Prognostic and predictive significance of tumor infiltrating lymphocytes for ductal carcinoma in situ

References

• DeSantis CE, Ma J, Gaudet MM, Newman LA, Miller KD, Goding Sauer A, Jemal A, Siegel RL. Breast cancer statistics, 2019. CA Cancer J Clin. 2019;69(6):438–9. doi:10.3322/caac.21583.
   PubMed Web of Science ®Google Scholar
• Lari SA, Kuerer HM. Biological markers in DCIS and risk of breast recurrence: a systematic review. J Cancer. 2011;2:232. doi:10.7150/jca.2.232.
   PubMed Web of Science ®Google Scholar
• Correa C, McGale P, Taylor C, Wang Y, Clarke M, Davies C, Peto R, Bijker N, Solin L, Darby S. Overview of the randomized trials of radiotherapy in ductal carcinoma in situ of the breast. J Natl Cancer Inst Monogr. 2010;2010:162–177.
   PubMedGoogle Scholar
• Benson JR, Jatoi I, Toi M. Treatment of low-risk ductal carcinoma in situ: is nothing better than something? Lancet Oncol. 2016;17:e442–e451. doi:10.1016/S1470-2045(16)30367-9.
   PubMed Web of Science ®Google Scholar
• Whiteside TL. Immune responses to cancer: are they potential biomarkers of prognosis? Front Oncol. 2013;3:107. doi:10.3389/fonc.2013.00107.
   PubMedGoogle Scholar
• Mao Y, Qu Q, Chen X, Huang O, Wu J, Shen K. The prognostic value of tumor-infiltrating lymphocytes in breast cancer: a systematic review and meta-analysis. PLoS One. 2016;11(4):e0152500. doi:10.1371/journal.pone.0152500.
   PubMed Web of Science ®Google Scholar
• Hendrickx W, Simeone I, Anjum S, Mokrab Y, Bertucci F, Finetti P, Curigliano G, Seliger B, Cerulo L, Tomei S, et al. Identification of genetic determinants of breast cancer immune phenotypes by integrative genome-scale analysis. Oncoimmunology. 2017;6(2):e1253654. doi:10.1080/2162402X.2016.1253654.
   PubMed Web of Science ®Google Scholar
• Denkert C, von Minckwitz G, Darb-Esfahani S, Lederer B, Heppner BI, Weber KE, Budczies J, Huober J, Klauschen F, Furlanetto J, 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. doi:10.1016/S1470-2045(17)30904-X.
   PubMed Web of Science ®Google Scholar
• Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, Rouas G, Francis P, Crown JPA, 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(7):860–867. doi:10.1200/JCO.2011.41.0902.
   PubMed Web of Science ®Google Scholar
• Gil Del Alcazar CR, Huh SJ, Ekram MB, Trinh A, Liu LL, Beca F, Zi X, Kwak M, Bergholtz H, Su Y, et al. Immune escape in breast cancer during in situ to invasive carcinoma transition. Cancer Discov. 2017;7(10):1098–1115. doi:10.1158/2159-8290.CD-17-0222.
   PubMed Web of Science ®Google Scholar
• Kim M, Chung YR, Kim HJ, Woo JW, Ahn S, Park SY. Immune microenvironment in ductal carcinoma in situ: a comparison with invasive carcinoma of the breast. Breast Cancer Res. 2020;22(1):32. doi:10.1186/s13058-020-01267-w.
   PubMed Web of Science ®Google Scholar
• Thompson E, Taube JM, Elwood H, Sharma R, Meeker A, Warzecha HN, Argani P, Cimino-Mathews A, Emens LA. The immune microenvironment of breast ductal carcinoma in situ. Mod Pathol. 2016;29(3):249–258. doi:10.1038/modpathol.2015.158.
   PubMed Web of Science ®Google Scholar
• Morita M, Yamaguchi R, Tanaka M, Tse GM, Yamaguchi M, Otsuka H, Kanomata N, Minami S, Eguchi S, Yano H, et al. Two progressive pathways of microinvasive carcinoma: low-grade luminal pathway and high-grade HER2 pathway based on high tumour-infiltrating lymphocytes. J Clin Pathol. 2016;69(10):890–898. doi:10.1136/jclinpath-2015-203506.
   PubMed Web of Science ®Google Scholar
• Agahozo MC, Hammerl D, Debets R, Kok M, van Deurzen CHM. Tumor-infiltrating lymphocytes and ductal carcinoma in situ of the breast: friends or foes? Mod Pathol. 2018;31(7):1012–1025. doi:10.1038/s41379-018-0030-x.
   PubMed Web of Science ®Google Scholar
• Pruneri G, Lazzeroni M, Bagnardi V, Tiburzio GB, Rotmensz N, DeCensi A, Guerrieri-Gonzaga A, Vingiani A, Curigliano G, Zurrida S, et al. The prevalence and clinical relevance of tumor-infiltrating lymphocytes (TILs) in ductal carcinoma in situ of the breast. Ann Oncol. 2017;28(2):321–328. doi:10.1093/annonc/mdw623.
   PubMed Web of Science ®Google Scholar
• Dieci MV, Radosevic-Robin N, Fineberg S, van den Eynden G, Ternes N, Penault-Llorca F, Pruneri G, D’Alfonso TM, Demaria S, Castaneda C, et al. Update on tumor-infiltrating lymphocytes (TILs) in breast cancer, including recommendations to assess TILs in residual disease after neoadjuvant therapy and in carcinoma in situ: a report of the international immuno-oncology biomarker working group on breast cancer. Semin Cancer Biol. 2018;52:16–25. doi:10.1016/j.semcancer.2017.10.003.
   PubMed Web of Science ®Google Scholar
• Toss MS, Miligy I, Al-Kawaz A, Alsleem M, Khout H, Rida PC, Aneja R, Green AR, Ellis IO, Rakha EA, et al. Prognostic significance of tumor-infiltrating lymphocytes in ductal carcinoma in situ of the breast. Mod Pathol. 2018;31(8):1226–1236. doi:10.1038/s41379-018-0040-8.
   PubMed Web of Science ®Google Scholar
• Li X, Schwartz MR, Ro J, Hamilton CR, Ayala AG, Truong LD, Zhai QJ. Diagnostic utility of E-cadherin and P120 catenin cocktail immunostain in distinguishing DCIS from LCIS. Int J Clin Exp Pathol. 2014;7:2551–2557.
   PubMed Web of Science ®Google Scholar
• Dewar R, Fadare O, Gilmore H, Gown AM. Best practices in diagnostic immunohistochemistry: myoepithelial markers in breast pathology. Arch Pathol Lab Med. 2011;135:422–429. doi:10.1043/2010-0336-CP.1.
   PubMed Web of Science ®Google Scholar
• Yurchenco PD. Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harbor Perspect Biol. 2011;3. doi:10.1101/cshperspect.a004911.
   PubMed Web of Science ®Google Scholar
• Hendry S, Salgado R, Gevaert T, Russell PA, John T, Thapa B, Christie M, van de Vijver K, Estrada MV, Gonzalez-Ericsson PI, et al. Assessing tumor-infiltrating lymphocytes in solid tumors: a practical review for pathologists and proposal for a standardized method from the international immunooncology biomarkers working group: part 1: assessing the host immune response, TILs in invasive breast carcinoma and ductal carcinoma in situ, metastatic tumor deposits and areas for further research. Adv Anat Pathol. 2017;24:235–251. doi:10.1097/PAP.0000000000000162.
   PubMed Web of Science ®Google Scholar
• Chen XY, Yeong J, Thike AA, Bay BH, Tan PH. Prognostic role of immune infiltrates in breast ductal carcinoma in situ. Breast Cancer Res Treat. 2019;177:17–27. doi:10.1007/s10549-019-05272-2.
   PubMed Web of Science ®Google Scholar
• 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. doi:10.1200/JCO.2013.55.0491.
   PubMed Web of Science ®Google Scholar
• Perez EA, Ballman KV, Tenner KS, Thompson EA, Badve SS, Bailey H, Baehner FL. Association of stromal tumor-infiltrating lymphocytes with recurrence-free survival in the N9831 adjuvant trial in patients with early-stage HER2-positive breast cancer. JAMA Oncol. 2016;2:56–64. doi:10.1001/jamaoncol.2015.3239.
   PubMed Web of Science ®Google Scholar
• Darvishian F, Ozerdem U, Adams S, Chun J, Pirraglia E, Kaplowitz E, Guth A, Axelrod D, Shapiro R, Price A, et al. Tumor-infiltrating lymphocytes in a contemporary cohort of women with ductal carcinoma in situ (DCIS). Ann Surg Oncol. 2019;26:3337–3343. doi:10.1245/s10434-019-07562-x.
   PubMed Web of Science ®Google Scholar
• Cuzick J, Sestak I, Pinder SE, Ellis IO, Forsyth S, Bundred NJ, Forbes JF, Bishop H, Fentiman IS, George WD, et al. Effect of tamoxifen and radiotherapy in women with locally excised ductal carcinoma in situ: long-term results from the UK/ANZ DCIS trial. Lancet Oncol. 2011;12:21–29. doi:10.1016/S1470-2045(10)70266-7.
   PubMed Web of Science ®Google Scholar
• Margolese RG, Cecchini RS, Julian TB, Ganz PA, Costantino JP, Vallow LA, Albain KS, Whitworth PW, Cianfrocca ME, Brufsky AM, et al. Anastrozole versus tamoxifen in postmenopausal women with ductal carcinoma in situ undergoing lumpectomy plus radiotherapy (NSABP B-35): a randomised, double-blind, phase 3 clinical trial. Lancet. 2016;387:849–856. doi:10.1016/S0140-6736(15)01168-X.
   PubMed Web of Science ®Google Scholar
• Beguinot M, Dauplat MM, Kwiatkowski F, Lebouedec G, Tixier L, Pomel C, Penault-Llorca F, Radosevic-Robin N. Analysis of tumour-infiltrating lymphocytes reveals two new biologically different subgroups of breast ductal carcinoma in situ. BMC Cancer. 2018;18:129. doi:10.1186/s12885-018-4013-6.
   PubMed Web of Science ®Google Scholar
• Nelson AC, Machado HL, Schwertfeger KL. Breaking through to the other side: microenvironment contributions to DCIS initiation and progression. J Mammary Gland Biol Neoplasia. 2018;23:207–221. doi:10.1007/s10911-018-9409-z.
   PubMed Web of Science ®Google Scholar
• Kuerer HM, Buzdar AU, Mittendorf EA, Esteva FJ, Lucci A, Vence LM, Radvanyi L, Meric-Bernstam F, Hunt KK, Symmans WF, et al. Biologic and immunologic effects of preoperative trastuzumab for ductal carcinoma in situ of the breast. Cancer. 2011;117:39–47. doi:10.1002/cncr.25399.
   PubMed Web of Science ®Google Scholar
• Cobleigh MA, Anderson SJ, Siziopikou KP, Arthur DW, Julian TB, Rabinovitch R, Parda DS, Seaward SA, Carter DL, Lyons JA, et al. Primary results of NRG Oncology/NSABP B-43: phase III trial comparing concurrent trastuzumab (T) and radiation therapy (RT) with RT alone for women with HER2-positive ductal carcinoma in situ (DCIS) after lumpectomy. J Clin Oncol. 2020;38:508. doi:10.1200/JCO.2020.38.15_suppl.508.
   Web of Science ®Google Scholar
• Komforti M, Badve SS, Harmon B, Lo Y, Fineberg S. Tumour-infiltrating lymphocytes in ductal carcinoma in situ (DCIS)—assessment with three different methodologies and correlation with Oncotype DX DCIS Score. Histopathology. 2020;77:749–759. doi:10.1111/his.14181.
   PubMed Web of Science ®Google Scholar
• Hendry S, Pang JB, Byrne DJ, Lakhani SR, Cummings MC, Campbell IG, Mann GB, Gorringe KL, Fox SB. Relationship of the breast ductal carcinoma in situ immune microenvironment with clinicopathological and genetic features. Clin Cancer Res. 2017;23:5210–5217. doi:10.1158/1078-0432.CCR-17-0743.
   PubMed Web of Science ®Google Scholar
• Davoli T, Uno H, Wooten EC, Elledge SJ. Tumor aneuploidy correlates with markers of immune evasion and with reduced response to immunotherapy. Science. 2017;355:eaaf8399. doi:10.1126/science.aaf8399.
   PubMed Web of Science ®Google Scholar
• Toss MS, Abidi A, Lesche D, Joseph C, Mahale S, Saunders H, Kader T, Miligy IM, Green AR, Gorringe KL, et al. The prognostic significance of immune microenvironment in breast ductal carcinoma in situ. Br J Cancer. 2020;122:1496–1506. doi:10.1038/s41416-020-0797-7.
   PubMed Web of Science ®Google Scholar
• Thike AA, Chen X, Koh VCY, Binte Md Nasir ND, Yeong JPS, Bay BH, Tan PH. Higher densities of tumour-infiltrating lymphocytes and CD4 + T cells predict recurrence and progression of ductal carcinoma in situ of the breast. Histopathology. 2020;76(6):852–864. doi:10.1111/his.14055.
   PubMed Web of Science ®Google Scholar
• Semeraro M, Adam J, Stoll G, Louvet E, Chaba K, Poirier-Colame V, Sauvat A, Senovilla L, Vacchelli E, Bloy N, et al. The ratio of CD8 +/FOXP3 T lymphocytes infiltrating breast tissues predicts the relapse of ductal carcinoma in situ. Oncoimmunology. 2016;5:e1218106. doi:10.1080/2162402X.2016.1218106.
   PubMed Web of Science ®Google Scholar
• Campbell MJ, Baehner F, O’Meara T, Ojukwu E, Han B, Mukhtar R, Tandon V, Endicott M, Zhu Z, Wong J, et al. Characterizing the immune microenvironment in high-risk ductal carcinoma in situ of the breast. Breast Cancer Res Treat. 2017;161(1):17–28. doi:10.1007/s10549-016-4036-0.
   PubMed Web of Science ®Google Scholar
• Ishigami E, Sakakibara M, Sakakibara J, Masuda T, Fujimoto H, Hayama S, Nagashima T, Sangai T, Nakagawa A, Nakatani Y, et al. Coexistence of regulatory B cells and regulatory T cells in tumor-infiltrating lymphocyte aggregates is a prognostic factor in patients with breast cancer. Breast Cancer. 2019;26(2):180–189. doi:10.1007/s12282-018-0910-4.
   PubMed Web of Science ®Google Scholar
• Kovács A, Stenmark Tullberg A, Werner Rönnerman E, Holmberg E, Hartman L, Sjöström M, Lundstedt D, Malmström P, Fernö M, Karlsson P, et al. Effect of radiotherapy after breast-conserving surgery depending on the presence of tumor-infiltrating lymphocytes: a long-term follow-up of the SweBCG91RT randomized trial. J Clin Oncol. 2019;37:1179–1187. doi:10.1200/JCO.18.02157.
   PubMed Web of Science ®Google Scholar
• Shiao SL, Coussens LM. The tumor-immune microenvironment and response to radiation therapy. J Mammary Gland Biol Neoplasia. 2010;15:411–421. doi:10.1007/s10911-010-9194-9.
   PubMed Web of Science ®Google Scholar
• Burnette BC, Liang H, Lee Y, Chlewicki L, Khodarev NN, Weichselbaum RR, Fu Y-X, Auh SL. The efficacy of radiotherapy relies upon induction of type i interferon-dependent innate and adaptive immunity. Cancer Res. 2011;71:2488–2496. doi:10.1158/0008-5472.CAN-10-2820.
   PubMed Web of Science ®Google Scholar