The association between vascular endothelial growth factor expression in invasive breast cancer and survival varies with intrinsic subtypes and use of adjuvant systemic therapy: Results from the Nurses' Health Study

Breast Cancer Research and Treatment

Volumn 129, Issue 1, 2011, Pages 175-184

  Liu, Ying ^a   Tamimi, Rulla M ^b   Collins, Laura C ^c   Schnitt, Stuart J ^c   Gilmore, Hannah L ^c   Connolly, James L ^c   Colditz, Graham A ^a,d  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d USA   (United States)

Author keywords

Angiogenesis; Breast cancer; Prognosis; Survival; Vascular endothelial growth factor

Indexed keywords

ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HORMONE; VASCULOTROPIN;

ADULT; ARTICLE; BREAST CANCER; CANCER ADJUVANT THERAPY; CANCER HORMONE THERAPY; CANCER INVASION; CANCER MORTALITY; CANCER RADIOTHERAPY; CANCER RECURRENCE; CANCER SURGERY; CANCER SURVIVAL; COHORT ANALYSIS; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MASTECTOMY; PRIORITY JOURNAL; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; PROTEIN EXPRESSION; TISSUE MICROARRAY;

ADULT; ANTINEOPLASTIC AGENTS, HORMONAL; BREAST NEOPLASMS; CHEMOTHERAPY, ADJUVANT; FEMALE; HUMANS; MIDDLE AGED; NEOPLASM INVASIVENESS; NEOPLASM STAGING; PROGNOSIS; RECEPTOR, ERBB-2; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; RISK FACTORS; TREATMENT OUTCOME; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 79960847024     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-011-1432-3     Document Type: Article

References (38)

1. J Folkman 1992 The role of angiogenesis in tumor growth Semin Cancer Biol 3 65 71 1378311 1:STN:280:DyaK38zivFOgtA%3D%3D
2. N Weidner JP Semple WR Welch J Folkman 1991 Tumor angiogenesis and metastasis-correlation in invasive breast carcinoma N Engl J Med 324 1 8 1701519 10.1056/NEJM199101033240101 1:STN:280:DyaK3M%2FnsVWquw%3D%3D
3. AM Mercurio EA Lipscomb RE Bachelder 2005 Non-angiogenic functions of VEGF in breast cancer J Mammary Gland Biol Neoplasia 10 283 290 16924371 10.1007/s10911-006-9001-9 (Pubitemid 44256408)
4. MP Barr DJ Bouchier-Hayes JJ Harmey 2008 Vascular endothelial growth factor is an autocrine survival factor for breast tumour cells under hypoxia Int J Oncol 32 41 48 18097541 1:CAS:528:DC%2BD1cXhtVOltbs%3D (Pubitemid 351176060)
5. Y Liang RA Brekken SM Hyder 2006 Vascular endothelial growth factor induces proliferation of breast cancer cells and inhibits the anti-proliferative activity of anti-hormones Endocr Relat Cancer 13 905 919 16954439 10.1677/erc.1.01221 1:CAS:528:DC%2BD28Xhtlequr3O (Pubitemid 44763266)
6. A Rice CM Quinn 2002 Angiogenesis, thrombospondin, and ductal carcinoma in situ of the breast J Clin Pathol 55 569 574 12147647 10.1136/jcp.55.8.569 1:STN:280:DC%2BD38zpvVCmsA%3D%3D
7. F De Paola AM Granato E Scarpi F Monti L Medri S Bianchi D Amadori A Volpi 2002 Vascular endothelial growth factor and prognosis in patients with node-negative breast cancer Int J Cancer 98 228 233 11857413 10.1002/ijc.10118 (Pubitemid 34150807)
8. D Fuckar A Dekanic S Stifter E Mustac M Krstulja F Dobrila N Jonjic 2006 VEGF expression is associated with negative estrogen receptor status in patients with breast cancer Int J Surg Pathol 14 49 55 16501835 10.1177/ 106689690601400109 1:CAS:528:DC%2BD28XhvFGgs7s%3D (Pubitemid 43221616)
9. I Kostopoulos P Arapantoni-Dadioti H Gogas S Papadopoulos V Malamou-Mitsi CD Scopa S Markaki E Karagianni V Kyriakou A Margariti E Kyrkou K Pavlakis T Zaramboukas A Skordalaki A Bourli C Markopoulos D Pectasides MA Dimopoulos D Skarlos G Fountzilas 2006 Evaluation of the prognostic value of HER-2 and VEGF in breast cancer patients participating in a randomized study with dose-dense sequential adjuvant chemotherapy Breast Cancer Res Treat 96 251 261 16538542 10.1007/s10549-005-9062-2 1:CAS:528:DC%2BD28XjtlWnsbw%3D
10. G Vogl H Bartel O Dietze C Hauser-Kronberger 2006 HER2 is unlikely to be involved in directly regulating angiogenesis in human breast cancer Appl Immunohistochem Mol Morphol 14 138 145 16785780 10.1097/01.pai.0000168591.58721. a6 1:CAS:528:DC%2BD28XntFelsLo%3D (Pubitemid 43941175)
11. P Manders LV Beex VC Tjan-Heijnen J Geurts-Moespot TH Van Tienoven JA Foekens CG Sweep 2002 The prognostic value of vascular endothelial growth factor in 574 node-negative breast cancer patients who did not receive adjuvant systemic therapy Br J Cancer 87 772 778 12232762 10.1038/sj.bjc.6600555 1:STN:280:DC%2BD38vntVGjtA%3D%3D (Pubitemid 35178755)
12. B Linderholm J Bergqvist H Hellborg U Johansson M Linderholm E von Schoultz G Elmberger L Skoog J Bergh 2009 Shorter survival-times following adjuvant endocrine therapy in oestrogen- and progesterone-receptor positive breast cancer overexpressing HER2 and/or with an increased expression of vascular endothelial growth factor Med Oncol 26 480 490 19130322 10.1007/s12032-008-9157-9 1:CAS:528:DC%2BD1MXhsVKhurrL
13. H Bando HA Weich M Brokelmann S Horiguchi N Funata T Ogawa M Toi 2005 Association between intratumoral free and total VEGF, soluble VEGFR-1, VEGFR-2 and prognosis in breast cancer Br J Cancer 92 553 561 15668703 1:CAS:528:DC%2BD2MXhtFWntL0%3D (Pubitemid 40395537)
14. A Ribeiro-Silva F Ribeiro do Vale S Zucoloto 2006 Vascular endothelial growth factor expression in the basal subtype of breast carcinoma Am J Clin Pathol 125 512 518 16627261 1:CAS:528:DC%2BD28XjslGmsL4%3D
15. CL Roland SP Dineen KD Lynn LA Sullivan MT Dellinger L Sadegh JP Sullivan DS Shames RA Brekken 2009 Inhibition of vascular endothelial growth factor reduces angiogenesis and modulates immune cell infiltration of orthotopic breast cancer xenografts Mol Cancer Ther 8 1761 1771 19567820 10.1158/1535-7163.MCT- 09-0280 1:CAS:528:DC%2BD1MXosVynu78%3D
16. K Miller M Wang J Gralow M Dickler M Cobleigh EA Perez T Shenkier D Cella NE Davidson 2007 Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer N Engl J Med 357 2666 2676 18160686 10.1056/NEJMoa072113 1:CAS:528:DC%2BD1cXisVOnsg%3D%3D
17. MR Kim HS Choi JW Yang BC Park JA Kim KW Kang 2009 Enhancement of vascular endothelial growth factor-mediated angiogenesis in tamoxifen-resistant breast cancer cells: role of Pin1 overexpression Mol Cancer Ther 8 2163 2171 19671742 10.1158/1535-7163.MCT-08-1061 1:CAS:528:DC%2BD1MXpvFCnu74%3D
18. SF Dent 2009 The role of VEGF in triple-negative breast cancer: where do we go from here? Ann Oncol 20 1615 1617 19690059 10.1093/annonc/mdp410 1:STN:280:DC%2BD1MnktVCnsg%3D%3D
19. BK Linderholm H Hellborg U Johansson G Elmberger L Skoog J Lehtio R Lewensohn 2009 Significantly higher levels of vascular endothelial growth factor (VEGF) and shorter survival times for patients with primary operable triple-negative breast cancer Ann Oncol 20 1639 1646 19549711 10.1093/annonc/mdp062 1:STN:280:DC%2BD1MnjvFyitQ%3D%3D
20. L Ryden K Jirstrom M Haglund O Stal M Ferno 2010 Epidermal growth factor receptor and vascular endothelial growth factor receptor 2 are specific biomarkers in triple-negative breast cancer. Results from a controlled randomized trial with long-term follow-up Breast Cancer Res Treat 120 491 498 20135347 10.1007/s10549-010-0758-6 1:CAS:528:DC%2BC3cXjtlahtbY%3D
21. S Ghosh CA Sullivan MP Zerkowski AM Molinaro DL Rimm RL Camp GG Chung 2008 High levels of vascular endothelial growth factor and its receptors (VEGFR-1, VEGFR-2, neuropilin-1) are associated with worse outcome in breast cancer Hum Pathol 39 1835 1843 18715621 10.1016/j.humpath.2008.06.004 1:CAS:528:DC%2BD1cXhtlyltbzK
22. BK Linderholm S Gruvberger-Saal M Ferno PO Bendahl P Malmstrom 2008 Vascular endothelial growth factor is a strong predictor of early distant recurrences in a prospective study of premenopausal women with lymph-node negative breast cancer Breast 17 484 491 18508268 10.1016/j.breast.2008.02.010
23. AM Cimpean M Raica C Suciu D Tatucu S Sarb AM Muresan 2008 Vascular endothelial growth factor A (VEGF A) as individual prognostic factor in invasive breast carcinoma Rom J Morphol Embryol 49 303 308 18758633
24. Y Nieto J Woods F Nawaz A Baron RB Jones EJ Shpall S Nawaz 2007 Prognostic analysis of tumour angiogenesis, determined by microvessel density and expression of vascular endothelial growth factor, in high-risk primary breast cancer patients treated with high-dose chemotherapy Br J Cancer 97 391 397 17609662 10.1038/sj.bjc.6603875 1:CAS:528:DC%2BD2sXotlSgtro%3D (Pubitemid 47196747)
25. JD Marotti LC Collins R Hu RM Tamimi 2010 Estrogen receptor-beta expression in invasive breast cancer in relation to molecular phenotype: results from the Nurses' Health Study Mod Pathol 23 197 204 19898422 10.1038/modpathol.2009.158 1:CAS:528:DC%2BC3cXhsVyjur8%3D
26. MD Holmes WY Chen L Li E Hertzmark D Spiegelman SE Hankinson 2010 Aspirin intake and survival after breast cancer J Clin Oncol 28 1467 1472 20159825 10.1200/JCO.2009.22.7918 1:CAS:528:DC%2BC3cXltFGhsLw%3D
27. RM Tamimi HJ Baer J Marotti M Galan L Galaburda Y Fu AC Deitz JL Connolly SJ Schnitt GA Colditz LC Collins 2008 Comparison of molecular phenotypes of ductal carcinoma in situ and invasive breast cancer Breast Cancer Res 10 R67 18681955 10.1186/bcr2128
28. S Dawood R Hu MD Homes LC Collins SJ Schnitt J Connolly GA Colditz RM Tamimi 2011 Defining breast cancer prognosis based on molecular phenotypes: results from a large cohort study Breast Cancer Res Treat 126 185 192 20711652 10.1007/s10549-010-1113-7
29. D Coradini P Boracchi MG Daidone C Pellizzaro P Miodini M Ammatuna G Tomasic E Biganzoli 2001 Contribution of vascular endothelial growth factor to the Nottingham prognostic index in node-negative breast cancer Br J Cancer 85 795 797 11556826 10.1054/bjoc.2001.2019 1:STN:280:DC%2BD3MrgvF2isw%3D%3D (Pubitemid 33010542)
30. G Gasparini M Toi E Biganzoli R Dittadi M Fanelli A Morabito P Boracchi M Gion 2001 Thrombospondin-1 and -2 in node-negative breast cancer: correlation with angiogenic factors, p53, cathepsin D, hormone receptors and prognosis Oncology 60 72 80 11150912 10.1159/000055300 1:STN:280:DC%2BD3M7hvVSgsQ%3D%3D (Pubitemid 32041435)
31. Z Qu S Van Ginkel AM Roy L Westbrook M Nasrin Y Maxuitenko AR Frost D Carey W Wang R Li WE Grizzle JV Thottassery FG Kern 2008 Vascular endothelial growth factor reduces tamoxifen efficacy and promotes metastatic colonization and desmoplasia in breast tumors Cancer Res 68 6232 6240 18676847 10.1158/0008-5472.CAN-07-5654 1:CAS:528:DC%2BD1cXpt1Wjs74%3D
32. FM Blows KE Driver MK Schmidt A Broeks FE van Leeuwen J Wesseling MC Cheang K Gelmon TO Nielsen C Blomqvist P Heikkila T Heikkinen H Nevanlinna LA Akslen LR Begin WD Foulkes FJ Couch X Wang V Cafourek JE Olson L Baglietto GG Giles G Severi CA McLean MC Southey E Rakha AR Green IO Ellis ME Sherman J Lissowska WF Anderson A Cox SS Cross MW Reed E Provenzano SJ Dawson AM Dunning M Humphreys DF Easton M Garcia-Closas C Caldas PD Pharoah D Huntsman 2010 Subtyping of breast cancer by immunohistochemistry to investigate a relationship between subtype and short and long term survival: a collaborative analysis of data for 10, 159 cases from 12 studies PLoS Med 7 e1000279 20520800 10.1371/journal.pmed.1000279
33. LA Carey CM Perou CA Livasy LG Dressler D Cowan K Conway G Karaca MA Troester CK Tse S Edmiston SL Deming J Geradts MC Cheang TO Nielsen PG Moorman HS Earp RC Millikan 2006 Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study JAMA 295 2492 2502 16757721 10.1001/jama.295.21. 2492 1:CAS:528:DC%2BD28XlsV2rtLw%3D (Pubitemid 43854964)
34. MC Cheang D Voduc C Bajdik S Leung S McKinney SK Chia CM Perou TO Nielsen 2008 Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype Clin Cancer Res 14 1368 1376 18316557 10.1158/1078-0432.CCR-07-1658 1:CAS:528:DC%2BD1cXislSrs7o%3D (Pubitemid 351413917)
35. AM Mulligan D Pinnaduwage SB Bull FP O'Malley IL Andrulis 2008 Prognostic effect of basal-like breast cancers is time dependent: evidence from tissue microarray studies on a lymph node-negative cohort Clin Cancer Res 14 4168 4174 18593996 10.1158/1078-0432.CCR-07-4543 1:CAS:528:DC%2BD1cXnvFyksr4%3D
36. H Trihia S Murray K Price RD Gelber R Golouh A Goldhirsch AS Coates J Collins M Castiglione-Gertsch BA Gusterson 2003 Ki-67 expression in breast carcinoma: its association with grading systems, clinical parameters, and other prognostic factors-a surrogate marker? Cancer 97 1321 1331 12599241 10.1002/cncr.11188 1:CAS:528:DC%2BD3sXisVKhuro%3D (Pubitemid 36237320)
37. T Sorlie CM Perou R Tibshirani T Aas S Geisler H Johnsen T Hastie MB Eisen M van de Rijn SS Jeffrey T Thorsen H Quist JC Matese PO Brown D Botstein P Eystein Lonning AL Borresen-Dale 2001 Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications Proc Natl Acad Sci USA 98 10869 10874 11553815 10.1073/pnas.191367098 1:CAS:528: DC%2BD3MXntVGmsbo%3D (Pubitemid 32878711)
38. C Sotiriou SY Neo LM McShane EL Korn PM Long A Jazaeri P Martiat SB Fox AL Harris ET Liu 2003 Breast cancer classification and prognosis based on gene expression profiles from a population-based study Proc Natl Acad Sci USA 100 10393 10398 12917485 10.1073/pnas.1732912100 1:CAS:528:DC%2BD3sXntFynsrk%3D (Pubitemid 37071889)