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Original Article |
1 Department of Surgery, Duke University Medical Center, Durham, North Carolina
2 American College of Surgeons Oncology Group, Duke University Medical Center, Durham, North Carolina
3 Nashville Breast Center, Nashville, Tennessee
4 Lakeland Regional Cancer Center, Lakeland, Florida
5 Department of Surgery, University of Texas Southwestern Medical Center, Dallas, Texas
6 Department of Surgery, Emory University School of Medicine, Atlanta, Georgia
7 Department of Surgical Oncology, The University of Texas M. D. Anderson Cancer Center, Houston, Texas
8 Department of Surgical Oncology, H. Lee Moffitt Cancer Center, Tampa, Florida
9 Department of Surgical Oncology, John Wayne Cancer Institute, 2200 Santa Monica Boulevard, Santa Monica, California 90404
Correspondence: Address correspondence and reprint requests to: Armando E. Giuliano, MD; E-mail: giulianoa{at}jwci.org.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Methods: Eligible patients included women with clinical T1/2N0M0 breast cancer. Surgical outcomes were available at 30 days and 6 months after surgery for 5327 patients. Patients who had a failed sentinel node mapping (n = 71, 1.4%) or a completion lymph node dissection (n = 814, 15%) were excluded. Univariate and multivariate analyses were performed to identify predictors for the measured surgical complications.
Results: In patients who received isosulfan blue dye alone (n = 783) or a combination of blue dye and radiocolloid (n = 4192), anaphylaxis was reported in .1% of subjects (5 of 4975). Other complications included axillary wound infection in 1.0%, axillary seroma in 7.1%, and axillary hematoma in 1.4% of subjects. Only increasing age and an increasing number of sentinel lymph nodes removed were significantly associated with an increasing incidence of axillary seroma. At 6 months, 8.6% of patients reported axillary paresthesias, 3.8% had a decreased upper extremity range of motion, and 6.9% demonstrated proximal upper extremity lymphedema (change from baseline arm circumference of >2 cm). Significant predictors for surgical complications at 6 months were a decreasing age for axillary paresthesias and increasing body mass index and increasing age for upper extremity lymphedema.
Conclusions: This study provides a prospective assessment of the sentinel lymph node biopsy procedure, as performed by a wide range of surgeons, demonstrating a low complication rate.
Key Words: Breast cancer • Sentinel lymph node • Complications • Biopsy
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The interest in SLNB, both the technique and its outcomes, has been intense, with >800 articles published in the English medical literature in the past 5 years.10 One of the primary issues discussed in this body of literature is the morbidity associated with SLNB in comparison to that of a standard level I and II axillary lymph node dissection (ALND).10–15 With improved technology in breast imaging, the number of early-stage breast cancers is expected to increase over time, thereby decreasing the relative number of women with axillary metastases.16 Although local and regional control and improved survival are the major therapeutic goals for breast cancer treatment, limiting treatment-related morbidity and optimizing functional outcomes will become increasingly important in women with early-stage breast carcinoma. By removing only the node(s) most likely to contain metastases, the sentinel node procedure potentially avoids the complications commonly described for ALND. These complications include a reduced range of motion in the upper extremity, axillary paresthesias, and upper extremity lymphedema.17–22
In 1999, the American College of Surgeons Oncology Group (ACOSOG) opened the Z0010 clinical trial with the primary objective of determining the prognostic significance of micrometastases in the sentinel lymph node (SLN) and bone marrow of women with clinical T1/2N0 breast cancer. This trial completed accrual in May 2003 with 5539 patients. Each of the patients enrolled in this prospective study had intraoperative SLN mapping and dissection. We present here the 30-day and 6-month surgical morbidity for the SLNB procedure only.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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. The primary objectives for this trial were (1) to estimate the prevalence and evaluate the prognostic significance of sentinel node micrometastases detected by immunohistochemistry, (2) to estimate the prevalence and evaluate the prognostic significance of bone marrow micrometastases detected by immunocytochemistry, and (3) to determine the hazard rate for regional recurrence in women whose sentinel nodes were negative by hematoxylin and eosin staining. The primary study end point was overall survival, with secondary end points of distant disease–free survival and axillary recurrence. This prospective study was approved by the National Cancer Institute and the institutional review board of each participating institution. Before patient enrollment, 198 participating surgeons completed a skills-verification requirement. This consisted of 20 consecutive SLNB procedures with ALND or completion of an oncology fellowship or residency program with adequate SLNB training documented by the program director. The participating surgeons had to demonstrate an identification and accuracy rate of 
85% when performing the SLNB procedure before patients were enrolled on Z0010.
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Requirements for study participation included a negative pregnancy test and a functional status (Eastern Cooperative Oncology Group/Zubrod) score of 2. Women with prior malignancies had to be free of disease for 5 years. Exclusion criteria included multicentric disease, neoadjuvant systemic therapy, a prepectoral breast implant, or prior ipsilateral axillary surgery. Before registration, women were asked to read and sign a written informed consent document.
Surgery
The operative procedure for ACOSOG Z0010 participants consisted of bilateral anterior iliac crest bone marrow aspiration, SLNB, and segmental mastectomy. Bone marrow aspiration was not a requirement for participation in the initial phase of the trial. Educational materials for this aspect of the procedure were provided to each participating surgeon. The segmental mastectomy was performed according to the individual surgeon’s technique but required documentation of negative pathologic margins, as determined by the local pathologist, before whole-breast irradiation. Patients remained eligible if they required a re-excision segmental mastectomy procedure to attain pathologically negative margins. The third component of the operative procedure was the SLNB. The SLN procedure could be performed with isosulfan blue dye, a radiopharmaceutical, or a combination of the two. The volume of injection, the timing of the injections, and the site of the injections within the breast were determined by the individual surgeon. Recommendations for the procedure were provided in the protocol document, but each surgeon was permitted to perform the procedure according to his or her individual training. While ACOSOG Z0010 was open to accrual, isosulfan blue dye was unavailable from the manufacturer for a short time. Methylene blue was therefore used in a small number of patients. These patients were not eliminated from the analyses. If the patient had a medial hemisphere lesion, defined as the entire mass medial to the medial edge of the areola, lymphoscintigraphy or documented intraoperative gamma counting was required to confirm axillary drainage. At the completion of removal of the blue and/or hot nodes, any remaining axillary nodes that were suspicious based on palpation were removed and considered SLNs. If an axillary SLN could not be identified, a full ALND was performed.
Surgical Outcomes
Surgical side effects for the SLNB procedure were recorded within 30 days and at 6-month intervals to year 3 and then annually thereafter. Short-term surgical effects documented at day 30 included allergic reaction to the isosulfan blue dye, wound infection, axillary seroma, axillary hematoma, axillary paresthesia, and brachial plexus injury. Each of these outcome assessments was determined by the treating physician’s physical examination of the patient. Allergic reaction to the isosulfan blue dye was documented by the treating physician as mild, moderate, or severe. Collected data included the type of treatment as either inpatient or outpatient. The individual source documentation for each patient who had a reported allergic reaction to the isosulfan blue dye was reviewed centrally and re-evaluated and reported by using the standard Common Toxicity Criteria (CTC). The CTC grade allergic reaction to an injected substance in the following manner: (1) transient flushing or rash; (2) rash, flushing, urticaria, or dyspnea; (3) bronchospasm, edema, or hypotension; and (4) anaphylaxis. Ultrasound evaluation was not used to confirm a physician-documented axillary seroma or hematoma.
Long-term surgical effects documented at 6-month intervals included evidence of axillary paresthesia, lymphedema, and brachial plexus injury. The follow-up arm assessment documented the arm circumference both 10 cm distal and proximal to the medial epicondyle at 30 days, 6 months, and annually thereafter. Lymphedema was defined as an increase of 2 cm from the presurgical arm measurement when compared with the contralateral arm:
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where I indicates ipsilateral; C indicates contralateral, P indicates proximal, FU indicates follow-up, and B indicates baseline. The ipsilateral shoulder range of motion was also documented at these time points and was defined as degrees of abduction from a 45° angle to a maximum of 180°. Clinical site audits were performed to validate, via source documentation, the data provided to ACOSOG. Audits were performed in accordance with guidelines provided by the Clinical Trials Monitoring Branch of the National Cancer Institute.
Statistical Analysis
Frequency distributions were used to summarize the characteristics of patients and the frequency of adverse effects and surgical complications and morbidity. Contingency tables, 
2 tests, and logistic regression were used to model the effect of individual patient clinical characteristics, including age (two outcomes: 10-year increments and <70 years old vs. 70 years old), body mass index (BMI; five categories defined as <18.5, 18.5–24.9, 25–29.9, 30–49.9, and >50 kg/m2), the number of SLNs removed (two outcomes: 1, 2, 3, 4, and 5 and 
4 vs. 5), and the SLN identification technique used (isosulfan blue, radio-pharmaceutical, or both). Multivariate logistic regression was also used to examine the joint effect of clinical predictors for surgical outcomes. All multivariate logistic regression models were fit by using backward stepwise procedures, and only data sets that were complete for every outcome analyzed were used. For outcomes that had more than one significant predictor, Hosmer-Lemeshow goodness-of-fit indices were used. All analyses were performed with SAS statistical analysis software (SAS Institute, Cary, NC).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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. The median age for these 5327 patients was 56 years (range, 23–95 years). Twenty-four percent of the patients had metastases in the SLN detected by hematoxylin and eosin staining. The average number of SLNs removed was 2.3. The median BMI was 26.4 kg/m2 (range, 14.6–72.6 kg/m2). With the exception of analysis for allergic reactions to the isosulfan blue dye, patients who had a failed SLN mapping (n = 71, 1.4%) or those who received a subsequent completion ALND (n = 814, 15%) were excluded from the analysis. Of the 5327 assessable patients, 885 were eliminated from the 30-day analysis. Of the remaining 4442 patients, 373 were excluded as a result of incomplete demographic data. For the 30-day morbidity outcomes, therefore, 4069 patients had data available for analysis. For each of the 6-month surgical outcomes, the sample size varied depending on the data provided from the sites on the individual categories of axillary paresthesias, range of motion, and lymphedema (as determined by arm measurements). As a new organization that encouraged participation from a wide range of surgeons from around the United States and the international community, ACOSOG provided educational sessions regarding data management for surgeons who had not previously participated in clinical trials. Not all surgeons participated in these educational sessions, and as a result, the number of patients with 6-month data available for statistical review varied for each of the outcome parameters. Arm circumference measurements and, therefore, lymphedema rates were infrequently reported because of patient follow-up outside the surgeon’s customary practice.
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The 30-day operative morbidity for the SLNB procedure is listed in Table 2. No operative mortality was documented during this study. Data were assessable for 4069 patients. Patients with five or more SLNs removed had a significantly greater incidence of axillary wound infection compared with those who had four or fewer SLNs removed (2.1% vs. 9%; P = .02). No clinical parameters were significantly associated with the incidence of axillary hematoma. Multivariate logistic regression revealed that age 70 years, a pathologic SLN count 5, and the use of a radiopharmaceutical alone were significantly associated with the development of an axillary seroma. Table 3 details the odds ratios for each of these variables. Patients who were at least 70 years old were 2.4 times more likely to develop an axillary seroma than their younger counterparts. Patients who had five or more SLNs removed were 3.1 times more likely to experience axillary seromas than those who had four or fewer SLNs removed. Patients who were mapped with the radiopharmaceutical technique alone were 1.8 times more likely to experience axillary seromas than those who had mapping with either blue dye alone or a combination technique. Hosmer-Lemeshow goodness-of-fit analysis of axillary seroma confirmed the appropriateness of the multivariate model (P = .657).
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Six months after the procedure, 8.6% (307 of 3573) of patients were reported as having axillary paresthesias. Among these 307 patients with paresthesias, 282 (92%) indicated that the paresthesias were mild. In multivariate analysis, both decreasing age (P = .0004; odds ratio, .79; 95% confidence interval (CI), .71–.87) and the use of radiopharmaceutical alone (P = .0004; odds ratio, 2.22; 95% CI, 1.51–3.28) were significantly associated with the presence of paresthesias. Table 4 shows the linear association between paresthesias and decreasing age. The Hosmer-Lemeshow goodness-of-fit analysis confirmed the accuracy of the model (P = .841).
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20°. In multivariate analysis, only the patients whose SLNB was performed with radiopharmaceutical alone had a significant (P = .0008) decrease in the range of their upper extremity range of motion after SLNB.
The occurrence of lymphedema 6 months after SLNB was determined by the patient’s arm circumference measurements. These measurements, taken both 10 cm proximal and distal to the medial epicondyle, were compared with presurgical measurements. A change of >2 cm from baseline when compared with the contralateral arm was defined as evidence of lymphedema. In 2904 patients from whom data were available, 7% had lymphedema. In multivariate logistic analysis, increasing age and increasing BMI were significantly associated with the incidence of lymphedema, as shown in Table 5. The odds ratios for these two clinical parameters are listed in Table 6. With each decade increase in age, there was a 1.4 times increased likelihood of having lymphedema 6 months after SLNB. With each incremental increase in BMI by 5 kg/m2, there was a 1.1 times increased incidence of postoperative lymphedema (Hosmer-Lemeshow goodness of fit; P = .644).
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2 association analysis, 7.3% of patients who received whole-breast radiotherapy and 9.9% of patients not receiving the radiation treatment had lymphedema as documented by arm circumference measurements (P = .112). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The Z0010 trial was an international multicenter prospective trial that permitted the use of several techniques for identification of the sentinel node. Once the surgeon documented skills verification with the procedure, the technical details were left to the discretion of the individual surgeon. Most patients (4978) entered onto ACOSOG Z0010 were mapped with the aid of isosulfan blue dye, either alone or in combination with a radioisotope. Isosulfan blue dye (Lymphazurin; US Surgical Corp.) is a vital blue dye that is taken up by the lymphatic channels and entrapped within the primary draining nodal basin. Over the past 15 years, this dye has been used extensively for lymphatic mapping in patients with melanoma and breast cancer. In the Z0010 study, five (.1%) patients had a documented anaphylactic reaction when the blue dye was used. A recent comprehensive review of the literature describing allergic reactions to isosulfan blue dye revealed 1 to 12 cases of anaphylaxis in each series, with incidence rates up to 2%.25 The largest series, from Memorial Sloan-Kettering Cancer Center in New York (2392 patients), described a .5% incidence of hypotension and a 1.6% incidence of allergic reactions to isosulfan blue dye.26 None of the published series reported deaths from an anaphylactic reaction to the isosulfan blue dye. Despite attempts to define high-risk patients, there are no known allergic associations that can identify patients who should not receive isosulfan blue dye.25–29 The NSABP investigators recently reported the incidence of allergic reactions to isosulfan blue dye in the B-32 trial to be <1%.24 This is comparable to the rate seen in the Z0010 trial and highlights the rare but important incidence of this allergy.
Analysis of the 30-day operative morbidity for the SLNB procedure demonstrated a low rate of complications associated with this operation performed by a wide range of surgeons in both academic and community hospitals. The variables included in the univariate and multivariate analyses were selected on the basis of their published associations with the complications of both SLNB and ALND. In the ACOSOG Z0010 trial, the outcomes were reported from data collected by the surgeon at 30 days after SLNB. The clinical sites were asked to report the interventions required to treat each outcome: drainage, operative re-exploration, or antibiotic treatment.
The axillary wound-infection rate for 4069 patients in ACOSOG Z0010 was 1.0%, and .1% required inpatient treatment with antibiotics. The reported incidences of wound infection after axillary node dissection range from 6% to 19%.30,31 For ACOSOG Z0010 patients with more than five SLNs removed, the incidence of axillary wound infection increased from .9% to 2.1%. Although this study was not a randomized study and additional clinical parameters were not equalized, this significant trend suggests that with more extensive dissection, the risk of infectious complications increases. Investigators from the ALMANAC trial reported that the incidence of axillary infection was significantly reduced in the patients who underwent SLNB alone as compared with those who had SLNB with ALND (P = .035).23 It is interesting to note that in ACOSOG Z0010, increasing age and BMI did not influence the wound-infection rate. The axillary hematoma rate was also not significantly associated with the selected demographic variables. The re-exploration rate for hematoma evacuation after SLN biopsy was low (.3%) and was not associated with the number of SLNs removed.
Axillary seromas are an expected outcome after ALND, and the great majority of patients have a drain placed to evacuate the fluid for 4 to 10 days after surgery.32,33 Several studies have examined the possibility of eliminating drains in patients who undergo ALND, with limited success.34–37 In 1995, Jeffrey et al.37 described the outcomes in 81 patients treated without a drain after ALND. Aspiration of a seroma was required in 34% of the patients. Zavotsky et al.35 found that 50% of patients (n = 43) without a drain placed after ALND required seroma aspiration, and Roses et al.38 reported a 59.5% incidence of seromas requiring aspiration. In each of these studies, >10 axillary lymph nodes were removed during the ALND, thus indicating that seroma formation occurs in 30% to 60% of patients undergoing ALND: this is much greater than the rate reported for patients undergoing SLNB in the Z0010 trial.
In comparing ALND with SLNB, several studies have highlighted the differences in seroma formation and drainage. Giuliano et al.11 described a 1.5% incidence of axillary seroma formation in patients undergoing SLNB and a 15% incidence in patients with SLNB followed by ALND, despite the use of a closed-suction drainage catheter after ALND. Burak et al.39 compared their outcomes in patients undergoing SLNB versus those undergoing SLNB plus ALND and discovered that the patients who had SLNB alone did not experience postoperative seromas (n = 49). In a similar study, Schrenk et al.40 reported no axillary seromas in their SLNB subgroup versus a 48% requirement for axillary seroma drainage after catheter removal in patients who underwent ALND (48 per study group). In the Z0010 trial, 290 (7.1%) patients were reported as having a seroma. Sixteen (.4%) patients required placement of a drainage catheter after surgery. In multivariate analysis, increasing age, an increasing number of SLNs removed, and the use of a radiopharmaceutical alone were significantly associated with the presence of seromas. Increasing age and seroma formation were similarly reported by Burak et al.36 in a study evaluating the use of thrombin to prevent seroma formation. The increased rate of seroma formation with more SLNs removed is intuitive. What was unexpected was the increased seroma rate with the use of a radiopharmaceutical alone for the SLNB procedure. Because this was a small group of patients (n = 302) registered by 35 surgeons, this may be the result of increased dissection to reach the first SLN that is not "highlighted" by the isosulfan blue dye or, more likely, may be a clinically nonsignificant statistical finding.
The reported incidence of brachial plexus injuries at 30 days was .2% (seven patients). It is unclear whether this outcome can be attributed to the surgical procedure itself or to the patient’s arm placement during surgery. In six of seven patients, however, this outcome was no longer present at 6 months, thus highlighting the fact that it was most likely a complication of arm placement versus the nodal dissection.
Axillary paresthesia data were available at 6 months after SLNB for 3573 patients. Three hundred seven (8.6%) patients reported axillary paresthesias. This study provided subjective data from the surgeons’ interviews of their patients and did not require neurological examination. Various studies have documented a wide range (7%–75%) of outcomes for axillary paresthesias or numbness after ALND. 38–43 In studies evaluating SLNB versus ALND, the incidence of this complication is consistently reported to be lower for SLNB patients than for patients who undergo ALND. Veronesi et al.,15 in a randomized study comparing SLNB with ALND, found a 2% incidence of axillary paresthesias in the SLNB group versus 85% in the ALND cohort. In a follow-up survey of 247 women who had either SLNB or ALND, at 6 months 30% of SLNB respondents had axillary numbness, versus 82% of ALND respondents.44 Burak et al.39 reported a 16% (n = 48) incidence of arm numbness in follow-up from SLNB, in comparison to 81% (n = 48) for patients with ALND. The only study to report comparable incidences between the SLNB and ALND cohorts evaluated patients at 6 weeks after the procedure. At that time point, 64% of SLNB patients and 70% of ALND patients reported axillary numbness.14 Criticisms of this study highlight the early learning curve for the surgeons involved in the study; this may have led to an increased dissection in the axilla to identify the SLNs.45 Despite these findings, the cumulative review of axillary paresthesias after SLNB reveals a decreased incidence compared with ALND. Our study highlights the low incidence of this complication (8.6%) at 6 months after the procedure.
On multivariate analysis, decreasing age was significantly associated with the incidence of axillary numbness. This finding has been noted by several other authors in both ALND and SLNB patients.21,44
The upper extremity abduction 6 months after the procedure was decreased in 3.8% of patients in AC-OSOG Z0010 (n = 3071). In 2002, Swenson et al.44 described a low incidence of changes in range of motion of the ipsilateral upper extremity in patients undergoing SLNB. Patients undergoing both SLNB and ALND, however, had incidences of <15% at 6 months after the procedure. Shrenk et al.40 reported no decrease in the range of motion in their study of 35 patients undergoing SLNB, whereas 6 of 35 patients had limitations in arm mobility after ALND. Similarly, the ALMANAC trial reported nonsignificant differences between the SLNB and ALND groups at 6 months after the procedure for shoulder flexion and abduction.46 These studies support our findings that most (63%) patients with a range-of-motion deficit had a small change (<20°) from baseline function. It will be important to evaluate 12- and 24-month follow-up data to determine whether there is resolution of the range-of-motion deficits in these 115 patients.
Lymphedema remains the most published complication of ALND.47–57 Because of the long-term sequelae of this complication, this surgical outcome is an important measurement when a replacement procedure for ALND is evaluated. In the Z0010 study, 2904 patients had arm circumference data both before surgery and again 6 months after surgery available for analysis. Lymphedema was defined in this study as a change in arm circumference of >2 cm when compared with the contralateral or control arm and with baseline measurements. Previous authors have used this definition for upper extremity lymphedema, yet this definition is not standardized, and other definitions include changes in arm circumference of 5% to 10%.15,17,32,38 Seven percent of the patients had a change in arm circumference >2 cm. Increasing age and BMI were significantly associated with this outcome. Others have confirmed these associations: most notably, the risk of lymphedema with obesity.21,38,50,55,58 Other investigators have reported a 0% incidence of lymphedema with SLNB.15,40 The most recent studies of lymphedema after ALND report incidences of lymphedema in the 7% to 20% range.32,38,44,55 ACOSOG Z0010 identified a lower, but not negligible, rate of lymphedema for patients undergoing SLNB. In addition, the effect of whole-breast radiation on this early lymphedema rate seems to be nonsignificant but may change as the data mature over the next 5 years, when the full effects of radiation are realized. Once data from both NSABP B-32 and ACOSOG Z0011 mature, the difference in rates of lymphedema between patients undergoing SLNB and those undergoing ALND will be assessed. In the ALMANAC trial, lymphedema rates were most prominent at 3 months after surgery but remained significantly different between the two groups at 18 months after the procedure.46
ACOSOG Z0010 is a large prospective clinical trial evaluating the use of SLNB in early-stage breast cancer patients undergoing breast-conserving surgery. In this article, we present the morbidity associated with the SLNB procedure and highlight the fact that despite a surgeon skill requirement, the procedure is not without complications. This initial data suggest that sentinel node biopsy is a safe alternative to axillary node dissection in women with early-stage breast cancer. Additional data are required to assess the significance of micrometastases in this patient population regarding long-term survival and local-regional recurrence patterns.
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ACKNOWLEDGMENTS |
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Received for publication June 8, 2005. Accepted for publication November 9, 2005.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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