DOI QR코드

DOI QR Code

Risk factors for cytological progression in HPV 16 infected women with ASC-US or LSIL: The Korean HPV cohort

  • So, Kyeong A (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, College of Medicine, Dankook University) ;
  • Kim, Seon Ah (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, College of Medicine, Dankook University) ;
  • Lee, Yoo Kyung (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, College of Medicine, Dankook University) ;
  • Lee, In Ho (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, College of Medicine, Dankook University) ;
  • Lee, Ki Heon (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, College of Medicine, Dankook University) ;
  • Rhee, Jee Eun (Division of Viral Disease Research Center for Infectious Disease Research, National Institute of Health, Korea Centers for Disease Control and Prevention) ;
  • Kee, Mee Kyung (Division of Viral Disease Research Center for Infectious Disease Research, National Institute of Health, Korea Centers for Disease Control and Prevention) ;
  • Cho, Chi Heum (Department of Obstetrics and Gynecology, Keimyung University Dongsan Medical Center) ;
  • Hong, Sung Ran (Department of Pathology, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Hwang, Chang Sun (Human Resource Biobank, Cheil General Hospital and Women's Healthcare Center, Dankook University College of Medicine) ;
  • Jeong, Mi Seon (Laboratory of R&D for Genomics, Cheil General Hospital and Women's Healthcare Center, College of Medicine, Dankook University) ;
  • Kim, Ki Tae (Department of Obstetrics and Gynecology, Busan Paik Hospital, Inje University College of Medicine) ;
  • Ki, Moran (Department of Cancer Control and Policy, Graduate School of Cancer Science and Policy, National Cancer Center) ;
  • Hur, Soo Young (Department of Obstetrics and Gynecology, Seoul St. Mary's Hospital, The Catholic University) ;
  • Park, Jong Sup (Department of Obstetrics and Gynecology, Seoul St. Mary's Hospital, The Catholic University) ;
  • Kim, Tae Jin (Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center, College of Medicine, Dankook University)
  • Received : 2017.11.18
  • Accepted : 2018.03.08
  • Published : 2018.11.15

Abstract

Objective This study was to identify the risk factors for cytological progression in women with atypical squamous cells of undetermined significance (ASC-US) or low-grade squamous intraepithelial lesions (LSIL). Methods We analyzed data from women infected with the human papillomavirus (HPV) who participated in the Korean HPV cohort study. The cohort recruited women aged 20-60 years with abnormal cervical cytology (ASC-US or LSIL) from April 2010. All women were followed-up at every 6-month intervals with cervical cytology and HPV DNA testing. Results Of the 1,158 women included, 654 (56.5%) and 504 (43.5%) women showed ASC-US and LSIL, respectively. At the time of enrollment, 143 women tested positive for HPV 16 (85 single and 58 multiple infections). Cervical cytology performed in the HPV 16-positive women showed progression in 27%, no change in 23%, and regression in 50% of the women at the six-month follow-up. The progression rate associated with HPV 16 infection was higher than that with infection caused by other HPV types (relative risk [RR], 1.75; 95% confidence interval [CI], 1.08-2.84; P=0.028). The cytological progression rate in women with persistent HPV 16 infection was higher than that in women with incidental or cleared infections (P<0.001). Logistic regression analysis showed a significant relationship between cigarette smoking and cytological progression (RR, 4.15; 95% CI, 1.01-17.00). Conclusion The cytological progression rate in HPV 16-positive women with ASC-US or LSIL is higher than that in women infected with other HPV types. Additionally, cigarette smoking may play a role in cytological progression.

Keywords

Acknowledgement

Supported by : Korea Centers for Disease Control and Prevention

References

  1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin 2015;65:87-108. https://doi.org/10.3322/caac.21262
  2. Jung KW, Won YJ, Oh CM, Kong HJ, Cho H, Lee DH, et al. Prediction of cancer incidence and mortality in Korea, 2015. Cancer Res Treat 2015;47:142-8. https://doi.org/10.4143/crt.2015.066
  3. Jung KW, Won YJ, Oh CM, Kong HJ, Lee DH, Lee KH; et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2014. Cancer Res Treat 2017;49:292-305. https://doi.org/10.4143/crt.2017.118
  4. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-9. https://doi.org/10.1002/(SICI)1096-9896(199909)189:1<12::AID-PATH431>3.0.CO;2-F
  5. Choi YJ, Park JS. Clinical significance of human papillomavirus genotyping. J Gynecol Oncol 2016;27:e21. https://doi.org/10.3802/jgo.2016.27.e21
  6. Cho HW, So KA, Lee JK, Hong JH. Type-specific persistence or regression of human papillomavirus genotypes in women with cervical intraepithelial neoplasia 1: a prospective cohort study. Obstet Gynecol Sci 2015;58:40-5. https://doi.org/10.5468/ogs.2015.58.1.40
  7. Koshiol J, Lindsay L, Pimenta JM, Poole C, Jenkins D, Smith JS. Persistent human papillomavirus infection and cervical neoplasia: a systematic review and meta-analysis. Am J Epidemiol 2008;168:123-37. https://doi.org/10.1093/aje/kwn036
  8. Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003;348:518-27. https://doi.org/10.1056/NEJMoa021641
  9. Castellsague X. Natural history and epidemiology of HPV infection and cervical cancer. Gynecol Oncol 2008;110 Suppl 2:S4-7. https://doi.org/10.1016/j.ygyno.2008.07.045
  10. Khan MJ, Castle PE, Lorincz AT, Wacholder S, Sherman M, Scott DR, et al. The elevated 10-year risk of cervical precancer and cancer in women with human papillomavirus (HPV) type 16 or 18 and the possible utility of typespecific HPV testing in clinical practice. J Natl Cancer Inst 2005;97:1072-9. https://doi.org/10.1093/jnci/dji187
  11. Cox JT, Schiffman M, Solomon D; ASCUS-LSIL Triage Study (ALTS) Group. Prospective follow-up suggests similar risk of subsequent cervical intraepithelial neoplasia grade 2 or 3 among women with cervical intraepithelial neoplasia grade 1 or negative colposcopy and directed biopsy. Am J Obstet Gynecol 2003;188:1406-12. https://doi.org/10.1067/mob.2003.461
  12. Pretorius RG, Peterson P, Azizi F, Burchette RJ. Subsequent risk and presentation of cervical intraepithelial neoplasia (CIN) 3 or cancer after a colposcopic diagnosis of CIN 1 or less. Am J Obstet Gynecol 2006;195:1260-5. https://doi.org/10.1016/j.ajog.2006.07.036
  13. Chen EY, Tran A, Raho CJ, Birch CM, Crum CP, Hirsch MS. Histological 'progression' from low (LSIL) to high (HSIL) squamous intraepithelial lesion is an uncommon event and an indication for quality assurance review. Mod Pathol 2010;23:1045-51. https://doi.org/10.1038/modpathol.2010.85
  14. Kim JY, Nam BH, Lee JA. Is human papillomavirus genotype an influencing factor on radiotherapy outcome? Ambiguity caused by an association of HPV 18 genotype and adenocarcinoma histology. J Gynecol Oncol 2011;22:32-8. https://doi.org/10.3802/jgo.2011.22.1.32
  15. Lee WC, Lee SY, Koo YJ, Kim TJ, Hur SY, Hong SR, et al. Establishment of a Korea HPV cohort study. J Gynecol Oncol 2013;24:59-65. https://doi.org/10.3802/jgo.2013.24.1.59
  16. Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, et al. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer 2007;121:621-32. https://doi.org/10.1002/ijc.22527
  17. Saslow D, Solomon D, Lawson HW, Killackey M, Kulasingam SL, Cain J, et al. American Cancer Society, American Society for Colposcopy and Cervical Pathology, and American Society for Clinical Pathology screening guidelines for the prevention and early detection of cervical cancer. Am J Clin Pathol 2012;137:516-42. https://doi.org/10.1309/AJCPTGD94EVRSJCG
  18. Wang SS, Zuna RE, Wentzensen N, Dunn ST, Sherman ME, Gold MA, et al. Human papillomavirus cofactors by disease progression and human papillomavirus types in the study to understand cervical cancer early endpoints and determinants. Cancer Epidemiol Biomarkers Prev 2009;18:113-20. https://doi.org/10.1158/1055-9965.EPI-08-0591
  19. Castellsague X, Munoz N. Chapter 3: cofactors in human papillomavirus carcinogenesis--role of parity, oral contraceptives, and tobacco smoking. J Natl Cancer Inst Monogr 2003;31:20-8.
  20. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Tobacco smoke and involuntary smoking. IARC Monogr Eval Carcinog Risks Hum 2004;83:1-1438.
  21. Appleby P, Beral V, Berrington de Gonzalez A, Colin D, Franceschi S, Goodill A, et al. Carcinoma of the cervix and tobacco smoking: collaborative reanalysis of individual data on 13,541 women with carcinoma of the cervix and 23,017 women without carcinoma of the cervix from 23 epidemiological studies. Int J Cancer 2006;118:1481-95. https://doi.org/10.1002/ijc.21493
  22. Vaccarella S, Herrero R, Snijders PJ, Dai M, Thomas JO, Hieu NT, et al. Smoking and human papillomavirus infection: pooled analysis of the International Agency for Research on Cancer HPV Prevalence Surveys. Int J Epidemiol 2008;37:536-46. https://doi.org/10.1093/ije/dyn033
  23. Poppe WA, Ide PS, Drijkoningen MP, Lauweryns JM, Van Assche FA. Tobacco smoking impairs the local immunosurveillance in the uterine cervix. An immunohistochemical study. Gynecol Obstet Invest 1995;39:34-8. https://doi.org/10.1159/000292372
  24. Poppe WA, Peeters R, Drijkoningen M, Ide PS, Daenens P, Lauweryns JM, et al. Cervical cotinine and macrophage-Langerhans cell density in the normal human uterine cervix. Gynecol Obstet Invest 1996;41:253-9. https://doi.org/10.1159/000292280
  25. Barton SE, Maddox PH, Jenkins D, Edwards R, Cuzick J, Singer A. Effect of cigarette smoking on cervical epithelial immunity: a mechanism for neoplastic change? Lancet 1988;2:652-4.
  26. de Jong A, van Poelgeest MI, van der Hulst JM, Drijfhout JW, Fleuren GJ, Melief CJ, et al. Human papillomavirus type 16-positive cervical cancer is associated with impaired CD4+ T-cell immunity against early antigens E2 and E6. Cancer Res 2004;64:5449-55. https://doi.org/10.1158/0008-5472.CAN-04-0831
  27. Evans EM, Man S, Evans AS, Borysiewicz LK. Infiltration of cervical cancer tissue with human papillomavirus-specific cytotoxic T-lymphocytes. Cancer Res 1997;57:2943-50.
  28. Herrero R, Brinton LA, Reeves WC, Brenes MM, Tenorio F, de Britton RC, et al. Invasive cervical cancer and smoking in Latin America. J Natl Cancer Inst 1989;81:205-11. https://doi.org/10.1093/jnci/81.3.205
  29. Schlecht NF, Platt RW, Duarte-Franco E, Costa MC, Sobrinho JP, Prado JC, et al. Human papillomavirus infection and time to progression and regression of cervical intraepithelial neoplasia. J Natl Cancer Inst 2003;95:1336-43. https://doi.org/10.1093/jnci/djg037

Cited by

  1. Combined Effect of Secondhand Smoking and Alcohol Drinking on Risk of Persistent Human Papillomavirus Infection vol.2019, pp.None, 2019, https://doi.org/10.1155/2019/5829676
  2. Role of polycyclic aromatic hydrocarbons as a co-factor in human papillomavirus-mediated carcinogenesis vol.19, pp.None, 2018, https://doi.org/10.1186/s12885-019-5347-4
  3. Association of HLA-A, -B, DRB, and DQB Alleles with Persistent HPV-16 Infection in Women from Tamil Nadu, India vol.32, pp.10, 2018, https://doi.org/10.1089/vim.2019.0094
  4. Vaccination in Inflammatory Bowel Disease: Utility and Future Perspective vol.2, pp.2, 2018, https://doi.org/10.3390/gidisord2020019
  5. Enhanced disease progression due to persistent HPV-16/58 infections in Korean women: a systematic review and the Korea HPV cohort study vol.18, pp.1, 2018, https://doi.org/10.1186/s12985-021-01657-2