Impact of neoadjuvant chemotherapy on surgical treatment of breast cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

YANG Xiwen ,  CHEN Jie

Breast Center, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

CHEN Jie, Email: chenjiedoctor@126.com

Keywords：

breast cancer; neoadjuvant chemotherapy; surgery; pathological complete remission; axillary lymph nodes; review

DOI：

10.7507/1007-9424.202404112

Video：

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Objective To summarize recent research on the surgical treatment of breast cancer after neoadjuvant chemotherapy (NAC) and to review the impact of NAC on the surgical treatment of breast cancer. Method Relevant studies on NAC and surgical treatment of breast cancer from both domestic and international sources were reviewed. The literatures were analyzed, summarized, and discussed. Results Following NAC, the survival outcomes and risk of local recurrence in patients undergoing breast-conserving surgery were similar to those undergoing mastectomy. The using of image-guided minimally invasive biopsy accurately predicted pathological complete remission (pCR) of breast lesions after NAC, potentially allowed some breast cancer patients to undergo only radiation therapy after NAC, thus avoiding breast surgery. For patients with positive axillary lymph nodes, techniques such as dual-tracer, triple-tracer, and targeted axillary lymph node dissection had achieved clinical requirements in terms of detection rate and false-negative rate of sentinel lymph node biopsy, provided a safe alternative to axillary lymph node dissection. Conclusions NAC is an important component of comprehensive breast cancer treatment. However, there is still controversy regarding the local treatment of the primary breast lesion and axillary lymph nodes after NAC. Currently, individualized treatment based on the specific circumstances of the patient remains the approach in clinical practice, aiming to achieve the optimal control of local recurrence and survival benefits for patients.

Citation： YANG Xiwen, CHEN Jie. Impact of neoadjuvant chemotherapy on surgical treatment of breast cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2024, 31(9): 1025-1032. doi: 10.7507/1007-9424.202404112 Copy

1.	中国乳腺癌新辅助治疗专家共识(2022年版)专家组. 中国乳腺癌新辅助治疗专家共识(2022年版). 中国癌症杂志, 2022, 32(1): 80-89.
2.	Mauri D, Pavlidis N, Ioannidis JP. Neoadjuvant versus adjuvant systemic treatment in breast cancer: a meta-analysis. J Natl Cancer Inst, 2005, 97(3): 188-194.
3.	Karanlik H, Ozgur I, Cabioglu N, et al. Preoperative chemotherapy for T2 breast cancer is associated with improved surgical outcome. Eur J Surg Oncol, 2015, 41(9): 1226-1233.
4.	Burstein HJ, Curigliano G, Loibl S, et al. Estimating the benefits of therapy for early-stage breast cancer: the St. Gallen International Consensus Guidelines for the primary therapy of early breast cancer 2019. Ann Oncol, 2019, 30(10): 1541-1557.
5.	Petruolo O, Sevilimedu V, Montagna G, et al. How often does modern neoadjuvant chemotherapy downstage patients to breast-conserving surgery? Ann Surg Oncol, 2021, 28(1): 287-294.
6.	Charfare H, Limongelli S, Purushotham AD. Neoadjuvant chemotherapy in breast cancer. Br J Surg, 2005, 92(1): 14-23.
7.	Krzos A, Stanisławek A, Jędrych M, et al. Satisfaction with the aesthetic effect and quality of life for women after breast conserving therapy (BCT)-preliminary research. Int J Environ Res Public Health, 2019, 16(23): 4682. doi: 10.3390/ijerph16234682.
8.	Early Breast Cancer Trialists’ Collaborative Group (EBCTCG). Long-term outcomes for neoadjuvant versus adjuvant chemotherapy in early breast cancer: meta-analysis of individual patient data from ten randomised trials. Lancet Oncol, 2018, 19(1): 27-39.
9.	Werutsky G, Untch M, Hanusch C, et al. Locoregional recurrence risk after neoadjuvant chemotherapy: A pooled analysis of nine prospective neoadjuvant breast cancer trials. Eur J Cancer, 2020, 130: 92-101.
10.	Mamtani A, Sevilimedu V, Le T, et al. Is local recurrence higher among patients who downstage to breast conservation after neoadjuvant chemotherapy? Cancer, 2022, 128(3): 471-478.
11.	Chou HH, Chung WS, Ding RY, et al. Factors affecting locoregional recurrence in breast cancer patients undergoing surgery following neoadjuvant treatment. BMC Surg, 2021, 21(1): 160. doi: 10.1186/s12893-021-01158-7.
12.	Mukhtar RA, Chau H, Woriax H, et al. Breast conservation surgery and mastectomy have similar locoregional recurrence after neoadjuvant chemotherapy: Results from 1 462 patients on the prospective, randomized I-SPY2 trial. Ann Surg, 2023, 278(3): 320-327.
13.	中国抗癌协会乳腺癌专业委员会, 中华医学会肿瘤学分会乳腺肿瘤学组, 邵志敏. 中国抗癌协会乳腺癌诊治指南与规范(2024年版). 中国癌症杂志, 2023, 33(12): 1092-1186.
14.	Schaefgen B, Mati M, Sinn HP, et al. Can routine imaging after neoadjuvant chemotherapy in breast cancer predict pathologic complete response? Ann Surg Oncol, 2016, 23(3): 789-795.
15.	Heil J, Kümmel S, Schaefgen B, et al. Diagnosis of pathological complete response to neoadjuvant chemotherapy in breast cancer by minimal invasive biopsy techniques. Br J Cancer, 2015, 113(11): 1565-1570.
16.	Heil J, Schaefgen B, Sinn P, et al. Can a pathological complete response of breast cancer after neoadjuvant chemotherapy be diagnosed by minimal invasive biopsy? Eur J Cancer, 2016, 69: 142-150.
17.	潘鑫源, 李孟宇, 吴佳星, 等. 增强磁共振成像对乳腺癌新辅助化疗后病理完全缓解的预测价值. 中国普外基础与临床杂志, 2023, 30(3): 320-326.
18.	陈进, 胡美雪, 权毅. 动态增强磁共振成像联合多层螺旋CT增强扫描对乳腺癌新辅助化疗后病理缓解程度的预测价值. 中国普外基础与临床杂志, 2023, 30(1): 65-71.
19.	Kuerer HM, Rauch GM, Krishnamurthy S, et al. A clinical feasibility trial for identification of exceptional responders in whom breast cancer surgery can be eliminated following neoadjuvant systemic therapy. Ann Surg, 2018, 267(5): 946-951.
20.	Rossi EMC, Invento A, Pesapane F, et al. Diagnostic performance of image-guided vacuum-assisted breast biopsy after neoadjuvant therapy for breast cancer: prospective pilot study. Br J Surg, 2023, 110(2): 217-224.
21.	Pfob A, Sidey-Gibbons C, Rauch G, et al. Intelligent vacuum-assisted biopsy to identify breast cancer patients with pathologic complete response (ypT0 and ypN0) after neoadjuvant systemic treatment for omission of breast and axillary surgery. J Clin Oncol, 2022, 40(17): 1903-1915.
22.	Curigliano G, Burstein HJ, Winer EP, et al. De-escalating and escalating treatments for early-stage breast cancer: the St. Gallen International Expert Consensus Conference on the Primary Therapy of Early Breast Cancer 2017. Ann Oncol, 2017, 28(8): 1700-1712.
23.	Daveau C, Savignoni A, Abrous-Anane S, et al. Is radiotherapy an option for early breast cancers with complete clinical response after neoadjuvant chemotherapy? Int J Radiat Oncol Biol Phys, 2011, 79(5): 1452-1459.
24.	von Minckwitz G, Untch M, Blohmer JU, 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): 1796-1804.
25.	Prowell TM, Pazdur R. Pathological complete response and accelerated drug approval in early breast cancer. N Engl J Med, 2012, 366(26): 2438-2441.
26.	Esserman LJ, Woodcock J. Accelerating identification and regulatory approval of investigational cancer drugs. JAMA, 2011, 306(23): 2608-2609.
27.	Clouth B, Chandrasekharan S, Inwang R, et al. The surgical management of patients who achieve a complete pathological response after primary chemotherapy for locally advanced breast cancer. Eur J Surg Oncol, 2007, 33(8): 961-966.
28.	Berruti A, Amoroso V, Gallo F, et al. Pathologic complete response as a potential surrogate for the clinical outcome in patients with breast cancer after neoadjuvant therapy: a meta-regression of 29 randomized prospective studies. J Clin Oncol, 2014, 32(34): 3883-3891.
29.	Kuerer HM, Smith BD, Krishnamurthy S, et al. Eliminating breast surgery for invasive breast cancer in exceptional responders to neoadjuvant systemic therapy: a multicentre, single-arm, phase 2 trial. Lancet Oncol, 2022, 23(12): 1517-1524.
30.	Martelli G, Barretta F, Miceli R, et al. Sentinel node biopsy alone or with axillary dissection in breast cancer patients after primary chemotherapy: long-term results of a prospective interventional study. Ann Surg, 2022, 276(5): e544-e552. doi: 10.1097/SLA0000000000004562.
31.	Caudle AS, Yang WT, Krishnamurthy S, et al. Improved axillary evaluation following neoadjuvant therapy for patients with node-positive breast cancer using selective evaluation of clipped nodes: implementation of targeted axillary dissection. J Clin Oncol, 2016, 34(10): 1072-1078.
32.	Boughey JC, Ballman KV, Le-Petross HT, et al. Identification and resection of clipped node decreases the false-negative rate of sentinel lymph node surgery in patients presenting with node-positive breast cancer (T0-T4, N1-N2) who receive neoadjuvant chemotherapy: Results From ACOSOG Z1071 (Alliance). Ann Surg, 2016, 263(4): 802-807.
33.	Boughey JC, Suman VJ, Mittendorf EA, et al. Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA, 2013, 310(14): 1455-1461.
34.	Kuehn T, Bauerfeind I, Fehm T, et al. Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): a prospective, multicentre cohort study. Lancet Oncol, 2013, 14(7): 609-618.
35.	Classe JM, Loaec C, Gimbergues P, et al. Sentinel lymph node biopsy without axillary lymphadenectomy after neoadjuvant chemotherapy is accurate and safe for selected patients: the GANEA 2 study. Breast Cancer Res Treat, 2019, 173(2): 343-352.
36.	Boileau JF, Poirier B, Basik M, et al. Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: The SN FNAC study. J Clin Oncol, 2015, 33(3): 258-64.
37.	Yang J, He T, Wu Y, et al. Nanoparticle-assisted axillary staging: an alternative approach after neoadjuvant chemotherapy in patients with pretreatment node-positive breast cancers. Breast Cancer Res Treat, 2022, 192(3): 573-582.
38.	Simons JM, van Nijnatten TJA, van der Pol CC, et al. Diagnostic accuracy of radioactive iodine seed placement in the axilla with sentinel lymph node biopsy after neoadjuvant chemotherapy in node-positive breast cancer. JAMA Surg, 2022, 157(11): 991-999.
39.	Rastogi P, Anderson SJ, Bear HD, et al. Preoperative chemotherapy: updates of National Surgical Adjuvant Breast and Bowel Project Protocols B-18 and B-27. J Clin Oncol, 2008, 26(5): 778-785.
40.	Wu SY, Li JW, Wang YJ, et al. Clinical feasibility and oncological safety of non-radioactive targeted axillary dissection after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: a prospective diagnostic and prognostic study. Int J Surg, 2023, 109(7): 1863-1870.
41.	Kuemmel S, Heil J, Bruzas S, et al. Safety of targeted axillary dissection after neoadjuvant therapy in patients with node-positive breast cancer. JAMA Surg, 2023, 158(8): 807-815.
42.	Mamounas E P, Bandos H, White J, et al. Loco-regional irradiation in patients with biopsy-proven axillary node involvement at presentation who become pathologically node-negative after neoadjuvant chemotherapy: primary outcomes of NRG Oncology[C]. NSABP B-51/RTOG 1304. Presented at the 2023 San Antonio Breast Cancer Symposium, December 5–9, San Antonio, Texas, 2023. Abstrast GS02–GS07, 2023.
43.	Reimer T, Glass A, Botteri E, et al. Avoiding axillary sentinel lymph node biopsy after neoadjuvant systemic therapy in breast cancer: rationale for the prospective, multicentric EUBREAST-01 trial. Cancers (Basel). 2020;12(12): 3698.
44.	Comparison of axillary lymph node dissection with axillary radiation for patients with node-positive breast cancer treated with chemotherapy. https://clinicaltrials.gov/ ct2/show/NCT01901094.

1. 中国乳腺癌新辅助治疗专家共识(2022年版)专家组. 中国乳腺癌新辅助治疗专家共识(2022年版). 中国癌症杂志, 2022, 32(1): 80-89.
2. Mauri D, Pavlidis N, Ioannidis JP. Neoadjuvant versus adjuvant systemic treatment in breast cancer: a meta-analysis. J Natl Cancer Inst, 2005, 97(3): 188-194.
3. Karanlik H, Ozgur I, Cabioglu N, et al. Preoperative chemotherapy for T2 breast cancer is associated with improved surgical outcome. Eur J Surg Oncol, 2015, 41(9): 1226-1233.
4. Burstein HJ, Curigliano G, Loibl S, et al. Estimating the benefits of therapy for early-stage breast cancer: the St. Gallen International Consensus Guidelines for the primary therapy of early breast cancer 2019. Ann Oncol, 2019, 30(10): 1541-1557.
5. Petruolo O, Sevilimedu V, Montagna G, et al. How often does modern neoadjuvant chemotherapy downstage patients to breast-conserving surgery? Ann Surg Oncol, 2021, 28(1): 287-294.
6. Charfare H, Limongelli S, Purushotham AD. Neoadjuvant chemotherapy in breast cancer. Br J Surg, 2005, 92(1): 14-23.
7. Krzos A, Stanisławek A, Jędrych M, et al. Satisfaction with the aesthetic effect and quality of life for women after breast conserving therapy (BCT)-preliminary research. Int J Environ Res Public Health, 2019, 16(23): 4682. doi: 10.3390/ijerph16234682.
8. Early Breast Cancer Trialists’ Collaborative Group (EBCTCG). Long-term outcomes for neoadjuvant versus adjuvant chemotherapy in early breast cancer: meta-analysis of individual patient data from ten randomised trials. Lancet Oncol, 2018, 19(1): 27-39.
9. Werutsky G, Untch M, Hanusch C, et al. Locoregional recurrence risk after neoadjuvant chemotherapy: A pooled analysis of nine prospective neoadjuvant breast cancer trials. Eur J Cancer, 2020, 130: 92-101.
10. Mamtani A, Sevilimedu V, Le T, et al. Is local recurrence higher among patients who downstage to breast conservation after neoadjuvant chemotherapy? Cancer, 2022, 128(3): 471-478.
11. Chou HH, Chung WS, Ding RY, et al. Factors affecting locoregional recurrence in breast cancer patients undergoing surgery following neoadjuvant treatment. BMC Surg, 2021, 21(1): 160. doi: 10.1186/s12893-021-01158-7.
12. Mukhtar RA, Chau H, Woriax H, et al. Breast conservation surgery and mastectomy have similar locoregional recurrence after neoadjuvant chemotherapy: Results from 1 462 patients on the prospective, randomized I-SPY2 trial. Ann Surg, 2023, 278(3): 320-327.
13. 中国抗癌协会乳腺癌专业委员会, 中华医学会肿瘤学分会乳腺肿瘤学组, 邵志敏. 中国抗癌协会乳腺癌诊治指南与规范(2024年版). 中国癌症杂志, 2023, 33(12): 1092-1186.
14. Schaefgen B, Mati M, Sinn HP, et al. Can routine imaging after neoadjuvant chemotherapy in breast cancer predict pathologic complete response? Ann Surg Oncol, 2016, 23(3): 789-795.
15. Heil J, Kümmel S, Schaefgen B, et al. Diagnosis of pathological complete response to neoadjuvant chemotherapy in breast cancer by minimal invasive biopsy techniques. Br J Cancer, 2015, 113(11): 1565-1570.
16. Heil J, Schaefgen B, Sinn P, et al. Can a pathological complete response of breast cancer after neoadjuvant chemotherapy be diagnosed by minimal invasive biopsy? Eur J Cancer, 2016, 69: 142-150.
17. 潘鑫源, 李孟宇, 吴佳星, 等. 增强磁共振成像对乳腺癌新辅助化疗后病理完全缓解的预测价值. 中国普外基础与临床杂志, 2023, 30(3): 320-326.
18. 陈进, 胡美雪, 权毅. 动态增强磁共振成像联合多层螺旋CT增强扫描对乳腺癌新辅助化疗后病理缓解程度的预测价值. 中国普外基础与临床杂志, 2023, 30(1): 65-71.
19. Kuerer HM, Rauch GM, Krishnamurthy S, et al. A clinical feasibility trial for identification of exceptional responders in whom breast cancer surgery can be eliminated following neoadjuvant systemic therapy. Ann Surg, 2018, 267(5): 946-951.
20. Rossi EMC, Invento A, Pesapane F, et al. Diagnostic performance of image-guided vacuum-assisted breast biopsy after neoadjuvant therapy for breast cancer: prospective pilot study. Br J Surg, 2023, 110(2): 217-224.
21. Pfob A, Sidey-Gibbons C, Rauch G, et al. Intelligent vacuum-assisted biopsy to identify breast cancer patients with pathologic complete response (ypT0 and ypN0) after neoadjuvant systemic treatment for omission of breast and axillary surgery. J Clin Oncol, 2022, 40(17): 1903-1915.
22. Curigliano G, Burstein HJ, Winer EP, et al. De-escalating and escalating treatments for early-stage breast cancer: the St. Gallen International Expert Consensus Conference on the Primary Therapy of Early Breast Cancer 2017. Ann Oncol, 2017, 28(8): 1700-1712.
23. Daveau C, Savignoni A, Abrous-Anane S, et al. Is radiotherapy an option for early breast cancers with complete clinical response after neoadjuvant chemotherapy? Int J Radiat Oncol Biol Phys, 2011, 79(5): 1452-1459.
24. von Minckwitz G, Untch M, Blohmer JU, 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): 1796-1804.
25. Prowell TM, Pazdur R. Pathological complete response and accelerated drug approval in early breast cancer. N Engl J Med, 2012, 366(26): 2438-2441.
26. Esserman LJ, Woodcock J. Accelerating identification and regulatory approval of investigational cancer drugs. JAMA, 2011, 306(23): 2608-2609.
27. Clouth B, Chandrasekharan S, Inwang R, et al. The surgical management of patients who achieve a complete pathological response after primary chemotherapy for locally advanced breast cancer. Eur J Surg Oncol, 2007, 33(8): 961-966.
28. Berruti A, Amoroso V, Gallo F, et al. Pathologic complete response as a potential surrogate for the clinical outcome in patients with breast cancer after neoadjuvant therapy: a meta-regression of 29 randomized prospective studies. J Clin Oncol, 2014, 32(34): 3883-3891.
29. Kuerer HM, Smith BD, Krishnamurthy S, et al. Eliminating breast surgery for invasive breast cancer in exceptional responders to neoadjuvant systemic therapy: a multicentre, single-arm, phase 2 trial. Lancet Oncol, 2022, 23(12): 1517-1524.
30. Martelli G, Barretta F, Miceli R, et al. Sentinel node biopsy alone or with axillary dissection in breast cancer patients after primary chemotherapy: long-term results of a prospective interventional study. Ann Surg, 2022, 276(5): e544-e552. doi: 10.1097/SLA0000000000004562.
31. Caudle AS, Yang WT, Krishnamurthy S, et al. Improved axillary evaluation following neoadjuvant therapy for patients with node-positive breast cancer using selective evaluation of clipped nodes: implementation of targeted axillary dissection. J Clin Oncol, 2016, 34(10): 1072-1078.
32. Boughey JC, Ballman KV, Le-Petross HT, et al. Identification and resection of clipped node decreases the false-negative rate of sentinel lymph node surgery in patients presenting with node-positive breast cancer (T0-T4, N1-N2) who receive neoadjuvant chemotherapy: Results From ACOSOG Z1071 (Alliance). Ann Surg, 2016, 263(4): 802-807.
33. Boughey JC, Suman VJ, Mittendorf EA, et al. Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA, 2013, 310(14): 1455-1461.
34. Kuehn T, Bauerfeind I, Fehm T, et al. Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): a prospective, multicentre cohort study. Lancet Oncol, 2013, 14(7): 609-618.
35. Classe JM, Loaec C, Gimbergues P, et al. Sentinel lymph node biopsy without axillary lymphadenectomy after neoadjuvant chemotherapy is accurate and safe for selected patients: the GANEA 2 study. Breast Cancer Res Treat, 2019, 173(2): 343-352.
36. Boileau JF, Poirier B, Basik M, et al. Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: The SN FNAC study. J Clin Oncol, 2015, 33(3): 258-64.
37. Yang J, He T, Wu Y, et al. Nanoparticle-assisted axillary staging: an alternative approach after neoadjuvant chemotherapy in patients with pretreatment node-positive breast cancers. Breast Cancer Res Treat, 2022, 192(3): 573-582.
38. Simons JM, van Nijnatten TJA, van der Pol CC, et al. Diagnostic accuracy of radioactive iodine seed placement in the axilla with sentinel lymph node biopsy after neoadjuvant chemotherapy in node-positive breast cancer. JAMA Surg, 2022, 157(11): 991-999.
39. Rastogi P, Anderson SJ, Bear HD, et al. Preoperative chemotherapy: updates of National Surgical Adjuvant Breast and Bowel Project Protocols B-18 and B-27. J Clin Oncol, 2008, 26(5): 778-785.
40. Wu SY, Li JW, Wang YJ, et al. Clinical feasibility and oncological safety of non-radioactive targeted axillary dissection after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: a prospective diagnostic and prognostic study. Int J Surg, 2023, 109(7): 1863-1870.
41. Kuemmel S, Heil J, Bruzas S, et al. Safety of targeted axillary dissection after neoadjuvant therapy in patients with node-positive breast cancer. JAMA Surg, 2023, 158(8): 807-815.
42. Mamounas E P, Bandos H, White J, et al. Loco-regional irradiation in patients with biopsy-proven axillary node involvement at presentation who become pathologically node-negative after neoadjuvant chemotherapy: primary outcomes of NRG Oncology[C]. NSABP B-51/RTOG 1304. Presented at the 2023 San Antonio Breast Cancer Symposium, December 5–9, San Antonio, Texas, 2023. Abstrast GS02–GS07, 2023.
43. Reimer T, Glass A, Botteri E, et al. Avoiding axillary sentinel lymph node biopsy after neoadjuvant systemic therapy in breast cancer: rationale for the prospective, multicentric EUBREAST-01 trial. Cancers (Basel). 2020;12(12): 3698.
44. Comparison of axillary lymph node dissection with axillary radiation for patients with node-positive breast cancer treated with chemotherapy. https://clinicaltrials.gov/ ct2/show/NCT01901094.

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