Diagnostic accuracy of serum derived exosomes for hepatocellular carcinoma: a systematic review and meta-analysis

References

• Ahmed I, Lobo DN. Malignant tumours of the liver. Surgery (Oxford). 2009;27(1):30–37. doi: 10.1016/j.mpsur.2008.12.005
   Google Scholar
• Turdean S, Gurzu S, Turcu M, et al. Current data in clinicopathological characteristics of primary hepatic tumors. Rom J Morphol Embryol. 2012;53(3 Suppl):719–724.
   PubMed Web of Science ®Google Scholar
• Bragazzi MC, Ridola L, Safarikia S, et al. New insights into cholangiocarcinoma: multiple stems and related cell lineages of origin. Ann Gastroenterol. 2018 Jan;31(1):42–55. doi: 10.20524/aog.2017.0209
   PubMed Web of Science ®Google Scholar
• Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2018 Nov;68(6):394–424. doi: 10.3322/caac.21492
   PubMed Web of Science ®Google Scholar
• Gomes MA, Priolli DG, Tralhao JG, et al. Hepatocellular carcinoma: epidemiology, biology, diagnosis, and therapies. Rev Assoc Med Bras. 2013;59(5):514–524. doi: 10.1016/j.ramb.2013.03.005
   PubMed Web of Science ®Google Scholar
• Pimenta JR, Massabki PS. Carcinoma hepatocelular: um panorama clínico. Rev Bras Clin Med. 2010;8:59–67.
   Google Scholar
• Hollebecque A, Malka D, Ferté C, et al. Systemic treatment of advanced hepatocellular carcinoma: from disillusions to new horizons. Eur J Cancer. 2015;51(3):327–339. doi: 10.1016/j.ejca.2014.12.005
   PubMed Web of Science ®Google Scholar
• Thrift AP, El-Serag HB, Kanwal F. Global epidemiology and burden of HCV infection and HCV-related disease. Nat Rev Gastroenterol Hepatol. 2017 Feb;14(2):122–132. doi: 10.1038/nrgastro.2016.176
   PubMed Web of Science ®Google Scholar
• Erstad DJ, Tanabe KK. Hepatocellular carcinoma: early-stage management challenges. J Hepatocell Carcinoma. 2017;4:81–92. doi: 10.2147/JHC.S107370
   PubMed Web of Science ®Google Scholar
• Ghouri YA, Mian I, Rowe JH. Review of hepatocellular carcinoma: epidemiology, etiology, and carcinogenesis. J Carcinog. 2017;16(1):1. doi: 10.4103/jcar.JCar_9_16
   PubMedGoogle Scholar
• Knudsen ES, Gopal P, Singal AG. The changing landscape of hepatocellular carcinoma: etiology, genetics, and therapy. Am J Pathol. 2014 Mar;184(3):574–583. doi: 10.1016/j.ajpath.2013.10.028
   PubMed Web of Science ®Google Scholar
• Brito AF, Abrantes AM, Tralhão JG, et al. Targeting hepatocellular carcinoma: what did we discover so far? Oncol Rev. 2016;10(2): doi: 10.4081/oncol.2016.302
   PubMedGoogle Scholar
• Llovet JM, Montal R, Sia D, et al. Molecular therapies and precision medicine for hepatocellular carcinoma. Nat Rev Clin Oncol. 2018 Oct;15(10):599–616. doi: 10.1038/s41571-018-0073-4
   PubMed Web of Science ®Google Scholar
• Mazzanti R, Arena U, Tassi R. Hepatocellular carcinoma: where are we? World J Exp Med. 2016;6(1):21. doi: 10.5493/wjem.v6.i1.21
   PubMedGoogle Scholar
• Gandhi S, Khubchandani S, Iyer R. Quality of life and hepatocellular carcinoma. J Gastrointest Oncol. 2014 Aug;5(4):296–317. doi: 10.3978/j.issn.2078-6891.2014.046
   PubMedGoogle Scholar
• Guo J, Li L, Guo B, et al. Mechanisms of resistance to chemotherapy and radiotherapy in hepatocellular carcinoma. Transl Cancer Res. 2018;7(3):765–781. doi: 10.21037/tcr.2018.05.20
   Web of Science ®Google Scholar
• Sangiovanni A, Manini MA, Iavarone M, et al. The diagnostic and economic impact of contrast imaging techniques in the diagnosis of small hepatocellular carcinoma in cirrhosis. Gut. 2010 May;59(5):638–644. doi: 10.1136/gut.2009.187286
   PubMed Web of Science ®Google Scholar
• Galle PR, Forner A, Llovet JM, et al. EASL clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2018 Jul;69(1):182–236. doi: 10.1016/j.jhep.2018.03.019
   PubMed Web of Science ®Google Scholar
• Durazo FA, Blatt LM, Corey WG, et al. Des-gamma-carboxyprothrombin, alpha-fetoprotein and AFP-L3 in patients with chronic hepatitis, cirrhosis and hepatocellular carcinoma. J Gastroenterol Hepatol. 2008 Oct;23(10):1541–1548. doi: 10.1111/j.1440-1746.2008.05395.x
   PubMed Web of Science ®Google Scholar
• Ye Q, Ling S, Zheng S, et al. Liquid biopsy in hepatocellular carcinoma: circulating tumor cells and circulating tumor DNA. Mol Cancer. 2019;18(1):114. doi: 10.1186/s12943-019-1043-x
   PubMed Web of Science ®Google Scholar
• Jafari D, Malih S, Eslami SS, et al. The relationship between molecular content of mesenchymal stem cells derived exosomes and their potentials: opening the way for exosomes based therapeutics. Biochimie. 2019 [2019 Oct 1];165:76–89.
   PubMed Web of Science ®Google Scholar
• Li X, Corbett AL, Taatizadeh E, et al. Challenges and opportunities in exosome research-perspectives from biology, engineering, and cancer therapy. APL Bioeng. 2019 Mar;3(1):011503. doi: 10.1063/1.5087122
   PubMed Web of Science ®Google Scholar
• Syn NL, Wang L, Chow EK, et al. Exosomes in cancer nanomedicine and immunotherapy: prospects and challenges. Trends Biotechnol. 2017 Jul;35(7):665–676. doi: 10.1016/j.tibtech.2017.03.004
   PubMed Web of Science ®Google Scholar
• Li X, Wang Y, Wang Q, et al. Exosomes in cancer: small transporters with big functions. Cancer Lett. 2018 Oct 28;435:55–65.
   PubMed Web of Science ®Google Scholar
• Chen R, Xu X, Tao Y, et al. Exosomes in hepatocellular carcinoma: a new horizon. Cell Commun Signal. 2019 Jan 7;17(1):1. doi: 10.1186/s12964-018-0315-1
   PubMedGoogle Scholar
• Xu H, Dong X, Chen Y, et al. Serum exosomal hnRNPH1 mRNA as a novel marker for hepatocellular carcinoma. Clin Chem Lab Med. 2018 Feb 23;56(3):479–484. doi: 10.1515/cclm-2017-0327
   PubMed Web of Science ®Google Scholar
• Wang H, Hou L, Li A, et al. Expression of serum exosomal microRNA-21 in human hepatocellular carcinoma. Biomed Res Int. 2014;2014:1–5. doi: 10.1155/2014/864894
   Web of Science ®Google Scholar
• Sohn W, Kim J, Kang SH, et al. Serum exosomal microRnas as novel biomarkers for hepatocellular carcinoma. Exp Mol Med. 2015 Sep 18;47(9):e184. doi: 10.1038/emm.2015.68
   PubMed Web of Science ®Google Scholar
• Liu W, Hu J, Zhou K, et al. Serum exosomal miR-125b is a novel prognostic marker for hepatocellular carcinoma. Onco Targets Ther. 2017;10:3843. doi: 10.2147/OTT.S140062
   PubMed Web of Science ®Google Scholar
• McInnes MDF, Moher D, Thombs BD, et al. Preferred reporting items for a systematic review and meta-analysis of diagnostic test accuracy studies the PRISMA-DTA statement. JAMA-J Am Med Assoc. 2018 Jan 23;319(4):388–396. doi: 10.1001/jama.2017.19163
   PubMed Web of Science ®Google Scholar
• Deeks JJ, Bossuyt PM, Leeflang MM, et al. Cochrane handbook for systematic reviews of diagnostic test accuracy. Wiley. Wiley Cochrane Series. 2023. p. 432. https://books.google.com/books?id=cL_HEAAAQBAJ.
   Google Scholar
• Harbord RM, Deeks JJ, Egger M, et al. A unification of models for meta-analysis of diagnostic accuracy studies. Biostatistics. 2007;8(2):239–251. doi: 10.1093/biostatistics/kxl004
   PubMed Web of Science ®Google Scholar
• Whiting PF, Rutjes AW, Westwood ME, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011 Oct 18;155(8):529–536. doi: 10.7326/0003-4819-155-8-201110180-00009
   PubMed Web of Science ®Google Scholar
• Dwamena B. MIDAS: stata module for meta-analytical integration of diagnostic test accuracy studies. Boston College Department of Economics; 2007. https://ideas.repec.org/c/boc/bocode/s456880.html
   Google Scholar
• Zhou Y, Dendukuri N. Statistics for quantifying heterogeneity in univariate and bivariate meta‐analyses of binary data: the case of meta‐analyses of diagnostic accuracy. Stat Med. 2014;33(16):2701–2717. doi: 10.1002/sim.6115
   PubMed Web of Science ®Google Scholar
• Deeks JJ, Macaskill P, Irwig L. The performance of tests of publication bias and other sample size effects in systematic reviews of diagnostic test accuracy was assessed. J Clin Epidemiol. 2005 Sep;58(9):882–893. doi: 10.1016/j.jclinepi.2005.01.016
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhang C, Zhang P, et al. Serum exosomal micro RNA s combined with alpha‐fetoprotein as diagnostic markers of hepatocellular carcinoma. Cancer Med. 2018;7(5):1670–1679. doi: 10.1002/cam4.1390
   PubMed Web of Science ®Google Scholar
• Xu H, Chen Y, Dong X, et al. Serum exosomal long noncoding RNAs ENSG00000258332. 1 and LINC00635 for the diagnosis and prognosis of hepatocellular carcinoma. Cancer Epidemiol Biomarkers Prev. 2018;27(6):710–716. doi: 10.1158/1055-9965.EPI-17-0770
   PubMed Web of Science ®Google Scholar
• Sun L, Xu M, Zhang G, et al. Identification of circulating exosomal miR-101 and miR-125b panel act as a potential biomarker for hepatocellular carcinoma. Int J Genomics. 2021;2021:1326463. doi: 10.1155/2021/1326463
   PubMed Web of Science ®Google Scholar
• El Gwad A A, Matboli M, El-Tawdi A, et al. Role of exosomal competing endogenous RNA in patients with hepatocellular carcinoma. J Cell Biochem. 2018 Nov;119(10):8600–8610. doi: 10.1002/jcb.27109
   PubMed Web of Science ®Google Scholar
• Chen S, Mao Y, Chen W, et al. Serum exosomal miR-34a as a potential biomarker for the diagnosis and prognostic of hepatocellular carcinoma. J Cancer. 2022;13(5):1410–1417. doi: 10.7150/jca.57205
   PubMed Web of Science ®Google Scholar
• Cho HJ, Baek GO, Seo CW, et al. Exosomal microRNA-4661-5p-based serum panel as a potential diagnostic biomarker for early-stage hepatocellular carcinoma. Cancer Med. 2020 Aug;9(15):5459–5472. doi: 10.1002/cam4.3230
   PubMed Web of Science ®Google Scholar
• Cho HJ, Eun JW, Baek GO, et al. Serum exosomal MicroRNA, miR-10b-5p, as a potential diagnostic biomarker for early-stage hepatocellular carcinoma. J Clin Med. 2020 Jan 20;9(1):281. doi: 10.3390/jcm9010281
   PubMed Web of Science ®Google Scholar
• Elghoroury EA, Abdelghaffar EE, Awadallah E, et al. Detection of exosomal miR-18a and miR-222 levels in Egyptian patients with hepatic cirrhosis and hepatocellular carcinoma. Int J Immunopathol Pharmacol. 2022 Jan;36:3946320221097832.
   Web of Science ®Google Scholar
• Fründt T, Krause L, Hussey E, et al. Diagnostic and prognostic value of miR-16, miR-146a, miR-192 and miR-221 in exosomes of hepatocellular carcinoma and liver cirrhosis patients. Cancers (Basel). 2021 May 19;13(10):2484. doi: 10.3390/cancers13102484
   PubMed Web of Science ®Google Scholar
• Guo S, Hu C, Zhai X, et al. Circular RNA 0006602 in plasma exosomes: a new potential diagnostic biomarker for hepatocellular carcinoma. Am J Transl Res. 2021;13(6):6001–6015.
   PubMed Web of Science ®Google Scholar
• Kim SS, Baek GO, Ahn HR, et al. Serum small extracellular vesicle-derived LINC00853 as a novel diagnostic marker for early hepatocellular carcinoma. Mol Oncol. 2020 Oct;14(10):2646–2659. doi: 10.1002/1878-0261.12745
   PubMed Web of Science ®Google Scholar
• Kim SS, Baek GO, Son JA, et al. Early detection of hepatocellular carcinoma via liquid biopsy: panel of small extracellular vesicle-derived long noncoding RNAs identified as markers. Mol Oncol. 2021 Oct;15(10):2715–2731. doi: 10.1002/1878-0261.13049
   PubMed Web of Science ®Google Scholar
• Matboli M, Labib ME, Nasser HE, et al. Exosomal miR-1298 and lncRNA-RP11-583F2.2 expression in Hepato-cellular carcinoma. Curr Genomics. 2020 Jan;21(1):46–55. doi: 10.2174/1389202920666191210111849
   PubMed Web of Science ®Google Scholar
• Wang S, Yang Y, Sun L, et al. Exosomal MicroRNAs as liquid biopsy biomarkers in hepatocellular carcinoma. Onco Targets Ther. 2020;13: 2021–2030. 10.2147/OTT.S232453.
   PubMed Web of Science ®Google Scholar
• Wang Y, Pei L, Yue Z, et al. The potential of Serum exosomal hsa_circ_0028861 as the novel diagnostic biomarker of HBV-Derived hepatocellular cancer. Front Genet. 2021;12:703205. doi: 10.3389/fgene.2021.703205
   PubMed Web of Science ®Google Scholar
• Yang J, Dong W, Zhang H, et al. Exosomal microRNA panel as a diagnostic biomarker in patients with hepatocellular carcinoma. Front Cell Dev Biol. 2022;10:927251. doi: 10.3389/fcell.2022.927251
   PubMed Web of Science ®Google Scholar
• Wei Y, Zhang Q, An L, et al. Serum exosomal microRNA-370-3p and microRNA-196a-5p are potential biomarkers for the diagnosis and prognosis of hepatocellular carcinoma. Folia Histochem Cytobiol. 2022;60(3):215–225. doi: 10.5603/FHC.a2022.0019
   PubMed Web of Science ®Google Scholar
• Sharma A, Dulta K, Nagraik R, et al. Potentialities of aptasensors in cancer diagnosis. Mater Lett. 2022;308:131240. doi: 10.1016/j.matlet.2021.131240
   Web of Science ®Google Scholar
• Villanueva A, Longo DL. Hepatocellular carcinoma. N Engl J Med. 2019;380(15):1450–1462. doi: 10.1056/NEJMra1713263
   PubMed Web of Science ®Google Scholar
• Balogh J, Victor ID, Asham EH, et al. Hepatocellular carcinoma: a review. J Hepatocell Carcinoma. 2016;3:41. doi: 10.2147/JHC.S61146
   PubMed Web of Science ®Google Scholar
• Zucman-Rossi J, Villanueva A, Nault J-C, et al. Genetic landscape and biomarkers of hepatocellular carcinoma. Gastroenterology. 2015;149(5):1226–1239. e4. doi: 10.1053/j.gastro.2015.05.061
   PubMed Web of Science ®Google Scholar
• Li R, Wang Y, Zhang X, et al. Exosome-mediated secretion of LOXL4 promotes hepatocellular carcinoma cell invasion and metastasis. Mol Cancer. 2019;18(1):1–19. doi: 10.1186/s12943-019-0948-8
   PubMedGoogle Scholar
• Lv LH, Wan YL, Lin Y, et al. Anticancer drugs cause release of exosomes with heat shock proteins from human hepatocellular carcinoma cells that elicit effective natural killer cell antitumor responses in vitro. J Biol Chem. 2012 May 4;287(19):15874–15885. doi: 10.1074/jbc.M112.340588
   PubMed Web of Science ®Google Scholar
• Ye L, Zhang Q, Cheng Y, et al. Tumor-derived exosomal HMGB1 fosters hepatocellular carcinoma immune evasion by promoting TIM-1(+) regulatory B cell expansion. J Immunother Cancer. 2018 Dec 10;6(1):145. doi: 10.1186/s40425-018-0451-6
   PubMed Web of Science ®Google Scholar
• Ferrín G, Ranchal I, Llamoza C, et al. Identification of candidate biomarkers for hepatocellular carcinoma in plasma of HCV-infected cirrhotic patients by 2-D DIGE. Liver Int. 2014 Mar;34(3):438–446. doi: 10.1111/liv.12277
   PubMed Web of Science ®Google Scholar
• Lee YR, Kim G, Tak WY, et al. Circulating exosomal noncoding RNAs as prognostic biomarkers in human hepatocellular carcinoma. Int J Cancer. 2019;144(6):1444–1452. doi: 10.1002/ijc.31931
   PubMed Web of Science ®Google Scholar
• Suehiro T, Miyaaki H, Kanda Y, et al. Serum exosomal microRNA‑122 and microRNA‑21 as predictive biomarkers in transarterial chemoembolization‑treated hepatocellular carcinoma patients. Oncol Lett. 2018;16(3):3267–3273. doi: 10.3892/ol.2018.8991
   PubMed Web of Science ®Google Scholar
• Villanueva A, Minguez B, Forner A, et al. Hepatocellular carcinoma: novel molecular approaches for diagnosis, prognosis and therapy. Annu Rev Med. 2010;61(1):317. doi: 10.1146/annurev.med.080608.100623
   PubMedGoogle Scholar
• Sukreet S, Silva BVRE, Adamec J, et al. Sonication and short-term incubation alter the content of Bovine milk exosome cargos and exosome bioavailability (OR26-08-19). Curr Dev Nutr. 2019;3(Supplement_1):nzz033.OR26-08–19. doi: 10.1093/cdn/nzz033.OR26-08-19
   Google Scholar
• Kanchanapally R, Deshmukh SK, Chavva SR, et al. Drug-loaded exosomal preparations from different cell types exhibit distinctive loading capability, yield, and antitumor efficacies: a comparative analysis. Int J Nanomedicine. 2019;14:531–541. doi: 10.2147/IJN.S191313
   PubMed Web of Science ®Google Scholar
• Tang YT, Huang YY, Zheng L, et al. Comparison of isolation methods of exosomes and exosomal RNA from cell culture medium and serum. Int J Mol Med. 2017 Sep;40(3):834–844. doi: 10.3892/ijmm.2017.3080
   PubMed Web of Science ®Google Scholar
• Van Deun J, Mestdagh P, Sormunen R, et al. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J Extracell Vesicles. 2014;3(1):24858. doi: 10.3402/jev.v3.24858
   PubMedGoogle Scholar
• Taylor DD, Shah S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods. 2015 Oct 1;87:3–10. doi: 10.1016/j.ymeth.2015.02.019
   PubMed Web of Science ®Google Scholar
• Zarovni N, Corrado A, Guazzi P, et al. Integrated isolation and quantitative analysis of exosome shuttled proteins and nucleic acids using immunocapture approaches. Methods. 2015;87:46–58. doi: 10.1016/j.ymeth.2015.05.028
   PubMed Web of Science ®Google Scholar
• Stranska R, Gysbrechts L, Wouters J, et al. Comparison of membrane affinity-based method with size-exclusion chromatography for isolation of exosome-like vesicles from human plasma. J Transl Med. 2018 Jan 9;16(1):1. doi: 10.1186/s12967-017-1374-6
   PubMed Web of Science ®Google Scholar
• Rekker K, Saare M, Roost AM, et al. Comparison of serum exosome isolation methods for microRNA profiling. Clin Biochem. 2014;47(1–2):135–138. doi: 10.1016/j.clinbiochem.2013.10.020
   PubMed Web of Science ®Google Scholar
• Tauro BJ, Greening DW, Mathias RA, et al. Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods. 2012 Feb;56(2):293–304. doi: 10.1016/j.ymeth.2012.01.002
   PubMed Web of Science ®Google Scholar
• Chen J, Parkin D, Chen Q, et al. Screening for liver cancer: results of a randomised controlled trial in Qidong, China. J Med Screen. 2003;10(4):204–209. doi: 10.1258/096914103771773320
   PubMed Web of Science ®Google Scholar
• Di Bisceglie AM, Sterling RK, Chung RT, et al. Serum alpha-fetoprotein levels in patients with advanced hepatitis C: results from the HALT-C trial. J Hepatol. 2005;43(3):434–441. doi: 10.1016/j.jhep.2005.03.019
   PubMed Web of Science ®Google Scholar
• Soreide O, Czemiak A, Bradpiece H, et al. Characteristics of fibrolamellar hepatocellular carcinoma: a study of nine cases and a review of the literature. Am J Surg. 1986;151(4):518–523. doi: 10.1016/0002-9610(86)90117-0
   PubMed Web of Science ®Google Scholar
• Chen D-S, Sung J-L, Shed J-C, et al. Serum α-fetoprotein in the early stage of human hepatocellular carcinoma. Gastroenterology. 1984;86(6):1404–1409. doi: 10.1016/S0016-5085(84)80151-1
   PubMed Web of Science ®Google Scholar
• Glas AS, Lijmer JG, Prins MH, et al. The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol. 2003 Nov;56(11):1129–1135. doi: 10.1016/S0895-4356(03)00177-X
   PubMed Web of Science ®Google Scholar
• Jones CM, Athanasiou T. Summary receiver operating characteristic curve analysis techniques in the evaluation of diagnostic tests.Ann Thorac Surg. 2005 Jan 1;79(1):16–20. doi: 10.1016/j.athoracsur.2004.09.040
   PubMed Web of Science ®Google Scholar
• Wu Z, Xu Z, Yu B, et al. The potential diagnostic value of exosomal long noncoding RNAs in solid tumors: a meta-analysis and systematic review. Biomed Res Int. 2020;2020: 6786875. doi: 10.1155/2020/6786875
   PubMed Web of Science ®Google Scholar