Journal List > Investig Magn Reson Imaging > v.23(2) > 1130367

Jeong, Choi, Choi, Park, and Song: Prediction of Axillary Lymph Node Metastasis in Early Breast Cancer Using Dynamic Contrast-Enhanced Magnetic Resonance Imaging and Diffusion-Weighted Imaging

Abstract

Purpose

The purpose of this study was to evaluate dynamic contrast-enhanced breast magnetic resonance imaging (DCE-MRI), and diffusion-weighted imaging (DWI) variables, for axillary lymph node (ALN) metastasis in the early stage of breast cancer.

Materials and Methods

January 2011-April 2015, 787 patients with early stage of breast cancer were retrospectively reviewed. Only cases of invasive ductal carcinoma, were included in the patient population. Among them, 240 patients who underwent 3.0-T DCE-MRI, including DWI with b value 0 and 800 s/mm2 were enrolled. MRI variables (adjacent vessel sign, whole-breast vascularity, initial enhancement pattern, quantitative kinetic parameters, signal enhancement ratio (SER), tumor apparent diffusion coefficient (ADC), peritumoral ADC, and peritumor-tumor ADC ratio) clinicopathologic variables (age, T stage, multifocality, extensive intraductal carcinoma component (EIC), estrogen receptor, progesterone receptor, HER-2 status, Ki-67, molecular subtype, histologic grade, and nuclear grade) were compared between patients with axillary lymph node metastasis and those with no lymph node metastasis. Multivariate regression analysis was performed, to determine independent variables associated with ALN metastasis, and the area under the receiver operating characteristic curve (AUC), for predicting ALN metastasis was analyzed, for those variables.

Results

On breast MRI, moderate or prominent ipsilateral whole-breast vascularity (moderate, odds ratio [OR] 3.45, 95% confidence interval [CI] 1.28–9.51 vs. prominent, OR = 15.59, 95% CI 2.52–96.46), SER (OR = 1.68, 95% CI 1.09–2.59), and peritumor-tumor ADC ratio (OR = 6.77, 95% CI 2.41–18.99), were independently associated with ALN metastasis. Among clinicopathologic variables, HER-2 positivity was independently associated, with ALN metastasis (OR = 23.71, 95% CI 10.50–53.54). The AUC for combining selected MRI variables and clinicopathologic variables, was higher than that of clinicopathologic variables (P < 0.05).

Conclusion

SER, moderate or prominent increased whole breast vascularity, and peritumor-tumor ADC ratio on breast MRI, are valuable in predicting ALN metastasis, in patients with early stage of breast cancer.

References

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Fig. 1.
Maximum-intensity-projection image (a) and ADC map (b) in a 70-year-old woman with invasive ductal carcinoma, show the method used for placing ROIs to obtain the tumor ADC, peritumor ADC. Regarding the tumor ADC, the slice with the largest tumor cross section is selected, and the largest oval ROI is placed inside the tumor (b) with reference to the MIP image (a). Mean value of the ROI 1193 × 10-6 mm2/s, is recorded as tumor ADC. For the peritumor ADC, three ROIs are placed where the ADC visually appears to be most increased on breast parenchymal tissue, adjacent to tumor contour on the ADC map (b): the three ROIs are 2328, 2062, and 2646 × 10-6 mm2/s, respectively. Maximum value 2646 × 10-6 mm2/s is recorded as peritumor ADC. ADC=apparent diffusion coefficient; ROI=region of interest
imri-23-125f1.tif
Fig. 2.
A 66-year-old woman with palpable mass (arrows) on the left breast, had pathologically confirmed invasive ductal carcinoma, with axillary lymph node metastasis after surgery. (a) Maximum-intensity-projection images show that the adjacent vessel sign is positive, and increased breast vascularity is prominent. (b) T2-weighted image shows that degree of edema around the tumor, corresponds to grade 1. Peritumor-tumor ADC ratio was calculated, using DWI (c) and ADC (d). On an ADC map, mean value of the tumor ADC, and mean value of three ROIs for peritumor ADC, were 782, 654, and 1615 × 10-6 mm2/s, respectively. So, peritumor-tumor ratio was calculated as 2.0. ADC = apparent diffusion coefficient; DWI = diffusion weighted image; ROI = region of interest
imri-23-125f2.tif
Fig. 3.
Receiver-operating characteristic (ROC) curve of predictive variables in MRI, and clinicopathologic validation, clinicopathologic validation and MRI validation. The area under the receiver operating characteristics curve (AUC) of MRI and clinicopathologic, clinicopathologic, and MRI variables, were 0.879, 0.835, and 0.729, respectively (P < 0.05).
imri-23-125f3.tif
Table 1.
Comparison of Clinicopathologic Variables between No Axillary Lymph Node Metastasis and Axillary Lymph Node Metastasis
Variables No ALN metastasis (n = 148) ALN metastasis (n = 92) P value
Age (years)     0.786
 < 50 67 (45.3) 40 (43.5)  
 ≥ 50 81 (54.7) 52 (56.5)  
T stage     < 0.001
 T1 110 (74.3) 42 (45.7)  
 T2 38 (25.7) 50 (54.4)  
Multifocality     0.318
 Negative 105 (71.0) 59 (64.1)  
 Positive 43 (29.1) 33 (35.9)  
EIC     1.00
 Negative 116 (73.4) 72 (78.3)  
 Positive 32 (21.6) 20 (21.7)  
ER     0.376
 Negative 22 (14.9) 18 (19.6)  
 Positive 126 (85.1) 74 (80.4)  
PR     0.873
 Negative 32 (21.6) 21 (22.8)  
 Positive 116 (78.4) 71 (77.2)  
HER-2     < 0.001
 Negative 134 (90.5) 32 (34.8)  
 Positive 14 (9.5) 60 (65.2)  
Ki67     0.185
 ≤ 14% 85 (57.8) 45 (48.9)  
 > 14% 62 (42.2) 47 (51.1)  
Molecular subtype     < 0.001
 Luminal A 117 (79.1) 28 (30.4)  
 Luminal B 12 (8.1) 47 (51.1)  
 HER-2 enriched 2 (1.4) 13 (14.1)  
 Triple negative 17 (11.5) 4 (4.4)  
Histologic grade     0.679
 I, II 57 (39.9) 33 (36.3)  
 III 86 (60.1) 58 (63.7)  
Nuclear grade     0.567
 I, II 105 (71.0) 62 (67.4)  
 III 43 (29.1) 30 (32.6)  

Numbers in parenthese represent percentages (%).

ALN = axillary lymph node; EIC = extensive intraductal carcinoma component; ER = estrogen receptor; HER-2 = human epidermal growth factor receptor-2; PR = progesterone receptor

Table 2.
Comparison of DCE-MRI and DWI Variables between No Axillary Lymph Node Metastasis and Axillary Lymph Node Metastasis
Variables No ALN metastasis (n = 148) ALN metastasis (n = 92) P value
Adjacent vessel sign     < 0.001
 Negative 87 (58.8) 32 (34.8)  
 Positive 61 (41.2) 60 (65.2)  
Whole breast vascularity     0.001
 Negative 102 (68.9) 46 (50.0)  
 Mild 28 (18.9) 20 (21.7)  
 Moderate 16 (10.8) 14 (15.2)  
 Prominent 2 (1.4) 12 (13.0)  
Quantitative parameters      
 E1* 89.7 ± 65.6 86.6 ± 68.5 0.726
 Epeak* 137.0 ± 104.1 126.4 ± 132.6 0.518
 SER* 0.9 ± 0.5 1.4 ± 1.9 0.017
 TTP* 176.3 ± 89.6 161.1 ± 84.1 0.187
T2WI edema     < 0.001
 Grade 0 66 (44.6) 32 (34.8)  
 Grade 1 56 (37.8) 22 (23.9)  
 Grade 2 26 (17.6) 38 (41.3)  
Diffusion weighted imaging      
 Tumor ADC* (10-6 mm2/s) 1056 ± 249.7 991.1 ± 215.4 0.04
 Peritumor ADC* (10-6 mm2/s) 1451.6 ± 331.2 1588.3 ± 328.5 0.002
 Peritumor-tumor ADC ratio* 1.4 ± 0.3 1.6 ± 0.4 < 0.001

ADC= apparent diffusion coefficient; ALN = axillary lymph node; DCE-MRI = dynamic contrast-enhanced magnetic resonance imaging; E1 = the initial enhancement percentage; Epeak = peak enhancement percentage; SER = signal enhancement ratio; T2WI = T2 weighted image; TTP = time to peak

* Data are mean ± standard deviation.

Table 3.
Univariate Analysis for Clinicopathologic Variables Associated with Axillary Lymph Node Metastasis
Variables Odds Ratio 95% CI P value
Age (years)      
 < 50 1    
 ≥ 50 1.07 0.64–1.81 0.786
T stage      
 T1 1    
 T2 3.45 1.99–5.99 < 0.001
Multifocality      
 Negative 1    
 Positive 1.36 0.78–2.38 0.271
EIC      
 Negative 1    
 Positive 1 0.54–1.89 0.983
PR      
 Negative 1    
 Positive 0.93 0.50–1.74 0.827
HER-2      
 Negative 1    
 Positive 17.94 8.93–36.07 < 0.001
Ki67      
 ≤ 14% 1    
 > 14% 1.42 0.85–2.42 0.179
Molecular subtype     < 0.001
 Luminal A 1    
 Luminal B 16.36 7.68–34.86 < 0.001
 HER-2 enriched 27.15 5.80–127.24 < 0.001
 Triple negative 0.98 0.31–3.15 0.977
Histologic grade      
 I, II 1    
 III 1.18 0.67–2.07 0.561
Nuclear grade      
 I, II 1    
 III 1.16 0.68–2.01 0.582

CI = confidence interval; EIC = extensive intraductal carcinom component; HER-2=human epidermal growth factor receptor-2; PR = progesterone receptor

Table 4.
Univariate Analysis for MRI Variables Associated with Axillary Lymph Node Metastasis
Variables Odds Ratio 95% CI P value
Adjacent vessel sign      
 Negative 1    
 Positive 2.67 1.56–4.59 < 0.001
Whole breast vascularity     0.004
 Negative 1    
 Mild 1.58 0.81–3.10 0.179
 Moderate 1.94 0.87–4.31 0.103
 Prominent 13.3 2.86–61.85 0.001
Quantitative parameters      
 E1 1 0.99–1.00 0.725
 Epeak 1 0.99–1.00 0.494
 SER 1.59 1.10–2.30 0.013
 TTP 1 0.99–1.00 0.194
T2WI Edema     < 0.001
 Grade 0 1    
 Grade 1 0.81 0.42–1.55 0.526
 Grade 2 3.01 1.57–5.79 0.001
Diffusion weighted imaging      
 Tumor ADC (10-6 mm2/s) 1 0.99–1.00 0.043
 Peritumor ADC (10-6 mm2/s) 1 1.00–1.00 0.003
 Peritumor-tumor ADC ratio 8.69 3.73–20.30 < 0.001

ADC = apparent diffusion coefficient; CI = confidence interval; DCE-MRI = dynamic contrast-enhanced magnetic resonance imaging; E1 = the initial enhancement percentage; Epeak = peak enhancement percentage; SER = signal enhancement ratio; T2WI = T2 weighted image; TTP = time to peak

Table 5.
Multivariate Analysis for Factors Associated with Axillary Lymph Node Metastasis
  Variables Odds Ratio (95% CI) P value
MRI variables Whole breast vascularity    
   Negative 1  
   Mild 1.72 (0.69–4.28) 0.240
   Moderate 3.44 (1.24–9.51) 0.017
   Prominent 15.59 (2.52–96.45) 0.003
  SER 1.67 (1.08–2.59) 0.020
  Peritumor-tumo ADC ratio or 6.77 (2.41–18.99) < 0.00
clinicopathologic variables HER-2    
   Negative 1  
   Positive 23.71 (10.50–53.53) 0.020

ADC = apparent diffusion coefficient; CI = confidence interval; HER-2 = huma epidermal growth factor receptor-2; SER = signal enhancement ratio

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