Predicting the response to neoadjuvant therapy for early-stage breast cancer: tumor-, blood-, and imaging-related biomarkers

Wenyong Tan, Ming Yang, Hongli Yang, Fangbin Zhou, Weixi Shen, Wenyong Tan, Ming Yang, Hongli Yang, Fangbin Zhou, Weixi Shen

Abstract

Neoadjuvant therapy (NAT) has been used increasingly in patients with locally advanced or early-stage breast cancer. However, the accurate evaluation and prediction of response to NAT remain the great challenge. Biomarkers could prove useful to identify responders or nonresponders, or even to distinguish between early and delayed responses. These biomarkers could include markers from the tumor itself, such as versatile proteins, genes, and ribonucleic acids, various biological factors or peripheral blood cells, and clinical and pathological features. Possible predictive markers could also include multiple features from functional imaging, such as standard uptake values in positron emission tomography, apparent diffusion coefficient in magnetic resonance, or radiomics imaging biomarkers. In addition, cells that indirectly present the immune status of tumor cells and/or their host could also potentially be used as biomarkers, eg, tumor-infiltrating lymphocytes, tumor-associated macrophages, and myeloid-derived suppressor cells. Though numerous biomarkers have been widely investigated, only estrogen and/or progesterone receptors and human epidermal growth factor receptor have been proven to be reliable biomarkers to predict the response to NAT. They are the only biomarkers recommended in several international guidelines. The other aforementioned biomarkers warrant further validation studies. Some multigene profiling assays that are commercially available, eg, Oncotype DX and MammaPrint, should be used with caution when extrapolated to NAT settings. A panel of combined multilevel biomarkers might be able to predict the response to NAT more robustly than individual biomarkers. To establish such a panel and its prediction model, reliable methods and extensive clinical validation are warranted.

Keywords: biomarker; breast cancer; drug therapy; predictive factor.

Conflict of interest statement

Disclosure The authors report no conflicts of interest in this work.

Figures

Figure 1
Figure 1
The schematic representation of a clinical trial merging biomarkers from tumor, blood, and imaging. Note: This clinical trial (NCT03242551), ie, BINC-B, aims to use a combination of multiple biomarkers to improve their ability to predict the response to neoadjuvant chemotherapy of patients with early-stage breast cancer. Abbreviations: BINC-B, Biomarkers Investigating Neoadjuvant Chemotherapy for Breast cancer; CEC, circulating endothelial cell; ctDNA, circulating tumor DNA; DCE, dynamic contrast enhanced; DWI, diffusion-weighted imaging; MRI, magnetic resonance imaging; NAT, neoadjuvant therapy.

References

    1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2017. CA: A Cancer Journal for Clinicians. 2017;67(1):7–30.
    1. Chen W, Zheng R, Baade PD, et al. Cancer statistics in China, 2015. CA: A Cancer Journal for Clinicians. 2016;66(2):115–132.
    1. Peart O. Breast intervention and breast cancer treatment options. Radiol Technol. 2015;86(5quiz 559-562):535M–5558.
    1. Cianfrocca M, Goldstein LJ. Prognostic and Predictive Factors in Early-Stage Breast Cancer. Oncologist. 2004;9(6):606–616.
    1. Sawyers CL. The cancer biomarker problem. Nature. 2008;452(7187):548–552.
    1. Kaufmann M, von Minckwitz G, Mamounas EP, et al. Recommendations from an international consensus conference on the current status and future of neoadjuvant systemic therapy in primary breast cancer. Annals of Surgical Oncology. 2012;19(5):1508–1516.
    1. Early Breast Cancer Trialists’ Collaborative Group (EBCTCG) Long-term outcomes for neoadjuvant versus adjuvant chemotherapy in early breast cancer: meta-analysis of individual patient data from ten randomised trials. Lancet Oncol. 2018;19(1):27–39.
    1. Rubovszky G, Horváth Z. Recent Advances in the Neoadjuvant Treatment of Breast Cancer. J Breast Cancer. 2017;20(2):119–131.
    1. Kaufmann M, Pusztai L. Use of standard markers and incorporation of molecular markers into breast cancer therapy: Consensus recommendations from an International Expert Panel. Cancer. 2011;117(8):1575–1582.
    1. Harris LN, Ismaila N, Mcshane LM, et al. Use of Biomarkers to Guide Decisions on Adjuvant Systemic Therapy for Women With Early-Stage Invasive Breast Cancer: American Society of Clinical Oncology Clinical Practice Guideline. J Clin Oncol. 2016;34(10):1134–1150.
    1. Brandt A, Lorenzo Bermejo J, Sundquist J, Hemminki K. Breast cancer risk in women who fulfill high-risk criteria: at what age should surveillance start? Breast Cancer Res Treat. 2010;121(1):133–141.
    1. Coates AS, Winer EP, Goldhirsch A, et al. Tailoring therapies--improving the management of early breast cancer: St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2015. Ann Oncol. 2015;26(8):1533–1546.
    1. Curigliano G, Burstein HJ, P Winer E. De-escalating and escalating treatments for early-stage breast cancer: the St. Gallen International Expert Consensus Conference on the Primary Therapy of Early Breast Cancer 2017. Ann Oncol. 2017;28(8):1700–1712.
    1. Loibl S, Jackisch C, Lederer B, et al. Outcome after neoadjuvant chemotherapy in young breast cancer patients: a pooled analysis of individual patient data from eight prospectively randomized controlled trials. Breast Cancer Res Treat. 2015;152(2):377–387.
    1. Elsamany S, Alzahrani A, Abozeed WN, et al. Mammographic breast density: Predictive value for pathological response to neoadjuvant chemotherapy in breast cancer patients. Breast. 2015;24(5):576–581.
    1. Rugo HS, Brufsky AM, Ulcickas Yood M, et al. Racial disparities in treatment patterns and clinical outcomes in patients with HER2-positive metastatic breast cancer. Breast Cancer Res Treat. 2013;141(3):461–470.
    1. Gao JJ, Swain SM. Luminal A Breast Cancer and Molecular Assays: A Review. Oncologist. 2018;23(5):556–565.
    1. Llombart-Cussac A, Cortés J, Paré L, et al. HER2-enriched subtype as a predictor of pathological complete response following trastuzumab and lapatinib without chemotherapy in early-stage HER2-positive breast cancer (PAMELA): an open-label, single-group, multicentre, phase 2 trial. Lancet Oncol. 2017;18(4):545–554.
    1. Loibl S, O’Shaughnessy J, Untch M, et al. Addition of the PARP inhibitor veliparib plus carboplatin or carboplatin alone to standard neoadjuvant chemotherapy in triple-negative breast cancer (BrighTNess): a randomised, phase 3 trial. Lancet Oncol. 2018;19(4):497–509.
    1. Balmativola D, Marchiò C, Maule M, et al. Pathological non-response to chemotherapy in a neoadjuvant setting of breast cancer: an inter-institutional study. Breast Cancer Res Treat. 2014;148(3):511–523.
    1. Maiorano E, Regan MM, Viale G, et al. Prognostic and predictive impact of central necrosis and fibrosis in early breast cancer: Results from two International Breast Cancer Study Group randomized trials of chemoendocrine adjuvant therapy. Breast Cancer Res Treat. 2010;121(1):211–218.
    1. Buhmeida A, Al-Maghrabi J, Merdad A, et al. Prognostic value of mitotic counts in breast cancer of Saudi Arabian patients. Anticancer Res. 2011;31(1):97–103.
    1. Petric M, Martinez S, Acevedo F, et al. Correlation between Ki67 and Histological Grade in Breast Cancer Patients Treated with Preoperative Chemotherapy. Asian Pacific Journal of Cancer Prevention. 2015;15(23):10277–10280.
    1. Macchia G, Gambacorta MA, Masciocchi C, et al. Time to surgery and pathologic complete response after neoadjuvant chemoradiation in rectal cancer: A population study on 2094 patients. Clin Transl Radiat Oncol. 2017;4:8–14.
    1. Cortazar P, Zhang L, Untch M, et al. Pathological complete response and long-term clinical benefit in breast cancer: the CTNeoBC pooled analysis. Lancet. 2014;384(9938):164–172.
    1. Cortazar P, Geyer CE. Pathological Complete Response in Neoadjuvant Treatment of Breast Cancer. Ann Surg Oncol. 2015;22(5):1441–1446.
    1. Houssami N, Macaskill P, von Minckwitz G, Marinovich ML, Mamounas E. Meta-analysis of the association of breast cancer subtype and pathologic complete response to neoadjuvant chemotherapy. Eur J Cancer. 2012;48(18):3342–3354.
    1. von Minckwitz G, Untch M, Blohmer JU, et al. Definition and impact of pathologic complete response on prognosis after neoadjuvant chemotherapy in various intrinsic breast cancer subtypes. J Clin Oncol. 2012;30(15):1796–1804.
    1. Mazouni C, Peintinger F, Wan-Kau S, et al. Residual Ductal Carcinoma In Situ in Patients With Complete Eradication of Invasive Breast Cancer After Neoadjuvant Chemotherapy Does Not Adversely Affect Patient Outcome. Journal of Clinical Oncology. 2007;25(19):2650–2655.
    1. Fung F, Cornacchi SD, Vanniyasingam T, et al. Predictors of 5-year local, regional, and distant recurrent events in a population-based cohort of breast cancer patients. Am J Surg. 2017;213(2):418–425.
    1. Rakha EA, El-Sayed ME, Menon S, Green AR, Lee AHS, Ellis IO. Histologic grading is an independent prognostic factor in invasive lobular carcinoma of the breast. Breast Cancer Res Treat. 2008;111(1):121–127.
    1. Alvarado-Cabrero I, Alderete-Vázquez G, Quintal-Ramírez M, Patiño M, Ruíz E. Incidence of pathologic complete response in women treated with preoperative chemotherapy for locally advanced breast cancer: correlation of histology, hormone receptor status, Her2/Neu, and gross pathologic findings. Ann Diagn Pathol. 2009;13(3):151–157.
    1. Giuliano AE, Connolly JL, Edge SB, et al. Breast Cancer-Major changes in the American Joint Committee on Cancer eighth edition cancer staging manual. CA: A Cancer Journal for Clinicians. 2017;67(4):290–303.
    1. Ravelli A, Reuben JM, Lanza F, et al. Breast cancer circulating biomarkers: advantages, drawbacks, and new insights. Tumor Biology. 2015;36(9):6653–6665.
    1. Bielčiková Z, Jakabová A, Pinkas M, Zemanová M, Kološtová K, Bobek V. Circulating tumor cells: what we know, what do we want to know about them and are they ready to be used in clinics? Am J Transl Res. 2017;9(6):2807–2823.
    1. Zhou F, Zhou Y, Dong J, Tan W. Circulating endothelial cells and their subsets: novel biomarkers for cancer. Biomark Med. 2017;11(8):665–676.
    1. Cristofanilli M, Budd GT, Ellis MJ, et al. Circulating Tumor Cells, Disease Progression, and Survival in Metastatic Breast Cancer. N Engl J Med Overseas Ed. 2004;351(8):781–791.
    1. Bidard FC, Vincent-Salomon A, Sigal-Zafrani B, et al. Prognosis of women with stage IV breast cancer depends on detection of circulating tumor cells rather than disseminated tumor cells. Ann Oncol. 2008;19(3):496–500.
    1. Budd GT, Cristofanilli M, Ellis MJ, et al. Circulating tumor cells versus imaging--predicting overall survival in metastatic breast cancer. Clin Cancer Res. 2006;12(21):6403–6409.
    1. Pierga JY, Hajage D, Bachelot T, et al. High independent prognostic and predictive value of circulating tumor cells compared with serum tumor markers in a large prospective trial in first-line chemotherapy for metastatic breast cancer patients. Ann Oncol. 2012;23(3):618–624.
    1. Tewes M, Aktas B, Welt A, et al. Molecular profiling and predictive value of circulating tumor cells in patients with metastatic breast cancer: an option for monitoring response to breast cancer related therapies. Breast Cancer Res Treat. 2009;115(3):581–590.
    1. Falck A-K, Bendahl P-O, Ingvar C, et al. Analysis of and prognostic information from disseminated tumour cells in bone marrow in primary breast cancer: a prospective observational study. BMC Cancer. 2012;12(1):403.
    1. Domschke C, Diel IJ, Englert S, et al. Prognostic Value of Disseminated Tumor Cells in the Bone Marrow of Patients with Operable Primary Breast Cancer: A Long-term Follow-up Study. Ann Surg Oncol. 2013;20(6):1865–1871.
    1. Hartkopf AD, Wallwiener M, Fehm TN, et al. Disseminated tumor cells from the bone marrow of patients with nonmetastatic primary breast cancer are predictive of locoregional relapse. Ann Oncol. 2015;26(6):1155–1160.
    1. Hall C, Krishnamurthy S, Lodhi A, et al. Disseminated tumor cells predict survival after neoadjuvant therapy in primary breast cancer. Cancer. 2012;118(2):342–348.
    1. Mathiesen RR, Borgen E, Renolen A, et al. Persistence of disseminated tumor cells after neoadjuvant treatment for locally advanced breast cancer predicts poor survival. Breast Cancer Research. 2012;14(4):R117.
    1. Pierga JY, Bidard FC, Autret A. Circulating tumour cells and pathological complete response: independent prognostic factors in inflammatory breast cancer in a pooled analysis of two multicentre phase II trials (BEVERLY-1 and -2) of neoadjuvant chemotherapy combined with bevacizumab. Anna Oncol. 2017;28(1):103–109.
    1. Bidard FC, Michiels S, Riethdorf S, et al. Circulating Tumor Cells in Breast Cancer Patients Treated by Neoadjuvant Chemotherapy: A Meta-analysis. J Natl Cancer Inst. 2018;110(6):560–567.
    1. Ignatiadis M, Dawson SJ. Circulating tumor cells and circulating tumor DNA for precision medicine: dream or reality? Ann Oncol. 2014;25(12):2304–2313.
    1. Jueckstock J, Rack B, Friedl TWP, et al. Detection of circulating tumor cells using manually performed immunocytochemistry (MICC) does not correlate with outcome in patients with early breast cancer – Results of the German SUCCESS-A- trial. BMC Cancer. 2016;16(1):401.
    1. Gormally E, Caboux E, Vineis P, Hainaut P. Circulating free DNA in plasma or serum as biomarker of carcinogenesis: Practical aspects and biological significance. Mutation Research/Reviews in Mutation Research. 2007;635(2-3):105–117.
    1. Cai C, Guo Z, Cao Y, Zhang W, Chen Y. A dual biomarker detection platform for quantitating circulating tumor DNA (ctDNA) Nanotheranostics. 2018;2(1):12–20.
    1. Jahr S, Hentze H, Englisch S, et al. DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res. 2001;61(4):1659–1665.
    1. Schwarzenbach H, Pantel K. Circulating DNA as biomarker in breast cancer. Breast Cancer Research. 2015;17(1):136.
    1. Fumagalli D, Venet D, Ignatiadis M, et al. RNA Sequencing to Predict Response to Neoadjuvant Anti-HER2 Therapy: A Secondary Analysis of the NeoALTTO Randomized Clinical Trial. JAMA Oncol. 2017;3(2):227–234.
    1. Jacques N, Vimond N, Conforti R, et al. Quantification of circulating mature endothelial cells using a whole blood four-color flow cytometric assay. J Immunol Methods. 2008;337(2):132–143.
    1. Woywodt A, Blann AD, Kirsch T, et al. Isolation and enumeration of circulating endothelial cells by immunomagnetic isolation: proposal of a definition and a consensus protocol. J Thromb Haemost. 2006;4(3):671–677.
    1. Zhou F, Zhou Y, Yang M, Wen J, Dong J, Tan W. Optimized multipara-metric flow cytometric analysis of circulating endothelial cells and their subpopulations in peripheral blood of patients with solid tumors: a technical analysis. Cancer Management and Research. 2018;10:447–464.
    1. Kuo Y-H, Lin C-H, Shau W-Y, et al. Dynamics of circulating endothelial cells and endothelial progenitor cells in breast cancer patients receiving cytotoxic chemotherapy. BMC Cancer. 2012;12(1):620.
    1. Tsuji W, Ishiguro H, Tanaka S, Takeuchi M, Ueno T, Toi M. Orally administered S-1 suppresses circulating endothelial cell counts in metastatic breast cancer patients. Int J Clin Oncol. 2014;19(3):452–459.
    1. Goon PK, Lip GY, Stonelake PS, Blann AD. Circulating endothelial cells and circulating progenitor cells in breast cancer: relationship to endothelial damage/dysfunction/apoptosis, clinicopathologic factors, and the Nottingham Prognostic Index. Neoplasia. 2009;11(8):771–779.
    1. Ali AM, Ueno T, Tanaka S, et al. Determining circulating endothelial cells using CellSearch system during preoperative systemic chemotherapy in breast cancer patients. Eur J Cancer. 2011;47(15):2265–2272.
    1. Botelho MC, Alves H. Endothelial Progenitor Cells in Breast Cancer. Int J Immunother Cancer Res. 2016;2:1–2.
    1. Gingras I, Salgado R, Ignatiadis M. Liquid biopsy: will it be the ‘magic tool’ for monitoring response of solid tumors to anticancer therapies? Curr Opin Oncol. 2015;27(6):560–567.
    1. Lowes L, Bratman S, Dittamore R, et al. Circulating Tumor Cells (CTC) and Cell-Free DNA (cfDNA) Workshop 2016: Scientific Opportunities and Logistics for Cancer Clinical Trial Incorporation. Int J Mol Sci. 2016;17(9):1505.
    1. O’Hanlon DM, Kerin MJ, Kent P, Maher D, Grimes H, Given HF. An evaluation of preoperative CA 15-3 measurement in primary breast carcinoma. Br J Cancer. 1995;71(6):1288–1291.
    1. Uehara M, Kinoshita T, Hojo T, Akashi-Tanaka S, Iwamoto E, Fukutomi T. Long-term prognostic study of carcinoembryonic antigen (CEA) and carbohydrate antigen 15-3 (CA 15-3) in breast cancer. Int J Clin Oncol. 2008;13(5):447–451.
    1. Park BW, Oh JW, Kim JH, et al. Preoperative CA 15-3 and CEA serum levels as predictor for breast cancer outcomes. Ann Oncol. 2008;19(4):675–681.
    1. Moazzezy N, Farahany TZ, Oloomi M, Bouzari S. Relationship between preoperative serum CA 15-3 and CEA levels and clinicopathological parameters in breast cancer. Asian Pac J Cancer Prev. 2014;15(4):1685–1688.
    1. Atoum M, Nimer N, Abdeldayem S, Nasr H. Relationships among serum CA15-3 tumor marker, TNM staging, and estrogen and progesterone receptor expression in benign and malignant breast lesions. Asian Pac J Cancer Prev. 2012;13(3):857–860.
    1. Samy N, Ragab HM, El Maksoud NA, Shaalan M. Prognostic significance of serum Her2/neu, BCL2, CA15-3 and CEA in breast cancer patients: A short follow-up. Cancer Biomarkers. 2010;6(2):63–72.
    1. Fu Y, Li H. Assessing Clinical Significance of Serum CA15-3 and Carcinoembryonic Antigen (CEA) Levels in Breast Cancer Patients: A Meta-Analysis. Med Sci Monit. 2016;22:3154–3162.
    1. Harris L, Fritsche H, Mennel R, et al. American Society of Clinical Oncology 2007 update of recommendations for the use of tumor markers in breast cancer. J Clin Oncol. 2007;25(33):5287–5312.
    1. Harris L, Fritsche H, Mennel R, et al. American Society of Clinical Oncology 2007 update of recommendations for the use of tumor markers in breast cancer. J Clin Oncol. 2007;25(33):5287–5312.
    1. Nassar FJ, Nasr R, Talhouk R. MicroRNAs as biomarkers for early breast cancer diagnosis, prognosis and therapy prediction. Pharmacol Ther. 2017;172:34–49.
    1. Amorim M, Salta S, Henrique R, Jerónimo C. Decoding the usefulness of non-coding RNAs as breast cancer markers. J Transl Med. 2016;14(1):265.
    1. Iorio MV, Casalini P, Tagliabue E, Ménard S, Croce CM. MicroRNA profiling as a tool to understand prognosis, therapy response and resistance in breast cancer. Eur J Cancer. 2008;44(18):2753–2759.
    1. Markou A, Yousef GM, Stathopoulos E, Georgoulias V, Lianidou E. Prognostic Significance of Metastasis-Related MicroRNAs in Early Breast Cancer Patients with a Long Follow-up. Clin Chem. 2014;60(1):197–205.
    1. D’Aiuto F, Callari M, Dugo M, et al. miR-30e* is an independent subtype-specific prognostic marker in breast cancer. Br J Cancer. 2015;113(2):290–298.
    1. Bailey ST, Westerling T, Brown M. Loss of Estrogen-Regulated microRNA Expression Increases HER2 Signaling and Is Prognostic of Poor Outcome in Luminal Breast Cancer. Cancer Res. 2015;75(2):436–445.
    1. Godinho MFE, Sieuwerts AM, Look MP, et al. Relevance of BCAR4 in tamoxifen resistance and tumour aggressiveness of human breast cancer. Br J Cancer. 2010;103(8):1284–1291.
    1. Chen Y-M, Liu Y, Wei H-Y, Lv K-Z, Fu P. Linc-ROR induces epithelial-mesenchymal transition and contributes to drug resistance and invasion of breast cancer cells. Tumor Biology. 2016;37(8):10861–10870.
    1. Paik S, Shak S, Tang G, et al. A Multigene Assay to Predict Recurrence of Tamoxifen-Treated, Node-Negative Breast Cancer. N Engl J Med Overseas Ed. 2004;351(27):2817–2826.
    1. Paik S, Tang G, Shak S, et al. Gene expression and benefit of chemotherapy in women with node-negative, estrogen receptor-positive breast cancer. J Clin Oncol. 2006;24(23):3726–3734.
    1. Sparano JA, Gray RJ, Makower DF, et al. Prospective Validation of a 21-Gene Expression Assay in Breast Cancer. N Engl J Med Overseas Ed. 2015;373(21):2005–2014.
    1. Albain KS, Barlow WE, Shak S, et al. Prognostic and predictive value of the 21-gene recurrence score assay in postmenopausal women with node-positive, oestrogen-receptor-positive breast cancer on chemotherapy: a retrospective analysis of a randomised trial. Lancet Oncol. 2010;11(1):55–65.
    1. Gluz O, Nitz UA, Christgen M, et al. West German Study Group Phase III PlanB Trial: First Prospective Outcome Data for the 21-Gene Recurrence Score Assay and Concordance of Prognostic Markers by Central and Local Pathology Assessment. J Clin Oncol. 2016;34(20):2341–2349.
    1. van ‘t Veer LJ, Dai H, van de Vijver MJ, et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature. 2002;415(6871):530–536.
    1. van de Vijver MJ, He YD, van ‘t Veer LJ, et al. A Gene-Expression Signature as a Predictor of Survival in Breast Cancer. N Engl J Med Overseas Ed. 2002;347(25):1999–2009.
    1. Esteva FJ, Sahin AA, Cristofanilli M, et al. Prognostic Role of a Multigene Reverse Transcriptase-PCR Assay in Patients with Node-Negative Breast Cancer Not Receiving Adjuvant Systemic Therapy. Clinical Cancer Research. 2005;11(9):3315–3319.
    1. Cardoso F, van’t Veer LJ, Bogaerts J, et al. 70-Gene Signature as an Aid to Treatment Decisions in Early-Stage Breast Cancer. N Engl J Med Overseas Ed. 2016;375(8):717–729.
    1. Duffy MJ, Harbeck N, Nap M, et al. Clinical use of biomarkers in breast cancer: Updated guidelines from the European Group on Tumor Markers (EGTM) Eur J Cancer. 2017;75:284–298.
    1. Gnant M, Filipits M, Greil R, et al. Predicting distant recurrence in receptor-positive breast cancer patients with limited clinicopathological risk: using the PAM50 Risk of Recurrence score in 1478 postmenopausal patients of the ABCSG-8 trial treated with adjuvant endocrine therapy alone. Ann Oncol. 2014;25(2):339–345.
    1. Parker JS, Mullins M, Cheang MC, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol. 2009;27(8):1160–1167.
    1. Filipits M, Rudas M, Jakesz R, et al. A New Molecular Predictor of Distant Recurrence in ER-Positive, HER2-Negative Breast Cancer Adds Independent Information to Conventional Clinical Risk Factors. Clinical Cancer Research. 2011;17(18):6012–6020.
    1. Zhang Y, Schnabel CA, Schroeder BE, et al. Breast Cancer Index Identifies Early-Stage Estrogen Receptor-Positive Breast Cancer Patients at Risk for Early- and Late-Distant Recurrence. Clinical Cancer Research. 2013;19(15):4196–4205.
    1. Demaria S, Pikarsky E, Karin M, et al. Cancer and inflammation: promise for biologic therapy. J Immunother. 2010;33(4):335–351.
    1. Mohme M, Riethdorf S, Pantel K. Circulating and disseminated tumour cells — mechanisms of immune surveillance and escape. Nat Rev Clin Oncol. 2017;14(3):155–167.
    1. Mittal D, Gubin MM, Schreiber RD, Smyth MJ. New insights into cancer immunoediting and its three component phases—elimination, equilibrium and escape. Curr Opin Immunol. 2014;27:16–25.
    1. Choi J, Gyamfi J, Jang H, Koo JS. The role of tumor-associated macrophage in breast cancer biology. Histol Histopathol. 2017;1916;1
    1. Anani W, Shurin MR. Targeting Myeloid-Derived Suppressor Cells in Cancer. Adv Exp Med Biol. 2017;1036:105–128.
    1. Wargo JA, Reuben A, Cooper ZA, Oh KS, Sullivan RJ. Immune Effects of Chemotherapy, Radiation, and Targeted Therapy and Opportunities for Combination With Immunotherapy. Semin Oncol. 2015;42(4):601–616.
    1. Savas P, Salgado R, Denkert C, et al. Clinical relevance of host immunity in breast cancer: from TILs to the clinic. Nat Rev Clin Oncol. 2016;13(4):228–241.
    1. Salgado R, Denkert C, Demaria S, et al. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol. 2015;26(2):259–271.
    1. Simon RM, Paik S, Hayes DF. Use of Archived Specimens in Evaluation of Prognostic and Predictive Biomarkers. JNCI Journal of the National Cancer Institute. 2009;101(21):1446–1452.
    1. Seo AN, Lee HJ, Kim EJ, et al. Tumour-infiltrating CD8+ lymphocytes as an independent predictive factor for pathological complete response to primary systemic therapy in breast cancer. Br J Cancer. 2013;109(10):2705–2713.
    1. Salgado R, Denkert C, Campbell C, et al. Tumor-Infiltrating Lymphocytes and Associations With Pathological Complete Response and Event-Free Survival in HER2-Positive Early-Stage Breast Cancer Treated With Lapatinib and Trastuzumab. JAMA Oncol. 2015;1(4):448–454.
    1. Ali HR, Provenzano E, Dawson S-J, et al. Association between CD8+ T-cell infiltration and breast cancer survival in 12 439 patients. Annals of Oncology. 2014;25(8):1536–1543.
    1. Loi S, Sirtaine N, Piette F, 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(7):860–867.
    1. Denkert C, von Minckwitz G, Darb-Esfahani S, et al. Tumour-infiltrating lymphocytes and prognosis in different subtypes of breast cancer: a pooled analysis of 3771 patients treated with neoadjuvant therapy. Lancet Oncol. 2018;19(1):40–50.
    1. Lewis CE, Pollard JW. Distinct Role of Macrophages in Different Tumor Microenvironments. Cancer Res. 2006;66(2):605–612.
    1. Mantovani A, Marchesi F, Malesci A, Laghi L, Allavena P. Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol. 2017;14(7):399–416.
    1. Biswas SK, Allavena P, Mantovani A. Tumor-associated macrophages: functional diversity, clinical significance, and open questions. Semin Immunopathol. 2013;35(5):585–600.
    1. Zhao X, Qu J, Sun Y, et al. Prognostic significance of tumor-associated macrophages in breast cancer: a meta-analysis of the literature. Oncotarget. 2017;8(18):30576–30586.
    1. Park K-Y, Li G, Platt MO. Monocyte-derived macrophage assisted breast cancer cell invasion as a personalized, predictive metric to score metastatic risk. Sci Rep. 2015;5(1):13855.
    1. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009;9(3):162–174.
    1. Condamine T, Gabrilovich DI. Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol. 2011;32(1):19–25.
    1. Toor SM, Syed Khaja AS, El Salhat H, et al. Myeloid cells in circulation and tumor microenvironment of breast cancer patients. Cancer Immunology, Immunotherapy. 2017;66(6):753–764.
    1. Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin–cyclophosphamide chemotherapy. Cancer Immunology, Immunotherapy. 2009;58(1):49–59.
    1. Wesolowski R, Duggan MC, Stiff A, et al. Circulating myeloid-derived suppressor cells increase in patients undergoing neo-adjuvant chemotherapy for breast cancer. Cancer Immunology, Immunotherapy. 2017;66(11):1437–1447.
    1. Lebien TW, Tedder TF. B lymphocytes: how they develop and function. Blood. 2008;112(5):1570–1580.
    1. Brown JR, Wimberly H, Lannin DR, Nixon C, Rimm DL, Bossuyt V. Multiplexed Quantitative Analysis of CD3, CD8, and CD20 Predicts Response to Neoadjuvant Chemotherapy in Breast Cancer. Clinical Cancer Research. 2014;20(23):5995–6005.
    1. Mehr R, Sternberg-Simon M, Michaeli M, Pickman Y. Models and methods for analysis of lymphocyte repertoire generation, development, selection and evolution. Immunol Lett. 2012;148(1):11–22.
    1. Wang J, Yang J. Identification of CD4+CD25+CD127− regulatory T cells and CD14+HLA−DR−/low myeloid-derived suppressor cells and their roles in the prognosis of breast cancer. Biomed Rep. 2016;5(2):208–212.
    1. Demir L, Yigit S, Ellidokuz H, et al. Predictive and prognostic factors in locally advanced breast cancer: effect of intratumoral FOXP3+ Tregs. Clin Exp Metastasis. 2013;30(8):1047–1062.
    1. Sage EK, Schmid TE, Sedelmayr M, et al. Comparative analysis of the effects of radiotherapy versus radiotherapy after adjuvant chemotherapy on the composition of lymphocyte subpopulations in breast cancer patients. Radiother Oncol. 2016;118(1):176–180.
    1. Song Q, Ren J, Zhou X, et al. Circulating CD8 + CD28 − suppressor T cells tied to poorer prognosis among metastatic breast cancer patients receiving adoptive T-cell therapy: A cohort study. Cytotherapy. 2018;20(1):126–133.
    1. Song G, Wang X, Jia J, et al. Elevated level of peripheral CD8+CD28− T lymphocytes are an independent predictor of progression-free survival in patients with metastatic breast cancer during the course of chemotherapy. Cancer Immunology, Immunotherapy. 2013;62(6):1123–1130.
    1. Datta J, Fracol M, Mcmillan MT, et al. Association of Depressed Anti-HER2 T-Helper Type 1 Response With Recurrence in Patients With Completely Treated HER2-Positive Breast Cancer. JAMA Oncol. 2016;2(2):242–246.
    1. Datta J, Berk E, Xu S, et al. Anti-HER2 CD4+ T-helper type 1 response is a novel immune correlate to pathologic response following neoadjuvant therapy in HER2-positive breast cancer. Breast Cancer Research. 2015;17(1):71.
    1. O’Connor JP, Aboagye EO, Adams JE, et al. Imaging biomarker roadmap for cancer studies. Nat Rev Clin Oncol. 2017;14(3):169–186.
    1. Chagpar AB, Middleton LP, Sahin AA, et al. Accuracy of Physical Examination, Ultrasonography, and Mammography in Predicting Residual Pathologic Tumor Size in Patients Treated With Neoadjuvant Chemotherapy. Ann Surg. 2006;243(2):257–264.
    1. Fowler AM, Mankoff DA, Joe BN. Imaging Neoadjuvant Therapy Response in Breast Cancer. Radiology. 2017;285(2):358–375.
    1. Croshaw R, Shapiro-Wright H, Svensson E, Erb K, Julian T. Accuracy of Clinical Examination, Digital Mammogram, Ultrasound, and MRI in Determining Postneoadjuvant Pathologic Tumor Response in Operable Breast Cancer Patients. Ann Surg Oncol. 2011;18(11):3160–3163.
    1. Keune JD, Jeffe DB, Schootman M, Hoffman A, Gillanders WE, Aft RL. Accuracy of ultrasonography and mammography in predicting pathologic response after neoadjuvant chemotherapy for breast cancer. Am J Surg. 2010;199(4):477–484.
    1. Heine JJ, Malhotra P, Tissue M. breast cancer risk, serial image analysis, and digital mammography. Part 1. Tissue and related risk factors. Acad Radiol. 2002;9(3):298–316.
    1. Jafari SH, Saadatpour Z, Salmaninejad A, et al. Breast cancer diagnosis: Imaging techniques and biochemical markers. J Cell Physiol. 2018;233(7):5200–5213.
    1. Schelling M, Avril N, Nährig J, et al. Positron emission tomography using [18F]Fluorodeoxyglucose for monitoring primary chemotherapy in breast cancer. J Clin Oncol. 2000;18(8):1689–1695.
    1. Lee HW, Lee HM, Choi SE, et al. The Prognostic Impact of Early Change in 18F-FDG PET SUV After Neoadjuvant Chemotherapy in Patients with Locally Advanced Breast Cancer. J Nucl Med. 2016;57(8):1183–1188.
    1. Dose Schwarz J, Bader M, Jenicke L, Hemminger G, Jänicke F, Avril N. Early prediction of response to chemotherapy in metastatic breast cancer using sequential 18F-FDG PET. J Nucl Med. 2005;46(7):1144–1150.
    1. Kostakoglu L, Duan F, Idowu MO, et al. A Phase II Study of 3’-Deoxy-3’-18F-Fluorothymidine PET in the Assessment of Early Response of Breast Cancer to Neoadjuvant Chemotherapy: Results from ACRIN 6688. J Nucl Med. 2015;56(11):1681–1689.
    1. Lindholm P, Lapela M, Någren K, Lehikoinen P, Minn H, Jyrkkiö S. Preliminary study of carbon-11 methionine PET in the evaluation of early response to therapy in advanced breast cancer. Nucl Med Commun. 2009;30(1):30–36.
    1. Kenny LM, Contractor KB, Hinz R, et al. Reproducibility of [11C] choline-positron emission tomography and effect of trastuzumab. Clin Cancer Res. 2010;16(16):4236–4245.
    1. Ulaner GA, Goldman DA, Corben A, et al. Prospective Clinical Trial of 18F-Fluciclovine PET/CT for Determining the Response to Neoadjuvant Therapy in Invasive Ductal and Invasive Lobular Breast Cancers. J Nucl Med. 2017;58(7):1037–1042.
    1. Pinker K, Helbich TH, Morris EA. The potential of multiparametric MRI of the breast. Br J Radiol. 2017;90(1069):20160715.
    1. Mariscotti G, Houssami N, Durando M, et al. Accuracy of mammography, digital breast tomosynthesis, ultrasound and MR imaging in preoperative assessment of breast cancer. Anticancer Res. 2014;34(3):1219–1225.
    1. Lobbes MBI, Prevos R, Smidt M, et al. The role of magnetic resonance imaging in assessing residual disease and pathologic complete response in breast cancer patients receiving neoadjuvant chemotherapy: a systematic review. Insights Imaging. 2013;4(2):163–175.
    1. Yuan Y, Chen XS, Liu SY, Shen KW. Accuracy of MRI in prediction of pathologic complete remission in breast cancer after preoperative therapy: a meta-analysis. AJR Am J Roentgenol. 2010;195(1):260–268.
    1. Marinovich ML, Houssami N, Macaskill P, et al. Meta-analysis of magnetic resonance imaging in detecting residual breast cancer after neoadjuvant therapy. J Natl Cancer Inst. 2013;105(5):321–333.
    1. Yl G, Pan SM, Ren J, Yang ZX, Jiang GQ. Role of Magnetic Resonance Imaging in Detection of Pathologic Complete Remission in Breast Cancer Patients Treated With Neoadjuvant Chemotherapy: A Meta-analysis. Clin Breast Cancer. 2017;17(4):245–255.
    1. Marino MA, Helbich T, Baltzer P, Pinker-Domenig K. Multiparametric MRI of the breast: A review. J Magn Reson Imaging. 2018;47(2):301–315.
    1. Marinovich ML, Sardanelli F, Ciatto S, et al. Early prediction of pathologic response to neoadjuvant therapy in breast cancer: Systematic review of the accuracy of MRI. Breast. 2012;21(5):669–677.
    1. Prevos R, Smidt ML, Tjan-Heijnen VCG, et al. Pre-treatment differences and early response monitoring of neoadjuvant chemotherapy in breast cancer patients using magnetic resonance imaging: a systematic review. Eur Radiol. 2012;22(12):2607–2616.
    1. Woolf DK, Padhani AR, Taylor NJ, et al. Assessing response in breast cancer with dynamic contrast-enhanced magnetic resonance imaging: Are signal intensity–time curves adequate? Breast Cancer Res Treat. 2014;147(2):335–343.
    1. Li SP, Makris A, Beresford MJ, et al. Use of dynamic contrast-enhanced MR imaging to predict survival in patients with primary breast cancer undergoing neoadjuvant chemotherapy. Radiology. 2011;260(1):68–78.
    1. Raunig DL, Mcshane LM, Pennello G, et al. Quantitative imaging biomarkers: A review of statistical methods for technical performance assessment. Stat Methods Med Res. 2015;24(1):27–67.
    1. Partridge SC, Mcdonald ES. Diffusion weighted magnetic resonance imaging of the breast: protocol optimization, interpretation, and clinical applications. Magn Reson Imaging Clin N Am. 2013;21(3):601–624.
    1. Park SH, Moon WK, Cho N, et al. Diffusion-weighted MR Imaging: Pretreatment Prediction of Response to Neoadjuvant Chemotherapy in Patients with Breast Cancer. Radiology. 2010;257(1):56–63.
    1. Belli P, Costantini M, Ierardi C, et al. Diffusion-weighted Imaging in Evaluating the Response to Neoadjuvant Breast Cancer Treatment. Breast J. 2011;17(6):610–619.
    1. Wu LM, Hu JN, Gu HY, Hua J, Chen J, Xu JR. Can diffusion-weighted MR imaging and contrast-enhanced MR imaging precisely evaluate and predict pathological response to neoadjuvant chemotherapy in patients with breast cancer? Breast Cancer Res Treat. 2012;135(1):17–28.
    1. Sardanelli F, Carbonaro LA, Montemezzi S, Cavedon C, Trimboli RM. Clinical Breast MR Using MRS or DWI: Who Is the Winner? Front Oncol. 2016;6(Suppl 1):217.
    1. Jagannathan NR, Kumar M, Seenu V, et al. Evaluation of total choline from in-vivo volume localized proton MR spectroscopy and its response to neoadjuvant chemotherapy in locally advanced breast cancer. Br J Cancer. 2001;84(8):1016–1022.
    1. Meisamy S, Bolan PJ, Baker EH, et al. Neoadjuvant Chemotherapy of Locally Advanced Breast Cancer: Predicting Response with in Vivo 1H MR Spectroscopy—A Pilot Study at 4 T. Radiology. 2004;233(2):424–431.
    1. Baek HM, Chen JH, Nalcioglu O, Su MY, My S. Proton MR spectroscopy for monitoring early treatment response of breast cancer to neo-adjuvant chemotherapy. Ann Oncol. 2008;19(5):1022–1024.
    1. Yamaguchi K, Nakazono T, Egashira R, et al. Diagnostic Performance of Diffusion Tensor Imaging with Readout-segmented Echo-planar Imaging for Invasive Breast Cancer: Correlation of ADC and FA with Pathological Prognostic Markers. Magn Reson Med Sci. 2017;16(3):245–252.
    1. Furman-Haran E, Nissan N, Ricart-Selma V, Martinez-Rubio C, Degani H, Camps-Herrero J. Quantitative evaluation of breast cancer response to neoadjuvant chemotherapy by diffusion tensor imaging: Initial results. J Magn Reson Imaging. 2017
    1. Fan M, Wu G, Cheng H, Zhang J, Shao G, Li L. Radiomic analysis of DCE-MRI for prediction of response to neoadjuvant chemotherapy in breast cancer patients. Eur J Radiol. 2017;94:140–147.
    1. Lambin P, Leijenaar RTH, Deist TM, et al. Radiomics: the bridge between medical imaging and personalized medicine. Nat Rev Clin Oncol. 2017;14(12):749–762.
    1. Wang J, Kato F, Oyama-Manabe N, et al. Identifying Triple-Negative Breast Cancer Using Background Parenchymal Enhancement Heterogeneity on Dynamic Contrast-Enhanced MRI: A Pilot Radiomics Study. PLoS One. 2015;10(11):e0143308.
    1. Wu J, Gong G, Cui Y, Li R. Intratumor partitioning and texture analysis of dynamic contrast-enhanced (DCE)-MRI identifies relevant tumor subregions to predict pathological response of breast cancer to neoadjuvant chemotherapy. J Magn Reson Imaging. 2016;44(5):1107–1115.
    1. Fan M, Cheng H, Zhang P, et al. DCE-MRI texture analysis with tumor subregion partitioning for predicting Ki-67 status of estrogen receptor-positive breast cancers. J Magn Reson Imaging. 2018;48(1):237–247.
    1. Ha S, Park S, Bang J-I, Kim E-K, Lee H-Y. Metabolic Radiomics for Pretreatment 18F-FDG PET/CT to Characterize Locally Advanced Breast Cancer: Histopathologic Characteristics, Response to Neoadjuvant Chemotherapy, and Prognosis. Sci Rep. 2017;7(1):1556.
    1. Park H, Lim Y, Ko ES, Es K, et al. Radiomics Signature on Magnetic Resonance Imaging: Association with Disease-Free Survival in Patients with Invasive Breast Cancer. Clinical Cancer Research. 2018 Jun 18; Epub.
    1. Eisenhauer EA, Therasse P, Bogaerts J, et al. New response evaluation criteria in solid tumours: Revised RECIST guideline (version 1.1) Eur J Cancer. 2009;45(2):228–247.
    1. Seymour L, Bogaerts J, Perrone A, et al. iRECIST: guidelines for response criteria for use in trials testing immunotherapeutics. Lancet Oncol. 2017;18(3):e143–e152.
    1. Wahl RL, Jacene H, Kasamon Y, Lodge MA. From RECIST to PER-CIST: Evolving Considerations for PET response criteria in solid tumors. J Nucl Med. 2009;50(Suppl 1):122S–150.
    1. Weaver O, Leung JWT. Biomarkers and Imaging of Breast Cancer. AJR Am J Roentgenol. 2018;210(2):271–278.
    1. Li H, Zhu Y, Burnside ES, et al. MR Imaging Radiomics Signatures for Predicting the Risk of Breast Cancer Recurrence as Given by Research Versions of MammaPrint, Oncotype DX, and PAM50 Gene Assays. Radiology. 2016;281(2):382–391.
    1. Pinker K, Shitano F, Sala E, et al. Background, current role, and potential applications of radiogenomics. J Magn Reson Imaging. 2018;47(3):604–620.
    1. Cx M, Gao F, Luo J, et al. NeoPalAna: Neoadjuvant Palbociclib, a Cyclin-Dependent Kinase 4/6 Inhibitor, and Anastrozole for Clinical Stage 2 or 3 Estrogen Receptor-Positive Breast Cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2017;23(15):4055–4065.
    1. Jovanović B, Mayer IA, Mayer EL, et al. A Randomized Phase II Neoadjuvant Study of Cisplatin, Paclitaxel With or Without Everolimus in Patients with Stage II/III Triple-Negative Breast Cancer (TNBC): Responses and Long-term Outcome Correlated with Increased Frequency of DNA Damage Response Gene Mutations, TNBC Subtype, AR Status, and Ki67. Clinical Cancer Research. 2017;23(15):4035–4045.
    1. Curigliano G, Romieu G, Campone M, et al. A phase I/II trial of the safety and clinical activity of a HER2-protein based immunotherapeutic for treating women with HER2-positive metastatic breast cancer. Breast Cancer Res Treat. 2016;156(2):301–310.
    1. Sturgeon C, Hill R, Hortin GL, Thompson D. Taking a new biomarker into routine use - A perspective from the routine clinical biochemistry laboratory. Proteomics Clin Appl. 2010;4(12):892–903.

Source: PubMed

3
Abonneren