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Journal of Cancer Research and Clinical Oncology

, Volume 143, Issue 1, pp 161–168 | Cite as

Chemotherapy response and survival of inflammatory breast cancer by hormone receptor- and HER2-defined molecular subtypes approximation: an analysis from the National Cancer Database

  • Jieqiong LiuEmail author
  • Kai Chen
  • Wen Jiang
  • Kai Mao
  • Shunrong Li
  • Min Ji Kim
  • Qiang Liu
  • Lisa K. JacobsEmail author
Original Article – Clinical Oncology

Abstract

Purpose

To study the impact of hormone receptor (HR)- and human epidermal growth factor receptor 2 (HER2)-defined subtypes on survival of inflammatory breast cancer (IBC), and to determine whether sensitivity to neoadjuvant chemotherapy (NAC) varies with subtypes in a large IBC population.

Methods

We analyzed 593 IBCs with known HR/HER2 statuses between 2010 and 2011 from National Cancer Database. We compared pathologic complete response (pCR) rates among four molecular subtypes by Chi-square test. Overall survival (OS) was compared among four subtypes and patients with or without pCR using log-rank test. Multivariate Cox model was performed to identify the impact of molecular subtype and other prognostic factors on OS.

Results

Of the 593 patients included, 231 (39.0 %) patients had HR+/HER2− tumors, 98 (16.5 %) had HR+/HER2+ disease, 112 (18.9 %) were HR-/HER2 + patients, and 152 (25.6 %) had triple-negative subtype. The pCR rates differed significantly by subtype (P < 0.001): HR−/HER2+ showed the highest, and HR+/HER2− exhibited the lowest. Multivariate analysis showed that triple-negative and HR+/HER2− IBCs had significantly worse survival compared with HR+/HER2+ or HR−/HER2+ subtype (P < 0.01 for all comparisons). Additional factors associated with worse OS included more comorbidities, lack or incomplete surgical resection, absence of radiotherapy, lack of hormone therapy, and more advanced stage.

Conclusions

IBC is an aggressive heterogeneous disease with distinct molecular subtypes associated with differential outcomes and sensitivities to NAC. Unlike in noninflammatory breast cancer, in IBC HR + disease was not associated with favorable prognosis. Triple-negative and HR+/HER2− subtypes are independent predictors for suboptimal OS in IBC.

Keywords

Inflammatory breast cancer Chemotherapy response Overall survival Molecular subtype National Cancer Database 

Notes

Acknowledgments

The data used in the study were derived from a de-identified NCDB file. The American College of Surgeons and the Commission on Cancer have not verified and are not responsible for the analytic or statistical methodology used or the conclusions drawn from these data by the investigator. We thank Professor Na You for helpful statistical discussion of this work.

Funding

This study was supported by Grant from the Natural Science Foundation of Guangdong Province (No.2014A030310507); Grant [2013]163 from Key Laboratory of Malignant Tumor Molecular Mechanism and Translational Medicine of Guangzhou Bureau of Science and Information Technology; Grant KLB09001 from the Key Laboratory of Malignant Tumor Gene Regulation and Target Therapy of Guangdong Higher Education Institutes; and Grant from Guangdong Science and Technology Department (2015B050501004).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Data within the NCDB were rendered anonymous, so this study was exempt from reviews by the Johns Hopkins Medicine and Sun Yat-sen Memorial Hospital Institutional Review Board, and no informed consent was needed in this study.

Supplementary material

432_2016_2281_MOESM1_ESM.tif (241 kb)
Fig. S1 Rate of overall survival stratified by pCR (breast and node pCR) status (TIFF 241 kb)

References

  1. Carey LA et al (2006) Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295:2492–2502. doi: 10.1001/jama.295.21.2492 CrossRefPubMedGoogle Scholar
  2. Chen X, Li J, Gray WH, Lehmann BD, Bauer JA, Shyr Y, Pietenpol JA (2012) TNBCtype: a subtyping tool for triple-negative breast cancer. Cancer Inform 11:147–156. doi: 10.4137/CIN.S9983 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Dawood S et al (2011) Differences in survival among women with stage III inflammatory and noninflammatory locally advanced breast cancer appear early: a large population-based study. Cancer 117:1819–1826. doi: 10.1002/cncr.25682 CrossRefPubMedGoogle Scholar
  4. Fritz A, Percy C, Jack A, Shanmugaratnam K, Sobin L, Parkin DM, Whelan S (2000) International classification of diseases for oncology (ICD-O) 3. World Health Organization, GenevaGoogle Scholar
  5. Gonzalez-Angulo AM et al (2009) High risk of recurrence for patients with breast cancer who have human epidermal growth factor receptor 2-positive, node-negative tumors 1 cm or smaller. J Clin Oncol 27:5700–5706. doi: 10.1200/JCO.2009.23.2025 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Hammond ME et al (2010) American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer (unabridged version). Arch Pathol Lab Med 134:e48–e72. doi: 10.1043/1543-2165-134.7.e48 PubMedGoogle Scholar
  7. Hance KW, Anderson WF, Devesa SS, Young HA, Levine PH (2005) Trends in inflammatory breast carcinoma incidence and survival: the surveillance, epidemiology, and end results program at the National Cancer Institute. J Natl Cancer Inst 97:966–975. doi: 10.1093/jnci/dji172 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Jezequel P et al (2015) Gene-expression molecular subtyping of triple-negative breast cancer tumours: importance of immune response. Breast Cancer Res 17:43. doi: 10.1186/s13058-015-0550-y CrossRefPubMedPubMedCentralGoogle Scholar
  9. Kyndi M, Sorensen FB, Knudsen H, Overgaard M, Nielsen HM, Overgaard J (2008) Estrogen receptor, progesterone receptor, HER-2, and response to postmastectomy radiotherapy in high-risk breast cancer: the Danish Breast Cancer Cooperative Group. J Clin Oncol 26:1419–1426. doi: 10.1200/JCO.2007.14.5565 CrossRefPubMedGoogle Scholar
  10. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, Pietenpol JA (2011) Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 121:2750–2767. doi: 10.1172/JCI45014 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Levine PH, Steinhorn SC, Ries LG, Aron JL (1985) Inflammatory breast cancer: the experience of the surveillance, epidemiology, and end results (SEER) program. J Natl Cancer Inst 74:291–297PubMedGoogle Scholar
  12. Li J et al (2011) Triple-negative subtype predicts poor overall survival and high locoregional relapse in inflammatory breast cancer. Oncologist 16:1675–1683. doi: 10.1634/theoncologist.2011-0196 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Logan BR, Wang H, Zhang MJ (2005) Pairwise multiple comparison adjustment in survival analysis. Stat Med 24:2509–2523. doi: 10.1002/sim.2125 CrossRefPubMedGoogle Scholar
  14. Masuda H et al (2014) Long-term treatment efficacy in primary inflammatory breast cancer by hormonal receptor- and HER2-defined subtypes. Ann Oncol 25:384–391. doi: 10.1093/annonc/mdt525 CrossRefPubMedGoogle Scholar
  15. Matro JM, Li T, Cristofanilli M, Hughes ME, Ottesen RA, Weeks JC, Wong YN (2015) Inflammatory breast cancer management in the national comprehensive cancer network: the disease, recurrence pattern, and outcome. Clin Breast Cancer 15:1–7. doi: 10.1016/j.clbc.2014.05.005 CrossRefPubMedGoogle Scholar
  16. Nguyen PL et al (2008) Breast cancer subtype approximated by estrogen receptor, progesterone receptor, and HER-2 is associated with local and distant recurrence after breast-conserving therapy. J Clin Oncol 26:2373–2378. doi: 10.1200/JCO.2007.14.4287 CrossRefPubMedGoogle Scholar
  17. Parker JS et al (2009) Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 27:1160–1167. doi: 10.1200/JCO.2008.18.1370 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Prat A, Perou CM (2011) Deconstructing the molecular portraits of breast cancer. Mol Oncol 5:5–23. doi: 10.1016/j.molonc.2010.11.003 CrossRefPubMedGoogle Scholar
  19. Rueth NM, Lin HY, Bedrosian I, Shaitelman SF, Ueno NT, Shen Y, Babiera G (2014) Underuse of trimodality treatment affects survival for patients with inflammatory breast cancer: an analysis of treatment and survival trends from the National Cancer Database. J Clin Oncol 32:2018–2024. doi: 10.1200/JCO.2014.55.1978 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Schlichting JA, Soliman AS, Schairer C, Schottenfeld D, Merajver SD (2012) Inflammatory and non-inflammatory breast cancer survival by socioeconomic position in the Surveillance, Epidemiology, and End Results database, 1990–2008. Breast Cancer Res Treat 134:1257–1268. doi: 10.1007/s10549-012-2133-2 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Zhou J et al (2014) Distinct outcomes in patients with different molecular subtypes of inflammatory breast cancer. Saudi Med J 35:1324–1330PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Jieqiong Liu
    • 1
    • 2
    Email author
  • Kai Chen
    • 1
    • 2
  • Wen Jiang
    • 3
  • Kai Mao
    • 4
  • Shunrong Li
    • 1
  • Min Ji Kim
    • 5
  • Qiang Liu
    • 1
  • Lisa K. Jacobs
    • 2
    Email author
  1. 1.Guangdong Provincial Key Laboratory of Malignant Tumor Epigenetics and Gene Regulation, Breast Tumor Center, Sun Yat-sen Memorial HospitalSun Yat-sen UniversityGuangzhouChina
  2. 2.Department of SurgeryJohns Hopkins University School of MedicineBaltimoreUSA
  3. 3.Department of Radiation OncologyMD Anderson Cancer CenterHoustonUSA
  4. 4.Guangdong Provincial Key Laboratory of Malignant Tumor Epigenetics and Gene Regulation, Department of General Surgery, Sun Yat-sen Memorial HospitalSun Yat-sen UniversityGuangzhouChina
  5. 5.Department of MedicineBaylor College of MedicineHoustonUSA

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