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10.1245/ASO.2005.03.050
Annals of Surgical Oncology 12:41-47 (2005)
© 2005 Society of Surgical Oncology
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Original Article

Beyond the Clinical Trials: How Often Is Sentinel Lymph Node Dissection Performed for Breast Cancer?

Melinda A. Maggard, MD1,2, Karen E. Lane, MD3, Jessica B. O’Connell, MD2,4, Deepa Dharshani Nanyakkara2 and Clifford Y. Ko, MD, MSHS2,4

1 Robert Wood Johnson VA Clinical Scholars Program, 911 Broxton Avenue, 3rd Floor, Los Angeles, California 90024
2 Department of Surgery, UCLA School of Medicine, 10833 Le Conte Avenue, CHS, Room 72-215, Los Angeles, California 90095
3 Department of Surgery, UCSF School of Medicine, 1600 Divisadero Street, Box 1710, San Francisco, California 94143
4 Department of Surgery, West Los Angeles Veterans Affairs Medical Center, 11301 Wilshire Boulevard, Building 304, Room E3-207, Los Angeles, California 90073

Correspondence: Address correspondence and reprint requests to: Melinda A. Maggard, MD, Department of Surgery, UCLA School of Medicine, 10833 Le Conte Avenue, CHS, Room 72-215, Los Angeles, CA 90095; E-mail: mmaggard{at}mednet.ucla.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Sentinel lymph node dissection (SLND) has been shown to be a reasonable treatment option for early-stage breast cancer. Until recently, SLND was limited to clinical trials. Because this technique is now offered outside of trials, its prevalence is unknown.

Methods: All patients with stage I or II breast cancer in the Surveillance, Epidemiology, and End Results national cancer registry (1998–2000) were evaluated. Data were collected for demographics, tumor characteristics, surgical resection, lymph node evaluation (SLND or complete axillary dissection), registry site, and year of diagnosis. Multivariate regression analysis was performed to identify predictors for receiving SLND.

Results: A total of 54,772 patients diagnosed with breast cancer had undergone surgical lymph node evaluation; 27.2% patients with stage I disease underwent SLND, as compared with 22.7% for stage II. Older patients and minority groups were less likely to receive SLND. Receipt of SLND varied by registry site (7.9%–32.7%). Multivariate regression showed that older patients had lower odds of receiving SLND (60–69 years: odds ratio, .73; P < .0001) as compared with younger patients. Additionally, blacks, Hispanics, and Asians had lower odds of receiving SLND (odds ratio of .64, .58, and .80, respectively; P < .0001). SLND use increased over the 3 years in the study (P < .0001).

Conclusions: This population-based analysis showed relatively infrequent use of SLND for early-stage breast cancer. These results suggest a slow transition of this procedure from clinical trials into the community. Future work should be targeted at improving the rate at which patients receive this procedure, particularly for elderly and minority groups and low-use regions.

Key Words: Breast cancer • Administrative data • Sentinel lymph node dissection • Quality of care


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Nodal staging is an important component of evaluating patients with breast cancer. The "gold standard" has long been complete axillary dissection; however, this procedure is associated with morbidity, including damage to nerves and blood vessels, postoperative pain, limited arm mobility, and lymphedema. A less invasive method of evaluating the axillary lymph nodes was sought and subsequently developed by Giuliano et al.,1 who reported the use of sentinel lymph node dissection (SLND) for breast cancer staging in 1994. Numerous studies have since validated the high sensitivity and specificity for this procedure and have confirmed that in experienced hands, SLND for early-stage breast cancer predicts the presence or absence of axillary lymph node metastases.2,3 When the procedure is performed for small breast tumors, an estimated 60% to 80% of patients will have sentinel nodes that are free of tumor. This substantially decreases the need for subsequent complete axillary lymph node dissection (ALND).1,4–6 Furthermore, SLND has significantly lower short-term morbidity (i.e., numbness, pain, and mobility) and lymphedema as compared with ALND.7–9 For example, lymphedema rates after SLND range from 0% to 2%, versus 10% to 30% for ALND.

Although many benefits associated with this procedure have been documented, it is important to emphasize that the adoption of the procedure requires coordinated efforts by a multidisciplinary team involving nuclear medicine and pathology, along with surgery. Furthermore, there is a significant learning curve for the technical aspects of the operation. Studies have shown that the rates of both sentinel lymph node identification and false-negative results improve as the surgeon gains more experience.10–11 False-negative rates of <5% after the initial learning curve are considered acceptable.

Over the past 10 years, SLND has markedly increased. Most academic centers routinely offer SLND for patients deemed appropriate—i.e., those with early-stage tumors without contraindications. In one study, Edge et al.12 reviewed data from five cancer centers in the United States and found that the rates of SLND increased from 8% in 1997 to 58% in 2000. Lucci et al.13 published a report surveying breast surgeons who were Fellows of the American College of Surgeons and found that 77% of responders performed SLND. However, this was a highly selected group of surgeons who may not represent practice patterns of the community at large.

Many breast cancer experts would argue that SLND is becoming the standard of care for the treatment of breast cancer. The question that remains is how prevalent is the use of this technique in the community? In addition, are there disparities in the receipt of SLND? We used a large national tumor registry to measure the use of this procedure across the nation and to identify predictors of who receives the procedure relative to those who do not.

The aims of the project were 5-fold: (1) to measure the use of SLND for early-stage breast cancers at a population-based level, (2) to determine whether disparities in the use of the procedure exist (e.g., age or race/ethnicity), (3) to determine whether patterns of use vary among registry sites, (4) to measure trends in use over the 3 years of the study, and (5) to identify predictors for use of this procedure.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
All female patients with a diagnosis of breast cancer recorded in the Surveillance, Epidemiology, and End Results (SEER) cancer registry from 1998 to 2000 were analyzed. The diagnosis was based on primary tumor location (i.e., breast), along with International Classification of Diseases, 9th revision, histology codes. Only patients with stage I (tumors ≤2 cm without nodal involvement) or stage II (tumors >2 cm to ≤ 5 cm without fixed nodes and >5 cm without nodal involvement) disease were selected for the analysis. Histologies corresponding to squamous cell, spindle cell, carcinoid, sarcoma, Paget’s disease, and in situ tumors were excluded from the analysis.

SEER collects patient records from multiple sites across the United States and is one of the better contemporary population-based tumor registries. This national program includes 12 regional registries, which capture approximately 14% of the population. The database was designed to reflect the overall characteristics of the United States, including the spectrum of racial/ethnic groups, geographical locations, and types of cities.

Patient Demographics
Demographics recorded for each patient included age at diagnosis (<40, 40–49, 50–59, 60–69, 70–79, and ≥ 80 years), race/ethnicity (i.e., white, black, Hispanic, Asian, and other), and marital status (single/not married vs. married). The tumor registry site where each patient was treated was also reported, which included entire states or cities (Los Angeles, San Jose–Monterey, Seattle–Puget Sound, Hawaii, Iowa, Utah, Connecticut, Alaska, New Mexico, Detroit-Metropolitan, Atlanta, and San Francisco). The year of diagnosis (i.e., 1998, 1999, and 2000) was also collected.

Tumor Characteristics
Tumor-specific information collected included tumor grade (i.e., well, moderately, or poorly differentiated or undifferentiated) and tumor stage (i.e., IandII).

Surgical Treatment
The type of surgical resection patients underwent was recorded as lumpectomy versus mastectomy, and whether or not patients underwent evaluation of the axillary lymph nodes was determined. We examined those who underwent SLND (with or without ALND) versus ALND alone.

Statistical Analysis
Chi-square analysis was completed for the previously described categorical comparisons; P values <.05 were considered to be statistically significant. Multivariate logistic regression was performed to identify predictors of the receipt of SLND for stage I and stage II disease. Patients who did not receive any evaluation of the axillary lymph nodes were excluded from the regression analysis. Age group, race/ethnicity, tumor grade, tumor stage, marital status, registry site, year of diagnosis, and type of surgical resection were controlled for in the model. All statistical analyses were completed with SAS version 8.01 (SAS Institute, Cary, NC) or Stata version 7.0 (Stata Corporation, College Station, TX).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Information on 61,474 patients with stage I or stage II breast cancer was collected. Most of these patients underwent surgical evaluation of their axillary lymph nodes: 85% of stage I and 94% of stage II patients underwent SLND or ALND. A total of 9.0% of stage I patients underwent SLND alone, and 14.2% had SLND followed by ALND, as compared with 4.6% of stage II patients who underwent SLND alone and 16.9% who had SLND followed by ALND (Table 1Go).


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  		TABLE 1. Receipt of sentinel lymph node dissectiona
 
Demographics
From the original cohort, 54,772 stage I or II breast cancer patients underwent some form of surgical lymph node evaluation. Slightly more than 50% of these patients had stage I disease. The average age for this group was 61.0 years (SD, 14 years), and 25% of patients were in the 50- to 59-year-old age group (Table 2Go). Race/ethnicity breakdown was reflective of the US population, with 76.1% whites, 7.5% blacks, 7.1% Hispanics, and 6.4% Asians. Almost 60% of patients were single (not married), and patients were evenly disbursed by year of diagnosis for the 3 years covered in the study (i.e., approximately 33% in each). More patients underwent lumpectomy (55% ) as compared with mastectomy (45%).


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  		TABLE 2. Demographics for stage I and II breast cancer patients: SEER 1998–2000a
 
Univariate Analysis: Receipt of SLND
Early-stage breast cancer patients (stage I and II) underwent SLND in 25.1% of cases (Table 3Go). Stage I patients were somewhat more likely (27.2%) to receive SLND than were stage II patients (22.7%). Receipt of SLND was highest (28.0%) in the 40- to 49-year-old and 50- to 59-year-old age groups (Fig. 1Go). Patients in the older age groups (60–69, 70–79, and ≥80 years) were less likely to undergo SLND as compared with the 40- to 49-year-old and 50- to 59-year-old groups. Blacks (21.2%), Hispanics (21.5%), and Asians (23.1%) were also less likely to receive SLND as compared with white patients (26.1%; P < .05 for all; Fig. 2Go).


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  		TABLE 3. Receipt of sentinel lymph node dissection: stage I or II breast cancer patients undergoing axillary lymph node evaluationa
 


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  		FIG. 1. Receipt of sentinel lymph node dissection (with or without axillary lymph node dissection) varies by age group (stage I and II disease for individuals who underwent a lymph node dissection). *P < .05 compared with the 50- to 59-year-old group.

 


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  		FIG. 2. Receipt of sentinel lymph node dissection (with or without axillary lymph node dissection) varies by race/ethnicity (stage I and II disease for individuals who underwent a lymph node dissection). *P < .05 as compared with white patients.

 
Wide variations in the use of SLND were seen between the SEER registry sites, ranging from a low of 7.9% to a high of 32.7% (Table 4Go). Receipt of SLND was lowest for patients in Utah, Alaska, and Iowa (<18% for each) and highest in Seattle–Puget Sound, Atlanta, and Los Angeles (>30% for each).


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  		TABLE 4. Receipt of sentinel lymph node dissection (SLND) by registry site for stage I or II diseasea
 
The use of SLND increased >100% throughout the 3 years of the study. In 1998, SLND was performed in 13.5% of patients, as compared with 36.4% in 2000 (Fig. 3Go).



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  		FIG. 3. Receipt of sentinel lymph node dissection (with or without axillary lymph node dissection) varies by year of diagnosis (stage I and II disease for individuals who underwent a lymph node dissection). *P < .05 as compared with the year 2000.

 
Multivariate Regression: Receipt of SLND
Patients who underwent evaluation of their axillary lymph nodes—either by SLND (with or without ALND) or ALND alone—were analyzed via multivariate logistic regression, controlling for tumor stage/grade, marital status, registry site, year of diagnosis, and type of surgical resection (Table 5Go). Patients in the older age groups had lower odds of receiving SLND versus ALND. For example, patients in the 60- to 69-year-old group had an odds ratio (OR) of .73 (95% confidence interval [CI], .66–.80; P < .0001) relative to the <40-year-old age group.


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  		TABLE 5. Multivariate regression to identify predictors of receipt of sentinel lymph node dissectiona,b
 
Furthermore, minority racial/ethnic groups also had lower odds of receiving SLND. Blacks had an OR of .64 (95% CI, .58–.69), Hispanics had an OR of .58 (95% CI, .53–.64), and Asians had an OR of .80 (95% CI, .73–.89; P < .0001 for each; Table 5Go).

Wide variations in use of SLND were also seen by SEER registry site in the regression analysis, which controlled for clinical and demographic characteristics. For example, patients treated in Iowa had a lower OR of receiving SLND (OR, .18; 95% CI, .16–.20; P < .0001), as did those in Utah (OR, .44; 95% CI, .39–.49; P < .0001), as compared with those in Los Angeles.

Finally, the type of surgery performed was highly predictive of receipt of SLND. Patients undergoing mastectomy had a lower OR of receiving SLND (OR, .35; 95% CI, .33–.36; P < .0001) as compared with lumpectomy patients.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Our population-based findings show low to moderate rates of use of SLND for early-stage breast cancers. This national look at a staging procedure includes an assessment of practices beyond the academic centers, because it includes community hospitals. The somewhat low rates of SLND are not entirely unexpected given that adopting a new technique usually requires additional resources (e.g., nuclear medicine technology/access, trained pathologists, and surgeon training), and some regions or hospitals may not have achieved these goals. Elderly patients (those ≥ 60 years old) were less likely to receive SLND. There are two opposing arguments about the benefit of SLND in elderly patients, who are likely to have estrogen or progesterone receptor–positive tumors. Some believe that the nodal status for these patients will not tend to change future adjuvant therapy choices—particularly those in the oldest age groups—whereas others believe that identification of a negative sentinel lymph node would alter treatment options and that these patients may receive the greatest potential benefit from this procedure. Furthermore, significant differences in the use of SLND were also noted for even the 50- to 59-year-old age group. Disparities in SLND use were apparent for the minority race/ethnicity groups, thus implying that socioeconomic status or cultural beliefs may also play a role in the receipt of this technique. Wide regional differences in the use of SLND were also seen among SEER registry sites, and this may in part reflect a greater density of cancer centers in the high-use sites, as well as a disparity in resources such as nuclear medicine.

In comparison to the results found by Edge et al.12 (that rates of SLND in 1997–2000 were 58% in cancer centers), our results suggest a lower rate of SLND in the general medical community. It is noteworthy, however, that the use of the procedure increased substantially over the 3 years of our study (1998–2000). These findings are encouraging, and it is likely that the rates have continued to increase.

The literature strongly supports SLND for treating breast cancer. The National Cancer Institute initiated two large-scale cooperative clinical studies of SLND in 1999—the National Surgical Adjuvant Breast and Bowel Project B-32 and American College of Surgeons Oncology Group Z0010/Z0011 trials—to address the only remaining issues: whether SLND will offer the same regional tumor control and survival rates (in sentinel lymph node–positive patients) as is achieved with complete ALND.14–15 These trials are anticipated to be completed in 2007, and their findings will likely highlight the importance of maintaining quality-control measures for this procedure.

Although we describe data representing a large number of breast cancer cases, our study does have several limitations. First, the data were derived from a nationwide cancer registry, which has shortcomings with regard to data collection. Although trained on-site nurse coordinators are responsible for collecting data, there may be problems with coding. Additionally, using this cancer registry, we were unable to consider other clinically relevant issues, such as tumor location (e.g., quadrant of the breast), patient preference, previous axillary surgery, and pregnancy status, which would affect the decision to perform SLND.

However, there are many advantages to using the SEER database. SEER uses several quality-control measures to ensure accuracy. In fact, this registry maintains the highest level of certification of data quality and completeness, as reported by the North American Association of Central Cancer Registries.16 SEER adheres to strict quality-assessment measures by checking the accuracy of sample cases by reabstracting data from the medical records each year. The completeness of each case is approximately 98%, and the accuracy for reporting the receipt of radiation is >90%.17 The main advantages of our study are that we were able to evaluate a very large sample of breast cancer patients (n = 61,474) and that the data were generated from a population-based cancer registry. The results should therefore offer a nationally representative picture of practice patterns in the United States.

SLND should be made available to most early-stage breast cancer patients, because it is associated with lower rates of morbidity than ALND, and data support its accuracy as a staging tool. It is critical that the adoption of this procedure be a coordinated effort between multidisciplinary specialties, with an emphasis on quality control. Future research should be directed at determining why there are variations in the receipt of SLND and to work specifically toward improving rates of this procedure in the elderly, in minority racial/ethnic groups, and in low-use regions.


   ACKNOWLEDGMENTS
 
Supported by the Robert Wood Johnson Clinical Scholars Program, Veterans Affairs, UCLA.

Received for publication March 19, 2004. Accepted for publication September 20, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Giuliano AE, Kirgan DM, Guenther JM, et al. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 1994;220:391–8: discussion 398–401.[Medline]
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  3. Krag D, Weaver D, Ashikaga T, et al. The sentinel node in breast cancer—a multicenter validation study. N Engl J Med 1998;339:941–6.[Abstract/Free Full Text]
  4. Giuliano AE, Dale PS, Turner RR, et al. Improved axillary staging of breast cancer with sentinel lymphadenectomy. Ann Surg 1995;222:394–9; discussion 399–401.[Medline]
  5. Guenther JM, Krishnamoorthy M, Tan LR. Sentinel lymphadenectomy for breast cancer in a community managed care setting. Cancer J Sci Am 1997;3:336–40.[Medline]
  6. Martin RC II, Edwards MJ, Wong SL, et al. Practical guidelines for optimal gamma probe detection of sentinel lymph nodes in breast cancer: results of a multi-institutional study. For the University of Louisville Breast Cancer Study Group. Surgery 2000;128:139–44.[CrossRef][Medline]
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  8. Golshan M, Martin WJ, Dowlatshahi K. Sentinel lymph node biopsy lowers the rate of lymphedema when compared with standard axillary lymph node dissection. Am Surg 2003;69:209–11; discussion 212.[Medline]
  9. Roumen RM, Kuijt GP, Liem IH, et al. Treatment of 100 patients with sentinel node-negative breast cancer without further axillary dissection. Br J Surg 2001;88:1639–43.[CrossRef][Medline]
  10. Cox CE, Salud CJ, Cantor A, et al. Learning curves for breast cancer sentinel lymph node mapping based on surgical volume analysis. J Am Coll Surg 2001;193:593–600.[CrossRef][Medline]
  11. McMasters KM, Wong SL, Chao C, et al. Defining the optimal surgeon experience for breast cancer sentinel lymph node biopsy: a model for implementation of new surgical techniques. Ann Surg 2001;234:292–9; discussion 299–300.[CrossRef][Medline]
  12. Edge SB, Niland JC, Bookman MA, et al. Emergence of sentinel node biopsy in breast cancer as standard-of-care in academic comprehensive cancer centers. J Natl Cancer Inst 2003;95:1514–21.[Abstract/Free Full Text]
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