Microbiology and Biotechnology Letters (한국미생물·생명공학회지)

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Prevalence of Human Papillomavirus Infection and Genotype Distribution Determined via Real-Time PCR in a Korean Medical Check-up Population

  • Jeon, Jae-Sik (Department of Biomedical Laboratory Science, Dankook University College of Health Sciences) ;
  • Kim, Jong Wan (Department of Laboratory Medicine, Dankook University College of Medicine) ;
  • Kim, Jae Kyung (Department of Biomedical Laboratory Science, Dankook University College of Health Sciences)
  • Received : 2018.03.06
  • Accepted : 2018.03.29
  • Published : 2018.06.28
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Abstract

Human papillomavirus (HPV) plays a critical role in the development of cervical carcinoma. This study analyzed the efficiency of multiplex real-time PCR in detecting and identifying HPV genotypes in samples from women who visited a Korean hospital for checkups. Cervical swab specimens were obtained from women who attended a checkup at the Health Improvement Center of Hospital in Dankook University Cheonan, South Korea and were referred for an HPV genotyping test between January and September 2014. A total of 1703 cervical swab specimens were collected consecutively during this period. PCR results were compared with those of the traditional cytological assay for the same population. Among the 1,703 specimens, 19.91% were HPV positive, of which 14.50% indicated a single infection and 5.40% indicated multiple infections. However, cytology identified only 2.52% of positive cases, including 1.23% cases of atypical squamous cells of undetermined significance, 1% of low grade squamous intra-epithelial lesion, and 0.29% of high grade squamous intra-epithelial lesion. The rate of high-risk and low-risk HPV in the abnormal cytology group was 48 and 23, respectively, and 274 and 136 in the normal group, respectively. HPV types 56, 52, 43 were the most prevalent in that order. Our results confirm the efficiency of the HPV DNA assay for the detection of 28 different HPV genotypes with reasonable sensitivity. A screening strategy that comprises the HPV DNA assay and cytology would help overcome the low sensitivity of a cytological diagnosis.

Keywords

References

  1. An HJ, Cho NH, Lee SY, Kim IH, Lee C, Kim SJ, et al. 2003. Correlation of cervical carcinoma and precancerous lesions with human papillomavirus (HPV) genotypes detected with the HPV DNA chip microarray method. Cancer 97: 1672-1680. https://doi.org/10.1002/cncr.11235
  2. Seol HJ, Ki KD, Lee JM. 2014. Epidemiologic characteristics of cervical cancer in Korean women. J. Gynecol. Oncol. 25: 70-74. https://doi.org/10.3802/jgo.2014.25.1.70
  3. Baudu A, Pretet JL, Riethmuller D, Chotard M, Mougin C, Mercier M. 2014. Prevalence and risk factors of human papillomavirus infection types 16/18/45 in a cohort of French females aged 15-23 years. J. Epidemiol. Glob. Health. 4: 35-43. https://doi.org/10.1016/j.jegh.2013.11.003
  4. Grinsztejn B, Veloso VG, Levi JE, Velasque L, Luz PM, Friedman RK, et al. 2009. Factors associated with increased prevalence of human papillomavirus infection in a cohort of HIV-infected Brazilian women. Int. J. Infect. Dis. 13: 72-80. https://doi.org/10.1016/j.ijid.2008.03.031
  5. Clifford GM, Smith JS, Plummer M, Munoz N, Franceschi S. 2003. Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. Br. J. Cancer. 88: 63-73. https://doi.org/10.1038/sj.bjc.6600688
  6. Jun SY, Park ES, Kim J, Kang J, Lee JJ, Bae Y, et al. 2015. Comparison of the Cobas 4800 HPV and HPV 9G DNA chip tests for detection of high-risk human papillomavirus in cervical specimens of women with consecutive positive HPV tests but negative Pap smears. PLoS One 10: e0140336. https://doi.org/10.1371/journal.pone.0140336
  7. Kim JK, Jeon JS, Lee CH, Kim JW. 2014. Prevalence and genotype distribution of human papillomavirus in Cheonan, Korea. J. Microbiol. Biotechnol. 24: 1143-1147. https://doi.org/10.4014/jmb.1405.05020
  8. Lee GH, Kang HJ, Kim SY, Park CM. 2011. The prevalence of human papilloma virus infections according to Pap smear results in Jeju island. Korean J. Obstet. Gynecol. 54: 689-695. https://doi.org/10.5468/KJOG.2011.54.11.689
  9. Parkin DM, Muir CS. 1992. Cancer incidence in five continents. Comparability and quality of data. IARC Sci. Publ. 120: 45-173.
  10. Pytynia KB, Dahlstrom KR, Sturgis EM. 2014. Epidemiology of HPV-associated oropharyngeal cancer. Oral. Oncol. 50: 380-386. https://doi.org/10.1016/j.oraloncology.2013.12.019
  11. Franco EL, Villa LL, Sobrinho JP, Prado JM, Rousseau MC, Desy M, et al. 1999. Epidemiology of acquisition and clearance of cervical human papillomavirus infection in women from a high-risk area for cervical cancer. J. Infect. Dis. 180: 1415-1423. https://doi.org/10.1086/315086
  12. Woodman CB, Collins S, Winter H, Bailey A, Ellis J, Prior P, et al. 2001. Natural history of cervical human papillomavirus infection in young women: a longitudinal cohort study. Lancet 357: 1831-1836. https://doi.org/10.1016/S0140-6736(00)04956-4
  13. Rosales R, Rosales C. 2014. Immune therapy for human papillomaviruses-related cancers. World. J. Clin. Oncol. 5: 1002-1019. https://doi.org/10.5306/wjco.v5.i5.1002
  14. Kim YJ, Kwon MJ, Woo HY, Paik SY. 2013. Prevalence of human papillomavirus infection and genotype distribution determined by the cyclic-catcher melting temperature analysis in Korean medical checkup population. J. Microbiol. 51: 665-670. https://doi.org/10.1007/s12275-013-3160-3
  15. Chen Q, Xie LX, Qing ZR, Li LJ, Luo ZY, Lin M, et al. 2012. Epidemiologic characterization of human papillomavirus infection in rural Chaozhou, eastern Guangdong Province of China. PLoS One 7: e32149. https://doi.org/10.1371/journal.pone.0032149
  16. Hwang HS, Park M, Lee SY, Kwon KH, Pang MG. 2004. Distribution and prevalence of human papillomavirus genotypes in routine pap smear of 2,470 Korean women determined by DNA chip. Cancer. Epidemiol. Biomarkers. Prev. 13: 2153-2156.
  17. Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, et al. 2003. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N. Engl. J. Med. 348: 518-527. https://doi.org/10.1056/NEJMoa021641
  18. Bosch FX, de Sanjose S. 2013. Chapter 1: human papillomavirus and cervical cancer--burden and assessment of causality. J. Natl. Cancer. Inst. Monogr. 31: 3-13.
  19. Estrade C, Menoud PA, Nardelli-Haefliger D, Sahli R. 2011. Validation of a low-cost human papillomavirus genotyping assay based on PGMY PCR and reverse blotting hybridization with reusable membranes. J. Clin. Microbiol. 49: 3474-3481. https://doi.org/10.1128/JCM.05039-11
  20. Vidal AC, Murphy SK, Hernandez BY, Vasquez B, Bartlett JA, Oneko O, et al. 2011. Distribution of HPV genotypes in cervical intraepithelial lesions and cervical cancer in Tanzanian women. Infect. Agent. Cancer. 6: 20. https://doi.org/10.1186/1750-9378-6-20
  21. Cox JT, Lorincz AT, Schiffman MH, Sherman ME, Cullen A, Kurman RJ. 1995. Human papillomavirus testing by hybrid capture appears to be useful in triaging women with a cytologic diagnosis of atypical squamous cells of undetermined significance. Am. J. Obstet. Gynecol. 172: 946-954. https://doi.org/10.1016/0002-9378(95)90026-8
  22. Cuzick J, Bergeron C, von Knebel Doeberitz M, Gravitt P, Jeronimo J, Lorincz AT, et al. 2012. New technologies and procedures for cervical cancer screening. Vaccine 30: F107-116. https://doi.org/10.1016/j.vaccine.2012.05.088
  23. Nobbenhuis MA, Meijer CJ, van den Brule AJ, Rozendaal L, Voorhorst FJ, Risse EK, et al. 2001. Addition of high-risk HPV testing improves the current guidelines on follow-up after treatment for cervical intraepithelial neoplasia. Br. J. Cancer. 84: 796-801. https://doi.org/10.1054/bjoc.2000.1689
  24. Rabaan AA, Taylor DR, Dawamneh MF, Al-Tawfiq JA. 2017. Comparison of Xpert(R) HPV and Hybrid Capture(R) 2 DNA TestTM for detection of high-risk HPV infection in cervical atypical squamous cells of undetermined significance. J. Infect. Public. Health. 10: 219-223. https://doi.org/10.1016/j.jiph.2016.04.017
  25. Cho NH, An HJ, Jeong JK, Kang S, Kim JW, Kim YT, et al. 2003. Genotyping of 22 human papillomavirus types by DNA chip in Korean women: comparison with cytologic diagnosis. Am. J. Obstet. Gynecol. 188: 56-62. https://doi.org/10.1067/mob.2003.120
  26. Nyitray AG, Iannacone MR. 2014. The epidemiology of human papillomaviruses. Curr. Probl. Dermatol. 45: 75-91.
  27. Seoud M. 2012. Burden of human papillomavirus-related cervical disease in the extended middle East and north Africa-a comprehensive literature review. J. Low. Genit. Tract. Dis. 16: 106-120. https://doi.org/10.1097/LGT.0b013e31823a0108
  28. Clifford GM, Gallus S, Herrero R, Munoz N, Snijders PJ, Vaccarella S, et al. 2005. Worldwide distribution of human papillomavirus types in cytologically normal women in the international agency for research on cancer HPV prevalence surveys: a pooled analysis. Lancet 366: 991-998. https://doi.org/10.1016/S0140-6736(05)67069-9
  29. de Sanjose S, Diaz M, Castellsague X, Clifford G, Bruni L, Munoz N, et al. 2007. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet. Infect. Dis. 7: 453-459. https://doi.org/10.1016/S1473-3099(07)70158-5
  30. Shin HR, Franceschi S, Vaccarella S, Roh JW, Ju YH, Oh JK, et al. 2004. Prevalence and determinants of genital infection with papillomavirus, in female and male university students in Busan, South Korea. J. Infect. Dis. 190: 468-476. https://doi.org/10.1086/421279
  31. Gargiulo F, De Francesco MA, Schreiber C, Ciravolo G, Salinaro F, Valloncini B, et al. 2007. Prevalence and distribution of single and multiple HPV infections in cytologically abnormal cervical samples from Italian women. Virus. Res. 125: 176-182. https://doi.org/10.1016/j.virusres.2006.12.017
  32. Chung S, Shin S, Yoon JH, Roh EY, Seoung SJ, Kim GP, et al. 2013. Prevalence and genotype of human papillomavirus infection and risk of cervical dysplasia among asymptomatic Korean women. Ann. Clin. Microbiol. 16: 87-91. https://doi.org/10.5145/ACM.2013.16.2.87
  33. Bosch FX, Manos MM, Munoz N, Sherman M, Jansen AM, Peto J, et al. 1995. Prevalence of human papillomavirus in cervical cancer: a worldwide perspective. International biological study on cervical cancer (IBSCC) Study Group. J. Natl. Cancer. Inst. 87: 796-802. https://doi.org/10.1093/jnci/87.11.796
  34. Castellsague X, Diaz M, de Sanjose S, Munoz N, Herrero R, Franceschi S, et al. 2006. Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: implications for screening and prevention. J. Natl. Cancer. Inst. 98: 303-315. https://doi.org/10.1093/jnci/djj067
  35. Shin E, Bae H, Song WK, Jung SK, Hwang YS. 2013. Comparative evaluation of the HPV28 detection and HPV DNA chip test for detecting and genotyping human papillomaviruses. Lab. Med. Online 3: 234-241. https://doi.org/10.3343/lmo.2013.3.4.234
  36. Shin HR, Lee DH, Herrero R, Smith JS, Vaccarella S, Hong SH, et al. 2003. Prevalence of human papillomavirus infection in women in Busan, South Korea. Int. J. Cancer. 103: 413-421. https://doi.org/10.1002/ijc.10825
  37. Chen HC, Schiffman M, Lin CY, Pan MH, You SL, Chuang LC, et al. 2011. Persistence of type-specific human papillomavirus infection and increased long-term risk of cervical cancer. J. Natl. Cancer. Inst. 103: 1387-1396. https://doi.org/10.1093/jnci/djr283
  38. Dalstein V, Riethmuller D, Pretet JL, Le Bail Carval K, Sautiere JL, Carbillet JP, et al. 2003. Persistence and load of high-risk HPV are predictors for development of high-grade cervical lesions: a longitudinal French cohort study. Int. J. Cancer. 106: 396-403. https://doi.org/10.1002/ijc.11222
  39. Ho GY, Bierman R, Beardsley L, Chang CJ, Burk RD. 1998. Natural history of cervicovaginal papillomavirus infection in young women. N. Engl. J. Med. 338: 423-428. https://doi.org/10.1056/NEJM199802123380703
  40. Nobbenhuis MA, Walboomers JM, Helmerhorst TJ, Rozendaal L, Remmink AJ, Risse EK, et al. 1999. Relation of human papillomavirus status to cervical lesions and consequences for cervicalcancer screening: a prospective study. Lancet 354: 20-25. https://doi.org/10.1016/S0140-6736(98)12490-X
  41. Wallin KL, Wiklund F, Angström T, Bergman F, Stendahl U, Wadell G, et al. 1999. Type-specific persistence of human papillomavirus DNA before the development of invasive cervical cancer. N. Engl. J. Med. 341: 1633-1638. https://doi.org/10.1056/NEJM199911253412201
  42. Gervais F, Dunton K, Jiang Y, Largeron N. 2017. Systematic review of cost-effectiveness analyses for combinations of prevention strategies against human papillomavirus (HPV) infection: a general trend. BMC Public. Health. 17: 283. https://doi.org/10.1186/s12889-017-4076-3
  43. Lu JF, Shen GR, Li Q, Chen X, Ma CF, Zhu TH. 2017. Genotype distribution characteristics of multiple human papillomavirus in women from the Taihu River Basin, on the coast of eastern China. BMC. Infect. Dis. 17: 226. https://doi.org/10.1186/s12879-017-2328-6
  44. Menon S, van den Broeck D, Rossi R, Ogbe E, Mabeya H. 2017. Multiple HPV infections in female sex workers in Western Kenya: implications for prophylactic vaccines within this sub population. Infect. Agent. Cancer. 12: 2. https://doi.org/10.1186/s13027-016-0114-5
  45. Chan PK, Li WH, Chan MY, Ma WL, Cheung JL, Cheng AF. 1999. High prevalence of human papillomavirus type 58 in Chinese women with cervical cancer and precancerous lesions. J. Med. Virol. 59: 232-238. https://doi.org/10.1002/(SICI)1096-9071(199910)59:2<232::AID-JMV18>3.0.CO;2-7
  46. Sasagawa T, Basha W, Yamazaki H, Inoue M. 2001. High-risk and multiple human papillomavirus infections associated with cervical abnormalities in Japanese women. Cancer. Epidemiol. Biomarkers. Prev. 10: 45-52.
  47. Chang DY, Chen RJ, Lee SC, Huang SC. 1997. Prevalence of single and multiple infection with human papillomaviruses in various grades of cervical neoplasia. J. Med. Microbiol. 46: 54-60. https://doi.org/10.1099/00222615-46-1-54
  48. Trottier H, Franco EL. 2006. Human papillomavirus and cervical cancer: burden of illness and basis for prevention. Am. J. Manag. Care. 12: S462-472.
  49. Trottier H, Mahmud S, Costa MC, Sobrinho JP, Duarte-Franco E, Rohan TE, et al. 2006. Human papillomavirus infections with multiple types and risk of cervical neoplasia. Cancer. Epidemiol. Biomarkers. Prev. 15: 1274-1280. https://doi.org/10.1158/1055-9965.EPI-06-0129