Histopathological growth patterns and tumor-infiltrating lymphocytes in breast cancer liver metastases.


Journal

NPJ breast cancer
ISSN: 2374-4677
Titre abrégé: NPJ Breast Cancer
Pays: United States
ID NLM: 101674891

Informations de publication

Date de publication:
15 Dec 2023
Historique:
received: 07 03 2023
accepted: 13 11 2023
medline: 16 12 2023
pubmed: 16 12 2023
entrez: 15 12 2023
Statut: epublish

Résumé

Liver is the third most common organ for breast cancer (BC) metastasis. Two main histopathological growth patterns (HGP) exist in liver metastases (LM): desmoplastic and replacement. Although a reduced immunotherapy efficacy is reported in patients with LM, tumor-infiltrating lymphocytes (TIL) have not yet been investigated in BCLM. Here, we evaluate the distribution of the HGP and TIL in BCLM, and their association with clinicopathological variables and survival. We collect samples from surgically resected BCLM (n = 133 patients, 568 H&E sections) and post-mortem derived BCLM (n = 23 patients, 97 H&E sections). HGP is assessed as the proportion of tumor liver interface and categorized as pure-replacement ('pure r-HGP') or any-desmoplastic ('any d-HGP'). We score the TIL according to LM-specific guidelines. Associations with progression-free (PFS) and overall survival (OS) are assessed using Cox regressions. We observe a higher prevalence of 'any d-HGP' (56%) in the surgical samples and a higher prevalence of 'pure r-HGP' (83%) in the post-mortem samples. In the surgical cohort, no evidence of the association between HGP and clinicopathological characteristics is observed except with the laterality of the primary tumor (p value = 0.049) and the systemic preoperative treatment before liver surgery (p value = .039). TIL is less prevalent in 'pure r-HGP' as compared to 'any d-HGP' (p value = 0.001). 'Pure r-HGP' predicts worse PFS (HR: 2.65; CI: (1.45-4.82); p value = 0.001) and OS (HR: 3.10; CI: (1.29-7.46); p value = 0.011) in the multivariable analyses. To conclude, we demonstrate that BCLM with a 'pure r-HGP' is associated with less TIL and with the worse outcome when compared with BCLM with 'any d-HGP'. These findings suggest that HGP could be considered to refine treatment approaches.

Identifiants

pubmed: 38102162
doi: 10.1038/s41523-023-00602-6
pii: 10.1038/s41523-023-00602-6
doi:

Types de publication

Journal Article

Langues

eng

Pagination

100

Subventions

Organisme : Stichting Tegen Kanker (Belgian Foundation Against Cancer)
ID : C/2020/1441
Organisme : Stichting Tegen Kanker (Belgian Foundation Against Cancer)
ID : C/2020/1441
Organisme : Stichting Tegen Kanker (Belgian Foundation Against Cancer)
ID : C/2020/1441

Informations de copyright

© 2023. The Author(s).

Références

Wang, R. et al. The Clinicopathological features and survival outcomes of patients with different metastatic sites in stage IV breast cancer. BMC Cancer 19, 1091 (2019).
Harbeck, N. et al. Breast cancer. Nat. Rev. Dis. Primers 5, 66 (2019).
Bale, R., Putzer, D. & Schullian, P. Local treatment of breast cancer liver metastasis. Cancers 11, 1341 (2019).
Rashid, N. S., Grible, J. M., Clevenger, C. V. & Harrell, J. C. Breast cancer liver metastasis: current and future treatment approaches. 38, 263–277 (2021).
Gulia, S., Khurana, S., Shet, T. & Gupta, S. Case report: radiographically occult intrasinusoidal liver metastases leading to hepatic failure in a case of breast cancer. BMJ Case Rep. 2016, bcr2015214120 (2016).
Allison, K. H., Fligner, C. L. & Parks, W. Tony. Radiographically occult, diffuse intrasinusoidal hepatic metastases from primary breast carcinomas a clinicopathologic study of 3 autopsy cases REPORT OF CASES case 1. Arch. Pathol. Lab. Med. 128, 1418–1423 (1418).
Simone, C., Murphy, M., Shifrin, R., Toro, T. Z. & Reisman, D. Rapid liver enlargement and hepatic failure secondary to radiographic occult tumor invasion: two case reports and review of the literature. J. Med. Case Rep. 6, 402 (2012).
Deodhar, K., Munot, S., Rojekar, A. & Vaideeswar, P. Hepatic diffuse intra-sinusoidal metastases of pulmonary small-cell carcinoma. J. Postgrad. Med. 58, 230 (2012).
doi: 10.4103/0022-3859.101654 pubmed: 23023366
Galjart, B. et al. Angiogenic desmoplastic histopathological growth pattern as a prognostic marker of good outcome in patients with colorectal liver metastases. Angiogenesis 1, 355–368 (2019).
doi: 10.1007/s10456-019-09661-5
Bohlok, A. et al. Association between the histopathological growth patterns of liver metastases and survival after hepatic surgery in breast cancer patients. NPJ Breast Cancer 6, 64 (2020).
Cremolini, C. et al. Differential histopathologic parameters in colorectal cancer liver metastases resected after triplets plus bevacizumab or cetuximab: a pooled analysis of five prospective trials. Br. J. Cancer 118, 955–965 (2018).
Nierop, P. M. H. et al. Salvage treatment for recurrences after first resection of colorectal liver metastases: the impact of histopathological growth patterns. Clin. Exp. Metastasis 36, 109–118 (2019).
doi: 10.1007/s10585-019-09960-7 pubmed: 30843120 pmcid: 6445820
Temido M. J. et al. Prognostic factors after hepatectomy for gastric adenocarcinoma liver metastases: desmoplastic growth pattern as the key to improved overall survival. Cancer Manag Res. 12, 11689–11699 (2020).
Vles, M. J. D. et al. Local tumour control after radiofrequency or microwave ablation for colorectal liver metastases in relation to histopathological growth patterns. HPB 24, 1443–1452 (2022).
doi: 10.1016/j.hpb.2022.01.010 pubmed: 35144863
Barnhill, R. et al. Replacement and desmoplastic histopathological growth patterns: a pilot study of prediction of outcome in patients with uveal melanoma liver metastases. J. Pathol. Clin. Res Oct. 4, 227–240 (2018).
doi: 10.1002/cjp2.105
Latacz, E. et al. Histopathological growth patterns of liver metastasis: updated consensus guidelines for pattern scoring, perspectives and recent mechanistic insights. Br. J. Cancer 127, 988–1013 (2022).
doi: 10.1038/s41416-022-01859-7 pubmed: 35650276 pmcid: 9470557
Salgado, R. et al. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol. 26, 259–2571 (2014).
Van Dam, P. J. et al. International consensus guidelines for scoring the histopathological growth patterns of liver metastasis. Br. J. Cancer 117, 1427–1441 (2017).
doi: 10.1038/bjc.2017.334 pubmed: 28982110 pmcid: 5680474
Wei, S. et al. Radiomics diagnosed histopathological growth pattern in prediction of response and 1-year progression free survival for colorectal liver metastases patients treated with bevacizumab containing chemotherapy. Eur. J. Radiol. 142, 109863 (2021).
Mentha, G. et al. Neoadjuvant chemotherapy and resection of advanced synchronous liver metastases before treatment of the colorectal primary. Br. J. Surg. 96, 95–103 (2006).
doi: 10.1002/bjs.6436
Rubbia-Brandt, L. et al. Importance of histological tumor response assessment in predicting the outcome in patients with colorectal liver metastases treated with neo-adjuvant chemotherapy followed by liver surgery. Ann. Oncol. 18, 299–304 (2007).
doi: 10.1093/annonc/mdl386 pubmed: 17060484
Starmans, M. P. A. et al. Distinguishing pure histopathological growth patterns of colorectal liver metastases on CT using deep learning and radiomics: a pilot study. Clin. Exp. Metastasis 38, 483–494 (2021).
Cheng, J. et al. Prediction of histopathologic growth patterns of colorectal liver metastases with a noninvasive imaging method. Ann. Surg. Oncol. 26, 4587–4598 (2019).
doi: 10.1245/s10434-019-07910-x pubmed: 31605342
Han, Y. et al. Identification of predominant histopathological growth patterns of colorectal liver metastasis by multi-habitat and multi-sequence based radiomics analysis. Front. Oncol. 10, 1363 (2020).
doi: 10.3389/fonc.2020.01363 pubmed: 32923388 pmcid: 7456817

Auteurs

Sophia Leduc (S)

Laboratory for Translational Breast Cancer Research, Department of Oncology, KU Leuven, Leuven, Belgium.

Maxim De Schepper (M)

Laboratory for Translational Breast Cancer Research, Department of Oncology, KU Leuven, Leuven, Belgium.
Department of Pathology, University Hospitals Leuven, Leuven, Belgium.

François Richard (F)

Laboratory for Translational Breast Cancer Research, Department of Oncology, KU Leuven, Leuven, Belgium.

Marion Maetens (M)

Laboratory for Translational Breast Cancer Research, Department of Oncology, KU Leuven, Leuven, Belgium.

Anirudh Pabba (A)

Laboratory for Translational Breast Cancer Research, Department of Oncology, KU Leuven, Leuven, Belgium.

Kristien Borremans (K)

Laboratory for Translational Breast Cancer Research, Department of Oncology, KU Leuven, Leuven, Belgium.
Department of Gynecological Oncology, University Hospitals Leuven, KU Leuven, Leuven, Belgium.

Joris Jaekers (J)

Department of Abdominal Surgery, University Hospitals Leuven, KU Leuven, Leuven, Belgium.

Emily Latacz (E)

Translational Cancer Research Unit, GZA Hospitals & CORE, MIPRO, University of Antwerp, Antwerp, Belgium.

Gitte Zels (G)

Laboratory for Translational Breast Cancer Research, Department of Oncology, KU Leuven, Leuven, Belgium.
Department of Pathology, University Hospitals Leuven, Leuven, Belgium.

Ali Bohlok (A)

Department of Surgical Oncology, Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium.

Karen Van Baelen (K)

Laboratory for Translational Breast Cancer Research, Department of Oncology, KU Leuven, Leuven, Belgium.
Department of Gynecological Oncology, University Hospitals Leuven, KU Leuven, Leuven, Belgium.

Ha Linh Nguyen (HL)

Laboratory for Translational Breast Cancer Research, Department of Oncology, KU Leuven, Leuven, Belgium.

Tatjana Geukens (T)

Laboratory for Translational Breast Cancer Research, Department of Oncology, KU Leuven, Leuven, Belgium.

Luc Dirix (L)

Translational Cancer Research Unit, GZA Hospitals & CORE, MIPRO, University of Antwerp, Antwerp, Belgium.

Denis Larsimont (D)

Department of Anatomopathology, Institut Jules Bordet, Brussels, Belgium.

Sophie Vankerckhove (S)

Department of Surgical Oncology, Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium.

Eva Santos (E)

General Surgery Department, Centro Hospitalar e Universitario de Coimbra, Coimbra, Portugal.

Rui Caetano Oliveira (RC)

General Surgery Department, Centro Hospitalar e Universitario de Coimbra, Coimbra, Portugal.

Kristòf Dede (K)

Department of Surgical Oncology, Uzsoki Hospital, Budapest, Hungary.

Janina Kulka (J)

Department of Pathology, Forensic and Insurance Medicine, Semmelweis University, Budapest, Hungary.

Székely Borbala (S)

Department of Pathology, Forensic and Insurance Medicine, Semmelweis University, Budapest, Hungary.

Ferenc Salamon (F)

Department of Pathology, Forensic and Insurance Medicine, Semmelweis University, Budapest, Hungary.

Lilla Madaras (L)

Department of Pathology, Forensic and Insurance Medicine, Semmelweis University, Budapest, Hungary.
Department of Pathology, Uzsoki Hospital, Budapest, Hungary.

A Marcell Szasz (A)

Division of Oncology, Department of Internal Medicine and Oncology, Semmelweis University, Budapest, Hungary.

Valerio Lucidi (V)

Department of Abdominal Surgery, Erasme Hospital, Université Libre de Bruxelles, Brussels, Belgium.

Yannick Meyer (Y)

Department of Surgical Oncology and Gastrointestinal Surgery, Erasmus MC Cancer Institute, Rotterdam, the Netherlands.

Baki Topal (B)

Department of Abdominal Surgery, University Hospitals Leuven, KU Leuven, Leuven, Belgium.

Cornelis Verhoef (C)

Department of Surgical Oncology and Gastrointestinal Surgery, Erasmus MC Cancer Institute, Rotterdam, the Netherlands.

Jennie Engstrand (J)

Division of Surgery, Department of Clinical Science, Intervention and Technology, Karolinska Institutet at Karolinska University Hospital, Stockholm, Sweden.

Carlos Fernandez Moro (CF)

Department of Biosciences and Nutrition, Karolinska Institute, Huddinge and Karolinska University Hospital, Solna, Sweden.

Marco Gerling (M)

Department of Biosciences and Nutrition, Karolinska Institute, Huddinge and Karolinska University Hospital, Solna, Sweden.

Imane Bachir (I)

Department of Anesthesiology, Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium.

Elia Biganzoli (E)

Unit of Medical Statistics, Biometry and Epidemiology, Department of Biomedical and Clinical Sciences (DIBIC) "L. Sacco" & DSRC, LITA Vialba campus, University of Milan, Milan, Italy.

Vincent Donckier (V)

Department of Surgical Oncology, Institut Jules Bordet, Université Libre de Bruxelles, Brussels, Belgium.

Giuseppe Floris (G)

Department of Pathology, University Hospitals Leuven, Leuven, Belgium.
Department of Imaging and Pathology, Laboratory of Translational Cell & Tissue Research and University Hospitals Leuven, KU Leuven, Leuven, Belgium.

Peter Vermeulen (P)

Translational Cancer Research Unit, GZA Hospitals & CORE, MIPRO, University of Antwerp, Antwerp, Belgium.

Christine Desmedt (C)

Laboratory for Translational Breast Cancer Research, Department of Oncology, KU Leuven, Leuven, Belgium. christine.desmedt@kuleuven.be.

Classifications MeSH