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Cited by 24Breast Cancer Treatment StudiesBreast Lesions and CarcinomasMRI in cancer diagnosis

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Association of tumor‐infiltrating lymphocytes before and after neoadjuvant chemotherapy with pathological complete response and prognosis in patients with breast cancer

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Hong, Jin, Rui, Weiwei, Fei, Xiaochun, Chen, Xiaosong, Shen, Kunwei·2021·Cancer Medicine
DOI 10.1002/cam4.4302PMC PMC8607245
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Abstract

PURPOSE: To evaluate the predictive and prognostic value of tumor-infiltrating lymphocytes (TILs) before and after neoadjuvant chemotherapy (NAC) in patients with breast cancer. PATIENTS AND METHODS: Consecutive breast cancer patients treated with NAC between August 2008 and November 2019 were retrospectively analyzed. TIL levels were evaluated of invasive tumor samples, and high expression was defined as TILs >10%. Total pathological complete response (pCR) was defined as no invasive tumor in the breast or lymph nodes. Univariate and multivariate analyses were used to assess factors associated with pCR rate, disease-free survival (DFS), and overall survival. RESULTS: A total of 461 patients were included. The mean pre-NAC TIL level was higher among patients with pCR than among patients without pCR (24.28% ± 2.34% vs. 11.34% ± 0.60%, respectively, p < 0.0001). The multivariate analysis demonstrated that a high pre-NAC TIL level was an independent risk factor for a higher pCR (odds ratio = 3.92, 95% CI = 2.23-6.90, p < 0.001). Patients with high pre-NAC TIL levels had a better 5-year DFS than those with low pre-NAC TIL levels (84.5% vs. 68.9%, HR = 0.50, 95% CI = 0.31-0.81, p = 0.005). The multivariate analysis showed that pre-NAC TIL (HR = 0.48; 95% CI = 0.29-0.81, p = 0.006) but not post-NAC TIL (HR = 0.89, 95% CI = 0.50-1.59, p = 0.699) was significantly associated with DFS among patients without pCR. Furthermore, patients with low pre- and post-NAC TIL levels had a worse 5-year DFS than those with high pre-NAC TIL levels (HR = 2.09, 95% CI = 1.23-3.56, p = 0.007). CONCLUSIONS: Pre-NAC TIL level can predict pCR and DFS in patients with breast cancer receiving NAC. For patients without pCR, pre-NAC TIL, and TIL category change, but not post-NAC TIL, were significantly associated with DFS.

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FIGURE 1 Distributions of pre‐NAC TILs and associations with pathological response. (A) Distribution of pre‐NAC TILs in all patients and the HR+HER2−, HER2+, and TNBC subgroups; (B) Mean pre‐NAC TIL of patients by molecular subtype; (C) Total pCR rate by 10% increment of pre‐NAC TIL; (D) Mean pre‐NAC TILs among patients with total pCR or non‐pCR; (E) Associations between pre‐NAC TIL and Miller‐Payne grade after NAC; (F) Area under the curve of pre‐NAC TIL for total pCR; (G) Total pCR rate of patients with high versus low pre‐NAC TILs. HER2, human epidermal growth factor receptor 2; HR, hormonal receptor; NAC, neoadjuvant chemotherapy; ns, nonsignificant; pCR, pathological complete response; TILs, tumor‐infiltrating lymphocytes; TNBC, triple‐negative breast cancer. *p < 0.05; **p < 0.01; ***p < 0.001; ****p < 0.0001
FIGURE 1 Distributions of pre‐NAC TILs and associations with pathological response. (A) Distribution of pre‐NAC TILs in all patients and the HR+HER2−, HER2+, and TNBC subgroups; (B) Mean pre‐NAC TIL of patients by molecular subtype; (C) Total pCR rate by 10% increment of pre‐NAC TIL; (D) Mean pre‐NAC TILs among patients with total pCR or non‐pCR; (E) Associations between pre‐NAC TIL and Miller‐Payne grade after NAC; (F) Area under the curve of pre‐NAC TIL for total pCR; (G) Total pCR rate of patients with high versus low pre‐NAC TILs. HER2, human epidermal growth factor receptor 2; HR, hormonal receptor; NAC, neoadjuvant chemotherapy; ns, nonsignificant; pCR, pathological complete response; TILs, tumor‐infiltrating lymphocytes; TNBC, triple‐negative breast cancer. *p < 0.05; **p < 0.01; ***p < 0.001; ****p < 0.0001CC BY · PubMed Central
FIGURE 2 Disease‐free survival and overall survival by pre‐NAC TIL category in the whole population. (A) DFS of all patients; (B) DFS of patients with the HR+HER2− subtype; (C) DFS of patients with the HER2+ subtype; (D) DFS of patients with the TNBC subtype; (E) OS of all patients; (F) OS of patients with the HR+HER2− subtype; (G) OS of patients with the HER2+ subtype; (H) OS of patients with the TNBC subtype. HER2, human epidermal growth factor receptor 2; HR, hormonal receptor; NAC, neoadjuvant chemotherapy; TILs, tumor‐infiltrating lymphocytes; TNBC, triple‐negative breast cancer
FIGURE 2 Disease‐free survival and overall survival by pre‐NAC TIL category in the whole population. (A) DFS of all patients; (B) DFS of patients with the HR+HER2− subtype; (C) DFS of patients with the HER2+ subtype; (D) DFS of patients with the TNBC subtype; (E) OS of all patients; (F) OS of patients with the HR+HER2− subtype; (G) OS of patients with the HER2+ subtype; (H) OS of patients with the TNBC subtype. HER2, human epidermal growth factor receptor 2; HR, hormonal receptor; NAC, neoadjuvant chemotherapy; TILs, tumor‐infiltrating lymphocytes; TNBC, triple‐negative breast cancerCC BY · PubMed Central
FIGURE 3 Distributions of post‐NAC TILs and associations with pathological response and survival among patients with invasive residual breast tumor after NAC. (A) Distribution of post‐NAC TILs in all patients and the HR+HER2−, HER2+, and TNBC subgroups; (B) associations between post‐NAC TIL and Miller‐Payne grade after NAC; (C) disease‐free survival by post‐NAC TIL category; (D) overall survival by post‐NAC TIL category. HER2, human epidermal growth factor receptor 2; HR, hormonal receptor; NAC, neoadjuvant chemotherapy; TILs, tumor‐infiltrating lymphocytes; TNBC, triple‐negative breast cancer
FIGURE 3 Distributions of post‐NAC TILs and associations with pathological response and survival among patients with invasive residual breast tumor after NAC. (A) Distribution of post‐NAC TILs in all patients and the HR+HER2−, HER2+, and TNBC subgroups; (B) associations between post‐NAC TIL and Miller‐Payne grade after NAC; (C) disease‐free survival by post‐NAC TIL category; (D) overall survival by post‐NAC TIL category. HER2, human epidermal growth factor receptor 2; HR, hormonal receptor; NAC, neoadjuvant chemotherapy; TILs, tumor‐infiltrating lymphocytes; TNBC, triple‐negative breast cancerCC BY · PubMed Central
FIGURE 4 Changes in TILs before versus after NAC and associations with survival in patients with invasive residual breast tumors after NAC. (A) Changes in TILs in all patients; (B) changes in TILs in the HR+HER2− subgroup; (C) changes in TILs in the HER2+ subgroup; (D) changes in TILs in the TNBC subgroup; (E) DFS by change in TIL category in all patients; (F) DFS by change in TIL category in the HR+HER2− subgroup; (G) DFS by change in TILs category in the HER2+ subgroup; (H) DFS by change in TIL category in the TNBC subgroup; (I) OS by change in TILs in all patients; (J) distributions of changes in TILs in all patients by molecular subgroup. DFS, disease‐free survival; HER2, human epidermal growth factor receptor 2; HR, hormonal receptor; OS, overall survival; TILs, tumor‐infiltrating lymphocytes; TNBC, triple‐negative breast cancer; NAC, neoadjuvant chemotherapy. *Group A: pre‐NAC TILs > 10% regardless of post‐NAC TILs; Group B: pre‐NAC TILs ≤ 10% and post‐NAC TILs > 10%; Group C: pre‐NAC and post‐NAC TILs ≤ 10%
FIGURE 4 Changes in TILs before versus after NAC and associations with survival in patients with invasive residual breast tumors after NAC. (A) Changes in TILs in all patients; (B) changes in TILs in the HR+HER2− subgroup; (C) changes in TILs in the HER2+ subgroup; (D) changes in TILs in the TNBC subgroup; (E) DFS by change in TIL category in all patients; (F) DFS by change in TIL category in the HR+HER2− subgroup; (G) DFS by change in TILs category in the HER2+ subgroup; (H) DFS by change in TIL category in the TNBC subgroup; (I) OS by change in TILs in all patients; (J) distributions of changes in TILs in all patients by molecular subgroup. DFS, disease‐free survival; HER2, human epidermal growth factor receptor 2; HR, hormonal receptor; OS, overall survival; TILs, tumor‐infiltrating lymphocytes; TNBC, triple‐negative breast cancer; NAC, neoadjuvant chemotherapy. *Group A: pre‐NAC TILs > 10% regardless of post‐NAC TILs; Group B: pre‐NAC TILs ≤ 10% and post‐NAC TILs > 10%; Group C: pre‐NAC and post‐NAC TILs ≤ 10%CC BY · PubMed Central

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Metadata

Authors
Hong, J., Rui, W., Fei, X., Chen, X., & Shen, K.
Affiliations
Shanghai Jiao Tong University (CN)
Corresponding author
  • Chen, Xiaosong
  • Shen, Kunwei
ORCID
Venue
Cancer Medicine
Publisher
Wiley
Published
2021-09-25
Volume
10
Issue
22
Pages
7921-7933
ISSN
2045-7634 (ISSN-L)
DOI
10.1002/cam4.4302
PMC
PMC8607245
OpenAlex
W3200545581
Cited by
24
References
34
Citations by year
2026: 3 · 2025: 6 · 2024: 6 · 2023: 6 · 2022: 2 · 2021: 1
FWCI
0.45
Type
journal article
Language
en
Open access
Licence
Locations
  • Cancer Medicine (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • National Natural Science Foundation of China (81772797, 82072897, 82072937)
  • Shanghai Municipal Education Commission (20172007)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Breast Cancer Treatment Studies
  • Health Sciences › Medicine › Pathology and Forensic Medicine › Breast Lesions and Carcinomas
  • Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › MRI in cancer diagnosis
Keywords
tumor-infiltrating lymphocytes, breast cancer, neoadjuvant chemotherapy, pathological complete response, predictive biomarkers, prognostic factors, disease-free survival, overall survival, tumor immune microenvironment, treatment response prediction, prognostic stratification, triple-negative breast cancer, HER2-positive breast cancer, hormone receptor-positive breast cancer
MeSH terms
Breast Neoplasms, Female, Humans, Middle Aged, Prognosis, Retrospective Studies, Lymphocytes, Tumor-Infiltrating, Disease-Free Survival

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