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Original Investigation
June27, 2024
Veerle C. M.Geurts,MD1; SaraBalduzzi,PhD2; Tessa G.Steenbruggen,MD, PhD3,4; et al Sabine C.Linn,MD, PhD3,5,6; SabineSiesling,PhD7,8; Sunil S.Badve,MD9,10; AngelaDeMichele,MD, MSCE11; MichailIgnatiadis,MD, PhD12; Roberto A.Leon-Ferre,MD13; Matthew P.Goetz,MD13; Antonio C.Wolff,MD14; NatalieKlar,MD15,16; StefanMichiels,PhD17; ShereneLoi,MD, PhD18,19; SylviaAdams,MD15,16; Hugo M.Horlings,MD, PhD5; Gabe S.Sonke,MD, PhD3; RobertoSalgado,MD, PhD20,21; MarleenKok,MD, PhD1,3
Author Affiliations Article Information
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1Division of Tumor Biology and Immunology, the Netherlands Cancer Institute, Amsterdam, the Netherlands
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2Department of Biometrics, the Netherlands Cancer Institute, Amsterdam, the Netherlands
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3Department of Medical Oncology, the Netherlands Cancer Institute, Amsterdam, the Netherlands
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4Department of Internal Medicine, St Antonius Hospital, Nieuwegein, the Netherlands
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5Department of Pathology, the Netherlands Cancer Institute, Amsterdam, the Netherlands
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6Division of Pathology, University Medical Center Utrecht, Utrecht, the Netherlands
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7Department of Research and Development, the Netherlands Comprehensive Cancer Organization (IKNL), Utrecht, the Netherlands
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8Department of Health, Technology and Services Research, Technical Medical Centre, University of Twente, Enschede, the Netherlands
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9Department of Pathology and Laboratory Medicine, Emory University School of Medicine, Atlanta, Georgia
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10Winship Cancer Institute, Emory University, Atlanta, Georgia
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11Department of Medicine, University of Pennsylvania, Philadelphia
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12Department of Medical Oncology, Université Libre de Bruxelles, Institut Jules Bordet, Brussels, Belgium
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13Department of Oncology, Mayo Clinic, Rochester, Minnesota
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14Department of Medicine, Johns Hopkins University, Baltimore, Maryland
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15Perlmutter Cancer Center, New York University, New York
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16Grossman School of Medicine, New York University, New York
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17Service de Biostatistique et d’Epidémiologie, Gustave Roussy, Oncostat U1018, Inserm, Paris-Saclay University, labeled Ligue Contre le Cancer, Villejuif, France
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18Division of Cancer Research, Peter Mac Callum Cancer Center, Melbourne, Victoria, Australia
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19The Sir Peter MacCallum Department of Medical Oncology, University of Melbourne, Parkville, Australia
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20Department of Pathology, Ziekenhuis aan de Stroom (ZAS), Antwerp, Belgium
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21Division of Research, Peter Mac Callum Cancer Center, Melbourne, Victoria, Australia
JAMA Oncol. Published online June 27, 2024. doi:10.1001/jamaoncol.2024.1917
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Question What is the role of stromal tumor-infiltrating lymphocytes (sTILs) in the outcome of patients with stage I triple-negative breast cancer (TNBC) who did not receive neoadjuvant or adjuvant chemotherapy?
Findings In this cohort study of 4511 females, sTILs were scored in 1041 patients with stage I TNBC. Patients with pT1c tumors and an sTIL level of 50% or greater had a 10-year survival of 95% without chemotherapy, increasing to 98% with an sTIL level of 75% or greater; an association with less magnitude was found between sTILs and outcome in patients with pT1ab tumors.
Meaning Findings of this study further support clinical trials to optimize chemotherapy for patients with stage I TNBC with a high level of sTILs.
Abstract
Importance The absolute benefit of chemotherapy for all patients with stage I triple-negative breast cancer (TNBC) is unclear, and biomarkers are not currently available for selecting patients with an excellent outcome for whom neoadjuvant or adjuvant chemotherapy may have negligible benefit. High levels of stromal tumor-infiltrating lymphocytes (sTILs) are associated with favorable survival in TNBC, but data solely in stage I TNBC are lacking.
Objective To examine the outcomes of patients of all ages with stage I TNBC solely and who received neither neoadjuvant nor adjuvant chemotherapy, according to centrally reviewed sTIL levels at prespecified cutoffs.
Design, Setting, and Participants This cohort study used the Netherlands Cancer Registry to identify patients diagnosed with stage I TNBC between January 1, 2005, and December 31, 2015, who were not treated with chemotherapy. Only patients who did not receive neoadjuvant and/or adjuvant chemotherapy were selected. The clinical data were matched with their corresponding pathology data provided by the Dutch Pathology Registry. Data analysis was performed between February and October 2023.
Main Outcomes and Measures The primary end point was breast cancer–specific survival (BCSS) at 5, 10, and 15 years for the prespecified sTIL level cutoffs of 30%, 50%, and 75%. Hematoxylin and eosin–stained slides were used for central review of histologic subtype, grade, and lymphovascular invasion. The International Immuno-Oncology Biomarker Working Group guidelines were used to score the sTIL levels; these levels were determined for 1041 patients.
Results A total of 4511 females with stage I TNBC (mean [SD] age at diagnosis, 64.4 [11.1] years; median follow-up, 11.4 [95% CI, 10.9-11.9] years) were included. Most tumors (952 [91.5%]) were invasive carcinomas of nonspecial histologic subtype. Most patients (548 [52.6%]) had pT1cN0 tumors. Median (range) sTIL level was 5% (1%-99%). A total of 775 patients (74.4%) had sTIL levels below 30%, 266 (25.6%) had 30% or greater, 203 (19.5%) had 50% or greater, and 141 (13.5%) had 75% or greater. Patients with pT1abN0 tumors had a more favorable outcome vs patients with pT1cN0 tumors, with a 10-year BCSS of 92% (95% CI, 89%-94%) vs 86% (95% CI, 82%-89%). In the overall cohort, sTIL levels of at least 30% were associated with better BCSS compared with sTIL levels less than 30% (96% and 87%, respectively; hazard ratio [HR], 0.45; 95% CI, 0.26-0.77). High sTIL levels of 50% or greater were associated with a better outcome than low sTIL levels of less than 50% (HR, 0.27; 95% CI, 0.10-0.74) in patients with pT1C tumors, with a 10-year BCSS of 95% increasing to 98% with sTIL levels of 75% or greater.
Conclusions and Relevance Results of this study showed that patients with stage I TNBC and high level of sTILs who did not receive neoadjuvant or adjuvant chemotherapy had excellent 10-year BCSS. The findings further support the role of sTILs as integral biomarkers in prospective clinical trials of therapy optimization for this patient population.
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Geurts VCM, Balduzzi S, Steenbruggen TG, et al. Tumor-Infiltrating Lymphocytes in Patients With Stage I Triple-Negative Breast Cancer Untreated With Chemotherapy. JAMA Oncol. Published online June 27, 2024. doi:10.1001/jamaoncol.2024.1917
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