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Annals of Surgical Oncology

, Volume 23, Issue 10, pp 3354–3364 | Cite as

A Population-Based Study of the Effects of a Regional Guideline for Completion Axillary Lymph Node Dissection on Axillary Surgery in Patients with Breast Cancer

  • Miriam W. Tsao
  • Sylvie D. Cornacchi
  • Nicole Hodgson
  • Marko Simunovic
  • Lehana Thabane
  • Ji Cheng
  • Mary Ann O’Brien
  • Barbara Strang
  • Som D. Mukherjee
  • Peter J. Lovrics
Breast Oncology

Abstract

Introduction

Evidence from the American College of Surgeons Oncology Group (ACOSOG) Z0011 trial suggests completion axillary lymph node dissection (cALND) after positive sentinel lymph node biopsy (+SLNB) does not improve outcomes in select patients, leading to practice variation. A multidisciplinary group of surgeons, oncologists, and pathologists developed a regional guideline for cALND which was disseminated in August 2012. We assessed the impact of Z0011 and the regional guideline on cALND rates.

Methods

Consecutive invasive breast cancer cases undergoing SLNB were reviewed at 12 hospitals. Patient, tumor, and process measures were collected for three time periods: TP1, before publication of Z0011 (May 2009–August 2010); TP2, after publication of Z0011 (March 2011–June 2012); and TP3, after guideline dissemination (January 2013–April 2014). Cases were categorized by whether they met the guideline criteria for cALND (i.e. ≤50 years, mastectomy, T3 tumor, three or more positive sentinel lymph nodes [SLNs]) or not (e.g. age > 50 years, breast-conserving surgery, T1/T2 tumor, and one to two positive SLNs).

Results

The SLNB rate increased from 56 % (n = 620), to 70 % (n = 774), to 78 % (n = 844) in TP1, TP2, and TP3, respectively. Among cases not recommended for cALND using the guideline criteria, cALND rates decreased significantly over time (TP1, 71 %; TP2, 43 %; TP3, 17 %) [p < 0.001]. The cALND rate also decreased over time among cases recommended to have cALND using the guideline criteria (TP1, 92 %; TP2, 69 %; TP3, 58 %) [p < 0.001]. Based on multivariable analysis, age and nodal factors appeared to be significant factors for cALND decision making.

Conclusion

Publication of ACOSOG Z0011 and regional guideline dissemination were associated with a marked decrease in cALND after +SLNB, even among several cases in which the guideline recommended cALND.

Keywords

Breast Cancer Sentinel Lymph Node Biopsy Axillary Lymph Node Dissection Lymph Node Ratio Positive Sentinel Lymph Node 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgment

The authors would like to thank Dyda Dao, Dominika Bhatia, and Olivia Lovrics for their assistance with data collection and management.

Funding

Funding was provided by the Hamilton Academic Health Sciences Organization (HAHSO) Innovation Grant, and by funds from the Department of Surgery, McMaster University and the McMaster Buffet Taylor Breast Cancer Research Chair, Department of Oncology, McMaster University. The funding sources played no role in the design, conduct, or reporting of this study.

Disclosure

Miriam W. Tsao, Sylvie D. Cornacchi, Nicole Hodgson, Marko Simunovic, Lehana Thabane, Ji Cheng, Mary Ann O’Brien, Barbara Strang, Som D. Mukherjee, and Peter J. Lovrics have no conflicts of interest to disclose.

References

  1. 1.
    Krag DN, Anderson SJ, Julian TB, et al. 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 randomized phase 3 trial. Lancet Oncol. 2010;11:927–33.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Purushotham AD, Upponi S, Klevesath MB, et al. Morbidity after sentinel lymph node biopsy in primary breast cancer: results from a randomized controlled trial. J Clin Oncol. 2005;23(19):4312–21.CrossRefPubMedGoogle Scholar
  3. 3.
    The American Society of Breast Surgeons Board of Directors. Position statement on management of the axilla in patients with invasive breast cancer. https://www.breastsurgeons.org/statements/index.php. Accessed 22 June 2016.
  4. 4.
    Lyman GH, Giuliano AE, Omerfield MR, et al. American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol. 2005;23:7703–20.CrossRefPubMedGoogle Scholar
  5. 5.
    George R, Quan ML, McCready D, et al. Expert panel on SLNB in breast cancer. Sentinel lymph node biopsy in early-stage breast cancer. Toronto, ON: Cancer Care Ontario, Jul 14 2009. Program in Evidence-Based Care Evidence-Based Series No.: 17–5. https://www.cancercare.on.ca/common/pages/UserFile.aspx?fileId=45870. Accessed 22 June 2016.
  6. 6.
    Anampa J, Makower D, Sparano JA. Progress in adjuvant chemotherapy for breast cancer: an overview. BMC Med. 2015;13:195.CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Giuliano AE, Hunt KK, Ballman KV, et al. Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA. 2011;305:569–75.CrossRefPubMedGoogle Scholar
  8. 8.
    Caudle AS, Hunt KK, Kuerer HM, et al. Multidisciplinary considerations in the implementation of the findings from the American College of Surgeons Oncology Group (ACOSOG) Z0011 study: a practice-changing trial. Ann Surg Oncol. 2011;18(9):2407–12.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Barry JM, Weber WP, Sacchini V. The evolving role of axillary lymph node dissection in the modern era of breast cancer management. Surg Oncol. 2012;21:143–5.CrossRefPubMedGoogle Scholar
  10. 10.
    Nakamura S. Axillary lymph node dissection in sentinel node positive breast cancer: is it necessary? Curr Opin Obstet Gynecol. 2013. doi: 10.1097/GCO.0b013e32834f3608.PubMedGoogle Scholar
  11. 11.
    Latosinsky S, Berrand TS, Cutter CS, et al. Axillary dissection versus no axillary dissection in women with invasive breast cancer and sentinel node metastasis. Can J Surg. 2012;55:66–69.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Giuliano AE, Morrow M, Duggal S, et al. Should ACOSOG Z0011 change practice with respect to axillary lymph node dissection for a positive sentinel lymph node biopsy in breast cancer? Clin Exp Metastasis. 2012;29:687–92.CrossRefPubMedGoogle Scholar
  13. 13.
    Voutsadakis IA, Spadafora S. Axillary lymph node management in breast cancer with positive sentinel lymph node biopsy. World J Clin Oncol. 2015;6(1):1–6.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Galimberti V, Chifu C, Perez SR, et al. Positive axillary sentinel lymph node: is axillary dissection always necessary? Breast. 2011;20(Suppl 3):S96–8.CrossRefPubMedGoogle Scholar
  15. 15.
    Morrow M, Giuliano AE. To cut is to cure: can we really apply Z11 in practice? Ann Surg Oncol. 2011;18:2413–5.CrossRefPubMedGoogle Scholar
  16. 16.
    Cody HS III, Houssami N. Axillary management in breast cancer: what’s new for 2012? Breast. 2012;21(3):411–5.CrossRefPubMedGoogle Scholar
  17. 17.
    Caudle AS, Hunt KK, Tucker SL, et al. American College of Surgeons Oncology Group (ACOSOG) Z0011: impact on surgeon practice patterns. Ann Surg Oncol. 2012;19(10):3144–51.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Joyce DP, Lowery AJ, McGrath-Soo LB, et al. Management of the axilla: has Z0011 had an impact? Ir J Med Sci. 2016;185(1):145–9.CrossRefPubMedGoogle Scholar
  19. 19.
    Wright GP, Mater ME, Sobel HL, et al. Measuring the impact of the American College of Surgeons Oncology Group Z0011 trial on breast cancer surgery in a community healthy system. Am J Surg. 2015;209:240–5.CrossRefPubMedGoogle Scholar
  20. 20.
    Jamtvedt G, Young JM, Kristoffersen DT, et al. Does telling people what they have been doing change what they do? A systematic review of the effects of audit and feedback. Qual Saf Health Care. 2006;15:433–6.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Grimshaw J, Eccles M, Walter A, et al. Changing physician’s behaviour; what works and thoughts on getting more things to work. J Cont Educ Health Prof. 2002;22:237–43.CrossRefGoogle Scholar
  22. 22.
    Flodgren G, Parmelli E, Doumit G, et al. Local opinion leaders: effects on professional practice and health care outcomes. Cochrane Database Syst Rev. 2011. doi: 10.1002/14651858.CD000125.pub4.Google Scholar
  23. 23.
    Forsetlund L, Bjorndal A, Rashidian A, et al. Continuing education meetings and workshops: effects on professional practice and health care outcomes. Cochrane Database Syst Rev. 2009. doi: 10.1002/14651858.CD003030.pub2.PubMedGoogle Scholar
  24. 24.
    O’Brien MA, Oxman AD, Davis DA, et al. Educational outreach visits: effects on professional practice and health care outcomes. Cochrane Database Syst Rev. 2007;(2):CD000409.Google Scholar
  25. 25.
    American Society of Breast Surgeons. Performance and practice guidelines for axillary lymph node dissection in breast cancer patients—Nov. 2014. https://www.breastsurgeons.org/new_layout/about/statements/PDF_Statements/PerformancePracticeGuidelines_ALND.pdf. Accessed Dec 2015.
  26. 26.
    Lyman GH, Temin S, Edge S, et al. Sentinel lymph node biopsy for patients with early-stage breast cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2014;32:1365–86.CrossRefPubMedGoogle Scholar
  27. 27.
    National Comprehensive Cancer Network. NCCN Clinical Practice Guidelines in Oncology V3.2015. www.consensocancermamario.com/guias/NCCN_2015.pdf. Accessed 23 June 2016.
  28. 28.
    Lovrics PJ, Hodgson N, O’Brien MA, et al. Results of a surgeon-directed quality improvement project on breast cancer surgery outcomes in South-Central Ontario. Ann Surg Oncol. 2014;21:2181–7.CrossRefPubMedGoogle Scholar
  29. 29.
    Tsao MW, Cornacchi SD, Lovrics PJ, et al. Factors affecting the implementation of a regional guideline for completion axillary lymph node dissection: a qualitative study of physician opinions. Canadian Centre for Applied Research in Cancer Control (ARCC) Conference 2016, Toronto, ON. 2016. http://cc-arcc.ca/wpcontent/uploads/2015/12/Final-Web-ARCC-Program.pdf. Accessed 22 June 2016.
  30. 30.
    Fisher B, Redmond C, Fisher ER, et al. Ten-year results of a randomized clinical trial comparing radical mastectomy and total mastectomy with or without radiation. N Engl J Med. 1985;312(11):674–81.CrossRefPubMedGoogle Scholar
  31. 31.
    Gatzemeier W, Mann GB. Which sentinel lymph-node (SLN) positive breast cancer patient needs an axillary lymph-node dissection (ALND)—ACOSOG Z0011 results and beyond. Breast J. 2013;22(3):211–6.CrossRefGoogle Scholar
  32. 32.
    Goyal A, Dodwell D, Reed MW, et al. Axillary treatment in women with one or two sentinel nodes with macrometastases: more evidence is needed to inform practice. J Clin Oncol. 2014;32:3902.CrossRefPubMedGoogle Scholar
  33. 33.
    Doherty S. History of evidence-based medicine. Oranges, chloride of lime and leeches: barriers to teaching old dogs new tricks. Emerg Med Australas. 2005;17:314–21.Google Scholar
  34. 34.
    Langer I, Guller U, Berclaz G, et al. Morbidity of sentinel lymph node biopsy (SLN) alone versus SLN and completion axillary lymph node dissection after breast cancer surgery: a prospective Swiss multicenter study on 659 patients. Ann Surg. 2007;245(3):452–61.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Yi M, Giordano SH, Meric-Bernstam F, et al. 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. 2010;17:343–51.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Bilimoria KY, Bentrem DJ, Hansen NM, et al. Comparison of sentinel lymph node biopsy alone and completion axillary lymph node dissection for node-positive breast cancer. J Clin Oncol. 2009;27(18):2946–53.CrossRefPubMedGoogle Scholar
  37. 37.
    Van Der Hage JA, Van de Velde JP, Tubiana-Hulin M, et al. Preoperative chemotherapy in primary operable breast cancer: results from the European Organization for Research and Treatment of Cancer trial 10902. J Clin Oncol. 2001;19:4224–37.PubMedGoogle Scholar
  38. 38.
    Donker M, Van Tienhoven G, Straver ME, et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): a randomized, multicenter, open-label, phase 3 non-inferiority trial. Lancet Oncol. 2014;15(12):1303–10.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Li CZ, Zhang P, Li RW, et al. Axillary lymph node dissection versus sentinel lymph node biopsy alone for early breast cancer with sentinel node metastasis: a meta-analysis. Eur J Surg Oncol. 2015;41:958–66.CrossRefPubMedGoogle Scholar
  40. 40.
    Wang J, Mittendorf EA, Sahin AA, et al. Outcomes of sentinel lymph node dissection alone vs. axillary lymph node dissection in early stage invasive lobular carcinoma: a retrospective study of the surveillance, epidemiology and end results (SEER) database. PLoS One. 2014;9:e89778.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Zakaria S, Degnim AC, Kleer CG, et al. Sentinel lymph node biopsy for breast cancer: how many nodes are enough? J Surg Oncol. 2007;96:554–9.CrossRefPubMedGoogle Scholar
  42. 42.
    Lee MK, Varzi LA, Chung DU, et al. The effect of young age in hormone receptor positive breast cancer. Biomed Res Int. 2015;2015:325715.PubMedPubMedCentralGoogle Scholar
  43. 43.
    Woolf SH, Grol R, Hutchinson A, et al. Clinical guidelines: potential benefits, limitations, and harms of clinical guidelines. BMJ. 1999;318:527–30.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Natsch S, van der Meer JWM. The role of clinical guidelines, policies and stewardship. J Hosp Infect. 2003;53(3):172–6.CrossRefPubMedGoogle Scholar

Copyright information

© Society of Surgical Oncology 2016

Authors and Affiliations

  • Miriam W. Tsao
    • 1
  • Sylvie D. Cornacchi
    • 1
  • Nicole Hodgson
    • 1
    • 2
  • Marko Simunovic
    • 1
    • 2
    • 3
  • Lehana Thabane
    • 3
    • 4
  • Ji Cheng
    • 4
  • Mary Ann O’Brien
    • 5
  • Barbara Strang
    • 6
  • Som D. Mukherjee
    • 6
  • Peter J. Lovrics
    • 1
    • 2
    • 7
  1. 1.Department of SurgeryMcMaster UniversityHamiltonCanada
  2. 2.Department of Surgical OncologyHamilton Health Sciences and Juravinski Hospital and Cancer CentreHamiltonCanada
  3. 3.Department of Clinical Epidemiology and BiostatisticsMcMaster UniversityHamiltonCanada
  4. 4.Biostatistics UnitSt. Joseph’s HealthcareHamiltonCanada
  5. 5.Department of Family and Community MedicineUniversity of TorontoTorontoCanada
  6. 6.Department of OncologyMcMaster UniversityHamiltonCanada
  7. 7.Department of SurgerySt. Joseph’s HealthcareHamiltonCanada

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