Detection of (pre)cancerous colorectal lesions in Lynch syndrome patients by microsatellite instability liquid biopsy.
Journal
Cancer gene therapy
ISSN: 1476-5500
Titre abrégé: Cancer Gene Ther
Pays: England
ID NLM: 9432230
Informations de publication
Date de publication:
09 Feb 2024
09 Feb 2024
Historique:
received:
14
09
2023
accepted:
12
12
2023
revised:
06
12
2023
medline:
9
2
2024
pubmed:
9
2
2024
entrez:
8
2
2024
Statut:
aheadofprint
Résumé
Lynch syndrome (LS) is an inherited condition characterized by an increased risk of developing cancer, in particular colorectal cancer (CRC). Microsatellite instability (MSI) is the main feature of (pre)cancerous lesions occurring in LS patients. Close endoscopic surveillance is the only option available to reduce CRC morbidity and mortality. However, it may fail to intercept interval cancers and patients' compliance to such an invasive procedure may decrease over the years. The development of a minimally invasive test able to detect (pre)cancerous colorectal lesions, could thus help tailor surveillance programs in LS patients. Taking advantage of an endoscopic surveillance program, we retrospectively assessed the instability of five microsatellites (BAT26, BAT25, NR24, NR21, and Mono27) in liquid biopsies collected at baseline and possibly at two further endoscopic rounds. For this purpose, we tested a new multiplex drop-off digital polymerase chain reaction (dPCR) assay, reaching mutant allele frequencies (MAFs) as low as 0.01%. Overall, 78 plasma samples at the three time-points from 18 patients with baseline (pre)cancerous lesions and 18 controls were available for molecular analysis. At baseline, the MAFs of BAT26, BAT25 and NR24 were significantly higher in samples of patients with lesions but did not differ with respect to the grade of dysplasia or any other clinico-pathological characteristics. When all markers were combined to determine MSI in blood, this test was able to discriminate lesion-bearing patients with an AUC of 0.80 (95%CI: 0.66; 0.94).
Identifiants
pubmed: 38332046
doi: 10.1038/s41417-023-00721-z
pii: 10.1038/s41417-023-00721-z
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Yurgelun MB, Hampel H. Recent advances in lynch syndrome: diagnosis, treatment, and cancer prevention. Am Soc Clin Oncol Educ B. 2018;38:101–9.
doi: 10.1200/EDBK_208341
Win AK, Jenkins MA, Dowty JG, Antoniou AC, Lee A, Giles GG, et al. Prevalence and penetrance of major genes and polygenes for colorectal cancer. Cancer Epidemiol Biomark Prev. 2017;26:404–12.
doi: 10.1158/1055-9965.EPI-16-0693
Abu-Ghazaleh N, Kaushik V, Gorelik A, Jenkins M, Macrae F. Worldwide prevalence of Lynch syndrome in patients with colorectal cancer: systematic review and meta-analysis. Genet Med. 2022;24:971–85.
doi: 10.1016/j.gim.2022.01.014
pubmed: 35177335
Hampel H, De La Chapelle A. How do we approach the goal of identifying everybody with Lynch Syndrome? Fam Cancer. 2013;12:313–7.
doi: 10.1007/s10689-013-9611-5
pubmed: 23568035
pmcid: 4337020
Ahadova A, Seppälä TT, Engel C, Gallon R, Burn J, Holinski-Feder E, et al. The “unnatural” history of colorectal cancer in Lynch syndrome: Lessons from colonoscopy surveillance. Int J Cancer. 2021 Feb 15 [cited 2023 Jan 17];148:800–11. https://onlinelibrary.wiley.com/doi/full/10.1002/ijc.33224
Ahadova A, Gallon R, Gebert J, Ballhausen A, Endris V, Kirchner M, et al. Three molecular pathways model colorectal carcinogenesis in Lynch syndrome. Int J Cancer. 2018;143:139–50.
doi: 10.1002/ijc.31300
pubmed: 29424427
Valle L. Lynch syndrome: a single hereditary cancer syndrome or multiple syndromes defined by different mismatch repair genes? Gastroenterology. 2023;165:20–3.
doi: 10.1053/j.gastro.2023.04.027
pubmed: 37142200
Hall G, Clarkson A, Shi A, Langford E, Leung H, Eckstein RP, et al. Immunohistochemistry for PMS2 and MSH6 alone can replace a four antibody panel for mismatch repair deficiency screening in colorectal adenocarcinoma. Pathology. 2010;42:409–13.
doi: 10.3109/00313025.2010.493871
pubmed: 20632815
Nowak JA, Yurgelun MB, Bruce JL, Rojas-Rudilla V, Hall DL, Shivdasani P, et al. Detection of mismatch repair deficiency and microsatellite instability in colorectal adenocarcinoma by targeted next-generation sequencing. J Mol Diagnostics. 2017;19:84–91.
doi: 10.1016/j.jmoldx.2016.07.010
Signoroni S, Tibiletti MG, Ricci MT, Milione M, Perrone F, Pensotti V, et al. Performance of tumor testing for Lynch syndrome identification in patients with colorectal cancer: a retrospective single-center study. Tumori [Internet]. 2019 Feb 1 [cited 2023 Jul 17];105(1):76–83. https://journals.sagepub.com/doi/10.1177/0300891618792460?url_ver=Z39.88-2003&rfr_id=ori%3Arid%3Acrossref.org&rfr_dat=cr_pub++0pubmed
Wu S, Liu X, Wang J, Zhou W, Guan M, Liu Y, et al. DNA mismatch repair deficiency detection in colorectal cancer by a new microsatellite instability analysis system. Interdiscip Sci – Comput Life Sci. 2020 Jun 1 [cited 2023 Mar 8];12(2):145–54. https://link.springer.com/article/10.1007/s12539-020-00358-8
Gilson P, Levy J, Rouyer M, Demange J, Husson M, Bonnet C, et al. Evaluation of 3 molecular-based assays for microsatellite instability detection in formalin-fixed tissues of patients with endometrial and colorectal cancers. Sci Rep. 2020;10:16386.
doi: 10.1038/s41598-020-73421-5
pubmed: 33009475
pmcid: 7532161
Baudrin LG, Deleuze JF, How-Kit A. Molecular and computational methods for the detection of microsatellite instability in cancer. Front Oncol. 2018;8:621.
doi: 10.3389/fonc.2018.00621
pubmed: 30631754
pmcid: 6315116
Sinicrope FA. Lynch syndrome–associated colorectal cancer. N Engl J Med. 2018;379:764–73.
doi: 10.1056/NEJMcp1714533
pubmed: 30134129
Signoroni S, Piozzi GN, Ricci MT, Mancini A, Morabito A, Bertario L, et al. Risk factors for metachronous colorectal cancer in Lynch syndrome patients: a registry-based observational mono-institutional study cohort. Int J Clin Oncol. 2020 Sep 1 [cited 2023 Jul 17];25(9):1644–52. https://pubmed.ncbi.nlm.nih.gov/32430733/
Giardiello FM, Allen JI, Axilbund JE, Boland CR, Burke CA, Burt RW, et al. Guidelines on genetic evaluation and management of lynch syndrome: a consensus statement by the us multi-society task force on colorectal cancer. Gastroenterology. 2014;147:502–26.
doi: 10.1053/j.gastro.2014.04.001
pubmed: 25043945
Møller P, Seppälä T, Bernstein I, Holinski-Feder E, Sala P, Evans DG, et al. Cancer incidence and survival in Lynch syndrome patients receiving colonoscopic and gynaecological surveillance: first report from the prospective Lynch syndrome database. Gut 2017;66:464–72.
doi: 10.1136/gutjnl-2015-309675
pubmed: 26657901
Seppälä TT, Ahadova A, Dominguez-Valentin M, Macrae F, Evans DG, Therkildsen C, et al. Lack of association between screening interval and cancer stage in Lynch syndrome may be accounted for by over-diagnosis; A prospective Lynch syndrome database report. Hered Cancer Clin Pract. 2019;17:8.
doi: 10.1186/s13053-019-0106-8
pubmed: 30858900
pmcid: 6394091
Gilson P, Merlin JL, Harlé A. Detection of microsatellite instability: State of the art and future applications in circulating tumour dna (ctdna). Cancers. 2021;13:1491. MDPI AG
doi: 10.3390/cancers13071491
pubmed: 33804907
pmcid: 8037825
Olmedillas-López S, Olivera-Salazar R, García-Arranz M, García-Olmo D. Current and emerging applications of droplet digital PCR in oncology: an updated review. Mol Diagnosis Ther. 2022;26:61–87.
doi: 10.1007/s40291-021-00562-2
Georgiadis A, Durham JN, Keefer LA, Bartlett BR, Zielonka M, Murphy D, et al. Noninvasive detection of microsatellite instabilit and high tumor mutation burden in cancer patients treated with PD-1 blockade. Clin Cancer Res. 2019;25:7024–34.
doi: 10.1158/1078-0432.CCR-19-1372
pubmed: 31506389
pmcid: 6892397
Crisafulli G, Sartore-Bianchi A, Lazzari L, Pietrantonio F, Amatu A, Macagno M, et al. Temozolomide treatment alters mismatch repair and boosts mutational burden in tumor and blood of colorectal cancer patients. Cancer Discov. 2022;12:1656–75.
doi: 10.1158/2159-8290.CD-21-1434
pubmed: 35522273
pmcid: 9394384
Silveira AB, Bidard FC, Kasperek A, Melaabi S, Tanguy ML, Rodrigues M, et al. High-accuracy determination of microsatellite instability compatible with liquid biopsies. Clin Chem. 2020;66:606–13.
doi: 10.1093/clinchem/hvaa013
pubmed: 32176763
Suraweera N, Duval A, Reperant M, Vaury C, Furlan D, Leroy K, et al. Evaluation of tumor microsatellite instability using five quasimonomorphic mononucleotide repeats and pentaplex PCR. Gastroenterology [Internet]. 2002;123(6):1804–11. https://pubmed.ncbi.nlm.nih.gov/12454837/
Whale AS, De Spiegelaere W, Trypsteen W, Nour AA, Bae YK, Benes V, et al. The Digital MIQE guidelines update: minimum information for publication of quantitative digital PCR experiments for 2020. Clin Chem. 2020;66:1012–29.
doi: 10.1093/clinchem/hvaa125
Corné J, Le Du F, Quillien V, Godey F, Robert L, Bourien H, et al. Development of multiplex digital PCR assays for the detection of PIK3CA mutations in the plasma of metastatic breast cancer patients. Sci Rep. 2021;11:17316.
doi: 10.1038/s41598-021-96644-6
pubmed: 34453076
pmcid: 8397758
Klouch KZ, Stern MH, Trabelsi-Grati O, Kiavue N, Cabel L, Silveira AB, et al. Microsatellite instability detection in breast cancer using drop-off droplet digital PCR. Oncogene. 2022;41:5289–97.
doi: 10.1038/s41388-022-02504-6
pubmed: 36329125
Hollander M, Wolfe DA, Chicken E. Nonparametric Statistical Methods, 3rd edn. Wiley; 2014. 848 p. https://www.wiley.com/en-ie/Nonparametric+Statistical+Methods%2C+3rd+Edition-p-9781118553299
Artusi R, Verderio P, Marubini E. Bravais-Pearson and spearman correlation coefficients: meaning, test of hypothesis and confidence interval. 2002;17:148–51. https://journals.sagepub.com/doi/10.1177/172460080201700213?url_ver=Z39.88-2003&rfr_id=ori%3Arid%3Acrossref.org&rfr_dat=cr_pub++0pubmed
Latham A, Srinivasan P, Kemel Y, Shia J, Bandlamudi C, Mandelker D, et al. Microsatellite instability is associated with the presence of lynch syndrome pan-cancer. J Clin Oncol. 2018;37:286–95. https://doi.org/10.1200/JCO.18.00283 .
doi: 10.1200/JCO.18.00283
pubmed: 30376427
pmcid: 6553803
Aharonov R, Lebanony D, Benjamin H, Gilad S, Ezagouri M, Dov A, et al. Diagnostic assay based on hsa-miR-205 expression distinguishes squamous from nonsquamous non-small-cell lung carcinoma. J Clin Oncol. 2009;27:2030–7. http://ascopubs.org/doi/10.1200/JCO.2008.19.4134
doi: 10.1200/JCO.2008.19.4134
pubmed: 19273703
Whale AS, Huggett JF, Tzonev S. Fundamentals of multiplexing with digital PCR. Biomol Detect Quantif. 2016;10:15–23.
doi: 10.1016/j.bdq.2016.05.002
pubmed: 27990345
pmcid: 5154634
Seppälä TT, Latchford A, Negoi I, Sampaio Soares A, Jimenez-Rodriguez R, Evans DG, et al. European guidelines from the EHTG and ESCP for Lynch syndrome: an updated third edition of the Mallorca guidelines based on gene and gender. Br J Surg. 2021;108:484–98. https://doi.org/10.1002/bjs.11902
doi: 10.1002/bjs.11902
pubmed: 34043773
pmcid: 10364896
Boldrin E, Piano MA, Alfieri R, Mazza M, Vassallo L, Scapinello A, et al. Msi analysis in solid and liquid biopsies of gastroesophageal adenocarcinoma patients: a molecular approach. Int J Mol Sci. 2021;22:7244.
doi: 10.3390/ijms22147244
pubmed: 34298864
pmcid: 8303574