Skip to main content
Top
Published in: Journal of Translational Medicine 1/2022

Open Access 01-12-2022 | Magnetic Resonance Imaging | Research

Radiomics features for assessing tumor-infiltrating lymphocytes correlate with molecular traits of triple-negative breast cancer

Authors: Guan-Hua Su, Yi Xiao, Lin Jiang, Ren-Cheng Zheng, He Wang, Yan Chen, Ya-Jia Gu, Chao You, Zhi-Ming Shao

Published in: Journal of Translational Medicine | Issue 1/2022

Login to get access

Abstract

Background

Tumor-infiltrating lymphocytes (TILs) have become a promising biomarker for assessing tumor immune microenvironment and predicting immunotherapy response. However, the assessment of TILs relies on invasive pathological slides.

Methods

We retrospectively extracted radiomics features from magnetic resonance imaging (MRI) to develop a radiomic cohort of triple-negative breast cancer (TNBC) (n = 139), among which 116 patients underwent transcriptomic sequencing. This radiomic cohort was randomly divided into the training cohort (n = 98) and validation cohort (n = 41) to develop radiomic signatures to predict the level of TILs through a non-invasive method. Pathologically evaluated TILs in the H&E sections were set as the gold standard. Elastic net and logistic regression were utilized to perform radiomics feature selection and model training, respectively. Transcriptomics was utilized to infer the detailed composition of the tumor microenvironment and to validate the radiomic signatures.

Results

We selected three radiomics features to develop a TILs-predicting radiomics model, which performed well in the validation cohort (AUC 0.790, 95% confidence interval (CI) 0.638–0.943). Further investigation with transcriptomics verified that tumors with high TILs predicted by radiomics (Rad-TILs) presented activated immune-related pathways, such as antigen processing and presentation, and immune checkpoints pathways. In addition, a hot immune microenvironment, including upregulated T cell infiltration gene signatures, cytokines, costimulators and major histocompatibility complexes (MHCs), as well as more CD8+ T cells, follicular helper T cells and memory B cells, was found in high Rad-TILs tumors.

Conclusions

Our study demonstrated the feasibility of radiomics model in predicting TILs status and provided a method to make the features interpretable, which will pave the way toward precision medicine for TNBC.
Appendix
Available only for authorised users
Literature
1.
go back to reference Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med. 2010;363:1938–48.PubMedCrossRef Foulkes WD, Smith IE, Reis-Filho JS. Triple-negative breast cancer. N Engl J Med. 2010;363:1938–48.PubMedCrossRef
2.
go back to reference Bianchini G, Balko JM, Mayer IA, Sanders ME, Gianni L. Triple-negative breast cancer: challenges and opportunities of a heterogeneous disease. Nat Rev Clin Oncol. 2016;13:674–90.PubMedPubMedCentralCrossRef Bianchini G, Balko JM, Mayer IA, Sanders ME, Gianni L. Triple-negative breast cancer: challenges and opportunities of a heterogeneous disease. Nat Rev Clin Oncol. 2016;13:674–90.PubMedPubMedCentralCrossRef
3.
go back to reference Savas P, Salgado R, Denkert C, Sotiriou C, Darcy PK, Smyth MJ, Loi S. Clinical relevance of host immunity in breast cancer: from TILs to the clinic. Nat Rev Clin Oncol. 2016;13:228–41.PubMedCrossRef Savas P, Salgado R, Denkert C, Sotiriou C, Darcy PK, Smyth MJ, Loi S. Clinical relevance of host immunity in breast cancer: from TILs to the clinic. Nat Rev Clin Oncol. 2016;13:228–41.PubMedCrossRef
4.
go back to reference Byrne A, Savas P, Sant S, Li R, Virassamy B, Luen SJ, Beavis PA, Mackay LK, Neeson PJ, Loi S. Tissue-resident memory T cells in breast cancer control and immunotherapy responses. Nat Rev Clin Oncol. 2020;17:341–8.PubMedCrossRef Byrne A, Savas P, Sant S, Li R, Virassamy B, Luen SJ, Beavis PA, Mackay LK, Neeson PJ, Loi S. Tissue-resident memory T cells in breast cancer control and immunotherapy responses. Nat Rev Clin Oncol. 2020;17:341–8.PubMedCrossRef
5.
go back to reference Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, Rouas G, Francis P, Crown JP, Hitre E, et al. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02–98. J Clin Oncol. 2013;31:860–7.PubMedCrossRef Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, Rouas G, Francis P, Crown JP, Hitre E, et al. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02–98. J Clin Oncol. 2013;31:860–7.PubMedCrossRef
6.
go back to reference Ali HR, Provenzano E, Dawson SJ, Blows FM, Liu B, Shah M, Earl HM, Poole CJ, Hiller L, Dunn JA, et al. Association between CD8+ T-cell infiltration and breast cancer survival in 12,439 patients. Ann Oncol. 2014;25:1536–43.PubMedCrossRef Ali HR, Provenzano E, Dawson SJ, Blows FM, Liu B, Shah M, Earl HM, Poole CJ, Hiller L, Dunn JA, et al. Association between CD8+ T-cell infiltration and breast cancer survival in 12,439 patients. Ann Oncol. 2014;25:1536–43.PubMedCrossRef
7.
go back to reference Adams S, Gray RJ, Demaria S, Goldstein L, Perez EA, Shulman LN, Martino S, Wang M, Jones VE, Saphner TJ, et al. Prognostic value of tumor-infiltrating lymphocytes in triple-negative breast cancers from two phase III randomized adjuvant breast cancer trials: ECOG 2197 and ECOG 1199. J Clin Oncol. 2014;32:2959–66.PubMedPubMedCentralCrossRef Adams S, Gray RJ, Demaria S, Goldstein L, Perez EA, Shulman LN, Martino S, Wang M, Jones VE, Saphner TJ, et al. Prognostic value of tumor-infiltrating lymphocytes in triple-negative breast cancers from two phase III randomized adjuvant breast cancer trials: ECOG 2197 and ECOG 1199. J Clin Oncol. 2014;32:2959–66.PubMedPubMedCentralCrossRef
8.
go back to reference Loi S, Michiels S, Salgado R, Sirtaine N, Jose V, Fumagalli D, Kellokumpu-Lehtinen PL, Bono P, Kataja V, Desmedt C, et al. Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Ann Oncol. 2014;25:1544–50.PubMedCrossRef Loi S, Michiels S, Salgado R, Sirtaine N, Jose V, Fumagalli D, Kellokumpu-Lehtinen PL, Bono P, Kataja V, Desmedt C, et al. Tumor infiltrating lymphocytes are prognostic in triple negative breast cancer and predictive for trastuzumab benefit in early breast cancer: results from the FinHER trial. Ann Oncol. 2014;25:1544–50.PubMedCrossRef
9.
go back to reference Pruneri G, Vingiani A, Bagnardi V, Rotmensz N, De Rose A, Palazzo A, Colleoni AM, Goldhirsch A, Viale G. Clinical validity of tumor-infiltrating lymphocytes analysis in patients with triple-negative breast cancer. Ann Oncol. 2016;27:249–56.PubMedCrossRef Pruneri G, Vingiani A, Bagnardi V, Rotmensz N, De Rose A, Palazzo A, Colleoni AM, Goldhirsch A, Viale G. Clinical validity of tumor-infiltrating lymphocytes analysis in patients with triple-negative breast cancer. Ann Oncol. 2016;27:249–56.PubMedCrossRef
10.
go back to reference Denkert C, Loibl S, Noske A, Roller M, Muller BM, Komor M, Budczies J, Darb-Esfahani S, Kronenwett R, Hanusch C, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol. 2010;28:105–13.PubMedCrossRef Denkert C, Loibl S, Noske A, Roller M, Muller BM, Komor M, Budczies J, Darb-Esfahani S, Kronenwett R, Hanusch C, et al. Tumor-associated lymphocytes as an independent predictor of response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol. 2010;28:105–13.PubMedCrossRef
11.
go back to reference Denkert C, von Minckwitz G, Brase JC, Sinn BV, Gade S, Kronenwett R, Pfitzner BM, Salat C, Loi S, Schmitt WD, et al. Tumor-infiltrating lymphocytes and response to neoadjuvant chemotherapy with or without carboplatin in human epidermal growth factor receptor 2-positive and triple-negative primary breast cancers. J Clin Oncol. 2015;33:983–91.PubMedCrossRef Denkert C, von Minckwitz G, Brase JC, Sinn BV, Gade S, Kronenwett R, Pfitzner BM, Salat C, Loi S, Schmitt WD, et al. Tumor-infiltrating lymphocytes and response to neoadjuvant chemotherapy with or without carboplatin in human epidermal growth factor receptor 2-positive and triple-negative primary breast cancers. J Clin Oncol. 2015;33:983–91.PubMedCrossRef
12.
go back to reference Issa-Nummer Y, Darb-Esfahani S, Loibl S, Kunz G, Nekljudova V, Schrader I, Sinn BV, Ulmer HU, Kronenwett R, Just M, et al. Prospective validation of immunological infiltrate for prediction of response to neoadjuvant chemotherapy in HER2-negative breast cancer—a substudy of the neoadjuvant GeparQuinto trial. PLoS ONE. 2013;8:e79775.PubMedPubMedCentralCrossRef Issa-Nummer Y, Darb-Esfahani S, Loibl S, Kunz G, Nekljudova V, Schrader I, Sinn BV, Ulmer HU, Kronenwett R, Just M, et al. Prospective validation of immunological infiltrate for prediction of response to neoadjuvant chemotherapy in HER2-negative breast cancer—a substudy of the neoadjuvant GeparQuinto trial. PLoS ONE. 2013;8:e79775.PubMedPubMedCentralCrossRef
13.
go back to reference Schmid P, Cortes J, Pusztai L, McArthur H, Kümmel S, Bergh J, Denkert C, Park YH, Hui R, Harbeck N, et al. Pembrolizumab for early triple-negative breast cancer. N Engl J Med. 2020;382:810–21.PubMedCrossRef Schmid P, Cortes J, Pusztai L, McArthur H, Kümmel S, Bergh J, Denkert C, Park YH, Hui R, Harbeck N, et al. Pembrolizumab for early triple-negative breast cancer. N Engl J Med. 2020;382:810–21.PubMedCrossRef
14.
go back to reference Schmid P, Rugo HS, Adams S, Schneeweiss A, Barrios CH, Iwata H, Diéras V, Henschel V, Molinero L, Chui SY, et al. Atezolizumab plus nab-paclitaxel as first-line treatment for unresectable, locally advanced or metastatic triple-negative breast cancer (IMpassion130): updated efficacy results from a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol. 2020;21:44–59.PubMedCrossRef Schmid P, Rugo HS, Adams S, Schneeweiss A, Barrios CH, Iwata H, Diéras V, Henschel V, Molinero L, Chui SY, et al. Atezolizumab plus nab-paclitaxel as first-line treatment for unresectable, locally advanced or metastatic triple-negative breast cancer (IMpassion130): updated efficacy results from a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet Oncol. 2020;21:44–59.PubMedCrossRef
15.
go back to reference Mittendorf EA, Zhang H, Barrios CH, Saji S, Jung KH, Hegg R, Koehler A, Sohn J, Iwata H, Telli ML, et al. Neoadjuvant atezolizumab in combination with sequential nab-paclitaxel and anthracycline-based chemotherapy versus placebo and chemotherapy in patients with early-stage triple-negative breast cancer (IMpassion031): a randomised, double-blind, phase 3 trial. Lancet. 2020;396:1090–100.PubMedCrossRef Mittendorf EA, Zhang H, Barrios CH, Saji S, Jung KH, Hegg R, Koehler A, Sohn J, Iwata H, Telli ML, et al. Neoadjuvant atezolizumab in combination with sequential nab-paclitaxel and anthracycline-based chemotherapy versus placebo and chemotherapy in patients with early-stage triple-negative breast cancer (IMpassion031): a randomised, double-blind, phase 3 trial. Lancet. 2020;396:1090–100.PubMedCrossRef
16.
go back to reference Goodman AM, Sokol ES, Frampton GM, Lippman SM, Kurzrock R. Microsatellite-stable tumors with high mutational burden benefit from immunotherapy. Cancer Immunol Res. 2019;7:1570–3.PubMedPubMedCentralCrossRef Goodman AM, Sokol ES, Frampton GM, Lippman SM, Kurzrock R. Microsatellite-stable tumors with high mutational burden benefit from immunotherapy. Cancer Immunol Res. 2019;7:1570–3.PubMedPubMedCentralCrossRef
17.
go back to reference Marabelle A, Le DT, Ascierto PA, Di Giacomo AM, De Jesus-Acosta A, Delord JP, Geva R, Gottfried M, Penel N, Hansen AR, et al. Efficacy of pembrolizumab in patients with noncolorectal high microsatellite instability/mismatch repair-deficient cancer: results from the phase II KEYNOTE-158 study. J Clin Oncol. 2020;38:1–10.PubMedCrossRef Marabelle A, Le DT, Ascierto PA, Di Giacomo AM, De Jesus-Acosta A, Delord JP, Geva R, Gottfried M, Penel N, Hansen AR, et al. Efficacy of pembrolizumab in patients with noncolorectal high microsatellite instability/mismatch repair-deficient cancer: results from the phase II KEYNOTE-158 study. J Clin Oncol. 2020;38:1–10.PubMedCrossRef
18.
go back to reference Lambin P, Rios-Velazquez E, Leijenaar R, Carvalho S, van Stiphout RG, Granton P, Zegers CM, Gillies R, Boellard R, Dekker A, Aerts HJ. Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer. 2012;48:441–6.PubMedPubMedCentralCrossRef Lambin P, Rios-Velazquez E, Leijenaar R, Carvalho S, van Stiphout RG, Granton P, Zegers CM, Gillies R, Boellard R, Dekker A, Aerts HJ. Radiomics: extracting more information from medical images using advanced feature analysis. Eur J Cancer. 2012;48:441–6.PubMedPubMedCentralCrossRef
19.
go back to reference Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures they are data. Radiology. 2016;278:563–77.PubMedCrossRef Gillies RJ, Kinahan PE, Hricak H. Radiomics: images are more than pictures they are data. Radiology. 2016;278:563–77.PubMedCrossRef
20.
go back to reference Grossmann P, Stringfield O, El-Hachem N, Bui MM, Rios Velazquez E, Parmar C, Leijenaar RT, Haibe-Kains B, Lambin P, Gillies RJ, Aerts HJ. Defining the biological basis of radiomic phenotypes in lung cancer. Elife. 2017;6:e23421.PubMedPubMedCentralCrossRef Grossmann P, Stringfield O, El-Hachem N, Bui MM, Rios Velazquez E, Parmar C, Leijenaar RT, Haibe-Kains B, Lambin P, Gillies RJ, Aerts HJ. Defining the biological basis of radiomic phenotypes in lung cancer. Elife. 2017;6:e23421.PubMedPubMedCentralCrossRef
21.
go back to reference Aerts HJ, Velazquez ER, Leijenaar RT, Parmar C, Grossmann P, Carvalho S, Bussink J, Monshouwer R, Haibe-Kains B, Rietveld D, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun. 2014;5:4006.PubMedCrossRef Aerts HJ, Velazquez ER, Leijenaar RT, Parmar C, Grossmann P, Carvalho S, Bussink J, Monshouwer R, Haibe-Kains B, Rietveld D, et al. Decoding tumour phenotype by noninvasive imaging using a quantitative radiomics approach. Nat Commun. 2014;5:4006.PubMedCrossRef
22.
go back to reference Huang YQ, Liang CH, He L, Tian J, Liang CS, Chen X, Ma ZL, Liu ZY. Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol. 2016;34:2157–64.PubMedCrossRef Huang YQ, Liang CH, He L, Tian J, Liang CS, Chen X, Ma ZL, Liu ZY. Development and validation of a radiomics nomogram for preoperative prediction of lymph node metastasis in colorectal cancer. J Clin Oncol. 2016;34:2157–64.PubMedCrossRef
23.
go back to reference Kong J, Zheng J, Wu J, Wu S, Cai J, Diao X, Xie W, Chen X, Yu H, Huang L, et al. Development of a radiomics model to diagnose pheochromocytoma preoperatively: a multicenter study with prospective validation. J Transl Med. 2022;20:31.PubMedPubMedCentralCrossRef Kong J, Zheng J, Wu J, Wu S, Cai J, Diao X, Xie W, Chen X, Yu H, Huang L, et al. Development of a radiomics model to diagnose pheochromocytoma preoperatively: a multicenter study with prospective validation. J Transl Med. 2022;20:31.PubMedPubMedCentralCrossRef
24.
go back to reference Sun K, Jiao Z, Zhu H, Chai W, Yan X, Fu C, Cheng JZ, Yan F, Shen D. Radiomics-based machine learning analysis and characterization of breast lesions with multiparametric diffusion-weighted MR. J Transl Med. 2021;19:443.PubMedPubMedCentralCrossRef Sun K, Jiao Z, Zhu H, Chai W, Yan X, Fu C, Cheng JZ, Yan F, Shen D. Radiomics-based machine learning analysis and characterization of breast lesions with multiparametric diffusion-weighted MR. J Transl Med. 2021;19:443.PubMedPubMedCentralCrossRef
25.
go back to reference Salgado R, Denkert C, Demaria S, Sirtaine N, Klauschen F, Pruneri G, Wienert S, Van den Eynden G, Baehner FL, Penault-Llorca F, et al. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol. 2015;26:259–71.PubMedCrossRef Salgado R, Denkert C, Demaria S, Sirtaine N, Klauschen F, Pruneri G, Wienert S, Van den Eynden G, Baehner FL, Penault-Llorca F, et al. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol. 2015;26:259–71.PubMedCrossRef
26.
go back to reference Hasebe T, Tsuda H, Hirohashi S, Shimosato Y, Tsubono Y, Yamamoto H, Mukai K. Fibrotic focus in infiltrating ductal carcinoma of the breast: a significant histopathological prognostic parameter for predicting the long-term survival of the patients. Breast Cancer Res Treat. 1998;49:195–208.PubMedCrossRef Hasebe T, Tsuda H, Hirohashi S, Shimosato Y, Tsubono Y, Yamamoto H, Mukai K. Fibrotic focus in infiltrating ductal carcinoma of the breast: a significant histopathological prognostic parameter for predicting the long-term survival of the patients. Breast Cancer Res Treat. 1998;49:195–208.PubMedCrossRef
27.
go back to reference Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–74.PubMedCrossRef Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33:159–74.PubMedCrossRef
28.
go back to reference Avants BB, Epstein CL, Grossman M, Gee JC. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal. 2008;12:26–41.PubMedCrossRef Avants BB, Epstein CL, Grossman M, Gee JC. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med Image Anal. 2008;12:26–41.PubMedCrossRef
29.
go back to reference Sled JG, Zijdenbos AP, Evans AC. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging. 1998;17:87–97.PubMedCrossRef Sled JG, Zijdenbos AP, Evans AC. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging. 1998;17:87–97.PubMedCrossRef
30.
go back to reference van Griethuysen JJM, Fedorov A, Parmar C, Hosny A, Aucoin N, Narayan V, Beets-Tan RGH, Fillion-Robin JC, Pieper S, Aerts H. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 2017;77:e104–7.PubMedPubMedCentralCrossRef van Griethuysen JJM, Fedorov A, Parmar C, Hosny A, Aucoin N, Narayan V, Beets-Tan RGH, Fillion-Robin JC, Pieper S, Aerts H. Computational radiomics system to decode the radiographic phenotype. Cancer Res. 2017;77:e104–7.PubMedPubMedCentralCrossRef
31.
go back to reference Zou H, Hastie T. Regularization and variable selection via the elastic net. J R Statist Soc: Ser B. 2005;67:301–20.CrossRef Zou H, Hastie T. Regularization and variable selection via the elastic net. J R Statist Soc: Ser B. 2005;67:301–20.CrossRef
32.
go back to reference Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43:e47.PubMedPubMedCentralCrossRef Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 2015;43:e47.PubMedPubMedCentralCrossRef
34.
go back to reference Xiao Y, Ma D, Zhao S, Suo C, Shi J, Xue MZ, Ruan M, Wang H, Zhao J, Li Q, et al. Multi-omics profiling reveals distinct microenvironment characterization and suggests immune escape mechanisms of triple-negative breast cancer. Clin Cancer Res. 2019;25:5002–14.PubMedCrossRef Xiao Y, Ma D, Zhao S, Suo C, Shi J, Xue MZ, Ruan M, Wang H, Zhao J, Li Q, et al. Multi-omics profiling reveals distinct microenvironment characterization and suggests immune escape mechanisms of triple-negative breast cancer. Clin Cancer Res. 2019;25:5002–14.PubMedCrossRef
36.
go back to reference Ott PA, Bang YJ, Piha-Paul SA, Razak ARA, Bennouna J, Soria JC, Rugo HS, Cohen RB, O’Neil BH, Mehnert JM, et al. T-cell-inflamed gene-expression profile, programmed death ligand 1 expression, and tumor mutational burden predict efficacy in patients treated with pembrolizumab across 20 cancers: KEYNOTE-028. J Clin Oncol. 2019;37:318–27.PubMedCrossRef Ott PA, Bang YJ, Piha-Paul SA, Razak ARA, Bennouna J, Soria JC, Rugo HS, Cohen RB, O’Neil BH, Mehnert JM, et al. T-cell-inflamed gene-expression profile, programmed death ligand 1 expression, and tumor mutational burden predict efficacy in patients treated with pembrolizumab across 20 cancers: KEYNOTE-028. J Clin Oncol. 2019;37:318–27.PubMedCrossRef
37.
go back to reference Rooney MS, Shukla SA, Wu CJ, Getz G, Hacohen N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell. 2015;160:48–61.PubMedPubMedCentralCrossRef Rooney MS, Shukla SA, Wu CJ, Getz G, Hacohen N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell. 2015;160:48–61.PubMedPubMedCentralCrossRef
38.
go back to reference Bian Y, Liu C, Li Q, Meng Y, Liu F, Zhang H, Fang X, Li J, Yu J, Feng X, et al. Preoperative radiomics approach to evaluating tumor-infiltrating CD8(+) T cells in patients with pancreatic ductal adenocarcinoma using noncontrast magnetic resonance imaging. J Magn Reson Imaging. 2022;55:803–14.PubMedCrossRef Bian Y, Liu C, Li Q, Meng Y, Liu F, Zhang H, Fang X, Li J, Yu J, Feng X, et al. Preoperative radiomics approach to evaluating tumor-infiltrating CD8(+) T cells in patients with pancreatic ductal adenocarcinoma using noncontrast magnetic resonance imaging. J Magn Reson Imaging. 2022;55:803–14.PubMedCrossRef
39.
go back to reference Bian Y, Liu YF, Jiang H, Meng Y, Liu F, Cao K, Zhang H, Fang X, Li J, Yu J, et al. Machine learning for MRI radiomics: a study predicting tumor-infiltrating lymphocytes in patients with pancreatic ductal adenocarcinoma. Abdom Radiol. 2021;46:4800–16.CrossRef Bian Y, Liu YF, Jiang H, Meng Y, Liu F, Cao K, Zhang H, Fang X, Li J, Yu J, et al. Machine learning for MRI radiomics: a study predicting tumor-infiltrating lymphocytes in patients with pancreatic ductal adenocarcinoma. Abdom Radiol. 2021;46:4800–16.CrossRef
40.
go back to reference Li J, Shi Z, Liu F, Fang X, Cao K, Meng Y, Zhang H, Yu J, Feng X, Li Q, et al. XGBoost classifier based on computed tomography radiomics for prediction of tumor-infiltrating CD8(+) T-cells in patients with pancreatic ductal adenocarcinoma. Front Oncol. 2021;11:671333.PubMedPubMedCentralCrossRef Li J, Shi Z, Liu F, Fang X, Cao K, Meng Y, Zhang H, Yu J, Feng X, Li Q, et al. XGBoost classifier based on computed tomography radiomics for prediction of tumor-infiltrating CD8(+) T-cells in patients with pancreatic ductal adenocarcinoma. Front Oncol. 2021;11:671333.PubMedPubMedCentralCrossRef
41.
go back to reference Liao H, Zhang Z, Chen J, Liao M, Xu L, Wu Z, Yuan K, Song B, Zeng Y. Preoperative radiomic approach to evaluate tumor-infiltrating CD8(+) T cells in hepatocellular carcinoma patients using contrast-enhanced computed tomography. Ann Surg Oncol. 2019;26:4537–47.PubMedCrossRef Liao H, Zhang Z, Chen J, Liao M, Xu L, Wu Z, Yuan K, Song B, Zeng Y. Preoperative radiomic approach to evaluate tumor-infiltrating CD8(+) T cells in hepatocellular carcinoma patients using contrast-enhanced computed tomography. Ann Surg Oncol. 2019;26:4537–47.PubMedCrossRef
42.
go back to reference Sun R, Limkin EJ, Vakalopoulou M, Dercle L, Champiat S, Han SR, Verlingue L, Brandao D, Lancia A, Ammari S, et al. A radiomics approach to assess tumour-infiltrating CD8 cells and response to anti-PD-1 or anti-PD-L1 immunotherapy: an imaging biomarker, retrospective multicohort study. Lancet Oncol. 2018;19:1180–91.PubMedCrossRef Sun R, Limkin EJ, Vakalopoulou M, Dercle L, Champiat S, Han SR, Verlingue L, Brandao D, Lancia A, Ammari S, et al. A radiomics approach to assess tumour-infiltrating CD8 cells and response to anti-PD-1 or anti-PD-L1 immunotherapy: an imaging biomarker, retrospective multicohort study. Lancet Oncol. 2018;19:1180–91.PubMedCrossRef
43.
go back to reference Tang WJ, Kong QC, Cheng ZX, Liang YS, Jin Z, Chen LX, Hu WK, Liang YY, Wei XH, Guo Y, Jiang XQ. Performance of radiomics models for tumour-infiltrating lymphocyte (TIL) prediction in breast cancer: the role of the dynamic contrast-enhanced (DCE) MRI phase. Eur Radiol. 2022;32:864–75.PubMedCrossRef Tang WJ, Kong QC, Cheng ZX, Liang YS, Jin Z, Chen LX, Hu WK, Liang YY, Wei XH, Guo Y, Jiang XQ. Performance of radiomics models for tumour-infiltrating lymphocyte (TIL) prediction in breast cancer: the role of the dynamic contrast-enhanced (DCE) MRI phase. Eur Radiol. 2022;32:864–75.PubMedCrossRef
44.
go back to reference Xu N, Zhou J, He X, Ye S, Miao H, Liu H, Chen Z, Zhao Y, Pan Z, Wang M. Radiomics model for evaluating the level of tumor-infiltrating lymphocytes in breast cancer based on dynamic contrast-enhanced MRI. Clin Breast Cancer. 2021;21:440-449.e441.PubMedCrossRef Xu N, Zhou J, He X, Ye S, Miao H, Liu H, Chen Z, Zhao Y, Pan Z, Wang M. Radiomics model for evaluating the level of tumor-infiltrating lymphocytes in breast cancer based on dynamic contrast-enhanced MRI. Clin Breast Cancer. 2021;21:440-449.e441.PubMedCrossRef
45.
go back to reference Yu H, Meng X, Chen H, Han X, Fan J, Gao W, Du L, Chen Y, Wang Y, Liu X, et al. Correlation between mammographic radiomics features and the level of tumor-infiltrating lymphocytes in patients with triple-negative breast cancer. Front Oncol. 2020;10:412.PubMedPubMedCentralCrossRef Yu H, Meng X, Chen H, Han X, Fan J, Gao W, Du L, Chen Y, Wang Y, Liu X, et al. Correlation between mammographic radiomics features and the level of tumor-infiltrating lymphocytes in patients with triple-negative breast cancer. Front Oncol. 2020;10:412.PubMedPubMedCentralCrossRef
46.
go back to reference Yu H, Meng X, Chen H, Liu J, Gao W, Du L, Chen Y, Wang Y, Liu X, Liu B, et al. Predicting the level of tumor-infiltrating lymphocytes in patients with breast cancer: usefulness of mammographic radiomics features. Front Oncol. 2021;11:628577.PubMedPubMedCentralCrossRef Yu H, Meng X, Chen H, Liu J, Gao W, Du L, Chen Y, Wang Y, Liu X, Liu B, et al. Predicting the level of tumor-infiltrating lymphocytes in patients with breast cancer: usefulness of mammographic radiomics features. Front Oncol. 2021;11:628577.PubMedPubMedCentralCrossRef
47.
go back to reference Ayers M, Lunceford J, Nebozhyn M, Murphy E, Loboda A, Kaufman DR, Albright A, Cheng JD, Kang SP, Shankaran V, et al. IFN-gamma-related mRNA profile predicts clinical response to PD-1 blockade. J Clin Invest. 2017;127:2930–40.PubMedPubMedCentralCrossRef Ayers M, Lunceford J, Nebozhyn M, Murphy E, Loboda A, Kaufman DR, Albright A, Cheng JD, Kang SP, Shankaran V, et al. IFN-gamma-related mRNA profile predicts clinical response to PD-1 blockade. J Clin Invest. 2017;127:2930–40.PubMedPubMedCentralCrossRef
48.
go back to reference Whitford P, George WD, Campbell AM. Flow cytometric analysis of tumour infiltrating lymphocyte activation and tumour cell MHC class I and II expression in breast cancer patients. Cancer Lett. 1992;61:157–64.PubMedCrossRef Whitford P, George WD, Campbell AM. Flow cytometric analysis of tumour infiltrating lymphocyte activation and tumour cell MHC class I and II expression in breast cancer patients. Cancer Lett. 1992;61:157–64.PubMedCrossRef
49.
go back to reference Chin Y, Janseens J, Vandepitte J, Vandenbrande J, Opdebeek L, Raus J. Phenotypic analysis of tumor-infiltrating lymphocytes from human breast cancer. Anticancer Res. 1992;12:1463–6.PubMed Chin Y, Janseens J, Vandepitte J, Vandenbrande J, Opdebeek L, Raus J. Phenotypic analysis of tumor-infiltrating lymphocytes from human breast cancer. Anticancer Res. 1992;12:1463–6.PubMed
51.
go back to reference Borst J, Ahrends T, Babala N, Melief CJM, Kastenmuller W. CD4(+) T cell help in cancer immunology and immunotherapy. Nat Rev Immunol. 2018;18:635–47.PubMedCrossRef Borst J, Ahrends T, Babala N, Melief CJM, Kastenmuller W. CD4(+) T cell help in cancer immunology and immunotherapy. Nat Rev Immunol. 2018;18:635–47.PubMedCrossRef
52.
go back to reference Sharonov GV, Serebrovskaya EO, Yuzhakova DV, Britanova OV, Chudakov DM. B cells, plasma cells and antibody repertoires in the tumour microenvironment. Nat Rev Immunol. 2020;20:294–307.PubMedCrossRef Sharonov GV, Serebrovskaya EO, Yuzhakova DV, Britanova OV, Chudakov DM. B cells, plasma cells and antibody repertoires in the tumour microenvironment. Nat Rev Immunol. 2020;20:294–307.PubMedCrossRef
53.
go back to reference Kroeger DR, Milne K, Nelson BH. Tumor-infiltrating plasma cells are associated with tertiary lymphoid structures, cytolytic T-cell responses, and superior prognosis in ovarian cancer. Clin Cancer Res. 2016;22:3005–15.PubMedCrossRef Kroeger DR, Milne K, Nelson BH. Tumor-infiltrating plasma cells are associated with tertiary lymphoid structures, cytolytic T-cell responses, and superior prognosis in ovarian cancer. Clin Cancer Res. 2016;22:3005–15.PubMedCrossRef
54.
go back to reference Park S, Ock CY, Kim H, Pereira S, Park S, Ma M, Choi S, Kim S, Shin S, Aum BJ, et al. Artificial intelligence-powered spatial analysis of tumor-infiltrating lymphocytes as complementary biomarker for immune checkpoint inhibition in non-small-cell lung cancer. J Clin Oncol. 2022;40:1916–28.PubMedPubMedCentralCrossRef Park S, Ock CY, Kim H, Pereira S, Park S, Ma M, Choi S, Kim S, Shin S, Aum BJ, et al. Artificial intelligence-powered spatial analysis of tumor-infiltrating lymphocytes as complementary biomarker for immune checkpoint inhibition in non-small-cell lung cancer. J Clin Oncol. 2022;40:1916–28.PubMedPubMedCentralCrossRef
Metadata
Title
Radiomics features for assessing tumor-infiltrating lymphocytes correlate with molecular traits of triple-negative breast cancer
Authors
Guan-Hua Su
Yi Xiao
Lin Jiang
Ren-Cheng Zheng
He Wang
Yan Chen
Ya-Jia Gu
Chao You
Zhi-Ming Shao
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2022
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-022-03688-x

Other articles of this Issue 1/2022

Journal of Translational Medicine 1/2022 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.