Abstract
Background
Breast-conserving surgery (BCS) still remains a blind surgery despite all available tumor localization methods. Intraoperative ultrasound (IOUS) allows real-time visualization during all resection phases.
Methods
This was a prospective observational cohort study conducted at the Veneto Institute of Oncology between January 2021 and June 2022. Patients with ductal carcinoma in situ, T1-2 invasive cancer, or post-neoadjuvant tumors, suitable for BCS, were recruited. All breast cancer lesion types were included, i.e. solid palpable, solid non-palpable, non-solid non-palpable, and post-neoadjuvant treatment residual lesions. Eligible participants were randomly assigned to either IOUS or traditional surgery (TS) in a 1:1 ratio. The main outcomes were surgical margin involvement, reoperation rate, closest margin width, main specimen and cavity shaving margin volumes, excess healthy tissue removal, and calculated resection ratio (CRR).
Results
Overall, 160 patients were enrolled: 80 patients were allocated to the TS group and 80 to the IOUS group. IOUS significantly reduced specimen volumes (16.8 cm3 [10.5–28.9] vs. 24.3 cm3 [15.0–41.3]; p = 0.015), with wider closest resection margin width (2.0 mm [1.0–4.0] vs. 1.0 mm [0.5–2.0] after TS; p < 0.001). Tumor volume to specimen volume ratio was significantly higher after IOUS (4.7% [2.5–9.1] vs. 2.9% [0.8–5.2]; p < 0.001). IOUS yielded significantly better CRR (84.5% [46–120.8] vs. 114% [81.8–193.2] after TS; p < 0.001), lower involved margin rate (2.5 vs. 15%; p = 0.009) and reduced re-excision rate (2.5 vs. 12.5%; p = 0.032).
Conclusions
IOUS allows real-time resection margin visualization and continuous control during BCS. It showed clear superiority over TS in both oncological and surgical outcomes for all breast cancer lesion types. These results disfavor the paradigm of blind breast surgery.
Similar content being viewed by others
References
De la Cruz KuG, Karamchandani M, Chambergo-Michilot D, et al. Does breast-conserving surgery with radiotherapy have a better survival than mastectomy? A meta-analysis of more than 1,500,000 patients. Ann Surg Oncol. 2022;29(10):6163–88. https://doi.org/10.1245/s10434-022-12133-8.
Lagendijk M, van Maaren MC, Saadatmand S, et al. Breast conserving therapy and mastectomy revisited: breast cancer-specific survival and the influence of prognostic factors in 129,692 patients. Int J Cancer. 2018;142(1):165–75. https://doi.org/10.1002/ijc.31034.
Gentilini OD, Cardoso MJ, Poortmans P. Less is more. Breast conservation might be even better than mastectomy in early breast cancer patients. Breast. 2017;35:32–3. https://doi.org/10.1016/j.breast.2017.06.004.
Davis KM, Raybon CP, Monga N, Waheed U, Michaels A, Henry C, Spalluto LB. Image-guided localization techniques for nonpalpable breast lesions: an opportunity for multidisciplinary patient-centered care. J Breast Imaging. 2021;3(5):542–55. https://doi.org/10.1093/jbi/wbab061.
Athanasiou C, Mallidis E, Tuffaha H. Comparative effectiveness of different localization techniques for non-palpable breast cancer. A systematic review and network meta-analysis. Eur J Surg Oncol. 2022;48(1):53–9. https://doi.org/10.1016/j.ejso.2021.10.001.
Krekel NM, Haloua MH, Lopes Cardozo AM, et al. Intraoperative ultrasound guidance for palpable breast cancer excision (COBALT trial): a multicentre, randomised controlled trial. Lancet Oncol. 2013;14(1):48–54. https://doi.org/10.1016/S1470-2045(12)70527-2.
Davis KM, Hsu CH, Bouton ME, Wilhelmson KL, Komenaka IK. Intraoperative ultrasound can decrease the re-excision lumpectomy rate in patients with palpable breast cancers. Am Surg. 2011;77(6):720–5.
Houssami N, Macaskill P, Marinovich ML, Morrow M. The association of surgical margins and local recurrence in women with early-stage invasive breast cancer treated with breast-conserving therapy: a meta-analysis. Ann Surg Oncol. 2014;21(3):717–30. https://doi.org/10.1245/s10434-014-3480-5.
Rifkin MD, Schwartz GF, Pasto ME, et al. Ultrasound for guidance of breast mass removal. J Ultrasound Med. 1988;7(5):261–3. https://doi.org/10.7863/jum.1988.7.5.261.
Eggemann H, Ignatov T, Beni A, Costa SD, Ignatov A. Ultrasonography-guided breast-conserving surgery is superior to palpation-guided surgery for palpable breast cancer. Clin Breast Cancer. 2014;14(1):40–5. https://doi.org/10.1016/j.clbc.2013.08.016.
Moore MM, Whitney LA, Cerilli L, et al. Intraoperative ultrasound is associated with clear lumpectomy margins for palpable infiltrating ductal breast cancer. Ann Surg. 2001;233(6):761–8. https://doi.org/10.1097/00000658-200106000-0.
Moore MM, Whitney LA, Cerilli L, et al. Intraoperative ultrasound is associated with clear lumpectomy margins for palpable infiltrating ductal breast cancer. Ann Surg. 2001;233(6):761–8. https://doi.org/10.1097/00000658-200106000-00005.
Volders JH, Haloua MH, Krekel NM, et al. Intraoperative ultrasound guidance in breast-conserving surgery shows superiority in oncological outcome, long-term cosmetic and patient-reported outcomes: final outcomes of a randomized controlled trial (COBALT). Eur J Surg Oncol. 2017;43(4):649–57. https://doi.org/10.1016/j.ejso.2016.11.004.
Esgueva A, Rodríguez-Revuelto R, Espinosa-Bravo M, Salazar JP, Rubio IT. Learning curves in intraoperative ultrasound guided surgery in breast cancer based on complete breast cancer excision and no need for second surgeries. Eur J Surg Oncol. 2019;45(4):578–83. https://doi.org/10.1016/j.ejso.2019.01.017.
Haid A, Knauer M, Dunzinger S, et al. Intra-operative sonography: a valuable aid during breast-conserving surgery for occult breast cancer. Ann Surg Oncol. 2007;14(11):3090–101. https://doi.org/10.1245/s10434-007-9490-9.
Tan PH, Ellis I, Allison K, et al. The 2019 World Health Organization classification of tumours of the breast. Histopathology. 2020;77(2):181–5. https://doi.org/10.1111/his.14091.
Cardoso F, Kyriakides S, Ohno S, et al. Early breast cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up [published correction appears in Ann Oncol 2019 1;30(10):1674] [published erratum appears in Ann Oncol. 2021 Feb;32(2):284]. Ann Oncol. 2019;30(8):1194–220. https://doi.org/10.1093/annonc/mdz173
Morrow M, Van Zee KJ, Solin LJ, et al. Society of surgical oncology-American society for radiation oncology-American society of clinical oncology consensus guideline on margins for breast-conserving surgery with whole-breast irradiation in ductal carcinoma in situ. Pract Radiat Oncol. 2016;6(5):287–95. https://doi.org/10.1016/j.prro.2016.06.011.
Moran MS, Schnitt SJ, Giuliano AE, et al. Society of surgical oncology-American society for radiation oncology consensus guideline on margins for breast-conserving surgery with whole-breast irradiation in stages I and II invasive breast cancer. Ann Surg Oncol. 2014;21(3):704–16. https://doi.org/10.1245/s10434-014-3481-4.
R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. 2022; Available at https://www.R-project.org/.
Gerrard AD, Shrotri A. Surgeon-led intraoperative ultrasound localization for nonpalpable breast cancers: results of 5 years of practice. Clin Breast Cancer. 2019;19(6):e748–52. https://doi.org/10.1016/j.clbc.2019.05.008.
Karadeniz Cakmak G, Emre AU, Tascilar O, Bahadir B, Ozkan S. Surgeon performed continuous intraoperative ultrasound guidance decreases re-excisions and mastectomy rates in breast cancer. Breast. 2017;33:23–8. https://doi.org/10.1016/j.breast.2017.02.014.
Hoffmann J, Marx M, Hengstmann A, et al. Ultrasound-assisted tumor surgery in breast cancer—a prospective, randomized, single-center study (MAC 001). Ultraschall Med. 2019;40(3):326–32. https://doi.org/10.1055/a-0637-1725.
Krekel NM, Zonderhuis BM, Stockmann HB, et al. A comparison of three methods for nonpalpable breast cancer excision. Eur J Surg Oncol. 2011;37(2):109–15. https://doi.org/10.1016/j.ejso.2010.12.006.
Rubio IT, Esgueva-Colmenarejo A, Espinosa-Bravo M, Salazar JP, Miranda I, Peg V. Intraoperative ultrasound-guided lumpectomy versus mammographic wire localization for breast cancer patients after neoadjuvant treatment. Ann Surg Oncol. 2016;23(1):38–43. https://doi.org/10.1245/s10434-015-4935-z.
James TA, Harlow S, Sheehey-Jones J, et al. Intraoperative ultrasound versus mammographic needle localization for ductal carcinoma in situ. Ann Surg Oncol. 2009;16(5):1164–9. https://doi.org/10.1245/s10434-009-0388-6.
Haloua MH, Krekel NM, Coupé VM, et al. Ultrasound-guided surgery for palpable breast cancer is cost-saving: results of a cost-benefit analysis. Breast. 2013;22(3):238–43. https://doi.org/10.1016/j.breast.2013.02.002.
Barellini L, Marcasciano M, Lo Torto F, Fausto A, Ribuffo D, Casella D. Intraoperative ultrasound and oncoplastic combined approach: an additional tool for the oncoplastic surgeon to obtain tumor-free margins in breast conservative surgery-a 2-year single-center prospective study. Clin Breast Cancer. 2020;20(3):e290–4. https://doi.org/10.1016/j.clbc.2019.10.004.
Cochrane RA, Valasiadou P, Wilson AR, Al-Ghazal SK, Macmillan RD. Cosmesis and satisfaction after breast-conserving surgery correlates with the percentage of breast volume excised. Br J Surg. 2003;90(12):1505–9. https://doi.org/10.1002/bjs.4344.
Hennigs A, Hartmann B, Rauch G, et al. Long-term objective esthetic outcome after breast-conserving therapy. Breast Cancer Res Treat. 2015;153(2):345–51. https://doi.org/10.1007/s10549-015-3540-y.
Klimberg VS. Intraoperative image-guided breast-conservation surgery should be the gold standard. Ann Surg Oncol. 2016;23(1):4–5. https://doi.org/10.1245/s10434-015-4936-y.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Disclosure
Massimo Ferrucci, Francesco Milardi, Daniele Passeri, Luaya Fabrizio Mpungu, Andrea Francavilla, Matteo Cagol, Tania Saibene, Silvia Michieletto, Mariacristina Toffanin, Paola Del Bianco, Ugo Grossi, and Alberto Marchet have no conflicts of interest to disclose.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ferrucci, M., Milardi, F., Passeri, D. et al. Intraoperative Ultrasound-Guided Conserving Surgery for Breast Cancer: No More Time for Blind Surgery. Ann Surg Oncol 30, 6201–6214 (2023). https://doi.org/10.1245/s10434-023-13900-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1245/s10434-023-13900-x