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Egyptian Journal of Radiology and Nuclear Medicine
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Can combined tomosynthesis with unenhanced MRI be used as a predictive tool for lymphovascular invasion?

Egyptian Journal of Radiology and Nuclear Medicine volume 55, Article number: 195 (2024) Cite this article

Abstract

Background

The presence of lymphovascular invasion (LVI) in cases with breast cancer is considered a bad prognostic sign. The purpose of this study is to compare the efficacy of dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) versus unenhanced magnetic resonance imaging (UE-MRI + DBT) in predicting LVI in women with pathologically confirmed breast cancer.

Methods

This prospective self-controlled study enrolled a total of 70 cases of pathologically proven breast cancer. All the patients underwent tomosynthesis, non-contrast, and post-contrast MRI. Depending on the broken halo sign seen in tomosynthesis, peritumoral edema, dark rim diffusion at diffusion-weighted imaging (DWI), and apparent diffusion coefficient (ADC) values evaluated in MRI.

Results

The accuracy of LVI detection by tomosynthesis was 58%; unenhanced and enhanced MRI had the same results at 60%. The accuracy of detecting LVI was raised to 64% by combining the tomosynthesis results with unenhanced MRI.

Conclusions

Tomosynthesis parameters are promising tools in detecting LVI in breast cancer with better diagnostic accuracy in combination with unenhanced MRI.

Introduction

Breast cancer is the most common cancer type in females and the second most common cause of death for women. In terms of prognosis, biomarker expression, and histologic appearance, it is a heterogeneous disease [1]. Conventional tools (full-field digital mammography, breast tomosynthesis, breast ultrasonography, percutaneous image-guided biopsy, and dynamic breast MRI) were traditionally considered the standard imaging modalities for diagnosing and staging breast cancer [2].

Compared to MRI, digital breast tomosynthesis (DBT) is a quick, widely accessible method that produces a 3D reconstruction of the breast and enhances lesion identification and characterization. Our goal is to lower the number of false positive and false negative results [3]. Furthermore, it has no notable contraindications and maintains a high sensitivity for tumor size and a high accuracy for breast cancer detection [4]. To detect breast cancer, dynamic contrast-enhanced (DCE) breast MRI is the most sensitive method currently available. Because of this, during the past 20 years, its usefulness in screening and diagnostic contexts has grown significantly [5].

Presumably, when paired with diffusion-weighted imaging (DWI) and T1-or T2-weighted morphological imaging, unenhanced magnetic resonance imaging (MRI) showed superior sensitivity and accuracy in tumor size assessment and lesion identification when compared to dynamic magnetic resonance imaging (MRI) [6]. Therefore, our goal was to compare the efficacy of dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI) versus unenhanced magnetic resonance imaging (U-MRI + DBT) in detecting LVI in females with pathologically proven breast cancer.

Methods

Mansoura Medical School's Institutional Research Board (IRB) (MD.22.01.587) gave its approval for the current study; seventy subjects in all were enrolled who qualified for surgery.

Inclusion criteria Patients with pathologically proven breast cancer.

Exclusion criteria.

  1. (1)

    Benign and inflammatory breast masses

  2. (2)

    Individuals with a history of prior cancers or distant metastases

  3. (3)

    Poor quality images (n = 11).

  4. (4)

    The cases with contraindications to MRI or IV contrast.

  5. (5)

    The cases with contraindications to mammography, e.g., pregnant woman.

Digital breast tomosynthesis (DBT)

Digital breast tomosynthesis is an imaging method that enables the volumetric reconstruction of the breast from several low-dose two-dimensional projections captured at various angles of the X-ray tube [7].

DBT was carried out utilizing AMULET Innovality, the outcome of Fujifilm's continuous research, with standard cranio-caudal and mediolateral oblique views. It uses an amorphous selenium (a-Se) direct-conversion flat panel detector, which has good conversion efficiency in the mammography X-ray spectrum. The angle of acquisition for HR (high resolution) mode: ± 20°While the ST (Standard) mode acquisition angle is ± 7.5°, the pixel size is 100/150 m.

With DBT, an arc is formed by the X-ray tube, resulting in a series of images that are taken at a dose that is a small portion of what is obtained with a typical mammogram. Any detector element that is part of the acquisition gets information about each object volume element's in-time sequence. As a result, the set of digital projections includes raw data that represents all of the object layers' structural information. After that, they are sent to a computer, where algorithms are used to reconstruct them using the projection values correctly summed, enabling an outcome [8].

Tomosynthesis is a technique that reconstructs images of individual layers by using various algorithms to eliminate “structured noise” associated with upper and lower slices. Since generation noise and artifacts make reconstruction algorithms used in the first generation of devices (such as the FBP—filtered backprojection algorithm, which is ideal for 360° CT acquisition reconstruction) less effective for DBT reconstruction. Today's commonly used algorithm has been replaced by iterative algorithms like maximum likelihood expectation maximization (MLEM) and SART (simultaneous algebraic reconstruction technique), which can enhance imaging quality by lowering streaking artifacts and enhancing the visibility of microcalcifications and skin edges [8]).

All DBT systems have the following features in common: single-slice or slab cine loop display mode; slice thickness of 1 mm; acquisition and reconstruction times of 10–20 and 40–180 s; the ability to perform standard mammograms; and FFDM/DBT real-time selection with breast compression in place [9].

Instead, there is a great deal of variation in the quantity (13–25) and angle (15–50°) of takeover acquisitions, which are crucial components of image quality in DBT that depend on the dosage, quantity of projections, angle of acquisition, and quantity of exposures [10].

The technique of MRI

  • Utilizing a 1.5 Tesla scanner (Ingenia, Philips), the technique was conducted.

  • A breast coil was employed.

  • During the imaging, the following standard MR sequences were employed:

Two-dimensional sagittal T1-weighted spin-echo localizer (500/8/1 [TR/TE/excitations], 90° flip angle, 24 × 24-cm FOV, 256 × 256 imaging matrix, 20 sections, 5-mm section thickness with 1.5-mm skip). In the steady state, 2D axial T2-weighted multiplanar prepared gradient-recalled acquisition (800/25/1, 20° flip angle, 22 _ 22-cm FOV, 256 _ 256 imaging matrix, 23 sections, 5-mm section thickness with 2-mm skip) is performed. Two-dimensional axial T1-weighted spin-echo (500/8/1, 90° flip angle, 24 _ 24*\-cm field of view, 256 _ 256 imaging matrix, 20 sections, 5-mm section thickness with 1.5-mm skip).

Contrast administration

After receiving an intravenous injection of gadolinium chelate at a dose of 0.1–0.2 mmol per kilogram, a 20-mL saline flush is administered [11].

Dynamic contrast-enhanced acquisition (DCE-MRI)

DCE-MRI is performed by sequentially imaging before and after the administration of contrast material. When imagining a single breast, the sagittal plane provides the most natural results. Most often, axial or coronal orientations are utilized for bilateral dynamic breast MRI [12].

Qualitative and quantitative assessment of DCE-MRI

Time-signal intensity curve (TIC) gives kinetic information about breast lesions useful for the characterization of lesions. TIC can be evaluated manually, or automatically [13].

TIC includes two phases

  1. (1)

    First phase: Two minutes following injection of contrast material; categorized as fast, medium, or slow.

  2. (2)

    Delayed phase: Beyond 2 min following injection of contrast and classified as persistent, plateau, or washout [13].

Types of curves

  • Type I (progressive curve) is described in benign lesions.

  • Type II (plateau curve) has a possibility of 64% malignancy.

  • Type III (washout curve) is the most common in 87% of malignant masses. [14, 15].

Diffusion-weighted imaging sequence

Echo-planner imaging (EPI) techniques, such as single-shot EPI (SS-EPI), are commonly used in DWI. These techniques sample data in fractions of a second following an RF pulse of 90 to 180, thereby eliminating the motion effect. The small bandwidth/pixel of EPI results in field inhomogeneity, chemical shift artifacts, and high susceptibility artifacts. SS-EPI is typically used in conjunction with parallel imaging methods to get around these artifacts [16]. In breast MRI, the most commonly utilized b-values range from 500 to 1000 [17]. Tissue cellularity and the ADC value are inversely correlated; for instance, malignancies with higher cellularity typically have lower ADC values [17].

After DBT and MRI imaging, all cases were pathologically analyzed after surgical excision according to the presence or absence of LVI. The presence of tumor emboli within the endothelium lining of lymphatic vessels or blood capillaries without underlying smooth muscle and elastic fibers was diagnosed as LVI. The pathological criteria for LVI invasion diagnosis must be extratumoral, usually peritumoral within 1 mm [18]

Statistical analysis of the data

Data were analyzed using SPSS software (PASW Statistics for Windows, version 25) (SPSS, Inc., Chicago). Categorical data were presented as numbers and percentages. After testing of normality by the Kolmogorov–Smirnov test, the quantitative data were shown as mean ± Standard deviation for parametric data. The obtained results were deemed significant at the (≤0.05) level.

When appropriate, Chi-square and Monte Carlo tests tested the significance between the groups with categorical data. The one-way ANOVA test was employed to test the significance between three or more groups with parametric quantitative data followed by post hoc Tukey test to illustrate pairwise comparisons.

The best cutoff point was determined by calculating the validity (sensitivity and specificity) of continuous variables using the receiver-operating characteristics curve (ROC curve). Cross-tabulation was utilized for categorical variables, and it is used to evaluate predictive values and accuracy. When evaluating agreement between various observations for categorical variables with kappa values greater than 0.7, kappa agreement was employed.

Results

Seventy cases with pathologically proven breast cancer were enrolled in this research, 8 of them show positive family history.

Baseline characteristics

The study's average age was 49.53 ± 10.56 with 8 cases having positive family history. No statistically significant variation was found between unenhanced MRI versus dynamic MRI regarding peritumoral edema and dark rim diffusion (P value 1.0) (Table 1). Only 39 cases were showing broken halo signs (55.7%) shown at DBT. There were 42 cases (60%) showing pathologically proven positive LVI.

Table 1 Comparison of peritumoral, intratumoral edema, and DWI dark sign between radiological techniques
Full size table

ROC curve analysis

The specificity of tomosynthesis in LVI detection was 53.6% with a PPV of 66.7%, 48.4% NPV, and an accuracy of 58.6%. The specificity of unenhanced and enhanced MRI in LVI detection was 57.1% with a PPV of 68.4%, 50% NPV, and an accuracy of 60%. The specificity of the combination of DBT and unenhanced MRI in LVI detection was 42.9% with a PPV of 67.3%, 57.1% NPV, and an accuracy of 64.3% (Table 2), (Fig. 1).

Table 2 Validity of MRI enhanced, unenhanced, tomosynthesis findings, and combination in detection of lymphovascular invasion
Full size table
Fig. 1
figure 1

ROC curve analysis showing the sensitivity, specificity, PPV %, NPP%, and accuracy of lymphovascular invasion between different imaging modalities with an accuracy 60% in enhanced MRI and 64% in combined imaging (tomosynthesis and unenhanced MRI)

Full size image

Discussion

The unfavorable outcome of many malignant tumors is closely associated with intra-lymphovascular tumor emboli, or LVI [19,20,21,22,23], a higher chance of breast cancer returning after a modified radical mastectomy. In the St Gallen Consensus for breast cancer, lymph vascular tumor emboli, particularly lymphatic tumor emboli included [23]. Karlsson et al. [24] reported a higher chemotherapy failure rate with the presence of LVI in cases with cancer breast. Shen et al. [21] showed that lymphovascular tumor emboli had increased incidence of local tumor recurrence and distant metastasis [25].

The purpose of this manuscript was to use different digital mammography features to predict the risk of LVI of breast cancer. The study compared pre- and post-contrast conventional MRI features, digital breast tomosynthesis features, and combining (DBT, UN-MRI) features in breast cancer patients with and without LVI.

In this study, we demonstrated the significance of tomosynthesis findings, such as irregular lesions with blurring subcutaneous fat and the broken halo sign (Fig. 2 A–F), which indicates the presence of thin, variable-diameter lines spanning the peritumoral hypodensity areas, a potent marker of malignancy. Compressed fat tissue [26], a perceptual illusion (Mach band), and other theories have been floated over the years regarding the existence of a perilesional halo [27], or technical limitations of DBT [28, 29] despite the reason of the halo sign remains indistinct. Peritumoral tissue undergoes several changes [30, 31], indicating desmoplastic reactions against malignant tumors [32]; moreover, periductal fibrotic reactions [33] may cause the peritumoral tissue to contract. In addition to these fibrotic alterations, malignant tumors impact the microvascular environment through lymphovascular invasion and extratumoral extension through the vascular endothelial growth factor (VEGF) pathway [34]. Johannes Deeg et al. [33] discovered that the majority of BI-RADS 5 tumors (77.5%, n = 93) as well as 50.0% of BI-RADS 3 tumors (p < 0.0001) and 27.0% (n = 17) of benign BI-RADS 2 tumors had the “broken halo sign,” a significant indicator of malignancy. The study of Johannes Deeg et al. did not show if the broken halo sign correlates with LVI or not, they showed this finding in different pathological types of breast cancer including low and high grade also in invasive ductal, lobular, and in situ carcinoma. The results of Johannes Deeg et al. were the majority of lesions of no special type (NST): 80.8% (97) with Grade 2 the highest results ~ 59.8 (58), then invasive lobular carcinoma (ILC): 6.7% (8) majority in Grade 2: 87.5 (7), ductal carcinoma in situ (DCIS): high results showed in high grade: 80.0 (4), other: 8.3%. Zhuang sheng Liu et al. [35] found that mammography findings of blurring of subcutaneous fat prediction of LVI showed sensitivity, specificity, accuracy, PPV, and NPV were about 19.0(8/42), 83.8(67/80), 61.2(75/122), 38.1(8/21), and 66.3(67/101). This manuscript illustrated the tomosynthesis findings which can predict LVI with sensitivity, specificity, and accuracy of about 66.7%, 48.4%, and 58.6%, respectively (table no.2). We found no statistically significant differences in age and family history between the LVI positive group and the LVI negative group, similar to Zhuangsheng Liu et al. results.

Fig. 2
figure 2

44 Y patient with no family history of breast cancer, underwent both tomosynthesis and MRI. The tomosynthesis showed multiple irregular spiculated masses with foci of amorphous calcification are noted at the largest one (arrow head at (A) image), broken halo sign seen at MLO view (arrows at B image), also CC view demonstrated multicentric spiculated masses (arrows at image C). MRI showed significant peritumoral edema on T2WI (D), STIR (E) images (white arrows) around multicentric masses and rim diffusion sign (F, G) (white arrows) (high signal intensity seen at the periphery of the lesion) in breast lesions. The biopsy revealed grade III infiltrative ductal carcinoma with positive lymphovascular invasion and luminal B molecular type

Full size image

MRI imaging can be used as a predictive tool in LVI prediction depending on the presence of peritumoral edema and rim diffusion sign. The peritumoral edema is best seen on T2W (Fig. 3, H, I), and STIR images (Fig. 3, F and G) as high signal intensity lines are seen around the suspicious lesions. Hyejin Cheon et al. [36] demonstrated in their investigation that the existence of peritumoral edema (hazard ratio = 2.77, P = 0.022) and lymphovascular invasion (hazard ratio = 2.48, P = 0.044) were independent variables linked to the recurrence of the disease. Bo Bae Choi discovered that, with a P value of 0.329, peritumoral edema was equally uncommon in the LVI positive and negative groups. Pamela Sung et al. [37] conducted a retrospective analysis on 899 breast cancer patients who were classified into edema-positive (EPG) and edema-negative (ENG) cases. It was observed that EPG cases had significantly higher rates of LVI (57.9% vs. 12.6%, p < 0.001) and axillary lymph node metastasis (55.6% vs. 19.2%, p < 0.001). Although that Cheon et al. [38] found no association between peritumoral edema and LVI (p = 0.210), the presence of edema showed a significant correlation with increased N stage (p = 0.047). Pre-pectoral and subcutaneous edema did not significantly differ between the groups, but peritumoral edema was more common in the LVI group (p = 0.030), according to a different earlier study [39]. Almıla Coşkun Bilge et al. [40] demonstrated in their investigation that there was a p value < 0.001 correlation between the presence of LVI and the presence of peritumoral edema. In the current study, 27 patients (38.9%) had peritumoral edema; there was no statistically significant difference in the evaluation of the pre- and post-contrast MRI study (p value = 1) (Table 1).

Fig. 3
figure 3

52-year-old patient with no family history of breast cancer. On tomosynthesis (few nearby irregular high density speculated masses were seen in CC view at outer quadrants (white arrows at image A) and broken halo sign seen in MLO view (arrow heads at image (B) MRI showed multifocal lower outer quadrant irregular enhancing masses (arrow heads at images C, D images), with significant peritumoral edema noted at T2WI (C), and STIR (E) images (white arrows), DWI showed peripheral rim signs of high SI at DWI (F) image, and low SI at ADC at the periphery of lesions (G) image (white arrows). After the biopsy diagnosed as multifocal grade II infiltrative ductal carcinoma with high-grade DCIS and positive lymphovascular invasion, the molecular subtype was luminal A

Full size image

The rim diffusion sign on MRI images means high SI seen at the periphery of the lesion on DWI, and low SI on ADC map images (Fig. 4 G and H). Bong Joo Kang MD et al. [34] revealed the term “rim diffusion sign” and discovered that 19.4% of benign lesions and 59.7% of malignant lesions in DWI had the rim sign. For the rim sign in DWI, the corresponding values for sensitivity, specificity, and area under the curve (AUC) were 59.7%, 80.6%, and 0. 701. They did not use this DWI sign in differentiation between lymphovascular invasion detection or not. Bong Joo Kang MD et al. mentioned in their study a standardized 5-point scheme for rim DWI sign. Lesions completely thick rim surrounding line outlining ≥ 90% of the lesion were graded “5.” Lesions with a completely thin rim were graded “4.” Lesions with an incomplete (outlining < 90% of the mass) thick rim were graded “3.” Lesions with an incomplete thin rim were graded “2.” A thick rim was defined as > 3 mm and when most of the mass showed high signal intensity and left a central non-enhanced area, similar to a donut. A thin rim was defined as ≤ 3 mm, with only the outermost margin of the mass showing a high signal on DWI. Lesions with an unclear, indefinite, or unobserved rim on DWI were classified as no rim sign and graded “1.” Bo Bae Choi [39] analyzed the relationship between LVI and DWI findings revealed that the LVI + group had a significantly higher incidence of the DWI rim sign than the LVI − group with P value 0.017. Choi's [41] study showed that: Significant correlations were found between LVI and pathological tumor size, mass margin, internal enhancement pattern, kinetic enhancement curve, DWI rim sign, and the difference between maximum and minimum ADC (p < 0.05). The current study included the 5 DWI rim sign features with no differentiation, revealed that the validity of ADC in differentiating high from low grade (P value 0.014) with a 0.65 true ADC cutoff value. We found 20 patients (28.6%) showing rim DWI sign with no statistical significance between pre- and post-contrast MRI study evaluation (p value = 1).

Fig. 4
figure 4

44-year-old lady with a positive family history of breast cancer underwent tomosynthesis. Tomosynthesis (CC view image A, ML view image B) showed irregular speculated mass (white arrows at images A and B) seen at outer quadrant with broken halo sign noted (black arrows at image A) and outer quadrant focal asymmetry is also seen (Arrow heads at image A and B). MRI showed an irregular mass (arrows at image C, D) with multiple anterior-related non-mass enhancement (Arrow head image C), and significant peritumoral edema seen on STIR (D) image (Black arrow) with rim diffusion sign on DWI (white arrows at E, F images). The pathology was grade II infiltrative ductal carcinoma, luminal B, and no lymphovascular invasion

Full size image

Zhang et al. [14] study stated that the following additional risk factors for LVI were found to be significantly different (all p < 0.05) between the LVI positive and LVI negative groups: age, CEA, CA-153, amount of fibroglandular tissue (FGT), background parenchymal enhancement, tumor size, shape, skin thickening, nipple retraction, adjacent vessel sign, and axillary lymph node (ALN) size.26. In this study, we used combined peritumoral edema as well as bright diffusion sign MRI were of the same results in pre- and post-contrast regarding LVI prediction with sensitivity, specificity, PPV, NPV, and accuracy of about 61.9%, 57.1%,68.4%, 50%, and 60%, respectively (Table 2).

Study limitation

This study has some limitations. A small number of patients were included. The study depended only on the peritumoral edema and bright rim diffusion which are seen on MRI and the broken halo sign seen on DBT in the prediction of lymphovascular invasion discarding other findings as lymph node affection, size of lesions, and the pattern of the enhancing mass. Also, this study did not categorize LV positive and negative groups and correlated with max and minimum ADC value.

Conclusion

The tomosynthesis and MRI parameters including broken halo sign, peritumoral edema, and rim diffusion sign are promising tools in the prediction of lymph vascular invasion in breast cancer with good diagnostic accuracy.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Abbreviations

LVI:

Lymphovascular invasion

DWI:

Diffusion-weighted images

DBT:

Digital breast tomosynthesis

DCE-MRI:

Dynamic contrast-enhanced magnetic resonance imaging

UE-MRI:

Unenhanced magnetic resonance imaging

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Acknowledgements

I acknowledge my husband, my father, and my mother for the great support through my work in this manuscript.

Funding

This study had no funding from any resource.

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Authors and Affiliations

  1. Diagnostic and Interventional Radiology, Faculty of Medicine, Mansoura University, Mansoura, Egypt

    Fatma Hefida, S. Tantawy & Mona Zaky

  2. Surgical Oncology, Faculty of Medicine, Mansoura University, Mansoura, Egypt

    Omar Hamdy

Authors
  1. Fatma Hefida
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  2. S. Tantawy
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  3. Omar Hamdy
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  4. Mona Zaky
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Contributions

All authors read and approved the final manuscript.

Corresponding author

Correspondence to Fatma Hefida.

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Ethics approval and consent to participate

This study was approved by the Research Ethics Committee of the Faculty of Medicine at Mansoura University in Egypt on 13 /1 /2022; reference number of approval: MD.22.01.587.

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All patients included in this research gave written informed consent to publish the data contained within this study.

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The authors declare that they have no competing interests.

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Hefida, F., Tantawy, S., Hamdy, O. et al. Can combined tomosynthesis with unenhanced MRI be used as a predictive tool for lymphovascular invasion?. Egypt J Radiol Nucl Med 55, 195 (2024). https://doi.org/10.1186/s43055-024-01346-4

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  • DOI: https://doi.org/10.1186/s43055-024-01346-4

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