Skip to main content

Advertisement

SpringerLink
Log in

Pattern of metastatic spread and subcategories of breast cancer

  • Gynecologic Oncology
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

Abstract

Purpose

The development of metastases is the most aggressive attribute of breast cancer. In this retrospective multicenter study, we evaluated if and how the different pathological breast cancer subtypes influence the spreading of tumor cells, the development of metastasis and the survival of breast cancer patients.

Methods

This retrospective German multicenter study is based on the BRENDA collective including 9625 breast cancer patients treated in the adjuvant setting. We used the χ 2 tests for the analysis of the categorical variables between groups of patients with different sites of metastasis. Survival distributions and median survival times were estimated using the Kaplan–Meier product-limit method. The log-rank test was applied to compare survival rates. The Cox proportional hazards model was used to estimate the hazard ratio and confidence intervals.

Results

886 women developed metastases during a time interval of 53 months after primary diagnosis. Luminal A tumor patients were more likely to get bone metastases than lung, liver or CNS metastases. Patients with a triple-negative subtype were, however, the least affected by metastasis in the skeleton. They were most likely to develop visceral metastases. Location, numbers of metastases herein and the subtype influenced the overall survival (OAS). Altogether, the best OAS was found in patients with the luminal A subtype, the worst in patients with the triple-negative subtype.

Conclusions

Knowledge of the typical metastatic pattern of the subtypes of breast cancer will help to personalize therapeutic options and follow-up examinations of cancer patients.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Tian S, Roepman P, Van’t Veer LJ, Bernards R, de Snoo F, Glas AM (2010) Biological functions of the genes in the mammaprint breast cancer profile reflect the hallmarks of cancer. Biomark Insights 5:129–138. doi:10.4137/BMI.S6184

    PubMed  PubMed Central  Google Scholar 

  2. Carlson JJ, Roth JA (2013) The impact of the Oncotype Dx breast cancer assay in clinical practice: a systematic review and meta-analysis. Breast Cancer Res Treat 141(1):13–22. doi:10.1007/s10549-013-2666-z

    Article  PubMed  PubMed Central  Google Scholar 

  3. Chang HY, Nuyten DS, Sneddon JB, Hastie T, Tibshirani R, Sorlie T, Dai H, He YD, van’t Veer LJ, Bartelink H, van de Rijn M, Brown PO, van de Vijver MJ (2005) Robustness, scalability, and integration of a wound-response gene expression signature in predicting breast cancer survival. Proc Natl Acad Sci USA 102(10):3738–3743. doi:10.1073/pnas.0409462102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Zhang Y, Sieuwerts AM, McGreevy M, Casey G, Cufer T, Paradiso A, Harbeck N, Span PN, Hicks DG, Crowe J, Tubbs RR, Budd GT, Lyons J, Sweep FC, Schmitt M, Schittulli F, Golouh R, Talantov D, Wang Y, Foekens JA (2009) The 76-gene signature defines high-risk patients that benefit from adjuvant tamoxifen therapy. Breast Cancer Res Treat 116(2):303–309. doi:10.1007/s10549-008-0183-2

    Article  CAS  PubMed  Google Scholar 

  5. Ma XJ, Patel R, Wang X, Salunga R, Murage J, Desai R, Tuggle JT, Wang W, Chu S, Stecker K, Raja R, Robin H, Moore M, Baunoch D, Sgroi D, Erlander M (2006) Molecular classification of human cancers using a 92-gene real-time quantitative polymerase chain reaction assay. Arch Pathol Lab Med 130(4):465–473. doi:10.1043/1543-2165(2006)130[465:MCOHCU]2.0.CO;2

  6. Perou CM, Sorlie T, Eisen MB, van de Rijn M, Jeffrey SS, Rees CA, Pollack JR, Ross DT, Johnsen H, Akslen LA, Fluge O, Pergamenschikov A, Williams C, Zhu SX, Lonning PE, Borresen-Dale AL, Brown PO, Botstein D (2000) Molecular portraits of human breast tumours. Nature 406(6797):747–752. doi:10.1038/35021093

    Article  CAS  PubMed  Google Scholar 

  7. Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thurlimann B, Senn HJ (2011) Strategies for subtypes–dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol Off J Eur Soc Med Oncol ESMO 22(8):1736–1747. doi:10.1093/annonc/mdr304

    Article  CAS  Google Scholar 

  8. von Minckwitz G, Untch M, Blohmer JU, Costa SD, Eidtmann H, Fasching PA, Gerber B, Eiermann W, Hilfrich J, Huober J, Jackisch C, Kaufmann M, Konecny GE, Denkert C, Nekljudova V, Mehta K, Loibl S (2012) Definition and impact of pathologic complete response on prognosis after neoadjuvant chemotherapy in various intrinsic breast cancer subtypes. J Clin Oncol Off J Am Soc Clin Oncol 30(15):1796–1804. doi:10.1200/JCO.2011.38.8595

    Article  Google Scholar 

  9. Parise CA, Caggiano V (2014) Breast cancer survival defined by the ER/PR/HER2 subtypes and a surrogate classification according to tumor grade and immunohistochemical biomarkers. J Cancer Epidemiol 2014:469251. doi:10.1155/2014/469251

    Article  PubMed  PubMed Central  Google Scholar 

  10. Goldhirsch A, Winer EP, Coates AS, Gelber RD, Piccart-Gebhart M, Thurlimann B, Senn HJ (2013) Personalizing the treatment of women with early breast cancer: highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2013. Ann Oncol Off J Eur Soc Med Oncol ESMO 24(9):2206–2223. doi:10.1093/annonc/mdt303

    Article  CAS  Google Scholar 

  11. Prat A, Cheang MC, Martin M, Parker JS, Carrasco E, Caballero R, Tyldesley S, Gelmon K, Bernard PS, Nielsen TO, Perou CM (2013) Prognostic significance of progesterone receptor-positive tumor cells within immunohistochemically defined luminal A breast cancer. J Clin Oncol Off J Am Soc Clin Oncol 31(2):203–209. doi:10.1200/JCO.2012.43.4134

    Article  CAS  Google Scholar 

  12. Gerratana L, Fanotto V, Bonotto M, Bolzonello S, Minisini AM, Fasola G, Puglisi F (2015) Pattern of metastasis and outcome in patients with breast cancer. Clin Exp Metastasis 32(2):125–133. doi:10.1007/s10585-015-9697-2

    Article  CAS  PubMed  Google Scholar 

  13. Kast K, Link T, Friedrich K, Petzold A, Niedostatek A, Schoffer O, Werner C, Klug SJ, Werner A, Gatzweiler A, Richter B, Baretton G, Wimberger P (2015) Impact of breast cancer subtypes and patterns of metastasis on outcome. Breast Cancer Res Treat 150(3):621–629. doi:10.1007/s10549-015-3341-3

    Article  CAS  PubMed  Google Scholar 

  14. Wenners A, Berlin L, Alkatout I, van Mackelenbergh M, Jonat W, Mundhenke C (2015) Clinical implications of first and multiple locoregional breast cancer recurrences. Arch Gynecol Obstet 292(1):165–173. doi:10.1007/s00404-014-3586-9

    Article  PubMed  Google Scholar 

  15. Blanco G, Holli K, Heikkinen M, Kallioniemi OP, Taskinen P (1990) Prognostic factors in recurrent breast cancer: relationships to site of recurrence, disease-free interval, female sex steroid receptors, ploidy and histological malignancy grading. Br J Cancer 62(1):142–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Savci-Heijink CD, Halfwerk H, Hooijer GK, Horlings HM, Wesseling J, van de Vijver MJ (2015) Retrospective analysis of metastatic behaviour of breast cancer subtypes. Breast Cancer Res Treat 150(3):547–557. doi:10.1007/s10549-015-3352-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Park HS, Kim S, Kim K, Yoo H, Chae BJ, Bae JS, Song BJ, Jung SS (2012) Pattern of distant recurrence according to the molecular subtypes in Korean women with breast cancer. World J Surg Oncol 10:4. doi:10.1186/1477-7819-10-4

    Article  PubMed  PubMed Central  Google Scholar 

  18. Dent R, Hanna WM, Trudeau M, Rawlinson E, Sun P, Narod SA (2009) Pattern of metastatic spread in triple-negative breast cancer. Breast Cancer Res Treat 115(2):423–428. doi:10.1007/s10549-008-0086-2

    Article  PubMed  Google Scholar 

  19. Metzger-Filho O, Sun Z, Viale G, Price KN, Crivellari D, Snyder RD, Gelber RD, Castiglione-Gertsch M, Coates AS, Goldhirsch A, Cardoso F (2013) Patterns of Recurrence and outcome according to breast cancer subtypes in lymph node-negative disease: results from international breast cancer study group trials VIII and IX. J Clin Oncol Off J Am Soc Clin Oncol 31(25):3083–3090. doi:10.1200/JCO.2012.46.1574

    Article  CAS  Google Scholar 

  20. Kallioniemi OP, Holli K, Visakorpi T, Koivula T, Helin HH, Isola JJ (1991) Association of c-erbB-2 protein over-expression with high rate of cell proliferation, increased risk of visceral metastasis and poor long-term survival in breast cancer. Int J Cancer J Int Du Cancer 49(5):650–655

    Article  CAS  Google Scholar 

  21. Paluch-Shimon S, Ben-Baruch N, Wolf I, Zach L, Kopolovic J, Kruglikova A, Modiano T, Yosepovich A, Catane R, Kaufman B (2009) Hormone receptor expression is associated with a unique pattern of metastatic spread and increased survival among HER2-overexpressing breast cancer patients. Am J Clin Oncol 32(5):504–508. doi:10.1097/COC.0b013e3181967d72

    Article  CAS  PubMed  Google Scholar 

  22. Kennecke H, Yerushalmi R, Woods R, Cheang MC, Voduc D, Speers CH, Nielsen TO, Gelmon K (2010) Metastatic behavior of breast cancer subtypes. J Clin Oncol Off J Am Soc Clin Oncol 28(20):3271–3277. doi:10.1200/JCO.2009.25.9820

    Article  Google Scholar 

  23. Brouckaert O, Wildiers H, Floris G, Neven P (2012) Update on triple-negative breast cancer: prognosis and management strategies. Int J Women’s Health 4:511–520. doi:10.2147/IJWH.S18541

    Google Scholar 

  24. Andre F, Zielinski CC (2012) Optimal strategies for the treatment of metastatic triple-negative breast cancer with currently approved agents. Ann oncol off j Eur Soc Med Oncol ESMO 23(Suppl 6):vi46–vi51. doi:10.1093/annonc/mds195

    Article  Google Scholar 

  25. Bramati A, Girelli S, Torri V, Farina G, Galfrascoli E, Piva S, Moretti A, Dazzani MC, Sburlati P, La Verde NM (2014) Efficacy of biological agents in metastatic triple-negative breast cancer. Cancer Treat Rev 40(5):605–613. doi:10.1016/j.ctrv.2014.01.003

    Article  CAS  PubMed  Google Scholar 

  26. Clark O, Botrel TE, Paladini L, Ferreira MB (2014) Targeted therapy in triple-negative metastatic breast cancer: a systematic review and meta-analysis. Core Evid 9:1–11. doi:10.2147/CE.S52197

    Article  PubMed  PubMed Central  Google Scholar 

  27. Wockel A, Wolters R, Wiegel T, Novopashenny I, Janni W, Kreienberg R, Wischnewsky M, Schwentner L (2014) The impact of adjuvant radiotherapy on the survival of primary breast cancer patients: a retrospective multicenter cohort study of 8935 subjects. Ann Oncol Off J Eur Soc Med Oncol ESMO 25(3):628–632. doi:10.1093/annonc/mdt584

    Article  CAS  Google Scholar 

  28. Wockel A, Kurzeder C, Geyer V, Novasphenny I, Wolters R, Wischnewsky M, Kreienberg R, Varga D (2010) Effects of guideline adherence in primary breast cancer–a 5-year multi-center cohort study of 3976 patients. Breast 19(2):120–127. doi:10.1016/j.breast.2009.12.006

    Article  PubMed  Google Scholar 

  29. Schwentner L, Wolters R, Koretz K, Wischnewsky MB, Kreienberg R, Rottscholl R, Wockel A (2012) Triple-negative breast cancer: the impact of guideline-adherent adjuvant treatment on survival–a retrospective multi-centre cohort study. Breast Cancer Res Treat 132(3):1073–1080. doi:10.1007/s10549-011-1935-y

    Article  CAS  PubMed  Google Scholar 

  30. Diessner J, Van Ewijk R, Weiss CR, Janni W, Wischnewsky MB, Kreienberg R, Hancke K, Blettner M, Wockel A, Schwentner L (2015) Identifying the impact of inflammatory breast cancer on survival: a retrospective multi-center cohort study. Arch Gynecol Obstet 292(3):655–664. doi:10.1007/s00404-015-3691-4

    Article  CAS  PubMed  Google Scholar 

  31. Peto R, Davies C, Godwin J, Gray R, Pan HC, Clarke M, Cutter D, Darby S, McGale P, Taylor C, Wang YC, Bergh J, Di Leo A, Albain K, Swain S, Piccart M, Pritchard K (2012) Comparisons between different polychemotherapy regimens for early breast cancer: meta-analyses of long-term outcome among 100,000 women in 123 randomised trials. Lancet 379(9814):432–444. doi:10.1016/S0140-6736(11)61625-5

    Article  CAS  PubMed  Google Scholar 

  32. Darby S, McGale P, Correa C, Taylor C, Arriagada R, Clarke M, Cutter D, Davies C, Ewertz M, Godwin J, Gray R, Pierce L, Whelan T, Wang Y, Peto R (2011) Effect of radiotherapy after breast-conserving surgery on 10-year recurrence and 15-year breast cancer death: meta-analysis of individual patient data for 10,801 women in 17 randomised trials. Lancet 378(9804):1707–1716. doi:10.1016/S0140-6736(11)61629-2

    Article  CAS  PubMed  Google Scholar 

  33. Redig AJ, McAllister SS (2013) Breast cancer as a systemic disease: a view of metastasis. J Intern Med 274(2):113–126. doi:10.1111/joim.12084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. van ‘t Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415(6871):530–536. doi:10.1038/415530a

    Article  PubMed  Google Scholar 

  35. Yan M, Shield-Artin K, Byrne D, Deb S, Waddell N, Haviv I, Fox SB (2015) Comparative microRNA profiling of sporadic and BRCA1 associated basal-like breast cancers. BMC Cancer 15:506. doi:10.1186/s12885-015-1522-4

    Article  PubMed  PubMed Central  Google Scholar 

  36. Spellman PT, Gray JW (2014) Detecting cancer by monitoring circulating tumor DNA. Nat Med 20(5):474–475. doi:10.1038/nm.3564

    Article  CAS  PubMed  Google Scholar 

  37. McInnes LM, Jacobson N, Redfern A, Dowling A, Thompson EW, Saunders CM (2015) Clinical implications of circulating tumor cells of breast cancer patients: role of epithelial-mesenchymal plasticity. Front Oncol 5:42. doi:10.3389/fonc.2015.00042

    Article  PubMed  PubMed Central  Google Scholar 

  38. Bidard FC, Peeters DJ, Fehm T, Nole F, Gisbert-Criado R, Mavroudis D, Grisanti S, Generali D, Garcia-Saenz JA, Stebbing J, Caldas C, Gazzaniga P, Manso L, Zamarchi R, de Lascoiti AF, De Mattos-Arruda L, Ignatiadis M, Lebofsky R, van Laere SJ, Meier-Stiegen F, Sandri MT, Vidal-Martinez J, Politaki E, Consoli F, Bottini A, Diaz-Rubio E, Krell J, Dawson SJ, Raimondi C, Rutten A, Janni W, Munzone E, Caranana V, Agelaki S, Almici C, Dirix L, Solomayer EF, Zorzino L, Johannes H, Reis-Filho JS, Pantel K, Pierga JY, Michiels S (2014) Clinical validity of circulating tumour cells in patients with metastatic breast cancer: a pooled analysis of individual patient data. Lancet Oncol 15(4):406–414. doi:10.1016/S1470-2045(14)70069-5

    Article  PubMed  Google Scholar 

  39. Diessner J, Bruttel V, Stein RG, Horn E, Hausler SF, Dietl J, Honig A, Wischhusen J (2014) Targeting of preexisting and induced breast cancer stem cells with trastuzumab and trastuzumab emtansine (T-DM1). Cell Death Dis 5:e1149. doi:10.1038/cddis.2014.115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Diessner J, Bruttel V, Becker K, Pawlik M, Stein R, Hausler S, Dietl J, Wischhusen J, Honig A (2013) Targeting breast cancer stem cells with HER2-specific antibodies and natural killer cells. Am J Cancer Res 3(2):211–220

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Verhaegh W, van Ooijen H, Inda MA, Hatzis P, Versteeg R, Smid M, Martens J, Foekens J, van de Wiel P, Clevers H, van de Stolpe A (2014) Selection of personalized patient therapy through the use of knowledge-based computational models that identify tumor-driving signal transduction pathways. Cancer Res 74(11):2936–2945. doi:10.1158/0008-5472.CAN-13-2515

    Article  CAS  PubMed  Google Scholar 

  42. Gabrilovich DI, Nagaraj S (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9(3):162–174. doi:10.1038/nri2506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Engel JB, Honig A, Kapp M, Hahne JC, Meyer SR, Dietl J, Segerer SE (2014) Mechanisms of tumor immune escape in triple-negative breast cancers (TNBC) with and without mutated BRCA 1. Arch Gynecol Obstet 289(1):141–147. doi:10.1007/s00404-013-2922-9

    Article  CAS  PubMed  Google Scholar 

  44. Pogoda K, Niwinska A, Murawska M, Pienkowski T (2013) Analysis of pattern, time and risk factors influencing recurrence in triple-negative breast cancer patients. Med Oncol 30(1):388. doi:10.1007/s12032-012-0388-4

    Article  PubMed  PubMed Central  Google Scholar 

  45. Sihto H, Lundin J, Lundin M, Lehtimaki T, Ristimaki A, Holli K, Sailas L, Kataja V, Turpeenniemi-Hujanen T, Isola J, Heikkila P, Joensuu H (2011) Breast cancer biological subtypes and protein expression predict for the preferential distant metastasis sites: a nationwide cohort study. Breast Cancer Res BCR 13(5):R87. doi:10.1186/bcr2944

    Article  CAS  PubMed  Google Scholar 

  46. Lobbezoo DJ, van Kampen RJ, Voogd AC, Dercksen MW, van den Berkmortel F, Smilde TJ, van de Wouw AJ, Peters FP, van Riel JM, Peters NA, de Boer M, Borm GF, Tjan-Heijnen VC (2013) Prognosis of metastatic breast cancer subtypes: the hormone receptor/HER2-positive subtype is associated with the most favorable outcome. Breast Cancer Res Treat 141(3):507–514. doi:10.1007/s10549-013-2711-y

    Article  CAS  PubMed  Google Scholar 

  47. Smid M, Wang Y, Zhang Y, Sieuwerts AM, Yu J, Klijn JG, Foekens JA, Martens JW (2008) Subtypes of breast cancer show preferential site of relapse. Cancer Res 68(9):3108–3114. doi:10.1158/0008-5472.CAN-07-5644

    Article  CAS  PubMed  Google Scholar 

  48. Yardley DA, Tripathy D, Brufsky AM, Rugo HS, Kaufman PA, Mayer M, Magidson J, Yoo B, Quah C, Ulcickas Yood M (2014) Long-term survivor characteristics in HER2-positive metastatic breast cancer from registHER. Br J Cancer 110(11):2756–2764. doi:10.1038/bjc.2014.174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Nam BH, Kim SY, Han HS, Kwon Y, Lee KS, Kim TH, Ro J (2008) Breast cancer subtypes and survival in patients with brain metastases. Breast Cancer Res BCR 10(1):R20. doi:10.1186/bcr1870

    Article  PubMed  Google Scholar 

  50. Lee SJ, Park S, Ahn HK, Yi JH, Cho EY, Sun JM, Lee JE, Nam SJ, Yang JH, Park YH, Ahn JS, Im YH (2011) Implications of bone-only metastases in breast cancer: favorable preference with excellent outcomes of hormone receptor positive breast cancer. Cancer Res Treat Off J Korean Cancer Assoc 43(2):89–95. doi:10.4143/crt.2011.43.2.89

    Google Scholar 

  51. Stebbing J, Payne R, Reise J, Frampton AE, Avery M, Woodley L, Di Leo A, Pestrin M, Krell J, Coombes RC (2013) The efficacy of lapatinib in metastatic breast cancer with HER2 non-amplified primary tumors and EGFR positive circulating tumor cells: a proof-of-concept study. PLoS One 8(5):e62543. doi:10.1371/journal.pone.0062543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Verma S, Miles D, Gianni L, Krop IE, Welslau M, Baselga J, Pegram M, Oh DY, Dieras V, Guardino E, Fang L, Lu MW, Olsen S, Blackwell K (2012) Trastuzumab emtansine for HER2-positive advanced breast cancer. N Engl J Med 367(19):1783–1791. doi:10.1056/NEJMoa1209124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Gianni L, Eiermann W, Semiglazov V, Lluch A, Tjulandin S, Zambetti M, Moliterni A, Vazquez F, Byakhov MJ, Lichinitser M, Climent MA, Ciruelos E, Ojeda B, Mansutti M, Bozhok A, Magazzu D, Heinzmann D, Steinseifer J, Valagussa P, Baselga J (2014) Neoadjuvant and adjuvant trastuzumab in patients with HER2-positive locally advanced breast cancer (NOAH): follow-up of a randomised controlled superiority trial with a parallel HER2-negative cohort. Lancet Oncol 15(6):640–647. doi:10.1016/S1470-2045(14)70080-4

    Article  CAS  PubMed  Google Scholar 

  54. Duan XF, Dong NN, Zhang T, Li Q (2013) The prognostic analysis of clinical breast cancer subtypes among patients with liver metastases from breast cancer. Int J Clin Oncol Jpn Soc Clin Oncol 18(1):26–32. doi:10.1007/s10147-011-0336-x

    Article  CAS  Google Scholar 

  55. Eichbaum MH, Kaltwasser M, Bruckner T, de Rossi TM, Schneeweiss A, Sohn C (2006) Prognostic factors for patients with liver metastases from breast cancer. Breast Cancer Res Treat 96(1):53–62. doi:10.1007/s10549-005-9039-1

    Article  PubMed  Google Scholar 

  56. Wyld L, Gutteridge E, Pinder SE, James JJ, Chan SY, Cheung KL, Robertson JF, Evans AJ (2003) Prognostic factors for patients with hepatic metastases from breast cancer. Br J Cancer 89(2):284–290. doi:10.1038/sj.bjc.6601038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Ge QD, Lv N, Kong YN, Xie XH, He N, Xie XM, Wei WD (2012) Clinical characteristics and survival analysis of breast cancer molecular subtypes with hepatic metastases. Asian Pac J Cancer Prev APJCP 13(10):5081–5086

    Article  PubMed  Google Scholar 

  58. Yhim HY, Han SW, Oh DY, Han W, Im SA, Kim TY, Kim YT, Noh DY, Chie EK, Ha SW, Park IA, Bang YJ (2010) Prognostic factors for recurrent breast cancer patients with an isolated, limited number of lung metastases and implications for pulmonary metastasectomy. Cancer 116(12):2890–2901. doi:10.1002/cncr.25054

    Article  PubMed  Google Scholar 

  59. Heitz F, Harter P, Lueck HJ, Fissler-Eckhoff A, Lorenz-Salehi F, Scheil-Bertram S, Traut A, du Bois A (2009) Triple-negative and HER2-overexpressing breast cancers exhibit an elevated risk and an earlier occurrence of cerebral metastases. Eur J Cancer 45(16):2792–2798. doi:10.1016/j.ejca.2009.06.027

    Article  CAS  PubMed  Google Scholar 

  60. Aversa C, Rossi V, Geuna E, Martinello R, Milani A, Redana S, Valabrega G, Aglietta M, Montemurro F (2014) Metastatic breast cancer subtypes and central nervous system metastases. Breast 23(5):623–628. doi:10.1016/j.breast.2014.06.009

    Article  CAS  PubMed  Google Scholar 

  61. Arslan UY, Oksuzoglu B, Aksoy S, Harputluoglu H, Turker I, Ozisik Y, Dizdar O, Altundag K, Alkis N, Zengin N (2011) Breast cancer subtypes and outcomes of central nervous system metastases. Breast 20(6):562–567. doi:10.1016/j.breast.2011.07.017

    Article  PubMed  Google Scholar 

  62. Coumans FA, Siesling S, Terstappen LW (2013) Detection of cancer before distant metastasis. BMC Cancer 13:283. doi:10.1186/1471-2407-13-283

    Article  PubMed  PubMed Central  Google Scholar 

  63. Ryu EB, Chang JM, Seo M, Kim SA, Lim JH, Moon WK (2014) Tumour volume doubling time of molecular breast cancer subtypes assessed by serial breast ultrasound. Eur Radiol 24(9):2227–2235. doi:10.1007/s00330-014-3256-0

    Article  PubMed  Google Scholar 

  64. Fornvik D, Lang K, Andersson I, Dustler M, Borgquist S, Timberg P (2015) Estimates of breast cancer growth rate from mammograms and its relation to tumour characteristics. Radiat Prot Dosim. doi:10.1093/rpd/ncv417

    Google Scholar 

Download references

Acknowledgements

We express our thanks to the following persons for their contributions to the BRENDA study: Karsten Gnauert (Ostalbklinikum, Aalen), Steffen Fritz (Kreisklinik Biberach), Ulf Göretzlehner (Kreiskrankenhaus Ehingen), Hans-Walter Vollert (Städt. Krankenhaus Friedrichshafen), Peter Jakob Albert (Klinikum Heidenheim), Ricardo Felberbaum (Klinikum Kempten), Andreas Zorr (Klinikum Konstanz), Felix Flock (Klinikum Memmingen), Erik Schlicht (Stauferklinik, Mutlangen), Martina Gropp-Meier (Oberschwabenklinik Ravensburg), Gerhard Bartzke (Kreiskrankenhaus Rottweil), Andreas Rempen (Diakonie-Krankenhaus, Schwäbisch Hall), Edgar Schelble (Kreiskrankenhaus Sigmaringen), Theodor Dinkelacker (Helfenstein-Klinik Geislingen), Andreas Grüneberger (Oberschwabenklinik Wangen) and Thorsten Kühn (Städt. Kliniken, Esslingen).

Author information

Authors and Affiliations

  1. Department for Obstetrics and Gynecology, University Hospital of Würzburg, Josef-Schneider-Str. 4, 97080, Würzburg, Germany

    Catharina Bartmann, Tanja Stüber, Roland Stein, Mathias Krockenberger, Sebastian Häusler, Achim Wöckel & Joachim Diessner

  2. Department for Obstetrics and Gynecology, University Hospital of Ulm, Prittwitzstr. 43, 89075, Ulm, Germany

    Wolfgang Janni, Rolf Kreienberg & Lukas Schwentner

  3. Faculty of Mathematics and Computer Science, University of Bremen, Universitätsallee GW1, 28359, Bremen, Germany

    Manfred Wischnewsky

  4. Institut für Medizinische Biometrie, Epidemiologie und Informatik (IMBEI), University of Mainz, Obere Zahlbacher Str. 69, 55131, Mainz, Germany

    Maria Blettner

Authors
  1. Catharina Bartmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Manfred Wischnewsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tanja Stüber
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Roland Stein
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mathias Krockenberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sebastian Häusler
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wolfgang Janni
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Rolf Kreienberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Maria Blettner
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Lukas Schwentner
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Achim Wöckel
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Joachim Diessner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Catharina Bartmann.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

The Ethics Committee of the University of Ulm, which covers all participating breast cancer centers of the BRENDA network, has approved this study and the BRENDA project.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Funding source

This work was supported by the German Federal Ministry of Education and Research (BMBF-Grant-01ZP0505).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bartmann, C., Wischnewsky, M., Stüber, T. et al. Pattern of metastatic spread and subcategories of breast cancer. Arch Gynecol Obstet 295, 211–223 (2017). https://doi.org/10.1007/s00404-016-4225-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00404-016-4225-4

Keywords

Search

Navigation