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Analysis of prognosis in different subtypes of invasive lobular carcinoma using the Japanese National Cancer Database-Breast Cancer Registry

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Abstract

Purpose

Many studies have shown that the prognosis of invasive lobular carcinoma (ILC) is better than that of invasive ductal carcinoma (IDC). However, both disorders exhibit different prognoses according to molecular subtype, and the prognosis of ILC subtypes might depend on their hormone receptor positivity rate. This study clarified the prognosis of ILC and IDC in each subtype and examined the effectiveness of adjuvant chemotherapy (CT) in luminal ILC.

Methods

We planned the analysis using data from the Breast Cancer Registry in Japan. Because it was presumed that there are differences in characteristics between ILC and IDC, we created matched cohorts using exact matching to compare their prognoses. We compared the prognosis of ILC and IDC for each subtype. We also compared the prognosis of luminal ILC between the CT and non-CT groups.

Results

For all subtypes, the disease-free survival (DFS) and overall survival (OS) of ILC were poorer than those of IDC. In the analysis by each subtype, no statistically significant difference was found in DFS and OS in luminal human epidermal growth factor 2 (HER2), HER2, and triple-negative cohorts; however, luminal ILC had significantly poorer DFS and OS than luminal IDC. The CT effects on the prognosis of luminal ILC were greater in more advanced cases.

Conclusion

Luminal ILC had a poorer prognosis than luminal IDC, contributing to the worse prognosis of ILC than that of IDC in the overall cohort. Different therapeutic approaches from luminal IDC are essential for a better prognosis of luminal ILC.

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Data availability

The datasets generated during and/or analyzed during the current study are not publicly available due to ethical restrictions but are available from the corresponding author on reasonable request.

Abbreviations

ILC:

Invasive lobular carcinoma

IDC:

Invasive ductal carcinoma

CT:

Chemotherapy

DFS:

Disease-free survival

OS:

Overall survival

HER2:

Luminal human epidermal growth factor 2

JBCR:

Japanese Breast Cancer Registry

NCD:

National Clinical Database

HR:

Hormone receptor

IHC:

Immunohistochemistry

ER:

Estrogen receptor

PR:

Progesterone receptor

TN:

Triple-negative

CI:

Confidence interval

ET:

Endocrine therapy

SEER:

Surveillance, Epidemiology, and End Results

RS:

Recurrence score

References

  1. Cristofanilli M, Gonzalez-Angulo A, Sneige N et al (2005) Invasive lobular carcinoma classic type: response to primary chemotherapy and survival outcomes. J Clin Oncol 23:41–48. https://doi.org/10.1200/JCO.2005.03.111

    Article  PubMed  Google Scholar 

  2. Van Baelen K, Geukens T, Maetens M et al (2022) Current and future diagnostic and treatment strategies for patients with invasive lobular breast cancer. Ann Oncol 33:769–785. https://doi.org/10.1016/j.annonc.2022.05.006

    Article  CAS  PubMed  Google Scholar 

  3. Mouabbi JA, Hassan A, Lim B, Hortobagyi GN, Tripathy D, Layman RM (2022) Invasive lobular carcinoma: an understudied emergent subtype of breast cancer. Breast Cancer Res Treat 193:253–264. https://doi.org/10.1007/s10549-022-06572-w

    Article  PubMed  Google Scholar 

  4. Pestalozzi BC, Zahrieh D, Mallon E et al (2008) Distinct clinical and prognostic features of infiltrating lobular carcinoma of the breast: combined results of 15 international breast Cancer Study Group clinical trials. J Clin Oncol 26:3006–3014. https://doi.org/10.1200/JCO.2007.14.9336

    Article  PubMed  Google Scholar 

  5. Adachi Y, Ishiguro J, Kotani H et al (2016) Comparison of clinical outcomes between luminal invasive ductal carcinoma and luminal invasive lobular carcinoma. BMC Cancer 16:248. https://doi.org/10.1186/s12885-016-2275-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Sorlie T, Tibshirani R, Parker J et al (2003) Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci U S A 100:8418–8423. https://doi.org/10.1073/pnas.0932692100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Iorfida M, Maiorano E, Orvieto E et al (2012) Invasive lobular breast cancer: subtypes and outcome. Breast Cancer Res Treat 133:713–723. https://doi.org/10.1007/s10549-012-2002-z

    Article  CAS  PubMed  Google Scholar 

  8. Carey LA, Dees EC, Sawyer L et al (2007) The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res 13:2329–2334. https://doi.org/10.1158/1078-0432.CCR-06-1109

    Article  CAS  PubMed  Google Scholar 

  9. Kubo M, Kumamaru H, Isozumi U et al (2020) Annual report of the japanese breast Cancer Society registry for 2016. Breast Cancer 27:511–518. https://doi.org/10.1007/s12282-020-01081-4

    Article  PubMed  Google Scholar 

  10. Hayashi N, Kumamaru H, Isozumi U et al (2020) Annual report of the japanese breast Cancer Registry for 2017. Breast Cancer 27:803–809. https://doi.org/10.1007/s12282-020-01139-3

    Article  PubMed  Google Scholar 

  11. Miyata H, Gotoh M, Hashimoto H et al (2014) Challenges and prospects of a clinical database linked to the board certification system. Surg Today 44:1991–1999. https://doi.org/10.1007/s00595-013-0802-3

    Article  PubMed  Google Scholar 

  12. Greene (2003) AJCC cancer staging manual. Springer, New York

    Google Scholar 

  13. Organization WH (2003) Tumours of the breast and female genital organs. Oxford University Press, Oxford

    Google Scholar 

  14. Yang C, Lei C, Zhang Y et al (2020) Comparison of overall survival between invasive lobular breast carcinoma and invasive ductal breast carcinoma: a propensity score matching study based on SEER Database. Front Oncol 10:590643. https://doi.org/10.3389/fonc.2020.590643

    Article  PubMed  PubMed Central  Google Scholar 

  15. Xiao Y, Ma D, Ruan M et al (2017) Mixed invasive ductal and lobular carcinoma has distinct clinical features and predicts worse prognosis when stratified by estrogen receptor status. Sci Rep 7:10380. https://doi.org/10.1038/s41598-017-10789-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Chen Z, Yang J, Li S et al (2017) Invasive lobular carcinoma of the breast: a special histological type compared with invasive ductal carcinoma. PLoS ONE 12:e0182397. https://doi.org/10.1371/journal.pone.0182397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Lim ST, Yu JH, Park HK, Moon BI, Ko BK, Suh YJ (2014) A comparison of the clinical outcomes of patients with invasive lobular carcinoma and invasive ductal carcinoma of the breast according to molecular subtype in a korean population. World J Surg Oncol 12:56. https://doi.org/10.1186/1477-7819-12-56

    Article  PubMed  PubMed Central  Google Scholar 

  18. Engstrom MJ, Opdahl S, Vatten LJ, Haugen OA, Bofin AM (2015) Invasive lobular breast cancer: the prognostic impact of histopathological grade, E-cadherin and molecular subtypes. Histopathology 66:409–419. https://doi.org/10.1111/his.12572

    Article  PubMed  Google Scholar 

  19. Weiser R, Polychronopoulou E, Hatch SS et al (2022) Adjuvant chemotherapy in patients with invasive lobular carcinoma and use of the 21-gene recurrence score: a National Cancer database analysis. Cancer 128:1738–1747. https://doi.org/10.1002/cncr.34127

    Article  CAS  PubMed  Google Scholar 

  20. Richard F, Majjaj S, Venet D et al (2020) Characterization of stromal tumor-infiltrating lymphocytes and genomic alterations in metastatic lobular breast Cancer. Clin Cancer Res 26:6254–6265. https://doi.org/10.1158/1078-0432.CCR-20-2268

    Article  CAS  PubMed  Google Scholar 

  21. Hanker AB, Sudhan DR, Arteaga CL (2020) Overcoming endocrine resistance in breast Cancer. Cancer Cell 37:496–513. https://doi.org/10.1016/j.ccell.2020.03.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Metzger Filho O, Giobbie-Hurder A, Mallon E et al (2015) Relative effectiveness of Letrozole compared with tamoxifen for patients with lobular carcinoma in the BIG 1–98 trial. J Clin Oncol 33:2772–2779. https://doi.org/10.1200/JCO.2015.60.8133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Strasser-Weippl K, Sudan G, Ramjeesingh R et al (2018) Outcomes in women with invasive ductal or invasive lobular early stage breast cancer treated with anastrozole or exemestane in CCTG (NCIC CTG) MA.27. Eur J Cancer 90:19–25. https://doi.org/10.1016/j.ejca.2017.11.014

    Article  CAS  PubMed  Google Scholar 

  24. Marmor S, Hui JYC, Huang JL et al (2017) Relative effectiveness of adjuvant chemotherapy for invasive lobular compared with invasive ductal carcinoma of the breast. Cancer 123:3015–3021. https://doi.org/10.1002/cncr.30699

    Article  CAS  PubMed  Google Scholar 

  25. de Nonneville A, Jauffret C, Goncalves A et al (2019) Adjuvant chemotherapy in lobular carcinoma of the breast: a clinicopathological score identifies high-risk patient with survival benefit. Breast Cancer Res Treat 175:379–387. https://doi.org/10.1007/s10549-019-05160-9

    Article  CAS  PubMed  Google Scholar 

  26. Trapani D, Gandini S, Corti C et al (2021) Benefit of adjuvant chemotherapy in patients with lobular breast cancer: a systematic review of the literature and metanalysis. Cancer Treat Rev 97:102205. https://doi.org/10.1016/j.ctrv.2021.102205

    Article  CAS  PubMed  Google Scholar 

  27. McCart Reed AE, Kalinowski L, Simpson PT, Lakhani SR (2021) Invasive lobular carcinoma of the breast: the increasing importance of this special subtype. Breast Cancer Res 23:6. https://doi.org/10.1186/s13058-020-01384-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Singh K, He X, Kalife ET, Ehdaivand S, Wang Y, Sung CJ (2018) Relationship of histologic grade and histologic subtype with oncotype dx recurrence score; retrospective review of 863 breast cancer oncotype dx results. Breast Cancer Res Treat 168:29–34. https://doi.org/10.1007/s10549-017-4619-4

    Article  CAS  PubMed  Google Scholar 

  29. Kizy S, Huang JL, Marmor S, Tuttle TM, Hui JYC (2017) Impact of the 21-gene recurrence score on outcome in patients with invasive lobular carcinoma of the breast. Breast Cancer Res Treat 165:757–763. https://doi.org/10.1007/s10549-017-4355-9

    Article  PubMed  Google Scholar 

  30. Metzger O, Cardoso F, Poncet C et al (2020) Clinical utility of MammaPrint testing in Invasive Lobular Carcinoma: results from the MINDACT phase III trial. Eur J Cancer 138:S5–S6. https://doi.org/10.1016/S0959-8049(20)30542-6

    Article  Google Scholar 

  31. Christgen M, Gluz O, Harbeck N et al (2020) Differential impact of prognostic parameters in hormone receptor-positive lobular breast cancer. Cancer 126:4847–4858. https://doi.org/10.1002/cncr.33104

    Article  CAS  PubMed  Google Scholar 

  32. Rakha EA, Reis-Filho JS, Baehner F et al (2010) Breast cancer prognostic classification in the molecular era: the role of histological grade. Breast Cancer Res 12:207. https://doi.org/10.1186/bcr2607

    Article  PubMed  PubMed Central  Google Scholar 

  33. Oesterreich S, Nasrazadani A, Zou J et al (2022) Clinicopathological features and outcomes comparing patients with invasive ductal and lobular breast Cancer. J Natl Cancer Inst 114:1511–1522. https://doi.org/10.1093/jnci/djac157

    Article  CAS  PubMed  Google Scholar 

  34. Wilson IB, Cleary PD (1995) Linking clinical variables with health-related quality of life. A conceptual model of patient outcomes. JAMA 273:59–65

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank the JBCS staff and the National Clinical Database Office staff for their support in this study. YA would like to thank Mitsuo Terada and Hiroji Iwata at Aichi Cancer Center for their support in the application of this research.

Funding

This work was supported by the Japanese Breast Cancer Society.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by YA, SA, HK, NK, YS, NN, HJ, SS and MT. The first draft of the manuscript was written by YA, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yayoi Adachi.

Ethics declarations

Competing interests

HK reports received consultation fees from Mitsubishi-Tanabe Pharma Corporation and EPS Corporation and speaker fees from Chugai Pharmaceutical Co., Ltd. and Johnson and Johnson KK. HK and NK are affiliated with the Department of Health Quality Assessment at the University of Tokyo, a social collaboration department supported by the National Clinical Database, Johnson and Johnson K.K., Nipro Corporation, and Intuitive Surgical Sàrl. NN received honoraria from Astra Zeneca, Chugai, Daiichi Sankyo, Pfizer, Eli Lilly and MSD; and research funding from Chugai, Daiichi Sankyo, Pfizer, Eisai, Mochida and Novartis. SS received honoraria from Astra Zeneca, Chugai, Daiichi Sankyo, Eisai, Eli Lilly, Kyowa Kirin, MSD, Ono, Pfizer, Taiho and Takeda; and research funding from Astra Zeneca, Chugai, Daiichi Sankyo, MSD and Taiho. MT reports received honoraria from Chugai, Takeda, Pfizer, Kyowa-Kirin, Taiho, Eisai, Daiichi-Sankyo, AstraZeneca, Eli Lilly and companies, MSD, Exact Science, Novartis, Shimadzu, Yakult, Nippon Kayaku, Devicore Medical Japan, and Sysmex; and research funding from Chugai, Takeda, Pfizer, Taiho, JBCRG assoc., KBCRN assoc., Eisai, Eli Lilly, Daiichi-Sankyo, AstraZeneca, Astellas, Shimadzu, Yakult, Nippon Kayaku, AFI technology, Luxonus, Shionogi, GL Science, and Sanwa Shurui. YA, SA, NK, YS, HJ, and MT have no relevant financial or non-financial interests to disclose.

Ethics approval

This study was performed in accordance with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Aichi Cancer Center (5.8.2019/No.2019-1-042).

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Adachi, Y., Asaga, S., Kumamaru, H. et al. Analysis of prognosis in different subtypes of invasive lobular carcinoma using the Japanese National Cancer Database-Breast Cancer Registry. Breast Cancer Res Treat 201, 397–408 (2023). https://doi.org/10.1007/s10549-023-07022-x

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