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The impact of preoperative axillary ultrasonography in T1 breast tumours

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European Radiology Aims and scope Submit manuscript

Abstract

Objectives

To (a) determine the diagnostic validity of axillary ultrasound (AUS) in pT1 tumours and whether fine-needle aspiration (FNA) improves its diagnostic performance, and (b) determine the negative predictive value (NPV) of AUS in a simulation environment (cutoff: two lymph nodes with macrometastases) in patients fulfilling American College of Surgeons Oncology Group (ACOSOG) Z0011 criteria.

Materials and methods

This retrospective multicentre cross-sectional study analysed diagnostic accuracy in 355 pT1 breast cancers. All patients underwent AUS; visible nodes underwent FNA regardless of their AUS appearance. Sentinel node biopsy and axillary lymph node dissection (ALND) were gold standards. Data were analysed considering micrometastases ‘positive’ and considering micrometastases ‘N negative’. The simulation environment included all patients fulfilling ACOSOG Z0011 criteria.

Results

Axillary involvement: 22.8 %; AUS sensitivity: 46.9 % (Nmic positive)/66.7 % (Nmic negative); AUS+FNA sensitivity: 52.6 % (pNmic positive)/72.0 % (pNmic negative). In the simulation environment, AUS had 75.0 % sensitivity, 88.9 % specificity and 99.2 % NPV.

Conclusion

AUS has moderate sensitivity in T1 tumours. As ALND is unnecessary in micrometastases, considering micrometastases ‘N negative’ increases the practical impact of AUS.

In patients fulfilling ACOSOG Z0011 criteria, AUS alone can predict cases unlikely to benefit from ALND.

Key Points

AUS+FNA can predict axillary involvement, thus avoiding SNB.

Not all patients with axillary involvement need ALND.

Axillary tumour load determines axillary management.

AUS could classify patients according to axillary load.

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Abbreviations

ALND:

Axillary lymph node dissection

AUS:

Axillary ultrasound

BCS:

Breast-conserving surgery

FNA:

Fine-needle aspiration

PLN:

Palpable lymph node

SNB:

Sentinel node biopsy

WBRT:

Whole-breast radiotherapy

References

  1. Veronesi U, Paganelli G, Viale G et al (2006) Sentinel-lymph-node biopsy as a staging procedure in breast cancer: update of a randomised controlled study. Lancet Oncol 7:983–990

    Article  PubMed  Google Scholar 

  2. Caudle AS, Cupp JA, Kuerer HM (2014) Management of axillary disease. Surg Oncol Clin N Am 23:473–486

    Article  PubMed  Google Scholar 

  3. Van der Ploeg IMC, Nieweg OE, van Rijk MC et al (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

    Article  PubMed  Google Scholar 

  4. Kell MR, Burke JP, Barry M, Morrow M (2010) Outcome of axillary staging in early breast cancer: a meta-analysis. Breast Cancer Res Treat 120:441–447

    Article  PubMed  Google Scholar 

  5. Mansel RE, Fallowfield L, Kissin M et al (2006) Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC Trial. J Natl Cancer Inst 98:599–609

    Article  PubMed  Google Scholar 

  6. Jeruss JS, Winchester DJ, Sener SF et al (2005) Axillary recurrence after sentinel node biopsy. Ann Surg Oncol 12:34–41

    Article  PubMed  Google Scholar 

  7. Krag DN, Anderson SJ, Julian TB et al (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

    Article  PubMed  PubMed Central  Google Scholar 

  8. Giuliano AE, McCall L, Beitsch P et al (2010) Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: the American College of Surgeons Oncology Group Z0011 randomized trial. Ann Surg 252:426–432, discussion 432–3

    PubMed  Google Scholar 

  9. Moorman AM, Bourez RLJH, Heijmans HJ, Kouwenhoven EA (2014) Axillary ultrasonography in breast cancer patients helps in identifying patients preoperatively with limited disease of the axilla. Ann Surg Oncol. doi:10.1245/s10434-014-3674-x

    PubMed  Google Scholar 

  10. Baré M, Bonfill X, Andreu X (2006) Relationship between the method of detection and prognostic factors for breast cancer in a community with a screening programme. J Med Screen 13:183–191

    PubMed  Google Scholar 

  11. Dengel LT, Van Zee KJ, King TA et al (2014) Axillary dissection can be avoided in the majority of clinically node-negative patients undergoing breast-conserving therapy. Ann Surg Oncol 21:22–27

    Article  PubMed  PubMed Central  Google Scholar 

  12. Cianfrocca M (2004) Prognostic and predictive factors in early-stage breast cancer. Oncologist 9:606–616

    Article  PubMed  Google Scholar 

  13. Agresti R, Martelli G, Sandri M et al (2014) Axillary lymph node dissection versus no dissection in patients with T1N0 breast cancer: a randomized clinical trial (INT09/98). Cancer 120:885–893

    Article  CAS  PubMed  Google Scholar 

  14. Giuliano AE, Han SH (2011) Local and regional control in breast cancer: role of sentinel node biopsy. Adv Surg 45:101–116

    Article  PubMed  Google Scholar 

  15. Pilewskie ML, Morrow M (2014) Management of the clinically node-negative axilla: what have we learned from the clinical trials? Oncology (Williston Park) 28:371–378

    Google Scholar 

  16. Gangi A, Mirocha J, Leong T, Giuliano AE (2014) Triple-negative breast cancer is not associated with increased likelihood of nodal metastases. Ann Surg Oncol 21:4098–4103

    Article  PubMed  Google Scholar 

  17. Donker M, Van Tienhoven G, Straver ME et al (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. Lancet Oncol 15:1303–1310

    Article  PubMed  PubMed Central  Google Scholar 

  18. Houssami N, Diepstraten SCE, Cody HS et al (2014) Clinical utility of ultrasound-needle biopsy for preoperative staging of the axilla in invasive breast cancer. Anticancer Res 34:1087–1097

    PubMed  Google Scholar 

  19. Van Rijk MC, Deurloo EE, Nieweg OE et al (2006) Ultrasonography and fine-needle aspiration cytology can spare breast cancer patients unnecessary sentinel lymph node biopsy. Ann Surg Oncol 13:31–35

    Article  PubMed  Google Scholar 

  20. Park SH, Kim MJ, Park B-W et al (2011) Impact of preoperative ultrasonography and fine-needle aspiration of axillary lymph nodes on surgical management of primary breast cancer. Ann Surg Oncol 18:738–744

    Article  PubMed  Google Scholar 

  21. Torres Sousa MY, Illescas Banegas M, Rozas Rodríguez ML et al (2011) Preoperative staging of axillary lymph nodes in breast cancer: ultrasonographic parameters and ultrasound-guided core needle biopsy. Radiologia 53:544–551

    Article  CAS  PubMed  Google Scholar 

  22. Houssami N, Ciatto S, Turner RM et al (2011) Preoperative ultrasound-guided needle biopsy of axillary nodes in invasive breast cancer: meta-analysis of its accuracy and utility in staging the axilla. Ann Surg 254:243–251

    Article  PubMed  Google Scholar 

  23. Diepstraten SCE, Sever AR, Buckens CFM et al (2014) Value of preoperative ultrasound-guided axillary lymph node biopsy for preventing completion axillary lymph node dissection in breast cancer: a systematic review and meta-analysis. Ann Surg Oncol 21:51–59

    Article  PubMed  Google Scholar 

  24. Alvarez S, Añorbe E, Alcorta P et al (2006) Role of sonography in the diagnosis of axillary lymph node metastases in breast cancer: a systematic review. AJR Am J Roentgenol 186:1342–1348

    Article  PubMed  Google Scholar 

  25. Altomare V, Guerriero G, Carino R et al (2007) Axillary lymph node echo-guided fine-needle aspiration cytology enables breast cancer patients to avoid a sentinel lymph node biopsy. Preliminary experience and a review of the literature. Surg Today 37:735–739

    Article  PubMed  Google Scholar 

  26. Reyna C, Lee MC, Frelick A et al (2014) Axillary burden of disease following false- negative preoperative axillary evaluation. Am J Surg 208:577–581

  27. Galimberti V, Cole BF, Zurrida S et al (2013) Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23-01): a phase 3 randomised controlled trial. Lancet Oncol 14:297–305

    Article  PubMed  PubMed Central  Google Scholar 

  28. Hansen NM, Grube B, Ye X et al (2009) Impact of micrometastases in the sentinel node of patients with invasive breast cancer. J Clin Oncol 27:4679–4684

    Article  PubMed  Google Scholar 

  29. Galimberti V, Botteri E, Chifu C et al (2012) Can we avoid axillary dissection in the micrometastatic sentinel node in breast cancer? Breast Cancer Res Treat 131:819–825

    Article  PubMed  Google Scholar 

  30. Giuliano AE, Hunt KK, Ballman KV et al (2011) Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 305:569–575

    Article  CAS  PubMed  Google Scholar 

  31. Yi M, Giordano SH, Meric-Bernstam F et al (2010) Trends in and outcomes from sentinel lymph node biopsy (SLNB) alone vs. SLNB with axillary lymph node dissection for node-positive breast cancer patients: experience from the SEER database. Ann Surg Oncol 17:343–351

    Article  PubMed  PubMed Central  Google Scholar 

  32. Bilimoria KY, Bentrem DJ, Hansen NM et al (2009) Comparison of sentinel lymph node biopsy alone and completion axillary lymph node dissection for node-positive breast cancer. J Clin Oncol. doi:10.1200/JCO.2008.19.5750

    Google Scholar 

  33. Caudle AS, Hunt KK, Tucker SL et al (2012) American College of Surgeons Oncology Group (ACOSOG) Z0011: impact on surgeon practice patterns. Ann Surg Oncol 19:3144–3151

    Article  PubMed  PubMed Central  Google Scholar 

  34. Boughey JC (2014) Axillary dissection can be avoided in the majority of clinically node-negative patients undergoing breast-conserving therapy, by Dengel et al. Ann Surg Oncol 21:8–10

    Article  PubMed  Google Scholar 

  35. Cody HS, Houssami N (2012) Axillary management in breast cancer: what’s new for 2012? Breast 21:411–415

    Article  PubMed  Google Scholar 

  36. Caudle AS, Kuerer HM, Le-Petross HT et al (2014) Predicting the extent of nodal disease in early-stage breast cancer. Ann Surg Oncol. doi:10.1245/s10434-014-3813-4

    Google Scholar 

  37. Gentilini O, Veronesi U (2012) Abandoning sentinel lymph node biopsy in early breast cancer? A new trial in progress at the European Institute of Oncology of Milan (SOUND: sentinel node vs observation after axillary UltraSouND). Breast 21:678–681

    Article  PubMed  Google Scholar 

  38. Ahmed M, Usiskin SI, Hall-Craggs MA, Douek M (2014) Is imaging the future of axillary staging in breast cancer? Eur Radiol 24:288–293

    Article  CAS  PubMed  Google Scholar 

  39. Dialani V, James DF, Slanetz PJ (2015) A practical approach to imaging the axilla. Insights Imaging. doi:10.1007/s13244-014-0367-8

    PubMed  PubMed Central  Google Scholar 

  40. Klinger S, Marchal F, Rauch P, Kenouchi O, Chrétien SGP (2013) Using one-step nucleic acid amplification (OSNA) for intraoperative detection of lymph node metastasis and accelerates initiation of adjuvant therapy. Ann Oncol 24:2305–2309

    Article  Google Scholar 

  41. Cheang MCU, Chia SK, Voduc D et al (2009) Ki67 index, HER2 status, and prognosis of patients with luminal B breast cancer. doi:10.1093/jnci/djp082

  42. Garcia-Ortega MJ, Benito MA, Vahamonde EF et al (2009) Pretreatment axillary ultrasonography and core biopsy in patients with suspected breast cancer: diagnostic accuracy and impact on management. Eur J Radiol 79:64–72

    Article  Google Scholar 

  43. Gradishar WJ, Anderson BO, Blair SL et al (2014) Breast cancer version 3.2014. J Natl Compr Canc Netw 12:542–590

    CAS  PubMed  Google Scholar 

  44. Mainiero MB, Cinelli CM, Koelliker SL et al (2010) Axillary ultrasound and fine-needle aspiration in the preoperative evaluation of the breast cancer patient: an algorithm based on tumor size and lymph node appearance. AJR Am J Roentgenol 195:1261–1267

    Article  PubMed  Google Scholar 

  45. Lyman GH, Temin S, Edge SB et al (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

    Article  PubMed  Google Scholar 

  46. Schipper RJ, van Roozendaal LM, de Vries B et al (2013) Axillary ultrasound for preoperative nodal staging in breast cancer patients: is it of added value? Breast 22:1108–1113

    Article  CAS  PubMed  Google Scholar 

  47. Amonkar S, Oates E, McLean L, Nicholson S (2013) Operative staging of the axilla in primary breast cancer. By redefining the abnormal appearing node can we reduce investigations without affecting overall treatment? Breast 22:1114–1118

    Article  CAS  PubMed  Google Scholar 

  48. Rao R, Euhus D, Mayo HG, Balch C (2013) Axillary node interventions in breast cancer: a systematic review. JAMA 310:1385–1394

    Article  CAS  PubMed  Google Scholar 

  49. Verheuvel NC, van den Hoven I, Ooms HWA et al (2015) The role of ultrasound-guided lymph node biopsy in axillary staging of invasive breast cancer in the post-ACOSOG Z0011 trial era. Ann Surg Oncol 22:409–415

    Article  CAS  PubMed  Google Scholar 

  50. Boone BA, Huynh C, Spangler ML et al (2015) Axillary lymph node burden in invasive breast cancer: a comparison of the predictive value of ultrasound-guided needle biopsy and sentinel lymph node biopsy. Clin Breast Cancer 1–6

  51. Roy PG, Chan SM, Ng V et al (2014) Risk stratification of patients with early breast cancer. Clin Breast Cancer 14:68–73

    Article  PubMed  Google Scholar 

  52. Farrell TPJ, Adams NC, Stenson M, Carroll PA (2015) The Z0011 Trial: is this the end of axillary ultrasound in the pre-operative assessment of breast cancer patients? Eur Radiol. doi:10.1007/s00330-015-3683-6

    PubMed  Google Scholar 

  53. Britton PD, Goud A, Godward S et al (2009) Use of ultrasound-guided axillary node core biopsy in staging of early breast cancer. Eur Radiol 19:561–569

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Other members of the GMVOB include: L.Tortajada, MD; M. Villajos, MD; S. Ganau, MD; F. Escribano, MD; A. Martín, MD; E. Picas, MD; N. Martinez, MD; S. Santos, MD; I. Romero, MD; J. Planas, MD; J. de Torres, MD; A. Reñé, MD; P. Palañá, MD.

We thank Xavier Andreu, MD PhD, for his great help in writing up the pathology analysis and John Giba for help with English.

The scientific guarantor of this publication is Melcior Sentís, MD, Head of Department. Women’s Imaging. Department of Radiology. UDIAT Centre Diagnòstic. Institut Universitari Parc Taulí – UAB. The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article. The authors state that this work has not received any funding. Marisa Baré, MD, PhD, epidemiologist at the Clinical Epidemiology Unit and Screening Office kindly provided statistical advice for this manuscript.

Each institution’s review board approved the study. Written informed consent was not required for this study because the data analyzed were collected as part of the routine protocols in force at each institution. Methodology: retrospective, diagnostic or prognostic study, multicentre study.

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Correspondence to Javier del Riego.

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Fig. 2

Clinical management for the entire series (GIF 143 kb)

High resolution image (TIFF 1520 kb)

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del Riego, J., Diaz-Ruiz, M.J., Teixidó, M. et al. The impact of preoperative axillary ultrasonography in T1 breast tumours. Eur Radiol 26, 1073–1081 (2016). https://doi.org/10.1007/s00330-015-3901-2

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  • DOI: https://doi.org/10.1007/s00330-015-3901-2

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