Skip to main content
Top
Published in: Breast Cancer Research 6/2000

01-12-2000 | Review

Molecular biology of breast cancer metastasis Clinical implications of experimental studies on metastatic inefficiency

Authors: Ann F Chambers, George N Naumov, Sharon A Vantyghem, Alan B Tuck

Published in: Breast Cancer Research | Issue 6/2000

Login to get access

Abstract

Recent technological advances have led to an increasing ability to detect isolated tumour cells and groups of tumour cells in patients' blood, lymph nodes or bone marrow. However, the clinical significance of these cells is unclear. Should they be considered as evidence of metastasis, necessitating aggressive treatment, or are they in some cases unrelated to clinical outcome? Quantitative experimental studies on the basic biology of metastatic inefficiency are providing clues that may help in understanding the significance of these cells. This understanding will be of use in guiding clinical studies to assess the significance of isolated tumour cells and micrometastases in cancer patients.
Literature
1.
go back to reference Pisani P, Parkin DM, Bray F, Ferlay J: Estimates of the worldwide mortality from 25 cancers in 1990. Int J Cancer. 1999, 83: 18-29. 10.1002/(SICI)1097-0215(1999)83:12+<18::AID-IJC5>3.0.CO;2-L.CrossRefPubMed Pisani P, Parkin DM, Bray F, Ferlay J: Estimates of the worldwide mortality from 25 cancers in 1990. Int J Cancer. 1999, 83: 18-29. 10.1002/(SICI)1097-0215(1999)83:12+<18::AID-IJC5>3.0.CO;2-L.CrossRefPubMed
2.
go back to reference Pisani P, Parkin DM, Bray F, Ferlay J: Erratum: estimates of the worldwide mortality from 25 cancers in 1990. Int J Cancer. 1999, 83: 870-873. 10.1002/(SICI)1097-0215(19991210)83:6<870::AID-IJC35>3.0.CO;2-9.CrossRefPubMed Pisani P, Parkin DM, Bray F, Ferlay J: Erratum: estimates of the worldwide mortality from 25 cancers in 1990. Int J Cancer. 1999, 83: 870-873. 10.1002/(SICI)1097-0215(19991210)83:6<870::AID-IJC35>3.0.CO;2-9.CrossRefPubMed
3.
go back to reference Funke I, Schraut W: Meta-analyses of studies on bone marrow micrometastases: an independent prognostic impact remains to be substantiated. J Clin Oncol. 1998, 16: 557-566., This is an important meta-analysis of the literature to date on the prognostic significance of isolated tumour cells in bone marrowPubMed Funke I, Schraut W: Meta-analyses of studies on bone marrow micrometastases: an independent prognostic impact remains to be substantiated. J Clin Oncol. 1998, 16: 557-566., This is an important meta-analysis of the literature to date on the prognostic significance of isolated tumour cells in bone marrowPubMed
4.
go back to reference Page DL, Anderson TJ, Carter BA: Minimal solid tumor involvement of regional and distant sites: when is a metastasis not a metastasis? [editorial]. Cancer. 1999, 86: 2589-2592. 10.1002/(SICI)1097-0142(19991215)86:12<2589::AID-CNCR1>3.3.CO;2-Z., This is an excellent editorial, which comments on [34] and discusses the clinical significance of micrometastases and isolated tumour cells.CrossRefPubMed Page DL, Anderson TJ, Carter BA: Minimal solid tumor involvement of regional and distant sites: when is a metastasis not a metastasis? [editorial]. Cancer. 1999, 86: 2589-2592. 10.1002/(SICI)1097-0142(19991215)86:12<2589::AID-CNCR1>3.3.CO;2-Z., This is an excellent editorial, which comments on [34] and discusses the clinical significance of micrometastases and isolated tumour cells.CrossRefPubMed
6.
go back to reference Tarin D, Vass AC, Kettlewell MG, Price JE: Absence of metastatic sequelae during long-term treatment of malignant ascites by peritoneo-venous shunting. A clinico-pathological report. Invasion Metastasis. 1984, 4: 1-12.PubMed Tarin D, Vass AC, Kettlewell MG, Price JE: Absence of metastatic sequelae during long-term treatment of malignant ascites by peritoneo-venous shunting. A clinico-pathological report. Invasion Metastasis. 1984, 4: 1-12.PubMed
7.
go back to reference Tarin D, Price JE, Kettlewell MG, Souter RG, Vass AC, Crossley B: Mechanisms of human tumor metastasis studied in patients with peritoneovenous shunts. Cancer Res. 1984, 44: 3584-3592.PubMed Tarin D, Price JE, Kettlewell MG, Souter RG, Vass AC, Crossley B: Mechanisms of human tumor metastasis studied in patients with peritoneovenous shunts. Cancer Res. 1984, 44: 3584-3592.PubMed
8.
go back to reference Fidler IJ: Metastasis: quantitative analysis of distribution and fate of tumor emboli labeled with 125I-5-iodo-2'-deoxyuridine. J Natl Cancer Inst. 1970, 45: 773-782.PubMed Fidler IJ: Metastasis: quantitative analysis of distribution and fate of tumor emboli labeled with 125I-5-iodo-2'-deoxyuridine. J Natl Cancer Inst. 1970, 45: 773-782.PubMed
9.
go back to reference Butler TP, Gullino PM: Quantitation of cell shedding into efferent blood of mammary adenocarcinoma. Cancer Res. 1975, 35: 512-516.PubMed Butler TP, Gullino PM: Quantitation of cell shedding into efferent blood of mammary adenocarcinoma. Cancer Res. 1975, 35: 512-516.PubMed
10.
go back to reference Liotta LA, Kleinerman J, Saidel GM: Quantitative relationships of intravascular tumor cells, tumor vessels, and pulmonary metastases following tumor implantation. Cancer Res. 1974, 34: 997-1004.PubMed Liotta LA, Kleinerman J, Saidel GM: Quantitative relationships of intravascular tumor cells, tumor vessels, and pulmonary metastases following tumor implantation. Cancer Res. 1974, 34: 997-1004.PubMed
11.
go back to reference Chambers AF, MacDonald IC, Schmidt EE, Koop S, Morris VL, Khokha R, Groom AC: Steps in tumor metastasis: new concepts from intravital videomicroscopy. Cancer Metastasis Rev. 1995, 14: 279-301.CrossRefPubMed Chambers AF, MacDonald IC, Schmidt EE, Koop S, Morris VL, Khokha R, Groom AC: Steps in tumor metastasis: new concepts from intravital videomicroscopy. Cancer Metastasis Rev. 1995, 14: 279-301.CrossRefPubMed
12.
go back to reference MacDonald IC, Schmidt EE, Morris V, Groom AC, Chambers AF: In vivo videomicroscopy of experimental hematogenous metastasis: cancer cell arrest, extravasation and migration. In: Motion Analysis of Living Cells. Edited by Soll DR, Wessels D. New York: John Wiley and Sons,. 1998, 263-287., This is a review of IVVM and cell ‘accounting’ procedures, with an especially technical focus MacDonald IC, Schmidt EE, Morris V, Groom AC, Chambers AF: In vivo videomicroscopy of experimental hematogenous metastasis: cancer cell arrest, extravasation and migration. In: Motion Analysis of Living Cells. Edited by Soll DR, Wessels D. New York: John Wiley and Sons,. 1998, 263-287., This is a review of IVVM and cell ‘accounting’ procedures, with an especially technical focus
13.
go back to reference Chambers AF, MacDonald IC, Schmidt EE, Morris VL, Groom AC: Pre-clinical assessment of anti-cancer therapeutic strategies using in vivo videomicroscopy. Cancer Metastasis Rev. 1999, 17: 263-269. 10.1023/A:1006136428254.CrossRef Chambers AF, MacDonald IC, Schmidt EE, Morris VL, Groom AC: Pre-clinical assessment of anti-cancer therapeutic strategies using in vivo videomicroscopy. Cancer Metastasis Rev. 1999, 17: 263-269. 10.1023/A:1006136428254.CrossRef
14.
go back to reference Chambers AF: The metastatic process: basic research and clinical implications. Oncol Res. 1999, 11: 161-168.PubMed Chambers AF: The metastatic process: basic research and clinical implications. Oncol Res. 1999, 11: 161-168.PubMed
15.
go back to reference Chambers AF, MacDonald IC, Schmidt EE, Morris VL, Groom AC: Clinical targets for anti-metastasis therapy. Adv Cancer Res. 2000, 79: 91-121., This is an extensive review of findings to date using IVVM and cell ‘accounting’ procedures to clarify the metastatic processCrossRefPubMed Chambers AF, MacDonald IC, Schmidt EE, Morris VL, Groom AC: Clinical targets for anti-metastasis therapy. Adv Cancer Res. 2000, 79: 91-121., This is an extensive review of findings to date using IVVM and cell ‘accounting’ procedures to clarify the metastatic processCrossRefPubMed
16.
go back to reference Koop S, MacDonald IC, Luzzi K, Schmidt EE, Morris VL, Grattan M, Khokha R, Chambers AF, Groom AC: Fate of melanoma cells entering the microcirculation: over 80% survive and extravasate. Cancer Res . 1995, 55: 2520-2523.PubMed Koop S, MacDonald IC, Luzzi K, Schmidt EE, Morris VL, Grattan M, Khokha R, Chambers AF, Groom AC: Fate of melanoma cells entering the microcirculation: over 80% survive and extravasate. Cancer Res . 1995, 55: 2520-2523.PubMed
17.
go back to reference Luzzi KJ, MacDonald IC, Schmidt EE, Kerkvliet N, Morris VL, Chambers AC, Groom AC: Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation, and limited survival of early micrometastases. Am J Pathol. 1998, 153: 865-873.CrossRefPubMedPubMedCentral Luzzi KJ, MacDonald IC, Schmidt EE, Kerkvliet N, Morris VL, Chambers AC, Groom AC: Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation, and limited survival of early micrometastases. Am J Pathol. 1998, 153: 865-873.CrossRefPubMedPubMedCentral
18.
go back to reference Morris VL, MacDonald IC, Koop S, Schmidt EE, Chambers AF, Groom AC: Early interactions of cancer cells with the microvasculature in mouse liver and muscle during hematogenous metastasis: videomicroscopic analysis. Clin Exptl Metastasis. 1993, 11: 377-390.CrossRef Morris VL, MacDonald IC, Koop S, Schmidt EE, Chambers AF, Groom AC: Early interactions of cancer cells with the microvasculature in mouse liver and muscle during hematogenous metastasis: videomicroscopic analysis. Clin Exptl Metastasis. 1993, 11: 377-390.CrossRef
19.
go back to reference Morris VL, Koop S, MacDonald IC, Schmidt EE, Grattan M, Percy D, Chambers AF, Groom AC: Mammary carcinoma cell lines of high and low metastatic potential differ not in extravasation but in subsequent migration and growth. Clin Exptl Metastasis. 1994, 12: 357-367.CrossRef Morris VL, Koop S, MacDonald IC, Schmidt EE, Grattan M, Percy D, Chambers AF, Groom AC: Mammary carcinoma cell lines of high and low metastatic potential differ not in extravasation but in subsequent migration and growth. Clin Exptl Metastasis. 1994, 12: 357-367.CrossRef
20.
go back to reference Naumov GN, Wilson SM, MacDonald IC, Schmidt EE, Morris VL, Groom AC, Hoffman RM, Chambers AF: Cellular expression of green fluorescent protein, coupled with high-resolution in vivo videomicroscopy, to monitor steps in tumor metastasis. J Cell Sci. 1999, 112: 1835-1842.PubMed Naumov GN, Wilson SM, MacDonald IC, Schmidt EE, Morris VL, Groom AC, Hoffman RM, Chambers AF: Cellular expression of green fluorescent protein, coupled with high-resolution in vivo videomicroscopy, to monitor steps in tumor metastasis. J Cell Sci. 1999, 112: 1835-1842.PubMed
21.
go back to reference Farina KL, Wyckoff JB, Rivera J, Lee H, Segall JE, Condeelis JS, Jones JG: Cell motility of tumor cells visualized in living intact primary tumors using green fluorescent protein. Cancer Res. 1998, 58: 2528-2532.PubMed Farina KL, Wyckoff JB, Rivera J, Lee H, Segall JE, Condeelis JS, Jones JG: Cell motility of tumor cells visualized in living intact primary tumors using green fluorescent protein. Cancer Res. 1998, 58: 2528-2532.PubMed
22.
go back to reference Sckell A, Safabakhsh N, Dellian M, Jain RK: Primary tumor size-dependent inhibition of angiogenesis at a secondary site: an intravital microscopic study in mice. Cancer Res. 1998, 58: 5866-5869.PubMed Sckell A, Safabakhsh N, Dellian M, Jain RK: Primary tumor size-dependent inhibition of angiogenesis at a secondary site: an intravital microscopic study in mice. Cancer Res. 1998, 58: 5866-5869.PubMed
23.
go back to reference Scherbarth S, Orr FW: Intravital videomicroscopic evidence for regulation of metastasis by the hepatic microvasculature: effects of interleukin-1α on metastasis and the location of B16F1 melanoma cell arrest. Cancer Res. 1997, 57: 4105-4110.PubMed Scherbarth S, Orr FW: Intravital videomicroscopic evidence for regulation of metastasis by the hepatic microvasculature: effects of interleukin-1α on metastasis and the location of B16F1 melanoma cell arrest. Cancer Res. 1997, 57: 4105-4110.PubMed
24.
go back to reference Talmadge JE, Wolman SR, Fidler IJ: Evidence for the clonal origin of spontaneous metastases. Science. 1982, 217: 361-363.CrossRefPubMed Talmadge JE, Wolman SR, Fidler IJ: Evidence for the clonal origin of spontaneous metastases. Science. 1982, 217: 361-363.CrossRefPubMed
25.
go back to reference Chambers AF, Wilson S: Use of NeoR B16F1 murine melanoma cells to assess clonality of experimental metastases in the immune-deficient chick embryo. Clin Exptl Metastasis. 1982, 6: 171-182.CrossRef Chambers AF, Wilson S: Use of NeoR B16F1 murine melanoma cells to assess clonality of experimental metastases in the immune-deficient chick embryo. Clin Exptl Metastasis. 1982, 6: 171-182.CrossRef
26.
go back to reference Koop S, Schmidt EE, MacDonald IC, Morris VL, Khokha R, Grattan M, Leone J, Chambers AF, Groom AC: Independence of metastatic ability and extravasation: metastatic ras-transformed and control fibroblasts extravasate equally well. Proc Natl Acad Sci USA. 1996, 93: 11080-11084. 10.1073/pnas.93.20.11080.CrossRefPubMedPubMedCentral Koop S, Schmidt EE, MacDonald IC, Morris VL, Khokha R, Grattan M, Leone J, Chambers AF, Groom AC: Independence of metastatic ability and extravasation: metastatic ras-transformed and control fibroblasts extravasate equally well. Proc Natl Acad Sci USA. 1996, 93: 11080-11084. 10.1073/pnas.93.20.11080.CrossRefPubMedPubMedCentral
27.
go back to reference Welch DR: Technical considerations for studying cancer metastasis in vivo. Clin Exp Metastasis . 1997, 15: 272-301. 10.1023/A:1018477516367., This is an excellent and comprehensive review on experimental methods used to study tumour metastasisCrossRefPubMed Welch DR: Technical considerations for studying cancer metastasis in vivo. Clin Exp Metastasis . 1997, 15: 272-301. 10.1023/A:1018477516367., This is an excellent and comprehensive review on experimental methods used to study tumour metastasisCrossRefPubMed
28.
go back to reference Cameron MD, Schmidt EE, Kerkvliet N, Nadkarni KV, Morris VL, Groom AC, Chambers AF, MacDonald IC: Temporal progression of metastasis in lung: cell survival, dormancy, and location dependence of metastatic inefficiency. Cancer Res. 2000, 60: 2541-2546.PubMed Cameron MD, Schmidt EE, Kerkvliet N, Nadkarni KV, Morris VL, Groom AC, Chambers AF, MacDonald IC: Temporal progression of metastasis in lung: cell survival, dormancy, and location dependence of metastatic inefficiency. Cancer Res. 2000, 60: 2541-2546.PubMed
29.
go back to reference Welch DR, Steeg PS, Rinker-Schaeffer CW: Molecular biology of breast cancer metastasis: genetic regulation of human breast carcinoma metastasis. Breast Cancer Res. 2000, 2: Welch DR, Steeg PS, Rinker-Schaeffer CW: Molecular biology of breast cancer metastasis: genetic regulation of human breast carcinoma metastasis. Breast Cancer Res. 2000, 2:
30.
go back to reference Chekmareva MA, Kadkhodaian MM, Hollowell CM, Kim H, Yoshida BA, Luu HH, Stadler WM, Rinker-Schaeffer CW: Chromosome 17-mediated dormancy of AT6.1 prostate cancer micrometastases. Cancer Res . 1998, 58: 4963-4969., This is an important study that demonstrates that a metastasis-suppressor gene functions by blocking growth of cells that successfully arrive at a secondary site.PubMed Chekmareva MA, Kadkhodaian MM, Hollowell CM, Kim H, Yoshida BA, Luu HH, Stadler WM, Rinker-Schaeffer CW: Chromosome 17-mediated dormancy of AT6.1 prostate cancer micrometastases. Cancer Res . 1998, 58: 4963-4969., This is an important study that demonstrates that a metastasis-suppressor gene functions by blocking growth of cells that successfully arrive at a secondary site.PubMed
31.
go back to reference Goldberg SF, Harms JF, Quon K, Welch DR: Metastasis-suppressed C8161 melanoma cell arrest in lung but fail to proliferate. Clin Exp Metastasis. 1999, 17: 601-617. 10.1023/A:1006718800891., This paper shows that a second, unrelated metastasis-suppressor gene also functions by blocking growth of cells that successfully arrive at a secondary site (see also [30])CrossRefPubMed Goldberg SF, Harms JF, Quon K, Welch DR: Metastasis-suppressed C8161 melanoma cell arrest in lung but fail to proliferate. Clin Exp Metastasis. 1999, 17: 601-617. 10.1023/A:1006718800891., This paper shows that a second, unrelated metastasis-suppressor gene also functions by blocking growth of cells that successfully arrive at a secondary site (see also [30])CrossRefPubMed
32.
go back to reference Wyckoff JB, Jones JG, Condeelis JS, Segall JE: A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res. 2000, 60: 2504-2511.PubMed Wyckoff JB, Jones JG, Condeelis JS, Segall JE: A critical step in metastasis: in vivo analysis of intravasation at the primary tumor. Cancer Res. 2000, 60: 2504-2511.PubMed
33.
go back to reference Swartz MA, Kristensen CA, Melder RJ, Roberge S, Calautti E, Fukumura D, Jain RK: Cells shed from tumours show reduced clonogenicity, resistance to apoptosis, and in vivo tumorigenicity. Br J Cancer. 1999, 81: 756-759. 10.1038/sj.bjc.6690760.CrossRefPubMedPubMedCentral Swartz MA, Kristensen CA, Melder RJ, Roberge S, Calautti E, Fukumura D, Jain RK: Cells shed from tumours show reduced clonogenicity, resistance to apoptosis, and in vivo tumorigenicity. Br J Cancer. 1999, 81: 756-759. 10.1038/sj.bjc.6690760.CrossRefPubMedPubMedCentral
34.
go back to reference Dowlatshahi K, Fan M, Bloom KJ, Spitz DJ, Patel S, Snider HC: Occult metastases in the sentinel lymph nodes of patients with early stage breast carcinoma: a preliminary study. Cancer. 1999, 86: 990-996. 10.1002/(SICI)1097-0142(19990915)86:6<990::AID-CNCR14>3.0.CO;2-D.CrossRefPubMed Dowlatshahi K, Fan M, Bloom KJ, Spitz DJ, Patel S, Snider HC: Occult metastases in the sentinel lymph nodes of patients with early stage breast carcinoma: a preliminary study. Cancer. 1999, 86: 990-996. 10.1002/(SICI)1097-0142(19990915)86:6<990::AID-CNCR14>3.0.CO;2-D.CrossRefPubMed
35.
go back to reference Allred DC, Elledge RM: Caution concerning micrometastatic breast carcinoma in sentinel lymph nodes [editorial]. Cancer. 1999, 86: 905-907. 10.1002/(SICI)1097-0142(19990915)86:6<905::AID-CNCR1>3.0.CO;2-K., A good editorial is presented, which comments on the significance of [34]CrossRefPubMed Allred DC, Elledge RM: Caution concerning micrometastatic breast carcinoma in sentinel lymph nodes [editorial]. Cancer. 1999, 86: 905-907. 10.1002/(SICI)1097-0142(19990915)86:6<905::AID-CNCR1>3.0.CO;2-K., A good editorial is presented, which comments on the significance of [34]CrossRefPubMed
36.
go back to reference Hermanek P, Hutter RV, Sobin LH, Wittekind C: Classification of isolated tumor cells and micrometastasis. Cancer. 1999, 86: 2668-2673. 10.1002/(SICI)1097-0142(19991215)86:12<2668::AID-CNCR11>3.0.CO;2-R., This paper identifies the need to consider isolated tumour cells separately from micrometastases, and establishes a working definition of a ‘micrometastasis’CrossRefPubMed Hermanek P, Hutter RV, Sobin LH, Wittekind C: Classification of isolated tumor cells and micrometastasis. Cancer. 1999, 86: 2668-2673. 10.1002/(SICI)1097-0142(19991215)86:12<2668::AID-CNCR11>3.0.CO;2-R., This paper identifies the need to consider isolated tumour cells separately from micrometastases, and establishes a working definition of a ‘micrometastasis’CrossRefPubMed
37.
go back to reference Racila E, Euhus D, Weiss AJ, Rao C, McConnell J, Terstappen LW, Uhr JW: Detection and characterization of carcinoma cells in the blood. Proc Natl Acad Sci USA. 1998, 95: 4589-4594. 10.1073/pnas.95.8.4589.CrossRefPubMedPubMedCentral Racila E, Euhus D, Weiss AJ, Rao C, McConnell J, Terstappen LW, Uhr JW: Detection and characterization of carcinoma cells in the blood. Proc Natl Acad Sci USA. 1998, 95: 4589-4594. 10.1073/pnas.95.8.4589.CrossRefPubMedPubMedCentral
38.
go back to reference Brown DC, Purushotham AD, Birnie GD, George WD: Detection of intraoperative tumor cell dissemination in patients with breast cancer by use of reverse transcription and polymerase chain reaction. Surgery . 1995, 117: 95-101.CrossRefPubMed Brown DC, Purushotham AD, Birnie GD, George WD: Detection of intraoperative tumor cell dissemination in patients with breast cancer by use of reverse transcription and polymerase chain reaction. Surgery . 1995, 117: 95-101.CrossRefPubMed
40.
go back to reference Mori M, Mimori K, Ueo H, Karimine N, Barnard GF, Sugimachi K, Akiyoshi T: Molecular detection of circulating solid carcinoma cells in the peripheral blood: the concept of early systemic disease. Int J Cancer. 1996, 68: 739-743. 10.1002/(SICI)1097-0215(19961211)68:6<739::AID-IJC8>3.3.CO;2-Q.CrossRefPubMed Mori M, Mimori K, Ueo H, Karimine N, Barnard GF, Sugimachi K, Akiyoshi T: Molecular detection of circulating solid carcinoma cells in the peripheral blood: the concept of early systemic disease. Int J Cancer. 1996, 68: 739-743. 10.1002/(SICI)1097-0215(19961211)68:6<739::AID-IJC8>3.3.CO;2-Q.CrossRefPubMed
41.
go back to reference Mori M, Mimori K, Ueo H, Tsuji K, Shiraishi T, Barnard GF, Sugimachi K, Akiyoshi T: Clinical significance of molecular detection of carcinoma cells in lymph nodes and peripheral blood by reverse transcription-polymerase chain reaction in patients with gastrointestinal or breast carcinomas. J Clin Oncol. 1998, 16: 128-132.PubMed Mori M, Mimori K, Ueo H, Tsuji K, Shiraishi T, Barnard GF, Sugimachi K, Akiyoshi T: Clinical significance of molecular detection of carcinoma cells in lymph nodes and peripheral blood by reverse transcription-polymerase chain reaction in patients with gastrointestinal or breast carcinomas. J Clin Oncol. 1998, 16: 128-132.PubMed
42.
go back to reference Golinger RC, Gregorio RM, Fisher ER: Tumor cells in venous blood draining mammary carcinomas. Arch Surg. 1977, 112: 707-708.CrossRefPubMed Golinger RC, Gregorio RM, Fisher ER: Tumor cells in venous blood draining mammary carcinomas. Arch Surg. 1977, 112: 707-708.CrossRefPubMed
43.
go back to reference Cady B: Lymph node metastases. Indicators, but not governors of survival. Arch Surg. 1984, 119: 1067-1072.CrossRefPubMed Cady B: Lymph node metastases. Indicators, but not governors of survival. Arch Surg. 1984, 119: 1067-1072.CrossRefPubMed
44.
go back to reference Jatoi I: Breast cancer: a systemic or local disease?. Am J Clin Oncol. 1997, 20: 536-539. 10.1097/00000421-199710000-00022.CrossRefPubMed Jatoi I: Breast cancer: a systemic or local disease?. Am J Clin Oncol. 1997, 20: 536-539. 10.1097/00000421-199710000-00022.CrossRefPubMed
Metadata
Title
Molecular biology of breast cancer metastasis Clinical implications of experimental studies on metastatic inefficiency
Authors
Ann F Chambers
George N Naumov
Sharon A Vantyghem
Alan B Tuck
Publication date
01-12-2000
Publisher
BioMed Central
Published in
Breast Cancer Research / Issue 6/2000
Electronic ISSN: 1465-542X
DOI
https://doi.org/10.1186/bcr86

Other articles of this Issue 6/2000

Breast Cancer Research 6/2000 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine