Skip to main content
Top
Published in: Clinical & Experimental Metastasis 5-6/2018

01-08-2018 | Research Paper

Breast cancer metastasis through the lympho-vascular system

Authors: S. David Nathanson, David Krag, Henry M. Kuerer, Lisa A. Newman, Markus Brown, Dontscho Kerjaschki, Ethel R. Pereira, Timothy P. Padera

Published in: Clinical & Experimental Metastasis | Issue 5-6/2018

Login to get access

Abstract

Breast cancer metastasizes through the lymphovascular system to the regional lymph nodes in the axilla and to both visceral and non-visceral sites. Renewed interest in the route by which tumor cells gain access to blood and lymphatic capillaries are the subject of research at mechanical, anatomic, pathologic, genetic, epidemiologic and molecular levels. Two papers presented at the 7th International Symposium on Cancer Metastasis in San Francisco showed tumor cells entering the systemic circulation through the sentinel lymph node. This information challenges the current paradigm where clinicians believe that access is gained through intra- and peri-tumoral blood vessels and that metastasis to axillary lymph nodes is an interesting epi-phenomenon. The sentinel lymph node era has changed the modern surgical approach to the axilla and the basis of this change is summarized in this paper. A new approach to the management of axillary metastases after systemic therapy relies on determining whether there is a complete pathologic response; if no tumor is found in the previously biopsied node, a complete axillary lymph node dissection may be avoided. African American women seem to inherit a trait from West African ancestors and tend to develop more lethal types of breast cancer. These tumors may have a molecular machinery that enhances their ability to metastasize to visceral sites and future research may unearth the mechanisms for this phenomenon.
Literature
1.
go back to reference Virchow R (1860) Cellular pathology: as based upon physiological and pathological histology, twenty lectures delivered in the Pathological Institute of Berlin during the months of February, March and April, 1858. John Churchill, London Virchow R (1860) Cellular pathology: as based upon physiological and pathological histology, twenty lectures delivered in the Pathological Institute of Berlin during the months of February, March and April, 1858. John Churchill, London
2.
go back to reference Halsted WS (1894) I. The results of operations for the cure of cancer of the breast performed at the Johns Hopkins Hospital from June, 1889, to January, 1894. Ann Surg 20:497–555CrossRef Halsted WS (1894) I. The results of operations for the cure of cancer of the breast performed at the Johns Hopkins Hospital from June, 1889, to January, 1894. Ann Surg 20:497–555CrossRef
3.
go back to reference Fisher B (1980) Laboratory and clinical research in breast cancer–a personal adventure: the David A. Karnofsky memorial lecture. Cancer Res 40:3863–3874 Fisher B (1980) Laboratory and clinical research in breast cancer–a personal adventure: the David A. Karnofsky memorial lecture. Cancer Res 40:3863–3874
4.
go back to reference Folkman J (1974) Tumor angiogenesis factor. Cancer Res 34:2109–2113 Folkman J (1974) Tumor angiogenesis factor. Cancer Res 34:2109–2113
5.
go back to reference Mohammed RA et al (2007) Improved methods of detection of lymphovascular invasion demonstrate that it is the predominant method of vascular invasion in breast cancer and has important clinical consequences. Am J Surg Pathol 31:1825–1833CrossRef Mohammed RA et al (2007) Improved methods of detection of lymphovascular invasion demonstrate that it is the predominant method of vascular invasion in breast cancer and has important clinical consequences. Am J Surg Pathol 31:1825–1833CrossRef
6.
go back to reference Nathanson SD et al (2009) The role of lymph node metastasis in the systemic dissemination of breast cancer. Ann Surg Oncol 16:3396–3405CrossRef Nathanson SD et al (2009) The role of lymph node metastasis in the systemic dissemination of breast cancer. Ann Surg Oncol 16:3396–3405CrossRef
7.
go back to reference Hoshida T et al (2006) Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications. Cancer Res 66:8065–8075CrossRef Hoshida T et al (2006) Imaging steps of lymphatic metastasis reveals that vascular endothelial growth factor-C increases metastasis by increasing delivery of cancer cells to lymph nodes: therapeutic implications. Cancer Res 66:8065–8075CrossRef
8.
go back to reference Stacker SA et al (2014) Lymphangiogenesis and lymphatic vessel remodelling in cancer. Nat Rev Cancer 14:159–172CrossRef Stacker SA et al (2014) Lymphangiogenesis and lymphatic vessel remodelling in cancer. Nat Rev Cancer 14:159–172CrossRef
9.
go back to reference Pereira ER et al (2018) Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice. Science 359:1403–1407CrossRef Pereira ER et al (2018) Lymph node metastases can invade local blood vessels, exit the node, and colonize distant organs in mice. Science 359:1403–1407CrossRef
10.
go back to reference Brown M et al (2018) Lymph node blood vessels provide exit routes for metastatic tumor cell dissemination in mice. Science 359:1408–1411CrossRef Brown M et al (2018) Lymph node blood vessels provide exit routes for metastatic tumor cell dissemination in mice. Science 359:1408–1411CrossRef
11.
go back to reference Naxerova K et al (2017) Origins of lymphatic and distant metastases in human colorectal cancer. Science 357:55–60CrossRef Naxerova K et al (2017) Origins of lymphatic and distant metastases in human colorectal cancer. Science 357:55–60CrossRef
12.
go back to reference Quiet CA et al (1995) Natural history of node-negative breast cancer: a study of 826 patients with long-term follow-up. J Clin Oncol 13:1144–1151CrossRef Quiet CA et al (1995) Natural history of node-negative breast cancer: a study of 826 patients with long-term follow-up. J Clin Oncol 13:1144–1151CrossRef
13.
go back to reference Giuliano AE et al (1994) Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 220:391–398; discussion 398–401CrossRef Giuliano AE et al (1994) Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 220:391–398; discussion 398–401CrossRef
14.
go back to reference Krag DN et al (1993) Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol 2:335–339; discussion 340CrossRef Krag DN et al (1993) Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol 2:335–339; discussion 340CrossRef
15.
go back to reference Giuliano AE et al (2011) Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 305:569–575CrossRef Giuliano AE et al (2011) Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 305:569–575CrossRef
16.
go back to reference Lyman GH et al (2005) American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol 23:7703–7720CrossRef Lyman GH et al (2005) American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol 23:7703–7720CrossRef
17.
go back to reference Lyman GH et al (2014) Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol 32:1365–1383CrossRef Lyman GH et al (2014) Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol 32:1365–1383CrossRef
18.
go back to reference Lyman GH (2015) Appropriate role for sentinel node biopsy after neoadjuvant chemotherapy in patients with early-stage breast cancer. J Clin Oncol 33:232–234CrossRef Lyman GH (2015) Appropriate role for sentinel node biopsy after neoadjuvant chemotherapy in patients with early-stage breast cancer. J Clin Oncol 33:232–234CrossRef
19.
go back to reference Mamounas EP et al (2005) Sentinel node biopsy after neoadjuvant chemotherapy in breast cancer: results from National Surgical Adjuvant Breast and Bowel Project Protocol B-27. J Clin Oncol 23:2694–2702CrossRef Mamounas EP et al (2005) Sentinel node biopsy after neoadjuvant chemotherapy in breast cancer: results from National Surgical Adjuvant Breast and Bowel Project Protocol B-27. J Clin Oncol 23:2694–2702CrossRef
20.
go back to reference Nathanson SD et al (2007) Preoperative identification of the sentinel lymph node in breast cancer. Ann Surg Oncol 14:3102–3110CrossRef Nathanson SD et al (2007) Preoperative identification of the sentinel lymph node in breast cancer. Ann Surg Oncol 14:3102–3110CrossRef
21.
go back to reference Caudle AS et al (2016) Improved axillary evaluation following neoadjuvant therapy for patients with node-positive breast cancer using selective evaluation of clipped nodes: implementation of targeted axillary dissection. J Clin Oncol 34:1072–1078CrossRef Caudle AS et al (2016) Improved axillary evaluation following neoadjuvant therapy for patients with node-positive breast cancer using selective evaluation of clipped nodes: implementation of targeted axillary dissection. J Clin Oncol 34:1072–1078CrossRef
22.
go back to reference Boughey JC et al (2013) Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA 310:1455–1461CrossRef Boughey JC et al (2013) Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA 310:1455–1461CrossRef
23.
go back to reference Barrio AV et al (2016) How often is treatment effect identified in axillary nodes with a pathologic complete response after neoadjuvant chemotherapy? Ann Surg Oncol 23:3475–3480CrossRef Barrio AV et al (2016) How often is treatment effect identified in axillary nodes with a pathologic complete response after neoadjuvant chemotherapy? Ann Surg Oncol 23:3475–3480CrossRef
24.
go back to reference Shah R et al (2015) The association amongst ‘triple negative’ breast cancers, lymph node metastasis, disease free and overall survival. J Cancer Sci 2:5 Shah R et al (2015) The association amongst ‘triple negative’ breast cancers, lymph node metastasis, disease free and overall survival. J Cancer Sci 2:5
25.
go back to reference Krag D et al (1998) The sentinel node in breast cancer–a multicenter validation study. N Engl J Med 339:941–946CrossRef Krag D et al (1998) The sentinel node in breast cancer–a multicenter validation study. N Engl J Med 339:941–946CrossRef
26.
go back to reference Krag DN et al (2009) Surgeon training, protocol compliance, and technical outcomes from breast cancer sentinel lymph node randomized trial. J Natl Cancer Inst 101:1356–1362CrossRef Krag DN et al (2009) Surgeon training, protocol compliance, and technical outcomes from breast cancer sentinel lymph node randomized trial. J Natl Cancer Inst 101:1356–1362CrossRef
27.
go back to reference Krag DN et al (2010) Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol 11:927–933CrossRef Krag DN et al (2010) Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol 11:927–933CrossRef
28.
go back to reference Giuliano AE et al (2016) Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: long-term follow-up from the American College of Surgeons Oncology Group (Alliance) ACOSOG Z0011 randomized trial. Ann Surg 264:413–420CrossRef Giuliano AE et al (2016) Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: long-term follow-up from the American College of Surgeons Oncology Group (Alliance) ACOSOG Z0011 randomized trial. Ann Surg 264:413–420CrossRef
29.
go back to reference Galimberti V et al (2013) Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23 – 01): a phase 3 randomised controlled trial. Lancet Oncol 14:297–305CrossRef Galimberti V et al (2013) Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23 – 01): a phase 3 randomised controlled trial. Lancet Oncol 14:297–305CrossRef
30.
go back to reference Sola M et al (2013) Complete axillary lymph node dissection versus clinical follow-up in breast cancer patients with sentinel node micrometastasis: final results from the multicenter clinical trial AATRM 048/13/2000. Ann Surg Oncol 20:120–127CrossRef Sola M et al (2013) Complete axillary lymph node dissection versus clinical follow-up in breast cancer patients with sentinel node micrometastasis: final results from the multicenter clinical trial AATRM 048/13/2000. Ann Surg Oncol 20:120–127CrossRef
31.
go back to reference Zavagno G et al (2008) A Randomized clinical trial on sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer: results of the Sentinella/GIVOM trial. Ann Surg 247:207–213CrossRef Zavagno G et al (2008) A Randomized clinical trial on sentinel lymph node biopsy versus axillary lymph node dissection in breast cancer: results of the Sentinella/GIVOM trial. Ann Surg 247:207–213CrossRef
32.
go back to reference Canavese G et al (2016) Sentinel lymph node biopsy versus axillary dissection in node-negative early-stage breast cancer: 15-year follow-up update of a randomized clinical trial. Ann Surg Oncol 23:2494–2500CrossRef Canavese G et al (2016) Sentinel lymph node biopsy versus axillary dissection in node-negative early-stage breast cancer: 15-year follow-up update of a randomized clinical trial. Ann Surg Oncol 23:2494–2500CrossRef
33.
go back to reference Robertson JF et al (2017) Treatment of the axilla in patients with primary breast cancer and low burden axillary disease: Limitations of the evidence from randomised controlled trials. Crit Rev Oncol Hematol 110:74–80CrossRef Robertson JF et al (2017) Treatment of the axilla in patients with primary breast cancer and low burden axillary disease: Limitations of the evidence from randomised controlled trials. Crit Rev Oncol Hematol 110:74–80CrossRef
35.
go back to reference Tsao MW et al (2016) A population-based study of the effects of a regional guideline for completion axillary lymph node dissection on axillary surgery in patients with breast cancer. Ann Surg Oncol 23:3354–3364CrossRef Tsao MW et al (2016) A population-based study of the effects of a regional guideline for completion axillary lymph node dissection on axillary surgery in patients with breast cancer. Ann Surg Oncol 23:3354–3364CrossRef
36.
go back to reference van la Parra RF, Kuerer HM (2016) Selective elimination of breast cancer surgery in exceptional responders: historical perspective and current trials. Breast Cancer Res 18:28CrossRef van la Parra RF, Kuerer HM (2016) Selective elimination of breast cancer surgery in exceptional responders: historical perspective and current trials. Breast Cancer Res 18:28CrossRef
37.
go back to reference Fisher B et al (1998) Effect of preoperative chemotherapy on the outcome of women with operable breast cancer. J Clin Oncol 16:2672–2685CrossRef Fisher B et al (1998) Effect of preoperative chemotherapy on the outcome of women with operable breast cancer. J Clin Oncol 16:2672–2685CrossRef
38.
go back to reference Kuerer HM et al (1999) Clinical course of breast cancer patients with complete pathologic primary tumor and axillary lymph node response to doxorubicin-based neoadjuvant chemotherapy. J Clin Oncol 17:460–469CrossRef Kuerer HM et al (1999) Clinical course of breast cancer patients with complete pathologic primary tumor and axillary lymph node response to doxorubicin-based neoadjuvant chemotherapy. J Clin Oncol 17:460–469CrossRef
39.
go back to reference Kuerer HM et al (1999) Incidence and impact of documented eradication of breast cancer axillary lymph node metastases before surgery in patients treated with neoadjuvant chemotherapy. Ann Surg 230:72–78CrossRef Kuerer HM et al (1999) Incidence and impact of documented eradication of breast cancer axillary lymph node metastases before surgery in patients treated with neoadjuvant chemotherapy. Ann Surg 230:72–78CrossRef
40.
go back to reference Dominici LS et al (2010) Cytologically proven axillary lymph node metastases are eradicated in patients receiving preoperative chemotherapy with concurrent trastuzumab for HER2-positive breast cancer. Cancer 116:2884–2889CrossRef Dominici LS et al (2010) Cytologically proven axillary lymph node metastases are eradicated in patients receiving preoperative chemotherapy with concurrent trastuzumab for HER2-positive breast cancer. Cancer 116:2884–2889CrossRef
41.
go back to reference Shen J et al (2007) Feasibility and accuracy of sentinel lymph node biopsy after preoperative chemotherapy in breast cancer patients with documented axillary metastases. Cancer 109:1255–1263CrossRef Shen J et al (2007) Feasibility and accuracy of sentinel lymph node biopsy after preoperative chemotherapy in breast cancer patients with documented axillary metastases. Cancer 109:1255–1263CrossRef
42.
go back to reference Alvarado R et al (2012) The role for sentinel lymph node dissection after neoadjuvant chemotherapy in patients who present with node-positive breast cancer. Ann Surg Oncol 19:3177–3184CrossRef Alvarado R et al (2012) The role for sentinel lymph node dissection after neoadjuvant chemotherapy in patients who present with node-positive breast cancer. Ann Surg Oncol 19:3177–3184CrossRef
43.
go back to reference Boileau JF et al (2015) Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: the SN FNAC study. J Clin Oncol 33:258–264CrossRef Boileau JF et al (2015) Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: the SN FNAC study. J Clin Oncol 33:258–264CrossRef
44.
go back to reference Caudle AS, Kuerer HM (2015) Targeting and limiting surgery for patients with node-positive breast cancer. BMC Med 13:149CrossRef Caudle AS, Kuerer HM (2015) Targeting and limiting surgery for patients with node-positive breast cancer. BMC Med 13:149CrossRef
45.
go back to reference Kuehn T et al (2013) Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): a prospective, multicentre cohort study. Lancet Oncol 14:609–618CrossRef Kuehn T et al (2013) Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): a prospective, multicentre cohort study. Lancet Oncol 14:609–618CrossRef
46.
go back to reference Caudle AS et al (2015) Selective surgical localization of axillary lymph nodes containing metastases in patients with breast cancer: a prospective feasibility trial. JAMA Surg 150:137–143CrossRef Caudle AS et al (2015) Selective surgical localization of axillary lymph nodes containing metastases in patients with breast cancer: a prospective feasibility trial. JAMA Surg 150:137–143CrossRef
47.
go back to reference Donker M et al (2015) Marking axillary lymph nodes with radioactive iodine seeds for axillary staging after neoadjuvant systemic treatment in breast cancer patients: the MARI procedure. Ann Surg 261:378–382CrossRef Donker M et al (2015) Marking axillary lymph nodes with radioactive iodine seeds for axillary staging after neoadjuvant systemic treatment in breast cancer patients: the MARI procedure. Ann Surg 261:378–382CrossRef
48.
go back to reference Choy N et al (2015) Initial results with preoperative tattooing of biopsied axillary lymph nodes and correlation to sentinel lymph nodes in breast cancer patients. Ann Surg Oncol 22:377–382CrossRef Choy N et al (2015) Initial results with preoperative tattooing of biopsied axillary lymph nodes and correlation to sentinel lymph nodes in breast cancer patients. Ann Surg Oncol 22:377–382CrossRef
49.
go back to reference Plecha D et al (2015) Improving the accuracy of axillary lymph node surgery in breast cancer with ultrasound-guided wire localization of biopsy proven metastatic lymph nodes. Ann Surg Oncol 22:4241–4246CrossRef Plecha D et al (2015) Improving the accuracy of axillary lymph node surgery in breast cancer with ultrasound-guided wire localization of biopsy proven metastatic lymph nodes. Ann Surg Oncol 22:4241–4246CrossRef
50.
go back to reference Diego EJ et al (2016) Axillary staging after neoadjuvant chemotherapy for breast cancer: a pilot study combining sentinel lymph node biopsy with radioactive seed localization of pre-treatment positive axillary lymph nodes. Ann Surg Oncol 23:1549–1553CrossRef Diego EJ et al (2016) Axillary staging after neoadjuvant chemotherapy for breast cancer: a pilot study combining sentinel lymph node biopsy with radioactive seed localization of pre-treatment positive axillary lymph nodes. Ann Surg Oncol 23:1549–1553CrossRef
51.
go back to reference Caudle AS et al (2017) Use of sentinel lymph node dissection after neoadjuvant chemotherapy in patients with node-positive breast cancer at diagnosis: practice patterns of American Society of Breast Surgeons members. Ann Surg Oncol 24:2925–2934CrossRef Caudle AS et al (2017) Use of sentinel lymph node dissection after neoadjuvant chemotherapy in patients with node-positive breast cancer at diagnosis: practice patterns of American Society of Breast Surgeons members. Ann Surg Oncol 24:2925–2934CrossRef
52.
go back to reference Brown AS et al (2010) Histologic changes associated with false-negative sentinel lymph nodes after preoperative chemotherapy in patients with confirmed lymph node-positive breast cancer before treatment. Cancer 116:2878–2883CrossRef Brown AS et al (2010) Histologic changes associated with false-negative sentinel lymph nodes after preoperative chemotherapy in patients with confirmed lymph node-positive breast cancer before treatment. Cancer 116:2878–2883CrossRef
53.
go back to reference Oh JL et al (2007) Placement of radiopaque clips for tumor localization in patients undergoing neoadjuvant chemotherapy and breast conservation therapy. Cancer 110:2420–2427CrossRef Oh JL et al (2007) Placement of radiopaque clips for tumor localization in patients undergoing neoadjuvant chemotherapy and breast conservation therapy. Cancer 110:2420–2427CrossRef
54.
go back to reference Galimberti V et al (2016) Sentinel node biopsy after neoadjuvant treatment in breast cancer: five-year follow-up of patients with clinically node-negative or node-positive disease before treatment. Eur J Surg Oncol 42:361–368CrossRef Galimberti V et al (2016) Sentinel node biopsy after neoadjuvant treatment in breast cancer: five-year follow-up of patients with clinically node-negative or node-positive disease before treatment. Eur J Surg Oncol 42:361–368CrossRef
55.
go back to reference DeSantis CE et al (2016) Breast cancer statistics, 2015: convergence of incidence rates between black and white women. CA Cancer J Clin 66:31–42CrossRef DeSantis CE et al (2016) Breast cancer statistics, 2015: convergence of incidence rates between black and white women. CA Cancer J Clin 66:31–42CrossRef
56.
go back to reference DeSantis CE et al (2017) Breast cancer statistics, 2017, racial disparity in mortality by state. CA Cancer J Clin 67:439–448CrossRef DeSantis CE et al (2017) Breast cancer statistics, 2017, racial disparity in mortality by state. CA Cancer J Clin 67:439–448CrossRef
59.
go back to reference Iqbal J et al (2015) Differences in breast cancer stage at diagnosis and cancer-specific survival by race and ethnicity in the United States. JAMA 313:165–173CrossRef Iqbal J et al (2015) Differences in breast cancer stage at diagnosis and cancer-specific survival by race and ethnicity in the United States. JAMA 313:165–173CrossRef
60.
go back to reference American Cancer Society (2017) Breast cancer facts & Figs. 2017–2018. American Cancer Society, Atlanta American Cancer Society (2017) Breast cancer facts & Figs. 2017–2018. American Cancer Society, Atlanta
61.
go back to reference Eley JW et al (1994) Racial differences in survival from breast cancer. Results of the National Cancer Institute Black/White Cancer Survival Study. JAMA 272:947–954CrossRef Eley JW et al (1994) Racial differences in survival from breast cancer. Results of the National Cancer Institute Black/White Cancer Survival Study. JAMA 272:947–954CrossRef
62.
go back to reference Newman LA et al (2006) Meta-analysis of survival in African American and white American patients with breast cancer: ethnicity compared with socioeconomic status. J Clin Oncol 24:1342–1349CrossRef Newman LA et al (2006) Meta-analysis of survival in African American and white American patients with breast cancer: ethnicity compared with socioeconomic status. J Clin Oncol 24:1342–1349CrossRef
63.
go back to reference Albain KS et al (2009) Racial disparities in cancer survival among randomized clinical trials patients of the Southwest Oncology Group. J Natl Cancer Inst 101:984–992CrossRef Albain KS et al (2009) Racial disparities in cancer survival among randomized clinical trials patients of the Southwest Oncology Group. J Natl Cancer Inst 101:984–992CrossRef
64.
go back to reference Newman LA (2017) Breast cancer disparities: socioeconomic factors versus biology. Ann Surg Oncol 24:2869–2875CrossRef Newman LA (2017) Breast cancer disparities: socioeconomic factors versus biology. Ann Surg Oncol 24:2869–2875CrossRef
65.
go back to reference Newman LA, Kaljee LM (2017) Health disparities and triple-negative breast cancer in African American women: a review. JAMA Surg 152:485–493CrossRef Newman LA, Kaljee LM (2017) Health disparities and triple-negative breast cancer in African American women: a review. JAMA Surg 152:485–493CrossRef
67.
go back to reference Newman LA (2016) Parsing the etiology of breast cancer disparities. J Clin Oncol 34:1013–1014CrossRef Newman LA (2016) Parsing the etiology of breast cancer disparities. J Clin Oncol 34:1013–1014CrossRef
68.
go back to reference Li CI, Malone KE, Daling JR (2003) Differences in breast cancer stage, treatment, and survival by race and ethnicity. Arch Intern Med 163:49–56CrossRef Li CI, Malone KE, Daling JR (2003) Differences in breast cancer stage, treatment, and survival by race and ethnicity. Arch Intern Med 163:49–56CrossRef
69.
go back to reference Newman LA et al. (2015) The 2014 Society of Surgical Oncology Susan G. Komen for the Cure Symposium: triple-negative breast cancer. Ann Surg Oncol 22:874–882CrossRef Newman LA et al. (2015) The 2014 Society of Surgical Oncology Susan G. Komen for the Cure Symposium: triple-negative breast cancer. Ann Surg Oncol 22:874–882CrossRef
70.
go back to reference Kohler BA et al. (2015) Annual report to the nation on the status of cancer, 1975–2011, featuring incidence of breast cancer subtypes by race/ethnicity, poverty, and state. J Natl Cancer Inst 107:djv048CrossRef Kohler BA et al. (2015) Annual report to the nation on the status of cancer, 1975–2011, featuring incidence of breast cancer subtypes by race/ethnicity, poverty, and state. J Natl Cancer Inst 107:djv048CrossRef
71.
go back to reference Amirikia KC et al (2011) Higher population-based incidence rates of triple-negative breast cancer among young African-American women: Implications for breast cancer screening recommendations. Cancer 117:2747–2753CrossRef Amirikia KC et al (2011) Higher population-based incidence rates of triple-negative breast cancer among young African-American women: Implications for breast cancer screening recommendations. Cancer 117:2747–2753CrossRef
72.
go back to reference Carey LA et al (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295:2492–2502CrossRef Carey LA et al (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295:2492–2502CrossRef
73.
go back to reference Troester MA et al (2018) Racial differences in PAM50 subtypes in the Carolina Breast Cancer Study. J Natl Cancer Inst 110:176–182CrossRef Troester MA et al (2018) Racial differences in PAM50 subtypes in the Carolina Breast Cancer Study. J Natl Cancer Inst 110:176–182CrossRef
74.
go back to reference Plasilova ML et al (2016) Features of triple-negative breast cancer: Analysis of 38,813 cases from the national cancer database. Medicine 95:e4614CrossRef Plasilova ML et al (2016) Features of triple-negative breast cancer: Analysis of 38,813 cases from the national cancer database. Medicine 95:e4614CrossRef
75.
go back to reference Akinyemiju T, Moore JX, Altekruse SF (2015) Breast cancer survival in African–American women by hormone receptor subtypes. Breast Cancer Res Treat 153:211–218CrossRef Akinyemiju T, Moore JX, Altekruse SF (2015) Breast cancer survival in African–American women by hormone receptor subtypes. Breast Cancer Res Treat 153:211–218CrossRef
76.
go back to reference Kroenke CH et al (2014) Race and breast cancer survival by intrinsic subtype based on PAM50 gene expression. Breast Cancer Res Treat 144:689–699CrossRef Kroenke CH et al (2014) Race and breast cancer survival by intrinsic subtype based on PAM50 gene expression. Breast Cancer Res Treat 144:689–699CrossRef
77.
go back to reference Lindner R et al (2013) Molecular phenotypes in triple negative breast cancer from African American patients suggest targets for therapy. PLoS ONE 8:e71915CrossRef Lindner R et al (2013) Molecular phenotypes in triple negative breast cancer from African American patients suggest targets for therapy. PLoS ONE 8:e71915CrossRef
78.
go back to reference Keenan T et al (2015) Comparison of the genomic landscape between primary breast cancer in African American versus white women and the association of racial differences with tumor recurrence. J Clin Oncol 33:3621–3627CrossRef Keenan T et al (2015) Comparison of the genomic landscape between primary breast cancer in African American versus white women and the association of racial differences with tumor recurrence. J Clin Oncol 33:3621–3627CrossRef
79.
go back to reference Ademuyiwa FO et al (2017) Differences in the mutational landscape of triple-negative breast cancer in African Americans and Caucasians. Breast Cancer Res Treat 161:491–499CrossRef Ademuyiwa FO et al (2017) Differences in the mutational landscape of triple-negative breast cancer in African Americans and Caucasians. Breast Cancer Res Treat 161:491–499CrossRef
80.
go back to reference Huo D et al (2017) Comparison of breast cancer molecular features and survival by African and European ancestry in The Cancer Genome Atlas. JAMA Oncol 3:1654–1662CrossRef Huo D et al (2017) Comparison of breast cancer molecular features and survival by African and European ancestry in The Cancer Genome Atlas. JAMA Oncol 3:1654–1662CrossRef
81.
go back to reference Lopez-Garcia MA et al (2010) Breast cancer precursors revisited: molecular features and progression pathways. Histopathology 57:171–192CrossRef Lopez-Garcia MA et al (2010) Breast cancer precursors revisited: molecular features and progression pathways. Histopathology 57:171–192CrossRef
82.
go back to reference Visscher DW et al (2016) Clinicopathologic features of breast cancers that develop in women with previous benign breast disease. Cancer 122:378–385CrossRef Visscher DW et al (2016) Clinicopathologic features of breast cancers that develop in women with previous benign breast disease. Cancer 122:378–385CrossRef
83.
go back to reference Bowen RL et al (2008) Early onset of breast cancer in a group of British black women. Br J Cancer 98:277–281CrossRef Bowen RL et al (2008) Early onset of breast cancer in a group of British black women. Br J Cancer 98:277–281CrossRef
84.
go back to reference Copson E et al (2014) Ethnicity and outcome of young breast cancer patients in the United Kingdom: the POSH study. Br J Cancer 110:230–241CrossRef Copson E et al (2014) Ethnicity and outcome of young breast cancer patients in the United Kingdom: the POSH study. Br J Cancer 110:230–241CrossRef
85.
go back to reference Rapiti E et al (2017) Opportunities for improving triple-negative breast cancer outcomes: results of a population-based study. Cancer Med 6:526–536CrossRef Rapiti E et al (2017) Opportunities for improving triple-negative breast cancer outcomes: results of a population-based study. Cancer Med 6:526–536CrossRef
86.
go back to reference Carvalho FM et al (2014) Geographic differences in the distribution of molecular subtypes of breast cancer in Brazil. BMC Womens Health 14:102CrossRef Carvalho FM et al (2014) Geographic differences in the distribution of molecular subtypes of breast cancer in Brazil. BMC Womens Health 14:102CrossRef
87.
go back to reference Jiagge E et al (2016) Comparative analysis of breast cancer phenotypes in African American, White American, and West Versus East African patients: correlation between African ancestry and triple-negative breast cancer. Ann Surg Oncol 23:3843–3849CrossRef Jiagge E et al (2016) Comparative analysis of breast cancer phenotypes in African American, White American, and West Versus East African patients: correlation between African ancestry and triple-negative breast cancer. Ann Surg Oncol 23:3843–3849CrossRef
Metadata
Title
Breast cancer metastasis through the lympho-vascular system
Authors
S. David Nathanson
David Krag
Henry M. Kuerer
Lisa A. Newman
Markus Brown
Dontscho Kerjaschki
Ethel R. Pereira
Timothy P. Padera
Publication date
01-08-2018
Publisher
Springer Netherlands
Published in
Clinical & Experimental Metastasis / Issue 5-6/2018
Print ISSN: 0262-0898
Electronic ISSN: 1573-7276
DOI
https://doi.org/10.1007/s10585-018-9902-1

Other articles of this Issue 5-6/2018

Clinical & Experimental Metastasis 5-6/2018 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