Skip to main content
Top
Published in: Breast Cancer Research and Treatment 3/2014

Open Access 01-08-2014 | Epidemiology

Differences in metastatic patterns in relation to time between primary surgery and first relapse from breast cancer suggest synchronized growth of dormant micrometastases

Authors: Hanna Dillekås, Monica Transeth, Martin Pilskog, Jörg Assmus, Oddbjørn Straume

Published in: Breast Cancer Research and Treatment | Issue 3/2014

Login to get access

Abstract

A significant variation in the metastatic pattern among breast cancer patients exists. Clinical observations suggest that these differences are related to time to recurrence (TTR), thus suggesting a common systemic growth signal at the time of surgery. Our goal was to identify a marker for synchronized growth of micrometastases. To quantify the metastatic pattern at first relapse, 180 patients with metastatic breast cancer were studied. Standard deviation (SD) of lesions size and lesion number was calculated and served as a marker for variation. Patients with low SD (multiple/similar sized lesions) were assumed to have synchronized growth, whereas patients with high SD were assumed to have unsynchronized growth. Patients were grouped according to TTR; early (< 3 years-) or late (> 3 years- after surgery). In patients not receiving systemic adjuvant treatment, median SD was significantly lower in the early group (2.5 mm) compared with 6.4 mm in the late group (p = 0.005). In node negative patients, median SD was significantly lower in the early group (3.0 mm) when compared with the late group (5.7 mm, p = 0.02). An additional drop in SD was observed immediately after end of adjuvant endocrine therapy. Our results identify SD as a marker of synchronized metastatic growth in breast cancer. A metastatic phenotype characterized by multiple similar sized metastases, suggesting synchronized onset of growth of micrometastases was predominantly found in patients recurring early after surgery and was counteracted by adjuvant treatment. Systemic growth signals caused by surgery might be antagonized during the time window following surgery.
Literature
1.
go back to reference Brewster AM, Hortobagyi GN, Broglio KR, Kau SW, Santa-Maria CA, Arun B, Buzdar AU, Booser DJ, Valero V, Bondy M, Esteva FJ (2008) Residual risk of breast cancer recurrence 5 years after adjuvant therapy. J Natl Cancer Inst 100(16):1179–1183. doi:10.1093/jnci/djn233 PubMedCrossRef Brewster AM, Hortobagyi GN, Broglio KR, Kau SW, Santa-Maria CA, Arun B, Buzdar AU, Booser DJ, Valero V, Bondy M, Esteva FJ (2008) Residual risk of breast cancer recurrence 5 years after adjuvant therapy. J Natl Cancer Inst 100(16):1179–1183. doi:10.​1093/​jnci/​djn233 PubMedCrossRef
2.
go back to reference Demicheli R, Biganzoli E, Ardoino I, Boracchi P, Coradini D, Greco M, Moliterni A, Zambetti M, Valagussa P, Gukas ID, Bonadonna G (2010) Recurrence and mortality dynamics for breast cancer patients undergoing mastectomy according to estrogen receptor status: different mortality but similar recurrence. Cancer Sci 101(3):826–830. doi:10.1111/j.1349-7006.2009.01472.x PubMedCrossRef Demicheli R, Biganzoli E, Ardoino I, Boracchi P, Coradini D, Greco M, Moliterni A, Zambetti M, Valagussa P, Gukas ID, Bonadonna G (2010) Recurrence and mortality dynamics for breast cancer patients undergoing mastectomy according to estrogen receptor status: different mortality but similar recurrence. Cancer Sci 101(3):826–830. doi:10.​1111/​j.​1349-7006.​2009.​01472.​x PubMedCrossRef
3.
go back to reference Ribelles N, Perez-Villa L, Jerez JM, Pajares B, Vicioso L, Jimenez B, de Luque V, Franco L, Gallego E, Marquez A, Alvarez M, Sanchez-Munoz A, Perez-Rivas L, Alba E (2013) Pattern of recurrence of early breast cancer is different according to intrinsic subtype and proliferation index. Breast Cancer Res 15(5):R98. doi:10.1186/bcr3559 PubMedCentralPubMedCrossRef Ribelles N, Perez-Villa L, Jerez JM, Pajares B, Vicioso L, Jimenez B, de Luque V, Franco L, Gallego E, Marquez A, Alvarez M, Sanchez-Munoz A, Perez-Rivas L, Alba E (2013) Pattern of recurrence of early breast cancer is different according to intrinsic subtype and proliferation index. Breast Cancer Res 15(5):R98. doi:10.​1186/​bcr3559 PubMedCentralPubMedCrossRef
6.
go back to reference Esserman LJ, Moore DH, Tsing PJ, Chu PW, Yau C, Ozanne E, Chung RE, Tandon VJ, Park JW, Baehner FL, Kreps S, Tutt AN, Gillett CE, Benz CC (2011) Biologic markers determine both the risk and the timing of recurrence in breast cancer. Breast Cancer Res Treat 129(2):607–616. doi:10.1007/s10549-011-1564-5 PubMedCrossRef Esserman LJ, Moore DH, Tsing PJ, Chu PW, Yau C, Ozanne E, Chung RE, Tandon VJ, Park JW, Baehner FL, Kreps S, Tutt AN, Gillett CE, Benz CC (2011) Biologic markers determine both the risk and the timing of recurrence in breast cancer. Breast Cancer Res Treat 129(2):607–616. doi:10.​1007/​s10549-011-1564-5 PubMedCrossRef
10.
go back to reference Holmgren L, O’Reilly MS, Folkman J (1995) Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med 1(2):149–153PubMedCrossRef Holmgren L, O’Reilly MS, Folkman J (1995) Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med 1(2):149–153PubMedCrossRef
11.
go back to reference Koebel CM, Vermi W, Swann JB, Zerafa N, Rodig SJ, Old LJ, Smyth MJ, Schreiber RD (2007) Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450(7171):903–907. doi:10.1038/nature06309 PubMedCrossRef Koebel CM, Vermi W, Swann JB, Zerafa N, Rodig SJ, Old LJ, Smyth MJ, Schreiber RD (2007) Adaptive immunity maintains occult cancer in an equilibrium state. Nature 450(7171):903–907. doi:10.​1038/​nature06309 PubMedCrossRef
12.
go back to reference Ranganathan AC, Adam AP, Aguirre-Ghiso JA (2006) Opposing roles of mitogenic and stress signaling pathways in the induction of cancer dormancy. Cell Cycle 5(16):1799–1807PubMedCentralPubMedCrossRef Ranganathan AC, Adam AP, Aguirre-Ghiso JA (2006) Opposing roles of mitogenic and stress signaling pathways in the induction of cancer dormancy. Cell Cycle 5(16):1799–1807PubMedCentralPubMedCrossRef
14.
go back to reference Davies C, Pan H, Godwin J, Gray R, Arriagada R, Raina V, Abraham M, Medeiros Alencar VH, Badran A, Bonfill X, Bradbury J, Clarke M, Collins R, Davis SR, Delmestri A, Forbes JF, Haddad P, Hou MF, Inbar M, Khaled H, Kielanowska J, Kwan WH, Mathew BS, Mittra I, Muller B, Nicolucci A, Peralta O, Pernas F, Petruzelka L, Pienkowski T, Radhika R, Rajan B, Rubach MT, Tort S, Urrutia G, Valentini M, Wang Y, Peto R, Adjuvant Tamoxifen: Longer Against Shorter Collaborative G (2013) Long-term effects of continuing adjuvant tamoxifen to 10 years versus stopping at 5 years after diagnosis of oestrogen receptor-positive breast cancer: ATLAS, a randomised trial. Lancet 381(9869):805–816. doi:10.1016/S0140-6736(12)61963-1 PubMedCentralPubMedCrossRef Davies C, Pan H, Godwin J, Gray R, Arriagada R, Raina V, Abraham M, Medeiros Alencar VH, Badran A, Bonfill X, Bradbury J, Clarke M, Collins R, Davis SR, Delmestri A, Forbes JF, Haddad P, Hou MF, Inbar M, Khaled H, Kielanowska J, Kwan WH, Mathew BS, Mittra I, Muller B, Nicolucci A, Peralta O, Pernas F, Petruzelka L, Pienkowski T, Radhika R, Rajan B, Rubach MT, Tort S, Urrutia G, Valentini M, Wang Y, Peto R, Adjuvant Tamoxifen: Longer Against Shorter Collaborative G (2013) Long-term effects of continuing adjuvant tamoxifen to 10 years versus stopping at 5 years after diagnosis of oestrogen receptor-positive breast cancer: ATLAS, a randomised trial. Lancet 381(9869):805–816. doi:10.​1016/​S0140-6736(12)61963-1 PubMedCentralPubMedCrossRef
15.
go back to reference Straume O, Shimamura T, Lampa MJ, Carretero J, Oyan AM, Jia D, Borgman CL, Soucheray M, Downing SR, Short SM, Kang SY, Wang S, Chen L, Collett K, Bachmann I, Wong KK, Shapiro GI, Kalland KH, Folkman J, Watnick RS, Akslen LA, Naumov GN (2012) Suppression of heat shock protein 27 induces long-term dormancy in human breast cancer. Proc Natl Acad Sci USA 109(22):8699–8704. doi:10.1073/pnas.1017909109 PubMedCentralPubMedCrossRef Straume O, Shimamura T, Lampa MJ, Carretero J, Oyan AM, Jia D, Borgman CL, Soucheray M, Downing SR, Short SM, Kang SY, Wang S, Chen L, Collett K, Bachmann I, Wong KK, Shapiro GI, Kalland KH, Folkman J, Watnick RS, Akslen LA, Naumov GN (2012) Suppression of heat shock protein 27 induces long-term dormancy in human breast cancer. Proc Natl Acad Sci USA 109(22):8699–8704. doi:10.​1073/​pnas.​1017909109 PubMedCentralPubMedCrossRef
16.
go back to reference Murthy SM, Goldschmidt RA, Rao LN, Ammirati M, Buchmann T, Scanlon EF (1989) The influence of surgical trauma on experimental metastasis. Cancer 64(10):2035–2044PubMedCrossRef Murthy SM, Goldschmidt RA, Rao LN, Ammirati M, Buchmann T, Scanlon EF (1989) The influence of surgical trauma on experimental metastasis. Cancer 64(10):2035–2044PubMedCrossRef
17.
go back to reference Gill M, Dias S, Hattori K, Rivera ML, Hicklin D, Witte L, Girardi L, Yurt R, Himel H, Rafii S (2001) Vascular trauma induces rapid but transient mobilization of VEGFR2(+) AC133(+) endothelial precursor cells. Circ Res 88(2):167–174PubMedCrossRef Gill M, Dias S, Hattori K, Rivera ML, Hicklin D, Witte L, Girardi L, Yurt R, Himel H, Rafii S (2001) Vascular trauma induces rapid but transient mobilization of VEGFR2(+) AC133(+) endothelial precursor cells. Circ Res 88(2):167–174PubMedCrossRef
18.
go back to reference Indraccolo S, Stievano L, Minuzzo S, Tosello V, Esposito G, Piovan E, Zamarchi R, Chieco-Bianchi L, Amadori A (2006) Interruption of tumor dormancy by a transient angiogenic burst within the tumor microenvironment. Proc Natl Acad Sci USA 103(11):4216–4221PubMedCentralPubMedCrossRef Indraccolo S, Stievano L, Minuzzo S, Tosello V, Esposito G, Piovan E, Zamarchi R, Chieco-Bianchi L, Amadori A (2006) Interruption of tumor dormancy by a transient angiogenic burst within the tumor microenvironment. Proc Natl Acad Sci USA 103(11):4216–4221PubMedCentralPubMedCrossRef
20.
go back to reference Demicheli R, Abbattista A, Miceli R, Valagussa P, Bonadonna G (1996) Time distribution of the recurrence risk for breast cancer patients undergoing mastectomy: further support about the concept of tumor dormancy. Breast Cancer Res Treat 41(2):177–185PubMedCrossRef Demicheli R, Abbattista A, Miceli R, Valagussa P, Bonadonna G (1996) Time distribution of the recurrence risk for breast cancer patients undergoing mastectomy: further support about the concept of tumor dormancy. Breast Cancer Res Treat 41(2):177–185PubMedCrossRef
22.
go back to reference Demicheli R, Ardoino I, Boracchi P, Coradini D, Agresti R, Ferraris C, Gennaro M, Hrushesky WJ, Biganzoli E (2010) Recurrence and mortality according to estrogen receptor status for breast cancer patients undergoing conservative surgery. Ipsilateral breast tumour recurrence dynamics provides clues for tumour biology within the residual breast. BMC Cancer 10:656. doi:10.1186/1471-2407-10-656 PubMedCentralPubMedCrossRef Demicheli R, Ardoino I, Boracchi P, Coradini D, Agresti R, Ferraris C, Gennaro M, Hrushesky WJ, Biganzoli E (2010) Recurrence and mortality according to estrogen receptor status for breast cancer patients undergoing conservative surgery. Ipsilateral breast tumour recurrence dynamics provides clues for tumour biology within the residual breast. BMC Cancer 10:656. doi:10.​1186/​1471-2407-10-656 PubMedCentralPubMedCrossRef
23.
go back to reference Singletary SE, Allred C, Ashley P, Bassett LW, Berry D, Bland KI, Borgen PI, Clark G, Edge SB, Hayes DF, Hughes LL, Hutter RV, Morrow M, Page DL, Recht A, Theriault RL, Thor A, Weaver DL, Wieand HS, Greene FL (2002) Revision of the American Joint Committee on Cancer staging system for breast cancer. J Clin Oncol 20(17):3628–3636PubMedCrossRef Singletary SE, Allred C, Ashley P, Bassett LW, Berry D, Bland KI, Borgen PI, Clark G, Edge SB, Hayes DF, Hughes LL, Hutter RV, Morrow M, Page DL, Recht A, Theriault RL, Thor A, Weaver DL, Wieand HS, Greene FL (2002) Revision of the American Joint Committee on Cancer staging system for breast cancer. J Clin Oncol 20(17):3628–3636PubMedCrossRef
24.
go back to reference Carter CL, Allen C, Henson DE (1989) Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer 63(1):181–187PubMedCrossRef Carter CL, Allen C, Henson DE (1989) Relation of tumor size, lymph node status, and survival in 24,740 breast cancer cases. Cancer 63(1):181–187PubMedCrossRef
25.
go back to reference Saphner T, Tormey DC, Gray R (1996) Annual hazard rates of recurrence for breast cancer after primary therapy. J Clin Oncol 14(10):2738–2746PubMed Saphner T, Tormey DC, Gray R (1996) Annual hazard rates of recurrence for breast cancer after primary therapy. J Clin Oncol 14(10):2738–2746PubMed
26.
go back to reference Cuzick J, Sestak I, Baum M, Buzdar A, Howell A, Dowsett M, Forbes JF, Investigators AL (2010) Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 10-year analysis of the ATAC trial. Lancet Oncol 11(12):1135–1141. doi:10.1016/S1470-2045(10)70257-6 PubMedCrossRef Cuzick J, Sestak I, Baum M, Buzdar A, Howell A, Dowsett M, Forbes JF, Investigators AL (2010) Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 10-year analysis of the ATAC trial. Lancet Oncol 11(12):1135–1141. doi:10.​1016/​S1470-2045(10)70257-6 PubMedCrossRef
28.
go back to reference Naumov GN, Folkman J, Straume O, Akslen LA (2008) Tumor-vascular interactions and tumor dormancy. Apmis 116(7–8):569–585PubMedCrossRef Naumov GN, Folkman J, Straume O, Akslen LA (2008) Tumor-vascular interactions and tumor dormancy. Apmis 116(7–8):569–585PubMedCrossRef
30.
go back to reference Fisher B, Montague E, Redmond C, Barton B, Borland D, Fisher ER, Deutsch M, Schwarz G, Margolese R, Donegan W, Volk H, Konvolinka C, Cohn I Jr, Lesnick G, Cruz AB, Lawrence W, Nealon T, Butcher H, Lawton R (1977) Comparison of radical mastectomy with alternative treatments for primary breast cancer. A first report of results from a prospective randomized clinical trial. Cancer 39(6):2827–2839PubMedCrossRef Fisher B, Montague E, Redmond C, Barton B, Borland D, Fisher ER, Deutsch M, Schwarz G, Margolese R, Donegan W, Volk H, Konvolinka C, Cohn I Jr, Lesnick G, Cruz AB, Lawrence W, Nealon T, Butcher H, Lawton R (1977) Comparison of radical mastectomy with alternative treatments for primary breast cancer. A first report of results from a prospective randomized clinical trial. Cancer 39(6):2827–2839PubMedCrossRef
31.
go back to reference Poggi MM, Danforth DN, Sciuto LC, Smith SL, Steinberg SM, Liewehr DJ, Menard C, Lippman ME, Lichter AS, Altemus RM (2003) Eighteen-year results in the treatment of early breast carcinoma with mastectomy versus breast conservation therapy: the National Cancer Institute Randomized Trial. Cancer 98(4):697–702. doi:10.1002/cncr.11580 PubMedCrossRef Poggi MM, Danforth DN, Sciuto LC, Smith SL, Steinberg SM, Liewehr DJ, Menard C, Lippman ME, Lichter AS, Altemus RM (2003) Eighteen-year results in the treatment of early breast carcinoma with mastectomy versus breast conservation therapy: the National Cancer Institute Randomized Trial. Cancer 98(4):697–702. doi:10.​1002/​cncr.​11580 PubMedCrossRef
32.
33.
go back to reference Fisher B (1999) From Halsted to prevention and beyond: advances in the management of breast cancer during the twentieth century. Eur J Cancer 35(14):1963–1973PubMedCrossRef Fisher B (1999) From Halsted to prevention and beyond: advances in the management of breast cancer during the twentieth century. Eur J Cancer 35(14):1963–1973PubMedCrossRef
34.
go back to reference Giuliano AE, Hunt KK, Ballman KV, Beitsch PD, Whitworth PW, Blumencranz PW, Leitch AM, Saha S, McCall LM, Morrow M (2011) Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 305(6):569–575. doi:10.1001/jama.2011.90 PubMedCrossRef Giuliano AE, Hunt KK, Ballman KV, Beitsch PD, Whitworth PW, Blumencranz PW, Leitch AM, Saha S, McCall LM, Morrow M (2011) Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 305(6):569–575. doi:10.​1001/​jama.​2011.​90 PubMedCrossRef
35.
go back to reference Walters S, Maringe C, Butler J, Rachet B, Barrett-Lee P, Bergh J, Boyages J, Christiansen P, Lee M, Warnberg F, Allemani C, Engholm G, Fornander T, Gjerstorff ML, Johannesen TB, Lawrence G, McGahan CE, Middleton R, Steward J, Tracey E, Turner D, Richards MA, Coleman MP, Group IMW (2013) Breast cancer survival and stage at diagnosis in Australia, Canada, Denmark, Norway, Sweden and the UK, 2000–2007: a population-based study. Br J Cancer 108(5):1195–1208. doi:10.1038/bjc.2013.6 PubMedCentralPubMedCrossRef Walters S, Maringe C, Butler J, Rachet B, Barrett-Lee P, Bergh J, Boyages J, Christiansen P, Lee M, Warnberg F, Allemani C, Engholm G, Fornander T, Gjerstorff ML, Johannesen TB, Lawrence G, McGahan CE, Middleton R, Steward J, Tracey E, Turner D, Richards MA, Coleman MP, Group IMW (2013) Breast cancer survival and stage at diagnosis in Australia, Canada, Denmark, Norway, Sweden and the UK, 2000–2007: a population-based study. Br J Cancer 108(5):1195–1208. doi:10.​1038/​bjc.​2013.​6 PubMedCentralPubMedCrossRef
37.
go back to reference Norton L (1988) A gompertzian model of human breast cancer growth. Cancer Res 48(24 Pt 1):7067–7071PubMed Norton L (1988) A gompertzian model of human breast cancer growth. Cancer Res 48(24 Pt 1):7067–7071PubMed
38.
go back to reference Speer JF, Petrosky VE, Retsky MW, Wardwell RH (1984) A stochastic numerical model of breast cancer growth that simulates clinical data. Cancer Res 44(9):4124–4130PubMed Speer JF, Petrosky VE, Retsky MW, Wardwell RH (1984) A stochastic numerical model of breast cancer growth that simulates clinical data. Cancer Res 44(9):4124–4130PubMed
39.
go back to reference Withers HR, Lee SP (2006) Modeling growth kinetics and statistical distribution of oligometastases. Semin Radiat Oncol 16(2):111–119PubMedCrossRef Withers HR, Lee SP (2006) Modeling growth kinetics and statistical distribution of oligometastases. Semin Radiat Oncol 16(2):111–119PubMedCrossRef
43.
go back to reference Gao F, Tan SB, Machin D, Wong NS (2007) Confirmation of double-peaked time distribution of mortality among Asian breast cancer patients in a population-based study. Breast Cancer Res 9(2):R21PubMedCentralPubMedCrossRef Gao F, Tan SB, Machin D, Wong NS (2007) Confirmation of double-peaked time distribution of mortality among Asian breast cancer patients in a population-based study. Breast Cancer Res 9(2):R21PubMedCentralPubMedCrossRef
45.
go back to reference Gagliato Dde M, Gonzalez-Angulo AM, Lei X, Theriault RL, Giordano SH, Valero V, Hortobagyi GN, Chavez-Macgregor M (2014) Clinical impact of delaying initiation of adjuvant chemotherapy in patients with breast cancer. J Clin Oncol 32(8):735–744. doi:10.1200/JCO.2013.49.7693 PubMedCrossRef Gagliato Dde M, Gonzalez-Angulo AM, Lei X, Theriault RL, Giordano SH, Valero V, Hortobagyi GN, Chavez-Macgregor M (2014) Clinical impact of delaying initiation of adjuvant chemotherapy in patients with breast cancer. J Clin Oncol 32(8):735–744. doi:10.​1200/​JCO.​2013.​49.​7693 PubMedCrossRef
46.
go back to reference Torres L, Ribeiro FR, Pandis N, Andersen JA, Heim S, Teixeira MR (2007) Intratumor genomic heterogeneity in breast cancer with clonal divergence between primary carcinomas and lymph node metastases. Breast Cancer Res Treat 102(2):143–155. doi:10.1007/s10549-006-9317-6 PubMedCrossRef Torres L, Ribeiro FR, Pandis N, Andersen JA, Heim S, Teixeira MR (2007) Intratumor genomic heterogeneity in breast cancer with clonal divergence between primary carcinomas and lymph node metastases. Breast Cancer Res Treat 102(2):143–155. doi:10.​1007/​s10549-006-9317-6 PubMedCrossRef
47.
go back to reference Cummings MC, Simpson PT, Reid LE, Jayanthan J, Skerman J, Song S, McCart Reed AE, Kutasovic JR, Morey AL, Marquart L, O’Rourke P, Lakhani SR (2013) Metastatic progression of breast cancer: insights from 50 years of autopsies. J Pathol. doi:10.1002/path.4288 Cummings MC, Simpson PT, Reid LE, Jayanthan J, Skerman J, Song S, McCart Reed AE, Kutasovic JR, Morey AL, Marquart L, O’Rourke P, Lakhani SR (2013) Metastatic progression of breast cancer: insights from 50 years of autopsies. J Pathol. doi:10.​1002/​path.​4288
48.
go back to reference Barista I, Baltali E, Gullu IH, Guler N, Celik I, Saracbasi O, Tekuzman G, Kars A, Ozisik Y, Ruacan S, Atahan IL, Firat D (1996) Factors influencing the distribution of metastases and survival in metastatic breast carcinoma. Am J Clin Oncol 19(6):569–573PubMedCrossRef Barista I, Baltali E, Gullu IH, Guler N, Celik I, Saracbasi O, Tekuzman G, Kars A, Ozisik Y, Ruacan S, Atahan IL, Firat D (1996) Factors influencing the distribution of metastases and survival in metastatic breast carcinoma. Am J Clin Oncol 19(6):569–573PubMedCrossRef
49.
go back to reference Hormbrey E, Han C, Roberts A, McGrouther DA, Harris AL (2003) The relationship of human wound vascular endothelial growth factor (VEGF) after breast cancer surgery to circulating VEGF and angiogenesis. Clin Cancer Res 9(12):4332–4339PubMed Hormbrey E, Han C, Roberts A, McGrouther DA, Harris AL (2003) The relationship of human wound vascular endothelial growth factor (VEGF) after breast cancer surgery to circulating VEGF and angiogenesis. Clin Cancer Res 9(12):4332–4339PubMed
50.
go back to reference O’Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, Lane WS, Cao Y, Sage EH, Folkman J (1994) Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79(2):315–328PubMedCrossRef O’Reilly MS, Holmgren L, Shing Y, Chen C, Rosenthal RA, Moses M, Lane WS, Cao Y, Sage EH, Folkman J (1994) Angiostatin: a novel angiogenesis inhibitor that mediates the suppression of metastases by a Lewis lung carcinoma. Cell 79(2):315–328PubMedCrossRef
51.
go back to reference Camphausen K, Moses MA, Beecken WD, Khan MK, Folkman J, O’Reilly MS (2001) Radiation therapy to a primary tumor accelerates metastatic growth in mice. Cancer Res 61(5):2207–2211PubMed Camphausen K, Moses MA, Beecken WD, Khan MK, Folkman J, O’Reilly MS (2001) Radiation therapy to a primary tumor accelerates metastatic growth in mice. Cancer Res 61(5):2207–2211PubMed
54.
go back to reference Badwe R (2013) Surgical removal of primary tumor and axillary lymph nodes in women with metastatic breast cancer at first presentation: a randomized controlled trial. In: SABCS, San Antonio Badwe R (2013) Surgical removal of primary tumor and axillary lymph nodes in women with metastatic breast cancer at first presentation: a randomized controlled trial. In: SABCS, San Antonio
55.
go back to reference Fisher B, Gunduz N, Saffer EA (1983) Influence of the interval between primary tumor removal and chemotherapy on kinetics and growth of metastases. Cancer Res 43(4):1488–1492PubMed Fisher B, Gunduz N, Saffer EA (1983) Influence of the interval between primary tumor removal and chemotherapy on kinetics and growth of metastases. Cancer Res 43(4):1488–1492PubMed
Metadata
Title
Differences in metastatic patterns in relation to time between primary surgery and first relapse from breast cancer suggest synchronized growth of dormant micrometastases
Authors
Hanna Dillekås
Monica Transeth
Martin Pilskog
Jörg Assmus
Oddbjørn Straume
Publication date
01-08-2014
Publisher
Springer US
Published in
Breast Cancer Research and Treatment / Issue 3/2014
Print ISSN: 0167-6806
Electronic ISSN: 1573-7217
DOI
https://doi.org/10.1007/s10549-014-3057-9

Other articles of this Issue 3/2014

Breast Cancer Research and Treatment 3/2014 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