Top

Published in:

Open Access 01-12-2016 | Research article

Prognostic impact of AJCC response criteria for neoadjuvant chemotherapy in stage II/III breast cancer patients: breast cancer subtype analyses

Authors: Yaewon Yang, Seock-Ah Im, Bhumsuk Keam, Kyung‑Hun Lee, Tae‑Yong Kim, Koung Jin Suh, Han Suk Ryu, Hyeong-Gon Moon, Sae‑Won Han, Do‑Youn Oh, Wonshik Han, Tae‑You Kim, In Ae Park, Dong-Young Noh

Published in: BMC Cancer | Issue 1/2016

Abstract

Background

Neoadjuvant chemotherapy (NAC) is a standard treatment for stage II/III breast cancer patients, and response to NAC is a useful prognostic marker. Since its introduction, 6–8 cycles of NAC has become the standard regimen to improve the outcome of these patients. The purpose of this study is to evaluate the prognostic impact of the American Joint Committee on Cancer (AJCC) response criteria and this tool’s usefulness in four different breast cancer subtypes.

Methods

We conducted a retrospective cohort study of clinical stage II/III breast cancer patients who received NAC of more than 6 cycles. Response after NAC and the clinicopathological factors were reviewed. AJCC response criteria for NAC were adopted from the AJCC Manual, 7th edition: complete response (CR), partial response (PR), and no response (NR).

Results

A total of 183 patients were enrolled; 22 (12.0 %), 123 (67.2 %), and 38 (20.8 %) patients showed CR, PR, and NR, respectively. The AJCC response was significantly associated with relapse-free survival (RFS) (P < 0.001), whereas pathologic CR (pCR), the current gold standard for response evaluation for NAC, was not (P = 0.140). AJCC response was a significant prognostic factor for RFS in all four breast cancer subtypes, namely luminal A (P = 0.006), luminal B (P = 0.001), HER-2 enriched (P = 0.039), and triple-negative breast cancer (P = 0.035).

Conclusions

The AJCC response criteria represent a simple and easily reproducible tool for response evaluation of NAC patients and a useful clinical prognostic marker for RFS. These criteria also have a prognostic impact in all four breast cancer subtypes, including luminal A in which pCR has a limited role.

Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86. doi:10.1002/ijc.29210.CrossRefPubMed

Jung KW, Won YJ, Kong HJ, Oh CM, Lee DH, Lee JS. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2011. Cancer Res Treat. 2014;46(2):109–23. doi:10.4143/crt.2014.46.2.109.CrossRefPubMedPubMedCentral

Korean Breast Cancer Society. Breast cancer facts and figures. 2013. http://www.kbcs.or.kr/journal/file/2013_Breast_Cancer_Facts_and_Figures_updated.pdf. Accessed 16 Oct 2013.

Kaufmann M. Recommendations from an International Expert Panel on the use of neoadjuvant (Primary) systemic treatment of operable breast cancer: an update. J Clin Oncol. 2006;24(12):1940–9. doi:10.1200/jco.2005.02.6187.CrossRefPubMed

Bear HD, Anderson S, Smith RE, Geyer Jr CE, 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(13):2019–27. doi:10.1200/jco.2005.04.1665.CrossRefPubMed

Bonadonna G, Valagussa P, Brambilla C, Ferrari L, Moliterni A, Terenziani M, et al. Primary chemotherapy in operable breast cancer: eight-year experience at the Milan Cancer Institute. J Clin Oncol. 1998;16(1):93–100.CrossRefPubMed

Fisher B, Brown A, Mamounas E, Wieand S, Robidoux A, Margolese RG, et al. Effect of preoperative chemotherapy on local-regional disease in women with operable breast cancer: findings from National Surgical Adjuvant Breast and Bowel Project B-18. J Clin Oncol. 1997;15(7):2483–93.CrossRefPubMed

Cortazar P, Zhang L, Untch M, Mehta K, Costantino JP, Wolmark N, et al. Pathological complete response and long-term clinical benefit in breast cancer: the CTNeoBC pooled analysis. Lancet. 2014;384(9938):164–72. doi:10.1016/s0140-6736(13)62422-8.CrossRefPubMed

Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17(6):1471–4. doi:10.1245/s10434-010-0985-4.CrossRefPubMed

10.

Keam B, Im S-A, Lim Y, Han S-W, Moon H-G, Oh D-Y, et al. Clinical usefulness of AJCC response criteria for neoadjuvant chemotherapy in breast cancer. Ann Surg Oncol. 2013;20(7):2242–9. doi:10.1245/s10434-012-2756-x.CrossRefPubMed

11.

Smith IC, Heys SD, Hutcheon AW, Miller ID, Payne S, Gilbert FJ, et al. Neoadjuvant chemotherapy in breast cancer: significantly enhanced response with docetaxel. J Clin Oncol. 2002;20(6):1456–66.CrossRefPubMed

12.

von Minckwitz G, Kummel S, Vogel P, Hanusch C, Eidtmann H, Hilfrich J, et al. Intensified neoadjuvant chemotherapy in early-responding breast cancer: phase III randomized GeparTrio study. J Natl Cancer Inst. 2008;100(8):552–62. doi:10.1093/jnci/djn089.CrossRef

13.

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(15):1796–804. doi:10.1200/jco.2011.38.8595.CrossRef

14.

Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009;45(2):228–47. doi:10.1016/j.ejca.2008.10.026.CrossRefPubMed

15.

Loprinzi CL, Thome SD. Understanding the utility of adjuvant systemic therapy for primary breast cancer. J Clin Oncol. 2001;19(4):972–9.CrossRefPubMed

16.

Overgaard M, Hansen PS, Overgaard J, Rose C, Andersson M, Bach F, et al. Postoperative radiotherapy in high-risk premenopausal women with breast cancer who receive adjuvant chemotherapy. Danish Breast Cancer Cooperative Group 82b Trial. N Engl J Med. 1997;337(14):949–55. doi:10.1056/nejm199710023371401.CrossRefPubMed

17.

Moja L, Tagliabue L, Balduzzi S, Parmelli E, Pistotti V, Guarneri V, et al. Trastuzumab containing regimens for early breast cancer. Cochrane Database Syst Rev. 2012;4:Cd006243. doi:10.1002/14651858.CD006243.pub2.

18.

Romond EH, Perez EA, Bryant J, Suman VJ, Geyer Jr CE, Davidson NE, et al. Trastuzumab plus adjuvant chemotherapy for operable HER2-positive breast cancer. N Engl J Med. 2005;353(16):1673–84. doi:10.1056/NEJMoa052122.CrossRefPubMed

19.

EBCTCG. Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet. 2005;365(9472):1687–717. doi:10.1016/s0140-6736(05)66544-0.CrossRef

20.

Burger HG, Dudley EC, Robertson DM, Dennerstein L. Hormonal changes in the menopause transition. Recent Prog Horm Res. 2002;57:257–75.CrossRefPubMed

21.

Jung SY, Han W, Lee JW, Ko E, Kim E, Yu JH, et al. Ki-67 expression gives additional prognostic information on St. Gallen 2007 and Adjuvant! Online risk categories in early breast cancer. Ann Surg Oncol. 2009;16(5):1112–21. doi:10.1245/s10434-009-0334-7.CrossRefPubMed

22.

Keam B, Im SA, Kim HJ, Oh DY, Kim JH, Lee SH, et al. Prognostic impact of clinicopathologic parameters in stage II/III breast cancer treated with neoadjuvant docetaxel and doxorubicin chemotherapy: paradoxical features of the triple negative breast cancer. BMC Cancer. 2007;7:203. doi:10.1186/1471-2407-7-203.CrossRefPubMedPubMedCentral

23.

Keam B, Im S-A, Lee K-H, Han S-W, Oh D-Y, Kim J, et al. Ki-67 can be used for further classification of triple negative breast cancer into two subtypes with different response and prognosis. Breast Cancer Res. 2011;13(2):R22. doi:10.1186/bcr2834.CrossRefPubMedPubMedCentral

24.

Lee KH, Im SA, Oh DY, Lee SH, Chie EK, Han W, et al. Prognostic significance of bcl-2 expression in stage III breast cancer patients who had received doxorubicin and cyclophosphamide followed by paclitaxel as adjuvant chemotherapy. BMC Cancer. 2007;7:63. doi:10.1186/1471-2407-7-63.CrossRefPubMedPubMedCentral

25.

Hammond ME, Hayes DF, Dowsett M, Allred DC, Hagerty KL, Badve S, et al. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. J Clin Oncol. 2010;28(16):2784–95. doi:10.1200/JCO.2009.25.6529.CrossRefPubMedPubMedCentral

26.

Wolff AC, Hammond ME, Schwartz JN, Hagerty KL, Allred DC, Cote RJ, et al. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for human epidermal growth factor receptor 2 testing in breast cancer. J Clin Oncol. 2007;25(1):118–45. doi:10.1200/jco.2006.09.2775.CrossRefPubMed

27.

Yaziji H, Goldstein LC, Barry TS, Werling R, Hwang H, Ellis GK, et al. HER-2 testing in breast cancer using parallel tissue-based methods. JAMA. 2004;291(16):1972–7. doi:10.1001/jama.291.16.1972.CrossRefPubMed

28.

Kim T, Han W, Kim MK, Lee JW, Kim J, Ahn SK, et al. Predictive significance of p53, Ki-67, and Bcl-2 expression for pathologic complete response after neoadjuvant chemotherapy for triple-negative breast cancer. J Breast Cancer. 2015;18(1):16–21. doi:10.4048/jbc.2015.18.1.16.CrossRefPubMedPubMedCentral

29.

Cheang MC, Chia SK, Voduc D, Gao D, Leung S, Snider J, et al. Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. J Natl Cancer Inst. 2009;101(10):736–50. doi:10.1093/jnci/djp082.CrossRefPubMedPubMedCentral

30.

Goldhirsch A, Wood WC, Coates AS, Gelber RD, Thurlimann B, Senn HJ. Strategies for subtypes--dealing with the diversity of breast cancer: highlights of the St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann Oncol. 2011;22(8):1736–47. doi:10.1093/annonc/mdr304.CrossRefPubMedPubMedCentral

31.

Hammond ME. ASCO-CAP guidelines for breast predictive factor testing: an update. Appl Immunohistochem Mol Morphol. 2011;19(6):499–500. doi:10.1097/PAI.0b013e31822a8eac.CrossRefPubMed

32.

Allred DC, Carlson RW, Berry DA, Burstein HJ, Edge SB, Goldstein LJ, et al. NCCN task force report: estrogen receptor and progesterone receptor testing in breast cancer by immunohistochemistry. J Natl Compr Canc Netw. 2009;7 Suppl 6:S1–21. quiz S2-3.CrossRefPubMed

33.

Liedtke C, Mazouni C, Hess KR, Andre 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(8):1275–81. doi:10.1200/JCO.2007.14.4147.CrossRefPubMed

34.

Schott AF, Hayes DF. Defining the benefits of neoadjuvant chemotherapy for breast cancer. J Clin Oncol. 2012;30(15):1747–9. doi:10.1200/JCO.2011.41.3161.CrossRefPubMed

35.

Symmans WF, Peintinger F, Hatzis C, Rajan R, Kuerer H, Valero V, et al. Measurement of residual breast cancer burden to predict survival after neoadjuvant chemotherapy. J Clin Oncol. 2007;25(28):4414–22. doi:10.1200/jco.2007.10.6823.CrossRefPubMed

36.

Vriens BEPJ, Aarts MJB, de Vries B, van Gastel SM, Wals J, Smilde TJ, et al. Doxorubicin/cyclophosphamide with concurrent versus sequential docetaxel as neoadjuvant treatment in patients with breast cancer. Eur J Cancer. 2013. doi:10.1016/j.ejca.2013.06.012.

37.

Oakman C, Francis PA, Crown J, Quinaux E, Buyse M, De Azambuja E, et al. Overall survival benefit for sequential doxorubicin-docetaxel compared with concurrent doxorubicin and docetaxel in node-positive breast cancer--8-year results of the Breast International Group 02–98 phase III trial. Ann Oncol. 2013;24(5):1203–11. doi:10.1093/annonc/mds627.CrossRefPubMed

38.

Ogston KN, Miller ID, Payne S, Hutcheon AW, Sarkar TK, Smith I, et al. A new histological grading system to assess response of breast cancers to primary chemotherapy: prognostic significance and survival. Breast. 2003;12(5):320–7.CrossRefPubMed

39.

Rodenhuis S, Mandjes IA, Wesseling J, van de Vijver MJ, Peeters MJ, Sonke GS, et al. A simple system for grading the response of breast cancer to neoadjuvant chemotherapy. Ann Oncol. 2010;21(3):481–7. doi:10.1093/annonc/mdp348.CrossRefPubMed

40.

Moon HG, Im SA, Han W, Oh DY, Han SW, Keam B, et al. Estrogen receptor status confers a distinct pattern of response to neoadjuvant chemotherapy: implications for optimal durations of therapy: distinct patterns of response according to ER expression. Breast Cancer Res Treat. 2012;134(3):1133–40. doi:10.1007/s10549-012-2145-y.CrossRefPubMed

41.

Lee S, Toi M, Lee E, Ohtani S, Im Y, Im S, et al. A phase III trial of adjuvant capecitabine in breast cancer patients with HER2-negative pathologic residual invasive disease after neoadjuvant chemotherapy (CREATE-X, JBCRG-04), San Antonio Breast Cancer Symposium. 2015. Abstract S1-07.

Title: Prognostic impact of AJCC response criteria for neoadjuvant chemotherapy in stage II/III breast cancer patients: breast cancer subtype analyses
Authors: Yaewon Yang
Seock-Ah Im
Bhumsuk Keam
Kyung‑Hun Lee
Tae‑Yong Kim
Koung Jin Suh
Han Suk Ryu
Hyeong-Gon Moon
Sae‑Won Han
Do‑Youn Oh
Wonshik Han
Tae‑You Kim
In Ae Park
Dong-Young Noh
Publication date: 01-12-2016
Publisher: BioMed Central
Published in: BMC Cancer / Issue 1/2016
Electronic ISSN: 1471-2407
DOI: https://doi.org/10.1186/s12885-016-2500-1

Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras

Prof. Fabrice Barlesi

Developed by: Springer Medicine

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2016

CPA-7 influences immune profile and elicits anti-prostate cancer effects by inhibiting activated STAT3

Analysis of functional germline variants in APOBEC3 and driver genes on breast cancer risk in Moroccan study population

PTEN mRNA expression is less pronounced in left- than right-sided colon cancer: a retrospective observational study

Optimizing the process of fertility preservation in pediatric female cancer patients – a multidisciplinary program

ESOPEC: prospective randomized controlled multicenter phase III trial comparing perioperative chemotherapy (FLOT protocol) to neoadjuvant chemoradiation (CROSS protocol) in patients with adenocarcinoma of the esophagus (NCT02509286)

Study protocol of the CAREST-trial: a randomised controlled trial on the (cost-) effectiveness of a CBT-based online self-help training for fear of cancer recurrence in women with curatively treated breast cancer

Keynote webinar | Spotlight on antibody–drug conjugates in cancer