Efficacy of shear-wave elastography versus dynamic optical breast imaging for predicting the pathological response to neoadjuvant chemotherapy in breast cancer

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Highlights

  • Performance of SWE, DOBI and tumor size for predicting the NACT response in BC.

  • SWE, DOBI and tumor size after the second NACT cycle (t2) show the best predictive power.

  • SWE and DOBI are better than tumor size for predicting the NACT response.

  • SWE and DOBI have similar power for predicting a favorable response.

  • SWE performs better than DOBI in predicting NACT resistance.

Abstract

Purpose

Explore the value of shear-wave elastography (SWE) parameters and dynamic optical breast imaging features for predicting pathological responses to neoadjuvant chemotherapy (NACT) in breast cancer (BC).

Method

This prospective cohort study included 91 BC patients receiving NACT. Tumor size, SWE (maximum stiffness [Emax] and mean stiffness [Emean]), blood score (BS), and oxygen score (OS) and their relative changes were collected before (t0), during (t1–t5), and after NACT (t6). The pathological response was classified according to the residual cancer burden. Relationships between tumor size, SWE stiffness, BS, and OS at t0–t6 were analyzed, and their predictive power was compared.

Results

During six NACT cycles, tumor size, tumor stiffness, and BS decreased, and tumor OS increased. ΔEmean (t2), E2mean, BS2, and OS2 had a greater power than other indexes for predicting a favorable response (AUC = 0.79, 0.71, 0.77, 0.78) and a resistance response (0.86, 0.74, 0.71, 0.71). For the favorable response, predictive power did not differ significantly between ΔEmean (t2), E2mean, BS2, and OS2, whereas for the resistance response, ΔEmean (t2) showed better prediction than E2mean, BS2, and OS2.

Conclusions

SWE stiffness, BS, and OS exhibited good and similar performances in predicting a NACT favorable response, and SWE stiffness showed better performance than BS and OS in predicting NACT resistance. These results may provide an important reference for individualized treatment in BC patients receiving NACT.

Introduction

Neoadjuvant chemotherapy (NACT) is currently the standard treatment for patients with locally advanced or inflammatory breast cancer (BC). Pathological complete response (pCR) can be used as a surrogate prognostic marker for long-term disease-free survival after NACT in BC patients [1]. Several clinical studies have shown good results, with an objective response rate of approximately 70 % and a pCR rate of up to 30 % [1,2]. However, certain risk factors are associated with a higher likelihood of acquiring resistance to chemotherapy [3]. Therefore, the ability to predict the NACT response early in BC patients is critical.

Among the common clinicopathological markers, the ability of Ki-67, ER, PR, and HER2 to predict the NACT response in BC seems to be insufficient [4,5]. Studies to date have focused on the application of imaging modalities to predict and evaluate the NACT response [2,[6], [7], [8], [9], [10], [11], [12], [13], [14]]. Magnetic resonance imaging (MRI) is widely available and serves as an important tool for monitoring NACT and predicting its pathologic outcome [[7], [8], [9], [10]]. However, MRI has practical constraints for some patients [13,14]. Ultrasound (US) is a first-line non-invasive modality for breast disease; however, grey-scale US does not perform well in early prediction of the NACT response [15]. To date, there is still no overall satisfactory imaging modality for predicting the NACT response.

Shear-wave elastography (SWE) is a non-invasive ultrasound imaging method that can visualize and quantify tissue stiffness in vivo, and its usefulness for differentiating benign from malignant breast masses has been verified. SWE is an important complement to grey-scale US [16,17]. High stiffness on SWE is associated with chemotherapy resistance in BC, although this finding has been reported in relatively few studies [6,18,19].

Optical imaging, based on different absorption coefficients in the near-infrared region of blood hemoglobin (Hb), oxygenated hemoglobin (oxy-Hb), and deoxygenated hemoglobin (deoxy-Hb) can be used to detect breast vasculature and tumor microvasculature, owing to the inherent capability to differentiate hypoxic from normally oxygenated tissue [12,[20], [21], [22]]. Several dynamic optical imaging features acquired within 10 days to 2 weeks of NACT initiation were recently shown capable of early identification of BC patients with a pCR to NACT [[12], [13], [14]]. Dynamic optical breast imaging (DOBI) is a non-invasive optical imaging method. It can help distinguish breast regions with abnormal blood volume and oxygen saturation (which are suspected for malignancy) from normal tissue [21,23].

Optical imaging and ultrasonic elastography are potentially capable of early prediction of the NACT response [[12], [13], [14],18,19]. To the best of our knowledge, the power of the two non-invasive imaging modalities for predicting NACT responses has not been compared. Here, we examined 91 BC patients receiving NACT to compare the performance of SWE stiffness, optical imaging features, and tumor size for early prediction of the NACT response.

Section snippets

Patients

Ninety-seven eligible women were enrolled between April 2014 and September 2019. All patients were diagnosed with invasive BC by ultrasound-guided core needle biopsy and received NACT and subsequent surgical intervention. Six patients were excluded: three whose treatment plans changed and three with unqualified images (lesion maximum diameter ≥10 cm and/or deeper than 4 cm on US). The chemotherapy regimens are shown in Supplementary material 1. The study was conducted with the approval of the

Patient and lesion characteristics

The STARD flow diagram of patient inclusion is presented in Fig. 1. The baseline characteristics are shown in Table 1. Of the 91 patients, 19 (21 %) showed a favorable response (pCR and RCB-I), 43 (47 %) showed a moderate response (RCB-II), and 29 (32 %) showed NACT resistance (RCB-III). There were significant differences among the three RCB groups (P <  0.05) in most clinical indicators, except for age, HER2 positivity in ‘Immunohistochemical marker’ and Grade.

Tumor size and SWE evaluation

Interobserver reliability of

Discussion

A salient feature of grey-scale US in evaluating the NACT response is that the dynamic change in the echo, shape, and size of BC can be monitored. However, in our study, no differences in tumor size and relative change rate were observed among the groups, except for the parameters at t6. This indicates that the dynamic change of tumor size is not a sensitive indicator to differentiate between responders and non-responders, which is consistent with previous studies [15,27]. Grey-scale US can

Conclusions

SWE, OS, and BS exhibited excellent and similar performances for the early prediction of a favorable response, and SWE showed a better diagnostic performance than BS and OS for the early prediction of NACT resistance. ΔEmean (t2) showed a particularly impressing potential for the early prediction of NACT resistance. The results of this study may help guide the formulation of individualized treatment schemes for BC patients undergoing NACT.

CRediT authorship contribution statement

Jing Zhang: Conceptualization, Methodology, Software, Writing - original draft. Xueying Tan: Data curation, Formal analysis. Xintong Zhang: Visualization, Investigation. Ye Kang: Writing - review & editing. Jianyi Li: Resources. Weidong Ren: Resources. Yan Ma: Supervision, Validation, Project administration, Funding acquisition.

Declaration of Competing Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

This work was supported by National Natural Science Foundation of China (81801710, 81571686), Science and Technology Project Funds from Education Department of Liaoning Province (LK2016022, LK2016021).

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