© 1992 by Oxford University Press
Journal of the National Cancer Institute, Vol. 84, No. 24, 1875-1887,
December 16, 1992
© 1992 Oxford University Press
Tumor Angiogenesis: A New Significant and Independent Prognostic Indicator in Early-Stage Breast Carcinoma
Department of Pathology, University of California San Francisco
Departments of Surgery and Anatomy and Cellular Biology, Children's Hospital, Harvard Medical School Boston, Mass
St. Bortolo Regional Medical Center Vicenza-Veneto, Italy
Statistical and Data Base Consulting Gardener House, Boston, Mass
Lawrence Livermore National Laboratory, University of California Livermore
*Correspondence to: Noel Weidner, M.D., Department of Pathology, University of California, San Francisco, Box 0102, San Francisco, CA 94143-0102.
Address reprint requests to: Giampietro Gasparini, M.D., Department of Oncology and Radiotherapy, St. Bortolo Regional Hospital, 36100 Vicenza, Italy.
Background: Axillary lymph node status has been the most important prognostic factor in operable breast carcinoma, but it does not fully account for the varied disease outcome. More accurate prognostic indicators would help in selection of patients at high risk for disease recurrence and death who are candidates for systemic adjuvant therapy. Our recent findings indicated that microvessel density (count or grade) in invasive breast carcinoma (a measure of tumor angiogenesis) is associated with metastasis and thus may be a prognostic indicator. Purpose: This study was designed to further define the relationship of microvessel density with overall and relapse-free survival and with other reported prognostic indicators in breast carcinoma. Methods: In a prospective, blinded study of 165 consecutive patients, the microvessels within primary invasive breast carcinoma were highlighted by immunocytochemical staining to detect factor VIII-related antigen. Using light micros copy, we counted microvessels per 200x field in the most active areas of neovascularization and graded microvessel density. These findings were correlated, by univariate and multivariate analyses, with overall and relapse-free survival, axillary node status, and other prognostic indicators (median follow-up, 51 months). Results: There was a highly significant (P
.001) association of microvessel density with overall survival and relapse-free survival in all patients, including node-negative and node-positive subsets. All patients with breast carcinomas having more than 100 microvessels per 200 x field experienced tumor recurrence within 33 months of diagnosis, compared with less than 5% of the patients with breast carcinoma having 33 or fewer microvessels per 200x field. Moreover, microvessel density was the only statistically significant predictor of overall survival among node-negative women (P<.001). Only microvessel density (P<.001) and histologic grade (P=.04) showed statistically significant correlations with relapse-free survival in the node-negative subset. Conclusions: Microvessel density in the area of the most intense neovascularization in invasive breast carcinoma is an independent and highly significant prognostic indicator for overall and relapse-free survival in patients with early-stage breast carcinoma (I or II by International Union Against Cancer criteria). Implications: Such an indicator would be useful in selection of those node-negative patients with breast carcinoma who are high risk for having occult metastasis at presentation. These patients could then be given systemic adjuvent therapy. [J Natl Cancer Inst 84:1875–1887, 1992]
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S. Fujioka, G. M. Sclabas, C. Schmidt, W. A. Frederick, Q. G. Dong, J. L. Abbruzzese, D. B. Evans, C. Baker, and P. J. Chiao Function of Nuclear Factor {kappa}B in Pancreatic Cancer Metastasis Clin. Cancer Res., January 1, 2003; 9(1): 346 - 354. [Abstract] [Full Text] [PDF]
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C. Bremer, M. Mustafa, A. Bogdanov Jr, V. Ntziachristos, A. Petrovsky, and R. Weissleder Steady-State Blood Volume Measurements in Experimental Tumors with Different Angiogenic Burdens--A Study in Mice Radiology, January 1, 2003; 226(1): 214 - 220. [Abstract] [Full Text] [PDF]
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O. Straume, P. O. Chappuis, H. B. Salvesen, O. J. Halvorsen, S. A. Haukaas, J. R. Goffin, L. R. Begin, W. D. Foulkes, and L. A. Akslen Prognostic Importance of Glomeruloid Microvascular Proliferation Indicates an Aggressive Angiogenic Phenotype in Human Cancers Cancer Res., December 1, 2002; 62(23): 6808 - 6811. [Abstract] [Full Text] [PDF]
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A J Rice, M A Steward, and C M Quinn Thrombospondin 1 protein expression relates to good prognostic indices in ductal carcinoma in situ of the breast J. Clin. Pathol., December 1, 2002; 55(12): 921 - 925. [Abstract] [Full Text] [PDF]
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C. Cohen, A. Zavala-Pompa, J. H. Sequeira, M. Shoji, D. G. Sexton, G. Cotsonis, F. Cerimele, B. Govindarajan, N. Macaron, and J. L. Arbiser Mitogen-actived Protein Kinase Activation Is an Early Event in Melanoma Progression Clin. Cancer Res., December 1, 2002; 8(12): 3728 - 3733. [Abstract] [Full Text] [PDF]
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N. J. McCarthy, X. Yang, I. R. Linnoila, M. J. Merino, S. M. Hewitt, A. L. Parr, S. Paik, S. M. Steinberg, D. P. Hartmann, N. Mourali, et al. Microvessel Density, Expression of Estrogen Receptor {alpha}, MIB-1, p53, and c-erbB-2 in Inflammatory Breast Cancer Clin. Cancer Res., December 1, 2002; 8(12): 3857 - 3862. [Abstract] [Full Text] [PDF]
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W. D. Fox, B. Higgins, K. M. Maiese, M. Drobnjak, C. Cordon-Cardo, H. I. Scher, and D. B. Agus Antibody to Vascular Endothelial Growth Factor Slows Growth of an Androgen-independent Xenograft Model of Prostate Cancer Clin. Cancer Res., October 1, 2002; 8(10): 3226 - 3231. [Abstract] [Full Text] [PDF]
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S. J. Welsh, W. T. Bellamy, M. M. Briehl, and G. Powis The Redox Protein Thioredoxin-1 (Trx-1) Increases Hypoxia-inducible Factor 1{alpha} Protein Expression: Trx-1 Overexpression Results in Increased Vascular Endothelial Growth Factor Production and Enhanced Tumor Angiogenesis Cancer Res., September 1, 2002; 62(17): 5089 - 5095. [Abstract] [Full Text] [PDF]
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 X. Chen, A. J. Maniotis, D. Majumdar, J. Pe'er, and R. Folberg Uveal Melanoma Cell Staining for CD34 and Assessment of Tumor Vascularity Invest. Ophthalmol. Vis. Sci., August 1, 2002; 43(8): 2533 - 2539. [Abstract] [Full Text] [PDF]
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P. A. Burke, S. J. DeNardo, L. A. Miers, K. R. Lamborn, S. Matzku, and G. L. DeNardo Cilengitide Targeting of {alpha}v{beta}3 Integrin Receptor Synergizes with Radioimmunotherapy to Increase Efficacy and Apoptosis in Breast Cancer Xenografts Cancer Res., August 1, 2002; 62(15): 4263 - 4272. [Abstract] [Full Text] [PDF]
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A Rice and C M Quinn Angiogenesis, thrombospondin, and ductal carcinoma in situ of the breast J. Clin. Pathol., August 1, 2002; 55(8): 569 - 574. [Abstract] [Full Text] [PDF]
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L. Hlatky, P. Hahnfeldt, and J. Folkman Clinical Application of Antiangiogenic Therapy: Microvessel Density, What It Does and Doesn't Tell Us J Natl Cancer Inst, June 19, 2002; 94(12): 883 - 893. [Full Text] [PDF]
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C Costa, R Soares, J S Reis-Filho, D Leitao, I Amendoeira, and F C Schmitt Cyclo-oxygenase 2 expression is associated with angiogenesis and lymph node metastasis in human breast cancer J. Clin. Pathol., June 1, 2002; 55(6): 429 - 434. [Abstract] [Full Text] [PDF]
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R. T.-P. Poon, I. O.-L. Ng, C. Lau, W.-C. Yu, Z.-F. Yang, S.-T. Fan, and J. Wong Tumor Microvessel Density as a Predictor of Recurrence After Resection of Hepatocellular Carcinoma: A Prospective Study J. Clin. Oncol., April 1, 2002; 20(7): 1775 - 1785. [Abstract] [Full Text] [PDF]
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J. L. Yu, J. W. Rak, G. Klement, and R. S. Kerbel Vascular Endothelial Growth Factor Isoform Expression as a Determinant of Blood Vessel Patterning in Human Melanoma Xenografts Cancer Res., March 1, 2002; 62(6): 1838 - 1846. [Abstract] [Full Text] [PDF]
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A. J. Guidi, D. A. Berry, G. Broadwater, B. Helmchen, I. J. Bleiweiss, D. R. Budman, I. C. Henderson, L. Norton, and D. F. Hayes Association of Angiogenesis and Disease Outcome in Node-Positive Breast Cancer Patients Treated With Adjuvant Cyclophosphamide, Doxorubicin, and Fluorouracil: A Cancer and Leukemia Group B Correlative Science Study From Protocols 8541/8869 J. Clin. Oncol., February 1, 2002; 20(3): 732 - 742. [Abstract] [Full Text] [PDF]
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R. Bos, J. J.M. van der Hoeven, E. van der Wall, P. van der Groep, P. J. van Diest, E. F.I. Comans, U. Joshi, G. L. Semenza, O. S. Hoekstra, A. A. Lammertsma, et al. Biologic Correlates of 18Fluorodeoxyglucose Uptake in Human Breast Cancer Measured by Positron Emission Tomography J. Clin. Oncol., January 15, 2002; 20(2): 379 - 387. [Abstract] [Full Text] [PDF]
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 S. J. Schnitt Traditional and Newer Pathologic Factors J Natl Cancer Inst Monographs, December 1, 2001; 2001(30): 22 - 26. [Abstract] [Full Text] [PDF]
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 Y. Hamma-Kourbali, R. Vassy, A. Starzec, V. Le Meuth-Metzinger, O. Oudar, R. Bagheri-Yarmand, G. Perret, and M. Crepin Vascular Endothelial Growth Factor 165 (VEGF165) Activities Are Inhibited by Carboxymethyl Benzylamide Dextran That Competes for Heparin Binding to VEGF165 and VEGF165{middle dot}KDR Complexes J. Biol. Chem., October 19, 2001; 276(43): 39748 - 39754. [Abstract] [Full Text] [PDF]
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 J. Xu, D. Rodriguez, E. Petitclerc, J. J. Kim, M. Hangai, S. M. Yuen, G. E. Davis, and P. C. Brooks Proteolytic exposure of a cryptic site within collagen type IV is required for angiogenesis and tumor growth in vivo J. Cell Biol., September 3, 2001; 154(5): 1069 - 1080. [Abstract] [Full Text] [PDF]
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W. T. Yang, C. Metreweli, P. K. W. Lam, and J. Chang Benign and Malignant Breast Masses and Axillary Nodes: Evaluation with Echo-enhanced Color Power Doppler US Radiology, September 1, 2001; 220(3): 795 - 802. [Abstract] [Full Text] [PDF]
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I. J. Fidler Angiogenic Heterogeneity: Regulation of Neoplastic Angiogenesis by the Organ Microenvironment J Natl Cancer Inst, July 18, 2001; 93(14): 1040 - 1041. [Full Text] [PDF]
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J. A. Foekens, H. A. Peters, N. Grebenchtchikov, M. P. Look, M. E. Meijer-van Gelder, A. Geurts-Moespot, T. H. van der Kwast, C. G. J. Sweep, and J. G. M. Klijn High Tumor Levels of Vascular Endothelial Growth Factor Predict Poor Response to Systemic Therapy in Advanced Breast Cancer Cancer Res., July 1, 2001; 61(14): 5407 - 5414. [Abstract] [Full Text] [PDF]
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 R. J Bing Myocardial ischemia and infarction: growth of ideas Cardiovasc Res, July 1, 2001; 51(1): 13 - 20. [Abstract] [Full Text] [PDF]
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 E. Laughner, P. Taghavi, K. Chiles, P. C. Mahon, and G. L. Semenza HER2 (neu) Signaling Increases the Rate of Hypoxia-Inducible Factor 1{alpha} (HIF-1{alpha}) Synthesis: Novel Mechanism for HIF-1-Mediated Vascular Endothelial Growth Factor Expression Mol. Cell. Biol., June 15, 2001; 21(12): 3995 - 4004. [Abstract] [Full Text]
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R. Bagheri-Yarmand, Y. Hamma-Kourbali, P. Bissieres, J.-F. Morere, and M. Crepin Carboxymethyl Benzylamide Dextran and Tamoxifen Combination Inhibits Tumor Growth and Angiogenesis Clin. Cancer Res., June 1, 2001; 7(6): 1805 - 1811. [Abstract] [Full Text] [PDF]
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M. S. Gee, H. M. Saunders, J. C. Lee, J. F. Sanzo, W. T. Jenkins, S. M. Evans, G. Trinchieri, C. M. Sehgal, M. D. Feldman, and W. M. F. Lee Doppler Ultrasound Imaging Detects Changes in Tumor Perfusion during Antivascular Therapy Associated with Vascular Anatomic Alterations Cancer Res., April 1, 2001; 61(7): 2974 - 2982. [Abstract] [Full Text]
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T. Etoh, H. Inoue, S. Tanaka, G. F. Barnard, S. Kitano, and M. Mori Angiopoietin-2 Is Related to Tumor Angiogenesis in Gastric Carcinoma: Possible in Vivo Regulation via Induction of Proteases Cancer Res., March 1, 2001; 61(5): 2145 - 2153. [Abstract] [Full Text]
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