International experience of laboratory methods in the cervical cancer screening

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Cervical cancer (CC) is a serious health problem all over the world. CC is a fully preventable disease; however, it remains one of the leading causes of death among women with carcinomas. The screening helps to reduce morbidity and mortality. Two tests are used as screening tests in the world: сervical cytology and detection of human papillomavirus (HPV). Cervical cytology (Pap test) is a traditional test of CC screening. Two types of Pap test are used in modern laboratory practice: liquid and traditional methods. HPV testing is now used as the primary screening tool for СС in some countries. However, a key factor in effective screening is the coverage of the population and the organization of the screening. Immunocytochemical examination is an additional method used to improve the accuracy of diagnosis, p16/Ki-67 dual staining. This review focuses on the laboratory methods used in the world practice of screening. The literature search for this review was conducted using PubMed, MedLine and Embase.

About the authors

Marina V. Enaeva

The Loginov Moscow Clinical Scientific Center

Author for correspondence.
Email: m.enaeva@mknc.ru
ORCID iD: 0000-0003-2537-2284
SPIN-code: 9817-5470
Russian Federation, Moscow

Karina K. Noskova

The Loginov Moscow Clinical Scientific Center

Email: k.noskova@mknc.ru
ORCID iD: 0000-0001-5734-0995
SPIN-code: 1241-0195

MD, Cand. Sci. (Med.)

Russian Federation, Moscow

References

  1. Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2020. CA Cancer J Clin. 2020;70(1):7–30. doi: 10.3322/caac.21590
  2. Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers iN 185 countries. CA Cancer J Clin. 2021;71(3): 209–49. doi: 10.3322/caac.21660
  3. Kaprin AD, Starinskij VV, Petrova GV. Malignant neoplasms in Russia in 2018 (Morbidity and mortality). FGBU «MNIOI im. P.A. Gercena» Minzdrava Rossii. 2019. (In Russ).
  4. Aksel EM, Vinogradova NN. Statistics of malignant neoplasms of female reproductive organs. Gynecologic Oncology. 2018;(3):64–78. (In Russ.).
  5. Cochrane AL, Holland WW. Validation of screening procedures. Br Med Bull. 1971;27(1): 3–8. doi: 10.1093/oxfordjournals.bmb.a070810
  6. Chrysostomou AC, Stylianou DC, Constantinidou A, Kostrikis LG. Cervical Cancer Screening Programs in Europe: the transition towards HPV vaccination and population-based HPV testing. Viruses. 2018;10(12):729. doi: 10.3390/v10120729
  7. Toropovskiy AN, Pavlova ON, Viktorov DA, et al. Cervical cancer epidemiology and significance of its diagnosis and screening (literature review). Gynecologic Oncology. 2019;(4):45–53. (In Russ).
  8. Papanicolaou GN, Traut HF. The diagnostic value of vaginal smears in carcinoma of the uterus. Am J Obstet Gynecol. 1941;42(2):193. doi: 10.1016/S0002-9378(16)40621-6
  9. Cervical cancer screening programs: summary of the 1982. Canadian Task Force report. Can Med Assoc J. 1982;127(7):581–9.
  10. Ng E, Wilkins R, Fung MF, Berthelot JM. Cervical cancer mortality by neighbourhood income in urban Canada from 1971 to 1996. Can Med Assoc J. 2004;170(10):1545–9. doi: 10.1503/cmaj.1031528
  11. Maxwell CJ, Bancej CM, Snider J, Vik SA. Factors important in promoting cervical cancer screening among Canadian women: Findings from the 1996–97 national population health survey (NPHS). Can J Public Health. 2001;92(2):127–33. doi: 10.1007/BF03404946
  12. Bray F, Loos A, McCarron P, et al. Trends in cervical squamous cell carcinoma incidence in 13 European countries: Changing risk and the effects of screening. Cancer Epidemiol Biomarkers Prev. 2005;14(3):677–86. doi: 10.1158/1055-9965.EPI-04-0569
  13. ACOG. Practice Bulletin No. 168: cervical cancer screening and prevention. Obstet Gynecol. 2016; 128(4): e111–30. doi: 10.1097/AOG.0000000000001708
  14. Toropovskiy AN, Pavlova, Viktorov DA, Nikitin AG. New screening and diagnostic methods for cervical cancer. Bulletin of the Medical Institute «REAVIZ» (REHABILITATION, DOCTOR AND HEALTH). 2019;4 :51–64. (In Russ).
  15. Novik VI. Discussion questions of cytological screening of cervical cancer (literature review). Tumors of Female Reproductive System. 2020;16(2):63–71. (In Russ). doi: 10.17650/1994-4098-2020-16-2-63-71
  16. Minkina GN. Cytological screening of the cervical cancer: from the traditional Pap test to computer technologies. Obstetrics, Gynecology and Reproduction. 2017;11(1):56–63. (In Russ). doi: 10.17749/2313-7347.2017.11.1.056-063
  17. Nanda K, McCrory DC, Myers ER, et al. Accuracy of the Papanicolaou test in screening for and follow-up of cervical cytologic abnormalities: a systematic review. Ann Intern Med. 2000;132(10):810–9. doi: 10.7326/0003-4819-132-10-200005160-00009
  18. Srisomboon S, Tantipalakorn C, Charoenkwan K, Srisomboon J. Cervical screening results leading to detection of adenocarcinoma in situ of the uterine cervix. Asian Pac J Cancer Prev. 2019;20(2):377–382. doi: 10.31557/APJCP.2019.20.2.377
  19. Savostikova MV, Korolenkova LI, Fedoseeva ES, Pimenova VV. The experience of the use of liquid-based technology BD SUREPATH™ for early diagnosis and screening for cervical precancerous lesions and cervical cancer in Rostov region. Gynecologic Oncology. 2018;4:50–60. (In Russ).
  20. Bollman N R. Liquid-based cytology for risk-adapted cervical screening. Reproductive Endocrinology. 2015;(21):95–101. doi: 10.18370/2309-4117.2015.21.95-101
  21. Rozemeijer K, Naber SK, Penning C, Overbeek LI, et al. Cervical cancer incidence after normal cytological sample in routine screening using SurePath, ThinPrep, and conventional cytology: population based study. BMJ. 2017;356:j504. doi: 10.1136/bmj.j504
  22. Rozemeijer K, Penning C, Siebers AG, et al. Comparing SurePath, ThinPrep, and conventional cytology as primary test method: SurePath is associated with increased CIN II+ detection rates. Cancer Causes Control. 2016;27(1):15–25. doi: 10.1007/s10552-015-0678-1
  23. Phaliwong P, Pariyawateekul P, Khuakoonratt N, Sirichai W, et al. Cervical Cancer detection between conventional and liquid based cervical cytology: a 6-year experience in Northern Bangkok Thailand. Asian Pac J Cancer Prev. 2018;19(5):1331–36. doi: 10.22034/APJCP.2018.19.5.1331
  24. Ito K, Kimura R, Konishi H, et al. A comparison of liquid-based and conventional cytology using data for cervical cancer screening from the Japan Cancer Society. Jpn J Clin Oncol. 2020;50(2):138–144. doi: 10.1093/jjco/hyz161
  25. Hosono S, Terasawa T, Katayama T, Sasaki S, et al. Hosono S, Terasawa T, Katayama T, Sasaki S, et al. Frequency of unsatisfactory cervical cytology smears in cancer screening of Japanese women: a systematic review and meta-analysis. Cancer Sci. 2018;109(4):934–43. doi: 10.1111/cas.13549
  26. Boshart M, GissmanN L, Ikenberg H, et al. A new type of papillomavirus DNA, its presence in genital cancer biopsies and in cell lines derived from cervical cancer. EMBO J. 1984;3(5):1151–7. doi: 10.1002/j.1460-2075.1984.tb01944.x
  27. Schwarz E, Freese UK, Gissmann L, et al. Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature. 1985;314(6006):111–4. doi: 10.1038/314111a0
  28. de Villiers EM, Wagner D, Schneider A, et al. Human papillomavirus infections in women with and without abnormal cervical cytology. Lancet. 1987;2(8561):703–6. doi: 10.1016/s0140-6736(87)91072-5
  29. Okunade KS. Human papillomavirus and cervical cancer. J Obstet Gynaecol. 2020;40(5):602–8. doi: 10.1080/01443615.2019.1634030
  30. Salazar KL, Duhon DJ, Olsen R, Thrall M. A review of the FDA-approved molecular testing platforms for human papillomavirus. J Am Soc Cytopathol. 2019;8(5):284–92. doi: 10.1016/j.jasc.2019.06.001
  31. Sitarz K, Szostek S. Food and drug administration – approved molecular methods for detecting human papillomavirus infection. Ginekol Pol. 2019;90(2):104–8. doi: 10.5603/GP.2019.0018
  32. PAHO. Integrating HPV testing in cervical cancer screening program: a manual for program managers. Washington, D.C. : PAHO, 2016 [cited 2020 Jul 9]. Available from: https://www.paho.org/hq/dmdocuments/2016/manual-VPH-English-FINAL-version.pdf.
  33. Meijer CJ, Berkhof J, Castle PE, et al. Guidelines for human papillomavirus DNA test requirements for primary cervical cancer screening in women 30 years and older. Int J Cancer. 2009;124(3):516–20. doi: 10.1002/ijc.24010
  34. Alameda F, Garrote L, Mojal S, Sousa C, et al. Cervista HPV HR test for cervical cancer screening: a comparative study in the Catalonian population. Arch Pathol Lab Med. 2015;139:241–4. doi: 10.5858/arpa.2014-0012-OA
  35. Ejegod DM, Hansen M, Christiansen IK, et al. Clinical validation of the Cobas 4800 HPV assay using cervical samples in SurePath medium under the VALGENT4 framework. J Clin Virol. 2020;128:104336. doi: 10.1016/j.jcv.2020.104336
  36. Iftner T, Neis KJ, Castanon A, Landy R, et al. Longitudinal clinical performance of the RNA-based Aptima Human Papillomavirus (AHPV) Assay in comparison to the DNA-based Hybrid Capture 2 HPV test in two consecutive screening rounds with a 6-year interval in Germany. J Clin Microbiol. 2019;57(1):e01177–18. doi: 10.1128/JCM.01177-18
  37. Bonde JH, Pedersen H, Quint W, et al. Clinical and analytical performance of the BD Onclarity HPV assay with SurePath screening samples from the Danish Cervical Screening Program using the VALGENT framework. J Clin Microbiol. 2020;58(2):e01518–19. doi: 10.1128/JCM.01518-19
  38. Iftner T, Wang L, Iftner A, Holz B, et al. Study-based evaluation of the Abbott RealTime High Risk HPV test in comparison to the HC2 HR HPV test in women aged ≥30 years using residual LBC ThinPrep specimens. BMC Infect Dis. 2016;16(1):672. doi: 10.1186/s12879-016-1994-0
  39. IARC. Cervix Cancer Screening: IARC Handbooks of Cancer Prevention. Vol. 10. Lyon : IARC Press, 2005. 302 p.
  40. Tewari P, White C, Kelly L, Pilkington L, et al. Clinical performance of the Cobas 4800 HPV test and the Aptima HPV assay in the management of women referred to colposcopy with minor cytological abnormalities. Diagn Cytopathol. 2018;46(12):987–92. doi: 10.1002/dc.24066
  41. Bottari F, Boveri S, Iacobone AD, Gulmini C, et al. Transition from Hybrid Capture 2 to Cobas 4800 in HPV detection: sensitivity and specificity for Cin2+ in two time periods. Infect Dis (Lond). 2018;50(7):554–9. doi: 10.1080/23744235.2018.1441538
  42. Curry SJ, Krist AH, Owens DK; US Preventive Services Task Force, et al. Screening for cervical cancer: US Preventive Services Task Force Recommendation Statement. JAMA. 2018;320(7):674–86. doi: 10.1001/jama.2018.10897
  43. Tjalma WAA. Diagnostic performance of dual-staining cytology for cervical cancer screening: A systematic literature review. Eur J Obstet Gynecol Reprod Biol. 2017;210:275–80. doi: 10.1016/j.ejogrb.2017.01.009
  44. Zhang R, Ge X, You K, et al. p16/Ki67 dual staining improves the detection specificity of high-grade cervical lesions. J Obstet Gynaecol Res. 2018;44(11):2077–84. doi: 10.1111/jog.13760
  45. Kyrgiou M, ArbyN M, BergeroN C, Bosch FX, et al. Cervical screening: ESGO-EFC position paper of the European Society of Gynaecologic Oncology (ESGO) and the European Federation of Colposcopy (EFC). Br J Cancer. 2020;123(4):510–7. doi: 10.1038/s41416-020-0920-9
  46. Allia E, Ronco G, Coccia A, et al. Interpretation of p16(INK4a) /Ki-67 dual immunostaining for the triage of human papillomavirus-positive women by experts and nonexperts in cervical cytology. Cancer Cytopathol. 2015;123(4):212–8. doi: 10.1002/cncy.21511
  47. Bergeron C, von Knebel Doeberitz M. The Role of cytology in the 21st century: the integration of cells and molecules. Acta Cytol. 2016;60(6):540–2. doi: 10.1159/000449402
  48. von Knebel Doeberitz M. New molecular tools for efficient screening of cervical cancer. Dis Markers. 2001;17(3):123–8. doi: 10.1155/2001/249506
  49. Shiraz A, Crawford R, Egawa N, et al. The early detection of cervical cancer. The current and changing landscape of cervical disease detection. Cytopathology. 2020;31(4):258–70. doi: 10.1111/cyt.12835
  50. Magkana M, Mentzelopoulou P, Magkana E, et al. The p16/Ki-67 assay is a safe, effective and rapid approach to triage womeN with mild cervical lesions. PLoS One. 2021 Jun [cited 2021 Dec 12];16(6):e0253045 [18 p.]. doi: 10.1371/journal.pone.0253045
  51. Ebisch RM, van der Horst J, Hermsen M, et al. EvaluatioN of p16/Ki-67 dual-stained cytology as triage test for high-risk human papillomavirus-positive women. Mod Pathol. 2017;30(7):1021–31. doi: 10.1038/modpathol.2017.16
  52. Li YC, Zhao YQ, Li TY, et al. The performance of immunocytochemistry staining as triaging tests for high-risk HPV-positive women: a 24-month prospective study. J Oncol. 2020 May [cited 2021 Dec 12]; 2020:6878761 [8 p.]. Available from: https://downloads.hindawi.com/journals/jo/2020/6878761.pdf. doi: 10.1155/2020/6878761
  53. Uijterwaal MH, PolmaN NJ, Witte BI, et al. Triaging HPV-positive women with normal cytology by p16/Ki-67 dual-stained cytology testing: baseline and longitudinal data. Int J Cancer. 2015;136(10):2361–8. doi: 10.1002/ijc.29290
  54. Abreu AL, Silva RA, Fernandes S. Validation of CINtec® PLUS cytology kit in the diagnosis of persistent HPV infections – cohort study in the Portuguese population. J Cytol. 2021;38(2):94–100. doi: 10.4103/JOC.JOC_173_20
  55. Bergeron C, Ikenberg H, Sideri M, Denton K; PALMS Study Group, et al. Prospective evaluation of p16/Ki-67 dual-stained cytology for managing women with abnormal Papanicolaou cytology: PALMS study results. Cancer Cytopathol. 2015;123(6):373–81. doi: 10.1002/cncy.21542
  56. Wright TC Jr, Behrens CM, Ranger-Moore J, et al. Triaging HPV-positive women with p16/Ki-67 dual-stained cytology: Results from a sub-study nested into the ATHENA trial. Gynecol Oncol. 2017;144(1):51–6. doi: 10.1016/j.ygyno.2016.10.031
  57. Benevolo M, Allia E, Gustinucci D; New Technologies for Cervical Cancer Screening 2 (NTCC2) Working Group, et al. Interobserver reproducibility of cytologic p16INK4a/Ki-67 dual immunostaining in human papillomavirus-positive women. Cancer Cytopathol. 2017;125(3):212–20. doi: 10.1002/cncy.21800

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2021 Enaeva M.V., Noskova K.K.

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
 


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies