Clinical Significance and Role of Lymphatic Vessel Invasion as a Major Prognostic Implication in Non-Small Cell Lung Cancer: A Meta-Analysis

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Wang, Jun ^a   Wang, Baocheng ^a   Zhao, Weipeng ^b   Guo, Yan ^c   Chen, Hong ^d   Chu, Huili ^a   Liang, Xiuju ^a   Bi, Jingwang ^a  

^a GENERAL HOSPITAL OF NORTHERN THEATER COMMAND   (China)

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c Military Command of Shandong Province ^*  (China)

^d AFFILIATED HOSPITAL OF NORTH SICHUAN MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CANCER INVASION; CANCER MORTALITY; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER STAGING; HUMAN; IMMUNOHISTOCHEMISTRY; LUNG ADENOCARCINOMA; LUNG NON SMALL CELL CANCER; LYMPH VESSEL METASTASIS; META ANALYSIS (TOPIC); OVERALL SURVIVAL; RECURRENCE FREE SURVIVAL;

ADENOCARCINOMA; CARCINOMA, NON-SMALL-CELL LUNG; HUMANS; LUNG NEOPLASMS; LYMPHATIC METASTASIS; LYMPHATIC VESSELS; NEOPLASM STAGING; PROGNOSIS; PUBLICATION BIAS; RETROSPECTIVE STUDIES;

EID: 84871429609     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052704     Document Type: Article

References (81)

1. Jemal A, Bray F, (2011) Center MM, Ferlay J, Ward E, et al (2011) CA Cancer J Clin. 61: 69-90.
2. Chansky K, Sculier JP, Crowley JJ, Giroux D, Van Meerbeeck J, et al. (2009) The International Association for the Study of Lung Cancer Staging Project: prognostic factors and pathologic TNM stage in surgically managed non-small cell lung cancer. J Thorac Oncol 4: 792-801.
3. Brundage MD, Davies D, Mackillop WJ, (2002) Prognostic factors in non-small cell lung cancer: a decade of progress. Chest 122: 1037-1057.
4. Steels E, Paesmans M, Berghmans T, Branle F, Lemaitre F, et al. (2001) 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 18: 705-719.
5. Martin B, Paesmans M, Berghmans T, Branle F, Ghisdal L, et al. (2003) Role of Bcl-2 as a prognostic factor for survival in lung cancer: a systematic review of the literature with meta-analysis. Br J Cancer 89: 55-64.
6. Meert AP, Martin B, Delmotte P, Berghmans T, Lafitte JJ, et al. (2002) The role of EGF-R expression on patient survival in lung cancer: a systematic review with meta-analysis. Eur Respir J 20: 975-981.
7. Wang J, Wang B, Chen X, Bi J, (2011) The prognostic value of RASSF1A promoter hypermethylation in non-small cell lung carcinoma: a systematic review and meta-analysis. Carcinogenesis 32: 411-416.
8. Wang J, Chen J, Chen X, Wang B, Li K, (2011) Blood vessel invasion as a strong independent prognostic indicator in non-small cell lung cancer: a systematic review and meta-analysis. PLoS One 6: e28844.
9. Rouzaut A, Irigoyen M, Montuenga LM, (2007) Lymphangiogenesis and lung cancer. J Thorac Oncol 2: 384-386.
10. Saijo T, Ishii G, Ochiai A, Hasebe T, Yoshida J, et al. (2007) Evaluation of extratumoral lymphatic permeation in non-small cell lung cancer as a means of predicting outcome. Lung Cancer 55: 61-66.
11. Parmar MK, Torri V, Stewart L, (1998) Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med 17: 2815-2834.
12. Whitehead A, Whitehead J, (1991) A general parametric approach to the meta-analysis of randomized clinical trials. Stat Med 10: 1665-1677.
13. Egger M, Davey Smith G, Schneider M, Minder C, (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315: 629-634.
14. Maeda R, Yoshida J, Ishii G, Aokage K, Hishida T, et al. (2010) Long-term outcome and late recurrence in patients with completely resected stage IA non-small cell lung cancer. J Thorac Oncol 5: 1246-1250.
15. Maeda R, Yoshida J, Hishida T, Aokage K, Nishimura M, et al. (2010) Late recurrence of non-small cell lung cancer more than 5 years after complete resection: incidence and clinical implications in patient follow-up. Chest 138: 145-150.
16. Ichinose Y, Hara N, Ohta M, Yano T, Maeda K, et al. (1993) Is T factor of the TNM staging system a predominant prognostic factor in pathologic stage I non-small-cell lung cancer? A multivariate prognostic factor analysis of 151 patients. J Thorac Cardiovasc Surg 106: 90-94.
17. Ichinose Y, Yano T, Yokoyama H, Inoue T, Asoh H, et al. (1994) The correlation between tumor size and lymphatic vessel invasion in resected peripheral stage I non-small-cell lung cancer. A potential risk of limited resection. J Thorac Cardiovasc Surg 108: 684-686.
18. Fu X, Jiang G, Wu K, Zhu X, Shi D, et al. (2001) Multivariate analysis for prognostic predictors in non-small cell lung cancer. Zhongguo Fei Ai Za Zhi 4: 459-462.
19. Gabor S, Renner H, Popper H, Anegg U, Sankin O, et al. (2004) Invasion of blood vessels as significant prognostic factor in radically resected T1-3N0M0 non-small-cell lung cancer. Eur J Cardiothorac Surg 25: 439-442.
20. Sayar A, Turna A, Solak O, Kiliçgün A, Urer N, et al. (2004) Nonanatomic prognostic factors in resected nonsmall cell lung carcinoma: the importance of perineural invasion as a new prognostic marker. Ann Thorac Surg 77: 421-425.
21. Duarte IG, Bufkin BL, Pennington MF, Gal AA, Cohen C, et al. (1998) Angiogenesis as a predictor of survival after surgical resection for stage I non-small-cell lung cancer. J Thorac Cardiovasc Surg 115: 652-658.
22. Roberts TE, Hasleton PS, Musgrove C, Swindell R, Lawson RA, (1992) Vascular invasion in non-small cell lung carcinoma. J Clin Pathol 45: 591-593.
23. Okada M, Nishio W, Sakamoto T, Uchino K, Tsubota N, (2003) Discrepancy of computed tomographic image between lung and mediastinal windows as a prognostic implication in small lung adenocarcinoma. Ann Thorac Surg 76: 1828-1832.
24. Kawata Y, Niki N, Ohmatsu H, Kusumoto M, Tsuchida T, et al. (2012) Quantitative classification based on CT histogram analysis of non-small cell lung cancer: correlation with histopathological characteristics and recurrence-free survival. Med Phys 39: 988-1000.
25. Araki K, Adachi Y, Metsugi H, Tokushima T, (2011) Prognostic implication of lymphatic vessel invasion in stage IB (pT2aN0M0). Gen Thorac Cardiovasc Surg 59: 605-608.
26. Maeda R, Yoshida J, Ishii G, Hishida T, Nishimura M, et al. (2010) Prognostic impact of intratumoral vascular invasion in non-small cell lung cancer patients. Thorax 65: 1092-1098.
27. Maeda R, Yoshida J, Ishii G, Hishida T, Nishimura M, et al. (2011) Poor prognostic factors in patients with stage IB non-small cell lung cancer according to the seventh edition TNM classification. Chest 139: 855-861.
28. Cho S, Sung SW, Jheon S, Chung JH, (2008) Risk of recurrence in surgically resected stage I adenocarcinoma of the lung. Lung 186: 411-419.
29. Okada M, Sakamoto T, Nishio W, Uchino K, Tsubota N, (2003) Characteristics and prognosis of patients after resection of nonsmall cell lung. Cancer 98: 535-541.
30. Poleri C, Morero JL, Nieva B, Vazquez MF, Rodriguez C, et al. (2003) Risk of recurrence in patients with surgically resected stage I non-small cell lung carcinoma: histopathologic and immunohistochemical analysis. Chest 123: 1858-1867.
31. Bréchot JM, Chevret S, Charpentier MC, Appere de Vecchi C, Capron F, et al. (1996) Blood vessel and lymphatic vessel invasion in resected nonsmall cell lung. Cancer 78: 2111-2118.
32. Ogawa J, Tsurumi T, Yamada S, Koide S, Shohtsu A, (1994) Blood vessel invasion and expression of sialyl Lewisx and proliferating cell nuclear antigen in stage I non-small cell lung cancer. Relation to postoperative recurrence. Cancer 73: 1177-1183.
33. Yamamoto S, Tomita Y, Hoshida Y, Iizuka N, Monden M, et al. (2004) Expression level of valosin-containing protein (p97) is correlated with progression and prognosis of non-small-cell lung carcinoma. Ann Surg Oncol 11: 697-704.
34. Rigau V, Molina TJ, Chaffaud C, Huchon G, Audouin J, et al. (2002) Blood vessel invasion in resected non small cell lung carcinomas is predictive of metastatic occurrence. Lung Cancer 38: 169-176.
35. Maeda R, Ishii G, Yoshida J, Hishida T, Nishimura M, et al. (2011) Influence of cigarette smoking on histological subtypes of stage I lung adenocarcinoma. J Thorac Oncol 6: 743-750.
36. Shoji F, Haro A, Yoshida T, Ito K, Morodomi Y, et al. (2010) Prognostic significance of intratumoral blood vessel invasion in pathologic stage IA non-small cell lung cancer. Ann Thorac Surg 89: 864-869.
37. Kawachi R, Tsukada H, Nakazato Y, Takei H, Furuyashiki G, et al. (2009) Early recurrence after surgical resection in patients with pathological stage I non-small cell lung cancer. Thorac Cardiovasc Surg 57: 472-475.
38. Hashizume T, Yamada K, Okamoto N, Saito H, Oshita F, et al. (2008) Prognostic significance of thin-section CT scan findings in small-sized lung. Chest 133: 441-447.
39. Maeda R, Yoshida J, Ishii G, Hishida T, Nishimura M, et al. (2012) Influence of Cigarette Smoking on Survival and Tumor Invasiveness in Clinical Stage IA Lung Adenocarcinoma. Ann Thorac Surg 93: 1626-1632.
40. Hanagiri T, Takenaka M, Oka S, Shigematsu Y, Nagata Y, et al. (2011) Prognostic significance of lymphovascular invasion for patients with stage I non-small cell lung cancer. Eur Surg Res 47: 211-217.
41. Funai K, Sugimura H, Morita T, Shundo Y, Shimizu K, et al. (2011) Lymphatic vessel invasion is a significant prognostic indicator in stage IA lung adenocarcinoma. Ann Surg Oncol 18: 2968-2972.
42. Harada M, Hato T, Horio H, (2011) Intratumoral lymphatic vessel involvement is an invasive indicator of completely resected pathologic stage I non-small cell lung cancer. J Thorac Oncol 6: 48-54.
43. Ryuge S, Sato Y, Wang GQ, Matsumoto T, Jiang SX, et al. (2011) Prognostic significance of nestin expression in resected non-small cell lung cancer. Chest 139: 862-869.
44. Yamaguchi Y, Ishii G, Kojima M, Yoh K, Otsuka H, et al. (2010) Histopathologic features of the tumor budding in adenocarcinoma of the lung: tumor budding as an index to predict the potential aggressiveness. J Thorac Oncol 5: 1361-1368.
45. Shimada Y, Ishii G, Hishida T, Yoshida J, Nishimura M, et al. (2010) Extratumoral vascular invasion is a significant prognostic indicator and a predicting factor of distant metastasis in non-small cell lung cancer. J Thorac Oncol 5: 970-975.
46. Sun JG, Wang Y, Chen ZT, Zhuo WL, Zhu B, et al. (2009) Detection of lymphangiogenesis in non-small cell lung cancer and its prognostic value. J Exp Clin Cancer Res 28: 21.
47. Hashizume S, Nagayasu T, Hayashi T, Hidaka S, Tsuchiya T, et al. (2009) Accuracy and prognostic impact of a vessel invasion grading system for stage IA non-small cell lung cancer. Lung Cancer 65: 363-370.
48. Mizuno T, Ishii G, Nagai K, Yoshida J, Nishimura M, et al. (2008) Identification of a low risk subgroup of stage IB lung adenocarcinoma patients. Lung Cancer 62: 302-308.
49. Higashiyama M, Oda K, Okami J, Maeda J, Kodama K, et al. (2009) Prognostic value of intraoperative pleural lavage cytology for lung cancer. Eur J Cardiothorac Surg 35: 337-342.
50. Bodendorf MO, Haas V, Laberke HG, Blumenstock G, Wex P, et al. (2009) Prognostic value and therapeutic consequences of vascular invasion in non-small cell lung carcinoma. Lung Cancer 64: 71-78.
51. Shimizu K, Yoshida J, Nagai K, Nishimura M, Ishii G, et al. (2005) Visceral pleural invasion is an invasive and aggressive indicator of non-small cell lung cancer. J Thorac Cardiovasc Surg 130: 160-165.
52. Takanami I, (2005) Increased expression of integrin-linked kinase is associated with shorter survival in non-small cell lung cancer. BMC Cancer 5: 1.
53. Maeshima AM, Niki T, Maeshima A, Yamada T, Kondo H, et al. (2002) Modified scar grade: a prognostic indicator in small peripheral lung adenocarcinoma. Cancer 95: 2546-2554.
54. Saito M, Furukawa K, Miura T, Kato H, (2002) Evaluation of T factor, surgical method, and prognostic factors in central type lung cancer. Jpn J Thorac Cardiovasc Surg 50: 413-417.
55. Moriya Y, Niki T, Yamada T, Matsuno Y, Kondo H, et al. (2001) Increased expression of laminin-5 and its prognostic significance in lung adenocarcinomas of small size. An immunohistochemical analysis of 102 cases. Cancer 91: 1129-1141.
56. Suzuki K, Nagai K, Yoshida J, Nishimura M, Takahashi K, et al. (1999) Conventional clinicopathologic prognostic factors in surgically resected nonsmall cell lung carcinoma. A comparison of prognostic factors for each pathologic TNM stage based on multivariate analyses. Cancer 86: 1976-1984.
57. Fu XL, Zhu XZ, Shi DR, Xiu LZ, Wang LJ, et al. (1999) Study of prognostic predictors for non-small cell lung cancer. Lung Cancer 23: 143-152.
58. Fujisawa T, Yamaguchi Y, Saitoh Y, Hiroshima K, Ohwada H, (1995) Blood and lymphatic vessel invasion as prognostic factors for patients with primary resected nonsmall cell carcinoma of the lung with intrapulmonary metastases. Cancer 76: 2464-2470.
59. Thomas P, Doddoli C, Thirion X, Ghez O, Payan-Defais MJ, et al. (2002) Stage I non-small cell lung cancer: a pragmatic approach to prognosis after complete resection. Ann Thorac Surg 73: 1065-1070.
60. Yokose T, Suzuki K, Nagai K, Nishiwaki Y, Sasaki S, et al. (2000) Favorable and unfavorable morphological prognostic factors in peripheral adenocarcinoma of the lung 3 cm or less in diameter. Lung Cancer 29: 179-188.
61. Hirata T, Fukuse T, Naiki H, Hitomi S, Wada H, (1998) Expression of CD44 variant exon 6 in stage I non-small cell lung carcinoma as a prognostic factor. Cancer Res 58: 1108-1110.
62. Harpole DH Jr, Herndon JE 2nd, Young WG Jr, Wolfe WG, Sabiston DC Jr (1995) Stage I nonsmall cell lung cancer. A multivariate analysis of treatment methods and patterns of recurrence. Cancer 76: 787-796.
63. Ichinose Y, Yano T, Asoh H, Yokoyama H, Yoshino I, et al. (1995) Prognostic factors obtained by a pathologic examination in completely resected non-small-cell lung cancer. An analysis in each pathologic stage. J Thorac Cardiovasc Surg 110: 601-605.
64. Sakai Y, Ohbayashi C, Kanomata N, Kajimoto K, Sakuma T, et al. (2011) Significance of microscopic invasion into hilar peribronchovascular soft tissue in resection specimens of primary non-small cell lung cancer. Lung Cancer 73: 89-95.
65. Kawachi R, Nakazato Y, Masui K, Takei H, Koshi-ishi Y, et al. (2009) Clinical significance of pleural lavage cytology for non-small cell lung cancer: is surgical resection valid for patients with positive pleural lavage cytology? Interact Cardiovasc Thorac Surg 9: 265-268.
66. Takanami I, (2005) The prognostic value of overexpression of Skp2 mRNA in non-small cell lung cancer. Oncol Rep 13: 727-731.
67. Okada M, Sakamoto T, Nishio W, Uchino K, Tsuboshima K, et al. (2003) Pleural lavage cytology in non-small cell lung cancer: lessons from 1000 consecutive resections. J Thorac Cardiovasc Surg 126: 1911-1915.
68. Matsuguma H, Nakahara R, Igarashi S, Ishikawa Y, Suzuki H, et al. (2008) Pathologic stage I non-small cell lung cancer with high levels of preoperative serum carcinoembryonic antigen: clinicopathologic characteristics and prognosis. J Thorac Cardiovasc Surg 135: 44-49.
69. Yoshida T, Tanaka S, Mogi A, Shitara Y, Kuwano H, (2004) The clinical significance of Cyclin B1 and Wee1 expression in non-small-cell lung cancer. Ann Oncol 15: 252-256.
70. Suzuki H, Kawaguchi T, Higuchi M, Shio Y, Fujiu K, et al. (2002) Expression of peanut agglutinin-binding carbohydrates correlates with nodal involvement in human lung adenocarcinoma. Cancer Lett 187: 215-221.
71. Hanahan D, Weinberg RA, (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674.
72. Kahn HJ, Marks A, (2002) A new monoclonal antibody, D2-40, for detection of lymphatic invasion in primary tumors. Lab Invest 82: 1255-1257.
73. Arigami T, Natsugoe S, Uenosono Y, Arima H, Mataki Y, et al. (2005) Lymphatic invasion using D2-40 monoclonal antibody and its relationship to lymph node micrometastasis in pN0 gastric cancer. Br J Cancer 93: 688-693.
74. Kaiserling E, (2004) Immunohistochemical identification of lymph vessels with D2-40 in diagnostic pathology. Pathologe 25: 362-374.
75. Ordonez NG, (2005) D2-40 and podoplanin are highly specific and sensitive immunohistochemical markers of epithelioid malignant mesothelioma. Hum Pathol 36: 372-380.
76. Van den Eynden GG, Van der Auwera I, Van Laere SJ, Colpaert CG, van Dam P, et al. (2006) Distinguishing blood and lymph vessel invasion in breast cancer: a prospective immunohistochemical study. Br J Cancer 94: 1643-1649.
77. Wang XL, Fang JP, Tang RY, Chen XM, (2010) Different significance between intratumoral and peritumoral lymphatic vessel density in gastric cancer: a retrospective study of 123 cases. BMC Cancer 10: 299.
78. Roma AA, Magi-Galluzzi C, Kral MA, Jin TT, Klein EA, et al. (2006) Peritumoral lymphatic invasion is associated with regional lymph node metastases in prostate adenocarcinoma. Mod Pathol 19: 392-398.
79. Zhou Q, Suzuki K, Anami Y, Oh S, Takamochi K, (2010) Clinicopathologic features in resected subcentimeter lung cancer-status of lymph node metastases. Interact Cardiovasc Thorac Surg 10: 53-57.
80. Padera TP, Kadambi A, di Tomaso E, Carreira CM, Brown EB, et al. (2002) Lymphatic metastasis in the absence of functional intratumor lymphatics. Science 296: 1883-1886.
81. Macchiarini P, Fontanini G, Hardin MJ, Chuanchieh H, Bigini D, et al. (1993) Blood vessel invasion by tumor cells predicts recurrence in completely resected T1 N0 M0 non-small-cell lung cancer. J Thorac Cardiovasc Surg 106: 80-89.