Skip to main content
Top
Published in: Tumor Biology 5/2013

01-10-2013 | Research Article

Prognostic significance of VEGF immunohistochemical expression in oral cancer: a meta-analysis of the literature

Authors: Su-Feng Zhao, Xu-Dong Yang, Ming-Xing Lu, Guo-Wen Sun, Yu-Xin Wang, Yin-Kai Zhang, Yu-Mei Pu, En-Yi Tang

Published in: Tumor Biology | Issue 5/2013

Login to get access

Abstract

Vascular endothelial growth factor (VEGF) is considered as a prime mediator of angiogenesis and has been implicated in carcinogenesis and metastasis. Various studies examined the relationship between VEGF protein overexpression with the clinical outcome in patients with oral cancer, but yielded conflicting results. Electronic databases updated to March 2013 were searched to find relevant studies. A meta-analysis was conducted with eligible studies which quantitatively evaluated the relationship between VEGF overexpression and survival of patients with oral cancer. Survival data were aggregated and quantitatively analyzed. We performed a meta-analysis of 17 studies (n = 1,207 patients) that evaluated the correlation between VEGF overexpression detected by immunohistochemistry and survival in patients with oral cancer. Combined hazard ratios suggested that VEGF overexpression had an unfavorable impact on overall survival (hazard ratio [HR] = 1.89; 95 % confidence interval [CI], 1.24–2.55) and disease-free survival (HR = 2.08; 95 % CI, 1.14–3.02) in patients with oral cancer: 1.77 (1.09–1.44) in oral squamous cell carcinoma (SCC) patients and 4.28 (1.35–7.21) in adenoid cystic carcinoma (ACC) and mucoepidermoid carcinoma (MEC) of the salivary glands. No significant heterogeneity was observed among all studies. VEGF overexpression indicates a poor prognosis for patients with oral SCC, ACC, and MEC of the salivary glands.
Literature
1.
go back to reference Zygog ianni AG, Kyrgias G, Karak itsos P, et al. Oral squamous cell cancer: early detection and the role of alcohol and smoking. Head Neck Oncol. 2011;3:2.CrossRef Zygog ianni AG, Kyrgias G, Karak itsos P, et al. Oral squamous cell cancer: early detection and the role of alcohol and smoking. Head Neck Oncol. 2011;3:2.CrossRef
2.
go back to reference Reichart PA, Nguyen XH. Betel quid chewing, oral cancer and other oral mucosal diseases in Vietnam: a review. J Oral Pathol Med. 2008;37:511–4.CrossRefPubMed Reichart PA, Nguyen XH. Betel quid chewing, oral cancer and other oral mucosal diseases in Vietnam: a review. J Oral Pathol Med. 2008;37:511–4.CrossRefPubMed
3.
go back to reference Eveson JW, Cawson RA. Salivary gland tumors. A review of 2410 cases with particular reference to histological types, site, age and sex distribution. J Pathol. 1985;146:51–8.CrossRefPubMed Eveson JW, Cawson RA. Salivary gland tumors. A review of 2410 cases with particular reference to histological types, site, age and sex distribution. J Pathol. 1985;146:51–8.CrossRefPubMed
4.
5.
go back to reference Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol. 2005;23:1011–27.CrossRefPubMed Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol. 2005;23:1011–27.CrossRefPubMed
7.
go back to reference Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med. 1998;17:2815–34.CrossRefPubMed Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med. 1998;17:2815–34.CrossRefPubMed
8.
go back to reference Yusuf S, Peto R, Lewis J, et al. Blockade during and after myocardial infarction: an overview of the randomized trials. Prog Cardiovasc Dis. 1985;27:335–71.CrossRefPubMed Yusuf S, Peto R, Lewis J, et al. Blockade during and after myocardial infarction: an overview of the randomized trials. Prog Cardiovasc Dis. 1985;27:335–71.CrossRefPubMed
9.
11.
go back to reference Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.CrossRefPubMed Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50:1088–101.CrossRefPubMed
12.
go back to reference Maeda T, Matsumura S, Hiranuma H, et al. Expression of vascular endothelial growth factor in human oral squamous cell carcinoma: its association with tumour progression and p53 gene status. J Clin Pathol. 1998;51(10):771–5.PubMedCentralCrossRefPubMed Maeda T, Matsumura S, Hiranuma H, et al. Expression of vascular endothelial growth factor in human oral squamous cell carcinoma: its association with tumour progression and p53 gene status. J Clin Pathol. 1998;51(10):771–5.PubMedCentralCrossRefPubMed
13.
go back to reference Smith BD, Smith GL, Carter D, Sasaki CT, Haffty BG. Prognostic significance of vascular endothelial growth factor protein levels in oral and oropharyngeal squamous cell carcinoma. J Clin Oncol. 2000;18(10):2046–52.PubMed Smith BD, Smith GL, Carter D, Sasaki CT, Haffty BG. Prognostic significance of vascular endothelial growth factor protein levels in oral and oropharyngeal squamous cell carcinoma. J Clin Oncol. 2000;18(10):2046–52.PubMed
14.
go back to reference Yu F, Jiang X, Chen W, et al. Microvessel density and expression of vascular endothelial growth factor in adenoid cystid carcinoma of salivary gland. Shanghai J Stomatol. 2003;12:443–6. Yu F, Jiang X, Chen W, et al. Microvessel density and expression of vascular endothelial growth factor in adenoid cystid carcinoma of salivary gland. Shanghai J Stomatol. 2003;12:443–6.
15.
go back to reference Li X, Li N, Liu T, et al. Significance of VEGF expression and microvessel count in oral carcinoma. Shanghai J Stomatol. 2003;12:123–6. Li X, Li N, Liu T, et al. Significance of VEGF expression and microvessel count in oral carcinoma. Shanghai J Stomatol. 2003;12:123–6.
16.
go back to reference Kishimoto K, Sasaki A, Yoshihama Y, Mese H, Tsukamoto G, Matsumura T. Expression of vascular endothelial growth factor-C predicts regional lymph node metastasis in early oral squamous cell carcinoma. Oral Oncol. 2003;39(4):391–6.CrossRefPubMed Kishimoto K, Sasaki A, Yoshihama Y, Mese H, Tsukamoto G, Matsumura T. Expression of vascular endothelial growth factor-C predicts regional lymph node metastasis in early oral squamous cell carcinoma. Oral Oncol. 2003;39(4):391–6.CrossRefPubMed
17.
go back to reference Lim JJ, Kang S, Lee MR, et al. Expression of vascular endothelial growth factor in salivary gland carcinomas and its relation to p53, Ki-67 and prognosis. J Oral Pathol Med. 2003;32(9):552–61.PubMed Lim JJ, Kang S, Lee MR, et al. Expression of vascular endothelial growth factor in salivary gland carcinomas and its relation to p53, Ki-67 and prognosis. J Oral Pathol Med. 2003;32(9):552–61.PubMed
18.
19.
go back to reference Zhang J, Peng B, Chen X. Expressions of nuclear factor kappaB, inducible nitric oxide synthase, and vascular endothelial growth factor in adenoid cystic carcinoma of salivary glands: correlations with the angiogenesis and clinical outcome. Clin Cancer Res. 2005;11(20):7334–43.CrossRefPubMed Zhang J, Peng B, Chen X. Expressions of nuclear factor kappaB, inducible nitric oxide synthase, and vascular endothelial growth factor in adenoid cystic carcinoma of salivary glands: correlations with the angiogenesis and clinical outcome. Clin Cancer Res. 2005;11(20):7334–43.CrossRefPubMed
20.
go back to reference Chien CY, Su CY, Hwang CF, Chuang HC, Chen CM, Huang CC. High expressions of CD105 and VEGF in early oral cancer predict potential cervical metastasis. J Surg Oncol. 2006;94(5):413–7.CrossRefPubMed Chien CY, Su CY, Hwang CF, Chuang HC, Chen CM, Huang CC. High expressions of CD105 and VEGF in early oral cancer predict potential cervical metastasis. J Surg Oncol. 2006;94(5):413–7.CrossRefPubMed
21.
go back to reference Chuang HC, Su CY, Huang HY, Chien CY, Chen CM, Huang CC. High expression of CD105 as a prognostic predictor of early tongue cancer. Laryngoscope. 2006;116(7):1175–9.CrossRefPubMed Chuang HC, Su CY, Huang HY, Chien CY, Chen CM, Huang CC. High expression of CD105 as a prognostic predictor of early tongue cancer. Laryngoscope. 2006;116(7):1175–9.CrossRefPubMed
22.
go back to reference Kim SH, Cho NH, Kim K, et al. Correlations of oral tongue cancer invasion with matrix metalloproteinases (MMPs) and vascular endothelial growth factor (VEGF) expression. J Surg Oncol. 2006;93(4):330–7.CrossRefPubMed Kim SH, Cho NH, Kim K, et al. Correlations of oral tongue cancer invasion with matrix metalloproteinases (MMPs) and vascular endothelial growth factor (VEGF) expression. J Surg Oncol. 2006;93(4):330–7.CrossRefPubMed
23.
go back to reference Shi L, Chen XM, Wang L, Zhang L, Chen Z. Expression of caveolin-1 in mucoepidermoid carcinoma of the salivary glands: correlation with vascular endothelial growth factor, microvessel density, and clinical outcome. Cancer. 2007;109(8):1523–31.CrossRefPubMed Shi L, Chen XM, Wang L, Zhang L, Chen Z. Expression of caveolin-1 in mucoepidermoid carcinoma of the salivary glands: correlation with vascular endothelial growth factor, microvessel density, and clinical outcome. Cancer. 2007;109(8):1523–31.CrossRefPubMed
24.
go back to reference Cho JH, Kim HS, Park CS, et al. Maspin expression in early oral tongue cancer and its relation to expression of mutant-type p53 and vascular endothelial growth factor (VEGF). Oral Oncol. 2007;43(3):272–7.CrossRefPubMed Cho JH, Kim HS, Park CS, et al. Maspin expression in early oral tongue cancer and its relation to expression of mutant-type p53 and vascular endothelial growth factor (VEGF). Oral Oncol. 2007;43(3):272–7.CrossRefPubMed
25.
go back to reference Ou Yang KX, Liang J, Huang ZQ. Association of clinicopathologic parameters with the expression of inducible nitric oxide synthase and vascular endothelial growth factor in mucoepidermoid carcinoma. Oral Dis. 2011;17(6):590–6.CrossRefPubMed Ou Yang KX, Liang J, Huang ZQ. Association of clinicopathologic parameters with the expression of inducible nitric oxide synthase and vascular endothelial growth factor in mucoepidermoid carcinoma. Oral Dis. 2011;17(6):590–6.CrossRefPubMed
26.
go back to reference Seki S, Fujiwara M, Matsuura M, et al. Prediction of outcome of patients with oral squamous cell carcinoma using vascular invasion and the strongly positive expression of vascular endothelial growth factors. Oral Oncol. 2011;47(7):588–93.CrossRefPubMed Seki S, Fujiwara M, Matsuura M, et al. Prediction of outcome of patients with oral squamous cell carcinoma using vascular invasion and the strongly positive expression of vascular endothelial growth factors. Oral Oncol. 2011;47(7):588–93.CrossRefPubMed
27.
go back to reference Cheng SJ, Lee JJ, Kok SH, et al. Expression of vascular endothelial growth factor is significantly associated with progression and prognosis of oral squamous cell carcinomas in Taiwan. J Formos Med Assoc. 2011;110(1):50–7.CrossRefPubMed Cheng SJ, Lee JJ, Kok SH, et al. Expression of vascular endothelial growth factor is significantly associated with progression and prognosis of oral squamous cell carcinomas in Taiwan. J Formos Med Assoc. 2011;110(1):50–7.CrossRefPubMed
28.
go back to reference Huang C, Sun Z, Sun Y, et al. Association of increased ligand cyclophilin A and receptor CD147 with hypoxia, angiogenesis, metastasis and prognosis of tongue squamous cell carcinoma. Histopathology. 2012;60(5):793–803.CrossRefPubMed Huang C, Sun Z, Sun Y, et al. Association of increased ligand cyclophilin A and receptor CD147 with hypoxia, angiogenesis, metastasis and prognosis of tongue squamous cell carcinoma. Histopathology. 2012;60(5):793–803.CrossRefPubMed
29.
go back to reference Parikh AA, Ellis LM. The vascular endothelial growth factor family and its receptors. Hematol Oncol Clin N Am. 2004;18(5):951–71. vii.CrossRef Parikh AA, Ellis LM. The vascular endothelial growth factor family and its receptors. Hematol Oncol Clin N Am. 2004;18(5):951–71. vii.CrossRef
30.
go back to reference Xie K, Wei D, Shi Q, Huang S. Constitutive and inducible expression and regulation of vascular endothelial growth factor. Cytokine Growth Factor Rev. 2004;15(5):297–324.CrossRefPubMed Xie K, Wei D, Shi Q, Huang S. Constitutive and inducible expression and regulation of vascular endothelial growth factor. Cytokine Growth Factor Rev. 2004;15(5):297–324.CrossRefPubMed
31.
go back to reference Lee J, Gray A, Yuan J, Luoh SM, Avraham H, Wood WI. Vascular endothelial growth factor-related protein: a ligand and specific activator of the tyrosine kinase receptor Flt4. Proc Natl Acad Sci USA. 1996;93(5):1988–92.PubMedCentralCrossRefPubMed Lee J, Gray A, Yuan J, Luoh SM, Avraham H, Wood WI. Vascular endothelial growth factor-related protein: a ligand and specific activator of the tyrosine kinase receptor Flt4. Proc Natl Acad Sci USA. 1996;93(5):1988–92.PubMedCentralCrossRefPubMed
32.
go back to reference Jeltsch M, Kaipainen A, Joukov V, et al. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science. 1997;276(5317):1423–5.CrossRefPubMed Jeltsch M, Kaipainen A, Joukov V, et al. Hyperplasia of lymphatic vessels in VEGF-C transgenic mice. Science. 1997;276(5317):1423–5.CrossRefPubMed
33.
go back to reference Kyzas PA, Cunha IW, Ioannidis JP. Prognostic significance of vascular endothelial growth factor immunohistochemical expression in head and neck squamous cell carcinoma: a meta-analysis. Clin Cancer Res. 2005;11(4):1434–40.CrossRefPubMed Kyzas PA, Cunha IW, Ioannidis JP. Prognostic significance of vascular endothelial growth factor immunohistochemical expression in head and neck squamous cell carcinoma: a meta-analysis. Clin Cancer Res. 2005;11(4):1434–40.CrossRefPubMed
34.
go back to reference Zhan P, Wang J, Lv XJ, et al. Prognostic value of vascular endothelial growth factor expression in patients with lung cancer: a systematic review with meta-analysis. J Thorac Oncol. 2009;4(9):1094–103.CrossRefPubMed Zhan P, Wang J, Lv XJ, et al. Prognostic value of vascular endothelial growth factor expression in patients with lung cancer: a systematic review with meta-analysis. J Thorac Oncol. 2009;4(9):1094–103.CrossRefPubMed
37.
go back to reference Des Guetz G, Uzzan B, Nicolas P, et al. Microvessel density and VEGF expression are prognostic factors in colorectal cancer. Meta-analysis of the literature. Br J Cancer. 2006;94(12):1823–32.PubMedCentralCrossRefPubMed Des Guetz G, Uzzan B, Nicolas P, et al. Microvessel density and VEGF expression are prognostic factors in colorectal cancer. Meta-analysis of the literature. Br J Cancer. 2006;94(12):1823–32.PubMedCentralCrossRefPubMed
38.
go back to reference Peng L, Zhan P, Zhou Y, et al. Prognostic significance of vascular endothelial growth factor immunohistochemical expression in gastric cancer: a meta-analysis. Mol Biol Rep. 2012;39(10):9473–84. Oct.CrossRefPubMed Peng L, Zhan P, Zhou Y, et al. Prognostic significance of vascular endothelial growth factor immunohistochemical expression in gastric cancer: a meta-analysis. Mol Biol Rep. 2012;39(10):9473–84. Oct.CrossRefPubMed
39.
go back to reference Schoenleber SJ, Kurtz DM, Talwalkar JA, Roberts LR, Gores GJ. Prognostic role of vascular endothelial growth factor in hepatocellular carcinoma: systematic review and meta-analysis. Br J Cancer. 2009;100(9):1385–92.PubMedCentralCrossRefPubMed Schoenleber SJ, Kurtz DM, Talwalkar JA, Roberts LR, Gores GJ. Prognostic role of vascular endothelial growth factor in hepatocellular carcinoma: systematic review and meta-analysis. Br J Cancer. 2009;100(9):1385–92.PubMedCentralCrossRefPubMed
40.
go back to reference Kowanetz M, Ferrara N. Vascular endothelial growth factor signaling pathways: therapeutic perspective. Clin Cancer Res. 2006;12(17):5018–22.CrossRefPubMed Kowanetz M, Ferrara N. Vascular endothelial growth factor signaling pathways: therapeutic perspective. Clin Cancer Res. 2006;12(17):5018–22.CrossRefPubMed
41.
go back to reference Ferrara N, Hillan KJ, Gerber HP, Novotny W. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov. 2004;3(5):391–400.CrossRefPubMed Ferrara N, Hillan KJ, Gerber HP, Novotny W. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat Rev Drug Discov. 2004;3(5):391–400.CrossRefPubMed
42.
go back to reference Begg CB, Berlin JA. Publication bias: a problem in interpreting medical data. J R Stat Soc A. 1988;151:419–63.CrossRef Begg CB, Berlin JA. Publication bias: a problem in interpreting medical data. J R Stat Soc A. 1988;151:419–63.CrossRef
Metadata
Title
Prognostic significance of VEGF immunohistochemical expression in oral cancer: a meta-analysis of the literature
Authors
Su-Feng Zhao
Xu-Dong Yang
Ming-Xing Lu
Guo-Wen Sun
Yu-Xin Wang
Yin-Kai Zhang
Yu-Mei Pu
En-Yi Tang
Publication date
01-10-2013
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 5/2013
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-013-0886-9

Other articles of this Issue 5/2013

Tumor Biology 5/2013 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine