[Skip to Content]
Sign In
Individual Sign In
Create an Account
Institutional Sign In
OpenAthens Shibboleth
[Skip to Content Landing]
Views 1,531
Citations 0
Invited Commentary
July 12, 2018

Delayed Adoption of Evidence-Based Breast Cancer Surgical PracticesHistory Repeats Itself

Author Affiliations
  • 1Department of Surgery, University of Washington, Seattle
  • 2Department of Global Health-Medicine, University of Washington, Seattle
JAMA Oncol. Published online July 12, 2018. doi:10.1001/jamaoncol.2018.1939

Management of the axilla has arguably evolved more rapidly than any other area of breast surgery over the past 20 years. Sentinel lymph node (SLN) biopsy superseded axillary lymph node dissection (ALND) for staging the clinically negative axilla and was adopted as the standard of care in the early 2000s after several single-institution and multicenter trials demonstrated test equivalence of SLN biopsy to ALND for axillary staging among patients with early-stage disease.

Skepticism endured that patients with node-positive, clinically negative axillae could safely undergo SLN biopsy alone, recalling the outcome of the National Surgical Adjuvant Breast and Bowel Project (NSABP) B-04 randomized trial from the 1970s in which half of the women with node-positive tumors who did not undergo ALND or axillary irradiation developed axillary recurrences at a median of 15 months after surgery. So when the American College of Surgeons Oncology Group Z0011 trial was published in 2011, showing that women with clinical T1-2N0 breast cancer undergoing breast-conserving therapy (BCT) with 1 to 2 positive SLNs could forego ALND without detriment to survival or locoregional recurrence risk, this initial report received criticism for inadequate follow-up (6 years).

Subsequent prospective randomized trials similarly found that SLN biopsy alone is sufficient for patients with clinically node-negative cancer when axillary irradiation is given (AMAROS [After Mapping of the Axilla: Radiotherapy or Surgery?]1 and International Breast Cancer Study Group Trial 23-012 trials), lending further credence to support the omission of ALND among patients undergoing BCT who had limited axillary SLN metastases.

In 2016, updated results from Z11 confirmed that 10-year locoregional recurrence remained equivalent in women who underwent SLN biopsy alone vs ALND (5.3% vs 6.2%, respectively, P = .28).3 Nonetheless, the degree to which this practice favoring reduction in therapy (ALND) has been accepted and adopted in the surgical community outside of major academic medical centers has remained uncertain.4

In this issue of JAMA Oncology, Morrow and colleagues5 sought to assess surgeon perspectives regarding the omission of ALND in the post-Z0011 era and determine how these perspectives relate to surgical specialty, geographic location of practice, case volume, and involvement in multidisciplinary breast cancer care. They also compared the association of surgical attitudes regarding axillary surgery with adoption of other changing breast surgical practices (in this case, acceptance of no ink on tumor as a negative margin). Of 488 invited surgeons who cared for 5080 patients with stage I/II cancer treated between 2013 and 2015 in either the Georgia or Los Angeles Surveillance, Epidemiology, and End Results Registry (SEER) regions, 376 surgeons (77.0%) responded. Surveys outlined case scenarios to inquire whether surgeons would be apt to perform ALND for patients with clinical stage I breast cancer with varying degrees of SLN involvement in the setting of BCT or mastectomy, from which surgeons were categorized into 1 of 3 groups based on their propensity to perform ALND (low, selective, high). In parallel, surgeons were asked how they define a negative surgical margin precluding the need for lumpectomy re-excision.

In the setting of minimal SLN disease (isolated tumor cells and/or micrometastases), the majority of surgeons (approximately 87%) would omit ALND in alignment with Z0011 findings. However, only about 37% stated that they would omit ALND in the setting of 2 SLNs with macrometastatic disease, which is a scenario encompassed within the inclusion criteria of the Z0011 trial. Surgeons performing fewer annual breast surgical cases were more likely to recommend ALND. Conversely, low-propensity surgeons less inclined to perform ALND were more likely to accept lumpectomy margins of no ink on tumor compared with high-propensity surgeons (approximately 72% vs 45%, respectively). Multivariable regression analysis demonstrated that lower propensity to recommend ALND was associated with higher breast patient annual volumes, acceptance of no ink on tumor lumpectomy margins, multidisciplinary breast cancer care, and geographic site of practice.

The finding that surgeons have been slow to adopt major practice changes is not new. Despite publication in 1985 of the NSABP B-06 randomized trial demonstrating the balance of BCT to mastectomy for the treatment of early-stage breast cancer, only 35% of women in the SEER registry with stage I breast cancer underwent BCT in the 5 years after publication.6 Even after the 1990 National Institutes of Health Consensus Conference recommendation for BCT with early-stage breast cancer, only 60% of patients with stage I and 39% of those with stage II breast cancer underwent BCT by 1995, with wide geographic variation by SEER region. In 2005, the American College of Surgeons recommended core needle biopsy (CNB) as the standard compared with surgical biopsy for diagnosing image-detected breast abnormalities, an approach that subsequently was incorporated as a quality metric by the National Accreditation Program for Breast Centers (2010), the American Society of Breast Surgeons (2010), and the Agency for Healthcare Research and Quality (2014). Despite these major endeavors, surgical breast biopsy rates in the United States remain as high as 32% nationally.7

What will shift surgeon behavior toward higher quality, evidenced-based practices? It has long been recognized that making people aware of their own performance relative to peers can successfully improve the quality of their work, known as the Hawthorne effect. A prospective study by Tjoe and colleagues8 examined this phenomenon in 46 surgeons (breast-dedicated and general surgeons) in a large, 14-hospital health care system. They examined the association between providing individual and system-wide performance results to surgeons and their resultant adherence to the quality metric of CNB for breast cancer diagnosis. Surgeons received data electronically and in letter form on their adherence to the quality metric as well as the combined and deidentified individual adherence of all surgeons in their health care system. This intervention was accompanied by an education-focused summary of national guidelines recommending CNB as the standard of care. Surgeons were informed that their data on CNB use would be reviewed annually and shared with hospital leadership. System-wide adherence to this metric improved from a baseline rate of 80% preceding intervention to 96% post intervention. When provided this high level of performance feedback, general surgeons performed as well as breast-dedicated surgeons.

Morrow and colleagues5 posit that education strategies targeting low-volume surgeons should be developed to encourage changes in surgeon behavior. Additional, more-stringent strategies may be required. In this evolving era of specialty-specific maintenance of board certification by the American Board of Surgery, an opportunity exists to introduce the concept of adherence to quality metrics, such as the omission of ALND in the setting of SLN metastases, as performance benchmarks upon which surgeons will be evaluated. With increased visibility of one’s own performance relative to peers and evidence-based standards of practice, combined with the support of a respected credentialing body, such as the American Board of Surgery, toward the delivery and measurement of care, meaningful change is plausible.

Back to top
Article Information

Corresponding Author: Benjamin O. Anderson, MD, Department of Surgery, University of Washington, PO Box 356410, Seattle, WA 98195 (banderso@uw.edu).

Published Online: July 12, 2018. doi:10.1001/jamaoncol.2018.1939

Conflict of Interest Disclosures: None reported.

References
1.
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 randomised, multicentre, open-label, phase 3 non-inferiority trial.  Lancet Oncol. 2014;15(12):1303-1310. doi:10.1016/S1470-2045(14)70460-7PubMedGoogle ScholarCrossref
2.
Galimberti  V, Cole  BF, Zurrida  S,  et al; International Breast Cancer Study Group Trial 23-01 investigators.  Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23-01): a phase 3 randomised controlled trial.  Lancet Oncol. 2013;14(4):297-305. doi:10.1016/S1470-2045(13)70035-4PubMedGoogle ScholarCrossref
3.
Giuliano  AE, Ballman  K, McCall  L,  et al.  Locoregional recurrence after sentinel lymph node dissection with or without axillary dissection in patients with sentinel lymph node metastases: long-term follow-up from the American College of Surgeons Oncology Group (Alliance) ACOSOG Z0011 Randomized Trial.  Ann Surg. 2016;264(3):413-420. doi:10.1097/SLA.0000000000001863PubMedGoogle ScholarCrossref
4.
Morrow  M, Van Zee  KJ, Patil  S,  et al.  Axillary dissection and nodal irradiation can be avoided for most node-positive Z0011-eligible breast cancers: a prospective validation study of 793 patients.  Ann Surg. 2017;266(3):457-462. doi:10.1097/SLA.0000000000002354PubMedGoogle ScholarCrossref
5.
Morrow  M, Jagsi  R, McLeod  MC, Shumway  D, Katz  SJ.  Surgeon attitudes toward the omission of axillary dissection in early breast cancer  [published online July 12, 2018].  JAMA Oncol. doi:10.1001/jamaoncol.2018.1908Google Scholar
6.
Lazovich  D, Solomon  CC, Thomas  DB, Moe  RE, White  E.  Breast conservation therapy in the United States following the 1990 National Institutes of Health Consensus Development Conference on the treatment of patients with early stage invasive breast carcinoma.  Cancer. 1999;86(4):628-637. doi:10.1002/(SICI)1097-0142(19990815)86:4<628::AID-CNCR11>3.0.CO;2-LPubMedGoogle ScholarCrossref
7.
Eberth  JM, Xu  Y, Smith  GL,  et al.  Surgeon influence on use of needle biopsy in patients with breast cancer: a national Medicare study.  J Clin Oncol. 2014;32(21):2206-2216. doi:10.1200/JCO.2013.52.8257PubMedGoogle ScholarCrossref
8.
Tjoe  JA, Greer  DM, Ihde  SE, Bares  DA, Mikkelson  WM, Weese  JL.  Improving quality metric adherence to minimally invasive breast biopsy among surgeons within a multihospital health care system.  J Am Coll Surg. 2015;221(3):758-766. doi:10.1016/j.jamcollsurg.2015.06.003PubMedGoogle ScholarCrossref
×