Comparison of molecular techniques for the detection of high and low risk types of human papillomavirus in cervical cell samples from Paraguayan women.
DOI:
https://doi.org/10.18004/mem.iics/1812-9528/2024.%20e22122405Keywords:
HR-HPV (High-risk human papillomavirus), cervical cancer (CC), Diagnostic TestsAbstract
The human papillomavirus (HPV) is related to the development of cervical cancer (CCU), the fourth leading cause of death in women worldwide. In our country, the incidence and mortality rate of CCU is 30.6 and 16.7 per 100,000 women, respectively; being a public health problem. HPVs are divided into those of high oncogenic risk (HR-HPV), associated with cervical intraepithelial neoplasia (CIN) and low oncogenic risk (LR-HPV), related to genital warts. In this study, we use exfoliated cervical cells from 218 randomly selected Paraguayan women that were analyzed by real-time PCR (Abbott). In addition, the samples were analyzed by reverse hybridization (CLART® HPV2), which detects 35 types of HR-HPV and also types of probable HR-HPV and LR-HPV. Of the samples tested by reverse hybridization, the most prevalent types in single infections were HPV-16 and HPV-18 of the HR-HPVs. Among the HR-HPVs, HPV-53 was the most detected type and among the HR-HPVs, HPV-84. HPV-6 (low-risk) was detected in only one single sample and in 3 multiple infections. The concordance for detection of HR-HPV, comparing both methods, was 78.44%, with a kappa coefficient of 0.50; 95% CI (0.38-0.62), similar to that reported in studies in other countries. This is one of the first studies with the reverse hybridization technique in the country, a useful technique for post-vaccination studies, since it detects types not included in the vaccines.
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References
1. Szymonowicz KA, Chen J. Biological and clinical aspects of VPH-related cancers. Cancer Biol Med. 2020 Nov 15; 17(4): 864-78. 10.20892/j.issn.2095-3941.2020.0370
2. Piña-Sánchez P. Human Papillomavirus: Challenges and Opportunities for the Control of Cervical Cancer. Arch Med Res. 2022 Dec; 53(8): 753-769. 10.1016/j.arcmed.2022.11.009
3. Estrategia mundial para acelerar la eliminación del cáncer del cuello uterino como problema de salud pública [Global strategy to accelerate the elimination of cervical cancer as a public health problem]. Ginebra: Organización Mundial de la Salud; 2022. Licencia: CC BY-NC-SA 3.0 IGO. https://iris.who.int/bitstream/handle/10665/336583/9789240014107-eng.pdf?sequence=1
4. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, et al. WHO International Agency for Research on Cancer Monograph Working Group. A review of human carcinogens--Part B: biological agents. Lancet Oncol. 2009 Apr; 10(4): 321-2. 10.1016/s1470-2045(09)70096-8
5. Meisal R, Rounge TB, Christiansen IK, Eieland AK, Worren MM, Molden TF, et al. VPH Genotyping of Modified General Primer-Amplicons Is More Analytically Sensitive and Specific by Sequencing than by Hybridization. PLoS One. 2017 Jan 3;12(1) 10.1371/journal.pone.0169074.
6. Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries. CA Cancer J Clin. 2021 May; 71(3): 209-49 10.3322/caac.21660.
7. Global Cancer Observatory. International Agency for Research on Cancer. WHO 2022. Estimated age-standarized cancer incidence, mortality and prevalence worldwide in 2022. Disponible en: https://gco.iarc.fr/today/home (Acceso febrero de 2024).
8. Ronco G, Dillner J, Elfström KM, Tunesi S, Snijders PJ, Arbyn M, et al. International VPH screening working group. Efficacy of VPH-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials. Lancet. 2014 Feb 8;383 (9916): 524-32. 10.1016/S0140-6736(13)62218-7
9. Bruni L, Serrano B, Roura E, Alemany L, Cowan M, Herrero R, et al Cervical cancer screening programmes and age-specific coverage estimates for 202 countries and territories worldwide: a review and synthetic analysis. Lancet Glob Health. 2022 Aug; 10(8). 10.1016/S2214-109X(22)00241-8
10. Ramírez AT, Valls J, Baena A, Rojas FD, Villagra V, Herrero R; ESTAMPA Study Group. Performance of cervical cytology and HPV testing for primary cervical cancer screening in Latin America: an analysis within the ESTAMPA study. Lancet Reg Health Am. 2023 Sep 20; 26: 100593. 10.1016/j.lana.2023.100593
11. Salazar-Fajardo Lida Janneth, Benavides-Delgado Mónica Rocío Boogaard Sabine, Marín Yolanda. Estrategias Latinoamericanas para la Vacunación contra el Virus Del Papiloma Humano - Una Revisión Temática. Hacia promoc. Salud. 2017 Dec; 22(2): 129-143. 10.17151/hpsal.2017.22.2.10
12. Bobadilla ML, Zorrilla ME, Villagra V, Olmedo G, Roscher G, Franco F et al. Detección molecular del virus papiloma humano de alto riesgo oncogénico en muestras cervicales. Laboratorio Central de Salud Pública: Primeros Resultados. Mem. Inst. Investig. Cienc. Salud. 2015 Apr; 13(1): 17-23. https://doi.org/10.18004/Mem.iics/1812-9528/2015.013(01)17-023
13. Bobadilla ML, Villagra V, Ortiz V, Deluca G, de Paula VS. High prevalence and co-infection of high-risk Human Papillomavirus genotypes among unvaccinated young women from Paraguay. PLoS One. 2023 Apr 6;18(4). 10.1371/journal.pone.0283542
14. Ejegod DM, Rebolj M, Bonde J. Comparison of analytical and clinical performance of CLART VPH2 genotyping assay to Linear Array and Hybrid Capture 2: a split-sample study. BMC Cancer. 2015 Apr 2; 15:216. 10.1186/s12885-015-1223-z
15. Smelov V, Elfstrom KM, Johansson AL, Eklund C, Naucler P, et al Long-term HPV type-specific risks of high-grade cervical intraepithelial lesions: a 14-year follow-up of a randomized primary HPV screening trial. Int J Cancer 2015 Mar 1;136 (5):1171-80. 10.1002/ijc.29085
16. 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 Dec 15;202(12):1789-99. 10.1086/657321
17. Correa RM, Baena A, Valls J, Colucci MC, Mendoza L, Rol M, et al. ESTAMPA Study Group. Distribution of human papillomavirus genotypes by severity of cervical lesions in HPV screened positive women from the ESTAMPA study in Latin America. PLoS One. 2022 Jul 29;17(7): e0272205. 10.1371/journal.pone.0272205
18. Cohen CM, Wentzensen N, Castle PE, Schiffman M, Zuna R, Arend RC, et al Racial and Ethnic Disparities in Cervical Cancer Incidence, Survival, and Mortality by Histologic Subtype. J Clin Oncol. 2023 Feb 10;41(5):1059-1068. 10.1200/JCO.22.01424
19. De Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, et al; Retrospective International Survey and HPV Time Trends Study Group. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol. 2010 Nov;11(11):1048-56. 10.1016/S1470-2045(10)70230-8
20. Clifford GM, Gallus S, Herrero R, Muñoz N, Snijders PJ, Vaccarella S, et al IARC HPV Prevalence Surveys Study Group. 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. 2005 Sep 17-23;366(9490):991-8. 10.1016/S0140-6736(05)67069-9
21. Bobadilla ML, Villagra V, Zorrilla ME, Olmedo G, Riveros MC, Franco F, et al. Detección y tipificación del Virus Papiloma Humano en el marco del tamizaje virológico para la detección de lesiones del cuello uterino en Asunción, Paraguay. Mem. Inst. Investig. Cienc. Salud. 2019; 17(1): 6-15. https://doi.org/10.18004/Mem.iics/1812-9528/2019.017(01)06-015
22. Villagra-Carrón V, Bobadilla ML, Olmedo GB, Pratt-Santacruz P, Ortiz Rocio V, Lopez-Ibarra G, et al. Distribución de virus de papiloma humano de alto riesgo oncogénico y otras infecciones de transmisión sexual en mujeres paraguayas con y sin virus de la inmunodeficiencia humana. Mem. Inst. Investig. Cienc. Salud. 2022; 20(3): 134-141. http://dx.doi.org/10.18004/mem.iics/1812-9528/2022.020.03.134
23. Mendoza LP, Arbiza J, Paez M, Kasamatsu E, Castro A, Giménez G, et al. Distribution of human papillomavirus genotypes in Paraguayan women according to the severity of the cervical lesion. J Med Virol. 2011 Aug; 83(8): 1351-7. 10.1002/jmv.22112
24. Schiffman M, Wentzensen N, Wacholder S, Kinney W, Gage JC, Castle PE. Human papillomavirus testing in the prevention of cervical cancer. J Natl Cancer Inst. 2011 Mar 2; 103(5): 368-83. 10.1093/jnci/djq562
25. Ministerio de Salud Pública y Bienestar Social. SBN 978-99925-11-05-3. Manual nacional de normas y procedimientos para la prevención y el control del cáncer del tracto genital inferior femenino Disponible en: https://isbn.bibliotecanacional.gov.py/catalogo.php?mode=detalle&nt=14258
26. De Thurah L, Bonde J, Lam JUH, Rebolj M. Concordant testing results between various human papillomavirus assays in primary cervical cancer screening: systematic review. Clin Microbiol Infect. 2018 Jan;24(1):29-36. 10.1016/j.cmi.2017.05.020
27. Bonde J, Rebolj M, Ejegod DM, Preisler S, Lynge E, Rygaard C. HPV prevalence and genotype distribution in a population-based split-sample study of well-screened women using CLART HPV2 human papillomavirus genotype microarray system. BMC Infect Dis. 2014 Jul 26; 14: 413. 10.1186/1471-2334-14-413
28. Stoler MH, Wright TC Jr, Parvu V, Vaughan L, Yanson K, Eckert K, et al. The Oncoclarity Human Papillomavirus Trial: Design, methods, and baseline results. Gynecol Oncol. 2018 Jun; 149 (3): 498-505. 10.1016/j.ygyno.2018.04.007
29. Arrossi S, Paolino M, Laudi R, Thouyaret L. Changing the paradigm of cervical cancer prevention through introduction of VPH-testing: evaluation of the implementation process of the Jujuy Demonstration Project in Argentina. Ecancermedicalscience. 2021 Mar 4; 15:1199. 10.3332/ecancer.2021.1199
30. Del Pino M, Alonso I, Rodriguez-Trujillo A, Bernal S, Geraets D, Guimerà N et al. Comparison of the analytical and clinical performance of five tests for the detection of human papillomavirus genital infection. J Virol Methods. 2017 Oct; 248: 238-243. 10.1016/j.jviromet.2017.07.009
31. Perkins RB, Guido RS, Castle PE, Chelmow D, Einstein MH, Garcia F, et al .2019 ASCCP Risk-Based Management Consensus Guidelines Committee. 2019 ASCCP Risk-Based Management Consensus Guidelines for Abnormal Cervical Cancer Screening Tests and Cancer Precursors. J Low Genit Tract Dis. 2020 Apr;24(2): 102-131. 10.1097/LGT.0000000000000525
32. Bhatla N, Singhal S. Primary HPV screening for cervical cancer. Best Pract Res Clin Obstet Gynaecol. 2020 May; 65:98-108. 10.1016/j.bpobgyn.2020.02.008
33. Mongelos P, Mendoza LP, Rodriguez-Riveros I, Castro A, Gimenez G, Araujo P, et al. Distribution of human papillomavirus (HPV) genotypes and bacterial vaginosis presence in cervical samples from Paraguayan indigenous. Int J Infect Dis. 2015 Oct; 39: 44-9. 10.1016/j.ijid.2015.08.007
34. Rebolj M, Preisler S, Ejegod DM, Rygaard C, Lynge E, Bonde J. Disagreement between human papillomavirus assays: an unexpected challenge for the choice of an assay in primary cervical screening. PLoS One. 2014 Jan 20; 9(1). 10.1371/journal.pone.0086835
35. Lim YK, Choi JH, Park S, Kweon OJ, Park AJ. Comparison of Three Different Commercial Kits for the Human Papilloma Virus Genotyping. J Clin Lab Anal. 2016 nov; 30(6): 1110-1115. 10.1002/jcla.21989
36. Ki EY, Lee YK, Lee A, Park JS. Comparison of the PANArray HPV Genotyping Chip Test with the Cobas 4800 HPV and Hybrid Capture 2 Tests for Detection of HPV in ASCUS Women. Yonsei Med J. 2018 Jul; 59(5): 662-668. 10.3349/ymj.2018.59.5.662
37. Sias C, Garbuglia AR, Piselli P, Cimaglia C, Lapa D, Del Nonno F, et al Comparison of the Abbott RealTime High Risk HPV with Genomica HPV Clinical Array for the detection of human papillomavirus DNA. APMIS. 2013 Nov; 121 (11): 1054-639 (5) : 662-668. 10.1111/apm.12054
38. Rebolj M, Bonde J, Preisler S, Ejegod D, Rygaard C, Lynge E. Human Papillomavirus Assays and Cytology in Primary Cervical Screening of Women Aged 30 Years and Above. PLoS One. 2016 Jan 20; 11(1).
39. Nygård M, Hansen BT, Kjaer SK, Hortlund M, Tryggvadóttir L, Munk et al papillomavirus genotype-specific risks for cervical intraepithelial lesions. Hum Vaccin Immunother. 2021 Apr 3; 17(4): 972-981. 10.1080/21645515.2020.1814097
40. Kamolratanakul S, Pitisuttithum P. Human Papillomavirus Vaccine Efficacy and Effectiveness against Cancer. Vaccines (Basel). 2021 Nov 30; 9(12): 1413. 10.3390/vaccines9121413