Skip to main content
Top
Published in: Journal of Cancer Research and Clinical Oncology 7/2013

01-07-2013 | Original Paper

High circulating VEGF level predicts poor overall survival in lung cancer

Authors: Pingping Hu, Weidong Liu, Liguang Wang, Miaomiao Yang, Jiajun Du

Published in: Journal of Cancer Research and Clinical Oncology | Issue 7/2013

Login to get access

Abstract

Purpose

Vascular endothelial growth factor (VEGF) is considered as the best-validated key regulator of angiogenesis, while the prognostic role of circulating VEGF in lung cancer remains controversial. We conducted a meta-analysis to evaluate the prognostic role of circulating VEGF.

Methods

Nineteen studies with a total number of 2,890 patients were analyzed in our meta-analysis. Hazard ratios (HRs) and their 95 % confidence intervals (CIs) were used to quantify the predictive ability of circulating VEGF on survival.

Results

The pooled HR of all 17 studies evaluating overall survival (OS) was 1.29 (95 % CI 1.19–1.40, p < 0.001), indicating high circulating VEGF predicted poor OS. When grouped by disease stages, the pooled HRs were 0.97 (95 % CI 0.47–1.47, p < 0.001) for operable stage and 1.34 (95 % CI 1.18–1.49, p < 0.001) for inoperable stage. The pooled HRs were 1.28 (95 % CI 1.15–1.42, p < 0.001) for serum and 1.31 (95 % CI 1.13–1.49, p < 0.001) for plasma, when categorized by blood sample. Meta-analysis of circulating VEGF related to progression-free survival (PFS) was performed in 7 studies, and the pooled HR was 1.03 (95 % CI 0.96–1.09).

Conclusions

Our results indicate that high level of circulating VEGF predicts poor OS in lung cancer, yet it does not predict poor PFS.
Literature
go back to reference Altman DG (2001) Systematic reviews of evaluations of prognostic variables. BMJ 323(7306):224–228PubMedCrossRef Altman DG (2001) Systematic reviews of evaluations of prognostic variables. BMJ 323(7306):224–228PubMedCrossRef
go back to reference An SJ, Huang YS, Chen ZH, Su J, Yang Y, Chen JG, Yan HH, Lin QX, Yang JJ, Yang XN, Zhou Q, Zhang XC, Wu YL (2012) Posttreatment plasma VEGF levels may be associated with the overall survival of patients with advanced non-small cell lung cancer treated with bevacizumab plus chemotherapy. Med Oncol 29(2):627–632. doi:10.1007/s12032-011-9924-x PubMedCrossRef An SJ, Huang YS, Chen ZH, Su J, Yang Y, Chen JG, Yan HH, Lin QX, Yang JJ, Yang XN, Zhou Q, Zhang XC, Wu YL (2012) Posttreatment plasma VEGF levels may be associated with the overall survival of patients with advanced non-small cell lung cancer treated with bevacizumab plus chemotherapy. Med Oncol 29(2):627–632. doi:10.​1007/​s12032-011-9924-x PubMedCrossRef
go back to reference Brattstrom D, Bergqvist M, Larsson A, Holmertz J, Hesselius P, Rosenberg L, Brodin O, Wagenius G (1998) Basic fibroblast growth factor and vascular endothelial growth factor in sera from non-small cell lung cancer patients. Anticancer Res 18(2A):1123–1127PubMed Brattstrom D, Bergqvist M, Larsson A, Holmertz J, Hesselius P, Rosenberg L, Brodin O, Wagenius G (1998) Basic fibroblast growth factor and vascular endothelial growth factor in sera from non-small cell lung cancer patients. Anticancer Res 18(2A):1123–1127PubMed
go back to reference Brattstrom D, Bergqvist M, Hesselius P, Larsson A, Lamberg K, Wernlund J, Brodin O, Wagenius G (2002) Elevated preoperative serum levels of angiogenic cytokines correlate to larger primary tumours and poorer survival in non-small cell lung cancer patients. Lung Cancer 37(1):57–63PubMedCrossRef Brattstrom D, Bergqvist M, Hesselius P, Larsson A, Lamberg K, Wernlund J, Brodin O, Wagenius G (2002) Elevated preoperative serum levels of angiogenic cytokines correlate to larger primary tumours and poorer survival in non-small cell lung cancer patients. Lung Cancer 37(1):57–63PubMedCrossRef
go back to reference Carrillo-de Santa Pau E, Carrillo Arias F, Caso Pelaez E, Muguruza Trueba I, Sanchez Hernandez I, Munoz Molina GM, Moreno Balsalobre R, Sacristan Lopez S, Gomez-Pinillos A, Toledo Lobo Mdel V (2010) Vascular endothelial growth factor (VEGF) serum levels are associated with survival in early stages of lung cancer patients. Cancer Invest 28(4):393–398. doi:10.3109/07357900903405900 PubMed Carrillo-de Santa Pau E, Carrillo Arias F, Caso Pelaez E, Muguruza Trueba I, Sanchez Hernandez I, Munoz Molina GM, Moreno Balsalobre R, Sacristan Lopez S, Gomez-Pinillos A, Toledo Lobo Mdel V (2010) Vascular endothelial growth factor (VEGF) serum levels are associated with survival in early stages of lung cancer patients. Cancer Invest 28(4):393–398. doi:10.​3109/​0735790090340590​0 PubMed
go back to reference Choi JH, Kim HC, Lim HY, Nam DK, Kim HS, Yi JW, Chun M, Oh YT, Kang S, Park KJ, Hwang SC, Lee YH, Hahn MH (2001) Vascular endothelial growth factor in the serum of patients with non-small cell lung cancer: correlation with platelet and leukocyte counts. Lung Cancer 33(2–3):171–179PubMedCrossRef Choi JH, Kim HC, Lim HY, Nam DK, Kim HS, Yi JW, Chun M, Oh YT, Kang S, Park KJ, Hwang SC, Lee YH, Hahn MH (2001) Vascular endothelial growth factor in the serum of patients with non-small cell lung cancer: correlation with platelet and leukocyte counts. Lung Cancer 33(2–3):171–179PubMedCrossRef
go back to reference Des Guetz G, Uzzan B, Nicolas P, Cucherat M, Morere J, Benamouzig R, Breau J, Perret G (2006) Microvessel density and VEGF expression are prognostic factors in colorectal cancer. Meta-analysis of the literature. Br J Cancer 94(12):1823–1832PubMedCrossRef Des Guetz G, Uzzan B, Nicolas P, Cucherat M, Morere J, Benamouzig R, Breau J, Perret G (2006) Microvessel density and VEGF expression are prognostic factors in colorectal cancer. Meta-analysis of the literature. Br J Cancer 94(12):1823–1832PubMedCrossRef
go back to reference Dudek AZ, Mahaseth H (2005) Circulating angiogenic cytokines in patients with advanced non-small cell lung cancer: correlation with treatment response and survival. Cancer Invest 23(3):193–200PubMedCrossRef Dudek AZ, Mahaseth H (2005) Circulating angiogenic cytokines in patients with advanced non-small cell lung cancer: correlation with treatment response and survival. Cancer Invest 23(3):193–200PubMedCrossRef
go back to reference Edelman MJ, Hodgson L, Wang XF, Christenson R, Jewell S, Vokes E, Kratzke R (2011) Serum vascular endothelial growth factor and COX-2/5-LOX inhibition in advanced non-small cell lung cancer: cancer and leukemia group B 150304. J Thorac Oncol 6(11):1902–1906. doi:10.1097/JTO.0b013e31822a7383 PubMedCrossRef Edelman MJ, Hodgson L, Wang XF, Christenson R, Jewell S, Vokes E, Kratzke R (2011) Serum vascular endothelial growth factor and COX-2/5-LOX inhibition in advanced non-small cell lung cancer: cancer and leukemia group B 150304. J Thorac Oncol 6(11):1902–1906. doi:10.​1097/​JTO.​0b013e31822a7383​ PubMedCrossRef
go back to reference Egger M, Zellweger-Zähner T, Schneider M, Junker C, Lengeler C, Antes G (1997) Language bias in randomised controlled trials published in English and German. Lancet 350(9074):326PubMedCrossRef Egger M, Zellweger-Zähner T, Schneider M, Junker C, Lengeler C, Antes G (1997) Language bias in randomised controlled trials published in English and German. Lancet 350(9074):326PubMedCrossRef
go back to reference Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9(6):669–676PubMedCrossRef Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nat Med 9(6):669–676PubMedCrossRef
go back to reference Firat S, Bousamra M, Gore E, Byhardt RW (2002) Comorbidity and KPS are independent prognostic factors in stage I non-small-cell lung cancer. Int J Radiat Oncol Biol Phys 52(4):1047PubMedCrossRef Firat S, Bousamra M, Gore E, Byhardt RW (2002) Comorbidity and KPS are independent prognostic factors in stage I non-small-cell lung cancer. Int J Radiat Oncol Biol Phys 52(4):1047PubMedCrossRef
go back to reference Hanrahan EO, Ryan AJ, Mann H, Kennedy SJ, Langmuir P, Natale RB, Herbst RS, Johnson BE, Heymach JV (2009) Baseline vascular endothelial growth factor concentration as a potential predictive marker of benefit from vandetanib in non-small cell lung cancer. Clin Cancer Res 15(10):3600–3609. doi:10.1158/1078-0432.CCR-08-2568 PubMedCrossRef Hanrahan EO, Ryan AJ, Mann H, Kennedy SJ, Langmuir P, Natale RB, Herbst RS, Johnson BE, Heymach JV (2009) Baseline vascular endothelial growth factor concentration as a potential predictive marker of benefit from vandetanib in non-small cell lung cancer. Clin Cancer Res 15(10):3600–3609. doi:10.​1158/​1078-0432.​CCR-08-2568 PubMedCrossRef
go back to reference Hasegawa Y, Takanashi S, Okudera K, Kumagai M, Hayashi A, Morimoto T, Okumura K (2005) Vascular endothelial growth factor level as a prognostic determinant of small cell lung cancer in Japanese patients. Intern Med 44(1):26–34PubMedCrossRef Hasegawa Y, Takanashi S, Okudera K, Kumagai M, Hayashi A, Morimoto T, Okumura K (2005) Vascular endothelial growth factor level as a prognostic determinant of small cell lung cancer in Japanese patients. Intern Med 44(1):26–34PubMedCrossRef
go back to reference Hegde PS, Jubb AM, Chen D, Li NF, Meng G, Bernaards C, Elliott R, Scherer S, Chen DS (2012) Predictive impact of circulating vascular endothelial growth factor in 4 phase III trials evaluating bevacizumab. Clin Cancer Res. doi:10.1158/1078-0432.ccr-12-2535 Hegde PS, Jubb AM, Chen D, Li NF, Meng G, Bernaards C, Elliott R, Scherer S, Chen DS (2012) Predictive impact of circulating vascular endothelial growth factor in 4 phase III trials evaluating bevacizumab. Clin Cancer Res. doi:10.​1158/​1078-0432.​ccr-12-2535
go back to reference Imoto H, Osaki T, Taga S, Ohgami A, Ichiyoshi Y, Yasumoto K (1998) Vascular endothelial growth factor expression in non-small-cell lung cancer: prognostic significance in squamous cell carcinoma. J Thorac Cardiovasc Surg 115(5):1007–1014PubMedCrossRef Imoto H, Osaki T, Taga S, Ohgami A, Ichiyoshi Y, Yasumoto K (1998) Vascular endothelial growth factor expression in non-small-cell lung cancer: prognostic significance in squamous cell carcinoma. J Thorac Cardiovasc Surg 115(5):1007–1014PubMedCrossRef
go back to reference Jantus-Lewintre E, Sanmartin E, Sirera R, Blasco A, Sanchez JJ, Taron M, Rosell R, Camps C (2011) Combined VEGF-A and VEGFR-2 concentrations in plasma: diagnostic and prognostic implications in patients with advanced NSCLC. Lung Cancer 74(2):326–331. doi:10.1016/j.lungcan.2011.02.016 PubMedCrossRef Jantus-Lewintre E, Sanmartin E, Sirera R, Blasco A, Sanchez JJ, Taron M, Rosell R, Camps C (2011) Combined VEGF-A and VEGFR-2 concentrations in plasma: diagnostic and prognostic implications in patients with advanced NSCLC. Lung Cancer 74(2):326–331. doi:10.​1016/​j.​lungcan.​2011.​02.​016 PubMedCrossRef
go back to reference Jelkmann W (2001) Pitfalls in the measurement of circulating vascular endothelial growth factor. Clin Chem 47(4):617–623PubMed Jelkmann W (2001) Pitfalls in the measurement of circulating vascular endothelial growth factor. Clin Chem 47(4):617–623PubMed
go back to reference Kondo S, Asano M, Matsuo K, Ohmori I, Suzuki H (1994) Vascular endothelial growth factor/vascular permeability factor is detectable in the sera of tumor-bearing mice and cancer patients. Biochim Biophys Acta 1221(2):211–214PubMedCrossRef Kondo S, Asano M, Matsuo K, Ohmori I, Suzuki H (1994) Vascular endothelial growth factor/vascular permeability factor is detectable in the sera of tumor-bearing mice and cancer patients. Biochim Biophys Acta 1221(2):211–214PubMedCrossRef
go back to reference Kyzas PA, Cunha IW, Ioannidis JPA (2005) Prognostic significance of vascular endothelial growth factor immunohistochemical expression in head and neck squamous cell carcinoma: a meta-analysis. Clin Cancer Res 11(4):1434–1440PubMedCrossRef Kyzas PA, Cunha IW, Ioannidis JPA (2005) Prognostic significance of vascular endothelial growth factor immunohistochemical expression in head and neck squamous cell carcinoma: a meta-analysis. Clin Cancer Res 11(4):1434–1440PubMedCrossRef
go back to reference Laack E, Scheffler A, Burkholder I, Boeters I, Andritzky B, Schuch G, Gorn M, Vohwinkel G, Edler L, Fiedler W, Hossfeld DK (2005) Pretreatment vascular endothelial growth factor (VEGF) and matrix metalloproteinase-9 (MMP-9) serum levels in patients with metastatic non-small cell lung cancer (NSCLC). Lung Cancer 50(1):51–58. doi:10.1016/j.lungcan.2005.05.011 PubMedCrossRef Laack E, Scheffler A, Burkholder I, Boeters I, Andritzky B, Schuch G, Gorn M, Vohwinkel G, Edler L, Fiedler W, Hossfeld DK (2005) Pretreatment vascular endothelial growth factor (VEGF) and matrix metalloproteinase-9 (MMP-9) serum levels in patients with metastatic non-small cell lung cancer (NSCLC). Lung Cancer 50(1):51–58. doi:10.​1016/​j.​lungcan.​2005.​05.​011 PubMedCrossRef
go back to reference Lakatos E (1988) Sample sizes based on the log-rank statistic in complex clinical trials. Biometrics 44(1):229–241PubMedCrossRef Lakatos E (1988) Sample sizes based on the log-rank statistic in complex clinical trials. Biometrics 44(1):229–241PubMedCrossRef
go back to reference Lee J, Hong Y, Han C, Hwang D, Hong S (2000) Clinical usefulness of serum and plasma vascular endothelial growth factor in cancer patients: which is the optimal specimen? Int J Oncol 17(1):149–152PubMed Lee J, Hong Y, Han C, Hwang D, Hong S (2000) Clinical usefulness of serum and plasma vascular endothelial growth factor in cancer patients: which is the optimal specimen? Int J Oncol 17(1):149–152PubMed
go back to reference Mack PC, Redman MW, Chansky K, Williamson SK, Farneth NC, Lara PN Jr, Franklin WA, Le QT, Crowley JJ, Gandara DR (2008) Lower osteopontin plasma levels are associated with superior outcomes in advanced non-small-cell lung cancer patients receiving platinum-based chemotherapy: SWOG Study S0003. J Clin Oncol 26(29):4771–4776. doi:10.1200/JCO.2008.17.0662 PubMedCrossRef Mack PC, Redman MW, Chansky K, Williamson SK, Farneth NC, Lara PN Jr, Franklin WA, Le QT, Crowley JJ, Gandara DR (2008) Lower osteopontin plasma levels are associated with superior outcomes in advanced non-small-cell lung cancer patients receiving platinum-based chemotherapy: SWOG Study S0003. J Clin Oncol 26(29):4771–4776. doi:10.​1200/​JCO.​2008.​17.​0662 PubMedCrossRef
go back to reference Mascaux C, Iannino N, Martin B, Paesmans M, Berghmans T, Dusart M, Haller A, Lothaire P, Meert AP, Noel S, Lafitte JJ, Sculier JP (2005) The role of RAS oncogene in survival of patients with lung cancer: a systematic review of the literature with meta-analysis. Br J Cancer 92(1):131–139. doi:10.1038/sj.bjc.6602258 PubMedCrossRef Mascaux C, Iannino N, Martin B, Paesmans M, Berghmans T, Dusart M, Haller A, Lothaire P, Meert AP, Noel S, Lafitte JJ, Sculier JP (2005) The role of RAS oncogene in survival of patients with lung cancer: a systematic review of the literature with meta-analysis. Br J Cancer 92(1):131–139. doi:10.​1038/​sj.​bjc.​6602258 PubMedCrossRef
go back to reference Paesmans M, Sculier JP, Libert P, Bureau G, Dabouis G, Thiriaux J, Michel J, Van Cutsem O, Sergysels R, Mommen P et al (1995) Prognostic factors for survival in advanced non-small-cell lung cancer: univariate and multivariate analyses including recursive partitioning and amalgamation algorithms in 1,052 patients. The European Lung Cancer Working Party. J Clin Oncol 13(5):1221–1230PubMed Paesmans M, Sculier JP, Libert P, Bureau G, Dabouis G, Thiriaux J, Michel J, Van Cutsem O, Sergysels R, Mommen P et al (1995) Prognostic factors for survival in advanced non-small-cell lung cancer: univariate and multivariate analyses including recursive partitioning and amalgamation algorithms in 1,052 patients. The European Lung Cancer Working Party. J Clin Oncol 13(5):1221–1230PubMed
go back to reference Qin L, Bromberg-White J, Qian C (2012) Opportunities and challenges in tumor angiogenesis research: back and forth between bench and bed. Adv Cancer Res 113:191PubMedCrossRef Qin L, Bromberg-White J, Qian C (2012) Opportunities and challenges in tumor angiogenesis research: back and forth between bench and bed. Adv Cancer Res 113:191PubMedCrossRef
go back to reference Qu JT, Wang M, He HL, Tang Y, Ye XJ (2012) The prognostic value of elevated vascular endothelial growth factor in patients with osteosarcoma: a meta-analysis and systemic review. J Can Res Clin Oncol 138(5):819–825CrossRef Qu JT, Wang M, He HL, Tang Y, Ye XJ (2012) The prognostic value of elevated vascular endothelial growth factor in patients with osteosarcoma: a meta-analysis and systemic review. J Can Res Clin Oncol 138(5):819–825CrossRef
go back to reference Salven P, Ruotsalainen T, Mattson K, Joensuu H (1998) High pre-treatment serum level of vascular endothelial growth factor (VEGF) is associated with poor outcome in small-cell lung cancer. Int J Cancer 79(2):144–146PubMedCrossRef Salven P, Ruotsalainen T, Mattson K, Joensuu H (1998) High pre-treatment serum level of vascular endothelial growth factor (VEGF) is associated with poor outcome in small-cell lung cancer. Int J Cancer 79(2):144–146PubMedCrossRef
go back to reference Schoenleber S, Kurtz D, Talwalkar J, Roberts L, Gores G (2009) Prognostic role of vascular endothelial growth factor in hepatocellular carcinoma: systematic review and meta-analysis. Br J Cancer 100(9):1385–1392PubMedCrossRef Schoenleber S, Kurtz D, Talwalkar J, Roberts L, Gores G (2009) Prognostic role of vascular endothelial growth factor in hepatocellular carcinoma: systematic review and meta-analysis. Br J Cancer 100(9):1385–1392PubMedCrossRef
go back to reference Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF (1983) Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219(4587):983–985PubMedCrossRef Senger DR, Galli SJ, Dvorak AM, Perruzzi CA, Harvey VS, Dvorak HF (1983) Tumor cells secrete a vascular permeability factor that promotes accumulation of ascites fluid. Science 219(4587):983–985PubMedCrossRef
go back to reference Shimanuki Y, Takahashi K, Cui R, Hori S, Takahashi F, Miyamoto H, Fukurchi Y (2005) Role of serum vascular endothelial growth factor in the prediction of angiogenesis and prognosis for non-small cell lung cancer. Lung 183(1):29–42. doi:10.1007/s00408-004-2521-4 PubMedCrossRef Shimanuki Y, Takahashi K, Cui R, Hori S, Takahashi F, Miyamoto H, Fukurchi Y (2005) Role of serum vascular endothelial growth factor in the prediction of angiogenesis and prognosis for non-small cell lung cancer. Lung 183(1):29–42. doi:10.​1007/​s00408-004-2521-4 PubMedCrossRef
go back to reference Smith R, Tang J, Tudur-Smith C, Neoptolemos J, Ghaneh P (2011) Meta-analysis of immunohistochemical prognostic markers in resected pancreatic cancer. Br J Cancer 104(9):1440–1451PubMedCrossRef Smith R, Tang J, Tudur-Smith C, Neoptolemos J, Ghaneh P (2011) Meta-analysis of immunohistochemical prognostic markers in resected pancreatic cancer. Br J Cancer 104(9):1440–1451PubMedCrossRef
go back to reference Sorenson S, Fohlin H, Lindgren A, Lindskog M, Bergman B, Sederholm C, Ek L, Lamberg K, Clinchy B (2012) Predictive role of plasma vascular endothelial growth factor for the effect of celecoxib in advanced non-small cell lung cancer treated with chemotherapy. Eur J Cancer. doi:10.1016/j.ejca.2012.07.032 PubMed Sorenson S, Fohlin H, Lindgren A, Lindskog M, Bergman B, Sederholm C, Ek L, Lamberg K, Clinchy B (2012) Predictive role of plasma vascular endothelial growth factor for the effect of celecoxib in advanced non-small cell lung cancer treated with chemotherapy. Eur J Cancer. doi:10.​1016/​j.​ejca.​2012.​07.​032 PubMed
go back to reference Stewart L, Parmar M (1993) Meta-analysis of the literature or of individual patient data: is there a difference? Lancet 341(8842):418–422PubMedCrossRef Stewart L, Parmar M (1993) Meta-analysis of the literature or of individual patient data: is there a difference? Lancet 341(8842):418–422PubMedCrossRef
go back to reference Thurston G, Kitajewski J (2008) VEGF and Delta-Notch: interacting signalling pathways in tumour angiogenesis. Br J Cancer 99(8):1204–1209PubMedCrossRef Thurston G, Kitajewski J (2008) VEGF and Delta-Notch: interacting signalling pathways in tumour angiogenesis. Br J Cancer 99(8):1204–1209PubMedCrossRef
go back to reference Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR (2007) Practical methods for incorporating summary time-to-event data into meta-analysis. Trials 8(1):16PubMedCrossRef Tierney JF, Stewart LA, Ghersi D, Burdett S, Sydes MR (2007) Practical methods for incorporating summary time-to-event data into meta-analysis. Trials 8(1):16PubMedCrossRef
go back to reference Tonini C, Beghi E, Berg AT, Bogliun G, Giordano L, Newton RW, Tetto A, Vitelli E, Vitezic D, Wiebe S (2004) Predictors of epilepsy surgery outcome: a meta-analysis. Epilepsy Res 62(1):75PubMedCrossRef Tonini C, Beghi E, Berg AT, Bogliun G, Giordano L, Newton RW, Tetto A, Vitelli E, Vitezic D, Wiebe S (2004) Predictors of epilepsy surgery outcome: a meta-analysis. Epilepsy Res 62(1):75PubMedCrossRef
go back to reference Young RJ, Tin AW, Brown NJ, Jitlal M, Lee SM, Woll PJ (2012) Analysis of circulating angiogenic biomarkers from patients in two phase III trials in lung cancer of chemotherapy alone or chemotherapy and thalidomide. Br J Cancer 106(6):1153–1159. doi:10.1038/bjc.2012.50 PubMedCrossRef Young RJ, Tin AW, Brown NJ, Jitlal M, Lee SM, Woll PJ (2012) Analysis of circulating angiogenic biomarkers from patients in two phase III trials in lung cancer of chemotherapy alone or chemotherapy and thalidomide. Br J Cancer 106(6):1153–1159. doi:10.​1038/​bjc.​2012.​50 PubMedCrossRef
go back to reference Zhan P, Wang J, Lv X, Wang Q, Qiu L, Lin X, Yu L, Song Y (2009) Prognostic value of vascular endothelial growth factor expression in patients with lung cancer: a systematic review with meta-analysis. J Thorac Oncol 4(9):1094PubMedCrossRef Zhan P, Wang J, Lv X, Wang Q, Qiu L, Lin X, Yu L, Song Y (2009) Prognostic value of vascular endothelial growth factor expression in patients with lung cancer: a systematic review with meta-analysis. J Thorac Oncol 4(9):1094PubMedCrossRef
Metadata
Title
High circulating VEGF level predicts poor overall survival in lung cancer
Authors
Pingping Hu
Weidong Liu
Liguang Wang
Miaomiao Yang
Jiajun Du
Publication date
01-07-2013
Publisher
Springer-Verlag
Published in
Journal of Cancer Research and Clinical Oncology / Issue 7/2013
Print ISSN: 0171-5216
Electronic ISSN: 1432-1335
DOI
https://doi.org/10.1007/s00432-013-1425-1

Other articles of this Issue 7/2013

Journal of Cancer Research and Clinical Oncology 7/2013 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.