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Published in: Tumor Biology 11/2014

01-11-2014 | Research Article

Identification of microRNAs as novel biomarkers for detecting esophageal squamous cell carcinoma in Asians: a meta-analysis

Authors: Yanying Wang, Qingxiu Wang, Na Zhang, Hong Ma, Yuchun Gu, Hongming Tang, Zengguang Xu, Yong Gao

Published in: Tumor Biology | Issue 11/2014

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Abstract

Accumulating evidence has suggested that microRNAs (miRNAs) may play potential role as ideal diagnostic indicators of esophageal squamous cell carcinoma (ESCC). However, previous studies have met discrepant results. Thus, we conducted this meta-analysis to assess the potential diagnostic value of miRNAs for ESCC. A systematic literature search was conducted in PubMed and other databases. The pooled sensitivity (SEN), specificity (SPE), positive likelihood ratio (PLR), negative likelihood ratio (NLR), diagnostic odds ratio (DOR), and area under the curve (AUC) were calculated to evaluate the overall test performance. The Q statistic and the I 2 test were used to assess between-study heterogeneity. The potential sources of heterogeneity were further analyzed by subgroup analyses and meta-regression. Seventeen studies from eight articles, including 995 ESCC patients and 733 healthy controls, were included in this meta-analysis. The pooled SEN and SPE were 0.81 (95 % confidence interval (CI) 0.76–0.85) and 0.83 (95 % CI 0.76–0.88), respectively. The pooled PLR was 4.6 (95 % CI 3.3–6.5), NLR was 0.23 (95 % CI 0.19–0.29), and DOR was 20 (95 % CI 13–31). The pooled AUC was 0.91 (95 % CI 0.88–0.93). Subgroup analyses indicated that blood-based miRNA assay displays better diagnostic accuracy than saliva-based miRNA assay. In summary, miRNA analysis may serve as novel noninvasive biomarkers for ESCC with excellent diagnostic characteristic. In addition, subgroup analysis suggested that blood-based assay yields better diagnostic characteristics than saliva-based assay. However, many issues should be managed before these findings can be translated into a clinically useful detection method for ESCC.
Literature
2.
go back to reference Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMedCrossRef Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.PubMedCrossRef
3.
go back to reference Hiyama T, Yoshihara M, Tanaka S, Chayama K. Genetic polymorphisms and esophageal cancer risk. Int J Cancer. 2007;121:1643–58.PubMedCrossRef Hiyama T, Yoshihara M, Tanaka S, Chayama K. Genetic polymorphisms and esophageal cancer risk. Int J Cancer. 2007;121:1643–58.PubMedCrossRef
4.
go back to reference Urba SG, Orringer MB, Turrisi A, Iannettoni M, Forastiere A, Strawderman M. Randomized trial of preoperative chemoradiation versus surgery alone in patients with locoregional esophageal carcinoma. J Clin Oncol. 2001;19:305–13.PubMed Urba SG, Orringer MB, Turrisi A, Iannettoni M, Forastiere A, Strawderman M. Randomized trial of preoperative chemoradiation versus surgery alone in patients with locoregional esophageal carcinoma. J Clin Oncol. 2001;19:305–13.PubMed
5.
go back to reference Kim T, Grobmyer SR, Smith R, Ben-David K, Ang D, Vogel SB, et al. Esophageal cancer—the five year survivors. J Surg Oncol. 2011;103:179–83.PubMedCrossRef Kim T, Grobmyer SR, Smith R, Ben-David K, Ang D, Vogel SB, et al. Esophageal cancer—the five year survivors. J Surg Oncol. 2011;103:179–83.PubMedCrossRef
6.
go back to reference Daly JM, Fry WA, Little AG, Winchester DP, McKee RF, Stewart AK, et al. Esophageal cancer: results of an American College of Surgeons Patient Care Evaluation Study. J Am Coll Surg. 2000;190:562–72. discussion 72-3.PubMedCrossRef Daly JM, Fry WA, Little AG, Winchester DP, McKee RF, Stewart AK, et al. Esophageal cancer: results of an American College of Surgeons Patient Care Evaluation Study. J Am Coll Surg. 2000;190:562–72. discussion 72-3.PubMedCrossRef
7.
go back to reference Barber TW, Duong CP, Leong T, Bressel M, Drummond EG, Hicks RJ. 18F-FDG PET/CT has a high impact on patient management and provides powerful prognostic stratification in the primary staging of esophageal cancer: a prospective study with mature survival data. J Nucl Med. 2012;53:864–71.PubMedCrossRef Barber TW, Duong CP, Leong T, Bressel M, Drummond EG, Hicks RJ. 18F-FDG PET/CT has a high impact on patient management and provides powerful prognostic stratification in the primary staging of esophageal cancer: a prospective study with mature survival data. J Nucl Med. 2012;53:864–71.PubMedCrossRef
8.
go back to reference Tachimori Y, Kanamori N, Uemura N, Hokamura N, Igaki H, Kato H. Salvage esophagectomy after high-dose chemoradiotherapy for esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg. 2009;137:49–54.PubMedCrossRef Tachimori Y, Kanamori N, Uemura N, Hokamura N, Igaki H, Kato H. Salvage esophagectomy after high-dose chemoradiotherapy for esophageal squamous cell carcinoma. J Thorac Cardiovasc Surg. 2009;137:49–54.PubMedCrossRef
9.
go back to reference Takeshita N, Hoshino I, Mori M, Akutsu Y, Hanari N, Yoneyama Y, et al. Serum microRNA expression profile: miR-1246 as a novel diagnostic and prognostic biomarker for oesophageal squamous cell carcinoma. Br J Cancer. 2013;108:644–52.PubMedCentralPubMedCrossRef Takeshita N, Hoshino I, Mori M, Akutsu Y, Hanari N, Yoneyama Y, et al. Serum microRNA expression profile: miR-1246 as a novel diagnostic and prognostic biomarker for oesophageal squamous cell carcinoma. Br J Cancer. 2013;108:644–52.PubMedCentralPubMedCrossRef
10.
go back to reference Xie Z, Chen G, Zhang X, Li D, Huang J, Yang C, et al. Salivary microRNAs as promising biomarkers for detection of esophageal cancer. PLoS One. 2013;8:e57502.PubMedCentralPubMedCrossRef Xie Z, Chen G, Zhang X, Li D, Huang J, Yang C, et al. Salivary microRNAs as promising biomarkers for detection of esophageal cancer. PLoS One. 2013;8:e57502.PubMedCentralPubMedCrossRef
11.
go back to reference Zhang T, Wang Q, Zhao D, Cui Y, Cao B, Guo L, et al. The oncogenetic role of microRNA-31 as a potential biomarker in oesophageal squamous cell carcinoma. Clin Sci (Lond). 2011;121:437–47.CrossRef Zhang T, Wang Q, Zhao D, Cui Y, Cao B, Guo L, et al. The oncogenetic role of microRNA-31 as a potential biomarker in oesophageal squamous cell carcinoma. Clin Sci (Lond). 2011;121:437–47.CrossRef
13.
go back to reference Visone R, Pallante P, Vecchione A, Cirombella R, Ferracin M, Ferraro A, et al. Specific microRNAs are downregulated in human thyroid anaplastic carcinomas. Oncogene. 2007;26:7590–5.PubMedCrossRef Visone R, Pallante P, Vecchione A, Cirombella R, Ferracin M, Ferraro A, et al. Specific microRNAs are downregulated in human thyroid anaplastic carcinomas. Oncogene. 2007;26:7590–5.PubMedCrossRef
16.
go back to reference Wilmott JS, Zhang XD, Hersey P, Scolyer RA. The emerging important role of microRNAs in the pathogenesis, diagnosis and treatment of human cancers. Pathology. 2011;43:657–71.PubMed Wilmott JS, Zhang XD, Hersey P, Scolyer RA. The emerging important role of microRNAs in the pathogenesis, diagnosis and treatment of human cancers. Pathology. 2011;43:657–71.PubMed
17.
go back to reference Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH, Lee MJ, et al. The microRNA spectrum in 12 body fluids. Clin Chem. 2010;56:1733–41.PubMedCrossRef Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH, Lee MJ, et al. The microRNA spectrum in 12 body fluids. Clin Chem. 2010;56:1733–41.PubMedCrossRef
18.
go back to reference Park NJ, Zhou H, Elashoff D, Henson BS, Kastratovic DA, Abemayor E, et al. Salivary microRNA: discovery, characterization, and clinical utility for oral cancer detection. Clin Cancer Res. 2009;15:5473–7.PubMedCentralPubMedCrossRef Park NJ, Zhou H, Elashoff D, Henson BS, Kastratovic DA, Abemayor E, et al. Salivary microRNA: discovery, characterization, and clinical utility for oral cancer detection. Clin Cancer Res. 2009;15:5473–7.PubMedCentralPubMedCrossRef
19.
go back to reference Hirajima S, Komatsu S, Ichikawa D, Takeshita H, Konishi H, Shiozaki A, et al. Clinical impact of circulating miR-18a in plasma of patients with oesophageal squamous cell carcinoma. Br J Cancer. 2013;108:1822–9.PubMedCentralPubMedCrossRef Hirajima S, Komatsu S, Ichikawa D, Takeshita H, Konishi H, Shiozaki A, et al. Clinical impact of circulating miR-18a in plasma of patients with oesophageal squamous cell carcinoma. Br J Cancer. 2013;108:1822–9.PubMedCentralPubMedCrossRef
20.
go back to reference Zhang C, Wang C, Chen X, Yang C, Li K, Wang J, et al. Expression profile of microRNAs in serum: a fingerprint for esophageal squamous cell carcinoma. Clin Chem. 2010;56:1871–9.PubMedCrossRef Zhang C, Wang C, Chen X, Yang C, Li K, Wang J, et al. Expression profile of microRNAs in serum: a fingerprint for esophageal squamous cell carcinoma. Clin Chem. 2010;56:1871–9.PubMedCrossRef
21.
go back to reference Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155:529–36.PubMedCrossRef Whiting PF, Rutjes AW, Westwood ME, Mallett S, Deeks JJ, Reitsma JB, et al. QUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studies. Ann Intern Med. 2011;155:529–36.PubMedCrossRef
22.
go back to reference Mitchell AJ, Vaze A, Rao S. Clinical diagnosis of depression in primary care: a meta-analysis. Lancet. 2009;374:609–19.PubMedCrossRef Mitchell AJ, Vaze A, Rao S. Clinical diagnosis of depression in primary care: a meta-analysis. Lancet. 2009;374:609–19.PubMedCrossRef
23.
go back to reference Harbord RM, Deeks JJ, Egger M, Whiting P, Sterne JA. A unification of models for meta-analysis of diagnostic accuracy studies. Biostatistics. 2007;8:239–51.PubMedCrossRef Harbord RM, Deeks JJ, Egger M, Whiting P, Sterne JA. A unification of models for meta-analysis of diagnostic accuracy studies. Biostatistics. 2007;8:239–51.PubMedCrossRef
24.
go back to reference Dinnes J, Deeks J, Kirby J, Roderick P. A methodological review of how heterogeneity has been examined in systematic reviews of diagnostic test accuracy. Health Technol Assess. 2005;9:1–113. iii. Dinnes J, Deeks J, Kirby J, Roderick P. A methodological review of how heterogeneity has been examined in systematic reviews of diagnostic test accuracy. Health Technol Assess. 2005;9:1–113. iii.
26.
go back to reference 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;58:882–93.PubMedCrossRef 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;58:882–93.PubMedCrossRef
27.
go back to reference Komatsu S, Ichikawa D, Takeshita H, Tsujiura M, Morimura R, Nagata H, et al. Circulating microRNAs in plasma of patients with oesophageal squamous cell carcinoma. Br J Cancer. 2011;105:104–11.PubMedCentralPubMedCrossRef Komatsu S, Ichikawa D, Takeshita H, Tsujiura M, Morimura R, Nagata H, et al. Circulating microRNAs in plasma of patients with oesophageal squamous cell carcinoma. Br J Cancer. 2011;105:104–11.PubMedCentralPubMedCrossRef
28.
go back to reference Wu W, Hou W, Wu Z, Wang Y, Yi Y. Lin W [miRNA-144 in the saliva is a genetic marker for early diagnosis of esophageal cancer]. Nan Fang Yi Ke Da Xue Xue Bao. 2013;33:1783–6.PubMed Wu W, Hou W, Wu Z, Wang Y, Yi Y. Lin W [miRNA-144 in the saliva is a genetic marker for early diagnosis of esophageal cancer]. Nan Fang Yi Ke Da Xue Xue Bao. 2013;33:1783–6.PubMed
29.
go back to reference Zhang T, Zhao D, Wang Q, Yu X, Cui Y, Guo L, et al. MicroRNA-1322 regulates ECRG2 allele specifically and acts as a potential biomarker in patients with esophageal squamous cell carcinoma. Mol Carcinog. 2013;52:581–90.PubMedCrossRef Zhang T, Zhao D, Wang Q, Yu X, Cui Y, Guo L, et al. MicroRNA-1322 regulates ECRG2 allele specifically and acts as a potential biomarker in patients with esophageal squamous cell carcinoma. Mol Carcinog. 2013;52:581–90.PubMedCrossRef
30.
go back to reference Holmes RS, Vaughan TL. Epidemiology and pathogenesis of esophageal cancer. Semin Radiat Oncol. 2007;17:2–9.PubMedCrossRef Holmes RS, Vaughan TL. Epidemiology and pathogenesis of esophageal cancer. Semin Radiat Oncol. 2007;17:2–9.PubMedCrossRef
31.
go back to reference Chen J, Pan J, Zheng X, Zhu K, Li J, Chen M, et al. Number and location of positive nodes, postoperative radiotherapy, and survival after esophagectomy with three-field lymph node dissection for thoracic esophageal squamous cell carcinoma. Int J Radiat Oncol Biol Phys. 2012;82:475–82.PubMedCrossRef Chen J, Pan J, Zheng X, Zhu K, Li J, Chen M, et al. Number and location of positive nodes, postoperative radiotherapy, and survival after esophagectomy with three-field lymph node dissection for thoracic esophageal squamous cell carcinoma. Int J Radiat Oncol Biol Phys. 2012;82:475–82.PubMedCrossRef
32.
go back to reference Yuequan J, Shifeng C, Bing Z. Prognostic factors and family history for survival of esophageal squamous cell carcinoma patients after surgery. Ann Thorac Surg. 2010;90:908–13.PubMedCrossRef Yuequan J, Shifeng C, Bing Z. Prognostic factors and family history for survival of esophageal squamous cell carcinoma patients after surgery. Ann Thorac Surg. 2010;90:908–13.PubMedCrossRef
33.
go back to reference Kelsen DP, Ginsberg R, Pajak TF, Sheahan DG, Gunderson L, Mortimer J, et al. Chemotherapy followed by surgery compared with surgery alone for localized esophageal cancer. N Engl J Med. 1998;339:1979–84.PubMedCrossRef Kelsen DP, Ginsberg R, Pajak TF, Sheahan DG, Gunderson L, Mortimer J, et al. Chemotherapy followed by surgery compared with surgery alone for localized esophageal cancer. N Engl J Med. 1998;339:1979–84.PubMedCrossRef
34.
go back to reference Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008;18:997–1006.PubMedCrossRef Chen X, Ba Y, Ma L, Cai X, Yin Y, Wang K, et al. Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008;18:997–1006.PubMedCrossRef
35.
go back to reference Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A. 2008;105:10513–8.PubMedCentralPubMedCrossRef Mitchell PS, Parkin RK, Kroh EM, Fritz BR, Wyman SK, Pogosova-Agadjanyan EL, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A. 2008;105:10513–8.PubMedCentralPubMedCrossRef
36.
go back to reference Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470–6.PubMedCentralPubMedCrossRef Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470–6.PubMedCentralPubMedCrossRef
37.
go back to reference Morimura R, Komatsu S, Ichikawa D, Takeshita H, Tsujiura M, Nagata H, et al. Novel diagnostic value of circulating miR-18a in plasma of patients with pancreatic cancer. Br J Cancer. 2011;105:1733–40.PubMedCentralPubMedCrossRef Morimura R, Komatsu S, Ichikawa D, Takeshita H, Tsujiura M, Nagata H, et al. Novel diagnostic value of circulating miR-18a in plasma of patients with pancreatic cancer. Br J Cancer. 2011;105:1733–40.PubMedCentralPubMedCrossRef
38.
go back to reference Piepoli A, Tavano F, Copetti M, Mazza T, Palumbo O, Panza A, et al. Mirna expression profiles identify drivers in colorectal and pancreatic cancers. PLoS One. 2012;7:e33663.PubMedCentralPubMedCrossRef Piepoli A, Tavano F, Copetti M, Mazza T, Palumbo O, Panza A, et al. Mirna expression profiles identify drivers in colorectal and pancreatic cancers. PLoS One. 2012;7:e33663.PubMedCentralPubMedCrossRef
39.
go back to reference Smith CM, Watson DI, Michael MZ, Hussey DJ. MicroRNAs, development of Barrett’s esophagus, and progression to esophageal adenocarcinoma. World J Gastroenterol. 2010;16:531–7.PubMedCentralPubMedCrossRef Smith CM, Watson DI, Michael MZ, Hussey DJ. MicroRNAs, development of Barrett’s esophagus, and progression to esophageal adenocarcinoma. World J Gastroenterol. 2010;16:531–7.PubMedCentralPubMedCrossRef
40.
go back to reference Hummel R, Hussey DJ, Haier J. MicroRNAs: predictors and modifiers of chemo- and radiotherapy in different tumour types. Eur J Cancer. 2010;46:298–311.PubMedCrossRef Hummel R, Hussey DJ, Haier J. MicroRNAs: predictors and modifiers of chemo- and radiotherapy in different tumour types. Eur J Cancer. 2010;46:298–311.PubMedCrossRef
41.
go back to reference Lajer CB, Nielsen FC, Friis-Hansen L, Norrild B, Borup R, Garnaes E, et al. Different miRNA signatures of oral and pharyngeal squamous cell carcinomas: a prospective translational study. Br J Cancer. 2011;104:830–40.PubMedCentralPubMedCrossRef Lajer CB, Nielsen FC, Friis-Hansen L, Norrild B, Borup R, Garnaes E, et al. Different miRNA signatures of oral and pharyngeal squamous cell carcinomas: a prospective translational study. Br J Cancer. 2011;104:830–40.PubMedCentralPubMedCrossRef
42.
go back to reference Liu X, Sempere LF, Ouyang H, Memoli VA, Andrew AS, Luo Y, et al. MicroRNA-31 functions as an oncogenic microRNA in mouse and human lung cancer cells by repressing specific tumor suppressors. J Clin Invest. 2010;120:1298–309.PubMedCentralPubMedCrossRef Liu X, Sempere LF, Ouyang H, Memoli VA, Andrew AS, Luo Y, et al. MicroRNA-31 functions as an oncogenic microRNA in mouse and human lung cancer cells by repressing specific tumor suppressors. J Clin Invest. 2010;120:1298–309.PubMedCentralPubMedCrossRef
43.
go back to reference Wang HT, Liu ZH, Wang XQ. Wu M [Effect of EMP-1 gene on human esophageal cancer cell line]. Ai Zheng. 2002;21:229–32.PubMed Wang HT, Liu ZH, Wang XQ. Wu M [Effect of EMP-1 gene on human esophageal cancer cell line]. Ai Zheng. 2002;21:229–32.PubMed
44.
go back to reference Zinovyeva MV, Monastyrskaya GS, Kopantzev EP, Vinogradova TV, Kostina MB, Sass AV, et al. Identification of some human genes oppositely regulated during esophageal squamous cell carcinoma formation and human embryonic esophagus development. Dis Esophagus. 2010;23:260–70.PubMedCrossRef Zinovyeva MV, Monastyrskaya GS, Kopantzev EP, Vinogradova TV, Kostina MB, Sass AV, et al. Identification of some human genes oppositely regulated during esophageal squamous cell carcinoma formation and human embryonic esophagus development. Dis Esophagus. 2010;23:260–70.PubMedCrossRef
Metadata
Title
Identification of microRNAs as novel biomarkers for detecting esophageal squamous cell carcinoma in Asians: a meta-analysis
Authors
Yanying Wang
Qingxiu Wang
Na Zhang
Hong Ma
Yuchun Gu
Hongming Tang
Zengguang Xu
Yong Gao
Publication date
01-11-2014
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 11/2014
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-014-2350-x

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