Modern approaches to cervical cancer screening (a review)

Authors

DOI:

https://doi.org/10.14739/2310-1237.2023.1.264035

Keywords:

cervix, precancerous cervical pathology, cervical cancer, human papilloma virus, cervical screening, cytologic method, HPV DNA test, colposcopy

Abstract

The aim – systematization of data from modern scientific sources and own knowledge and experience regarding the problems, advantages and prospects of the development of various methods of diagnosing pathological conditions of the cervix.

The relevance of the problem of cervical cancer is beyond doubt, which is confirmed by the annual data of the official statistics and recommendations of WHO, European experts and relevant national recommendations. The analysis and generalization of information from the specialized literature regarding the assessment of problems and prospects for the development of leading methods of cervical screening in order to reduce the number of cervical cancer cases in the world is a priority task of the expert society.

Currently, the most recommended approach to cervical screening is to combine HPV testing with cytology but separate testing for HPV is the most promising. Colposcopy remains the only confirmatory method of diagnosing cervical pathology, subject to mandatory cervical biopsy and histopathological examination of the biopsy. Standardization of classifications and terminology in the assessment of cytological, histopathological and colposcopic conclusions will allow to reach an understanding in the issues of optimal management tactics for patients with cervical pathology.

Conclusions. Diagnosis of high-risk carcinogenic types of human papillomavirus is the most promising method of cervical screening in the near future. At the same time, at the moment, we consider it appropriate to use the cytology together with HPV testing, at least as a sorting method. Standardization of cytological/histopathological terminology should be done in accordance with the Bethesda 2014 system update.

Author Biographies

M. I. Pavliuchenko, Zaporizhzhia State Medical University, Ukraine

MD, PhD, Assosiate Professor of the Department of Obstetrics and Gynecology

Yu. Ya. Krut, Zaporizhzhia State Medical University, Ukraine

MD, PhD, DSc, Professor, Head of the Department of Obstetrics and Gynecology

V. H. Siusiuka, Zaporizhzhia State Medical University, Ukraine

MD, PhD, DSc, Assosiate Professor of the Department of Obstetrics and Gynecology

O. V. Deinichenko, Zaporizhzhia State Medical University, Ukraine

MD, PhD, Assistant of the Department of Obstetrics and Gynecology

References

World Health Organization. (2020, November 17). Global strategy to accelerate the elimination of cervical cancer as a public health problem. https://www.who.int/publications/i/item/9789240014107

Dürst, M., Gissmann, L., Ikenberg, H., & zur Hausen, H. (1983). A papillomavirus DNA from a cervical carcinoma and its prevalence in cancer biopsy samples from different geographic regions. Proceedings of the National Academy of Sciences of the United States of America, 80(12), 3812-3815. https://doi.org/10.1073/pnas.80.12.3812

Li, N., Franceschi, S., Howell-Jones, R., Snijders, P. J., & Clifford, G. M. (2011). Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: Variation by geographical region, histological type and year of publication. International journal of cancer, 128(4), 927-935. https://doi.org/10.1002/ijc.25396

Xing, B., Guo, J., Sheng, Y., Wu, G., & Zhao, Y. (2021). Human Papillomavirus-Negative Cervical Cancer: A Comprehensive Review. Frontiers in oncology, 10, 606335. https://doi.org/10.3389/fonc.2020.606335

Lee, J. E., Chung, Y., Rhee, S., & Kim, T. H. (2022). Untold story of human cervical cancers: HPV-negative cervical cancer. BMB reports, 55(9), 429-438. https://doi.org/10.5483/BMBRep.2022.55.9.042

Petry, K. U., Liebrich, C., Luyten, A., Zander, M., & Iftner, T. (2017). Surgical staging identified false HPV-negative cases in a large series of invasive cervical cancers. Papillomavirus research (Amsterdam, Netherlands), 4, 85-89. https://doi.org/10.1016/j.pvr.2017.10.003

Schiffman, M., & Wentzensen, N. (2016). A Suggested Approach to Simplify and Improve Cervical Screening in the United States. Journal of lower genital tract disease, 20(1), 1-7. https://doi.org/10.1097/LGT.0000000000000170

Brisson, M., Kim, J. J., Canfell, K., Drolet, M., Gingras, G., Burger, E. A., Martin, D., Simms, K. T., Bénard, É., Boily, M. C., Sy, S., Regan, C., Keane, A., Caruana, M., Nguyen, D. T. N., Smith, M. A., Laprise, J. F., Jit, M., Alary, M., Bray, F., … Hutubessy, R. (2020). Impact of HPV vaccination and cervical screening on cervical cancer elimination: a comparative modelling analysis in 78 low-income and lower-middle-income countries. Lancet, 395(10224), 575-590. https://doi.org/10.1016/S0140-6736(20)30068-4

Sundström, K., & Elfström, K. M. (2020). Advances in cervical cancer prevention: Efficacy, effectiveness, elimination?. PLoS medicine, 17(1), e1003035. https://doi.org/10.1371/journal.pmed.1003035

Meites, E., Szilagyi, P. G., Chesson, H. W., Unger, E. R., Romero, J. R., & Markowitz, L. E. (2019). Human Papillomavirus Vaccination for Adults: Updated Recommendations of the Advisory Committee on Immunization Practices. MMWR. Morbidity and mortality weekly report, 68(32), 698-702. https://doi.org/10.15585/mmwr.mm6832a3

Reagan-Steiner, S., Yankey, D., Jeyarajah, J., Elam-Evans, L. D., Curtis, C. R., MacNeil, J., Markowitz, L. E., & Singleton, J. A. (2016). National, Regional, State, and Selected Local Area Vaccination Coverage Among Adolescents Aged 13-17 Years – United States, 2015. MMWR. Morbidity and mortality weekly report, 65(33), 850-858. https://doi.org/10.15585/mmwr.mm6533a4

Canfell, K., Kim, J. J., Brisson, M., Keane, A., Simms, K. T., Caruana, M., Burger, E. A., Martin, D., Nguyen, D. T. N., Bénard, É., Sy, S., Regan, C., Drolet, M., Gingras, G., Laprise, J. F., Torode, J., Smith, M. A., Fidarova, E., Trapani, D., Bray, F., … Hutubessy, R. (2020). Mortality impact of achieving WHO cervical cancer elimination targets: a comparative modelling analysis in 78 low-income and lower-middle-income countries. Lancet, 395(10224), 591-603. https://doi.org/10.1016/S0140-6736(20)30157-4

Wang, J., Elfström, K. M., Andrae, B., Nordqvist Kleppe, S., Ploner, A., Lei, J., Dillner, J., Sundström, K., & Sparén, P. (2020). Cervical cancer case-control audit: Results from routine evaluation of a nationwide cervical screening program. International journal of cancer, 146(5), 1230-1240. https://doi.org/10.1002/ijc.32416

Jansen, E. E. L., Zielonke, N., Gini, A., Anttila, A., Segnan, N., Vokó, Z., Ivanuš, U., McKee, M., de Koning, H. J., de Kok, I. M. C. M., & EU-TOPIA consortium (2020). Effect of organised cervical cancer screening on cervical cancer mortality in Europe: a systematic review. European journal of cancer, 127, 207-223. https://doi.org/10.1016/j.ejca.2019.12.013

Wentzensen, N., & Schiffman, M. (2014). Filling a gap in cervical cancer screening programmes. The Lancet. Oncology, 15(3), 249-251. https://doi.org/10.1016/S1470-2045(14)70073-7

Massad, L. S., Einstein, M. H., Huh, W. K., Katki, H. A., Kinney, W. K., Schiffman, M., Solomon, D., Wentzensen, N., Lawson, H. W., & 2012 ASCCP Consensus Guidelines Conference (2013). 2012 updated consensus guidelines for the management of abnormal cervical cancer screening tests and cancer precursors. Journal of lower genital tract disease, 17(5 Suppl 1), S1-S27. https://doi.org/10.1097/LGT.0b013e318287d329

Huh, W. K., Ault, K. A., Chelmow, D., Davey, D. D., Goulart, R. A., Garcia, F. A., Kinney, W. K., Massad, L. S., Mayeaux, E. J., Saslow, D., Schiffman, M., Wentzensen, N., Lawson, H. W., & Einstein, M. H. (2015). Use of primary high-risk human papillomavirus testing for cervical cancer screening: interim clinical guidance. Journal of lower genital tract disease, 19(2), 91-96. https://doi.org/10.1097/LGT.0000000000000103

Canfell, K., Smith, M. A., & Bateson, D. J. (2021). Self-collection for HPV screening: a game changer in the elimination of cervical cancer. The Medical journal of Australia, 215(8), 347-348. https://doi.org/10.5694/mja2.51262

Maver, P. J., & Poljak, M. (2020). Primary HPV-based cervical cancer screening in Europe: implementation status, challenges, and future plans. Clinical microbiology and infection, 26(5), 579-583. https://doi.org/10.1016/j.cmi.2019.09.006

Cuzick, J., Cadman, L., Mesher, D., Austin, J., Ashdown-Barr, L., Ho, L., Terry, G., Liddle, S., Wright, C., Lyons, D., & Szarewski, A. (2013). Comparing the performance of six human papillomavirus tests in a screening population. British journal of cancer, 108(4), 908-913. https://doi.org/10.1038/bjc.2013.22

Kinney, W., Wright, T. C., Dinkelspiel, H. E., DeFrancesco, M., Thomas Cox, J., & Huh, W. (2015). Increased cervical cancer risk associated with screening at longer intervals. Obstetrics and gynecology, 125(2), 311-315. https://doi.org/10.1097/AOG.0000000000000632

Blatt, A. J., Kennedy, R., Luff, R. D., Austin, R. M., & Rabin, D. S. (2015). Comparison of cervical cancer screening results among 256,648 women in multiple clinical practices. Cancer cytopathology, 123(5), 282-288. https://doi.org/10.1002/cncy.21544

Giorgi-Rossi, P., Arbyn, M., & Meijer, C. J. (2015). Cervical cancer screening by human papillomavirus testing followed by cytology triage. JAMA internal medicine, 175(6), 1068. https://doi.org/10.1001/jamainternmed.2015.0592

Saei Ghare Naz, M., Kariman, N., Ebadi, A., Ozgoli, G., Ghasemi, V., & Rashidi Fakari, F. (2018). Educational Interventions for Cervical Cancer Screening Behavior of Women: A Systematic Review. Asian Pacific journal of cancer prevention : APJCP, 19(4), 875-884. https://doi.org/10.22034/APJCP.2018.19.4.875

Rahatgaonkar, V. G., Deshpande, A. A., & Oka, G. A. (2021). Screening for cervical cancer in HIV-infected women: A review of literature. Indian journal of cancer, 58(3), 317-325. https://doi.org/10.4103/ijc.IJC_888_19

Salehiniya, H., Momenimovahed, Z., Allahqoli, L., Momenimovahed, S., & Alkatout, I. (2021). Factors related to cervical cancer screening among Asian women. European review for medical and pharmacological sciences, 25(19), 6109-6122. https://doi.org/10.26355/eurrev_202110_26889

Cho, H. W., Hong, J. H., & Lee, J. K. (2021). Human papillomavirus testing as a primary screening tool for cervical cancer. Journal of gynecologic oncology, 32(3), e56. https://doi.org/10.3802/jgo.2021.32.e56

Bruni, L., Serrano, B., Roura, E., Alemany, L., Cowan, M., Herrero, R., Poljak, M., Murillo, R., Broutet, N., Riley, L. M., & de Sanjose, S. (2022). Cervical cancer screening programmes and age-specific coverage estimates for 202 countries and territories worldwide: a review and synthetic analysis. The Lancet. Global health, 10(8), e1115-e1127. https://doi.org/10.1016/S2214-109X(22)00241-8

Gage, J. C., Schiffman, M., Katki, H. A., Castle, P. E., Fetterman, B., Wentzensen, N., Poitras, N. E., Lorey, T., Cheung, L. C., & Kinney, W. K. (2014). Reassurance against future risk of precancer and cancer conferred by a negative human papillomavirus test. Journal of the National Cancer Institute, 106(8), dju153. https://doi.org/10.1093/jnci/dju153

Fontham, E. T. H., Wolf, A. M. D., Church, T. R., Etzioni, R., Flowers, C. R., Herzig, A., Guerra, C. E., Oeffinger, K. C., Shih, Y. T., Walter, L. C., Kim, J. J., Andrews, K. S., DeSantis, C. E., Fedewa, S. A., Manassaram-Baptiste, D., Saslow, D., Wender, R. C., & Smith, R. A. (2020). Cervical cancer screening for individuals at average risk: 2020 guideline update from the American Cancer Society. CA: a cancer journal for clinicians, 70(5), 321-346. https://doi.org/10.3322/caac.21628

Castle, P. E., Wheeler, C. M., Campos, N. G., Sy, S., Burger, E. A., Kim, J. J., & New Mexico HPV Pap Registry Steering Committee (2018). Inefficiencies of over-screening and under-screening for cervical cancer prevention in the U.S. Preventive medicine, 111, 177-179. https://doi.org/10.1016/j.ypmed.2018.03.011

Isaka, Y., Hori, A., Tanaka, R., & Ichikawa, M. (2021). Alleviating psychological distress associated with a positive cervical cancer screening result: a randomized control trial. BMC women’s health, 21(1), 64. https://doi.org/10.1186/s12905-021-01207-6

Bergeron, C., Ronco, G., Reuschenbach, M., Wentzensen, N., Arbyn, M., Stoler, M., & von Knebel Doeberitz, M. (2015). The clinical impact of using p16(INK4a) immunochemistry in cervical histopathology and cytology: an update of recent developments. International journal of cancer, 136(12), 2741-2751. https://doi.org/10.1002/ijc.28900

Zhao, C., Moriarty, A. T., Ghofrani, M., Husain, M., Tambouret, R. H., Laucirica, R., Laser, A., Fischer, A., Ocal, I. T., Souers, R. J., Russell, D. K., Fan, F., & Crothers, B. A. (2015). Human papillomavirus testing and reporting rates in 2012: results of a College of American Pathologists national survey. Archives of pathology & laboratory medicine, 139(6), 757-761. https://doi.org/10.5858/arpa.2014-0393-CP

Wentzensen, N., Fetterman, B., Castle, P. E., Schiffman, M., Wood, S. N., Stiemerling, E., Tokugawa, D., Bodelon, C., Poitras, N., Lorey, T., & Kinney, W. (2015). p16/Ki-67 Dual Stain Cytology for Detection of Cervical Precancer in HPV-Positive Women. Journal of the National Cancer Institute, 107(12), djv257. https://doi.org/10.1093/jnci/djv257

Cox, J. T., Castle, P. E., Behrens, C. M., Sharma, A., Wright, T. C., Jr, Cuzick, J., & Athena HPV Study Group (2013). Comparison of cervical cancer screening strategies incorporating different combinations of cytology, HPV testing, and genotyping for HPV 16/18: results from the ATHENA HPV study. American journal of obstetrics and gynecology, 208(3), 184.e1-184.e11. https://doi.org/10.1016/j.ajog.2012.11.020

Wentzensen, N., Sun, C., Ghosh, A., Kinney, W., Mirabello, L., Wacholder, S., Shaber, R., LaMere, B., Clarke, M., Lorincz, A. T., Castle, P. E., Schiffman, M., & Burk, R. D. (2012). Methylation of HPV18, HPV31, and HPV45 genomes and cervical intraepithelial neoplasia grade 3. Journal of the National Cancer Institute, 104(22), 1738-1749. https://doi.org/10.1093/jnci/djs425

Sawaya, G. F., Smith-McCune, K., & Kuppermann, M. (2019). Cervical Cancer Screening: More Choices in 2019. JAMA, 321(20), 2018-2019. https://doi.org/10.1001/jama.2019.4595

Marcus, P. M., Prorok, P. C., Miller, A. B., DeVoto, E. J., & Kramer, B. S. (2015). Conceptualizing overdiagnosis in cancer screening. Journal of the National Cancer Institute, 107(4), djv014. https://doi.org/10.1093/jnci/djv014

FDA. (2020, March 10). PMA P190024: FDA Summary of Safety and Effectiveness Data. https://www.accessdata.fda.gov/cdrh_docs/pdf19/P190024B.pdf

Darragh, T. M., Colgan, T. J., Cox, J. T., Heller, D. S., Henry, M. R., Luff, R. D., McCalmont, T., Nayar, R., Palefsky, J. M., Stoler, M. H., Wilkinson, E. J., Zaino, R. J., Wilbur, D. C., & Members of LAST Project Work Groups (2012). The Lower Anogenital Squamous Terminology Standardization Project for HPV-Associated Lesions: background and consensus recommendations from the College of American Pathologists and the American Society for Colposcopy and Cervical Pathology. Journal of lower genital tract disease, 16(3), 205-242. https://doi.org/10.1097/LGT.0b013e31825c31dd

Nayar, R., & Wilbur, D. C. (2015). The Pap test and Bethesda 2014. Cancer cytopathology, 123(5), 271-281. https://doi.org/10.1002/cncy.21521

Nayar, R., & Wilbur, D. C. (2015). The Bethesda System for Reporting Cervical Cytology: Definitions, Criteria, and Explanatory Notes (pp. 1-321). Springer International Publishing. https://doi.org/10.1007/978-3-319-11074-5

Giorgi Rossi, P., Carozzi, F., Ronco, G., Allia, E., Bisanzi, S., Gillio-Tos, A., De Marco, L., Rizzolo, R., Gustinucci, D., Del Mistro, A., Frayle, H., Confortini, M., Iossa, A., Cesarini, E., Bulletti, S., Passamonti, B., Gori, S., Toniolo, L., Barca, A., Bonvicini, L., … the New Technology for Cervical Cancer 2 Working Group (2021). p16/ki67 and E6/E7 mRNA Accuracy and Prognostic Value in Triaging HPV DNA-Positive Women. Journal of the National Cancer Institute, 113(3), 292-300. https://doi.org/10.1093/jnci/djaa105

Clarke, M. A., Cheung, L. C., Castle, P. E., Schiffman, M., Tokugawa, D., Poitras, N., Lorey, T., Kinney, W., & Wentzensen, N. (2019). Five-Year Risk of Cervical Precancer Following p16/Ki-67 Dual-Stain Triage of HPV-Positive Women. JAMA oncology, 5(2), 181-186. https://doi.org/10.1001/jamaoncol.2018.4270

Yang, D. X., Soulos, P. R., Davis, B., Gross, C. P., & Yu, J. B. (2018). Impact of Widespread Cervical Cancer Screening: Number of Cancers Prevented and Changes in Race-specific Incidence. American journal of clinical oncology, 41(3), 289-294. https://doi.org/10.1097/COC.0000000000000264

Hammer, A., & Gravitt, P. (2021). Clinical implications of transitioning from cytology to human papillomavirus-based cervical cancer screening. Acta obstetricia et gynecologica Scandinavica, 100(3), 371-372. https://doi.org/10.1111/aogs.14107

Koliopoulos, G., Nyaga, V. N., Santesso, N., Bryant, A., Martin-Hirsch, P. P., Mustafa, R. A., Schünemann, H., Paraskevaidis, E., & Arbyn, M. (2017). Cytology versus HPV testing for cervical cancer screening in the general population. The Cochrane database of systematic reviews, 8(8), CD008587. https://doi.org/10.1002/14651858.CD008587.pub2

Demarco, M., Hyun, N., Carter-Pokras, O., Raine-Bennett, T. R., Cheung, L., Chen, X., Hammer, A., Campos, N., Kinney, W., Gage, J. C., Befano, B., Perkins, R. B., He, X., Dallal, C., Chen, J., Poitras, N., Mayrand, M. H., Coutlee, F., Burk, R. D., Lorey, T., … Schiffman, M. (2020). A study of type-specific HPV natural history and implications for contemporary cervical cancer screening programs. EClinicalMedicine, 22, 100293. https://doi.org/10.1016/j.eclinm.2020.100293

Guan, P., Howell-Jones, R., Li, N., Bruni, L., de Sanjosé, S., Franceschi, S., & Clifford, G. M. (2012). Human papillomavirus types in 115,789 HPV-positive women: a meta-analysis from cervical infection to cancer. International journal of cancer, 131(10), 2349-2359. https://doi.org/10.1002/ijc.27485

Thomsen, L. T., Frederiksen, K., Munk, C., Junge, J., Castle, P. E., Iftner, T., & Kjaer, S. K. (2014). High-risk and low-risk human papillomavirus and the absolute risk of cervical intraepithelial neoplasia or cancer. Obstetrics and gynecology, 123(1), 57-64. https://doi.org/10.1097/AOG.0000000000000056

Schiffman, M., Burk, R. D., Boyle, S., Raine-Bennett, T., Katki, H. A., Gage, J. C., Wentzensen, N., Kornegay, J. R., Aldrich, C., Tam, T., Erlich, H., Apple, R., Befano, B., & Castle, P. E. (2015). A study of genotyping for management of human papillomavirus-positive, cytology-negative cervical screening results. Journal of clinical microbiology, 53(1), 52-59. https://doi.org/10.1128/JCM.02116-14

Hu, Z., & Ma, D. (2018). The precision prevention and therapy of HPV-related cervical cancer: new concepts and clinical implications. Cancer medicine, 7(10), 5217-5236. https://doi.org/10.1002/cam4.1501

Schiffman, M., & Wentzensen, N. (2021). The Orderly Incorporation of Continuing Technologic Advances Into Cervical Cancer Screening. Journal of the National Cancer Institute, 113(3), 231-233. https://doi.org/10.1093/jnci/djaa106

Wentzensen, N., Walker, J. L., Gold, M. A., Smith, K. M., Zuna, R. E., Mathews, C., Dunn, S. T., Zhang, R., Moxley, K., Bishop, E., Tenney, M., Nugent, E., Graubard, B. I., Wacholder, S., & Schiffman, M. (2015). Multiple biopsies and detection of cervical cancer precursors at colposcopy. Journal of clinical oncology, 33(1), 83-89. https://doi.org/10.1200/JCO.2014.55.9948

Davies, K. R., Cantor, S. B., Cox, D. D., & Follen, M. (2015). An alternative approach for estimating the accuracy of colposcopy in detecting cervical precancer. PloS one, 10(5), e0126573. https://doi.org/10.1371/journal.pone.0126573

Gage, J. C., Katki, H. A., Schiffman, M., Castle, P. E., Fetterman, B., Poitras, N. E., Lorey, T., Cheung, L. C., Behrens, C., Sharma, A., Zhao, F. H., Cuzick, J., Yang, Z. H., & Kinney, W. K. (2014). The low risk of precancer after a screening result of human papillomavirus-negative/atypical squamous cells of undetermined significance papanicolaou and implications for clinical management. Cancer cytopathology, 122(11), 842-850. https://doi.org/10.1002/cncy.21463

Katki, H. A., Schiffman, M., Castle, P. E., Fetterman, B., Poitras, N. E., Lorey, T., Cheung, L. C., Raine-Bennett, T., Gage, J. C., & Kinney, W. K. (2013). Five-year risks of CIN 3+ and cervical cancer among women with HPV-positive and HPV-negative high-grade Pap results. Journal of lower genital tract disease, 17(5 Suppl 1), S50-S55. https://doi.org/10.1097/LGT.0b013e3182854282

Katki, H. A., Schiffman, M., Castle, P. E., Fetterman, B., Poitras, N. E., Lorey, T., Cheung, L. C., Raine-Bennett, T., Gage, J. C., & Kinney, W. K. (2013). Five-year risks of CIN 3+ and cervical cancer among women who test Pap-negative but are HPV-positive. Journal of lower genital tract disease, 17(5 Suppl 1), S56-S63. https://doi.org/10.1097/LGT.0b013e318285437b

Schiffman, M., Vaughan, L. M., Raine-Bennett, T. R., Castle, P. E., Katki, H. A., Gage, J. C., Fetterman, B., Befano, B., & Wentzensen, N. (2015). A study of HPV typing for the management of HPV-positive ASC-US cervical cytologic results. Gynecologic oncology, 138(3), 573-578. https://doi.org/10.1016/j.ygyno.2015.06.040

Schiffman, M., & Wentzensen, N. (2015). Transitioning to a new era in cervical cancer screening. Gynecologic oncology, 136(2), 175-177. https://doi.org/10.1016/j.ygyno.2015.01.538

Reid, J. L., Wright, T. C., Jr, Stoler, M. H., Cuzick, J., Castle, P. E., Dockter, J., Getman, D., & Giachetti, C. (2015). Human papillomavirus oncogenic mRNA testing for cervical cancer screening: baseline and longitudinal results from the CLEAR study. American journal of clinical pathology, 144(3), 473-483. https://doi.org/10.1309/AJCPHVD7MIP3FYVV

Bedell, S. L., Goldstein, L. S., Goldstein, A. R., & Goldstein, A. T. (2020). Cervical Cancer Screening: Past, Present, and Future. Sexual medicine reviews, 8(1), 28-37. https://doi.org/10.1016/j.sxmr.2019.09.005

Xue, P., Ng, M. T. A., & Qiao, Y. (2020). The challenges of colposcopy for cervical cancer screening in LMICs and solutions by artificial intelligence. BMC medicine, 18(1), 169. https://doi.org/10.1186/s12916-020-01613-x

Katki, H. A., Gage, J. C., Schiffman, M., Castle, P. E., Fetterman, B., Poitras, N. E., Lorey, T., Cheung, L. C., Raine-Bennett, T., & Kinney, W. K. (2013). Follow-up testing after colposcopy: five-year risk of CIN 2+ after a colposcopic diagnosis of CIN 1 or less. Journal of lower genital tract disease, 17(5 Suppl 1), S69-S77. https://doi.org/10.1097/LGT.0b013e31828543b1

Kaufman, H. W., Alagia, D. P., Chen, Z., Onisko, A., & Austin, R. M. (2020). Contributions of Liquid-Based (Papanicolaou) Cytology and Human Papillomavirus Testing in Cotesting for Detection of Cervical Cancer and Precancer in the United States. American journal of clinical pathology, 154(4), 510-516. https://doi.org/10.1093/ajcp/aqaa074

Perkins, R. B., Guido, R. L., Saraiya, M., Sawaya, G. F., Wentzensen, N., Schiffman, M., & Feldman, S. (2021). Summary of Current Guidelines for Cervical Cancer Screening and Management of Abnormal Test Results: 2016-2020. Journal of women’s health (2002), 30(1), 5-13. https://doi.org/10.1089/jwh.2020.8918

Ronco, G., Dillner, J., Elfström, K. M., Tunesi, S., Snijders, P. J., Arbyn, M., Kitchener, H., Segnan, N., Gilham, C., Giorgi-Rossi, P., Berkhof, J., Peto, J., Meijer, C. J., & International HPV screening working group (2014). Efficacy of HPV-based screening for prevention of invasive cervical cancer: follow-up of four European randomised controlled trials. Lancet, 383(9916), 524-532. https://doi.org/10.1016/S0140-6736(13)62218-7

World Health Organization. (2021, July 6). WHO guideline for screening and treatment of cervical pre-cancer lesions for cervical cancer prevention, Second edition. https://www.who.int/publications/i/item/9789240030824

Arbyn, M., Smith, S. B., Temin, S., Sultana, F., Castle, P., & Collaboration on Self-Sampling and HPV Testing (2018). Detecting cervical precancer and reaching underscreened women by using HPV testing on self samples: updated meta-analyses. BMJ (Clinical research ed.), 363, k4823. https://doi.org/10.1136/bmj.k4823

Hawkes, D., Keung, M. H. T., Huang, Y., McDermott, T. L., Romano, J., Saville, M., & Brotherton, J. M. L. (2020). Self-Collection for Cervical Screening Programs: From Research to Reality. Cancers, 12(4), 1053. https://doi.org/10.3390/cancers12041053

Song, F., Du, H., Xiao, A., Wang, C., Huang, X., Liu, Z., Zhao, M., Men, H., & Wu, R. (2020). Evaluating the performance of three different cervical cancer screening modalities in a large prospective population-based cohort. Journal of infection and public health, 13(11), 1780-1786. https://doi.org/10.1016/j.jiph.2020.08.008

Katki, H. A., Schiffman, M., Castle, P. E., Fetterman, B., Poitras, N. E., Lorey, T., Cheung, L. C., Raine-Bennett, T., Gage, J. C., & Kinney, W. K. (2013). Five-year risks of CIN 3+ and cervical cancer among women with HPV testing of ASC-US Pap results. Journal of lower genital tract disease, 17(5 Suppl 1), S36-S42. https://doi.org/10.1097/LGT.0b013e3182854253

Perkins, R. B., Guido, R. S., Castle, P. E., Chelmow, D., Einstein, M. H., Garcia, F., Huh, W. K., Kim, J. J., Moscicki, A. B., Nayar, R., Saraiya, M., Sawaya, G. F., Wentzensen, N., Schiffman, M., & 2019 ASCCP Risk-Based Management Consensus Guidelines Committee (2020). 2019 ASCCP Risk-Based Management Consensus Guidelines for Abnormal Cervical Cancer Screening Tests and Cancer Precursors. Journal of lower genital tract disease, 24(2), 102-131. https://doi.org/10.1097/LGT.0000000000000525

Katki, H. A., Schiffman, M., Castle, P. E., Fetterman, B., Poitras, N. E., Lorey, T., Cheung, L. C., Raine-Bennett, T., Gage, J. C., & Kinney, W. K. (2013). Benchmarking CIN 3+ risk as the basis for incorporating HPV and Pap cotesting into cervical screening and management guidelines. Journal of lower genital tract disease, 17(5 Suppl 1), S28-S35. https://doi.org/10.1097/LGT.0b013e318285423c

Schiffman, M., & Wentzensen, N. (2021). Cervical Screening Performance. American journal of clinical pathology, 155(4), 616-620. https://doi.org/10.1093/ajcp/aqaa198

Egemen, D., Cheung, L. C., Chen, X., Demarco, M., Perkins, R. B., Kinney, W., Poitras, N., Befano, B., Locke, A., Guido, R. S., Wiser, A. L., Gage, J. C., Katki, H. A., Wentzensen, N., Castle, P. E., Schiffman, M., & Lorey, T. S. (2020). Risk Estimates Supporting the 2019 ASCCP Risk-Based Management Consensus Guidelines. Journal of lower genital tract disease, 24(2), 132-143. https://doi.org/10.1097/LGT.0000000000000529

Rodríguez, A. C., Solomon, D., Herrero, R., Hildesheim, A., Gon­zá­lez, P., Wacholder, S., Porras, C., Jiménez, S., Schiffman, M., & CVT Group (2013). Impact of human papillomavirus vaccination on cervical cytology screening, colposcopy, and treatment. American journal of epidemiology, 178(5), 752-760. https://doi.org/10.1093/aje/kwt047

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2023-04-28

How to Cite

1.
Pavliuchenko MI, Krut YY, Siusiuka VH, Deinichenko OV. Modern approaches to cervical cancer screening (a review). Pathologia [Internet]. 2023Apr.28 [cited 2024Nov.14];20(1):85-93. Available from: http://pat.zsmu.edu.ua/article/view/264035