Originally published as JCO Early Release 10.1200/JCO.2006.07.4062 on May 7 2007

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Surgical Complications Associated With Sentinel Lymph Node Dissection (SLND) Plus Axillary Lymph Node Dissection Compared With SLND Alone in the American College of Surgeons Oncology Group Trial Z0011

Anthony Lucci, Linda Mackie McCall, Peter D. Beitsch, Patrick W. Whitworth, Douglas S. Reintgen, Peter W. Blumencranz, A. Marilyn Leitch, Sukumal Saha, Kelly K. Hunt, Armando E. Giuliano

From the Department of Surgical Oncology, The University of Texas M.D. Anderson Cancer Center, Houston; Dallas Surgical Group; The University of Texas Southwestern, Dallas, TX; American College of Surgeons Oncology Group, Durham, NC; Nashville Breast Center, Nashville, TN; Lakeland Cancer Center, Lakeland; Morton Plant Mease Healthcare, Clearwater, FL; McClaren Regional Medical Center, Flint, MI; and John Wayne Cancer Institute, Santa Monica, CA

Address reprint requests to Anthony Lucci, MD, Department of Surgical Oncology, Unit 444, The University of Texas M.D. Anderson Cancer Center, 1515 Holcombe Blvd, Houston, TX 77030; e-mail: alucci{at}mdanderson.org

	ABSTRACT

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Purpose The American College of Surgeons Oncology Group trial Z0011 was a prospective, randomized, multicenter trial comparing overall survival between patients with positive sentinel lymph nodes (SLNs) who did and did not undergo axillary lymph node dissection (ALND). The current study compares complications associated with SLN dissection (SLND) plus ALND, versus SLND alone.

Patients and Methods From May 1999 to December 2004, 891 patients were randomly assigned to SLND + ALND (n = 445) or SLND alone (n = 446). Information on wound infection, axillary seroma, paresthesia, brachial plexus injury (BPI), and lymphedema was available for 821 patients.

Results Adverse surgical effects were reported in 70% (278 of 399) of patients after SLND + ALND and 25% (103 of 411) after SLND alone (P .001). Patients in the SLND + ALND group had more wound infections (P .0016), seromas (P .0001), and paresthesias (P .0001) than those in the SLND-alone group. At 1 year, lymphedema was reported subjectively by 13% (37 of 288) of patients after SLND + ALND and 2% (six of 268) after SLND alone (P .0001). The difference between the two groups' lymphedema, assessed by arm measurements at 30 days (P = .36), 6 months (P = .22), and 1 year (P = .078), although close to the cutoff for significance at 1 year, was not significant. BPIs occurred in less than 1% of patients.

Conclusion In trial Z0011, the use of SLND + ALND resulted in more wound infections, axillary seromas, and paresthesias than SLND alone. Lymphedema was more common after SLND + ALND but was significantly different only by subjective report. The use of SLND alone resulted in fewer complications.

	INTRODUCTION

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For patients with breast cancer, sentinel lymph node dissection (SLND) has gained favor over axillary lymph node dissection (ALND) for the axillary staging of early disease because of the morbidity and questionable survival benefits of ALND.^1-4 SLND enables accurate staging by allowing pathologists to focus their examination on the nodes most likely to contain metastasis. In addition, SLND identifies the patients most likely to benefit from ALNDs (those with documented regional nodal metastasis) and keeps patients unlikely to benefit from ALNDs (those with negative SLNs) from being subjected to the morbidity of ALND. Studies in which SLNs were the only positive nodes in at least 50% of patients with early-stage breast cancer have also suggested that SLND alone provides local control in many cases.^5,6 The American College of Surgeons Oncology Group (ACOSOG) therefore designed a prospective randomized trial, Z0011, to compare overall survival in SLN-positive patients who did and did not undergo completion ALND. If SLND alone offers survival benefits equivalent to those of completion ALND, avoiding ALNDs and the associated morbidity would be reasonable. Although it seems intuitive that SLNDs would be safer than ALNDs, a prospective randomized trial in the United States has not validated that insight. Thus, the secondary objective of trial Z0011 was to quantify and compare the surgical morbidities associated with SLND + ALND versus SLND alone.

Since the activation of trial Z0011 in May 1999, several retrospective studies and a prospective trial, the Axillary Lymphatic Mapping Against Nodal Axillary Clearance (ALMANAC) study, have documented that SLND alone has less morbidity than ALND.^7-10 Because trial Z0011 accrued participants slower than projected, and both patient groups' overall disease recurrence or death rate was much lower than expected, the ACOSOG Data and Safety Monitoring Committee closed trial Z0011 to new patients on December 15, 2004. These developments may have impaired the ability of trial Z0011 to fulfill its primary objective, but we were still able to use the data to compare the two groups' morbidities. This study analyzed the incidence and predictors of surgical complications associated with SLND + ALND versus SLND alone in trial Z0011.

	PATIENTS AND METHODS

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Study Design
All trial Z0011 participants were women at least 18 years old undergoing breast conservation therapy who had clinical T1 or T2, N0, M0 breast cancer; one or two positive SLNs; and an Eastern Cooperative Oncology Group/Zubrod functional status 2. Staging was performed using American Joint Committee on Cancer guidelines.¹¹

All patients received adjuvant systemic therapy (chemotherapy, endocrine therapy, or both, as a joint decision by the patient and treating physician) and whole-breast irradiation (45 to 50 Gy, in fractions of 1.8 to 2.0 Gy/d, 5 d/wk) delivered via tangential fields with a coplanar border.

SLNs were positive if analysis of frozen sections, touch preparations, or hematoxylin and eosin (HE) –stained permanent sections—but not immunohistochemistry—identified any metastasis; patients without positive SLNs were excluded from enrollment. In addition, a patient's first histologic diagnosis of invasive breast cancer had to be 60 or fewer days before her SLND. The human investigations committee at each participating institution approved this trial. Patients with an HE-confirmed positive SLN were offered enrollment through an informed consent process, and if a patient elected to participate by giving written informed consent, a computer would randomly assign her to either group 1 (SLND + ALND; n = 445) or group 2 (SLND alone; n = 446) in a 1:1 ratio (Fig 1). ALND was performed within 42 days of SLND for those with a positive SLN. Patients who preregistered before SLND were randomly assigned intraoperatively through an interactive automated telephone system when frozen section or touch preparation analysis documented a positive node. Participants could also wait for post-SLND pathology results and then be randomly assigned to either group. trial Z0011 excluded breastfeeding patients and those whose histories included another malignancy within 5 years; bilateral breast cancer; multicentric disease; three or more positive SLNs; gross extracapsular invasion or matted nodes at SLND; and medical contraindications to ALND or other risk factors precluding future treatment.

View larger version (20K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Study schema for American College of Surgeons Oncology Group trial Z0011. SLND, sentinel lymph node dissection; ALND, axillary lymph node dissection.

Surgery
All surgeons participating in trial Z0011 had documented experience with at least 20 SLNDs. SLNDs were performed with isosulfan blue, a radiopharmaceutical, or both. The protocol recommended the injection volume, timing, and site within the breast, but individual surgeons were permitted to rely on their experience. Patients with a medial hemisphere lesion had preoperative lymphoscintigraphy to confirm axillary drainage. After the blue and/or hot nodes were removed, any remaining axillary nodes were palpated; if suggestive of disease, they were considered SLNs and removed.

ALND was defined as the removal of all anatomic level I and II nodes on the affected side, with at least 10 identified nodes per axillary specimen.

Adverse Surgical Effects
Adverse effects for all operative procedures were recorded at 30 days, every 6 months until year 3, and then annually. Surgical effects assessed at day 30 included wound infections, axillary seroma, axillary paresthesia, and brachial plexus injury (BPI). The treating physician determined these effects by examining the patient, but paresthesia was a patient-reported effect. Ultrasound confirmation was not required for physician-documented seromas.

Surgical effects documented every 6 months included axillary paresthesia, lymphedema, and BPI. To ensure correct reporting, ACOSOG contacted study sites to re-evaluate all BPIs.

Lymphedemas were reported two ways. Every 6 months for 3 years and annually thereafter, they were recorded on the long-term surgical effects case report form according to patient self-report or physician diagnosis (subjective data). At 30 days, at 6 months, and annually thereafter, lymphedema was also diagnosed by comparing preoperative arm circumferences 10 cm proximal to the medial epicondyle with follow-up measurements (objective data). Lymphedema was defined as a 2-cm or greater postoperative increase in ipsilateral arm measurements compared with contralateral arm measurements based on the formula _P = (I_P/FU –I_P/B) –(C_P/FU –C_P/B), where I = ipsilateral, C = contralateral, P = proximal, FU = follow-up, and B = baseline.

Statistical Analysis
Frequency distributions were used to summarize patient characteristics and adverse effects. ² tests and logistic regressions were used to model the effect of clinical characteristics, including age, body mass index (BMI), and the total number of nodes removed on the occurrence of complications. Multivariate logistic regressions were also used to examine the combined effects of clinical predictors on surgical complications. All multivariate logistic regression models were fit by using backward stepwise procedures, and only data sets complete for every outcome analyzed were used. Because the number of nodes removed depended on a patient's assigned study group (patients undergoing an SLND alone would likely have fewer removed than those undergoing SLND + ALND), these data were included only in intragroup models, not models that used study group as a potential predictor. All analyses were performed with SAS statistical analysis software, version 8 (SAS Institute, Cary, NC). Values of P < .05 were considered significant.

To validate reported data via source documentation, clinical site audits were performed according to the National Cancer Institute's Clinical Trials Monitoring Branch guidelines.

	RESULTS

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Despite the early closure of trial Z0011, a balance in patient characteristics was achieved between the randomization arms (Table 1). As expected, the median numbers of lymph nodes removed in patients who did and did not have ALNDs were different (Table 1).

Axillary Paresthesias
Axillary paresthesias were the most common surgical effect at day 30 (Table 2). Having had an ALND was the only factor that predicted axillary paresthesias at any time point (Table 3). The number of nodes removed was a significant predictor of paresthesia 30 days after an ALND but not after SLND alone (Table 4).

There was no significant decline (P = not significant) in reported axillary paresthesias at 6 or 12 months compared with rates at 30 days (Table 2). Being younger remained a significant predictor for paresthesia 1 year after ALND, but the number of nodes removed did not remain a significant predictor (Table 3).

Lymphedema
According to subjective data (long-term surgical effects case report form), having had an ALND was not a significant predictor of lymphedema at 6 months, but it was significant at 1 year and afterward (Table 3). When subjective data from all follow-ups were combined, having had an ALND was also a significant predictor of lymphedema (P .0001). Based on proximal arm measurement data, no clinical factors (including number of nodes removed; Table 4) reliably predicted lymphedema at 30 days, 6 months, or 1 year (Table 3). However, because arm measurements were not always recorded at these follow-up times, the number of patients for whom data were available was much lower than the number of assessable patients.

BPI
Eighteen BPIs were reported originally, but after each injury was re-evaluated, it was discovered that 10 would have been more accurately classified as axillary paresthesias. Three BPIs occurred after SLND alone, but all of these had resolved at last follow-up, as had 88% of all BPIs. Figure 2 summarizes the outcomes of BPIs.

View larger version (30K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 2. Outcome of patients with brachial plexus injuries. BPI, brachial plexus; UE, upper extremity; ROM, range of motion.

	DISCUSSION

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We found that the number of nodes removed was a significant predictor for the development of paresthesia at 30 days, but only for the SLND + ALND arm, This result is unsurprising, given that transecting the axillary sensory nerves is more likely when all of the anatomic level I and II nodes are removed. Our finding that being younger predicted for post-ALND paresthesia corroborates several previous reports, including ACOSOG study Z0010.^15-17

Although the findings from trial Z0011 regarding increased rates of post-ALND infection, seroma formation, and paresthesia were expected, we did not expect the objective data, arm measurements, to fail to demonstrate significant differences in lymphedema rates between the study groups, even at 1 year. We might have questioned the validity of using arm measurements to assess upper extremity volume to explain this finding, but several controlled studies have shown that arm measurement data have a correlation coefficient of 0.99 with the gold standard, water displacement.¹⁸ In another study, the inter-rater and test-retest reliability correlation coefficients between circumferential and volumetric data were 0.99 and 0.99, respectively.¹⁹ These studies reported optimal accuracy when anatomic landmarks were used as reference points for taking measurements, as was done in trial Z0011. We therefore ruled out the test used to measure arm volume changes as the explanation for our findings.

Another possible explanation, BMI fluctuations, should not have had a significant effect on lymphedema assessment, because postoperative ipsilateral arm measurements were compared to the contralateral arm and presurgical measurements. Unfortunately, not all sites submitted complete arm measurement data, which resulted in fewer evaluable patients at each follow-up time; the study may therefore have lacked the power to demonstrate significant differences using arm measurements. When the data from follow-ups more than 12 months after surgery were assessed together, the number of assessable patients increased to 779 (from 468 at 1 year), with nearly significant results (P = .0572), suggesting that additional follow-ups may have shown significant differences in arm measurements between groups. It is also possible that 12 months was too little time to see significant differences between the two groups; proper assessment of lymphedema rates depends on evaluation of the long-term follow-up data. In a recent report of 204 early-stage breast cancer patients by Rietman et al,²⁰ the authors found the differences in lymphedema rates and quality of life (QOL) scores were not significant at short-term follow-up but were significant at 2-year follow-up. Furthermore, a study by Meric et al²¹ found that lymphedema occurred at a median of 17 months after ALND and breast conservation therapy. However, the trial Z0011 data do match the findings of a prospective study by Temple et al,²² in which investigators found no significant difference in arm circumferences at 12 months between patients with SLND and ALND. Schulze et al²³ also found no significant difference in lymphedema rates between SLND and ALND, even using water-displacement volume assessments.

The possibility exists that clinicians overestimated the incidence of lymphedema after ALND and underestimated it for SLND. Using arm measurements, lymphedema occurred in 8% of patients 6 months after SLND in trial Z0011, similar to the 7% lymphedema rates 6 months after SLND in ACOSOG Z0010.¹⁷ Similarly, the ALMANAC trial found a 7% incidence of post-SLND lymphedema.¹⁰ Most surgeons who treat breast cancer patients would likely assert that these figures overestimate the incidence of clinically relevant lymphedema after SLND alone. Yet three large prospective clinical trials have all reached the same conclusion: arm swelling, whether measured subjectively or objectively, occurs in at least 6% of patients undergoing SLND alone.^10,17 Conversely, post-ALND lymphedema diagnosed by arm measurements occurred in 11% of trial Z0011 patients, a figure slightly lower than the 14% reported in the ALMANAC study.¹⁰

Supraclavicular irradiation has been reported to increase the odds for lymphedema development, but irradiation of a specific supraclavicular field was not allowed in trial Z0011. Whole-breast irradiation was subject to review in trial Z0011; therefore, it is unlikely that variability in radiation delivery (or the inadvertent addition of a third field) explains the difference in lymphedema rates between groups. Several studies have shown that greater numbers of removed nodes correlated with lymphedema development,^24,25 whereas others have not.^21,26 The number of lymph nodes removed did not correlate with the risk of lymphedema in trial Z0011.

Published studies reporting subjective data on upper extremity function after breast cancer operations often contradict each other, making interpretation difficult. Many variables, including age, treatment of the dominant side, and socioeconomic status have all been shown to influence the reporting of arm complications.²⁷ Arm and shoulder pain after SLND alone have been reported subjectively by as many as 36% of patients.²⁸ The subjective self-reporting of post-ALND lymphedema by questionnaire has varied even more, with incidence rates of up to 49%.²⁹ Lastly, QOL instruments comparing SLND + ALND and SLND alone have shown no significant difference in global scores at short-term follow-up, despite disparate subjective rates of arm swelling and pain within the same groups of patients.³⁰ Regarding subjective data from trial Z0011, paresthesias improved over time, but not at significant rates, and this is consistent with previous reports.^22,31 Subjective data from trial Z0011 identified significant differences in the lymphedema rates at 1 year between patients who had and had not undergone ALNDs. Because as physicians we hope to maximize both survival and QOL for our patients, subjective outcomes must be considered alongside objective measurements. The fact that the incidence of paresthesias and subjective assessments of lymphedema favored SLND alone at 1 year supports its use as a means of providing superior long-term QOL outcomes for breast cancer patients.

BPIs, which mostly involved hand paresthesias or weakness, occurred in less than 1% of participants in trial Z0011, and the majority of these injuries had resolved at last follow-up. Interestingly, three of the BPIs occurred in patients who had undergone SLND alone. BPI has been reported to occur with hyperabduction of the arm during intraoperative positioning and with forceful upward traction beneath the pectoral muscles, possibly explaining the BPIs incurred in trial Z0011 by SLNDs alone.^32,33

In conclusion, our data support the hypothesis that SLND alone results in fewer surgical complications than does SLND + ALND. Common complications such as paresthesia, infection, and seroma were less likely to occur after SLND alone than after SLND + ALND. SLND offers patients with early-stage breast cancer a less morbid axillary staging alternative to ALND. The findings from trial Z0011 identify the need for additional study of the complex problem of assessing upper extremity lymphedema after axillary surgery.

	AUTHORS' DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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The author or immediate family members indicated a financial interest. No conflict exists for drugs or devices used in a study if they are not being evaluated as part of the investigation. For a detailed description of the disclosure categories, or for more information about ASCO's conflict of interest policy, please refer to the Author Disclosure Declaration and the Disclosures of Potential Conflicts of Interest section in Information for Contributors.

Employment: N/A Consultant: Patrick W. Whitworth, Ethicon Stock: N/A Honoraria: Patrick W. Whitworth, Ethicon; Douglas S. Reintgen, Schering Oncology Research Funds: Patrick W. Whitworth, Ethicon; Peter W. Blumencranz, ACOSOG; A. Marilyn Leitch, ACOSOG, NSABP Testimony: Patrick W. Whitworth, Ethicon Other: N/A

	AUTHOR CONTRIBUTIONS

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Conception and design: Anthony Lucci, Douglas S. Reintgen, Peter W. Blumencranz, A. Marilyn Leitch, Kelly K. Hunt, Armando E. Giuliano

Administrative support: Kelly K. Hunt

Provision of study materials or patients: Anthony Lucci, Peter D. Beitsch, Patrick W. Whitworth, Douglas S. Reintgen, Peter W. Blumencranz, A. Marilyn Leitch, Sukumal Saha, Kelly K. Hunt

Collection and assembly of data: Anthony Lucci, Linda Mackie McCall, Patrick W. Whitworth, Douglas S. Reintgen, A. Marilyn Leitch, Kelly K. Hunt, Armando E. Giuliano

Data analysis and interpretation: Anthony Lucci, Linda Mackie McCall, Patrick W. Whitworth, Douglas S. Reintgen, Peter W. Blumencranz, Kelly K. Hunt, Armando E. Giuliano

Manuscript writing: Anthony Lucci, Linda Mackie McCall, Kelly K. Hunt

Final approval of manuscript: Anthony Lucci, Linda Mackie McCall, Patrick W. Whitworth, Peter W. Blumencranz, A. Marilyn Leitch, Sukumal Saha, Kelly K. Hunt, Armando E. Giuliano

	ACKNOWLEDGMENTS

 
We thank Brenda Reid, Department of Surgical Oncology, and Angelique Siy, Department of Scientific Publications, the University of Texas M.D. Anderson Cancer Center, for their assistance in manuscript preparation.

	NOTES

 
published online ahead of print at www.jco.org on July 23, 2007.

Supported by the National Cancer Institute Grant No. U10-CA76001-09.

Presented in part at the Annual Meeting of the Society of Surgical Oncology, March 23-26, 2006, San Diego, CA.

Authors' disclosures of potential conflicts of interest and author contributions are found at the end of this article.

	REFERENCES

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Submitted November 21, 2006; accepted March 6, 2007.

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