Prognostic value of vascular endothelial growth factor expression in patients with esophageal cancer: A systematic review and meta-analysis

Cancer Epidemiology Biomarkers and Prevention

Volumn 21, Issue 7, 2012, Pages 1126-1134

  Chen, Meilan ^a   Cai, Erhui ^a   Huang, Jizheng ^a   Yu, Ping ^a   Li, Ke ^a  

^a SHANTOU UNIVERSITY MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULOTROPIN;

ARTICLE; CANCER PATIENT; CANCER PROGNOSIS; CANCER SURVIVAL; CORRELATION ANALYSIS; DISEASE ASSOCIATION; EMBASE; ENZYME LINKED IMMUNOSORBENT ASSAY; ESOPHAGEAL ADENOCARCINOMA; ESOPHAGEAL SQUAMOUS CELL CARCINOMA; ESOPHAGUS CANCER; HISTOPATHOLOGY; HUMAN; IMMUNOHISTOCHEMISTRY; INHIBITION KINETICS; MEDLINE; OVERALL SURVIVAL; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RISK ASSESSMENT; RISK FACTOR; SYSTEMATIC REVIEW;

ADENOCARCINOMA; CARCINOMA, SQUAMOUS CELL; ESOPHAGEAL NEOPLASMS; HUMANS; PROGNOSIS; REVIEW LITERATURE AS TOPIC; TUMOR MARKERS, BIOLOGICAL; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84863594122     PISSN: 10559965     EISSN: None     Source Type: Journal    
DOI: 10.1158/1055-9965.EPI-12-0020     Document Type: Article

References (78)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011;61:69-90.
2. Quiros RM, Bui CL. Multidisciplinary approach to esophageal and gastric cancer. Surg Clin North Am 2009;89:79-96, viii.
3. Roukos DH, Murray S, Briasoulis E. Molecular genetic tools shape a roadmap towards a more accurate prognostic prediction and personalized management of cancer. Cancer Biol Ther 2007;6:308-12. (Pubitemid 47328293)
4. Sarbia M, Stahl M, Fink U, Willers R, Seeber S, Gabbert HE. Expression of apoptosis-regulating proteins and outcome of esophageal cancer patients treated by combined therapy modalities. Clin Cancer Res 1998;4:2991-7. (Pubitemid 29001472)
5. Gibault L, Metges JP, Conan-Charlet V, Lozac'h P, Robaszkiewicz M, Bessaguet C, et al. Diffuse EGFR staining is associated with reduced overall survival in locally advanced oesophageal squamous cell cancer. Br J Cancer 2005;93:107-15. (Pubitemid 41076258)
6. Ishikawa T, Furihata M, Ohtsuki Y, Murakami H, Inoue A, Ogoshi S. Cyclin D1 overexpression related to retinoblastoma protein expression as a prognostic marker in human oesophageal squamous cell carcinoma. Br J Cancer 1998;77:92-7. (Pubitemid 28029778)
7. Langer R, Von Rahden BH, Nahrig J, Von Weyhern C, Reiter R, Feith M, et al. Prognostic significance of expression patterns of c-erbB-2, p53, p16INK4A, p27KIP1, cyclin D1 and epidermal growth factor receptor in oesophageal adenocarcinoma: a tissue microarray study. J Clin Pathol 2006;59:631-4. (Pubitemid 43886048)
8. Okuno Y, Nishimura Y, Kashu I, Ono K, Hiraoka M. Prognostic values of proliferating cell nuclear antigen (PCNA) and Ki-67 for radiotherapy of oesophageal squamous cell carcinomas. Br J Cancer 1999;80: 387-95. (Pubitemid 29213190)
9. Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol 2005;23: 1011-27. (Pubitemid 46202320)
10. Carmeliet P. VEGF as a key mediator of angiogenesis in cancer. Oncology 2005;69 Suppl 3:4-10. (Pubitemid 41680947)
11. 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;11:1434-40. (Pubitemid 40315223)
12. 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;100:1385-92.
13. Zhan P, Wang J, Lv XJ, Wang Q, Qiu LX, Lin XQ, 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;4:1094-103.
14. Altman DG. Systematic reviews of evaluations of prognostic variables. BMJ 2001;323:224-8.
15. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM. REporting recommendations for tumour MARKer prognostic studies (REMARK). Br J Cancer 2005;93:387-91. (Pubitemid 43080010)
16. Steels E, Paesmans M, Berghmans T, Branle F, Lemaitre F, Mascaux C, et al. Role of p53 as a prognostic factor for survival in lung cancer: a systematic review of the literature with a meta-analysis. Eur Respir J 2001;18:705-19. (Pubitemid 33040631)
17. Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival end-points. Stat Med 1998;17:2815-34. (Pubitemid 28562978)
18. Yusuf S, Peto R, Lewis J, Collins R, Sleight P. Beta blockade during and after myocardial infarction: an overview of the randomized trials. Prog Cardiovasc Dis 1985;27:335-71. (Pubitemid 15107153)
19. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003;327:557-60. (Pubitemid 37088507)
20. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986;7:177-88. (Pubitemid 17189972)
21. Song F, Gilbody S. Bias in meta-analysis detected by a simple, graphical test. Increase in studies of publication bias coincided with increasing use of meta-analysis. BMJ 1998;316:471.
22. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994;50:1088-101.
23. Peters JL, Sutton AJ, Jones DR, Abrams KR, Rushton L. Contour-enhanced meta-analysis funnel plots help distinguish publication bias from other causes of asymmetry. J Clin Epidemiol 2008;61:991-6.
24. Arii S, Mori A, Uchida S, Fujimoto K, Shimada Y, Imamura M. Implication of vascular endothelial growth factor in the development and metastasis of human cancers. Hum Cell 1999;12:25-30.
25. Kleespies A, Bruns CJ, Jauch KW. Clinical significance of VEGF-A, -C and -D expression in esophageal malignancies. Onkologie 2005;28: 281-8. (Pubitemid 40754676)
26. Andolfo I, Petrosino G, Vecchione L, De Antonellis P, Capasso M, Montanaro D, et al. Detection of erbB2 copy number variations in plasma of patients with esophageal carcinoma. BMC Cancer 2011;11:126.
27. Bedoya F, Meneu JC, Macias MI, Moreno A, Enriquez-De-Salamanca R, Gonzalez EM, et al. Mutation in CNR1 gene and VEGF expression in esophageal cancer. Tumori 2009;95:68-75.
28. Couvelard A, Paraf F, Gratio V, Scoazec JY, Henin D, Degott C, et al. Angiogenesis in the neoplastic sequence of Barrett's oesophagus. Correlation with VEGF expression. J Pathol 2000;192:14-8.
29. Driessen A, Landuyt W, Pastorekova S, Moons J, Goethals L, Haustermans K, et al. Expression of carbonic anhydrase IX (CA IX), a hypoxia-related protein, rather than vascular-endothelial growth factor (VEGF), a pro-angiogenic factor, correlates with an extremely poor prognosis in esophageal and gastric adenocarcinomas. Ann Surg 2006;243: 334-40. (Pubitemid 43327764)
30. Gold PJ, Goldman B, Iqbal S, Leichman LP, Zhang W, Lenz HJ, et al. Cetuximab as second-line therapy in patients with metastatic esophageal adenocarcinoma: a phase II Southwest Oncology Group Study. (S0415). J Thorac Oncol 2010;5:1472-6.
31. Koide N, Nishio A, Hiraguri M, Hanazaki K, Adachi W, Amano J. Coexpression of vascular endothelial growth factor and p53 protein in squamous cell carcinoma of the esophagus. Am J Gastroenterol 2001;96:1733-40. (Pubitemid 32552352)
32. Kulke MH, Odze RD, Mueller JD, Wang H, Redston M, Bertagnolli MM. Prognostic significance of vascular endothelial growth factor and cyclooxygenase 2 expression in patients receiving preoperative chemoradiation for esophageal cancer. J Thorac Cardiovasc Surg 2004;127:1579-86. (Pubitemid 38725434)
33. Luo KJ, Hu Y, Wen J, Fu JH. CyclinD1, p53, E-cadherin, and VEGF discordant expression in paired regional metastatic lymph nodes of esophageal squamous cell carcinoma: a tissue array analysis. J Surg Oncol 2011;104:236-43.
34. Millikan KW, Mall JW, Myers JA, Hollinger EF, Doolas A, Saclarides TJ. Do angiogenesis and growth factor expression predict prognosis of esophageal cancer? Am Surg 2000;66:401-5; discussion 405-6.
35. Mobius C, Freire J, Becker I, Feith M, Brucher BL, Hennig M, et al. VEGF-Cexpression in squamous cell carcinoma and adenocarcinoma of the esophagus. World J Surg 2007;31:1768-72; discussion 1773-4.
36. Mobius C, Stein HJ, Becker I, Feith M, Theisen J, Gais P, et al. Vascular endothelial growth factor expression and neovascularization in Barrett's carcinoma. World J Surg 2004;28:675-9. (Pubitemid 39097124)
37. Mukherjee T, Kumar A, Mathur M, Chattopadhyay TK, Ralhan R. Ets-1 and VEGF expression correlates with tumor angiogenesis, lymph node metastasis, and patient survival in esophageal squamous cell carcinoma. J Cancer Res Clin Oncol 2003;129:430-6. (Pubitemid 36995141)
38. Nomiya T, Nemoto K, Miyachi H, Fujimoto K, Takeda K, Ogawa Y, et al. Relationships between radiosensitivity and microvascular density in esophageal carcinoma: significance of hypoxic fraction. Int J Radiat Oncol Biol Phys 2004;58:589-96. (Pubitemid 38145594)
39. Pan XF, Bao GL, Fang WT, Chen WH. [VEGF-C mRNA expression and its relationship with clinicopathological parameters in esophageal squamous cell carcinoma]. Zhonghua Zhong Liu Za Zhi 2008;30: 437-40.
40. Rades D, Golke H, Schild SE, Kilic E. Impact of VEGF and VEGF receptor 1 (FLT1) expression on the prognosis of stage III esophageal cancer patients after radiochemotherapy. Strahlenther Onkol 2008;184:416-20.
41. Saad RS, El-Gohary Y, Memari E, Liu YL, Silverman JF. Endoglin (CD105) and vascular endothelial growth factor as prognostic markers in esophageal adenocarcinoma. Hum Pathol 2005;36:955-61. (Pubitemid 41253380)
42. Saad RS, Lindner JL, Liu Y, Silverman JF. Lymphatic vessel density as prognostic marker in esophageal adenocarcinoma. Am J Clin Pathol 2009;131:92-8.
43. Wang XS, Liu MZ, Zhang CQ, Cai L, Cui NJ. [Effect of concurrent chemoradiotherapy on serum vascular endothelial growth factor in esophageal squamous cell carcinoma patients-a report of 43 cases]. Ai Zheng 2006;25:1428-32.
44. Zhang HZ, Zhang J, Xu N, Duan XB, He CN. [Expression and clinical significance of hypoxia inducible factor-1alpha, survivin and vascular endothelial growth factor in esophageal squamous cell carcinoma]. Zhonghua Bing Li Xue Za Zhi 2007;36:689-90.
45. Hu CZ, Wang YX, Zhang XZ. [Correlation between expression of vascular endothelial growth factor and prognosis of patients with esophageal squamous cell carcinoma]. Ai Zheng 2002;21:301-4.
46. Inoue K, Ozeki Y, Suganuma T, Sugiura Y, Tanaka S. Vascular endothelial growth factor expression in primary esophageal squamous cell carcinoma. Association with angiogenesis and tumor progression. Cancer 1997;79:206-13. (Pubitemid 27029883)
47. Kimura H, Kato H, Tanaka N, Inose T, Faried A, Sohda M, et al. Preoperative serum vascular endothelial growth factor-C (VEGF-C) levels predict recurrence in patients with esophageal cancer. Anticancer Res 2008;28:165-9.
48. Kimura Y, Watanabe M, Ohga T, Saeki H, Kakeji Y, Baba H, et al. Vascular endothelial growth factor C expression correlates with lymphatic involvement and poor prognosis in patients with esophageal squamous cell carcinoma. Oncol Rep 2003;10:1747-51.
49. Kitadai Y, Haruma K, Tokutomi T, Tanaka S, Sumii K, Carvalho M, et al. Significance of vessel count and vascular endothelial growth factor in human esophageal carcinomas. Clin Cancer Res 1998;4: 2195-200. (Pubitemid 28415667)
50. Koide N, Nishio A, Kono T, Yazawa K, Igarashi J, Watanabe H, et al. Histochemical study of vascular endothelial growth factor in squamous cell carcinoma of the esophagus. Hepatogastroenterology 1999;46:952-8. (Pubitemid 29224771)
51. Kozlowski M, Kowalczuk O, Milewski R, Chyczewski L, Niklinski J, Laudanski J. Serum vascular endothelial growth factors C and D in patients with oesophageal cancer. Eur J Cardiothorac Surg 2010;38: 260-7.
52. Nomiya T, Nemoto K, Nakata E, Takai Y, Yamada S. Expression of thymidine phosphorylase and VEGF in esophageal squamous cell carcinoma. Oncol Rep 2006;15:1497-501.
53. Takeuchi H, Ozawa S, Shih CH, Ando N, Kitagawa Y, Ueda M, et al. Loss of p16INK4a expression is associated with vascular endothelial growth factor expression in squamous cell carcinoma of the esophagus. Int J Cancer 2004;109:483-90. (Pubitemid 38339637)
54. Xu W, Zhang L, Xie Y. [Expression of vascular endothelial growth factor in primary esophageal squamous cell carcinoma and its significance in angiogenesis and prognosis of the tumor]. Zhonghua Yi Xue Za Zhi 2001;81:860-2.
55. Yoshikawa R, Fujiwara Y, Koishi K, Kojima S, Matsumoto T, Yanagi H, et al. Cyclooxygenase-2 expression after preoperative chemoradiotherapy correlates with more frequent esophageal cancer recurrence. World J Gastroenterol 2007;13:2283-8. (Pubitemid 46860728)
56. Ahn MJ, Jang SJ, Park YW, Choi JH, Oh HS, Lee CB, et al. Clinical prognostic values of vascular endothelial growth factor, microvessel density, and p53 expression in esophageal carcinomas. J Korean Med Sci 2002;17:201-7.
57. Choi JY, Jang KT, Shim YM, Kim K, Ahn G, Lee KH, et al. Prognostic significance of vascular endothelial growth factor expression and microvessel density in esophageal squamous cell carcinoma: comparison with positron emission tomography. Ann Surg Oncol 2006;13:1054-62. (Pubitemid 44337964)
58. Inoue A, Moriya H, Katada N, Tanabe S, Kobayashi N, Watanabe M, et al. Intratumoral lymphangiogenesis of esophageal squamous cell carcinoma and relationship with regulatory factors and prognosis. Pathol Int 2008;58:611-9.
59. Kato H, Yoshikawa M, Miyazaki T, Nakajima M, Fukai Y, Masuda N, et al. Expression of vascular endothelial growth factor (VEGF) and its receptors (Flt-1 and Flk-1) in esophageal squamous cell carcinoma. Anticancer Res 2002;22:3977-84. (Pubitemid 36134422)
60. Kii T, Takiuchi H, Kawabe S, Gotoh M, Ohta S, Tanaka T, et al. Evaluation of prognostic factors of esophageal squamous cell carcinoma (stage II-III) after concurrent chemoradiotherapy using biopsy specimens. Jpn J Clin Oncol 2007;37:583-9. (Pubitemid 351790801)
61. Kimura S, Kitadai Y, Tanaka S, Kuwai T, Hihara J, Yoshida K, et al. Expression of hypoxia-inducible factor (HIF)-1alpha is associated with vascular endothelial growth factor expression and tumour angiogenesis in human oesophageal squamous cell carcinoma. Eur J Cancer 2004;40:1904-12. (Pubitemid 39036767)
62. Liu P, Chen W, Zhu H, Liu B, Song S, Shen W, et al. Expression of VEGF-C correlates with a poor prognosis based on analysis of prognostic factors in 73 patients with esophageal squamous cell carcinomas. Jpn J Clin Oncol 2009;39:644-50.
63. Ogata Y, Fujita H, Yamana H, Sueyoshi S, Shirouzu K. Expression of vascular endothelial growth factor as a prognostic factor in node-positive squamous cell carcinoma in the thoracic esophagus: long-term follow-up study. World J Surg 2003;27:584-9. (Pubitemid 36961131)
64. Rosa AR, Schirmer CC, Gurski RR, Meurer L, Edelweiss MI, Kruel CD. Prognostic value of p53 protein expression and vascular endothelial growth factor expression in resected squamous cell carcinoma of the esophagus. Dis Esophagus 2003;16:112-8. (Pubitemid 36992384)
65. Shih CH, Ozawa S, Ando N, Ueda M, Kitajima M. Vascular endothelial growth factor expression predicts outcome and lymph node metastasis in squamous cell carcinoma of the esophagus. Clin Cancer Res 2000;6:1161-8. (Pubitemid 30159380)
66. Shimada H, Hoshino T, Okazumi S, Matsubara H, Funami Y, Nabeya Y, et al. Expression of angiogenic factors predicts response to chemoradiotherapy and prognosis of oesophageal squamous cell carcinoma. Br J Cancer 2002;86:552-7. (Pubitemid 34185091)
67. Shimada H, Takeda A, Nabeya Y, Okazumi SI, Matsubara H, Funami Y, et al. Clinical significance of serum vascular endothelial growth factor in esophageal squamous cell carcinoma. Cancer 2001;92:663-9. (Pubitemid 32735204)
68. Shimada Y, Imamura M, Watanabe G, Uchida S, Harada H, Makino T, et al. Prognostic factors of oesophageal squamous cell carcinoma from the perspective of molecular biology. Br J Cancer 1999;80: 1281-8. (Pubitemid 29264093)
69. Tanaka T, Ishiguro H, Kuwabara Y, Kimura M, Mitsui A, Katada T, et al. Vascular endothelial growth factor C (VEGF-C) in esophageal cancer correlates with lymph node metastasis and poor patient prognosis. J Exp Clin Cancer Res 2010;29:83.
70. Tzao C, Lee SC, Tung HJ, Hsu HS, Hsu WH, Sun GH, et al. Expression of hypoxia-inducible factor (HIF)-1alpha and vascular endothelial growth factor (VEGF)-D as outcome predictors in resected esophageal squamous cell carcinoma. Dis Markers 2008;25:141-8.
71. Cavazzola LT, Rosa AR, Schirmer CC, Gurski RR, Telles JP, Mielke F, et al. Immunohistochemical evaluation for P53 and VEGF (Vascular Endothelial Growth Factor) is not prognostic for long term survival in end stage esophageal adenocarcinoma. Rev Col Bras Cir 2009;36: 24-34.
72. Kozlowski M, Naumnik W, Niklinski J, Milewski R, Dziegielewski P, Laudanski J. Vascular endothelial growth factor C and D expression correlates with lymph node metastasis and poor prognosis in patients with resected esophageal cancer. Neoplasma 2011;58:311-9.
73. Dreilich M, Wagenius G, Bergstrom S, Brattstrom D, Larsson A, Hesselius P, et al. The role of cystatin C and the angiogenic cytokines VEGF and bFGF in patients with esophageal carcinoma. Med Oncol 2005;22:29-38. (Pubitemid 40647227)
74. Sun ZG, Wang Z, Liu XY, Liu FY. Mucin 1 and vascular endothelial growth factor C expression correlates with lymph node metastatic recurrence in patients with N0 esophageal cancer after Ivor-Lewis esophagectomy. World J Surg 2011;35:70-7.
75. Uchida S, Shimada Y, Watanabe G, Tanaka H, Shibagaki I, Miyahara T, et al. In oesophageal squamous cell carcinoma vascular endothelial growth factor is associated with p53 mutation, advanced stage and poor prognosis. Br J Cancer 1998;77:1704-9. (Pubitemid 28230478)
76. Des Guetz G, Uzzan B, Nicolas P, Cucherat M, Morere JF, Benamouzig R, et al. Microvessel density and VEGF expression are prognostic factors in colorectal cancer. Meta-analysis of the literature. Br J Cancer 2006;94:1823-32. (Pubitemid 43882572)
77. Li C, Zang J, Li XS. [Prognostic role of vascular endothelial growth factor in oral carcinoma: a meta analysis]. Hua Xi Kou Qiang Yi Xue Za Zhi 2011;29:39-43.
78. Chen J, Li T, Wu Y, He L, Zhang L, Shi T, et al. Prognostic significance of vascular endothelial growth factor expression in gastric carcinoma: a meta-analysis. J Cancer Res Clin Oncol 2011;137:1799-812.