Tumor-Infiltrating Lymphocytes and Response to Platinum in Triple-Negative Breast Cancer
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1 VOLUME 33 NUMBER 9 MARCH JOURNAL OF CLINICAL ONCOLOGY E D I T O R I A L Tumor-Infiltrating Lymphocytes and Response to Platinum in Triple-Negative Breast Cancer Nadine M. Tung, Beth Israel Deaconess Medical Center, Boston, MA Eric P. Winer, Dana-Farber Cancer Institute, Boston, MA See accompanying article on page 983 Platinum has received much attention recently for the treatment of newly diagnosed triple-negative breast cancer (TNBC). Two randomized phase II neoadjuvant trials, GeparSixto and CALGB (Cancer and Leukemia Group B) (Alliance), reported that pathologic complete response (pcr) rates were approximately 15% higher with the addition of carboplatin to anthracyclines and taxanes. 1,2 Gepar- Sixto randomly assigned patients with TNBC to once-per-week paclitaxel and liposomal doxorubicin, with or without once-per-week carboplatin, for 18 weeks. Patients also received bevacizumab. The pathologic complete response (pcr) rate in patients with TNBC in the breast and axilla was significantly higher with the addition of carboplatin (53.2% v 36.9%; P.005). CALGB 40603(Alliance) also demonstrated an increased pcr rate in stage II and III TNBC with the addition of carboplatin (once every 3 weeks for four cycles) to paclitaxel and dose-dense doxorubicin and cyclophosphamide (54% v 41%; P.0029). Despite the higher pcr rates, neither study has reported a significant increase in the rate of breast conservation, and there is no long-term follow-up to assess the impact of platinum on either disease-free or overall survival. Even if we conclude that the platinum salts have a role in TNBC, it is not clear whether these agents should be added to current regimens or replace existing drugs. If platinum emerges as an important component of breast cancer treatment, it will be critical to identify biomarkers of benefit for this agent, particularly because it can be associated with substantial toxicity in some patients. Fortunately, there are some promising clues. Several studies have demonstrated that platinum has considerable activity in BRCA1-deficient TNBC. High pcr rates are achieved with neoadjuvant cisplatin in women with TNBC who have germline BRCA1 mutations, 3 and results from GeparSixto and PrECOG 0105 show that the benefit of neoadjuvant platinum may be greater for TNBC in BRCA mutation carriers than in noncarriers. 4,5 Silver et al 6 demonstrated that pcr after cisplatin was significantly higher in TNBC with low BRCA1 mrna expression. Because BRCA1 and BRCA2 play a crucial role in double-strand DNA break repair, measures of genomic instability, including telomeric allelic imbalance, loss of heterozygosity, and large scale transition scores, have been studied as biomarkers for homologous recombination deficiency and have shown predictive value for response to platinum agents in both TNBC and ovarian cancer Several studies have shown that tumor-infiltrating lymphocytes (TILs) predict response to anthracycline-based chemotherapy regimens. TILs are most often found in triple-negative (TN), human epidermal growth factor receptor (HER2) positive, and other highly proliferative breast cancers, and are associated with increased pcr, longer disease-free survival (DFS), and improved overall survival (OS), independent of other prognostic factors The strongest association of TILs and breast cancer outcomes has been shown for TNBC in four phase III adjuvant trials that demonstrated that for every 10% increase in TILs, there is a 15% to 20% increase in DFS and OS In the BIG (Breast International Group) 2-98 trial, for patients with TNBC and 50% TILs, 5-year DFS and OS rates were 92%, representing a significantly decreased risk for both relapse (hazard ratio, 0.3; 95% CI, 0.11 to 0.81) and death (hazard ratio, 0.3; 95% CI, 0.09 to 0.92) compared with patients with lower levels of TILs. 14 Higher pcr rates are also seen after neoadjuvant anthracycline and taxane-based chemotherapy in TN and HER2-positive breast cancer with higher levels of TILs Limited data exist regarding the prognostic value of TILs in the absence of chemotherapy; a few studies have reported that an increase in expression of immune markers in breast cancer is associated with decreased risk of relapse. 18 Borrowing from the lymphoma nomenclature, the term lymphocyte-predominant breast cancer (LPBC) has been used to describe breast cancers with lymphocytes in 50% to 60% or more of the tumor or stroma. 12,15 Between 4% and 11% of TNBCs have been characterized as LPBCs In the majority of studies, TILs in the stromal compartment provide more useful information than intratumoral TILs (itils); the latter are less abundant, and both stromal and itils provide similar prognostic information. When TILs in breast cancer have been characterized, the presence of cytotoxic CD8 T cells has most often been associated with response to therapy and patient survival. 17,19-21 Extensive lymphocytic infiltration in breast cancer is also correlated with higher expression of immune and inflammatory markers. 15,22,23 Among TNBC molecular subtypes, TILs are most frequently observed in the immunomodulatory subtype. 5,24 In the article that accompanies this editorial, Denkert et al 25 report that increasing stromal TILs (stils) and LPBC (20% of HER2- positive tumors and 28% of TNBCs) predict pcr in both TNBC and HER2-positive disease, an association that was significant in multivariable analysis, independent of clinical and other pathologic factors. Furthermore, TILs predicted a significant increase in pcr when platinum was added in a randomized fashion to treatment. Although the test for interaction between platinum and TILs was only significant in Journal of Clinical Oncology, Vol 33, No 9 (March 20), 2015: pp by American Society of Clinical Oncology 969
2 the entire study cohort and the HER2-positive subset, TILs were associated with a significantly higher chance of pcr with carboplatin in the TNBC subset as well. Patients with TNBC who received carboplatin had a significant three-fold increased probability of pcr if the breast cancer was LPBC. Although the focus of this commentary is TNBC, for which questions about the role of platinums are most intriguing, it is worth noting that the significant interaction in HER2- positive disease was actually driven by a particularly low response rate to the carboplatin-containing arm in patients with HER2-positive disease who had low TILs. What is the significance of these results? The finding that TILs predict pcr to chemotherapy in TNBC is consistent with previous studies. However, the finding that stils predict pcr with the addition of platinum to anthracycline and taxane based chemotherapy is intriguing but clearly needs validation. Does this result truly reflect a benefit that is specific to platinum or merely the response of chemosensitive tumors to more chemotherapy? PrECOG 0105 found a significantly higher pcr rate with increasing levels of itils among 70 patients with TNBC who were treated with neoadjuvant platinumbased chemotherapy. However, the PrECOG trial was a small study, and in the absence of a comparative arm, it is again not clear that the improved response to chemotherapy is specific to platinum. 5 If the platinum-induced pcr associated with TILs is confirmed, it could be mediated either by TILs or some other factor associated with TILs that predicts platinum responsiveness. For example, BRCA1-deficient breast cancers often have prominent lymphocytic infiltration and frequently respond to platinum, presumably from an inherent defect in DNA damage repair. 3-6,26 Although immune marker expression in GeparSixto was correlated with stils, it added little predictive value. This finding would suggest that routine hematoxylin and eosin slides, rather than molecular analysis, may be sufficient to predict the benefit of platinum. Why would TILs be predictive of a better response to chemotherapy? Increased chemosensitivity of immunogenic tumors may be a result of the ability of chemotherapy to facilitate an antitumor immune response. Chemotherapy may decrease tumor burden and enable a more effective immune response. Chemotherapy can also favorably modify the immune microenvironment. Indeed, some chemotherapy agents (eg, doxorubicin, cyclophosphamide, oxaliplatin) are believed to induce a so-called immunogenic tumor cell death, namely, one that activates adaptive immunity through antigen release. 27,28 Dieci et al 29 found that 85% of TNBCs that had high levels of lymphocytic infiltration after neoadjuvant chemotherapy actually had higher levels of TILs than before chemotherapy. Chemotherapy can deplete myeloid-derived suppressor cells and regulatory T cells that inhibit the immune antitumor response. 28,30,31 Finally, chemotherapy can create somatic mutations that may produce new peptide antigens that elicit immune responses. 32,33 This provides a rationale for combining immune modulators with chemotherapy to treat some highrisk, immunogenic breast cancers. There are a number of ways in which TILs may ultimately be used to personalize breast cancer treatment. First, a TIL score could serve as a clinically useful prognostic and predictive factor for TNBC and as a stratification factor in future clinical studies. From a therapeutic standpoint, if tumors with increased TILs respond best to chemotherapy, there may be no value in adding additional treatments. However, TILs may also provide the rationale for evaluating immunotherapeutic approaches in breast cancers that engender immune activation. It has been suggested that immune therapy may be most helpful for tumors with an intermediate TIL response in which there is some antitumor response but the response is ineffective or suppressed. 34 Can the successes achieved with T-cell checkpoint inhibitors (eg, anti cytotoxic T-lymphocyte antigen-4 and anti programmed death ligand-1 [PD-L1]) in melanoma, renal cancer, and non small-cell lung cancer be replicated in certain breast cancers? PD-L1 mrna expression is identified in nearly 60% of breast tumors, particularly in hormone receptor negative and high-grade tumors. 35,36 Higher PD-L1 mrna expression is associated with increased TILs, as reported in this study by Denkert et al 25 and other studies. 35,36 This finding may have practical application because the use of PD-L1 antibodies to measure protein expression in formalin-fixed paraffinembedded tissue has been problematic, given the absence of validated assays, reliable antibodies, and consensus regarding what constitutes a positive result. Before it can be used clinically, the methodology for evaluating TILs needs to be standardized to ensure consistency. The study by Denkert et al 25 assessed reproducibility among three independent pathologists in a small subset of tumors. For LPBC, agreement between two pathologists was good ( 0.90), but only moderate with the third evaluator ( 0.60 and 0.69). Consistency for TIL scoring was excellent (intraclass correlation coefficient, 0.97; 95% CI, 0.93 to 0.99; P.001) and better than that reported for Ki-67 evaluation of breast cancers (intraclass correlation coefficient, approximately 0.60). 37 In addition to issues of analytic validity, the clinical significance of TIL levels needs to be verified. If measuring the percentage of TILs in a breast tumor as a continuous variable makes more biologic sense than classifying a tumor as LPBC, is there a clinically significant threshold? Should manual counting of TILs or digital quantification be used? Toward this end, guidelines for assessing TILs have been developed, 38 and a TILs working group will soon be conducting an interlaboratory study to assess the reproducibility and clinical validity of assessing TILs by several methods. In conclusion, a TILs score may become a useful prognostic and predictive factor in TNBC. But before TILs can be used in treatment decisions to assess prognosis and determine therapy, the prognostic and predictive value of TILs needs further validation. Just as important, there are fundamental questions about how to assess TILs and other immune parameters that will need to be resolved through careful investigation. At present, and until outcome data from studies such as GeparSixto and CALGB are available, it is not clear how best to incorporate platinum into the treatment of early TNBC. Perhaps a biomarker of TILs will someday inform this decision. AUTHORS DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST Disclosures provided by the authors are available with this article at AUTHOR CONTRIBUTIONS Manuscript writing: All authors Final approval of manuscript: All authors REFERENCES 1. von Minckwitz G, Schneeweiss A, Loibl S, et al: Neoadjuvant carboplatin in patients with triple-negative and HER2-positive early breast cancer (GeparSixto; GBG 66): A randomised phase 2 trial. 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J Clin Invest 121: , Denkert C, von Minckwitz G, Brase JC, 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 33: , Turner NC, Reis-Filho JS: Basal-like breast cancer and the BRCA1 phenotype. Oncogene 25: , Obeid M, Tesniere A, Ghiringhelli F, et al: Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 13:54-61, Zitvogel L, Apetoh L, Ghiringhelli F, et al: Immunological aspects of cancer chemotherapy. Nat Rev Immunol 8:59-73, Dieci MV, Criscitiello C, Goubar A, et al: Prognostic value of tumorinfiltrating lymphocytes on residual disease after primary chemotherapy for triple-negative breast cancer: A retrospective multicenter study. 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Cancer Immunol Res 2: , Schalper KA, Velcheti V, Carvajal D, et al: In situ tumor PD-L1 mrna expression is associated with increased TILs and better outcome in breast carcinomas. Clin Cancer Res 20: , Mikami Y, Ueno T, Yoshimura K, et al: Interobserver concordance of Ki67 labeling index in breast cancer: Japan Breast Cancer Research Group Ki67 ring study. Cancer Sci 104: , 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 Ann Oncol [epub ahead of print on September 11, 2014] DOI: /JCO ; published online ahead of print at on January 5, by American Society of Clinical Oncology 971
4 AUTHORS DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST Tumor-Infiltrating Lymphocytes and Response to Platinum in Triple-Negative Breast Cancer The following represents disclosure information provided by authors of this manuscript. All relationships are considered compensated. Relationships are self-held unless noted. I Immediate Family Member, Inst My Institution. Relationships may not relate to the subject matter of this manuscript. For more information about ASCO s conflict of interest policy, please refer to or jco.ascopubs.org/site/ifc. Nadine M. Tung Research Funding: Myriad Genetics Eric P. Winer Research Funding: Genentech, Novartis Travel, Accommodations, Expenses: Genentech 2015 by American Society of Clinical Oncology JOURNAL OF CLINICAL ONCOLOGY
5 Acknowledgment We thank David B. Page, Memorial Sloan Kettering Cancer Center, and Michele R. Hacker, Beth Israel Deaconess Medical Center, for helpful conversations in the preparation of this manuscript by American Society of Clinical Oncology
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