPubMed
17.
Zurück zum Zitat Hillman RJ, van Leeuwen MT, Vajdic CM et al (2012) Prevalence and predictors of high-grade anal intraepithelial neoplasia in a community-based sample of homosexual men. Sex Health 9:574–579CrossRefPubMed Hillman RJ, van Leeuwen MT, Vajdic CM et al (2012) Prevalence and predictors of high-grade anal intraepithelial neoplasia in a community-based sample of homosexual men. Sex Health 9:574–579CrossRefPubMed
18.
Zurück zum Zitat Sahasrabuddhe VV, Castle PE, Follansbee S et al (2013) Human papillomavirus genotype attribution and estimation of preventable fraction of anal intraepithelial neoplasia cases among HIV-infected men who have sex with men. J Infect Dis 207:392–401PubMedCentralCrossRefPubMed Sahasrabuddhe VV, Castle PE, Follansbee S et al (2013) Human papillomavirus genotype attribution and estimation of preventable fraction of anal intraepithelial neoplasia cases among HIV-infected men who have sex with men. J Infect Dis 207:392–401PubMedCentralCrossRefPubMed
19.
Zurück zum Zitat Goldstone SE, Enyinna CS, Davis TW (2009) Detection of oncogenic human papillomavirus and other predictors of anal high-grade dysplasia in men who have sex with men with abnormal cytology. Dis Colon Rectum 52:31–39CrossRefPubMed Goldstone SE, Enyinna CS, Davis TW (2009) Detection of oncogenic human papillomavirus and other predictors of anal high-grade dysplasia in men who have sex with men with abnormal cytology. Dis Colon Rectum 52:31–39CrossRefPubMed
20.
Zurück zum Zitat Goldstone SE, Moshier E (2010) Detection of oncogenic human papillomavirus impacts anal screening guidelines in men who have sex with men. Dis Colon Rectum 53:1135–1142CrossRefPubMed Goldstone SE, Moshier E (2010) Detection of oncogenic human papillomavirus impacts anal screening guidelines in men who have sex with men. Dis Colon Rectum 53:1135–1142CrossRefPubMed
21.
Zurück zum Zitat Tamalet C, Obry-Roguet V, Ressiot E et al (2014) Distribution of human papillomavirus genotypes, assessment of HPV 16 and 18 viral load and anal related lesions in HIV positive patients: a cross-sectional analysis. J Med Virol 87:419–425CrossRef Tamalet C, Obry-Roguet V, Ressiot E et al (2014) Distribution of human papillomavirus genotypes, assessment of HPV 16 and 18 viral load and anal related lesions in HIV positive patients: a cross-sectional analysis. J Med Virol 87:419–425CrossRef
22.
Zurück zum Zitat Svare EI, Kjaer SK, Worm AM et al (2002) Risk factors for genital HPV DNA in men resemble those found in women: a study of male attendees at a Danish STD clinic. Sex Transm Infect 78:215–218PubMedCentralCrossRefPubMed Svare EI, Kjaer SK, Worm AM et al (2002) Risk factors for genital HPV DNA in men resemble those found in women: a study of male attendees at a Danish STD clinic. Sex Transm Infect 78:215–218PubMedCentralCrossRefPubMed
23.
Zurück zum Zitat Syrjanen SM, von Krogh G, Syrjanen KJ (1989) Anal condylomas in men, part 1. Histopathological and virological assessment. Genitourin Med 65:216–224PubMedCentralPubMed Syrjanen SM, von Krogh G, Syrjanen KJ (1989) Anal condylomas in men, part 1. Histopathological and virological assessment. Genitourin Med 65:216–224PubMedCentralPubMed
24.
Zurück zum Zitat Holly EA, Whittemore AS, Aston DA et al (1989) Anal cancer incidence: genital warts, anal fissure or fistula, hemorrhoids, and smoking. J Natl Cancer Inst 81:1726–1731CrossRefPubMed Holly EA, Whittemore AS, Aston DA et al (1989) Anal cancer incidence: genital warts, anal fissure or fistula, hemorrhoids, and smoking. J Natl Cancer Inst 81:1726–1731CrossRefPubMed
25.
Zurück zum Zitat Stewart D, Kazemi S, Li S et al (2004) Ubiquitination and proteasome degradation of the E6 proteins of human papillomavirus types 11 and 18. J Gen Virol 85:1419–1426CrossRefPubMed Stewart D, Kazemi S, Li S et al (2004) Ubiquitination and proteasome degradation of the E6 proteins of human papillomavirus types 11 and 18. J Gen Virol 85:1419–1426CrossRefPubMed
26.
Zurück zum Zitat Crum-Cianflone NF, Hullsiek KH, Marconi VC et al (2010) Anal cancers among HIV-infected persons: HAART is not slowing rising incidence. AIDS 24:535–543PubMedCentralCrossRefPubMed Crum-Cianflone NF, Hullsiek KH, Marconi VC et al (2010) Anal cancers among HIV-infected persons: HAART is not slowing rising incidence. AIDS 24:535–543PubMedCentralCrossRefPubMed
27.
Zurück zum Zitat D’Souza G, Wiley DJ, Li X et al (2008) Incidence and epidemiology of anal cancer in the multicenter AIDS cohort study. J Acquir Immune Defic Syndr 48:491–499PubMedCentralCrossRefPubMed D’Souza G, Wiley DJ, Li X et al (2008) Incidence and epidemiology of anal cancer in the multicenter AIDS cohort study. J Acquir Immune Defic Syndr 48:491–499PubMedCentralCrossRefPubMed
28.
Zurück zum Zitat Silverberg MJ, Lau B, Justice AC et al (2012) Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America. Clin Infect Dis 54:1026–1034PubMedCentralCrossRefPubMed Silverberg MJ, Lau B, Justice AC et al (2012) Risk of anal cancer in HIV-infected and HIV-uninfected individuals in North America. Clin Infect Dis 54:1026–1034PubMedCentralCrossRefPubMed
29.
Zurück zum Zitat Dona MG, Benevolo M, Vocaturo A et al (2012) Anal cytological abnormalities and epidemiological correlates among men who have sex with men at risk for HIV-1 infection. BMC Cancer 12:476PubMedCentralCrossRefPubMed Dona MG, Benevolo M, Vocaturo A et al (2012) Anal cytological abnormalities and epidemiological correlates among men who have sex with men at risk for HIV-1 infection. BMC Cancer 12:476PubMedCentralCrossRefPubMed
30.
Zurück zum Zitat Cheng SH, Chu FY, Lin YS et al (2012) Influence of age and CD4+ T cell counts on the prevalence of genital human papillomavirus infection among HIV-seropositive men who have sex with men in Taiwan. J Med Virol 84:1876–1883CrossRefPubMed Cheng SH, Chu FY, Lin YS et al (2012) Influence of age and CD4+ T cell counts on the prevalence of genital human papillomavirus infection among HIV-seropositive men who have sex with men in Taiwan. J Med Virol 84:1876–1883CrossRefPubMed
31.
Zurück zum Zitat de Pokomandy A, Rouleau D, Ghattas G et al (2011) HAART and progression to high-grade anal intraepithelial neoplasia in men who have sex with men and are infected with HIV. Clin Infect Dis 52:1174–1181CrossRefPubMed de Pokomandy A, Rouleau D, Ghattas G et al (2011) HAART and progression to high-grade anal intraepithelial neoplasia in men who have sex with men and are infected with HIV. Clin Infect Dis 52:1174–1181CrossRefPubMed
32.
Zurück zum Zitat Palefsky JM, Holly EA (2003) Chapter 6: immunosuppression and co-infection with HIV. J Natl Cancer Inst Monogr 31:41–46CrossRefPubMed Palefsky JM, Holly EA (2003) Chapter 6: immunosuppression and co-infection with HIV. J Natl Cancer Inst Monogr 31:41–46CrossRefPubMed
33.
Zurück zum Zitat Salit IE, Lytwyn A, Raboud J et al (2010) The role of cytology (Pap tests) and human papillomavirus testing in anal cancer screening. AIDS 24:1307–1313PubMed Salit IE, Lytwyn A, Raboud J et al (2010) The role of cytology (Pap tests) and human papillomavirus testing in anal cancer screening. AIDS 24:1307–1313PubMed
34.
Zurück zum Zitat Lam JM, Hoch JS, Tinmouth J et al (2011) Cost-effectiveness of screening for anal precancers in HIV-positive men. AIDS 25:635–642CrossRefPubMed Lam JM, Hoch JS, Tinmouth J et al (2011) Cost-effectiveness of screening for anal precancers in HIV-positive men. AIDS 25:635–642CrossRefPubMed
35.
Zurück zum Zitat Palefsky JM, Holly EA, Gonzales J et al (1992) Natural history of anal cytologic abnormalities and papillomavirus infection among homosexual men with group IV HIV disease. J Acquir Immune Defic Syndr 5:1258–1265CrossRefPubMed Palefsky JM, Holly EA, Gonzales J et al (1992) Natural history of anal cytologic abnormalities and papillomavirus infection among homosexual men with group IV HIV disease. J Acquir Immune Defic Syndr 5:1258–1265CrossRefPubMed
36.
Zurück zum Zitat Cranston RD, Darragh TM, Holly EA et al (2004) Self-collected versus clinician-collected anal cytology specimens to diagnose anal intraepithelial neoplasia in HIV-positive men. J Acquir Immune Defic Syndr 36:915–920CrossRefPubMed Cranston RD, Darragh TM, Holly EA et al (2004) Self-collected versus clinician-collected anal cytology specimens to diagnose anal intraepithelial neoplasia in HIV-positive men. J Acquir Immune Defic Syndr 36:915–920CrossRefPubMed
37.
Zurück zum Zitat Fox PA, Seet JE, Stebbing J et al (2005) The value of anal cytology and human papillomavirus typing in the detection of anal intraepithelial neoplasia: a review of cases from an anoscopy clinic. Sex Transm Infect 81:142–146PubMedCentralCrossRefPubMed Fox PA, Seet JE, Stebbing J et al (2005) The value of anal cytology and human papillomavirus typing in the detection of anal intraepithelial neoplasia: a review of cases from an anoscopy clinic. Sex Transm Infect 81:142–146PubMedCentralCrossRefPubMed
38.
Zurück zum Zitat Betancourt EM, Wahbah MM, Been LC et al (2013) Anal cytology as a predictor of anal intraepithelial neoplasia in HIV-positive men and women. Diagn Cytopathol 41:697–702CrossRefPubMed Betancourt EM, Wahbah MM, Been LC et al (2013) Anal cytology as a predictor of anal intraepithelial neoplasia in HIV-positive men and women. Diagn Cytopathol 41:697–702CrossRefPubMed
39.
Zurück zum Zitat Berry JM, Palefsky JM, Jay N et al (2009) Performance characteristics of anal cytology and human papillomavirus testing in patients with high-resolution anoscopy-guided biopsy of high-grade anal intraepithelial neoplasia. Dis Colon Rectum 52:239–247CrossRefPubMed Berry JM, Palefsky JM, Jay N et al (2009) Performance characteristics of anal cytology and human papillomavirus testing in patients with high-resolution anoscopy-guided biopsy of high-grade anal intraepithelial neoplasia. Dis Colon Rectum 52:239–247CrossRefPubMed
40.
Zurück zum Zitat Wentzensen N, Follansbee S, Borgonovo S et al (2012) Human papillomavirus genotyping, human papillomavirus mRNA expression, and p16/Ki-67 cytology to detect anal cancer precursors in HIV-infected MSM. AIDS 26:2185–2192PubMedCentralCrossRefPubMed Wentzensen N, Follansbee S, Borgonovo S et al (2012) Human papillomavirus genotyping, human papillomavirus mRNA expression, and p16/Ki-67 cytology to detect anal cancer precursors in HIV-infected MSM. AIDS 26:2185–2192PubMedCentralCrossRefPubMed
Metadaten
Titel
Oncogenic human papillomavirus is not helpful for cytology screening of the precursor lesions of anal cancers in Taiwanese men who are infected with human immunodeficiency virus
verfasst von
Shu-Hsing Cheng
Chi-Chao Wang
Shih-Lung Chang
Fang-Yeh Chu
Yu-Mei Hsueh
Publikationsdatum
01.10.2015
Verlag
Springer Japan
Erschienen in
International Journal of Clinical Oncology / Ausgabe 5/2015
Print ISSN: 1341-9625
Elektronische ISSN: 1437-7772
DOI
https://doi.org/10.1007/s10147-015-0804-9

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