Retrospective analysis of metastatic behaviour of breast cancer subtypes

Breast Cancer Research and Treatment

Volumn 150, Issue 3, 2015, Pages 547-557

  Savci Heijink, C Dilara ^a   Halfwerk, Hans ^a   Hooijer, Gerrit K J ^a   Horlings, Hugo M ^a   Wesseling, Jelle ^b   van de Vijver, Marc J ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Immunohistochemistry; Organotropism; Pathology; Site specific relapse; Tumour

Indexed keywords

CYTOKERATIN 14; CYTOKERATIN 5; CYTOKERATIN 6; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; KI 67 ANTIGEN; PROGESTERONE RECEPTOR; PROTEIN P53; UVOMORULIN; TUMOR MARKER;

ADULT; AGED; ARTICLE; BONE METASTASIS; BREAST CANCER; CANCER GRADING; CANCER GROWTH; CANCER SURVIVAL; DISEASE ASSOCIATION; DISTANT METASTASIS; HUMAN; MAJOR CLINICAL STUDY; OVERALL SURVIVAL; PATIENT ASSESSMENT; PRIMARY TUMOR; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SURVIVAL TIME; TISSUE MICROARRAY; TUMOR VOLUME; VISCERAL METASTASIS; BREAST TUMOR; CLASSIFICATION; FEMALE; METABOLISM; METASTASIS; MIDDLE AGED; MORTALITY; PATHOLOGY; SURVIVAL ANALYSIS; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; BIOMARKERS, TUMOR; BREAST NEOPLASMS; FEMALE; HUMANS; MIDDLE AGED; NEOPLASM METASTASIS; RETROSPECTIVE STUDIES; SURVIVAL ANALYSIS; TISSUE ARRAY ANALYSIS;

EID: 84926194459     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-015-3352-0     Document Type: Article

References (70)

1. Malvezzi M, Bertuccio P, Levi F, La VC, Negri E (2012) European cancer mortality predictions for the year 2012. Ann Oncol 23(4):1044–1052. doi:10.1093/annonc/mds024
2. Lorusso G, Ruegg C (2012) New insights into the mechanisms of organ-specific breast cancer metastasis. Semin Cancer Biol 22(3):226–233. doi:10.1016/j.semcancer.2012.03.007
3. St RP, Madan R, Tawfik OW, Damjanov I, Fan F (2012) Organotropism and prognostic marker discordance in distant metastases of breast carcinoma: fact or fiction? A clinicopathologic analysis. Hum Pathol 43(3):398–404. doi:10.1016/j.humpath.2011.05.009
4. Lu X, Kang Y (2007) Organotropism of breast cancer metastasis. J Mammary Gland Biol Neoplasia 12(2–3):153–162. doi:10.1007/s10911-007-9047-3
5. Chiang AC, Massague J (2008) Molecular basis of metastasis. N Engl J Med 359(26):2814–2823. doi:10.1056/NEJMra0805239
6. Chambers AF, Groom AC, MacDonald IC (2002) Dissemination and growth of cancer cells in metastatic sites. Nat Rev Cancer 2(8):563–572. doi:10.1038/nrc865
7. Altundag K, Bondy ML, Mirza NQ, Kau SW, Broglio K, Hortobagyi GN, Rivera E (2007) Clinicopathologic characteristics and prognostic factors in 420 metastatic breast cancer patients with central nervous system metastasis. Cancer 110(12):2640–2647. doi:10.1002/cncr.23088
8. Bos PD, Zhang XH, Nadal C, Shu W, Gomis RR, Nguyen DX, Minn AJ, van de Vijver MJ, Gerald WL, Foekens JA, Massague J (2009) Genes that mediate breast cancer metastasis to the brain. Nature 459(7249):1005–1009. doi:10.1038/nature08021
9. Harrell JC, Prat A, Parker JS, Fan C, He X, Carey L, Anders C, Ewend M, Perou CM (2012) Genomic analysis identifies unique signatures predictive of brain, lung, and liver relapse. Breast Cancer Res Treat 132(2):523–535. doi:10.1007/s10549-011-1619-7
10. Landemaine T, Jackson A, Bellahcene A, Rucci N, Sin S, Abad BM, Sierra A, Boudinet A, Guinebretiere JM, Ricevuto E, Nogues C, Briffod M, Bieche I, Cherel P, Garcia T, Castronovo V, Teti A, Lidereau R, Driouch K (2008) A six-gene signature predicting breast cancer lung metastasis. Cancer Res 68(15):6092–6099. doi:10.1158/0008-5472.CAN-08-0436
11. Paik S, Shak S, Tang G, Kim C, Baker J, Cronin M, Baehner FL, Walker MG, Watson D, Park T, Hiller W, Fisher ER, Wickerham DL, Bryant J, Wolmark N (2004) A multigene assay to predict recurrence of tamoxifen-treated, node-negative breast cancer. N Engl J Med 351(27):2817–2826. doi:10.1056/NEJMoa041588
12. Slimane K, Andre F, Delaloge S, Dunant A, Perez A, Grenier J, Massard C, Spielmann M (2004) Risk factors for brain relapse in patients with metastatic breast cancer. Ann Oncol 15(11):1640–1644. doi:10.1093/annonc/mdh432
13. van de Vijver MJ, He YD, van’t Veer LJ, Dai H, Hart AA, Voskuil DW, Schreiber GJ, Peterse JL, Roberts C, Marton MJ, Parrish M, Atsma D, Witteveen A, Glas A, Delahaye L, van der Velde T, Bartelink H, Rodenhuis S, Rutgers ET, Friend SH, Bernards R (2002) A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 347(25):1999–2009. doi:10.1056/NEJMoa021967
14. Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F, Talantov D, Timmermans M, Meijer-van Gelder ME, Yu J, Jatkoe T, Berns EM, Atkins D, Foekens JA (2005) Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365(9460):671–679. doi:10.1016/S0140-6736(05)17947-1
15. Zhang XH, Wang Q, Gerald W, Hudis CA, Norton L, Smid M, Foekens JA, Massague J (2009) Latent bone metastasis in breast cancer tied to Src-dependent survival signals. Cancer Cell 16(1):67–78. doi:10.1016/j.ccr.2009.05.017
16. Koo JS, Jung W, Jeong J (2010) Metastatic breast cancer shows different immunohistochemical phenotype according to metastatic site. Tumori 96(3):424–432
17. Lin Y, Yin W, Yan T, Zhou L, Di G, Wu J, Shen Z, Shao Z, Lu J (2009) Site-specific relapse pattern of the triple negative tumors in Chinese breast cancer patients. BMC Cancer 9:342. doi:10.1186/1471-2407-9-342
18. Campbell FC, Blamey RW, Elston CW, Nicholson RI, Griffiths K, Haybittle JL (1981) Oestrogen-receptor status and sites of metastasis in breast cancer. Br J Cancer 44(3):456–459
19. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, Lickley LA, Rawlinson E, Sun P, Narod SA (2007) Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res 13(15 Pt 1):4429–4434. doi:10.1158/1078-0432.CCR-06-3045
20. 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
21. Fuqua SA (2001) The role of estrogen receptors in breast cancer metastasis. J Mammary Gland Biol Neoplasia 6(4):407–417
22. Haffty BG, Yang Q, Reiss M, Kearney T, Higgins SA, Weidhaas J, Harris L, Hait W, Toppmeyer D (2006) Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J Clin Oncol 24(36):5652–5657. doi:10.1200/JCO.2006.06.5664
23. Heitz F, Harter P, Lueck HJ, Fissler-Eckhoff A, Lorenz-Salehi F, Scheil-Bertram S, Traut A, du BA (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
24. 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 28(20):3271–3277. doi:10.1200/JCO.2009.25.9820
25. Largillier R, Ferrero JM, Doyen J, Barriere J, Namer M, Mari V, Courdi A, Hannoun-Levi JM, Ettore F, Birtwisle-Peyrottes I, Balu-Maestro C, Marcy PY, Raoust I, Lallement M, Chamorey E (2008) Prognostic factors in 1038 women with metastatic breast cancer. Ann Oncol 19(12):2012–2019. doi:10.1093/annonc/mdn424
26. Lin NU, Claus E, Sohl J, Razzak AR, Arnaout A, Winer EP (2008) Sites of distant recurrence and clinical outcomes in patients with metastatic triple-negative breast cancer: high incidence of central nervous system metastases. Cancer 113(10):2638–2645. doi:10.1002/cncr.23930
27. Tham YL, Sexton K, Kramer R, Hilsenbeck S, Elledge R (2006) Primary breast cancer phenotypes associated with propensity for central nervous system metastases. Cancer 107(4):696–704. doi:10.1002/cncr.22041
28. Chia SK, Speers CH, D’yachkova Y, Kang A, Malfair-Taylor S, Barnett J, Coldman A, Gelmon KA, O’reilly SE, Olivotto IA (2007) The impact of new chemotherapeutic and hormone agents on survival in a population-based cohort of women with metastatic breast cancer. Cancer 110(5):973–979. doi:10.1002/cncr.22867
29. Dawood S, Broglio K, Gonzalez-Angulo AM, Buzdar AU, Hortobagyi GN, Giordano SH (2008) Trends in survival over the past two decades among white and black patients with newly diagnosed stage IV breast cancer. J Clin Oncol 26(30):4891–4898. doi:10.1200/JCO.2007.14.1168
30. Giordano SH, Buzdar AU, Smith TL, Kau SW, Yang Y, Hortobagyi GN (2004) Is breast cancer survival improving? Cancer 100(1):44–52. doi:10.1002/cncr.11859
31. Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V (2007) Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California cancer Registry. Cancer 109(9):1721–1728. doi:10.1002/cncr.22618
32. Foulkes WD, Brunet JS, Stefansson IM, Straume O, Chappuis PO, Begin LR, Hamel N, Goffin JR, Wong N, Trudel M, Kapusta L, Porter P, Akslen LA (2004) The prognostic implication of the basal-like (cyclin E high/p27 low/p53+/glomeruloid-microvascular-proliferation+) phenotype of BRCA1-related breast cancer. Cancer Res 64(3):830–835
33. 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
34. Vermeulen E, Geesink I, Schmidt MK, Steegers C, Verhue D, Brom FW, Aaronson NK, van Leeuwen FE (2009) Secondary use of human tissue: consent and better information required. Ned Tijdschr Geneeskd 153:A948
35. Elston CW, Ellis IO (2002) Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology 1991; 19:403–410. Histopathology 41(3A):151–152, discussion
36. Wolff AC, Hammond ME, Schwartz JN, Hagerty KL, Allred DC, Cote RJ, Dowsett M, Fitzgibbons PL, Hanna WM, Langer A, McShane LM, Paik S, Pegram MD, Perez EA, Press MF, Rhodes A, Sturgeon C, Taube SE, Tubbs R, Vance GH, van de Vijver M, Wheeler TM, Hayes DF (2007) American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. Arch Pathol Lab Med 131(1):18–43
37. Cheang MC, Chia SK, Voduc D, Gao D, Leung S, Snider J, Watson M, Davies S, Bernard PS, Parker JS, Perou CM, Ellis MJ, Nielsen TO (2009) Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. J Natl Cancer Inst 101(10):736–750. doi:10.1093/jnci/djp082
38. 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 22(8):1736–1747. doi:10.1093/annonc/mdr304
39. Kim MJ, Ro JY, Ahn SH, Kim HH, Kim SB, Gong G (2006) Clinicopathologic significance of the basal-like subtype of breast cancer: a comparison with hormone receptor and Her2/neu-overexpressing phenotypes. Hum Pathol 37(9):1217–1226. doi:10.1016/j.humpath.2006.04.015
40. Kreike B, van Kouwenhove M, Horlings H, Weigelt B, Peterse H, Bartelink H, van de Vijver MJ (2007) Gene expression profiling and histopathological characterization of triple-negative/basal-like breast carcinomas. Breast Cancer Res 9(5):R65. doi:10.1186/bcr1771
41. Paget S (1989) The distribution of secondary growths in cancer of the breast. 1889. Cancer Metastasis Rev 8(2):98–101
42. Fidler IJ (1973) Selection of successive tumour lines for metastasis. Nat New Biol 242(118):148–149
43. Langley RR, Fidler IJ (2011) The seed and soil hypothesis revisited–the role of tumor-stroma interactions in metastasis to different organs. Int J Cancer 128(11):2527–2535. doi:10.1002/ijc.26031
44. Andry G, Suciu S, Pratola D, Sylvester R, Leclercq G, da Costa PM, Legros N, Andry-t’Hooft M, Verhest A, Mattheiem W (1989) Relation between estrogen receptor concentration and clinical and histological factors: their relative prognostic importance after radical mastectomy for primary breast cancer. Eur J Cancer Clin Oncol 25(2):319–329
45. Hess KR, Pusztai L, Buzdar AU, Hortobagyi GN (2003) Estrogen receptors and distinct patterns of breast cancer relapse. Breast Cancer Res Treat 78(1):105–118
46. Koenders PG, Beex LV, Langens R, Kloppenborg PW, Smals AG, Benraad TJ (1991) Steroid hormone receptor activity of primary human breast cancer and pattern of first metastasis. The Breast Cancer Study Group. Breast Cancer Res Treat 18(1):27–32
47. Raemaekers JM, Beex LV, Koenders AJ, Pieters GF, Smals AG, Benraad TJ, Kloppenborg PW (1985) Disease-free interval and estrogen receptor activity in tumor tissue of patients with primary breast cancer: analysis after long-term follow-up. Breast Cancer Res Treat 6(2):123–130
48. Winstanley J, Cooke T, Murray GD, Platt-Higgins A, George WD, Holt S, Myskov M, Spedding A, Barraclough BR, Rudland PS (1991) The long term prognostic significance of c-erbB-2 in primary breast cancer. Br J Cancer 63(3):447–450
49. Solomayer EF, Diel IJ, Meyberg GC, Gollan C, Bastert G (2000) Metastatic breast cancer: clinical course, prognosis and therapy related to the first site of metastasis. Breast Cancer Res Treat 59(3):271–278
50. Hicks DG, Short SM, Prescott NL, Tarr SM, Coleman KA, Yoder BJ, Crowe JP, Choueiri TK, Dawson AE, Budd GT, Tubbs RR, Casey G, Weil RJ (2006) Breast cancers with brain metastases are more likely to be estrogen receptor negative, express the basal cytokeratin CK5/6, and overexpress HER2 or EGFR. Am J Surg Pathol 30(9):1097–1104. doi:10.1097/01.pas.0000213306.05811.b9
51. 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
52. Planchat E, Durando X, Abrial C, Thivat E, Mouret-Reynier MA, Ferriere JP, Pomel C, Kwiatkowski F, Chollet P, Nabholtz JM (2011) Prognostic value of initial tumor parameters after metastatic relapse. Cancer Invest 29(9):635–643. doi:10.3109/07357907.2011.621911
53. Rosa Mendoza ES, Moreno E, Caguioa PB (2013) Predictors of early distant metastasis in women with breast cancer. J Cancer Res Clin Oncol. doi:10.1007/s00432-012-1367-z
54. Badve S, Dabbs DJ, Schnitt SJ, Baehner FL, Decker T, Eusebi V, Fox SB, Ichihara S, Jacquemier J, Lakhani SR, Palacios J, Rakha EA, Richardson AL, Schmitt FC, Tan PH, Tse GM, Weigelt B, Ellis IO, Reis-Filho JS (2011) Basal-like and triple-negative breast cancers: a critical review with an emphasis on the implications for pathologists and oncologists. Mod Pathol: Off J US Can Acad Pathol, Inc 24(2):157–167. doi:10.1038/modpathol.2010.200
55. Keam B, Im SA, Lee KH, Han SW, Oh DY, Kim JH, Lee SH, Han W, Kim DW, Kim TY, Park IA, Noh DY, Heo DS, Bang YJ (2011) Ki-67 can be used for further classification of triple negative breast cancer into two subtypes with different response and prognosis. Breast Cancer Res 13(2):R22. doi:10.1186/bcr2834
56. Nielsen TO, Hsu FD, Jensen K, Cheang M, Karaca G, Hu Z, Hernandez-Boussard T, Livasy C, Cowan D, Dressler L, Akslen LA, Ragaz J, Gown AM, Gilks CB, van de Rijn M, Perou CM (2004) Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res: Off J Am Assoc Cancer Res 10(16):5367–5374. doi:10.1158/1078-0432.CCR-04-0220
57. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, Pietenpol JA (2011) Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Investig 121(7):2750–2767. doi:10.1172/JCI45014
58. Oka H, Shiozaki H, Kobayashi K, Inoue M, Tahara H, Kobayashi T, Takatsuka Y, Matsuyoshi N, Hirano S, Takeichi M (1993) Expression of E-cadherin cell adhesion molecules in human breast cancer tissues and its relationship to metastasis. Cancer Res 53(7):1696–1701
59. Rimm DL, Sinard JH, Morrow JS (1995) Reduced alpha-catenin and E-cadherin expression in breast cancer. Lab Invest 72(5):506–512
60. Siitonen SM, Kononen JT, Helin HJ, Rantala IS, Holli KA, Isola JJ (1996) Reduced E-cadherin expression is associated with invasiveness and unfavorable prognosis in breast cancer. Am J Clin Pathol 105(4):394–402
61. Chen WC, Obrink B (1991) Cell-cell contacts mediated by E-cadherin (uvomorulin) restrict invasive behavior of L-cells. J Cell Biol 114(2):319–327
62. Frixen UH, Behrens J, Sachs M, Eberle G, Voss B, Warda A, Lochner D, Birchmeier W (1991) E-cadherin-mediated cell-cell adhesion prevents invasiveness of human carcinoma cells. J Cell Biol 113(1):173–185
63. Mareel MM, Behrens J, Birchmeier W, De Bruyne GK, Vleminckx K, Hoogewijs A, Fiers WC, Van Roy FM (1991) Down-regulation of E-cadherin expression in Madin Darby canine kidney (MDCK) cells inside tumors of nude mice. Int J Cancer 47(6):922–928
64. Pierceall WE, Woodard AS, Morrow JS, Rimm D, Fearon ER (1995) Frequent alterations in E-cadherin and alpha- and beta-catenin expression in human breast cancer cell lines. Oncogene 11(7):1319–1326
65. Vleminckx K, Vakaet L Jr, Mareel M, Fiers W, van Roy F (1991) Genetic manipulation of E-cadherin expression by epithelial tumor cells reveals an invasion suppressor role. Cell 66(1):107–119
66. Lipponen P, Saarelainen E, Ji H, Aaltomaa S, Syrjanen K (1994) Expression of E-cadherin (E-CD) as related to other prognostic factors and survival in breast cancer. J Pathol 174(2):101–109. doi:10.1002/path.1711740206
67. Parker C, Rampaul RS, Pinder SE, Bell JA, Wencyk PM, Blamey RW, Nicholson RI, Robertson JF (2001) E-cadherin as a prognostic indicator in primary breast cancer. Br J Cancer 85(12):1958–1963. doi:10.1054/bjoc.2001.2178
68. Ding L, Ellis MJ, Li S, Larson DE, Chen K, Wallis JW, Harris CC, McLellan MD, Fulton RS, Fulton LL, Abbott RM, Hoog J, Dooling DJ, Koboldt DC, Schmidt H, Kalicki J, Zhang Q, Chen L, Lin L, Wendl MC, McMichael JF, Magrini VJ, Cook L, McGrath SD, Vickery TL, Appelbaum E, Deschryver K, Davies S, Guintoli T, Lin L, Crowder R, Tao Y, Snider JE, Smith SM, Dukes AF, Sanderson GE, Pohl CS, Delehaunty KD, Fronick CC, Pape KA, Reed JS, Robinson JS, Hodges JS, Schierding W, Dees ND, Shen D, Locke DP, Wiechert ME, Eldred JM, Peck JB, Oberkfell BJ, Lolofie JT, Du F, Hawkins AE, O’Laughlin MD, Bernard KE, Cunningham M, Elliott G, Mason MD, Thompson DM Jr, Ivanovich JL, Goodfellow PJ, Perou CM, Weinstock GM, Aft R, Watson M, Ley TJ, Wilson RK, Mardis ER (2010) Genome remodelling in a basal-like breast cancer metastasis and xenograft. Nature 464(7291):999–1005. doi:10.1038/nature08989
69. Piccirilli C, Saxena A, Robertson J, Clark W, Ikejiri B, Oldfield E, Ali I (1994) Allelic deletions on chromosome-17 and mutations in the p53 gene in tumors metastatic to brain. Int J Oncol 4(1):37–42
70. Lo NC, Vivenza D, Monteverde M, Lattanzio L, Gojis O, Garrone O, Comino A, Merlano M, Quinlan PR, Syed N, Purdie CA, Thompson A, Palmieri C, Crook T (2012) High frequency of complex TP53 mutations in CNS metastases from breast cancer. Br J Cancer 106(2):397–404. doi:10.1038/bjc.2011.464