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Association of Macrophage Infiltration with Angiogenesis and Prognosis in Invasive Breast Carcinoma¹

Imperial Cancer Research Fund Molecular Oncology Laboratory, University of Oxford Institute of Molecular Medicine [R.D.L., R.W., A.L.H.], Nuffield Department of Pathology and Bacteriology [R.D.L., C.E.L.], and Department of Surgery [M.G., J.C.], University of Oxford, John Radcliffe Hospital, Headington, Oxford OX3 9DU, England

Angiogenesis is a key process in tumor growth and metastasis and is a major independent prognostic factor in breast cancer. A range of cytokines stimulate the tumor neovasculature, and tumor-associated macrophages have been shown recently to produce several important angiogenic factors.

We have quantified macrophage infiltration using Chalkley count morphometry in a series of invasive breast carcinomas to investigate the relationship between tumor-associated macrophage infiltration and tumor angiogenesis, and prognosis. There was a significant positive correlation between high vascular grade and increased macrophage index (P = 0.03), and a strong relationship was observed between increased macrophage counts and reduced relapse-free survival (P = 0.006) and reduced overall survival (P = 0.004) as an independent prognostic variable. These data indicate a role for macrophages in angiogenesis and prognosis in breast cancer and that this cell type may represent an important target for immunoinhibitory therapy in breast cancer.

¹ This project was funded by the Imperial Cancer Research Fund, P. O. Box 123, Lincoln's Inn Fields, London WC2A 3PX, England.

² To whom requests for reprints should be addressed.

Received 8/ 7/96. Accepted 8/28/96.

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				S. Shimura, G. Yang, S. Ebara, T. M. Wheeler, A. Frolov, and T. C. Thompson Reduced Infiltration of Tumor-associated Macrophages in Human Prostate Cancer: Association with Cancer Progression Cancer Res., October 1, 2000; 60(20): 5857 - 5861. [Abstract] [Full Text]

				T. Etoh, K. Shibuta, G. F. Barnard, S. Kitano, and M. Mori Angiogenin Expression in Human Colorectal Cancer: The Role of Focal Macrophage Infiltration Clin. Cancer Res., September 1, 2000; 6(9): 3545 - 3551. [Abstract] [Full Text]

				J.-i. Fukushi, M. Ono, W. Morikawa, Y. Iwamoto, and M. Kuwano The Activity of Soluble VCAM-1 in Angiogenesis Stimulated by IL-4 and IL-13 J. Immunol., September 1, 2000; 165(5): 2818 - 2823. [Abstract] [Full Text] [PDF]

				K. L. Talks, H. Turley, K. C. Gatter, P. H. Maxwell, C. W. Pugh, P. J. Ratcliffe, and A. L. Harris The Expression and Distribution of the Hypoxia-Inducible Factors HIF-1{alpha} and HIF-2{alpha} in Normal Human Tissues, Cancers, and Tumor-Associated Macrophages Am. J. Pathol., August 1, 2000; 157(2): 411 - 421. [Abstract] [Full Text] [PDF]

				T. Ueno, M. Toi, H. Saji, M. Muta, H. Bando, K. Kuroi, M. Koike, H. Inadera, and K. Matsushima Significance of Macrophage Chemoattractant Protein-1 in Macrophage Recruitment, Angiogenesis, and Survival in Human Breast Cancer Clin. Cancer Res., August 1, 2000; 6(8): 3282 - 3289. [Abstract] [Full Text]

				J. Fujimoto, H. Sakaguchi, I. Aoki, and T. Tamaya Clinical Implications of Expression of Interleukin 8 Related to Angiogenesis in Uterine Cervical Cancers Cancer Res., May 1, 2000; 60(10): 2632 - 2635. [Abstract] [Full Text]

				A.-K. Eerola, Y. Soini, and P. Paakko A High Number of Tumor-infiltrating Lymphocytes Are Associated with a Small Tumor Size, Low Tumor Stage, and a Favorable Prognosis in Operated Small Cell Lung Carcinoma Clin. Cancer Res., May 1, 2000; 6(5): 1875 - 1881. [Abstract] [Full Text] [PDF]

				P. Nangia-Makker, Y. Honjo, R. Sarvis, S. Akahani, V. Hogan, K. J. Pienta, and A. Raz Galectin-3 Induces Endothelial Cell Morphogenesis and Angiogenesis Am. J. Pathol., March 1, 2000; 156(3): 899 - 909. [Abstract] [Full Text] [PDF]

				M. G. Manfredi, S. Lim, K. P. Claffey, and T. N. Seyfried Gangliosides Influence Angiogenesis in an Experimental Mouse Brain Tumor Cancer Res., October 1, 1999; 59(20): 5392 - 5397. [Abstract] [Full Text] [PDF]

				G. Luboshits, S. Shina, O. Kaplan, S. Engelberg, D. Nass, B. Lifshitz-Mercer, S. Chaitchik, I. Keydar, and A. Ben-Baruch Elevated Expression of the CC Chemokine Regulated on Activation, Normal T Cell Expressed and Secreted (RANTES) in Advanced Breast Carcinoma Cancer Res., September 1, 1999; 59(18): 4681 - 4687. [Abstract] [Full Text] [PDF]

				M. Vasse, J. Pourtau, V. Trochon, M. Muraine, J.-P. Vannier, H. Lu, J. Soria, and C. Soria Oncostatin M Induces Angiogenesis In Vitro and In Vivo Arterioscler Thromb Vasc Biol, August 1, 1999; 19(8): 1835 - 1842. [Abstract] [Full Text] [PDF]

				A. Nishie, M. Ono, T. Shono, J. Fukushi, M. Otsubo, H. Onoue, Y. Ito, T. Inamura, K. Ikezaki, M. Fukui, et al. Macrophage Infiltration and Heme Oxygenase-1 Expression Correlate with Angiogenesis in Human Gliomas Clin. Cancer Res., May 1, 1999; 5(5): 1107 - 1113. [Abstract] [Full Text] [PDF]

				M. Toi, T. Ueno, H. Matsumoto, H. Saji, N. Funata, M. Koike, and T. Tominaga Significance of Thymidine Phosphorylase as a Marker of Protumor Monocytes in Breast Cancer Clin. Cancer Res., May 1, 1999; 5(5): 1131 - 1137. [Abstract] [Full Text] [PDF]

				J. A. Ecsedy, H. C. Yohe, A. J. Bergeron, and T. N. Seyfried Tumor-infiltrating macrophages influence the glycosphingolipid composition of murine brain tumors J. Lipid Res., November 1, 1998; 39(11): 2218 - 2227. [Abstract] [Full Text]

				M. J. Reed and A. Purohit Breast Cancer and the Role of Cytokines in Regulating Estrogen Synthesis: An Emerging Hypothesis Endocr. Rev., October 1, 1997; 18(5): 701 - 715. [Abstract] [Full Text]