Breast parenchymal signal enhancement ratio at preoperative magnetic resonance imaging: association with early recurrence in triple-negative breast cancer patients
Restricted accessResearch articleFirst published online July, 2016
Breast parenchymal signal enhancement ratio at preoperative magnetic resonance imaging: association with early recurrence in triple-negative breast cancer patients
The signal enhancement ratio (SER) of surrounding non-tumor parenchyma at breast magnetic resonance imaging (MRI) can be helpful in breast cancer patients, but has not been investigated in patients with triple negative breast cancer (TNBC).
Purpose
To investigate the association between background parenchymal SER around the tumor on preoperative dynamic contrast-enhanced MRI with recurrence-free survival in patients with TNBC.
Material and Methods
Between April 2012 and May 2013, 71 TNBC patients who underwent preoperative MRI were included. SER values were calculated from regions of interest placed in the breast parenchyma around the tumor. Cox proportional hazards models were used to determine associations between MRI variables, clinical-pathologic variables, and recurrence-free survival.
Results
Recurrence occurred in 8.5% (6/71) of patients. At univariate analysis, a higher SER around the tumor, larger tumor size, lymphovascular invasion, lymph node metastasis, receipt of neoadjuvant chemotherapy, receipt of total mastectomy, and not receiving adjuvant chemotherapy were associated with worse recurrence-free survival. At multivariate analysis of preoperative variables, a higher SER around the tumor was independently associated with worse recurrence-free survival (hazard ratio [HR] = 7.072, P = 0.003 for SER1; HR = 6.268, P = 0.006 for SER2; HR = 3.004, P = 0.039 for SER3).
Conclusion
Higher SER around the tumor at preoperative dynamic contrast-enhanced MRI is an independent predictor for recurrence in TNBC patients.
PerouCMSorlieTEisenMB. Molecular portraits of human breast tumours. Nature2000; 406: 747–752.
2.
SotiriouCNeoSYMcShaneLM. Breast cancer classification and prognosis based on gene expression profiles from a population-based study. Proc Natl Acad Sci U S A2003; 100: 10393–10398.
3.
VoducKDCheangMCTyldesleyS. Breast cancer subtypes and the risk of local and regional relapse. J Clin Oncol2010; 28: 1684–1691.
4.
MillarEKGrahamPHO'TooleSA. Prediction of local recurrence, distant metastases, and death after breast-conserving therapy in early-stage invasive breast cancer using a five-biomarker panel. J Clin Oncol2009; 27: 4701–4708.
5.
BhattiABKhanAISiddiquiN. Outcomes of triple-negative versus non-triple-negative breast cancers managed with breast-conserving therapy. Asian Pac J Cancer Prev2014; 15: 2577–2581.
6.
MoranMS. Should triple-negative breast cancer (TNBC) subtype affect local-regional therapy decision making?Am Soc Clin Oncol Educ Book2014; 34: e32–36.
7.
CareyLAPerouCMLivasyCA. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA2006; 295: 2492–2502.
8.
DentRTrudeauMPritchardKI. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res2007; 13: 4429–4434.
9.
Hattangadi-GluthJAWoJYNguyenPL. Basal subtype of invasive breast cancer is associated with a higher risk of true recurrence after conventional breast- conserving therapy. Int J Radiat Oncol Biol Phys2012; 82: 1185–1191.
10.
NguyenPLTaghianAGKatzMS. Breast cancer subtype approximated by estrogen receptor, progesterone receptor, and HER-2 is associated with local and distant recurrence after breast-conserving therapy. J Clin Oncol2008; 26: 2373–2378.
11.
HafftyBGYangQReissM. Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J Clin Oncol2006; 24: 5652–5657.
12.
DakuboGDJakupciakJPBirch-MachinMA. Clinical implications and utility of field cancerization. Cancer Cell Int2007; 7: 2.
13.
HeaphyCMBisoffiMFordyceCA. Telomere DNA content and allelic imbalance demonstrate field cancerization in histologically normal tissue adjacent to breast tumors. Int J Cancer2006; 119: 108–116.
14.
HeaphyCMGriffithJKBisoffiM. Mammary field cancerization: molecular evidence and clinical importance. Breast Cancer Res Treat2009; 118: 229–239.
15.
TrujilloKAHinesWCVargasKM. Breast field cancerization: isolation and comparison of telomerase-expressing cells in tumor and tumor adjacent, histologically normal breast tissue. Mol Cancer Res2011; 9: 1209–1221.
16.
CichonMADegnimACVisscherDW. Microenvironmental influences that drive progression from benign breast disease to invasive breast cancer. J Mammary Gland Biol Neoplasia2010; 15: 389–397.
17.
ChangHYNuytenDSSneddonJB. Robustness, scalability, and integration of a wound-response gene expression signature in predicting breast cancer survival. Proc Natl Acad Sci U S A2005; 102: 3738–3743.
18.
de KruijfEMvan NesJGvan de VeldeCJ. Tumor-stroma ratio in the primary tumor is a prognostic factor in early breast cancer patients, especially in triple-negative carcinoma patients. Breast Cancer Res Treat2011; 125: 687–696.
19.
DekkerTJvan de VeldeCJvan PeltGW. Prognostic significance of the tumor-stroma ratio: validation study in node-negative premenopausal breast cancer patients from the EORTC perioperative chemotherapy (POP) trial (10854). Breast Cancer Res Treat2013; 139: 371–379.
20.
MoormanAMVinkRHeijmansHJ. The prognostic value of tumour-stroma ratio in triple-negative breast cancer. Eur J Surg Oncol2012; 38: 307–313.
21.
HattangadiJParkCRembertJ. Breast stromal enhancement on MRI is associated with response to neoadjuvant chemotherapy. Am J Roentgenol2008; 190: 1630–1636.
22.
KimSAChoNRyuEB. Background parenchymal signal enhancement ratio at preoperative MR imaging: association with subsequent local recurrence in patients with ductal carcinoma in situ after breast conservation surgery. Radiology2014; 270: 699–707.
23.
HammondMEHayesDFDowsettM. American Society of Clinical Oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Clin Oncol2010; 28: 2784–2795.
24.
WolffACHammondMESchwartzJN. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. J Clin Oncol2007; 25: 118–145.
25.
MorrisEComstockCLeeCACR BI-RADS Magnetic Resonance Imaging. In: American College of Radiology (ed). ACR BI-RADS Atlas, Breast Imaging Reporting and Data System, Reston, VA: ACR, 2013.
26.
KingVBrooksJDBernsteinJL. Background parenchymal enhancement at breast MR imaging and breast cancer risk. Radiology2011; 260: 50–60.
27.
KingVGoldfarbSBBrooksJD. Effect of aromatase inhibitors on background parenchymal enhancement and amount of fibroglandular tissue at breast MR imaging. Radiology2012; 264: 670–678.
28.
EngelsBRowleyDASchreiberH. Targeting stroma to treat cancers. Semin Cancer Biol2012; 22: 41–49.
29.
FriedlPAlexanderS. Cancer invasion and the microenvironment: plasticity and reciprocity. Cell2011; 147: 992–1009.
30.
UzzanBNicolasPCucheratM. Microvessel density as a prognostic factor in women with breast cancer: a systematic review of the literature and meta-analysis. Cancer Res2004; 64: 2941–2955.
31.
GujamFJEdwardsJMohammedZM. The relationship between the tumour stroma percentage, clinicopathological characteristics and outcome in patients with operable ductal breast cancer. Br J Cancer2014; 111: 157–165.
32.
EllsworthDLEllsworthRELiebmanMN. Genomic instability in histologically normal breast tissues: implications for carcinogenesis. Lancet Oncol2004; 5: 753–758.
33.
NabavizadehNKlifaCNewittD. Topographic enhancement mapping of the cancer-associated breast stroma using breast MRI. Integr Biol (Camb)2011; 3: 490–496.
34.
LoweryAJKellMRGlynnRW. Locoregional recurrence after breast cancer surgery: a systematic review by receptor phenotype. Breast Cancer Res Treat2012; 133: 831–841.
35.
WangJXieXWangX. Locoregional and distant recurrences after breast conserving therapy in patients with triple-negative breast cancer: a meta-analysis. Surg Oncol2013; 22: 247–255.
36.
StewardLConantLGaoF. Predictive factors and patterns of recurrence in patients with triple negative breast cancer. Ann Surg Oncol2014; 21: 2165–2171.
37.
EliasAD. Triple-negative breast cancer: a short review. Am J Clin Oncol2010; 33: 637–645.
38.
SotiriouCPusztaiL. Gene-expression signatures in breast cancer. N Engl J Med2009; 360: 790–800.
39.
LeeJAKimKIBaeJW. Triple negative breast cancer in Korea-distinct biology with different impact of prognostic factors on survival. Breast Cancer Res Treat2010; 123: 177–187.
40.
Hernandez-AyaLFChavez-MacgregorMLeiX. Nodal status and clinical outcomes in a large cohort of patients with triple-negative breast cancer. J Clin Oncol2011; 29: 2628–2634.
41.
AbdulkarimBSCuarteroJHansonJ. Increased risk of locoregional recurrence for women with T1-2N0 triple-negative breast cancer treated with modified radical mastectomy without adjuvant radiation therapy compared with breast-conserving therapy. J Clin Oncol2011; 29: 2852–2858.
42.
KennedyCRGaoFMargenthalerJA. Neoadjuvant versus adjuvant chemotherapy for triple negative breast cancer. J Surg Res2010; 163: 52–57.
