Methylation testing for the detection of recurrent cervical intraepithelial neoplasia.


Journal

International journal of cancer
ISSN: 1097-0215
Titre abrégé: Int J Cancer
Pays: United States
ID NLM: 0042124

Informations de publication

Date de publication:
15 12 2023
Historique:
received: 13 06 2023
accepted: 19 07 2023
medline: 23 10 2023
pubmed: 4 8 2023
entrez: 4 8 2023
Statut: ppublish

Résumé

Women treated for CIN2/3 remain at increased risk of recurrent CIN and cervical cancer, and therefore posttreatment surveillance is recommended. This post hoc analysis evaluates the potential of methylation markers ASCL1/LHX8 and FAM19A4/miR124-2 for posttreatment detection of recurrent CIN2/3. Cervical scrapes taken at 6 and 12 months posttreatment of 364 women treated for CIN2/3 were tested for methylation of ASCL1/LHX8 and FAM19A4/miR124-2 using quantitative multiplex methylation-specific PCR. Performance of the methylation tests were calculated and compared with the performance of HPV and/or cytology. Methylation levels of recurrent CIN were compared between women with a persistent HPV infection, and women with an incident HPV infection or without HPV infection. Recurrent CIN2/3 was detected in 42 women (11.5%), including 28 women with CIN2 and 14 with CIN3. ASCL1/LHX8 tested positive in 13/14 (92.9%) of recurrent CIN3 and 13/27 (48.1%) of recurrent CIN2. FAM19A4/miR124-2 tested positive in 14/14 (100%) of recurrent CIN3 and 10/27 (37.0%) of recurrent CIN2. Combined HPV and/or methylation testing showed similar positivity rates as HPV and/or cytology. The CIN2/3 risk at 12 months posttreatment was 30.8% after a positive ASCL1/LHX8 result at 6 months posttreatment. Methylation levels of CIN2/3 in women with a persistent HPV infection were significantly higher compared with women with an incident or no HPV infection. In conclusion, posttreatment monitoring by methylation analysis of ASCL1/LHX8 and FAM19A4/miR124-2 showed a good performance for the detection of recurrent CIN. DNA methylation testing can help to identify women with recurrent CIN that require re-treatment.

Identifiants

pubmed: 37539971
doi: 10.1002/ijc.34678
doi:

Banques de données

NTR
['NTR1964']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2011-2018

Informations de copyright

© 2023 The Authors. International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.

Références

Soutter WP, Sasieni P, Panoskaltsis T. Long-term risk of invasive cervical cancer after treatment of squamous cervical intraepithelial neoplasia. Int J Cancer. 2006;118(8):2048-2055. doi:10.1002/ijc.21604
Rebolj M, Helmerhorst T, Habbema D, et al. Risk of cervical cancer after completed post-treatment follow-up of cervical intraepithelial neoplasia: population based cohort study. BMJ. 2012;345:e6855. doi:10.1136/bmj.e6855
Strander B, Andersson-Ellström A, Milsom I, Sparén P. Long term risk of invasive cancer after treatment for cervical intraepithelial neoplasia grade 3: population based cohort study. BMJ. 2007;335(7629):1077. doi:10.1136/bmj.39363.471806.BE
Strander B, Hällgren J, Sparén P. Effect of ageing on cervical or vaginal cancer in Swedish women previously treated for cervical intraepithelial neoplasia grade 3: population based cohort study of long term incidence and mortality. BMJ. 2014;348:f7361. doi:10.1136/bmj.f7361
Kocken M, Helmerhorst TJ, Berkhof J, et al. Risk of recurrent high-grade cervical intraepithelial neoplasia after successful treatment: a long-term multi-cohort study. Lancet Oncol. 2011;12(5):441-450. doi:10.1016/s1470-2045(11)70078-x
Arbyn M, Ronco G, Anttila A, et al. Evidence regarding human papillomavirus testing in secondary prevention of cervical cancer. Vaccine. 2012;30(suppl 5):F88-F99. doi:10.1016/j.vaccine.2012.06.095
Clarke MA, Unger ER, Zuna R, et al. A systematic review of tests for Postcolposcopy and Posttreatment surveillance. J Lower Genit Tract Dis. 2020;24(2):148-156. doi:10.1097/lgt.0000000000000526
Cuschieri K, Bhatia R, Cruickshank M, Hillemanns P, Arbyn M. HPV testing in the context of post-treatment follow up (test of cure). J Clin Virol. 2016;76(suppl 1):S56-s61. doi:10.1016/j.jcv.2015.10.008
Tainio K, Athanasiou A, Tikkinen KAO, et al. Clinical course of untreated cervical intraepithelial neoplasia grade 2 under active surveillance: systematic review and meta-analysis. BMJ. 2018;360:k499. doi:10.1136/bmj.k499
Castle PE, Schiffman M, Wheeler CM, Solomon D. Evidence for frequent regression of cervical intraepithelial neoplasia-grade 2. Obstet Gynecol. 2009;113(1):18-25. doi:10.1097/AOG.0b013e31818f5008
Kyrgiou M, Athanasiou A, Paraskevaidi M, et al. Adverse obstetric outcomes after local treatment for cervical preinvasive and early invasive disease according to cone depth: systematic review and meta-analysis. BMJ. 2016;354:i3633. doi:10.1136/bmj.i3633
Loopik DL, van Drongelen J, Bekkers RLM, et al. Cervical intraepithelial neoplasia and the risk of spontaneous preterm birth: a Dutch population-based cohort study with 45,259 pregnancy outcomes. PLoS Med. 2021;18(6):e1003665. doi:10.1371/journal.pmed.1003665
Wiik J, Nilsson S, Kärrberg C, Strander B, Jacobsson B, Sengpiel V. Associations of treated and untreated human papillomavirus infection with preterm delivery and neonatal mortality: a Swedish population-based study. PLoS Med. 2021;18(5):e1003641. doi:10.1371/journal.pmed.1003641
de Strooper LM, Meijer CJ, Berkhof J, et al. Methylation analysis of the FAM19A4 gene in cervical scrapes is highly efficient in detecting cervical carcinomas and advanced CIN2/3 lesions. Cancer Prev Res. 2014;7(12):1251-1257. doi:10.1158/1940-6207.capr-14-0237
Bierkens M, Hesselink AT, Meijer CJ, et al. CADM1 and MAL promoter methylation levels in hrHPV-positive cervical scrapes increase proportional to degree and duration of underlying cervical disease. Int J Cancer. 2013;133(6):1293-1299. doi:10.1002/ijc.28138
Kremer WW, Dick S, Heideman DAM, et al. Clinical regression of high-grade cervical intraepithelial neoplasia is associated with absence of FAM19A4/miR124-2 DNA methylation (CONCERVE study). J Clin Oncol. 2022;40(26):3037-3046. doi:10.1200/jco.21.02433
Uijterwaal MH, Van Zummeren M, Kocken M, et al. Performance of CADM1/MAL-methylation analysis for monitoring of women treated for high-grade CIN. Gynecol Oncol. 2016;143(1):135-142. doi:10.1016/j.ygyno.2016.07.089
Dick S, Verhoef L, De Strooper LM, et al. Evaluation of six methylation markers derived from genome-wide screens for detection of cervical precancer and cancer. Epigenomics. 2020;12(18):1569-1578. doi:10.2217/epi-2019-0331
Bonde J, Floore A, Ejegod D, et al. Methylation markers FAM19A4 and miR124-2 as triage strategy for primary human papillomavirus screen positive women: a large European multicenter study. Int J Cancer. 2021;148(2):396-405. doi:10.1002/ijc.33320
Verhoef L, Bleeker MCG, Polman N, et al. Performance of DNA methylation analysis of ASCL1, LHX8, ST6GALNAC5, GHSR, ZIC1 and SST for the triage of HPV-positive women: results from a Dutch primary HPV-based screening cohort. Int J Cancer. 2022;150(3):440-449. doi:10.1002/ijc.33820
Van den Brule AJ, Pol R, Fransen-Daalmeijer N, Schouls LM, Meijer CJLM, Snijders PJ. GP5+/6+ PCR followed by reverse line blot analysis enables rapid and high-throughput identification of human papillomavirus genotypes. J Clin Microbiol. 2002;40(3):779-787.
Bulk S, Van Kemenade FJ, Rozendaal L, Meijer CJ. The Dutch CISOE-A framework for cytology reporting increases efficacy of screening upon standardisation since 1996. J Clin Pathol. 2004;57(4):388-393.
Kennisinstituut van de Federatie van Medisch Specialisten. Richtllijn CIN, AIS en VAIN. https://richtlijnendatabase.nl/richtlijn/cin_ais_en_vain/follow_up/na_behandelde_cin2_3.html
Verlaat W, Snoek BC, Heideman DAM, et al. Identification and validation of a 3-gene methylation classifier for HPV-based cervical screening on self-samples. Clin Cancer Res. 2018;24(14):3456-3464. doi:10.1158/1078-0432.Ccr-17-3615
Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101-1108.
De Strooper LMA, Berkhof J, Steenbergen RDM, et al. Cervical cancer risk in HPV-positive women after a negative FAM19A4/mir124-2 methylation test: a post hoc analysis in the POBASCAM trial with 14 year follow-up. Int J Cancer. 2018;143(6):1541-1548. doi:10.1002/ijc.31539
Bottari F, Iacobone AD, Passerini R, et al. Human papillomavirus genotyping compared with a qualitative high-risk human papillomavirus test after treatment of high-grade cervical intraepithelial neoplasia: a systematic review. Obstet Gynecol. 2019;134(3):452-462. doi:10.1097/aog.0000000000003409
Iacobone AD, Radice D, Sandri MT, et al. Human papillomavirus same genotype persistence and risk of cervical intraepithelial Neoplasia2+ recurrence. Cancers. 2021;13(15). doi:10.3390/cancers13153664
Ouh YT, Cho HW, Kim SM, et al. Risk factors for type-specific persistence of high-risk human papillomavirus and residual/recurrent cervical intraepithelial neoplasia after surgical treatment. Obstet Gynecol Sci. 2020;63(5):631-642. doi:10.5468/ogs.20049
Söderlund-Strand A, Kjellberg L, Dillner J. Human papillomavirus type-specific persistence and recurrence after treatment for cervical dysplasia. J Med Virol. 2014;86(4):634-641. doi:10.1002/jmv.23806
Mariani L, Sandri MT, Preti M, et al. HPV-testing in follow-up of patients treated for CIN2+ lesions. J Cancer. 2016;7(1):107-114. doi:10.7150/jca.13503
Venturoli S, Ambretti S, Cricca M, et al. Correlation of high-risk human papillomavirus genotypes persistence and risk of residual or recurrent cervical disease after surgical treatment. J Med Virol. 2008;80(8):1434-1440. doi:10.1002/jmv.21198

Auteurs

Stèfanie Dick (S)

Department of Pathology, Amsterdam UMC, Location Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
Cancer Center Amsterdam, Imaging and Biomarkers, Amsterdam, The Netherlands.

Daniëlle A M Heideman (DAM)

Department of Pathology, Amsterdam UMC, Location Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
Cancer Center Amsterdam, Imaging and Biomarkers, Amsterdam, The Netherlands.

Constantijne H Mom (CH)

Cancer Center Amsterdam, Imaging and Biomarkers, Amsterdam, The Netherlands.
Department of Gynecological Oncology, Amsterdam UMC, Location University of Amsterdam, Amsterdam, The Netherlands.

Chris J L M Meijer (CJLM)

Department of Pathology, Amsterdam UMC, Location Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
Cancer Center Amsterdam, Imaging and Biomarkers, Amsterdam, The Netherlands.

Johannes Berkhof (J)

Cancer Center Amsterdam, Imaging and Biomarkers, Amsterdam, The Netherlands.
Department of Epidemiology and Data Science, Amsterdam UMC, Location Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.

Renske D M Steenbergen (RDM)

Department of Pathology, Amsterdam UMC, Location Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
Cancer Center Amsterdam, Imaging and Biomarkers, Amsterdam, The Netherlands.

Maaike C G Bleeker (MCG)

Department of Pathology, Amsterdam UMC, Location Vrije Universiteit Amsterdam, Amsterdam, The Netherlands.
Cancer Center Amsterdam, Imaging and Biomarkers, Amsterdam, The Netherlands.

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