DOI QR코드

DOI QR Code

Prognostic Significance of a Complete Response on Breast MRI in Patients Who Received Neoadjuvant Chemotherapy According to the Molecular Subtype

  • Ko, Eun Sook (Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Han, Heon (Department of Radiology, Kangwon National University Hospital) ;
  • Han, Boo-Kyung (Department of Radiology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Kim, Sun Mi (Department of Radiology, Seoul National University Bundang Hospital) ;
  • Kim, Rock Bum (Department of Preventive Medicine, Dong-A University School of Medicine) ;
  • Lee, Gyeong-Won (Division of Oncology-Hematology, Department of Internal Medicine, Gyeongsang National University School of Medicine) ;
  • Park, Yeon Hee (Division of Hematology/Oncology, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Nam, Seok Jin (Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine)
  • Received : 2014.10.15
  • Accepted : 2015.06.05
  • Published : 2015.09.01

Abstract

Objective: To evaluate the relationship between response categories assessed by magnetic resonance imaging (MRI) or pathology and survival outcomes, and to determine whether there are prognostic differences among molecular subtypes. Materials and Methods: We evaluated 174 patients with biopsy-confirmed invasive breast cancer who had undergone MRI before and after neoadjuvant chemotherapy, but before surgery. Pathology findings were classified as a pathologic complete response (pCR) or a non-pCR, and MRI findings were designated as a radiologic CR (rCR) or a non-rCR. We evaluated overall and subtype-specific associations between clinicopathological factors including the assessment categories and recurrence, using the Cox proportional hazards model. Results: There were 41 recurrences (9 locoregional and 32 distant recurrences). There were statistically significant differences in recurrence outcomes between patients who achieved a radiologic or a pCR and patients who did not achieve a radiologic or a pCR (recurrence hazard ratio, 11.02; p = 0.018 and recurrence hazard ratio, 3.93; p = 0.022, respectively). Kaplan-Meier curves for recurrence-free survival showed that triple-negative breast cancer was the only subtype that showed significantly better outcomes in patients who achieved a CR compared to patients who did not achieve a CR by both radiologic and pathologic assessments (p = 0.004 and 0.001, respectively). A multivariate analysis found that patients who achieved a rCR and a pCR did not display significantly different recurrence outcomes (recurrence hazard ratio, 2.02; p = 0.505 and recurrence hazard ratio, 1.12; p = 0.869, respectively). Conclusion: Outcomes of patients who achieved a rCR were similar to those of patients who achieved a pCR. To evaluate survival difference according to molecular subtypes, a larger study is needed.

Keywords

References

  1. Gralow JR, Burstein HJ, Wood W, Hortobagyi GN, Gianni L, von Minckwitz G, et al. Preoperative therapy in invasive breast cancer: pathologic assessment and systemic therapy issues in operable disease. J Clin Oncol 2008;26:814-819 https://doi.org/10.1200/JCO.2007.15.3510
  2. Rastogi P, Anderson SJ, Bear HD, Geyer CE, Kahlenberg MS, Robidoux A, et al. Preoperative chemotherapy: updates of National Surgical Adjuvant Breast and Bowel Project Protocols B-18 and B-27. J Clin Oncol 2008;26:778-785 https://doi.org/10.1200/JCO.2007.15.0235
  3. van der Hage JA, van de Velde CJ, Julien JP, Tubiana-Hulin M, Vandervelden C, Duchateau L. Preoperative chemotherapy in primary operable breast cancer: results from the European Organization for Research and Treatment of Cancer trial 10902. J Clin Oncol 2001;19:4224-4237 https://doi.org/10.1200/JCO.2001.19.22.4224
  4. Buchholz TA, Lehman CD, Harris JR, Pockaj BA, Khouri N, Hylton NF, et al. Statement of the science concerning locoregional treatments after preoperative chemotherapy for breast cancer: a National Cancer Institute conference. J Clin Oncol 2008;26:791-797 https://doi.org/10.1200/JCO.2007.15.0326
  5. von Minckwitz G, Blohmer JU, Costa SD, Denkert C, Eidtmann H, Eiermann W, et al. Response-guided neoadjuvant chemotherapy for breast cancer. J Clin Oncol 2013;31:3623-3630 https://doi.org/10.1200/JCO.2012.45.0940
  6. Cameron DA, Anderson ED, Levack P, Hawkins RA, Anderson TJ, Leonard RC, et al. Primary systemic therapy for operable breast cancer--10-year survival data after chemotherapy and hormone therapy. Br J Cancer 1997;76:1099-1105 https://doi.org/10.1038/bjc.1997.514
  7. Liedtke C, Mazouni C, Hess KR, André F, Tordai A, Mejia JA, et al. Response to neoadjuvant therapy and long-term survival in patients with triple-negative breast cancer. J Clin Oncol 2008;26:1275-1281 https://doi.org/10.1200/JCO.2007.14.4147
  8. Abraham DC, Jones RC, Jones SE, Cheek JH, Peters GN, Knox SM, et al. Evaluation of neoadjuvant chemotherapeutic response of locally advanced breast cancer by magnetic resonance imaging. Cancer 1996;78:91-100 https://doi.org/10.1002/(SICI)1097-0142(19960701)78:1<91::AID-CNCR14>3.0.CO;2-2
  9. Balu-Maestro C, Chapellier C, Bleuse A, Chanalet I, Chauvel C, Largillier R. Imaging in evaluation of response to neoadjuvant breast cancer treatment benefits of MRI. Breast Cancer Res Treat 2002;72:145-152 https://doi.org/10.1023/A:1014856713942
  10. Weatherall PT, Evans GF, Metzger GJ, Saborrian MH, Leitch AM. MRI vs. histologic measurement of breast cancer following chemotherapy: comparison with x-ray mammography and palpation. J Magn Reson Imaging 2001;13:868-875 https://doi.org/10.1002/jmri.1124
  11. Rieber A, Brambs HJ, Gabelmann A, Heilmann V, Kreienberg R, Kuhn T. Breast MRI for monitoring response of primary breast cancer to neo-adjuvant chemotherapy. Eur Radiol 2002;12:1711-1719 https://doi.org/10.1007/s00330-001-1233-x
  12. Carey LA, Dees EC, Sawyer L, Gatti L, Moore DT, Collichio F, et al. The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res 2007;13:2329-2334 https://doi.org/10.1158/1078-0432.CCR-06-1109
  13. Rouzier R, Perou CM, Symmans WF, Ibrahim N, Cristofanilli M, Anderson K, et al. Breast cancer molecular subtypes respond differently to preoperative chemotherapy. Clin Cancer Res 2005;11:5678-5685 https://doi.org/10.1158/1078-0432.CCR-04-2421
  14. Jones RL, Lakhani SR, Ring AE, Ashley S, Walsh G, Smith IE. Pathological complete response and residual DCIS following neoadjuvant chemotherapy for breast carcinoma. Br J Cancer 2006;94:358-362 https://doi.org/10.1038/sj.bjc.6602950
  15. Park YJ, Youk JH, Son EJ, Gweon HM, Kim JA. Comparison of hormonal receptor and HER2 status between ultrasoundguided 14-gauge core needle biopsy and surgery in breast cancer patients. Ultrasonography 2014;33:206-215 https://doi.org/10.14366/usg.14014
  16. Regan MM, Viale G, Mastropasqua MG, Maiorano E, Golouh R, Carbone A, et al. Re-evaluating adjuvant breast cancer trials:assessing hormone receptor status by immunohistochemical versus extraction assays. J Natl Cancer Inst 2006;98:1571-1581 https://doi.org/10.1093/jnci/djj415
  17. Hudis CA, Barlow WE, Costantino JP, Gray RJ, Pritchard KI, Chapman JA, et al. Proposal for standardized definitions for efficacy end points in adjuvant breast cancer trials: the STEEP system. J Clin Oncol 2007;25:2127-2132 https://doi.org/10.1200/JCO.2006.10.3523
  18. Chaturvedi S, McLaren C, Schofield AC, Ogston KN, Sarkar TK, Hutcheon AW, et al. Patterns of local and distant disease relapse in patients with breast cancer treated with primary chemotherapy: do patients with a complete pathological response differ from those with residual tumour in the breast? Breast Cancer Res Treat 2005;93:151-158 https://doi.org/10.1007/s10549-005-4615-y
  19. von Minckwitz G, Untch M, Blohmer JU, Costa SD, Eidtmann H, Fasching PA, et al. Definition and impact of pathologic complete response on prognosis after neoadjuvant chemotherapy in various intrinsic breast cancer subtypes. J Clin Oncol 2012;30:1796-1804 https://doi.org/10.1200/JCO.2011.38.8595
  20. von Minckwitz G, Untch M, Loibl S. Update on neoadjuvant/ preoperative therapy of breast cancer: experiences from the German Breast Group. Curr Opin Obstet Gynecol 2013;25:66-73 https://doi.org/10.1097/GCO.0b013e32835c0889
  21. von Minckwitz G, Untch M, Nüesch E, Loibl S, Kaufmann M, Kümmel S, et al. Impact of treatment characteristics on response of different breast cancer phenotypes: pooled analysis of the German neo-adjuvant chemotherapy trials. Breast Cancer Res Treat 2011;125:145-156 https://doi.org/10.1007/s10549-010-1228-x
  22. Bear HD, Anderson S, Smith RE, Geyer CE Jr, Mamounas EP, Fisher B, et al. Sequential preoperative or postoperative docetaxel added to preoperative doxorubicin plus cyclophosphamide for operable breast cancer: National Surgical Adjuvant Breast and Bowel Project Protocol B-27. J Clin Oncol 2006;24:2019-2027 https://doi.org/10.1200/JCO.2005.04.1665
  23. Cortazar P, Zhang L, Untch M, Mehta K, Costantino JP, Wolmark N, et al. Pathological complete response and longterm clinical benefit in breast cancer: the CTNeoBC pooled analysis. Lancet 2014;384:164-172 https://doi.org/10.1016/S0140-6736(13)62422-8
  24. Yi A, Cho N, Im SA, Chang JM, Kim SJ, Moon HG, et al. Survival outcomes of breast cancer patients who receive neoadjuvant chemotherapy: association with dynamic contrast-enhanced MR imaging with computer-aided evaluation. Radiology 2013;268:662-672 https://doi.org/10.1148/radiol.13121801
  25. Esserman LJ, Berry DA, DeMichele A, Carey L, Davis SE, Buxton M, et al. Pathologic complete response predicts recurrencefree survival more effectively by cancer subset: results from the I-SPY 1 TRIAL--CALGB 150007/150012, ACRIN 6657. J Clin Oncol 2012;30:3242-3249 https://doi.org/10.1200/JCO.2011.39.2779
  26. Berry DA, Cirrincione C, Henderson IC, Citron ML, Budman DR, Goldstein LJ, et al. Estrogen-receptor status and outcomes of modern chemotherapy for patients with node-positive breast cancer. JAMA 2006;295:1658-1667 https://doi.org/10.1001/jama.295.14.1658
  27. Hayes DF, Thor AD, Dressler LG, Weaver D, Edgerton S, Cowan D, et al. HER2 and response to paclitaxel in node-positive breast cancer. N Engl J Med 2007;357:1496-1506 https://doi.org/10.1056/NEJMoa071167
  28. Ko ES, Han BK, Kim RB, Ko EY, Shin JH, Hahn SY, et al. Analysis of factors that influence the accuracy of magnetic resonance imaging for predicting response after neoadjuvant chemotherapy in locally advanced breast cancer. Ann Surg Oncol 2013;20:2562-2568 https://doi.org/10.1245/s10434-013-2925-6
  29. Knauer M, Mook S, Rutgers EJ, Bender RA, Hauptmann M, van de Vijver MJ, et al. The predictive value of the 70-gene signature for adjuvant chemotherapy in early breast cancer. Breast Cancer Res Treat 2010;120:655-661 https://doi.org/10.1007/s10549-010-0814-2

Cited by

  1. MRI predicts pathologic complete response in HER2-positive breast cancer after neoadjuvant chemotherapy vol.164, pp.1, 2015, https://doi.org/10.1007/s10549-017-4254-0
  2. Accuracy of axillary ultrasound after different neoadjuvant chemotherapy cycles in breast cancer patients vol.8, pp.22, 2017, https://doi.org/10.18632/oncotarget.13313
  3. Estimation of T2* Relaxation Time of Breast Cancer: Correlation with Clinical, Imaging and Pathological Features vol.18, pp.1, 2015, https://doi.org/10.3348/kjr.2017.18.1.238
  4. Selection and Reporting of Statistical Methods to Assess Reliability of a Diagnostic Test: Conformity to Recommended Methods in a Peer-Reviewed Journal vol.18, pp.6, 2017, https://doi.org/10.3348/kjr.2017.18.6.888
  5. Early Prediction of Response to Neoadjuvant Chemotherapy Using Dynamic Contrast-Enhanced MRI and Ultrasound in Breast Cancer vol.19, pp.4, 2015, https://doi.org/10.3348/kjr.2018.19.4.682
  6. Higher underestimation of tumour size post-neoadjuvant chemotherapy with breast magnetic resonance imaging (MRI)-A concordance comparison cohort analysis vol.14, pp.10, 2015, https://doi.org/10.1371/journal.pone.0222917
  7. Radiologic complete response (rCR) in contrast-enhanced magnetic resonance imaging (CE-MRI) after neoadjuvant chemotherapy for early breast cancer predicts recurrence-free survival but not pathologic vol.21, pp.None, 2019, https://doi.org/10.1186/s13058-018-1091-y
  8. Pathologic Complete Response after Neoadjuvant Chemotherapy and Impact on Breast Cancer Recurrence and Survival: A Comprehensive Meta-analysis vol.26, pp.12, 2015, https://doi.org/10.1158/1078-0432.ccr-19-3492
  9. Pathologic Complete Response and Its Impact on Breast Cancer Recurrence and Patient’s Survival after Neoadjuvant Therapy: A Comprehensive Meta-Analysis vol.2021, pp.None, 2015, https://doi.org/10.1155/2021/7545091