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Caspase Recruitment Domain Containing Protein 9 Suppresses Non-Small Cell Lung Cancer Proliferation and Invasion via Inhibiting MAPK/p38 Pathway
Linyue Pan, Yuting Tan, Bin Wang, Wenjia Qiu, Yulei Yin, Haiyan Ge, Huili Zhu
Cancer Res Treat. 2020;52(3):867-885.   Published online March 11, 2020
DOI: https://doi.org/10.4143/crt.2019.606
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
Caspase recruitment domain containing protein 9 (CARD9) has been demonstrated to be a pro-tumor factor in various cancers. However, our previous study found a significant decrease of CARD9 in malignant pleural effusion compared with benign pleural effusion. So we investigated the role of CARD9 in non-small cell lung cancer (NSCLC) and its working mechanism.
Materials and Methods
Immunohistochemistry, western blot, and quantitative real-time polymerase chain reaction were used to detect the expression of CARD9 in specimens of NSCLC patients. The Cancer Genome Atlas (TCGA) databasewas also used to analyze the expression of CARD9 in NSCLC and its predicting value for prognosis. Immunofluorescence was used for CARD9 cellular location. Cell growth assay, clonal formation assay, wound healing assay, matrigel invasion assay, and flow cytometry were used to test cell proliferation, migration, invasion, apoptosis, and cycle progression of NSCLC cells with CARD9 knockdown or CARD9 overexpression. Co-immunoprecipitation was used to identify the interaction between CARD9 and B-cell lymphoma 10 (BCL10). SB203580 was used to inhibit p38 activation.
Results
CARD9 was decreased in NSCLC tissues compared with normal tissues; low CARD9 expression was associated with poor survival. CARD9 was expressed both in tumor cells and macrophages. Downregulation of CARD9 in NSCLC cells enhanced the abilities of proliferation, invasion and migration via activated MAPK/p38 signaling, while overexpression of CARD9 presented antitumor effects. BCL10 was identified to interact with CARD9.
Conclusion
We demonstrate that CARD9 is an independent prognostic factor in NSCLC patients and inhibits proliferation, migration, and invasion by suppressing MAPK/p38 pathway in NSCLC cells.

Citations

Citations to this article as recorded by  
  • The implication of microbiome in lungs cancer: mechanisms and strategies of cancer growth, diagnosis and therapy
    Yasmin Bano, Abhinav Shrivastava, Piyush Shukla, Anis Ahmad Chaudhary, Salah-Ud-Din Khan, Shahanavaj Khan
    Critical Reviews in Microbiology.2025; 51(1): 128.     CrossRef
  • CARD9 regulates myocardial inflammation, oxidative stress, and vascular dysfunction in hypertensive rats by activating MAPK/p38 pathway in combination with NOD2
    XiangBin Xin, Jing Zhang, YanQin Du, XiaoTing Jang, XinYi Tian, Fu Ma, Fang Chen
    Molecular & Cellular Toxicology.2024;[Epub]     CrossRef
  • Transcriptome Analysis of the Inhibitory Effects of 20(S)-Protopanaxadiol on NCI-H1299 Non-Small Cell Lung Cancer Cells
    Zhongyi Cong, Xinmin Zhang, Zeqi Lv, Jingyuan Jiang, Lei Wang, Jiapeng Li, Jie Wang, Jianjun Zhao
    Molecules.2023; 28(15): 5746.     CrossRef
  • Sericin enhances ammonia detoxification by promotes urea cycle enzyme genes and activates hepatic autophagy in relation to CARD-9/MAPK pathway
    Sumate Ampawong, Napatara Tirawanchai, Tapanee Kanjanapruthipong, Kamonpan Fongsodsri, Khwanchanok Tuentam, Duangnate Isarangkul, Pornanong Aramwit
    Heliyon.2023; 9(11): e21563.     CrossRef
  • Mycobiota and C-Type Lectin Receptors in Cancers: Know thy Neighbors
    Lilong Zhang, Dongqi Chai, Chen Chen, Chunlei Li, Zhendong Qiu, Tianrui Kuang, Mungur Parveena, Keshuai Dong, Jia Yu, Wenhong Deng, Weixing Wang
    Frontiers in Microbiology.2022;[Epub]     CrossRef
  • Alpha1B-adreneroceptor is involved in norepinephrine-induced pulmonary artery smooth muscle cell proliferation via p38 signaling
    Xiaolin Xiao, Ying Zhang, Shuaihu Tian, Xiaoyan Wang, Qianlong Zhang, Lixin Zhang, Xiufeng Yu, Cui Ma, Xiaodong Zheng, Yiying Li, Junting Zhang, Lihui Qu
    European Journal of Pharmacology.2022; 931: 175159.     CrossRef
  • Proteomic analysis provides insights into the function of Polian vesicles in the sea cucumber Apostichopus japonicus post-evisceration
    Jinlin Ji, Zhenhui Wang, Wei Zhu, Qiang Li, Yinan Wang
    Journal of Oceanology and Limnology.2022; 40(5): 2028.     CrossRef
  • CARD9 as a potential therapeutic target in lung cancer
    Ruanmei Sheng, Zhiwen Yang
    Frontiers in Bioscience-Landmark.2021;[Epub]     CrossRef
  • 10,030 View
  • 202 Download
  • 8 Web of Science
  • 8 Crossref
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Comparison of the Distribution Pattern of 21-Gene Recurrence Score between Mucinous Breast Cancer and Infiltrating Ductal Carcinoma in Chinese Population: A Retrospective Single-Center Study
Jiayi Wu, Shuning Ding, Lin Lin, Xiaochun Fei, Caijin Lin, Lisa Andriani, Chihwan Goh, Jiahui Huang, Jin Hong, Weiqi Gao, Siji Zhu, Hui Wang, Ou Huang, Xiaosong Chen, Jianrong He, Yafen Li, Kunwei Shen, Weiguo Chen, Li Zhu
Cancer Res Treat. 2020;52(3):671-679.   Published online January 28, 2020
DOI: https://doi.org/10.4143/crt.2019.387
AbstractAbstract PDFPubReaderePub
Purpose
This retrospective study aimed to evaluate the distribution pattern and prognostic value of 21-gene recurrence score (RS) in Chinese patients with mucinous breast cancer (MC) and compared with infiltrating ductal carcinoma (IDC).
Materials and Methods
Patients diagnosed with MC or IDC from January 2010 to January 2017 were retrospectively recruited. Reverse transcriptase–polymerase chain reaction assay of 21 genes was conducted to calculate the RS. Univariate and multivariate analyses were performed to assess the association between RS and clinicopathological factors. Survival outcomes including disease-free survival (DFS) and overall survival (OS) were estimated by Kaplan-Meier method and compared by log-rank test.
Results
The MC cohort included 128 patients and the IDC cohort included 707 patients. The proportions of patients with a low (RS < 18), intermediate (18-30), or high risk (RS > 30) were 32.0%, 48.4%, and 19.5% in MC cohort, and 26.9%, 46.8% and 26.3% in IDC cohort. The distribution of RS varied significantly according to different Ki-67 index and molecular subtype in both cohorts. Moreover, the receipt of chemotherapy was associated with RS in both cohorts. Among patients with MC, tumor stage was related to the DFS (p=0.040). No significant differences in DFS and OS were found among MC patients in different RS risk groups (OS, p=0.695; DFS, p=0.926).
Conclusion
RS was significantly related to Ki-67 index and molecular subtypes in MC patients, which is similar in IDC patients. However, RS was not able to predict DFS and OS in patients with MC.

Citations

Citations to this article as recorded by  
  • Clinicopathological characteristics and genomic profiling of pure mucinous breast cancer
    Qianyi Lu, Hanxing Zhou, Jianwei Zhang, Kaping Lee, Limin Chen, Ruoxi Hong, Kuikui Jiang, Fei Xu, Wen Xia, Boyang Cao, Jingmin Zhang, Kang Shao, Peng Sun, Shusen Wang
    The Breast.2024; 76: 103760.     CrossRef
  • A clinicopathologic analysis of 70 patients with mucinous breast carcinoma
    Rupali Sood, Karin Miller, Hua-Ling Tsai, Ashley Cimino-Mathews, Roisin M. Connolly
    Current Problems in Cancer: Case Reports.2024; 15: 100304.     CrossRef
  • Clinicopathological features and prognosis of mucinous breast carcinoma with a micropapillary structure
    Beibei Yang, Menglu Shen, Bo Sun, Jing Zhao, Meng Wang
    Thoracic Cancer.2024; 15(36): 2530.     CrossRef
  • Distribution, Chemotherapy Use, and Outcome of the 21-Gene Recurrence Score Between Chinese and White breast Cancer in the United States
    Guan-Qiao Li, Jia Yao, Ping Zhou, Dan-Xia Chen, Chen-Lu Lian, Shi-Ping Yang, Cai-Hong Huang, San-Gang Wu
    Clinical Breast Cancer.2022; 22(3): 279.     CrossRef
  • Association of tumor immune microenvironment profiling and 21-gene recurrence assay in early breast cancer patients
    Yiwei Tong, Jiahui Huang, Weili Ren, Jing Yu, Xu Zhang, Zheng Wang, Jin Hong, Weiqi Gao, Jiayi Wu, Min Ji, Kunwei Shen, Xiaosong Chen
    European Journal of Medical Research.2022;[Epub]     CrossRef
  • Concordance of the 21-gene assay between core needle biopsy and resection specimens in early breast cancer patients
    Peng Qi, Yu Yang, Qian-ming Bai, Tian Xue, Min Ren, Qian-lan Yao, Wen-tao Yang, Xiao-yan Zhou
    Breast Cancer Research and Treatment.2021; 186(2): 327.     CrossRef
  • Oncotype DX 21‑gene test has a low recurrence score in both pure and mixed mucinous breast carcinoma
    Rui Chen, Yun Wang, Taolang Li, Junyuan Lv, Guoli Feng, Na Tan, Jinjing Wang, Xiaoming Cheng
    Oncology Letters.2021;[Epub]     CrossRef
  • 7,648 View
  • 165 Download
  • 7 Web of Science
  • 7 Crossref
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Impact of Prior Cancer History on the Clinical Outcomes in Advanced Breast Cancer: A Propensity Score–Adjusted, Population-Based Study
Caijin Lin, Jiayi Wu, Shuning Ding, Chihwan Goh, Lisa Andriani, Kunwei Shen, Li Zhu
Cancer Res Treat. 2020;52(2):552-562.   Published online November 18, 2019
DOI: https://doi.org/10.4143/crt.2019.210
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
Despite the rapid growing of cancer survivors, prior cancer history is a commonly adopted exclusion criterion. Whether prior cancer will impact the survival of patients with advanced breast cancer (ABC) remains uncertain.
Materials and Methods
Patients with ABC diagnosed between 2004 and 2010 were identified using Surveillance, Epidemiology, and End Results (SEER) database. Timing, stage, and type were used to characterize prior cancer. Multivariable analyses using propensity score–adjusted Cox regression and competing risk regression were conducted to evaluate the prognostic effect of prior cancer on overall survival (OS) and breast cancer-specific survival (BCSS).
Results
A total of 14,176 ABC patients were identified, of whom 10.5% carried a prior cancer history. The most common type of prior cancer was female genital cancer (32.4%); more than half (51.7%) were diagnosed at localized stage; most were diagnosed more than 5 years (42.9%) or less than 1 year (28.3%) prior to the index cancer. In multivariate analyses, patients with prior cancer presented a slightly worse OS (hazard ratio, 1.18; 95% confidence interval [CI], 1.07 to 1.30; p=0.001) but a better BCSS (subdistribution hazard ratio, 0.64; 95% CI, 0.56 to 0.74; p < 0.001). In subset analyses, no survival detriment was observed in patients with prior malignancy from head and neck or endocrine system, at in situ or localized stage, or diagnosed more than 4 years.
Conclusion
Prior cancer provides an inferior OS but a superior BCSS for patients with ABC. It does not affect the survival adversely in some subgroups and these patients should not be excluded from clinical trials.

Citations

Citations to this article as recorded by  
  • Impact of childhood/adolescent cancer history on prognosis in parotid mucoepidermoid carcinoma
    Hefeng Gu, Sunyi Tu, Lan Ma, Kuiwei Su, Yeqing Zhou
    British Journal of Oral and Maxillofacial Surgery.2024; 62(7): 612.     CrossRef
  • Medical history of thyroid cancer does not impair prognosis in non-metastatic breast cancer patients: an analysis study based on SEER database and external cohort
    Shuai Li, Xiaosong Chen, Kunwei Shen
    Frontiers in Oncology.2024;[Epub]     CrossRef
  • Clinical characteristics and prostate-cancer-specific mortality of competitive risk nomogram in the second primary prostate cancer
    Chaojie Xu, Dongchen Pei, Yi Liu, Jianhua Guo, Nan Liu, Qian Wang, Yang Yu, Zhengjun Kang
    Frontiers in Oncology.2023;[Epub]     CrossRef
  • The Impact of a History of Different Other Cancers on the Long-Term Outcomes of Patients with Gallbladder Cancer: A Propensity Score–Adjusted, Population-Based Study
    Jing Wang, Chan Zhang, Dong Yan
    Technology in Cancer Research & Treatment.2023;[Epub]     CrossRef
  • Second primary malignancies in oral tongue cancer: A Surveillance, Epidemiology, and End Result–based analysis evaluating the basic characteristics, survival outcomes, and predictive factors
    Zicheng Xu, Jianxing Wang, Hongzhou Cai, Feng Qi, Qing Zou
    Precision Medical Sciences.2022; 11(1): 4.     CrossRef
  • Better Prognosis and Survival in Esophageal Cancer Survivors After Comorbid Second Primary Malignancies: A SEER Database-Based Study
    Jiayue Ye, Sheng Hu, Wenxiong Zhang, Deyuan Zhang, Yang Zhang, Dongliang Yu, Jinhua Peng, Jianjun Xu, Yiping Wei
    Frontiers in Surgery.2022;[Epub]     CrossRef
  • [Retracted] Effect of Previous Cancer History on Survival of Patients with Different Subtypes of Breast Cancer
    Weixun Lin, Yaokun Chen, Zeqi Ji, Lingzhi Chen, Jinyao Wu, Yexi Chen, Zhiyang Li, Nauman Rahim Khan
    BioMed Research International.2022;[Epub]     CrossRef
  • Association between a prior cancer history and prognosis in adult patients with high‑grade glioma
    Dongjie He, Peiwen Wu, Gaiyan Li, Siying Zhu, Qiming Wang, Qiuju Shao, Hao Chang
    Journal of Clinical Neuroscience.2022; 106: 20.     CrossRef
  • Impact of prior cancer history on survival of patients with gastric cancer
    Li Wen, Kun Yu, Hongjiang Lu, Guansheng Zhong
    European Journal of Surgical Oncology.2021; 47(9): 2286.     CrossRef
  • Effect of prior cancer on survival outcomes for patients with advanced prostate cancer
    Yechen Wu, Xi Chen, Duocheng Qian, Wei Wang, Yiping Zhang, Jinxin Hu, Jun Zhu, Qiang Wu, Tinghu Cao
    BMC Urology.2021;[Epub]     CrossRef
  • Survival of women diagnosed with breast cancer and who have survived a previous cancer
    Sandi L. Pruitt, Hong Zhu, Daniel F. Heitjan, Asal Rahimi, Bhumika Maddineni, Anna Tavakkoli, Ethan A. Halm, David E. Gerber, Danyi Xiong, Caitlin C. Murphy
    Breast Cancer Research and Treatment.2021; 187(3): 853.     CrossRef
  • Trends in the proportion of second or later primaries among all newly diagnosed malignant cancers
    Chelsea Anderson, Deborah K. Mayer, Hazel B. Nichols
    Cancer.2021; 127(15): 2736.     CrossRef
  • Survival analysis of patients with primary breast duct carcinoma and lung adenocarcinoma: a population-based study from SEER
    Fengyuan Lv, Mingliang Cheng, Liang Jiang, Xiaoping Zhao
    Scientific Reports.2021;[Epub]     CrossRef
  • Research on Effectiveness of Prior Cancer on Survival Outcomes for Patients with Nonmetastatic Triple-Negative Breast Cancer: A Competing Risk Analysis and Propensity Score Matching Analysis of the SEER Database
    Heyan Chen, Lutong Yan, Shengyu Pu, Lizhe Zhu, Huimin Zhang, Can Zhou, Raffaele Palmirotta
    Journal of Oncology.2021; 2021: 1.     CrossRef
  • Risk of breast cancer-related death in women with a prior cancer
    Fei Ji, Ci-Qiu Yang, Xiao-Ling Li, Liu-Lu Zhang, Mei Yang, Jie-Qing Li, Hong-Fei Gao, Teng Zhu, Min-Yi Cheng, Wei-Ping Li, Si-Yan Wu, Ai-Ling Zhong, Kun Wang
    Aging.2020; 12(7): 5894.     CrossRef
  • 8,097 View
  • 178 Download
  • 18 Web of Science
  • 15 Crossref
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Changes of Tumor Infiltrating Lymphocytes after Core Needle Biopsy and the Prognostic Implications in Early Stage Breast Cancer: A Retrospective Study
Jiahui Huang, Xiaosong Chen, Xiaochun Fei, Ou Huang, Jiayi Wu, Li Zhu, Jianrong He, Weiguo Chen, Yafen Li, Kunwei Shen
Cancer Res Treat. 2019;51(4):1336-1346.   Published online February 12, 2019
DOI: https://doi.org/10.4143/crt.2018.504
AbstractAbstract PDFPubReaderePub
Purpose
The purpose of this study was to investigate the changes of tumor infiltrating lymphocytes (TILs) between core needle biopsy (CNB) and surgery removed sample (SRS) in early stage breast cancer patients and to identify the correlating factors and prognostic significance of TILs changes.
Materials and Methods
A retrospective study was carried out on 255 patients who received CNB and underwent surgical resection for invasive breast cancer. Stromal TILs levels of CNB and SRS were evaluated respectively. Tumors with ≥50% stromal TILs were defined as lymphocyte-predominant breast cancer (LPBC). Clinicopathological variables were analyzed to determine whether there were factors associated with TILs changes. Log-rank tests and Cox proportional hazards models were used to analyze the influences of TILs and TILs changes on survival.
Results
SRS-TILs (median, 10.0%) were significant higher than CNB-TILs (median, 5.0%; p<0.001). Younger age (<60 years, p=0.016) and long surgery time interval (STI, ≥4 days; p=0.003) were independent factors correlating with higher TILs changes. CNB-LPBC patients showed better breast cancer-free interval (BCFI, p=0.021) than CNB-non-LPBC (CNB-nLPBC) patients. Patients were categorized into four groups according to the LPBC change pattern from CNB to SRS: LPBC→LPBC, LPBC→nLPBC, nLPBC→LPBC, and nLPBC→nLPBC, with estimated 5-year BCFI 100%, 100%, 69.7%, and 86.0% (p=0.016). nLPBC→LPBC pattern was an independent prognostic factor of worse BCFI (hazard ratio, 2.19; 95% confidence interval, 1.06 to 4.53; p=0.035) compared with other patterns.
Conclusion
TILs were significantly higher in SRS than in CNB. Higher TILs changes were associated with younger age and long STI. Changing from nLPBC to LPBC after CNB indicated a worse BCFI, which needs further validation.

Citations

Citations to this article as recorded by  
  • A nomogram to predict the pathological complete response in patients with breast cancer based on the TILs-US score
    Hideo Shigematsu, Kayo Fukui, Akiko Kanou, Mutsumi Fujimoto, Kanako Suzuki, Haruka Ikejiri, Ai Amioka, Emiko Hiraoka, Shinsuke Sasada, Akiko Emi, Koji Arihiro, Morihito Okada
    Japanese Journal of Clinical Oncology.2024; 54(9): 967.     CrossRef
  • Biomarker development for PD-(L)1 axis inhibition: a consensus view from the SITC Biomarkers Committee
    Anne Monette, Sarah Warren, J Carl Barrett, Charlie Garnett-Benson, Kurt A Schalper, Janis M Taube, Brian Topp, Alexandra Snyder
    Journal for ImmunoTherapy of Cancer.2024; 12(7): e009427.     CrossRef
  • Diagnostic performance of TILs–US score and LPBC in biopsy specimens for predicting pathological complete response in patients with breast cancer
    Hideo Shigematsu, Kayo Fukui, Akiko Kanou, Erika Yokoyama, Makiko Tanaka, Mutsumi Fujimoto, Kanako Suzuki, Haruka Ikejiri, Ai Amioka, Emiko Hiraoka, Shinsuke Sasada, Akiko Emi, Tetsuya Nakagiri, Koji Arihiro, Morihito Okada
    International Journal of Clinical Oncology.2024; 29(12): 1860.     CrossRef
  • Stromal grading predicts pathologic complete response and prognosis in triple-negative breast cancer
    Sean M. Hacking, Yihong Wang
    Virchows Archiv.2023; 483(6): 765.     CrossRef
  • Whole slide image features predict pathologic complete response and poor clinical outcomes in triple-negative breast cancer
    Sean M. Hacking, Julie Karam, Kamaljeet Singh, Ece D. Gamsiz Uzun, Arlen Brickman, Evgeny Yakirevich, Ross Taliano, Yihong Wang
    Pathology - Research and Practice.2023; 246: 154476.     CrossRef
  • Tumor infiltrating lymphocytes and radiological picture of the tumor
    Karolina Frankowska, Michał Zarobkiewicz, Izabela Dąbrowska, Agnieszka Bojarska-Junak
    Medical Oncology.2023;[Epub]     CrossRef
  • Core needle biopsies alter the amounts of CCR5, Siglec-15, and PD-L1 positivities in breast carcinoma
    Minna Mutka, Kristiina Joensuu, Marja Heiskala, Mine Eray, Päivi Heikkilä
    Virchows Archiv.2023; 483(2): 215.     CrossRef
  • Clinical characteristics, tumor‐infiltrating lymphocytes, and prognosis in HER2‐low breast cancer: A comparison study with HER2‐zero and HER2‐positive disease
    Yujie Lu, Yiwei Tong, Xiaochun Fei, Xiaosong Chen, Kunwei Shen
    Cancer Medicine.2023; 12(15): 16264.     CrossRef
  • Time interval between breast cancer diagnosis and surgery is associated with disease outcome
    Siji Zhu, Shuai Li, Jiahui Huang, Xiaochun Fei, Kunwei Shen, Xiaosong Chen
    Scientific Reports.2023;[Epub]     CrossRef
  • Evaluation of tumor-infiltrating lymphocytes and mammographic density as predictors of response to neoadjuvant systemic therapy in breast cancer
    Amalia H. Landén, Kian Chin, Anikó Kovács, Erik Holmberg, Eva Molnar, Axel Stenmark Tullberg, Fredrik Wärnberg, Per Karlsson
    Acta Oncologica.2023; 62(12): 1862.     CrossRef
  • Magnetic Resonance Imaging Features Associated with a High and Low Expression of Tumor-Infiltrating Lymphocytes: A Stratified Analysis According to Molecular Subtypes
    Jiejie Zhou, Yi Jin, Haiwei Miao, Shanshan Lu, Xinmiao Liu, Yun He, Huiru Liu, Youfan Zhao, Yang Zhang, Yan-Lin Liu, Zhifang Pan, Jeon-Hor Chen, Meihao Wang, Min-Ying Su
    Cancers.2023; 15(23): 5672.     CrossRef
  • Histopathological Evaluation of Tumor-Infiltrating Lymphocytes (TILs) as Predictive Biomarker for Hormone Receptors Status, Proliferative Activity and Clinical Outcome in Her-2 Positive Breast Cancer
    Giuseppe Angelico, Giuseppe Broggi, Rosario Caltabiano, Angela Santoro, Saveria Spadola, Nicoletta D’Alessandris, Giulia Scaglione, Michele Valente, Damiano Arciuolo, Alejandro Martin Sanchez, Gianluca Franceschini, Riccardo Masetti, Antonino Mulè, Gian F
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  • Pitfalls in assessing stromal tumor infiltrating lymphocytes (sTILs) in breast cancer
    Zuzana Kos, Elvire Roblin, Rim S. Kim, Stefan Michiels, Brandon D. Gallas, Weijie Chen, Koen K. van de Vijver, Shom Goel, Sylvia Adams, Sandra Demaria, Giuseppe Viale, Torsten O. Nielsen, Sunil S. Badve, W. Fraser Symmans, Christos Sotiriou, David L. Rimm
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  • Can Tumor-Infiltrating Lymphocytes (TILs) Be a Predictive Factor for Lymph Nodes Status in Both Early Stage and Locally Advanced Breast Cancer?
    Alexandra Caziuc, Diana Schlanger, Giorgiana Amarinei, George Calin Dindelegan
    Journal of Clinical Medicine.2019; 8(4): 545.     CrossRef
  • 7,141 View
  • 212 Download
  • 16 Web of Science
  • 14 Crossref
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