Serum microRNA-146a-5p and microRNA-221-3p as potential clinical biomarkers for papillary thyroid carcinoma.
Biomarkers
Circulating miRNA
Liquid biopsy
Papillary thyroid cancer
Patient follow-up
Journal
Journal of endocrinological investigation
ISSN: 1720-8386
Titre abrégé: J Endocrinol Invest
Pays: Italy
ID NLM: 7806594
Informations de publication
Date de publication:
19 Sep 2024
19 Sep 2024
Historique:
received:
16
04
2024
accepted:
08
09
2024
medline:
20
9
2024
pubmed:
20
9
2024
entrez:
19
9
2024
Statut:
aheadofprint
Résumé
Papillary thyroid carcinoma (PTC) is the most common malignant thyroid neoplasm, accounting for approximately 85% of all follicular cell-derived thyroid nodules. This study aimed to assess the diagnostic potential of circulating microRNA-146a-5p and microRNA-221-3p as biomarkers for PTC and their usefulness in monitoring disease progression during patient follow-up. An observational study was conducted on two cohorts of PTC patients and healthy controls (HCs) using digital PCR. We collected patients' clinical, biochemical, and imaging data during the post-surgery surveillance. We analyzed the levels of circulating miRNAs in serum samples of patients before surgery and during the follow-up, including those with indeterminate/biochemical incomplete response (IndR/BIR) and residual thyroid tissues (Thy Residue). Both miR-146a-5p and miR-221-3p were confirmed as effective biomarkers for PTC diagnosis. They enabled differentiation between pre-surgery PTC patients and HCs with an area under the curve (AUC) of 92% and 87.3%, respectively, using a threshold level of 768,545 copies/uL for miR-146a-5p and 389,331 copies/uL for miR-221-3p. It was found that miRNA fold change levels, rather than absolute levels, can be useful during patient follow-up. In particular, we found that a fold change of 2 for miR-146a-5p and 2.2 for miR-221-3p can identify a progressive disease, regardless of the presence of TgAbs or remnant thyroid. MiRNA-146a-5p and miRNA-221-3p, particularly the former, could be valuable diagnostic biomarkers for PTCs. They also seem to be effective in monitoring disease progression during patient follow-up by evaluating their fold change, even when thyroglobulin is uninformative.
Identifiants
pubmed: 39298113
doi: 10.1007/s40618-024-02467-3
pii: 10.1007/s40618-024-02467-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Kobaly K, Kim CS, Mandel SJ (2022) Contemporary management of thyroid nodules. Annu Rev Med 73:517–528. https://doi.org/10.1146/annurev-med-042220-015032
doi: 10.1146/annurev-med-042220-015032
pubmed: 34416120
Patel SG, Carty SE, Lee AJ (2021) Molecular testing for thyroid nodules including its interpretation and use in clinical practice. Ann Surg Oncol 28:8884–8891. https://doi.org/10.1245/s10434-021-10307-4
doi: 10.1245/s10434-021-10307-4
pubmed: 34275048
Grani G, Sponziello M, Pecce V, Ramundo V, Durante C (2020) Contemporary thyroid nodule evaluation and management. J Clin Endocrinol Metab 105:2869–2883. https://doi.org/10.1210/clinem/dgaa322
doi: 10.1210/clinem/dgaa322
pubmed: 32491169
pmcid: 7365695
Cibas ES, Ali SZ (2017) The 2017 Bethesda System for reporting thyroid cytopathology. Thyroid 27:1341–1346. https://doi.org/10.1089/thy.2017.0500
doi: 10.1089/thy.2017.0500
pubmed: 29091573
Sponziello M, Brunelli C, Verrienti A, Grani G, Pecce V, Abballe L, Ramundo V, Damante G, Russo D, Lombardi CP, Durante C, Rossi ED, Straccia P, Fadda G, Filetti S (2020) Performance of a dual-component molecular assay in cytologically indeterminate thyroid nodules. Endocrine. https://doi.org/10.1007/s12020-020-02271-y
doi: 10.1007/s12020-020-02271-y
pubmed: 33275186
Verrienti A, Pecce V, Abballe L, Ramundo V, Falcone R, Inanloo Nigi Jak F, Brunelli C, Fadda G, Bosco D, Ascoli V, Carletti R, Di Gioia C, Grani G, Sponziello M (2020) Analytical validation of a novel targeted next-generation sequencing assay for mutation detection in thyroid nodule aspirates and tissue. Endocrine. https://doi.org/10.1007/s12020-020-02372-8
doi: 10.1007/s12020-020-02372-8
pubmed: 33275186
Grani G, Sponziello M, Filetti S, Durante C (2021) Molecular analysis of fine-needle aspiration cytology in thyroid disease: where are we? Curr. Opin Otolaryngol Head Neck Surg 29:107–112. https://doi.org/10.1097/MOO.0000000000000698
doi: 10.1097/MOO.0000000000000698
Vignali P, Macerola E, Poma AM, Sparavelli R, Basolo F (2023) Indeterminate thyroid nodules: from cytology to Molecular Testing. Diagnostics 13. https://doi.org/10.3390/diagnostics13183008
Lam AK (2022) Papillary Thyroid Carcinoma: Current Position in Epidemiology, Genomics, and Classification. Presented at the
Campennì A, Aguennouz M, Siracusa M, Alibrandi A, Polito F, Oteri R, Baldari S, Ruggeri RM, Giovanella L (2022) Thyroid Cancer persistence in patients with unreliable thyroglobulin measurement: circulating microRNA as candidate alternative biomarkers. Cancers (Basel) 14. https://doi.org/10.3390/cancers14225620
Lamartina L, Grani G, Durante C, Borget I, Filetti S, Schlumberger M (2018) Follow-up of differentiated thyroid cancer – what should (and what should not) be done. Nat Rev Endocrinol 14:538–551. https://doi.org/10.1038/s41574-018-0068-3
doi: 10.1038/s41574-018-0068-3
pubmed: 30069030
Haugen BR, Alexander EK, Bible KC, Doherty GM, Mandel SJ, Nikiforov YE, Pacini F, Randolph GW, Sawka AM, Schlumberger M, Schuff KG, Sherman SI, Sosa JA, Steward DL, Tuttle RM, Wartofsky L (2016) 2015 American Thyroid Association Management Guidelines for adult patients with thyroid nodules and differentiated thyroid Cancer: the American Thyroid Association Guidelines Task Force on thyroid nodules and differentiated thyroid Cancer. Thyroid 26:1–133. https://doi.org/10.1089/THY.2015.0020
doi: 10.1089/THY.2015.0020
pubmed: 26462967
pmcid: 4739132
Evans C, Tennant S, Perros P (2015) Thyroglobulin in differentiated thyroid cancer. Clin Chim Acta 444:310–317. https://doi.org/10.1016/j.cca.2014.10.035
doi: 10.1016/j.cca.2014.10.035
pubmed: 25444737
Indrasena BSH (2017) Use of thyroglobulin as a tumour marker. World J Biol Chem 8:81. https://doi.org/10.4331/wjbc.v8.i1.81
doi: 10.4331/wjbc.v8.i1.81
pubmed: 28289520
pmcid: 5329716
Lin EC (2010) Radiation risk from medical imaging. Mayo Clin Proc 85:1142–1146. https://doi.org/10.4065/mcp.2010.0260
doi: 10.4065/mcp.2010.0260
pubmed: 21123642
pmcid: 2996147
Besharat ZM, Trocchianesi S, Verrienti A, Ciampi R, Cantara S, Romei C, Sabato C, Noviello TMR, Po A, Citarella A, Caruso FP, Panariello I, Gianno F, Carpino G, Gaudio E, Chiacchiarini M, Masuelli L, Sponziello M, Pecce V, Ramone T, Maino F, Dotta F, Ceccarelli M, Pezzullo L, Durante C, Castagna MG, Elisei R, Ferretti E (2023) Circulating miR-26b-5p and miR-451a as diagnostic biomarkers in medullary thyroid carcinoma patients. J Endocrinol Invest 46:2583–2599. https://doi.org/10.1007/s40618-023-02115-2
doi: 10.1007/s40618-023-02115-2
pubmed: 37286863
pmcid: 10632281
Geropoulos G, Psarras K, Papaioannou M, Giannis D, Meitanidou M, Kapriniotis K, Symeonidis N, Pavlidis ET, Pavlidis TE, Sapalidis K, Ahmed NM, Abdel-Aziz TE, Eddama MMR (2022) Circulating microRNAs and clinicopathological findings of papillary thyroid Cancer: a systematic review. Vivo (Brooklyn) 36:1551–1569. https://doi.org/10.21873/invivo.12866
doi: 10.21873/invivo.12866
Chen Y, Dong B, Huang L, Huang H (2022) Serum microRNAs as biomarkers for the diagnosis of papillary thyroid carcinoma: a meta-analysis. Bosn J Basic Med Sci 22:862–871. https://doi.org/10.17305/bjbms.2022.7343
doi: 10.17305/bjbms.2022.7343
pubmed: 35678022
pmcid: 9589316
Capriglione F, Verrienti A, Celano M, Maggisano V, Sponziello M, Pecce V, Gagliardi A, Giacomelli L, Aceti V, Durante C, Bulotta S, Russo D (2022) Analysis of serum microRNA in exosomal vehicles of papillary thyroid cancer. Endocrine 75:185–193. https://doi.org/10.1007/s12020-021-02847-2
doi: 10.1007/s12020-021-02847-2
pubmed: 34378123
Jankovic Miljus J, Guillén-Sacoto MA, Makiadi-Alvarado J, Wert-Lamas L, Ramirez-Moya J, Robledo M, Santisteban P, Riesco-Eizaguirre G (2022) Circulating MicroRNA profiles as potential biomarkers for differentiated thyroid Cancer recurrence. J Clin Endocrinol Metab 107:1280–1293. https://doi.org/10.1210/clinem/dgac009
doi: 10.1210/clinem/dgac009
pubmed: 35022762
Zhang Y, Xu D, Pan J, Yang Z, Chen M, Han J, Zhang S, Sun L, Qiao H (2017) Dynamic monitoring of circulating micrornas as a predictive biomarker for the diagnosis and recurrence of papillary thyroid carcinoma. Oncol Lett 13:4252–4266. https://doi.org/10.3892/ol.2017.6028
doi: 10.3892/ol.2017.6028
pubmed: 28599426
pmcid: 5452941
Celano M, Rosignolo F, Maggisano V, Pecce V, Iannone M, Russo D, Bulotta S (2017) MicroRNAs as biomarkers in thyroid carcinoma. Int J Genomics 2017. https://doi.org/10.1155/2017/6496570
Rosignolo F, Sponziello M, Giacomelli L, Russo D, Pecce V, Biffoni M, Bellantone R, Lombardi CP, Lamartina L, Grani G, Durante C, Filetti S, Verrienti A (2017) Identification of thyroid-Associated serum microRNA profiles and their potential use in thyroid Cancer Follow-Up. J Endocr Soc 1:3–13. https://doi.org/10.1210/JS.2016-1032
doi: 10.1210/JS.2016-1032
pubmed: 29264441
pmcid: 5677215
Mahul B, Amin SB, Edge FL, Greene DR, Byrd RK, Brookland MK, Washington JE, Gershenwald CC, Compton KR, Hess DC, Sullivan J, Milburn Jessup JD, Brierley LE, Gaspar (2017) AJCC Cancer Staging Manual. Springer Cham, Richard L, L.R.M.
Filetti S, Durante C, Hartl D, Leboulleux S, Locati LD, Newbold K, Papotti MG, Berruti A (2019) Thyroid cancer: ESMO Clinical Practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 30:1856–1883. https://doi.org/10.1093/annonc/mdz400
doi: 10.1093/annonc/mdz400
pubmed: 31549998
Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M, Rubinstein L, Shankar L, Dodd L, Kaplan R, Lacombe D, Verweij J (2009) New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer 45:228–247. https://doi.org/10.1016/j.ejca.2008.10.026
doi: 10.1016/j.ejca.2008.10.026
pubmed: 19097774
Suárez B, Solé C, Márquez M, Nanetti F, Lawrie CH (2022) Circulating MicroRNAs as Cancer biomarkers in Liquid biopsies. Adv Exp Med Biol 1385. https://doi.org/10.1007/978-3-031-08356-3_2
Graham MER, Hart RD, Douglas S, Makki FM, Pinto D, Butler AL, Bullock M, Rigby MH, Trites JRB, Taylorand SM, Singh R (2015) Serum microRNA profiling to distinguish papillary thyroid cancer from benign thyroid masses. J Otolaryngol - Head Neck Surg 44:1–9. https://doi.org/10.1186/s40463-015-0083-5
doi: 10.1186/s40463-015-0083-5
Zhang A, Wang C, Lu H, Chen X, Ba Y, Zhang C, Zhang CY (2019) Altered serum MicroRNA profile may serve as an auxiliary tool for discriminating aggressive thyroid carcinoma from nonaggressive thyroid cancer and benign thyroid nodules. Dis Markers 2019. https://doi.org/10.1155/2019/3717683