Skip to main content

Advertisement

SpringerLink
Log in

Sentinel lymph node assessment in breast cancer—an update on current recommendations

  • Review and Perspectives
  • Published:
Virchows Archiv Aims and scope Submit manuscript

Abstract

Sentinel lymph node biopsy (SLNB) has become the preferred method of surgical pathological nodal staging of early breast cancer by the end of the nineties. As the most likely sites of metastasis, the SLNs allow a more precise staging, and indeed gross sectioning, step sectioning, immunohistochemistry, and molecular staging methods have been used to disclose metastatic involvement of these lymph nodes. This review summarizes the backgrounds of SLNB, trends in related surgery and pathology. It also gives an insight into European National recommendations related to SLN and divergent daily practices in European pathology departments, on the basis of replies to questionnaires from 84 pathologists from 38 European countries. The questionnaires revealed the post-neoadjuvant setting as an area where a significant minority of pathologists report less confidence in classifying residual nodal involvement into TNM categories. The review also summarizes the neoadjuvant therapy-related aspects of SLNB.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

source of confusion may stem from the fact that the Royal College of Pathologists’ guidance on reporting breast diseases suggests to measure foci separated by less than 5 mm as a single lesion for the primary tumor, but no similar statements for the metastasis size measurement [72]

Similar content being viewed by others

Data availability

The results of the questionnaire-based survey are submitted (therefore available) as Supplementary material.

References

  1. Cady B (1973) (1973) Total mastectomy and partial axillary dissection. Surg Clin North Am 53:313–318. https://doi.org/10.1016/s0039-6109(16)39983-2

    Article  CAS  PubMed  Google Scholar 

  2. Forrest APM, Everington D, McDonald CC, Steele RJ, Chetty U, Stewart HJ (1995) The Edinburgh randomised trial of axillary sampling or clearance after mastectomy. Br J Surg 82:1504–1508. https://doi.org/10.1002/bjs.1800821118

    Article  CAS  PubMed  Google Scholar 

  3. Krag DN, Weaver DL, Alex JC, Fairbank JT (1993) Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol 2:335–340. https://doi.org/10.1016/0960-7404(93)90064-6

    Article  CAS  PubMed  Google Scholar 

  4. Giuliano AE, Kirgan DM, Guenther JM, Morton DL (1994) Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 220:391–398. https://doi.org/10.1097/00000658-199409000-00015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Albertini JJ, Lyman GH, Cox C, Yeatman T, Balducci L, Ku N, Shivers S, Berman C, Wells K, Rapaport D, Shons A, Horton J, Greenberg H, Nicosia S, Clark R, Cantor A, Reintgen DS (1996) Lymphatic mapping and sentinel node biopsy in the patient with breast cancer. JAMA 276:1818–1822

    Article  CAS  Google Scholar 

  6. Alvarado MD, Mittendorf EA, Teshome M, Thompson AM, Bold RJ, Gittleman MA, Beitsch PD, Blair SL, Kivilaid K, Harmer QJ, Hunt KK (2019) SentimagIC: a non-inferiority trial comparing superparamagnetic iron oxide versus technetium-99m and blue dye in the detection of axillary sentinel nodes in patients with early-stage breast cancer. Ann Surg Oncol 26:3510–3516. https://doi.org/10.1245/s10434-019-07577-4

    Article  PubMed  Google Scholar 

  7. Jeremiasse B, van den Bosch CH, Wijnen MWHA, Terwisscha van Scheltinga CEJ, Fiocco MF, van der Steeg AFW (2020) Systematic review and meta-analysis concerning near-infrared imaging with fluorescent agents to identify the sentinel lymph node in oncology patients. Eur J Surg Oncol 46:2011–2022. https://doi.org/10.1016/j.ejso.2020.07.012

    Article  CAS  PubMed  Google Scholar 

  8. Veronesi U, Viale G, Paganelli G, Zurrida S, Luini A, Galimberti V, Veronesi P, Intra M, Maisonneuve P, Zucca F, Gatti G, Mazzarol G, De Cicco C, Vezzoli D (2010) Sentinel lymph node biopsy in breast cancer: ten-year results of a randomized controlled study. Ann Surg 251:595–600. https://doi.org/10.1097/SLA.0b013e3181c0e92a

    Article  PubMed  Google Scholar 

  9. Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Costantino JP, Ashikaga T, Weaver DL, Mamounas EP, Jalovec LM, Frazier TG, Noyes RD, Robidoux A, Scarth HM, Wolmark N (2010) Sentinel-lymph-node resection compared with conventional axillary-lymph-node dissection in clinically node-negative patients with breast cancer: overall survival findings from the NSABP B-32 randomised phase 3 trial. Lancet Oncol 11:927–933. https://doi.org/10.1016/S1470-2045(10)70207-2

    Article  PubMed  PubMed Central  Google Scholar 

  10. Petrelli F, Lonati V, Barni S (2012) Axillary dissection compared to sentinel node biopsy for the treatment of pathologically node-negative breast cancer: a meta-analysis of four randomized trials with long-term follow up. Oncol Rev 6(2):e20. https://doi.org/10.4081/oncol.2012.e20

    Article  PubMed  PubMed Central  Google Scholar 

  11. van der Ploeg IM, Nieweg OE, van Rijk MC, Valdés Olmos RA, Kroon BB (2008) Axillary recurrence after a tumour-negative sentinel node biopsy in breast cancer patients: a systematic review and meta-analysis of the literature. Eur J Surg Oncol 34:1277–1284. https://doi.org/10.1016/j.ejso.2008.01.034

    Article  PubMed  Google Scholar 

  12. Galimberti V, Cole BF, Viale G, Veronesi P, Vicini E, Intra M, Mazzarol G, Massarut S, Zgajnar J, Taffurelli M, Littlejohn D, Knauer M, Tondini C, Di Leo A, Colleoni M, Regan MM, Coates AS, Gelber RD, Goldhirsch A; International Breast Cancer Study Group Trial 23–01 (2018) Axillary dissection versus no axillary dissection in patients with breast cancer and sentinel-node micrometastases (IBCSG 23–01): 10-year follow-up of a randomised, controlled phase 3 trial. Lancet Oncol 19:1385–1393. https://doi.org/10.1016/S1470-2045(18)30380-2

    Article  Google Scholar 

  13. Giuliano AE, Ballman KV, McCall L, Beitsch PD, Brennan MB, Kelemen PR, Ollila DW, Hansen NM, Whitworth PW, Blumencranz PW, Leitch AM, Saha S, Hunt KK, Morrow M (2017) Effect of axillary dissection vs no axillary dissection on 10-year overall survival among women with invasive breast cancer and sentinel node metastasis: the ACOSOG Z0011 (Alliance) randomized clinical trial. JAMA 318:918–926. https://doi.org/10.1001/jama.2017.11470

    Article  PubMed  PubMed Central  Google Scholar 

  14. Donker M, van Tienhoven G, Straver ME, Meijnen P, van de Velde CJH, Mansel RE, Cataliotti L, Westenberg AH, Klinkenbijl JH, Orzalesi L, Bouma WH, van der Mijle HC, Nieuwenhuijzen GA, Veltkamp SC, Slaets L, Duez NJ, de Graaf PW, van Dalen T, Marinelli A, Rijna H, Snoj M, Bundred NJ, Merkus JW, Belkacemi Y, Petignat P, Schinagl DA, Coens C, Messina CG, Bogaerts J, Rutgers EJ (2014) Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981–22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol 15:1303–1310. https://doi.org/10.1016/S1470-2045(14)70460-7

    Article  PubMed  PubMed Central  Google Scholar 

  15. Sávolt Á, Péley G, Polgár C, Udvarhelyi N, Rubovszky G, Kovács E, Győrffy B, Kásler M, Mátrai Z (2017) Eight-year follow up result of the OTOASOR trial: the optimal treatment of the axilla - surgery or radiotherapy after positive sentinel lymph node biopsy in early-stage breast cancer: a randomized, single centre, phase III, non-inferiority trial. Eur J Surg Oncol 43:672–679. https://doi.org/10.1016/j.ejso.2016.12.011

    Article  PubMed  Google Scholar 

  16. Kuehn T, Bauerfeind I, Fehm T, Fleige B, Hausschild M, Helms G, Lebeau A, Liedtke C, von Minckwitz G, Nekljudova V, Schmatloch S, Schrenk P, Staebler A, Untch M (2013) Sentinel-lymph-node biopsy in patients with breast cancer before and after neoadjuvant chemotherapy (SENTINA): a prospective, multicentre cohort study. Lancet Oncol 14:609–618. https://doi.org/10.1016/S1470-2045(13)70166-9

    Article  PubMed  Google Scholar 

  17. Geng C, Chen X, Pan X, Li J (2016) The feasibility and accuracy of sentinel lymph node biopsy in initially clinically node-negative breast cancer after neoadjuvant chemotherapy: a systematic review and meta-analysis. PLoS ONE 11(9):e0162605. https://doi.org/10.1371/journal.pone.0162605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Shirzadi A, Mahmoodzadeh H, Qorbani M (2019) Assessment of sentinel lymph node biopsy after neoadjuvant chemotherapy for breast cancer in two subgroups: initially node negative and node positive converted to node negative - a systemic review and meta-analysis. J Res Med Sci 24:18. https://doi.org/10.4103/jrms.JRMS_127_18

    Article  PubMed  PubMed Central  Google Scholar 

  19. Boughey JC, Suman VJ, Mittendorf EA, Ahewndt GM, Wilke LG, Taback B, Leitch AM, Kuerer HM, Bowling M, Flippo-Mortom TS, Byrd DR, Ollila DW, Julian TB, McLaughlin SA, McCall L, Symmans WF, Le-Petross HT, Haffty BG, Buchholz TA, Nelson H, Hunt KK, Alliance for Clinical Trials in Oncology, (2013) Sentinel lymph node surgery after neoadjuvant chemotherapy in patients with node-positive breast cancer: the ACOSOG Z1071 (Alliance) clinical trial. JAMA 310:1455–1461. https://doi.org/10.1001/jama.2013.278932

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Boileau JF, Poirier B, Basik M, Holloway CM, Gaboury L, Sideris L, Meterissioan S, Arnaout A, Brackstone M, McCready DR, Karp SE, Trop I, Lisbona A, Wright FC, Younan RJ, Provencher L, Patocskai E, Omeroglu A, Robidoux A (2015) Sentinel node biopsy after neoadjuvant chemotherapy in biopsy-proven node-positive breast cancer: the SN FNAC study. J Clin Oncol 33:258–264. https://doi.org/10.1200/JCO.2014.55.7827

    Article  PubMed  Google Scholar 

  21. King TA, Morrow M (2015) Surgical issues in patients with breast cancer receiving neoadjuvant chemotherapy. Nat Rev Clin Oncol 12:335–343. https://doi.org/10.1038/nrclinonc.2015.63

    Article  PubMed  Google Scholar 

  22. Boughey JC, Ballman KV, Hunt KK, McCall LM, Mittendorf EA, Ahrendt GM, Wilke LG, Le-Petross HT (2015) Axillary ultrasound after neoadjuvant chemotherapy and its impact on sentinel lymph node surgery: results from the American College of Surgeons Oncology Group Z1071 Trial (Alliance). J Clin Oncol 33:3386–3393. https://doi.org/10.1200/JCO.2014.57.8401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Donker M, Straver ME, Wesseling J, Loo CE, Schot M, Drukker CA, van Tinteren H, Sonke GS, Rutgers EJ, Vrancken Peeters MJ (2015) Marking axillary lymph nodes with radioactive iodine seeds for axillary staging after neoadjuvant systemic treatment in breast cancer patients: the MARI procedure. Ann Surg 261:378–382. https://doi.org/10.1097/SLA.0000000000000558

    Article  PubMed  Google Scholar 

  24. Boughey JC, Ballman KV, Le-Petross HT, McCall LM, Mittendorf EA, Ahrendt GM, Wilke LG, Taback B, Feliberti EC, Hunt KK (2016) 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 263:802–807. https://doi.org/10.1097/SLA.0000000000001375

    Article  PubMed  Google Scholar 

  25. Caudle AS, Yang WT, Krishnamurthy S, Mittendorf EA, Black DM, Gilcrease MZ, Bedrosian I, Hobbs BP, DeSnyder SM, Hwang RF, Adrada BE, Shaitelman SF, Chavez-MacGregor M, Smith BD, Candelaria RP, Babiera GV, Doagn BE, Santiago L, Hunt KK, Kuerer H (2016) 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 34:1072–1078. https://doi.org/10.1200/JCO.2015.64.0094

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Sentinel lymph node after neoadjuvant chemotherapy in breast carcinoma (GANEA3) Available from: https://clinicaltrials.gov/ct2/show/NCT03630913. Accessed 28 February 2021

  27. ATNEC - Axillary management in T1-3N1M0 breast cancer patients with needle biopsy proven nodal metastases at presentation after neoadjuvant chemotherapy. Available from: https://clinicaltrials.gov/ct2/show/NCT04109079. Accessed 28 February 2021

  28. Tailored axillary surgery with or without axillary lymph node dissection followed by radiotherapy in patients with clinically node-positive breast cancer (TAXIS) (TAXIS) [Available from: https://clinicaltrials.gov/ct2/show/NCT03513614]. Accessed 28 February 2021

  29. Reynolds JV, Mercer P, McDermot EWM, Cross S, Stokes M, Murphy D, O’Higgins NJ (1994) Audit of complete axillary dissection in early breast cancer. Eur J Cancer 30A:148–149. https://doi.org/10.1016/0959-8049(94)90075-2

    Article  CAS  PubMed  Google Scholar 

  30. Cserni G (1998) How to improve lymph node recovery rates from axillary clearance specimens of breast cancer? A short-term audit. J Clin Pathol 51:846–849. https://doi.org/10.1136/jcp.51.11.846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Huvos AG, Hutter RV, Berg JW (1971) Significance of axillary macrometastases and micrometastases in mammary cancer. Ann Surg 173:44–46. https://doi.org/10.1097/00000658-197101000-00006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Giuliano AE, Dale PS, Turner RR, Morton DL, Evans SW, Krasne DL (1995) Improved axillary staging of breast cancer with sentinel lymphadenectomy. Ann Surg 180:700–704. https://doi.org/10.1097/00000658-199509000-00016

    Article  Google Scholar 

  33. Cserni G, Amendoeira I, Apostolikas N, Bellocq JP, Bianchi S, Boecker W, Borisch B, Connolly CE, Decker T, Dervan P, Drijkoningen M, Ellis IO, Elston CW, Eusebi V, Faverly D, Heikkila P, Holland R, Kerner H, Kulka J, Jacquemier J, Lacerda M, Martinez-Penuela J, De Miguel C, Peterse JL, Rank F, Regitnig P, Reiner A, Sapino A, Sigal-Zafrani B, Tanous AM, Thorstenson S, Zozaya E, Fejes G, Wells CA (2004) Discrepancies in current practice of pathological evaluation of sentinel lymph nodes in breast cancer. Results of a questionnaire-based survey by the European Working Group for Breast Screening Pathology. J Clin Pathol 57:695–701. https://doi.org/10.1136/jcp.2003.013599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Cserni G, Amendoeira I, Apostolikas N, Bellocq JP, Bianchi S, Bussolati G, Boecker W, Borisch B, Connolly CE, Decker T, Dervan P, Drijkoningen M, Ellis IO, Elston CW, Eusebi V, Faverly D, Heikkila P, Holland R, Kerner H, Kulka J, Jacquemier J, Lacerda M, Martinez-Penuela J, De Miguel C, Peterse JL, Rank F, Regitnig P, Reiner A, Sapino A, Sigal-Zafrani B, Tanous AM, Thorstenson S, Zozaya E, Wells CA (2003) Pathological work-up of sentinel lymph nodes in breast cancer. Review of current data to be considered for the formulation of guidelines. Eur J Cancer 39:1654–1667. https://doi.org/10.1016/s0959-8049(03)00203-x

    Article  CAS  PubMed  Google Scholar 

  35. Feinstein AR, Sosin DM, Wells CK (1985) The Will Rogers phenomenon. Stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. N Engl J Med 312:1604–1608. https://doi.org/10.1056/NEJM198506203122504

    Article  CAS  PubMed  Google Scholar 

  36. Hermanek P, Hutter RVP, Sobin LH, Wittekind C (1999) Classification of isolated tumor cells and micrometastasis. Cancer 86:2668–2673

    Article  CAS  Google Scholar 

  37. Cserni G, Bianchi S, Boecker W, Decker T, Lacerda M, Rank F, Wells CA and the European Working Group for Breast Screening Pathology (2005) Improving the reproducibility of diagnosing micrometastases and isolated tumor cells. Cancer 103:358–367. https://doi.org/10.1002/cncr.20760

    Article  Google Scholar 

  38. De Mascarel I, MacGrogan G, Debled M, Brouste V, Mauriac L (2008) Distinction between isolated tumor cells and micrometastases in breast cancer: is it reliable and useful? Cancer 112:1672–1678. https://doi.org/10.1002/cncr.23368

    Article  PubMed  Google Scholar 

  39. Turner RR, Weaver DL, Cserni G, Lester SC, Hirsch K, Elashoff DA, Fitzgibbons PL, Viale G, Mazzarol G, Ibarra JA, Schnitt SJ, Giuliano AE (2008) Nodal stage classification for breast carcinoma: improving interobserver reproducibility through standardized histologic criteria and image-based training. J Clin Oncol 26:258–263. https://doi.org/10.1200/JCO.2007.13.0179

    Article  PubMed  Google Scholar 

  40. Cserni G, Amendoeira I, Bianchi S, Chmielik E, Degaetano J, Faverly D, Figueiredo P, Foschini MP, Grabau D, Jacquemier J, Kaya H, Kulka J, Lacerda M, Liepniece-Karele I, Penuela JM, Quinn C, Regitnig P, Reiner-Concin A, Sapino A, van Diest PJ, Varga Z, Vezzosi V, Wesseling J, Zolota V, Zozaya E, Wells CA (2011) Distinction of isolated tumour cells and micrometastasis in lymph nodes of breast cancer patients according to the new tumour node metastasis (TNM) definitions. Eur J Cancer 47:887–894. https://doi.org/10.1016/j.ejca.2010.11.011

    Article  PubMed  Google Scholar 

  41. Amin MB, Edge SB, Greene FL, Schilsky RL, Gaspar LE, Washington MK, Sullivan DC, Brookland RK, Brierley JD, Balch CM, Compton CC, Hess KR, Gershenwald JE, Jessup JM, Byrd DR, Winchester DP, Madera M, Assare EA (eds) (2017) American Joint Committee on Cancer (AJCC) cancer staging manual, 8th edn. Springer, New York

    Google Scholar 

  42. Cserni G, Brogi E, Cody HS III, Deb R, Farshid G, O’Toole S, Provenzano E, Quinn CM, Sahin A, Schmitt F, Weaver D, Yamaguchi R, Tan PH (2021) Surgically removed lymph nodes for breast tumours histopathology reporting guide, Sydney, International Collaboration on Cancer Reporting (ICCR), http://www.iccr-cancer.org/datasets/published-datasets/breast. Accessed 16 May 2021

  43. Weaver DL, Ashikaga T, Krag DN, Skelly JM, Anderson SJ, Harlow SP, Julian TB, Mamounas EP, Wolmark N (2011) Effect of occult metastases on survival in node-negative breast cancer. N Engl J Med 364:412–421. https://doi.org/10.1056/NEJMoa1008108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Giuliano AE, Hawes D, Ballman KV, Whitworth PW, Blumencranz PW, Reintgen DS, Morrow M, Leitch AM, Hunt KK, McCall LM, Abati A, Cote R (2011) Association of occult metastases in sentinel lymph nodes and bone marrow with survival among women with early-stage invasive breast cancer. JAMA 306:385–393. https://doi.org/10.1001/jama.2011.1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Goldhirsch A, Glick JH, Gelber RD, Coates AS, Thürlimann B, Senn HJ; Panel members (2005) Meeting highlights: international expert consensus on the primary therapy of early breast cancer 2005. Ann Oncol 16:1569–1583. https://doi.org/10.1093/annonc/mdi326

    Article  Google Scholar 

  46. Cardoso F, Kyriakides S, Ohno S, Penault-Llorca F, Poortmans P, Rubio IT, Zackrisson S, Senkus E, Guidelines Committee ESMO (2019) Early breast cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Electronic address: clinicalguidelines@esmo.org. Ann Oncol 30:1194–1220. https://doi.org/10.1093/annonc/mdz173

    Article  CAS  PubMed  Google Scholar 

  47. Weaver DL (2010) Pathology evaluation of sentinel lymph nodes in breast cancer: protocol recommendations and rationale. Mod Pathol 23(Suppl 2):S26-32. https://doi.org/10.1038/modpathol.2010.36

    Article  PubMed  Google Scholar 

  48. Cserni G (2012) How much is enough? Pathologic evaluation of sentinel lymph nodes. Current Breast Cancer Reports 4:89–95

    Article  Google Scholar 

  49. College of American Pathologists (2020) Protocol for the examination of resection specimens from patients with invasive carcinoma of the breast. https://documents.cap.org/protocols/cp-breast-invasive-resection-20-4400.pdf.  Accessed 06 March 2021.

  50. Lyman GH, Temin S, Edge SB, Newman LA, Turner RR, Weaver DL, Benson AB 3rd, Bosserman LD, Burstein HJ, Cody H 3rd, Hayman J, Perkins CL, Podoloff DA, Giuliano AE (2014) Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol 32:1365–1383. https://doi.org/10.1200/JCO.2013.54.1177

    Article  Google Scholar 

  51. Cserni G, Bianchi S, Vezzosi V, Peterse H, Sapino A, Arisio R, Reiner-Concin A, Regitnig P, Bellocq J-P, Marin C, Bori R, Martinez Penuela J, Córdoba Iturriagagoitia A (2006) The value of cytokeratin immunohistochemistry in the evaluation of axillary sentinel lymph nodes in patients with lobular breast carcinoma. J Clin Pathol 59:518–522. https://doi.org/10.1136/jcp.2005.029991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Gralow JR, Zujewski JA, Winer E (2008) Preoperative therapy in invasive breast cancer: reviewing the state of the science and exploring new research directions. J Clin Oncol 26:696–697. https://doi.org/10.1200/JCO.2007.15.9459

    Article  PubMed  Google Scholar 

  53. Zhang GC, Zhang YF, Xu FP, Qian XK, Guo ZB, Ren CY, Yao M (2013) Axillary lymph node status, adjusted for pathologic complete response in breast and axilla after neoadjuvant chemotherapy, predicts differential disease-free survival in breast cancer. Curr Oncol 20:e180–e192. https://doi.org/10.3747/co.20.1294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Krag DN, Anderson SJ, Julian TB, Brown AM, Harlow SP, Ashikaga T, Weaver DL, Miller BJ, Jalovec LM, Frazier TG, Noyes RD, Robidoux A, Scarth HMC, Mammolito DM, McCready DR, Mamounas EP, Costantino JP, Wolmark N, National Surgical Adjuvant Breast and Bowel Project (2007) Technical outcomes of sentinel-lymph-node resection and conventional axillary-lymph-node dissection in patients with clinically node-negative breast cancer: results from the NSABP B-32 randomised phase III trial. Lancet Oncol 8:881–888. https://doi.org/10.1016/S1470-2045(07)70278-4

    Article  CAS  Google Scholar 

  55. Mamounas EP, Brown A, Anderson S, Smith R, Julian T, Miller B, Bear HD, Caldwell CBm Walker AP, Mikkelson WM, Stauffer JS, Robidoux A, Theoret H, Soran A, Fisher B, Wickerham DL, Wolmark N. (2005) Sentinel node biopsy after neoadjuvant chemotherapy in breast cancer: results from National Surgical Adjuvant Breast and Bowel Project Protocol B-27. J Clin Oncol 23(12):2694–2702. https://doi.org/10.1200/JCO.2005.05.188

    Article  PubMed  Google Scholar 

  56. Gandhi A, Coles C, Makris A, Provenzano E, Goyal A, Maxwell AJ, Doughty J (2019) Axillary surgery following neoadjuvant chemotherapy - multidisciplinary guidance from the Association of Breast Surgery, Faculty of Clinical Oncology of the Royal College of Radiologists, UK Breast Cancer Group, National Coordinating Committee for Breast Pathology and British Society of Breast Radiology. Clin Oncol 31:664–668. https://doi.org/10.1016/j.clon.2019.05.021

    Article  CAS  Google Scholar 

  57. Pilewskie M, Morrow M (2017) Axillary nodal management following neoadjuvant chemotherapy: a review. JAMA Oncol 3:549–555. https://doi.org/10.1001/jamaoncol.2016.4163

    Article  PubMed  PubMed Central  Google Scholar 

  58. Curigliano G, Burstein HJ, Winer EP, Gnant M, Dubsky P, Loibl S, Colleoni M, Regan MM, Piccart-Gebhart M, Senn H-J, Thurlimann B, St. Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2017; Andre F, Baselga J, Bergh J, Bonnefoi H, Brucker SY, Cardoso F, Carey L, Ciruelos E, Cuzick J, Denkert C, Di Leo A, Ejlertsen B, Francis P, Galimberti V, Garber J, Gulluoglu B, Goodwin P, Harbeck N, Hayes DF, Huang C-S, Huober J, Hussein K, Jassem J, Jiang Z, Karlsson P. Morrow M, Orecchia R, Osborne KC, Pagani O, Partridge AH, Pritchard K, Ro J, Rutgers EJT, Sedlmayer F, Semiglazov v, Shao Z, Smith I, Toi M, Tutt A, Viale G, Watanabe T, Whelan TJ, Xu B (2017) 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 28(8):1700–1712. https://doi.org/10.1093/annonc/mdx308

    Article  PubMed  Google Scholar 

  59. Mamounas EP, White JR, Bandos H, Julian TB, Kahn AJ, Shaitelman SF, Torres MA, McCloskey SA, Vicini FA, Ganz P, Paik S, Gupta N, Costantino JP, Curran WJ, Wolmark N (2014) NSABP B-51/RTOG 1304: randomized phase III clinical trial evaluating the role of postmastectomy chest wall and regional nodal XRT (CWRNRT) and post-lumpectomy RNRT in patients (pts) with documented positive axillary (Ax) nodes before neoadjuvant chemotherapy (NC) who convert to pathologically negative Ax nodes after NC. J Clin Oncol 32(15 Suppl):tps1141. https://doi.org/10.1200/jco.2014.32.15_suppl.tps1141

    Article  Google Scholar 

  60. Fisher ER, Wang J, Bryant J, Fisher B, Mamounas E, Wolmark N (2002) Pathobiology of preoperative chemotherapy: findings from the National Surgical Adjuvant Breast and Bowel (NSABP) protocol B-18. Cancer 95:681–695. https://doi.org/10.1002/cncr.10741

    Article  PubMed  Google Scholar 

  61. Wong SM, Almana N, Choi J, Hu J, Gagnon H, Natsuhara K, Shen AH, DeSantis S, Dominic L, Golshan M, Weiss A, Bellon J, Mittendorf EA, King TA (2019) Prognostic significance of residual axillary nodal micrometastases and isolated tumor cells after neoadjuvant chemotherapy for breast cancer. Ann Surg Oncol 26:3502–3509. https://doi.org/10.1245/s10434-019-07517-2

    Article  PubMed  Google Scholar 

  62. Tinterri C, Canavese G, Bruzzi P, Dozin B (2020) NEONOD 2: Rationale and design of a multicenter non-inferiority trial to assess the effect of axillary surgery omission on the outcome of breast cancer patients presenting only micrometastasis in the sentinel lymph node after neoadjuvant chemotherapy. Contemp Clin Trials Commun 17:100496. https://doi.org/10.1016/j.conctc.2019.100496

    Article  PubMed  Google Scholar 

  63. Boughey J, Haffty B, Buchholz T, Symmans WF, Hunt K, Armer J, Suman V 2016) Alliance A011202: a randomized phase III trial comparing axillary lymph node dissection to axillary radiation in breast cancer patients (cT1–3 N1) who have positive sentinel lymph node disease after receiving neoadjuvant chemotherapy. [Available from: https://www.allianceforclinicaltrialsinoncology.org; https://www.allianceforclinicaltrialsinoncology.org/main/cmsfile?cmsPath=/Public/Annual%20Meeting/files/GUnzeitig-CRP%20Breakout-Breast-Nov2016.pdf]. Accessed 03 March 2021

  64. Kantor O, Sipsy LM, Yao K, James TA (2018) A predictive model for axillary node pathologic complete response after neoadjuvant chemotherapy for breast cancer. Ann Surg Oncol 25:1304–1311. https://doi.org/10.1245/s10434-018-6345-5

    Article  PubMed  Google Scholar 

  65. Symmans WF, Wei C, Gould R, Yu X, Zhang Y, Liu M, Walls A, Bousamra A, Maheshwari R, Sinn B, Hunt K, Buchholz TA, Valero V, Buzdar AU, Yang W, Brewater AM, Moulder S, Pusztai L, Hatzis C (2017) Hortobagyi GN (2017) Long-term prognostic risk after neoadjuvant chemotherapy associated with residual cancer burden and breast cancer subtype. J Clin Oncol 35(10):1049–1060. https://doi.org/10.1200/JCO.2015.63.1010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Hamy AS, Darrigues L, Laas E, De Croze D, Topciu L, Lam GT, Evrevin C, Rozette S, Laot L, Lerebours F, Pierga J-Y, Osdoit M, Faron M, Feron-J-G LM, Reyal F (2020) Prognostic value of the Residual Cancer Burden index according to breast cancer subtype: validation on a cohort of BC patients treated by neoadjuvant chemotherapy. PLoS ONE 15(6):e0234191. https://doi.org/10.1371/journal.pone.0234191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Masuda N, Lee SJ, Ohtani S, Im YH, Lee ES, Yokota I, Katsumasa K, Im S-A, Park B-W, Kim S-B, Yanagita Y, Ohno S, Takao S, Aogi K, Iwata H, Jeong J, Kim A, Park K-H, Sasano H, Ohashi Y, Masakazu T (2017) Adjuvant capecitabine for breast cancer after preoperative chemotherapy. N Engl J Med 376:2147–2159. https://doi.org/10.1056/NEJMoa1612645

    Article  CAS  PubMed  Google Scholar 

  68. von Minckwitz G, Huang CS, Mano MS, Loibl S, Mamounas EP, Untch M, Wolmark N, Rastogi P, Scheeweiss A, Redondo A, Fischer HH, Jacot W, Conlin AK, Arce-Salinas C, Wapnir IL, Jackisch C, DiGiovanna MP, Fasching PA, Crown JP, Wulfing P, Shao Z, Caremole ER, Wu H, Lam LH, Tesarowski D, Smitt M, Southwaite H, Singel S, Geyer CE Jr, KATHERINE investigators, (2019) Trastuzumab emtansine for residual invasive HER2-positive breast cancer. N Engl J Med 380:617–628. https://doi.org/10.1056/NEJMoa1814017

    Article  Google Scholar 

  69. Pinder SE, Rakha EA, Purdie CA, Bartlett JM, Francis A, Stein RC, Thompson AM, Shaaban A; Translational Subgroups of the NCRI Clinical Studies Group (2015) Macroscopic handling and reporting of breast cancer specimens pre- and post-neoadjuvant chemotherapy treatment: review of pathological issues and suggested approaches. Histopathology 67:279–293. https://doi.org/10.1111/his.12649

    Article  Google Scholar 

  70. Sahoo S, Lester SC (2009) Pathology of breast carcinomas after neoadjuvant chemotherapy: an overview with recommendations on specimen processing and reporting. Arch Pathol Lab Med 133:633–642. https://doi.org/10.1043/1543-2165-133.4.633

    Article  PubMed  Google Scholar 

  71. Barrio AV, Mamtani A, Edelweiss M, Eaton A, Stempel M, Murray MP, Morrow M (2016) How often is treatment effect identified in axillary nodes with a pathologic complete response after neoadjuvant chemotherapy? Ann Surg Oncol 23:3475–3480. https://doi.org/10.1245/s10434-016-5463-1

    Article  PubMed  PubMed Central  Google Scholar 

  72. Ellis IO, Carder P, Hales S, Lee AHS, Pinder SE, Rakha E, Stephenson T, Al-Sam S, Deb R, Hanby A, Liebmann R, Provenzano E, Rowlands D, Wells CA, Anderson A, Girling A, Ibrahim M, Mallon E, Quinn C. Pathology reporting of breast disease in surgical excision specimens incorporating the dataset for histological reporting of breast cancer. https://www.rcpath.org/uploads/assets/7763be1c-d330-40e8-95d08f955752792a/G148_BreastDataset-hires-Jun16.pdf. Accessed 06 March 2021

  73. Symmans F PS, Lester S, Kulka J. Post-therapy effects. In: Lakhani SR EI, Schnitt SJ, Tan PH, van de Vijver MJ editor (2012) WHO classification of tumours of the breast. 4th ed. Lyons, IARC. 24–26.

  74. Residual Cancer Burden calculator and associated documents (guide for measuring cancer cellularity, examples of gross and microscopic evaluation, pathology protocol for macroscopic and microscopic evaluation of RCB). http://www3.mdanderson.org/app/medcalc/index.cfm?pagename=jsconvert3. Accessed 06 March 2021.

Download references

Acknowledgements

The authors are greatly indebted to and acknowledge the help of those friends and colleagues who have circulated and filled in the questionnaires and also to all pathologists who have contributed by returning the forms. Contributors are acknowledged by name and country in Supplementary material 4. Beside these contributors, we are also grateful to Drs. Orsolya Serfőző and Éva Ambrózay for the radiological images and David Murphy for drawing Figs. 2 and 5.

Author information

Authors and Affiliations

  1. Department of Pathology, Bács-Kiskun County Teaching Hospital, Kecskemét, Hungary

    Gábor Cserni

  2. Department of Pathology, University of Szeged, Szeged, Hungary

    Gábor Cserni

  3. Department of Histopathology, Breast Check, Irish National Breast Screening Programme & St. Vincent’s University Hospital, Dublin, Ireland

    Aoife Maguire

  4. Department of Health Sciences, Division of Pathological Anatomy, University of Florence, Florence, Italy

    Simonetta Bianchi

  5. The Fingerland Department of Pathology, Charles University Medical Faculty Hospital, Hradec Kralove, Czech Republic

    Ales Ryska

  6. Department of Clinical Pathology, Sahlgrenska University Hospital, Gothenburg, Sweden

    Anikó Kovács

Authors
  1. Gábor Cserni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aoife Maguire
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simonetta Bianchi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ales Ryska
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anikó Kovács
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

G.Cs. and A.M. have drafted the manuscript; G.Cs., A.M., and S.B. have contributed the figures; all authors have contributed in answering and spreading the questionnaires; all authors have commented the draft manuscript on multiple occasions, and approved the final version submitted.

Corresponding author

Correspondence to Gábor Cserni.

Ethics declarations

Ethics approval

No ethical approval was deemed necessary for this review.

Consent to participate

Not applicable.

Consent for publication

There is no item requiring such a consent.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cserni, G., Maguire, A., Bianchi, S. et al. Sentinel lymph node assessment in breast cancer—an update on current recommendations. Virchows Arch 480, 95–107 (2022). https://doi.org/10.1007/s00428-021-03128-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00428-021-03128-z

Keywords

Search

Navigation