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      Whole-Lesion Histogram Analysis of the Apparent Diffusion Coefficient as a Quantitative Imaging Biomarker for Assessing the Level of Tumor-Infiltrating Lymphocytes: Value in Molecular Subtypes of Breast Cancer

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          Abstract

          Purpose

          To assess whether apparent diffusion coefficient (ADC) metrics can be used to assess tumor-infiltrating lymphocyte (TIL) levels in breast cancer, particularly in the molecular subtypes of breast cancer.

          Methods

          In total, 114 patients with breast cancer met the inclusion criteria (mean age: 52 years; range: 29–85 years) and underwent multi-parametric breast magnetic resonance imaging (MRI). The patients were imaged by diffusion-weighted (DW)-MRI (1.5 T) using a single-shot spin-echo echo-planar imaging sequence. Two readers independently drew a region of interest (ROI) on the ADC maps of the whole tumor. The mean ADC and histogram parameters (10 th, 25 th, 50 th, 75 th, and 90 th percentiles of ADC, skewness, entropy, and kurtosis) were used as features to analyze associations with the TIL levels in breast cancer. Additionally, the correlation between the ADC values and Ki-67 expression were analyzed. Continuous variables were compared with Student’s t-test or Mann-Whitney U test if the variables were not normally distributed. Categorical variables were compared using Pearson’s chi-square test or Fisher’s exact test. Associations between TIL levels and imaging features were evaluated by the Mann-Whitney U and Kruskal-Wallis tests.

          Results

          A statistically significant difference existed in the 10 th and 25 th percentile ADC values between the low and high TIL groups in breast cancer ( P=0.012 and 0.027). For the luminal subtype of breast cancer, the 10 th percentile ADC value was significantly lower in the low TIL group ( P=0.041); for the non-luminal subtype of breast cancer, the kurtosis was significantly lower in the low TIL group ( P=0.023). The Ki-67 index showed statistical significance for evaluating the TIL levels in breast cancer ( P=0.007). Additionally, the skewness was significantly higher for samples with high Ki-67 levels in breast cancer ( P=0.029).

          Conclusions

          Our findings suggest that whole-lesion ADC histogram parameters can be used as surrogate biomarkers to evaluate TIL levels in molecular subtypes of breast cancer.

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          Most cited references39

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          The Measurement of Observer Agreement for Categorical Data

          J Landis, Gary G. Koch (1977)
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            The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014.

            R. Salgado, C Denkert, S Demaria … (2015)
            The morphological evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer (BC) is gaining momentum as evidence strengthens for the clinical relevance of this immunological biomarker. Accumulating evidence suggests that the extent of lymphocytic infiltration in tumor tissue can be assessed as a major parameter by evaluation of hematoxylin and eosin (H&E)-stained tumor sections. TILs have been shown to provide prognostic and potentially predictive value, particularly in triple-negative and human epidermal growth factor receptor 2-overexpressing BC. A standardized methodology for evaluating TILs is now needed as a prerequisite for integrating this parameter in standard histopathological practice, in a research setting as well as in clinical trials. This article reviews current data on the clinical validity and utility of TILs in BC in an effort to foster better knowledge and insight in this rapidly evolving field, and to develop a standardized methodology for visual assessment on H&E sections, acknowledging the future potential of molecular/multiplexed approaches. The methodology provided is sufficiently detailed to offer a uniformly applied, pragmatic starting point and improve consistency and reproducibility in the measurement of TILs for future studies. © The Author 2014. Published by Oxford University Press on behalf of the European Society for Medical Oncology. All rights reserved. For permissions, please email: journals.permissions@oup.com.
            Article 0 comments Cited 742 times – based on 0 reviews     Review now
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              Tumour-infiltrating lymphocytes and prognosis in different subtypes of breast cancer: a pooled analysis of 3771 patients treated with neoadjuvant therapy

              Carsten Denkert, Gunter von Minckwitz, Silvia Darb-Esfahani … (2018)
              Tumour-infiltrating lymphocytes (TILs) are predictive for response to neoadjuvant chemotherapy in triple-negative breast cancer (TNBC) and HER2-positive breast cancer, but their role in luminal breast cancer and the effect of TILs on prognosis in all subtypes is less clear. Here, we assessed the relevance of TILs for chemotherapy response and prognosis in patients with TNBC, HER2-positive breast cancer, and luminal-HER2-negative breast cancer.
              Article 0 comments Cited 697 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                Journal
                Journal ID (nlm-ta): Front Oncol
                Journal ID (iso-abbrev): Front Oncol
                Journal ID (publisher-id): Front. Oncol.
                Title: Frontiers in Oncology
                Publisher: Frontiers Media S.A.
                ISSN (Electronic): 2234-943X
                Publication date (Electronic): 08 January 2021
                Publication date Collection: 2020
                Volume: 10
                Electronic Location Identifier: 611571
                Affiliations
                [1] 1 Department of Radiology, Guangzhou First People’s Hospital, School of Medicine, South China University of Technology , Guangzhou, China
                [2] 2 Department of Ultrasound, The Third Affiliated Hospital, Sun Yat-Sen University , Guangzhou, China
                [3] 3 Department of Pathology, Guangzhou First People’s Hospital, School of Medicine, South China University of Technology , Guangzhou, China
                [4] 4 Department of Radiology, The Third Affiliated Hospital, Sun Yat-Sen University , Guangzhou, China
                Author notes

                Edited by: Pilar López-Larrubia, Consejo Superior de Investigaciones Científicas (CSIC), Spain

                Reviewed by: Alexey Surov, Leipzig University, Germany; Hans-Jonas Meyer, Leipzig University, Germany

                This article was submitted to Cancer Imaging and Image-directed Interventions, a section of the journal Frontiers in Oncology

                Article
                DOI: 10.3389/fonc.2020.611571
                PMC ID: 7820903
                PubMed ID: 33489920
                SO-VID: 2a3234dd-20c5-4b1f-a3a1-d15a636e1289
                Copyright © Copyright © 2021 Tang, Jin, Zhang, Liang, Cheng, Chen, Liang, Wei, Kong, Guo and Jiang
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                Date received : 14 October 2020
                Date accepted : 19 November 2020
                Page count
                Figures: 6, Tables: 5, Equations: 0, References: 39, Pages: 11, Words: 5090
                Funding
                Funded by: National Natural Science Foundation of China 10.13039/501100001809
                Categories
                Subject: Oncology
                Subject: Original Research

                ScienceOpen disciplines: Oncology & Radiotherapy
                Keywords: tumor-infiltrating lymphocytes,breast cancer,apparent diffusion coefficient,magnetic resonance imaging,molecular subtypes
                Data availability:
                ScienceOpen disciplines: Oncology & Radiotherapy
                Keywords: tumor-infiltrating lymphocytes, breast cancer, apparent diffusion coefficient, magnetic resonance imaging, molecular subtypes

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