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Original Article |

The Learning Curve for Sentinel Node Biopsy in Breast Cancer:  Practical Considerations FREE

Richard K. Orr, MD, MPh; James L. Hoehn, MD, MS; Nananda F. Col, MD, MPh, MPP
[+] Author Affiliations

From the Department of Surgery, The Marshfield Clinic, Marshfield, Wis, and the University of Wisconsin Medical School, Madison (Drs Orr and Hoehn); and the Division of Clinical Decision Making, Informatics and Telemedicine, New England Medical Center and Tufts University School of Medicine, Boston, Mass (Dr Col).


Arch Surg. 1999;134(7):764-767. doi:10.1001/archsurg.134.7.764.
Text Size: A A A
Published online

Hypothesis  Performance of sentinel node biopsy (SNB) instead of full axillary lymph node dissection (ALND) by inexperienced surgeons will lead to understaging of some women with breast cancer and increased costs.

Design  A decision analysis model was used to investigate the implications of SNB vs full ALND during the learning phase (60-80 procedures). This model simulates a randomized trial of 10,000 women in each arm. Data regarding the learning curve were obtained from published series.

Main Outcome Measures  Percentage of women with inaccurate staging of their breast cancer, overall survival, quality-adjusted survival, and potential costs of SNB vs ALND.

Results  Performance of SNB instead of ALND results in inability to locate a sentinel node in 38% of attempts during the learning phase (compared with 10% in later cases) and understaging in 12% of patients during the learning phase (compared with 0% in later cases). This understaging is associated with a small decrement in survival (1%-2%) and an increased risk of axillary recurrence. Sentinel node biopsy is cost-effective only when the ability to detect sentinel nodes exceeds 80%; and the cost of SNB is less than 50% of the cost of ALND.

Conclusions  To ensure accurate staging of patients with breast cancer, all surgeons should perform full ALND while learning SNB techniques. Only after documentation of accuracy of SNB (sensitivity >90%) should full ALND be omitted for women with negative sentinel nodes.

AXILLARY LYMPH node dissection (ALND) has been a routine part of breast cancer surgery, although its necessity for women with clinically negative axillae is being questioned,1,2 In 1992, Morton et al3 introduced sentinel lymph node biopsy (SNB) as a less invasive alternative for assessing lymph node metastases in patients with melanoma. Subsequent investigations by Krag et al,4 using radiocolloid, and Giuliano et al,5 using isosulfan vital blue dye, proved the effectiveness of SNB for staging patients with breast cancer as well.

Turner and coworkers6 have shown that the sentinel node is the most likely axillary node to harbor metastases, and proposed that patients with histologically negative sentinel nodes may be spared full ALND. Several other research groups have also demonstrated promising results of SNB (Table 1). Despite this enthusiasm, Morton22 and Cox et al20 have commented on the "learning curve" inherent in mastering new procedures. Proper identification of the sentinel node requires multidisciplinary expertise, including a surgeon trained in the technique and nuclear medicine and pathologic experts. Morton22 recommends that surgeons learning SNB should perform a full axillary clearance on all patients during this learning phase (60-80 cases) to monitor the accuracy of the procedure. He asserts that a surgeon's inexperience (or lack of appropriate multidisciplinary support) will lead to understaging of patients and to increased breast cancer recurrence.

Table Graphic Jump LocationPublished Series of Sentinel Node Biopsies for Breast Cancer*

Apparently some surgeons are performing SNB instead of axillary clearance, forgoing the formal learning phase recommended by Reintgen.23 This trend will likely become more prevalent as SNB becomes popularized in the lay press, especially since few surgeons have access to the number of patients with breast cancer required to surmount the learning curve in a reasonable period. To assess the potential significance of performing SNB instead of ALND, we used a clinical decision analysis model to evaluate the effectiveness of SNB done by experienced vs inexperienced surgeons.

STATEMENT OF THE PROBLEM AND DECISION MODEL

Using decision analysis, we investigated the potential benefits of SNB, performed by experienced and inexperienced surgeons compared with full ALND for women with clinically negative axillary lymph nodes. This model simulates a randomized trial of 10,000 women in each treatment arm, estimating mean life expectancy for patients in each arm. In the ALND arm, all patients were assumed to have undergone ALND at the time of breast tumor resection, with subsequent therapy dictated by the results of ALND. In the SNB arm, all patients underwent SNB, with ALND reserved for patients in whom identification of the sentinel node was not technically possible or for those with histologically positive sentinel nodes. Women with histologically positive axillary nodes (in both groups) receive chemotherapy, whereas those with histologically negative nodes do not receive chemotherapy.

PROBABILITIES AND DATA SOURCES

Probabilities of 10-year survival were obtained from data of the Early Breast Cancer Trialists' Collaborative Group,24 and converted to life expectancy calculations using the DEALE method.25 On the basis of these calculations, the life expectancy for node-negative patients is 21.8 years. Node-positive women have a mean life expectancy of 13.1 years if they receive chemotherapy and 10.9 years if they do not. Since ALND may have an independent effect on survival,26 we added a 5% survival "bonus" to patients with positive nodes undergoing ALND. The alternative hypothesis, ie, that ALND has no independent survival benefit, was tested by sensitivity analysis. Data regarding axillary recurrence in the axillae of untreated patients (those SNB patients with false-negative results) were obtained from the National Surgical Adjuvant Breast and Bowel Project (NSABP B-04).27

Data regarding feasibility, sensitivity, and specificity for SNB during the learning phase were obtained from Giuliano et al5 and Guenther et al,7 and contrasted to other published series819,21 (Table 1) in sensitivity analyses. For our initial analysis, we averaged the data from the 2 series, using 62% as the percentage of patients in which a sentinel node could be identified, and 74% for the sensitivity (defined as the percentage of node-positive axillae that were correctly identified by SNB) of detecting occult malignancy. We assumed that all nodes defined as cancer by pathologic examination actually contained cancer (specificity, 100%). The cost of ALND was based on overnight hospitalization28 and compared (in sensitivity analyses) with costs for outpatient ALND.29 Since minimal data have been published regarding the actual cost of SNB,11 we assumed that the cost of SNB was half the cost of ALND, and varied this ratio in the sensitivity analysis.

Our principal outcome measure, life expectancy, accounts for differences in survival and recurrence rates affected by the chosen treatment, but does not account for ALND-associated morbidity, toxic effects of chemotherapy, or cancer recurrence. We adjusted our life expectancy estimates to include quality-of-life considerations by using a modification30 of a Markovian cost-effectiveness analysis of Hillner and Smith.31 We used quality-adjusted life expectancy as the unit measure, derived by depreciating the time spent in undesirable health states according to the perceived quality of life a patient experiences during that health state. We used published quality-of-life adjustments for various cancer states.31 Adjustments for possible long-term morbidity from ALND were derived from Velanovich,32 and local expert opinion. Models were created and analyses performed using the software DATA 3.0 (TreeAge Software Inc, Williamstown, Mass). All costs and utilities were discounted over time, using a discount rate of 3%. For our initial analysis, we assumed that the patients have palpable 3-cm tumors, and that the likelihood of positive nodes is 46%.

Use of SNB during the learning curve phase results in a significant number of incorrectly staged patients. For our baseline scenario (3-cm palpable tumor), 12% of patients declared "node negative" by SNB will actually harbor metastatic disease. This incorrect staging leads to a loss in life expectancy of 4 months (1.6%) for the SNB cohort, compared with patients receiving full ALND. Results of decision analysis were for ALND: life expectancy, 18.7 years; nondiscounted quality-adjusted life-years, 13.0; discounted quality-adjusted life-years, 10.2; and for SNB: life expectancy, 18.4 years; nondiscounted quality-adjusted life-years, 12.8; discounted quality-adjusted life-years, 10.0. Quality-adjusted survival figures are similar. Compared with ALND, patients receiving SNB averaged a 1.3% decrement in quality-adjusted life expectancy. Axillary recurrence occurs in 3% of patients with "negative" SNB results, with approximately half of these recurrences occurring within the first postoperative year.

SENSITIVITY ANALYSIS

As the sensitivity of SNB approaches 100%, the loss in expected survival related to the avoidance of full ALND becomes nil. For example, the expected survival decrement drops to 1 month if 90% of axillae with metastases are correctly diagnosed by SNB. As expected, the likelihood of positive lymph nodes is also a major determinant of the outcome following SNB. Fewer than 20% of patients with nonpalpable T1 tumors will have axillary nodal metastases. Consequently, patients in this subgroup experience less benefit from full ALND—1 month of better life expectancy than SNB. The incorporation of an independent survival benefit for ALND in our model and varying the percentage of cases in which a sentinel node could not be identified had little effect on the relative life expectancies for the 2 strategies. Other important variables having minimal effects on the model's predictions include baseline survival probabilities, patient age, and quality-of-life adjustments.

Our baseline analysis assumes that patients with histologically negative nodes did not receive chemotherapy. In reality, many patients with known risk factors (eg, premenopausal, T2 tumors, aggressive histological features, and estrogen receptor negative) are treated with chemotherapy irrespective of nodal status. If we assume that 50% of node-negative patients will receive chemotherapy, then the advantage of ALND declines significantly, with ALND patients gaining only 1 month of life expectancy over SNB patients. As the number of node-negative patients receiving chemotherapy increases, the benefit of full ALND decreases proportionately.

COST ANALYSIS

Because of the significant number of sentinel nodes not identified during the learning curve phase (38%), SNB is relatively expensive. Patients with unidentified sentinel nodes receive the expenses of ALND in addition to those of SNB, which include costs for additional operating room time, additional frozen sections, and radiocolloid localization (if used). The SNB arm is more expensive than the ALND arm during the learning curve phase unless the cost of SNB can be reduced to less than 40% of the cost of ALND. This implies a "break even" SNB cost of $4000 when compared with a typical overnight hospitalization, but only $1200 when compared with outpatient surgery. As surgical experience increases, with a consequent increase in the likelihood of identifying the sentinel node, the cost of SNB decreases proportionately. For example, if 90% of sentinel nodes are identified, the "break even" costs increase to $6000 (compared with inpatient ALND) and $1800 (compared with outpatient ALND).

The present analysis evaluated the implications of performing SNB by inexperienced surgeons in lieu of a formal validation period. Using decision analysis, we observed that 12% of patients declared node negative by SNB would be understaged by surgeons operating within the learning curve phase. This understaging leads to an increased risk of axillary recurrence and a decreased overall survival. The effect on a large cohort of women results in a small decrease in average life expectancy and quality-adjusted life expectancy. The high rate of unidentified sentinel nodes and the necessity for full ALND whenever the sentinel node cannot be identified increase the costs during the learning phase.

Our analysis has some important limitations. We cannot totally reconcile the suggestion that surgeons in the learning curve phase will identify some node-positive patients who would not have been identified without any axillary surgery. We believe that the literature does not support this approach, as series of axillary node sampling have shown higher rates of axillary recurrence,33 as well as suggesting diminished survival.34 We did not consider the possibility that SNB may identify more patients with positive nodes by using sophisticated histologic techniques for sentinel node examination, but doubt that omission of the possibility of increased detection of occult metastases will change the results of our analysis.

Many authors have described the learning curves peculiar to laparoscopic surgery, and guidelines have been proposed to ensure the safety of these procedures.35 In a review, Gates36 has outlined several key points that allow surgeons to learn new procedures while benefiting patients, including avoidance of harm, peer review, and informed consent. Obviously, prevention of harm to patients must be foremost. As Copeland37 observes, the learning phase for SNB is different from that of laparoscopic procedures. A technical failure of SNB will not be apparent in the short term, but may lead to grave long-term effects, as opposed to the technical failures of laparoscopy, which are apparent immediately, or in the discernible future. It is impossible to ensure the accuracy of SNB during the learning phase without comparison with the criterion standard—full ALND. Hospital peer reviewers must have this information to comfortably certify surgeons in their institutions to assure that patients are not harmed by inadequate operations. Patients must be informed of an individual surgeon's "track record" regarding SNB, as well as the potential of her being understaged by the procedure. This study strongly supports the requirement for surgeons to perform full ALND during the learning phase, until the surgeon can document acceptable identification of sentinel nodes and sensitivity for detecting metastatic disease.

Presented in part at the 79th Annual Meeting of the New England Surgical Society, Toronto, Ontario, September 26, 1998.

Corresponding author: Richard K. Orr, MD, MPH, Department of Surgical Education, Spartanburg Regional Medical Center, 101 E Wood St, Spartanburg, SC 29303 (e-mail: rorr@srhs.com).

Cady  BStone  MDWayne  J New therapeutic possibilities in primary invasive breast cancer. Ann Surg. 1993;218338- 349
Link to Article
Deckers  PJ Axillary dissection in breast cancer: when, why, how much, and for how long? another operation soon to be extinct? J Surg Oncol. 1991;48217- 219
Link to Article
Morton  DLWen  D-RWong  JH  et al.  Technical details of intraoperative lymphatic mapping for early-stage melanoma. Arch Surg. 1992;127392- 399
Link to Article
Krag  DNWeaver  DLAlex  JCFairbank  JT Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol. 1993;2335- 340
Link to Article
Giuliano  AEKirgan  DMGuenther  JMMorton  DL Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220391- 401
Link to Article
Turner  RROllila  DWKrasne  DLGiuliano  AE Histopathologic validation of the sentinel lymph node hypothesis for breast cancer. Ann Surg. 1997;226271- 278
Link to Article
Guenther  JMKrishnamoorthy  MTan  LT Sentinel lymphadenectomy for breast cancer in a community managed care setting. Cancer J Sci Am. 1997;3336- 340
Giuliano  AEJones  RCBrennan  MStatman  R Sentinel lymphadenectomy in breast cancer. J Clin Oncol. 1997;152345- 2350
Rodier  JFJanser  JC Surgical technical details improving sentinel node identification in breast cancer. Oncol Rep. 1997;4281- 283
Dale  PSWilliams  JT Axillary staging utilizing selective sentinel lymphadenectomy for patients with invasive breast cancer. Am Surg. 1998;6428- 32
Flett  MMGoing  JJStanton  PDCooke  TG Sentinel node localization in patients with breast cancer. Br J Surg. 1998;85991- 993
Link to Article
Pijpers  RMeijer  SHoekstra  OS  et al.  Impact of lymphoscintigraphy on sentinel node identification with technetium-99m-colloid albumin in breast cancer. J Nucl Med. 1997;38366- 368
Roumen  RMHValkenberg  JGMGeuskens  LM Lymphoscintigraphy and feasibility of sentinel node biopsy in 83 patients with primary breast cancer. Eur J Surg Oncol. 1997;23495- 502
Link to Article
Veronesi  UPaganelli  GGalimberti  V  et al.  Sentinel-node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph nodes. Lancet. 1997;3491864- 1867
Link to Article
Borgstein  PJPijpers  RComans  EF  et al.  Sentinel node biopsy in breast cancer: guidelines and pitfalls of lymphoscintigraphy and gamma probe detection. J Am Coll Surg. 1998;186275- 283
Link to Article
Crossin  JAJohnson  CStewart  PBTurner  WW  Jr γ-Probe-guide resection of the sentinel lymph node in breast cancer. Am Surg. 1998;64666- 669
Krag  DHarlow  SWeaver  DAshikaga  T Technique of sentinel node resection in melanoma and breast cancer: probe-guided surgery and lymphatic mapping. Eur J Surg Oncol. 1998;2489- 93
Link to Article
Albertini  JJLyman  GHCox  C  et al.  Lymphatic mapping and sentinel node biopsy in the patient with breast cancer. JAMA. 1996;2761818- 1822
Link to Article
Barnwell  JMArrendondo  MAKollmorgen  D  et al.  Sentinel node biopsy in breast cancer. Ann Surg Oncol. 1998;5126- 130
Link to Article
Cox  CEPendas  SCox  JM  et al.  Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg. 1998;227645- 653
Link to Article
O'Hea  BJHill  ADKEl-Shirbiny  AM  et al.  Sentinel lymph node biopsy in breast cancer: initial experience at Memorial Sloan-Kettering Cancer Center. J Am Coll Surg. 1998;186423- 427
Link to Article
Morton  DL Intraoperative lymphatic mapping and sentinel lymphadenectomy: community standard of care or clinical investigation? Cancer J Sci Am. 1997;3328- 329
Reintgen  D The credentialing of American Surgery [reply letter]. Ann Surg Oncol. 1997;4603
Link to Article
Early Breast Cancer Trialists' Collaborative Group, Systemic treatment of early breast cancer by hormonal, cytotoxic, or immune therapy. Lancet. 1992;3391- 1571- 85
Beck  RKassirer  JPPauker  SG Convenient approximation of life expectancy (the DEALE): validation of the method. Am J Med. 1982;73883- 888
Link to Article
Orr  RK The impact of prophylactic axillary node dissection on breast cancer survival: a Bayesian meta-analysis. Ann Surg Oncol. 1999;6109- 116
Link to Article
Fisher  BRedmond  CFisher  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;312674- 681
Link to Article
Cady  B The need to reexamine axillary lymph node dissection in invasive breast cancer. Cancer. 1994;73505- 507
Link to Article
Goodman  AAMendez  AL Definitive surgery for breast cancer performed on an outpatient basis. Arch Surg. 1993;1281149- 1152
Link to Article
Orr  RKCol  NF Should axillary node dissection be routine in post-menopausal women? a cost-effectiveness analysis of ER+ lumpectomy patients. Breast Cancer Res Treat. 1994;32(suppl)92
Hillner  BESmith  TJ A model of chemotherapy in node-negative breast cancer. Natl Cancer Inst Monogr. 1992;11143- 149
Velanovich  V Axillary lymph node dissection for breast cancer: a decision analysis of T1 lesions. Ann Surg Oncol. 1998;5131- 139
Link to Article
Forrest  APMEverington  DMcDonald  CCSteele  RJCChetty  UStewart  HJ The Edinburgh randomized trial of axillary sampling or clearance after mastectomy. Br J Surg. 1995;821504- 1508
Link to Article
Sosa  JADiener-West  MGusev  Y  et al.  Association between extent of axillary lymph node dissection and survival in patients with stage I breast cancer. Ann Surg Oncol. 1998;5140- 149
Link to Article
Sequeira  RWeinbaum  FSatterfield  JChassin  JMock  L Credentialing physicians for new technology: the physician's learning curve must not harm the patient. Am Surg. 1994;60821- 823
Gates  EA New surgical procedures: can our patients benefit while we learn? Am J Obstet Gynecol. 1997;1761293- 1299
Link to Article
Copeland  EM In discussion of: Cox CE, Pendas S, Cox JM, et al. Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg. 1998;227651

Figures

Tables

Table Graphic Jump LocationPublished Series of Sentinel Node Biopsies for Breast Cancer*

References

Cady  BStone  MDWayne  J New therapeutic possibilities in primary invasive breast cancer. Ann Surg. 1993;218338- 349
Link to Article
Deckers  PJ Axillary dissection in breast cancer: when, why, how much, and for how long? another operation soon to be extinct? J Surg Oncol. 1991;48217- 219
Link to Article
Morton  DLWen  D-RWong  JH  et al.  Technical details of intraoperative lymphatic mapping for early-stage melanoma. Arch Surg. 1992;127392- 399
Link to Article
Krag  DNWeaver  DLAlex  JCFairbank  JT Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol. 1993;2335- 340
Link to Article
Giuliano  AEKirgan  DMGuenther  JMMorton  DL Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg. 1994;220391- 401
Link to Article
Turner  RROllila  DWKrasne  DLGiuliano  AE Histopathologic validation of the sentinel lymph node hypothesis for breast cancer. Ann Surg. 1997;226271- 278
Link to Article
Guenther  JMKrishnamoorthy  MTan  LT Sentinel lymphadenectomy for breast cancer in a community managed care setting. Cancer J Sci Am. 1997;3336- 340
Giuliano  AEJones  RCBrennan  MStatman  R Sentinel lymphadenectomy in breast cancer. J Clin Oncol. 1997;152345- 2350
Rodier  JFJanser  JC Surgical technical details improving sentinel node identification in breast cancer. Oncol Rep. 1997;4281- 283
Dale  PSWilliams  JT Axillary staging utilizing selective sentinel lymphadenectomy for patients with invasive breast cancer. Am Surg. 1998;6428- 32
Flett  MMGoing  JJStanton  PDCooke  TG Sentinel node localization in patients with breast cancer. Br J Surg. 1998;85991- 993
Link to Article
Pijpers  RMeijer  SHoekstra  OS  et al.  Impact of lymphoscintigraphy on sentinel node identification with technetium-99m-colloid albumin in breast cancer. J Nucl Med. 1997;38366- 368
Roumen  RMHValkenberg  JGMGeuskens  LM Lymphoscintigraphy and feasibility of sentinel node biopsy in 83 patients with primary breast cancer. Eur J Surg Oncol. 1997;23495- 502
Link to Article
Veronesi  UPaganelli  GGalimberti  V  et al.  Sentinel-node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph nodes. Lancet. 1997;3491864- 1867
Link to Article
Borgstein  PJPijpers  RComans  EF  et al.  Sentinel node biopsy in breast cancer: guidelines and pitfalls of lymphoscintigraphy and gamma probe detection. J Am Coll Surg. 1998;186275- 283
Link to Article
Crossin  JAJohnson  CStewart  PBTurner  WW  Jr γ-Probe-guide resection of the sentinel lymph node in breast cancer. Am Surg. 1998;64666- 669
Krag  DHarlow  SWeaver  DAshikaga  T Technique of sentinel node resection in melanoma and breast cancer: probe-guided surgery and lymphatic mapping. Eur J Surg Oncol. 1998;2489- 93
Link to Article
Albertini  JJLyman  GHCox  C  et al.  Lymphatic mapping and sentinel node biopsy in the patient with breast cancer. JAMA. 1996;2761818- 1822
Link to Article
Barnwell  JMArrendondo  MAKollmorgen  D  et al.  Sentinel node biopsy in breast cancer. Ann Surg Oncol. 1998;5126- 130
Link to Article
Cox  CEPendas  SCox  JM  et al.  Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg. 1998;227645- 653
Link to Article
O'Hea  BJHill  ADKEl-Shirbiny  AM  et al.  Sentinel lymph node biopsy in breast cancer: initial experience at Memorial Sloan-Kettering Cancer Center. J Am Coll Surg. 1998;186423- 427
Link to Article
Morton  DL Intraoperative lymphatic mapping and sentinel lymphadenectomy: community standard of care or clinical investigation? Cancer J Sci Am. 1997;3328- 329
Reintgen  D The credentialing of American Surgery [reply letter]. Ann Surg Oncol. 1997;4603
Link to Article
Early Breast Cancer Trialists' Collaborative Group, Systemic treatment of early breast cancer by hormonal, cytotoxic, or immune therapy. Lancet. 1992;3391- 1571- 85
Beck  RKassirer  JPPauker  SG Convenient approximation of life expectancy (the DEALE): validation of the method. Am J Med. 1982;73883- 888
Link to Article
Orr  RK The impact of prophylactic axillary node dissection on breast cancer survival: a Bayesian meta-analysis. Ann Surg Oncol. 1999;6109- 116
Link to Article
Fisher  BRedmond  CFisher  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;312674- 681
Link to Article
Cady  B The need to reexamine axillary lymph node dissection in invasive breast cancer. Cancer. 1994;73505- 507
Link to Article
Goodman  AAMendez  AL Definitive surgery for breast cancer performed on an outpatient basis. Arch Surg. 1993;1281149- 1152
Link to Article
Orr  RKCol  NF Should axillary node dissection be routine in post-menopausal women? a cost-effectiveness analysis of ER+ lumpectomy patients. Breast Cancer Res Treat. 1994;32(suppl)92
Hillner  BESmith  TJ A model of chemotherapy in node-negative breast cancer. Natl Cancer Inst Monogr. 1992;11143- 149
Velanovich  V Axillary lymph node dissection for breast cancer: a decision analysis of T1 lesions. Ann Surg Oncol. 1998;5131- 139
Link to Article
Forrest  APMEverington  DMcDonald  CCSteele  RJCChetty  UStewart  HJ The Edinburgh randomized trial of axillary sampling or clearance after mastectomy. Br J Surg. 1995;821504- 1508
Link to Article
Sosa  JADiener-West  MGusev  Y  et al.  Association between extent of axillary lymph node dissection and survival in patients with stage I breast cancer. Ann Surg Oncol. 1998;5140- 149
Link to Article
Sequeira  RWeinbaum  FSatterfield  JChassin  JMock  L Credentialing physicians for new technology: the physician's learning curve must not harm the patient. Am Surg. 1994;60821- 823
Gates  EA New surgical procedures: can our patients benefit while we learn? Am J Obstet Gynecol. 1997;1761293- 1299
Link to Article
Copeland  EM In discussion of: Cox CE, Pendas S, Cox JM, et al. Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg. 1998;227651

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