Associations Between Dynamic Contrast Enhanced Magnetic Resonance Imaging and Clinically Relevant Histopathological Features in Breast Cancer. A Multicenter Analysis

doi:10.21203/rs.3.rs-111377/v1

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Associations Between Dynamic Contrast Enhanced Magnetic Resonance Imaging and Clinically Relevant Histopathological Features in Breast Cancer. A Multicenter Analysis

https://doi.org/10.21203/rs.3.rs-111377/v1

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published 30 Dec, 2021

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Background: To provide evident data regarding relationships between quantitative dynamic contrast enhanced magnetic resonance imaging (DCE MRI) and prognostic factors in breast cancer (BC).

Methods: Data from 4 centers (200 female patients, mean age, 51.2 ± 11.5 years) were acquired. The following data were collected: histopathological diagnosis, tumor grade, stage, hormone receptor status, KI 67, and DCE MRI values including K_trans (volume transfer constant), V_e (volume of the extravascular extracellular leakage space (EES) and K_ep (diffusion of contrast medium from the EES back to the plasma).

DCE MRI values between different groups were compared using the Mann–Whitney U test and by the Kruskal-Wallis H test. The association between DCE MRI and Ki 67 values was calculated by Spearman’s rank correlation coefficient.

Results: DCE MRI values of different tumor subtypes overlapped significantly. There were no statistically significant differences of DCE MRI values between different tumor grades. All DCE MRI parameters correlated with KI 67: K_trans, r = 0.44, p=0.0001; V_e, r = 0.34, p=0.0001; K_ep, r = 0.28, p=0.002. ROC analysis identified a K_trans threshold of 0.3 min^-1for discrimination of tumors with low KI 67 expression (<25%) and high KI 67 expression (≥25%): sensitivity, 75.5%, specificity, 73.0%, accuracy, 74.0%, AUC, 0.78. DCE MRI values overlapped between tumors with different T and N stages.

Conclusion: K_trans, K_ep, and V_e cannot be used as reliable a surrogate marker for hormone receptor status, tumor stage and grade in BC. K_trans may discriminate lesions with high and lower proliferation activity.

Cancer Biology

Oncology

breast cancer

DCE MRI

KI 67

hormone receptor

Breast cancer (BC) is the most common noncutaneous malignancy among women, representing 4 in 10 female cancer patients in the United States [1]. Radiological imaging plays an essential role in the diagnosis and staging of BC. Moreover, imaging can also predict some clinically important histopathological features like expression of proliferation marker KI 67 [2, 3]. So far, it has been shown that rim enhancement on dynamic magnetic resonance imaging (MRI) was associated with high expression of KI 67 and poor prognosis of BC [3]. Similarly, numerous studies analyzed the role of diffusion weighted imaging (DWI) in characterization of BC [4–7]. Some authors observed statistically significant correlations between apparent diffusion coefficient and expression of KI 67 [6, 7], as well as with hormone receptor status [8, 9]. However, it is a known phenomenon that frequently large studies do not confirm promising results of preliminary reports based on small numbers of patients/tumors. In fact, multicenter studies showed that ADC cannot reflect KI 67 and hormone receptor expression in BC [10, 11].

Previously, some reports also indicated that dynamic contrast enhanced MRI (DCE MRI) can be used as imaging biomarker in BC [6, 12, 13]. According to the literature, quantitative parameters of DCE MRI, namely volume transfer constant (K_trans), volume of the extravascular extracellular leakage space (V_e), and diffusion of contrast medium from the EES back to the plasma (K_ep) reflect different histopathological features in BC [6, 12, 13]. For example, Kang et al. showed that triple negative BC exhibited higher K_trans and K_ep in comparison to luminal cancers (P < 0.05) [13]. Furthermore, estrogen receptor (ER) negative tumors had higher K_trans than ER-positive tumors (P < 0.05) and progesterone receptor (PR) negative tumors presented higher V_e than PR-positive tumors (P < 0.05) [13]. Finally, tumors with higher KI 67 showed higher K_ep than tumors with lower Ki-67 (P < 0.05) [13]. Nagasaka et al. reported that the mean of V_e was lower in cancers with a high KI 67 index than in cancers with low KI 67 (P = 0.002) [14].

However, other authors did not find significant associatiations between V_e, K_ep and expression of KI 67 in BC [15].

The purpose of the present study was to provide evident data about relationships between DCE MRI parameters and clinically relevant histopathological features in BC.

Data acquisition and Patients

The present analysis was approved by the institutional review board (Number: 36/20, Otto-von-Guericke University, Magdeburg).

For analysis of associations between imaging and histopathology in BC a multicenter work group was established [10, 11]. For this study, the partners of our work group were contacted via email with the request to provide the data regarding DCE MRI in BC. There were the following centers:

Medical Research Institute, Pusan National University School of Medicine, Busan, Republic of Korea and Department of Radiology, Pusan National University Hospital, Busan, Republic of Korea (center 1);
RCCS SDN, Istituto di Ricerca, Naples, Italy (center 2);
Advanced Imaging Research Center, Oregon Health & Science University, Portland, OR, USA (center 3);
Departments of Biomedical Engineering, Diagnostic Medicine, and Oncology

Livestrong Cancer Institutes Oden Institute of Computational and Engineering Sciences The University of Texas at Austin, USA (center 4).

For every case of the investigated patients/tumors the following data were collected: age, precise histopathological diagnosis, tumor grade, tumor stage, hormone receptor status, KI 67 index, and DCE MRI values including K_trans or volume transfer constant, V_e or volume of the extravascular extracellular leakage space (EES) and K_ep or diffusion of contrast medium from the EES back to the plasma.

The acquired sample comprises 200 patients (Table 1). In every case, breast MRI was performed on a clinical scanner with dedicated breast radiofrequency coil. MR scanners and imaging protocols varied across the centers.

Table 1

Data regarding patients acquisition and technical details of breast DCE MRI in the involved centers
Center	Data acquisition	Patients, n (%)	MR scanner	DCE Sequence	TR/TE, ms	Slice thickness, mm	Field of view, mm	Contrast medium
1	prospective	80 (40.0%)	3T system (Trio Tim, Siemens Healthcare, Erlangen, Germany)	VIBE	3.5/3.1	2	320 × 320	gadobutrol (Gadovist; Bayer Schering Pharma, Berlin, Germany)
2	prospective	42 (21.0%)	3T system (Biograph, Siemens Healthcare, Erlangen, Germany)	VIBE	5.3/1.9	3.6	356 × 379	Gadopentate dimeglumine (Gd-DTPA; Magnevist, Bayer Pharma AG, Berlin, Germany
3	prospective	49 (24.5%)	3T system (Trio Tim, Siemens Healthcare, Erlangen, Germany)	TWIST	6.2/2.9	1.4	320 × 320	ProHance (Bracco Diagnostic Inc.)
4	retrospective	29 (14.5%)	Philips 3T Achieva MR scanner (Philips Healthcare, Best, The Netherlands)	RF-spoiled 3D gradient echo	7.9/1.3	5	220 × 220	Gadopentate dimeglumine (Gd-DTPA; Magnevist Wayne, NJ
VIBE, Volumetric Interpolated Breath-hold Examination
TWIST, Time-resolved angiography WIth Stochastic Trajectories;
RF, radio frequency

Statistical analysis

Continuous variables were described by mean value and standard deviation. Categorical variables were given as relative frequencies. The comparison of DCE MRI values in groups was performed by Mann-Whitney-U tests where the p-values are adjusted for multiple testing (Bonferroni correction). The association between DCE MRI values and KI 67 values was calculated by Spearman’s rank correlation coefficient. Sensitivity, specificity, negative and positive predictive values, accuracy, and area under the receiver operating characteristic curve (AUC) value were calculated for the diagnostic procedures. Thresholds are chosen to maximize the Youden index.

A total of 200 female patients, mean age, 51.2 ± 11.5 years was acquired for this study. The patients had a variety of different breast tumor histologic types (Table 2). The majority of tumors were invasive ductal carcinoma (IDC, 81.95%) with a limited number of other histopathological subypes.

Table 2

Tumor subtypes
Subtype	n (%)
Invasive ductal carcinoma	167 (83.5)
Invasive lobular carcinoma	6 (3.0)
Mucinous breast cancer	3 (1.5)
No special type	24 (12.0)
Receptor status
Luminal A	49 (24.5)
Luminal B	84 (42.0)
HER 2+	32 (16.0)
Triple negative	19 (9.5)
Not available	16 (8.0)
Tumor grade
1	25 (12.5)
2	96 (48.0)
3	79 (39.5)
T stage
1	73 (36.5)
2	78 (39.0)
3	22 (11.0)
4	27 (13.5)
N stage
0	104 (52.0)
1	51 (25.5)
2	22 (11.0)
3	23 (11.5)
M stage
0	186 (93.0)
1	14 (7.0)

The DCE MRI values (M ± SD) of the tumors were as follows: K_trans, 0.33 ± 0.65 min^− 1; V_e, 0.48 ± 0.41%; K_ep, 0.60 ± 0.60 min^− 1.

DCE MRI parameters and hormone receptor status

Hormone receptor status was available for 184 cases. Most frequently, luminal B cancers was diagnosed (Table 3). DCE MRI values in different BC subtypes are given in Table 4. Triple negative cancers had highest K_trans values, luminal B cancers had highest K_ep and V_e values, and HER 2 + BC had lowest K_trans and V_e values. There were no significant differences between K_trans and K_ep values in the BC subtypes. V_e values were different among the tumors with several receptor expressions (p = 0.003). However, all DCE MRI values of different tumor subtypes overlapped significantly (Fig. 1).

Table 3

DCE MRI values in BC with different hormone receptor status
	Luminal A cancer	Luminal B cancer	HER 2 + cancer	Triple negative cancer	P values
K_trans, min^− 1	0.24 ± 0.27	0.44 ± 0.44	0.22 ± 0.50	0.53 ± 1.71	0.161
V_e, %	0.50 ± 0.43	0.61 ± 0.43	0.30 ± 0.23	0.44 ± 0.44	0.003
K_ep, min^− 1	0.47 ± 0.31	0.72 ± 0.53	0.56 ± 0.58	0.62 ± 1.33	0.159

Table 4

DCE MRI values in BC with different tumor grades
	Grade 1	Grade 2	Grade 3	P values
K_trans, min^− 1	0.12 ± 0.10	0.32 ± 0.44	0.42 ± 0.90	0.135
V_e, %	0.35 ± 0.29	0.49 ± 0.39	0.52 ± 0.46	0.225
K_ep, min^− 1	0.34 ± 0.16	0.60 ± 0.54	0.67 ± 0.75	0.064

DCE MRI parameters and tumor grade

DCE MRI values in different tumor grades are given in Table 4. All DCE MRI values increased with tumor grade. However, there were no significant differences of DCE MRI values between several tumor grades and all DCE MRI values of different tumor types overlapped significantly (Fig. 2).

DCE MRI values and expression of KI 67

The level of the proliferation index KI 67 was available for 123 tumors. The mean value was 27.4 ± 23.6%, median value, 20%, range 1% – 90%.

All DCE MRI parameters correlated with KI 67. The correlation coefficients were as follows: K_trans, r = 0.44, p = 0.0001; V_e, r = 0.34, p = 0.0001; K_ep, r = 0.28, p = 0.002.

On the next step, ROC analysis was performed for distinguishing tumors with high proliferative potential from tumors with low proliferation rate using DCE MRI values. A KI 67 value of 25% was used as the threshold in discrimination between tumors with low KI 67 expression (< 25%) and high KI 67 expression (≥ 25%). Youden index identified threshold values of K_trans, V_e, and K_ep (Table 5). K_trans cut-off value of 0.3 min^− 1 showed best results (Fig. 3). Furthermore, other threshold values of KI 67 ranging from 10–50% were also analyzed (Table 6). DCE MRI values had low area under the curve for every KI 67 thresholds.

Table 5

Threshold values of K_trans, V_e, and K_ep for discrimination of tumors with high (> 25%) expression of KI 67
	Threshold	Sensitivity	Specificity	PPV	NPV	Accuracy
K_trans, min^− 1	0.3	75.5%	73.0%	64.9%	81.8%	74.0%
V_e, %	0.5	73.5%	66.2%	59.0%	79.0%	69.1%
K_ep, min^− 1	0.55	63.3%	63.5%	53.4%	72.3%	63.4%

Table 6

Areas under the curve for discrimination of tumors with different expression of KI 67 based on DCE MRI values
	KI 67 level
	≥ 10%	≥ 20%	≥ 30%	≥ 40%	≥ 50%
K_trans	0.72	0.77	0.70	0.74	0.68
V_e	0.67	0.73	0.64	0.63	0.55
K_ep	0.63	0.67	0.67	0.72	0.70

DCE MRI parameters and T stage

DCE MRI values differed significantly among the tumors with different T stages (Table 7). Carcinomas with T4 stage showed highest DCE MRI values in comparison to other tumor stages. However, DCE MRI values overlapped between the subgroups (Fig. 4).

Table 7

DCE MRI values in BC with different tumor (T) stages
	T1	T2	T3	T4	P values
K_trans, min^− 1	0.18 ± 0.13	0.27 ± 0.37	0.14 ± 0.17	1.08 ± 1.44	0.001
V_e, %	0.37 ± 0.19	0.44 ± 0.39	0.36 ± 0.33	0.99 ± 0.57	0.001
K_ep, min^− 1	0.50 ± 0.29	0.54 ± 0.41	0.36 ± 0.23	1.21 ± 1.26	0.001

DCE MRI parameters and nodal tumor stage

Overall, in 104 BC N0 and in 96 BC N + stages were diagnosed. All DCE MRI values were statistically significant higher in N + tumors than in N0 lesions (Table 8). However, the graphical distribution of DCE MRI values showed that they overlapped between the subgroups (Fig. 5). Furthermore, ROC analysis also showed that DCE MRI values had very low areas under the curve in prediction of nodal stage in BC (Fig. 6).

Table 8

Comparison of DCE MRI values in BC with and without nodal metastases
	BC with N0 stage, M ± SD	BC with N + stage, M ± SD	P values
K_trans, min^− 1	0.17 ± 0.15	0.50 ± 0.89	0.001
V_e, %	0.37 ± 0.21	0.60 ± 0.52	0.001
K_ep, min^− 1	0.48 ± 0.34	0.72 ± 0.79	0.007

The present study is the first multicenter project regarding associations between DCE MRI and clinically relevant histopathological features in BC.

Previously, the role of DCE MRI was analyzed systematically in prostate cancer, glioma, and squamous cell carcinoma of the head and neck region. In prostate cancer, it was shown that K_trans values were significantly higher for high-grade versus low-grade lesions [16]. Furthermore, K_ep correlated positively with mean blood vessel count and mean vessel area [17]. In glioma, K_trans and V_e values of grade 2 tumors were significantly lower than those of grade 3 [18]. Moreover, K_trans and V_e significantly correlated with the KI 67 index [18]. Finally, K_trans showed a significant positive correlation with VEGF expression in high grade gliomas (r = 0.505, P < 0.001) [19]. Also in head and neck squamous cell carcinomas DCE MRI can predict relevant histopathological features. So far, K_trans correlated well with expression of Ki 67 and V_e with the mean microvessel diameter [20].

In BC, only few studies reported data about associations between DCE MRI and histopathology. The published results are promising. For instance, it has been shown that parameters of DCE MRI were different in tumors with different hormone receptor expression and grade. So far, grade 3 cancers had higher K_trans and K_ep values in comparison to grade 1 lesions [12, 13]. Mean V_e was lower in tumors with a high histologic grade than in tumors with a low histologic grade [12]. Regarding expression of hormone receptors, triple negative BC showed higher K_trans and K_ep, but lower V_e values than luminal BC [13]. Furthermore, Ve correlated inversely with HER 2 expression [21].

Our data showed that HER 2 rich BC had lowest K_trans and V_e values in comparison to other subtypes. Furthermore, triple negative BC had highest K_trans values. However, as shown, values of DCE MRI overlapped significantly and, therefore, cannot be used for prediction of hormone receptor status in BC in clinical practice.

Furthermore, our data indicated that DCE MRI parameters did not reflect tumor grade in BC.

Another important aspect in BC is expression of proliferation marker KI 67. It is well known that high expression of KI 67 is associated with a greater risk of death compared with lower expression rates [22]. Therefore, prediction of proliferation potential of BC based on imaging is very important. According to previous reports, parameters of DCE MRI are associated with KI 67 index. However, the reported data are controversial [12, 13, 21, 23]. For example, Kang et al. showed that carcinomas with high expression KI 67 showed statistically significant higher Kep values in comparison to BC with low expression of KI 67 and K_trans and V_e values did not differ between the tumors [13]. Liu et al. found that only K_trans correlated with KI 67 [21]. Koo et al. did not observed statistically significant associations between DCE MRI values and KI 67 [12]. Finally, Kim et al. observed significant relationships between K_trans, K_ep and KI 67, but not between V_e and KI 67 [23]. Moreover, the previous studies used different thresholds of KI 67 expression for distinguishing tumors with low and high proliferation activity, namely 15% [13], 10% [21], and 5% [12]. In one study two threshold values, 5% and 15% were analyzed [23]. This fact relativizes the reported results. According to a large meta analysis based on data of 64,196 patients, the optimal KI 67 cut-off is 25% [22].

In the present work, KI 67 correlated statistically significant with all DCE MRI parameters. The strongest correlation was observed with K_trans (r = 0.44, p = 0.0001). However, the optimal threshold of K_trans to discriminate BC with high (> 25%) and low (< 25%) expression of KI 67 yielded a relatively low sensitivity (75.5%) and specificity (73.0%), as well as low accuracy (74.0%). Also, this applied for several alternate thresholds of KI 67 expression ranging from 10–50%.

Another important clinical question is, if imaging features of primary tumors can predict occurrence of nodal and/or distant metastases. Previously, it has been indicated that some MRI features of BC were associated with occurrence of nodal metastases [24]. Regarding DCE MRI, presumably, perfusion parameters of primary tumor may be able to predict occurrence of lymph node metastases. In fact, BC with lymphovascular space invasion (LVSI) had higher K_trans and K_ep than tumors without LVSI [13]. Our results, however, did not confirm this hypothesis. Although DCE MRI parameters of BC differed between N0 vs N + stages, all of them overlapped significantly. Therefore, parameters of DCE MRI obtained from primary tumors cannot be used for prediction of nodal stage in BC.

The present multicenter study is the largest to date. However, there are some limitations to address. The involved patients were investigated on different MR scanners with different technical parameters like field strength and other technical parameters. Furthermore, one center acquired patients with BC retrospectively with appropriate bias. Our sample consist predominantly on invasive ductal carcinomas. Therefore, this study could not compare DCE MRI values between different tumor types. Presumably, other types like lobular or mucinous carcinomas may have different DCE MRI parameters than ductal carcinomas.

Our multicenter study showed that DCE MRI parameters K_trans, K_ep, and V_e cannot be used as reliable a surrogate marker for hormone receptor status, tumor stage and grade in BC. K_trans correlated moderately with expression of KI 67 and may discriminate lesions with high and lower proliferation activity.

BC, breast cancer

DCE MRI, dynamic contrast enhanced magnetic resonance imaging

K_trans, volume transfer constant;

V_e,volume of the extravascular extracellular leakage space;

K_ep, diffusion of contrast medium from the extravascular extracellular leakage space back to the plasma

Ethics approval and consent to participate

The study protocol was approved by the Ethics Committee of the Medical Faculty of the Otto-von-Guericke-University Magdeburg.

Funding

None

Availability of data and materials

The data that support the findings of this study are available from professor Surov but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. Data are however available from the authors upon reasonable request and with permission of professor Surov.

Consent for publication

Not applicable

Competing interests

The authors declare that they have no competing interests

Acknowledgements

none

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Journal Publication

published 30 Dec, 2021

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Associations Between Dynamic Contrast Enhanced Magnetic Resonance Imaging and Clinically Relevant Histopathological Features in Breast Cancer. A Multicenter Analysis

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Journal Publication

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Abstract

Figures

Background

Methods

Data acquisition and Patients

Statistical analysis

Results

Discussion

Conclusions

Abbreviations

Declarations

References

Status:

Journal Publication

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