Evaluation of the Sensitivity and Specificity of MiRNAs in Discriminating Oral Squamous Cell Carcinoma: A Systematic Review and Meta-analysis

Document Type : Review Article

Authors

1 Department of Oral and Maxillofacial Radiology, School of Dentistry, Islamic Azad University, Isfahan (Khorasgan) Branch, Isfahan, Iran

2 Department of Oral Medicine, School of Dentistry, Shahid Beheshti University of Medical Sciences, Tehran, Iran

3 Department of Oral Medicine, School of Dentistry, Hamadan University of Medical Sciences, Hamadan, Iran

4 Student Research Committee, School of Dentistry, Babol University of Medical Sciences, Babol, Iran

5 Department of Periodontics, School of Dentistry, Tehran University of Medical Sciences, Tehran, Iran

Abstract

Background and aim: Approximately 90% of all oral malignant tumors are squamous cell carcinomas. This study aims to evaluate the sensitivity and specificity of miRNAs in discriminating oral squamous cell carcinoma.
Material and methods:
There are many international databases such as PubMed, Scopus, Science Direct, ISI, Web of Knowledge, Embase, and many other databases in oral squamous cell carcinoma searched until May 2023. Data analysis using STATA/MP. V17 software was done in 95% confidence intervals. Effect size (sensitivity and specificity) were calculated using a fixed effect model with an inverse-variance method.
Results:
The full text of 25 studies was reviewed; finally, 17 studies were selected according to the objectives of the present study and included in the meta-analysis. The sensitivity and specificity of miRNAs in diagnosing OSCC were 77% (ES, 77% CI; 70%, 84%; p<0.01) and 80% (ES, 80% CI; 73%, 87%; p<0.01), respectively. Test of group differences showed no significant difference between sensitivity and specificity of the salivary, blood, and serum miRNAs in diagnosing oral squamous cell carcinoma (OSCC) (p>0.05).
Conclusions:
Based on the meta-analysis of the present study, the diagnostic accuracy of miRNAs for the diagnosis of OSCC is high; Blood, saliva, and serum miRNAs had similar sensitivity and specificity.

Keywords

Main Subjects


[1]  Chandraprasad MS, Dey A, Swamy MK. Introduction to cancer and treatment approaches. InPaclitaxel 2022:1-27. https://doi.org/10.1016/B978-0-323-90951-8.00010-2.
[2]  Moretz-Sohn PF, Dias FL, de Carvalho Marques CM. Minor Salivary Gland Cancer of the Head and Neck: A Review of Epidemiologic Aspects, Prognostic Factors, and Outcomes. Current Oncology Reports. 2023;25(3):173-9. https://doi.org/10.1007/s11912-022-01356-3.
[3]  Racine F, Soudet S, Sevestre MA, Galmiche A, Saidak Z. The coagulome of oral squamous cell carcinoma: examining the role and regulation of coagulation in oral cancers using a systems approach. Current Opinion in Otolaryngology & Head and Neck Surgery. 2023;31(2):73-7. https://doi.org/10.1097/MOO.0000000000000870.
[4]  Chai AW, Lim KP, Cheong SC. Translational genomics and recent advances in oral squamous cell carcinoma. InSeminars in cancer biology 2020;61:71-83. https://doi.org/10.1016/j.semcancer.2019.09.011.
[5]  Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA: a cancer journal for clinicians. 2013;63(1):11-30. https://doi.org/10.3322/caac.21166.
[6]  Wu K, Wei J, Liu Z, Yu B, Yang X, Zhang C, et al. Can pattern and depth of invasion predict lymph node relapse and prognosis in tongue squamous cell carcinoma. BMC cancer. 2019;19:1-9. https://doi.org/10.1186/s12885-019-5859-y.
[7]  Abati S, Bramati C, Bondi S, Lissoni A, Trimarchi M. Oral cancer and precancer: a narrative review on the relevance of early diagnosis. International journal of environmental research and public health. 2020;17(24):9160. https://doi.org/10.3390/ijerph17249160.
[8]  Interval ET, Whitenack N, Panwar A. Role of Frailty and Comorbidity in Determination of Operability for Patients With Oral and Oropharyngeal Squamous Cell Carcinoma. Current Otorhinolaryngology Reports. 2019;7:39-48. https://doi.org/10.1007/s40136-019-00225-1.
[9]  Narimani A, Hosseini F, Bahrami N, Mohamadnia A. The Expression of MicroRNA-155 (miR-155) and Carcinoembryonic Antigen Messenger RNA (CEA mRNA) in Peripheral Blood of Patients with Oral Squamous Cell Carcinomas (OSCC). Journal of Isfahan Medical School. 2019;36(510):1597-601. https://doi.org/10.22122/jims.v36i510.10925.
[10] Thomas C, Gustafsson JÅ. The different roles of ER subtypes in cancer biology and therapy. Nature Reviews Cancer. 2011;11(8):597-608. https://doi.org/10.1038/nrc3093.
[11] Zehentner BK, Dillon DC, Jiang Y, Xu J, Bennington A, Molesh DA, et al. Application of a multigene reverse transcription-PCR assay for detection of mammaglobin and complementary transcribed genes in breast cancer lymph nodes. Clinical chemistry. 2002;48(8):1225-31. https://doi.org/10.1093/clinchem/48.8.1225.
[12] Hussen BM, Hidayat HJ, Salihi A, Sabir DK, Taheri M, Ghafouri-Fard S. MicroRNA: A signature for cancer progression. Biomedicine & Pharmacotherapy. 2021;138:111528. https://doi.org/10.1016/j.biopha.2021.111528.
[13] Reda El Sayed S, Cristante J, Guyon L, Denis J, Chabre O, Cherradi N. MicroRNA therapeutics in cancer: current advances and challenges. Cancers. 2021;13(11):2680. https://doi.org/10.3390/cancers13112680.
[14] Chakraborty C, Sharma AR, Sharma G, Lee SS. Therapeutic advances of miRNAs: A preclinical and clinical update. Journal of advanced research. 2021;28:127-38. https://doi.org/10.1016/j.jare.2020.08.012.
[15] Piao Y, Jung SN, Lim MA, Oh C, Jin YL, Kim HJ, et al. A circulating microRNA panel as a novel dynamic monitor for oral squamous cell carcinoma. Scientific Reports. 2023;13(1):2000. https://doi.org/10.1038/s41598-023-28550-y.
[16] Sethi N, Wright A, Wood H, Rabbitts P. MicroRNAs and head and neck cancer: reviewing the first decade of research. European Journal of Cancer. 2014;50(15):2619-35. https://doi.org/10.1016/j.ejca.2014.07.012.
[17] Tugwell P, Tovey D. PRISMA 2020. Journal of Clinical Epidemiology. 2021;134:A5-6. https://doi.org/10.1016/j.jclinepi.2021.04.008.
[18] Lee J, Mulder F, Leeflang M, Wolff R, Whiting P, Bossuyt PM. QUAPAS: An Adaptation of the QUADAS-2 Tool to Assess Prognostic Accuracy Studies. Annals of Internal Medicine. 2022;175(7):1010-8. https://doi.org/10.7326/M22-0276.
[19] Mazumder S, Basu B, Ray JG, Chatterjee R. MiRNAs as non-invasive biomarkers in the serum of Oral Squamous Cell Carcinoma (OSCC) and Oral Potentially Malignant Disorder (OPMD) patients. Archives of Oral Biology. 2023;147:105627. https://doi.org/10.1016/j.archoralbio.2023.105627.
[20] Ukey S, Jain A, Dwivedi S, Choudhury C, Vishnoi JR, Chugh A, et al. Study of MicroRNA (miR-221-3p, miR-133a-3p, and miR-9-5p) expressions in oral submucous fibrosis and squamous cell carcinoma. Indian Journal of Clinical Biochemistry. 2023;38(1):73-82. https://doi.org/10.1007/s12291-022-01035-x.
[21] Scholtz B, Horváth J, Tar I, Kiss C, Márton IJ. Salivary miR-31-5p, miR-345-3p, and miR-424-3p are reliable biomarkers in patients with oral squamous cell carcinoma. Pathogens. 2022;11(2):229. https://doi.org/10.3390/pathogens11020229.
[22] Jadhav KB, Shah V, Chauhan N, Shah N, Parmar G. Expression of microRNA-21 in saliva and tumor tissue of patients with oral squamous cell carcinoma: a predictor of cervical lymph node metastasis. Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology. 2022;133(1):60-9. https://doi.org/10.1016/j.oooo.2021.07.012.
[23] Karimi A, Bahrami N, Sayedyahossein A, Derakhshan S. Evaluation of circulating serum 3 types of microRNA as biomarkers of oral squamous cell carcinoma; A pilot study. Journal of Oral Pathology & Medicine. 2020;49(1):43-8. https://doi.org/10.1111/jop.12959.
[24] Emami N, Mohamadnia A, Mirzaei M, Bayat M, Mohammadi F, Bahrami N. miR-155, miR-191, and miR-494 as diagnostic biomarkers for oral squamous cell carcinoma and the effects of Avastin on these biomarkers. Journal of the Korean Association of Oral and Maxillofacial Surgeons. 2020;46(5):341-7. https://doi.org/10.5125/jkaoms.2020.46.5.341.
[25] He L, Ping F, Fan Z, Zhang C, Deng M, Cheng B, et al. Salivary exosomal miR-24-3p serves as a potential detective biomarker for oral squamous cell carcinoma screening. Biomedicine & Pharmacotherapy. 2020;121:109553. https://doi.org/10.1016/j.biopha.2019.109553.
[26] Chang YA, Weng SL, Yang SF, Chou CH, Huang WC, Tu SJ, et al. A three–microRNA signature as a potential biomarker for the early detection of oral cancer. International journal of molecular sciences. 2018;19(3):758. https://doi.org/10.3390/ijms19030758.
[27] Chen L, Hu J, Pan L, Yin X, Wang Q, Chen H. Diagnostic and prognostic value of serum miR-99a expression in oral squamous cell carcinoma. Cancer Biomarkers. 2018;23(3):333-9. https://doi.org/10.3233/CBM-181265.
[28] Sun G, Cao Y, Wang P, Song H, Bie T, Li M, et al. miR-200b-3p in plasma is a potential diagnostic biomarker in oral squamous cell carcinoma. Biomarkers. 2018;23(2):137-41. https://doi.org/10.1080/1354750X.2017.1289241.
[29] Wan Y, Vagenas D, Salazar C, Kenny L, Perry C, Calvopiña D, et al. Salivary miRNA panel to detect HPV-positive and HPV-negative head and neck cancer patients. Oncotarget. 2017;8(59):99990-100001. https://doi.org/10.18632/oncotarget.21725.
[30] Duz MB, Karatas OF, Guzel E, Turgut NF, Yilmaz M, Creighton CJ, et al. Identification of miR-139-5p as a saliva biomarker for tongue squamous cell carcinoma: a pilot study. Cellular Oncology. 2016;39:187-93. https://doi.org/10.1007/s13402-015-0259-z.
[31] Tachibana H, Sho R, Takeda Y, Zhang X, Yoshida Y, Narimatsu H, et al. Circulating miR-223 in oral cancer: its potential as a novel diagnostic biomarker and therapeutic target. PloS one. 2016;11(7):e0159693. https://doi.org/10.1371/journal.pone.0159693.
[32] Zahran F, Ghalwash D, Shaker O, Al-Johani K, Scully C. Salivary micro RNA s in oral cancer. Oral diseases. 2015;21(6):739-47. https://doi.org/10.1111/odi.12340.
[33] Momen-Heravi F, Trachtenberg AJ, Kuo WP, Cheng YS. Genomewide study of salivary microRNAs for detection of oral cancer. Journal of dental research. 2014;93(7_suppl):86S-93S. https://doi.org/10.1177/0022034514531018.
[34] Ren W, Qiang C, Gao L, Li SM, Zhang LM, Wang XL, et al. Circulating microRNA-21 (MIR-21) and phosphatase and tensin homolog (PTEN) are promising novel biomarkers for detection of oral squamous cell carcinoma. Biomarkers. 2014;19(7):590-6. https://doi.org/10.3109/1354750X.2014.955059.
[35] MacLellan SA, Lawson J, Baik J, Guillaud M, Poh CF, Garnis C. Differential expression of mi RNAs in the serum of patients with high‐risk oral lesions. Cancer medicine. 2012;1(2):268-74. https://doi.org/10.1002/cam4.17.
[36] Ramírez-Arroyo G, Hernaiz-Leonardo JC, Marvin-Huergo M, Dávalos-Fuentes MS. Types of Head and Neck Malignancy. Head and Neck Cancer: Hallmarks of the Inflammation Ecosystem. 2021;2:28-76.
[37] Abdollahzadeh R, Daraei A, Mansoori Y, Sepahvand M, Amoli MM, Tavakkoly-Bazzaz J. Competing endogenous RNA (ceRNA) cross talk and language in ceRNA regulatory networks: a new look at hallmarks of breast cancer. Journal of cellular physiology. 2019;234(7):10080-100. https://doi.org/10.1002/jcp.27941.
[38] Liu KY, Zhu SY, Brooks D, Bowlby R, Durham JS, Ma Y, et al. Tumor microRNA profile and prognostic value for lymph node metastasis in oral squamous cell carcinoma patients. Oncotarget. 2020;11(23):2204-15. https://doi.org/10.18632/oncotarget.27616.
[39] Yang J, Xu R, Wang C, Qiu J, Ren B, You L. Early screening and diagnosis strategies of pancreatic cancer: a comprehensive review. Cancer Communications. 2021;41(12):1257-74. https://doi.org/10.1002/cac2.12204.
[40] Sekikawa S, Kawachi H, Ogane S, Saito H, Takano M, Nomura T, et al. Which factors affect the long-term survival of patients with oral squamous cell carcinoma with distant metastasis?. Journal of oral and maxillofacial surgery. 2020;78(3):469-78. https://doi.org/10.1016/j.joms.2019.10.018.
[41] Romano A, Di Stasio D, Petruzzi M, Fiori F, Lajolo C, Santarelli A, et al. Noninvasive imaging methods to improve the diagnosis of oral carcinoma and its precursors: State of the art and proposal of a three-step diagnostic process. Cancers. 2021;13(12):2864. https://doi.org/10.3390/cancers13122864.