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Right arrow Sentinel lymph node
Annals of Surgical Oncology 8:13-19 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Complementarity of Blue Dye and Isotope in Sentinel Node Localization for Breast Cancer: Univariate and Multivariate Analysis of 966 Procedures

Hiram S. Cody III, MD, Jane Fey, MPH, Tim Akhurst, MD, Melissa Fazzari, PhD, Madhu Mazumdar, PhD, Henry Yeung, MD, Samuel D.J. Yeh, MD and Patrick I. Borgen, MD

From The Breast Service (Department of Surgery), Division of Nuclear Medicine (Department of Radiology), Department of Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Hiram S. Cody III. MD, Memorial Sloan-Kettering Cancer Center, 1275 York Avenue, NY, NY 10021; Fax: 212-794-5812; E-mail: codyh{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: The hypothesis that sentinel lymph node (SLN) mapping in breast cancer patients is optimized by combining blue dye and isotope is reasonable and intuitive. Despite this, few studies examine in detail the factors contributing to the success of these techniques, either individually or in combination.

Methods: During a time period of 21/2 years, 1000 consecutive patients at Memorial Sloan-Kettering Cancer Center had SLN mapping performed by using both blue dye and isotope, with preoperative lymphoscintigraphy (LSG). Among the 966 patients with invasive cancer, 12 variables were examined for their correlation with the success of SLN localization by blue dye, by isotope, and by the combined method, using univariate and multivariate models.

Results: By univariate analysis, blue dye success was more frequent in association with: a positive LSG (P = .02), age <=60 (P < .0005), a previous surgical biopsy (P = .03), and an outer quadrant tumor (P < .0005). Isotope success was more frequent with a positive LSG (P < .0005), age <=60 (P = .004), and intradermal isotope injection (P < .0005). Combined (dye and/or isotope) success was more frequent when there was a positive LSG (P < .0005), age <=60 (P = .006) and intradermal isotope injection (P < .0005).

In multivariate analysis, blue dye success remained uniquely associated with outer quadrant tumor location (P < .0005), and isotope success was uniquely associated with intradermal isotope injection (P = .012). Combined success was more frequent with a positive LSG (P < .0005), age <=60 (P = .033), and intradermal isotope injection (P = .003).

Conclusions: The five variables associated with successful SLN localization by blue dye or by isotope overlap but are not identical. Only three of these, intradermal isotope injection, a positive LSG, and age <60, predicted success by the dye-isotope combination in the multivariate model. Dye and isotope complement each other, and SLN biopsy for breast cancer should use both.

Key Words: Lymphoscintigraphy • —Sentinel node biopsy— • Breast cancer surgery.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Sentinel lymph node (SLN) biopsy represents a new standard of care for the patient with clinically node-negative breast cancer. Whether one uses blue dye, radioisotope, or both methods, SLN mapping is feasible and accurate. From 1993 to 1999, a series of 32 studies of SLN biopsy validated by a backup axillary dissection collectively confirmed that SLN can be found in 89% of cases, and that SLN biopsy detects nodal metastases in 93% of node-positive and 97% of all patients.1–32 Despite this wealth of published experience, the success of SLN localization varies widely (ranging from 66-100%), with little data and much controversy surrounding the most basic aspects of this exciting new technology. Which variables contribute significantly to the success of SLN mapping, and are these different whether a technique based on blue dye, isotope, or a combination is used? This report addresses these questions through a detailed univariate and multivariate analysis of the first 1000 SLN biopsies performed at Memorial Sloan-Kettering Cancer Center.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Between September 1996 and January 1999, 1000 patients had SLN biopsy at Memorial Sloan-Kettering Cancer Center. The methodology used and results of the first 60 cases,27 and of the first 500 cases,33 have been reported previously in detail.

Briefly, all patients had SLN mapping using a combination of isotope (99mTc-sulfur colloid) and blue dye. All had preoperative lymphoscintigraphy (LSG). Successful isotope mapping was defined as a ratio of SLN counts exceeding that of the postexcision axillary bed by at least 4–5 times. Successful blue dye mapping required the identification of a blue SLN or a blue afferent lymphatic vessel directly contiguous with a non-blue node.

Our technique of isotope preparation and injection evolved throughout this study. We previously reported comparisons of filtered vs. unfiltered isotope in 134 patients,34 and intraparenchymal vs. intradermal isotope injection in 200 patients,35 all of whom were included in this analysis. Excluded were 26 patients with intraductal carcinoma (DCIS), 4 patients in whom SLN biopsy was performed for suspicious breast lesions which proved to be benign, and 4 patients with missing data, leaving 966 cases for detailed analysis.

The frequency of successful SLN mapping as a function of 12 variables was analyzed separately for blue dye, for isotope, and for the combined method (SLN identified by dye and/or isotope), using both univariate and multivariate models. In the univariate model, the Fisher’s exact test was used to evaluate the significance of differences. The multivariate analysis employed stepwise logistic regression, with results expressed as odds ratios and 95% confidence intervals. SPSS statistical software (SPSS Inc., Chicago, IL) was used throughout.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
SLNs were identified by blue dye in 81% (785/966), by isotope in 87% (844/966), and by the combination of blue dye and isotope (i.e., dye and/or isotope) in 95% (922/966) of all patients. Results showed that 8–14% of SLN ( Table 1) and 11% of positive SLN ( Table 2) were identified by either dye alone or isotope alone.


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  		TABLE 1. Relative success of isotope and blue dye in finding the sentinel lymph node in 966 patients
 

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  		TABLE 2. Relative success of isotope and blue dye in finding the positive sentinel lymph node in 255 patients
 
In the univariate model ( Table 3), six histopathologic variables did not correlate with successful SLN identification: tumor size, type, multifocality/multicentricity, lymphovascular invasion, histologic grade, or nuclear grade. Blue dye was significantly more likely to be successful in patients with a positive LSG, an outer quadrant tumor, a previous surgical biopsy, and age <=60. Isotope was more likely to be successful with a positive LSG, intradermal injection of isotope, and age <=60. Dye and/or isotope were more likely to be successful with a positive LSG, intradermal injection, and age <=60.


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  		TABLE 3. Univariate analysis
 
In the multivariate model ( Table 4), blue dye was more likely to be successful with a positive LSG, outer quadrant tumor, and age <=60. Isotope was more likely to succeed with a positive LSG, intradermal injection, and age <=60. With the combined technique, dye and/or isotope success correlated with only three variables, a positive LSG, intradermal injection of isotope, and age <=60.


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  		TABLE 4. Multivariate analysis
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
This study is based on the hypothesis that the success of SLN mapping in breast cancer is optimized by the combined use of blue dye and isotope. Our initial pilot study of 60 cases,27 a detailed analysis of our first 500 procedures,33 and this series of 966 patients all support this concept; in 8–14% of cases the SLN (Table 1), and in 11% of cases the positive SLN (Table 2) were found by dye or isotope only and may have been missed by reliance on either method alone. To investigate this hypothesis in greater depth, we chose to examine in detail the variables which correlate with the success of SLN localization by dye, by isotope, and by the combined method.

Several caveats apply to this analysis. First, this study of SLN biopsy used both dye and isotope throughout, and was not specifically designed to test each method independently. We cannot eliminate the possibility that the results of each method were to some extent influenced by the other, and our findings should be considered valid only in the context of a dye-plus-isotope approach. Second, our technique (particularly regarding isotope) was not a constant and continued to evolve throughout the study period. Some of the patients were included in comparisons of filtered vs. unfiltered isotope34 and parenchymal vs. intradermal injection.35 Third, our results reflect the collective learning curve for the seven surgeons on our service and might be subject to inter-surgeon variation (although such variation was not significant in a learning curve audit of our first 500 procedures36). Finally, the goal of this study was to identify by univariate and multivariate analysis the variables which correlate with successful SLN localization, and not to establish the false-negative rate or accuracy of SLN biopsy. The extent to which these variables also correlate with an accurate result is the subject of separate studies.

Variables Not Correlated With Successful Mapping
Unfiltered Isotope
We previously reported34 that SLN localization by 99mTc-sulfur colloid was more successful with unfiltered (n = 77) than with a 0.22 µ filtered (n = 57) preparation: 88% vs. 73%. We continue to observe this difference for isotope success in the present study, although the difference loses significance. As our earlier study also demonstrated, the addition of blue dye ameliorated the deficiencies of filtered isotope and produced comparable overall success rates between the unfiltered and filtered groups.

Histopathologic Features
The success of SLN mapping did not correlate with any of the histopathologic features of the primary tumor (Table 3). Results (for dye, isotope, and the combined method) were comparable for T1 and T2–3 tumors, duct vs. lobular cancers, multifocal vs. non-multifocal lesions, present vs. absent lymphovascular invasion, and low vs. intermediate vs. high histologic/nuclear grade. The observation of more frequent isotope success with duct than with lobular cancers (88% vs. 81%) is of marginal significance (P = .06). The patients with multifocal/multicentric disease were usually identified in retrospect and represent only a subset of the multifocal/multicentric disease seen at our institution. Veronesi2,16 suggested that false-negative results might be more frequent in this group, and we share this concern. Most of our patients with clinically evident multicentricity were not considered candidates for SLN biopsy.

Univariate Correlates of Successful SLN Mapping
Intradermal Injection of Isotope
We previously demonstrated in a study of 200 consecutive operations by a single surgeon (HSC)35 that isotope localization of the SLN was significantly more successful with intradermal than with intraparenchymal injection. We confirm this finding in the present study, which now represents the collective experience of all our surgeons. The intradermal group succeeded significantly more often than the parenchymal group, both by isotope (92% vs. 84%), and by the combined method (98% vs. 93%). Intradermal isotope injection remains the single technical modification which has had the greatest impact in improving our ability to find the SLN.

Positive LSG
It comes as no surprise that a positive LSG is highly correlated with successful SLN localization by isotope. Virtually every SLN with sufficient isotope uptake to be imaged by a full-field-of-view gamma camera should be found at surgery using the far more sensitive hand-held gamma probe. Isotope identified the SLN in 94% of LSG-positive cases, and combined with blue dye in 99%. Less intuitive is the observation that a positive LSG strongly predicts SLN localization by blue dye (85% vs. 78%, P = .002). This may simply reflect the high correlation between dye and isotope success, because 73% of SLN were identified by both methods (Table 1). In addition, the discovery of a "hot" SLN may lead to the discovery of a blue SLN which might not otherwise have been found. Many surgeons using dye and isotope in combination will have experienced this in practice.

Outer Quadrant Tumor
Blue dye localization of the SLN succeeded significantly more often with outer than with central/inner quadrant tumors (85% vs. 75%). Tumor location did not significantly affect the success of SLN mapping by isotope or by the combined method. Route of injection may have biased this observation. Blue dye was always injected into the breast parenchyma, whereas isotope was injected intradermally in about half of the patients. Whereas isotope succeeds significantly more often with intradermal than with intraparenchymal injection, the same might be true for blue dye, especially with tumors further from the axilla. While Giuliano’s group, the most articulate and accomplished proponents of the blue dye technique, have recently reported from a series of 283 procedures that tumor location was unrelated to successful localization of the SLN,37 their own blue dye success rates for outer and central/inner quadrant tumors (82% vs. 78%) are strikingly similar to our own.

Previous Surgical Biopsy
Successful SLN localization in our first 500 cases33 and in the present study was unrelated overall to method of biopsy (fine needle, core needle, prior surgical, or concurrent surgical). However, blue dye was more successful in patients with a previous surgical biopsy than with a concurrent procedure (85% vs. 70%). The latter group of patients underwent surgery without a definite cancer diagnosis, and the tumor excision (with or without needle localization) was performed immediately prior to exploration for the SLN. In patients having concurrent surgical biopsy, we initially had difficulty with dye leaking back into the excision cavity or spilling into the axillary field of dissection. We have since learned to inject the dye prior to tumor excision (not into the wall of the excision cavity), thereby "capturing" intact lymphatics before they are disrupted by surgery, and to inject smaller volumes of dye for tumors close to the axilla, thereby minimizing the odds of axillary spillage. The blue dye technique may have a prolonged learning curve, and our own35,36 seems to parallel that reported by Giuliano.18,19 While his group reports no relation between the timing of biopsy and successful mapping,37 they do not distinguish between prior and same-day surgical biopsy. Notably, the timing of surgical biopsy in our own study had no impact on SLN localization by either isotope or the combined method.

Age <60
Younger age was a strong predictor of successful SLN mapping, both by dye (85% vs. 75%) and by isotope (90% vs. 82%). Despite improved success with the combined method, younger patients continued to show better results than those who were older (97% vs. 93%, P = .006). The advantage of combining dye and isotope for patients of all ages is particularly striking in this analysis. Moving from a single to a dual method of SLN localization, success in younger patients improved from 85–90% to 97%, and for older patients from 75–85% to 93%.

Multivariate Correlates of Successful Mapping
The multivariate analysis of these data is potentially limited by the high correlation between isotope and dye success, and by the possibility that each method might have influenced the success rate of the other. Despite these acknowledged limitations, it is striking that the variables which correlate with successful SLN mapping by dye and by isotope are not identical. Lateral tumor location was uniquely predictive of dye success, while intradermal isotope injection was uniquely predictive of success by isotope. Positive LSG and younger age were predictive of success by each method. Only three variables, two of them isotope-related, retained significance in the multivariate analysis for the combined technique: a positive LSG (P < .005), intradermal injection (P = .003), and age <=60.

Positive LSG
Whereas a positive LSG is the strongest predictor of successful mapping, the LSG imaged the SLN in fewer than half the procedures (Table 3). Although we continue to perform LSG in all patients having SLN biopsy for breast cancer, we agree with Burak et al.30 that intraoperative scanning with the hand-held gamma probe (and not the LSG per se) is the essence of the isotope technique. Although LSG is essential in defining unexpected patterns of lymphatic drainage in the patient with melanoma,38 and Jansen et al.39 have used LSG to demonstrate nonaxillary patterns of lymphatic drainage in as many as 19% of patients with primary breast cancer, the clinical relevance of this finding remains uncertain. For patients with early-stage breast cancer, an increasing proportion receive systemic adjuvant treatment regardless of nodal status, and clinical relapse in the supraclavicular, Rotter’s, internal mammary, or contralateral axillary nodes is a vanishing and rare event. For patients with Stage III disease, the group at greatest risk of locoregional relapse, most will receive adjuvant postmastectomy radiotherapy, thereby treating subclinical metastases in non-axillary sites: the internal mammary and supraclavicular nodes.

Intradermal Injection of Isotope
Intradermal isotope injection has dramatically improved our ability to find the SLN, both by isotope alone and with the combined technique. Although one might question whether the dermal and parenchymal lymphatics of the breast drain to the same SLN, Linehan et al.35 compared intradermal and parenchymal injection of isotope in a single-surgeon series of 200 consecutive patients (a subset of the present study, all of whom had intraparenchymal blue dye) and found that the same SLN was both blue and "hot" in 95% and 97% of cases, respectively. Furthermore, for 77 subsequent patients in whom SLN biopsy, using the intradermal technique, was followed by a planned backup axillary dissection,40 false-negative results were no more common than in our overall experience; only 3% of patients with T1–2 cancers (1 of 29 node-positive cases) had false-negative SLN.

Age <60
Younger age remains a significant predictor of successful SLN mapping by dye, by isotope, and by the combined method, even after using the multivariate analysis to correct for the substantial advantages of a positive LSG and intradermal isotope injection. This finding may reflect age-related differences in overall body mass, breast size, lymphatic flow, or the distribution and density of the lymphatic vessels draining the breast, and will be the subject of further study. Whatever the underlying reasons for this observation, the benefit of combining dye and isotope in patients of all ages is clear.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
A substantial literature confirms the validity of the SLN hypothesis for breast cancer patients. A growing number of institutions are completing their own pilot studies of the SLN technique and considering whether to accept a negative SLN biopsy on its own as adequate axillary staging. In this context, each failed mapping procedure will result in an axillary dissection which might not have been needed. The ideal technique of SLN biopsy is therefore that which finds the SLN as often as possible. This study affirms that (1) neither dye nor isotope alone are sufficient to achieve this goal, (2) the factors predicting the success of each method overlap but are not identical, and (3) the success of SLN mapping is optimized by using dye and isotope in combination.

Received for publication March 18, 2000. Accepted for publication August 14, 2000.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

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T. G. Zogakis, R. Essner, H.-j. Wang, R. R. Turner, Y. T. Takasumi, R. L. Gaffney, J. H. Lee, and D. L. Morton
Melanoma Recurrence Patterns After Negative Sentinel Lymphadenectomy
Arch Surg, September 1, 2005; 140(9): 865 - 872.
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J. E. Mendez, J. V. Fey, H. Cody, P. I. Borgen, and L. M. Sclafani
Can Sentinel Lymph Node Biopsy Be Omitted in Patients With Favorable Breast Cancer Histology?
Ann. Surg. Oncol., January 1, 2005; 12(1): 24 - 28.
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A. Chagpar, R. C. Martin III, C. Chao, S. L. Wong, M. J. Edwards, T. Tuttle, and K. M. McMasters
Validation of Subareolar and Periareolar Injection Techniques for Breast Sentinel Lymph Node Biopsy
Arch Surg, June 1, 2004; 139(6): 614 - 620.
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T. A. King, J. V. Fey, K. J. Van Zee, A. S. Heerdt, M. L. Gemignani, E. R. Port, L. Sclafani, V. Sacchini, J. A. Petrek, H. S. Cody III, et al.
A Prospective Analysis of the Effect of Blue-Dye Volume on Sentinel Lymph Node Mapping Success and Incidence of Allergic Reaction in Patients With Breast Cancer
Ann. Surg. Oncol., May 1, 2004; 11(5): 535 - 541.
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T. M. Pawlik, M. I. Ross, and J. E. Gershenwald
Lymphatic Mapping in the Molecular Era
Ann. Surg. Oncol., April 1, 2004; 11(4): 362 - 374.
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C A Murray, W L Leong, D R McCready, and D M Ghazarian
Histopathological patterns of melanoma metastases in sentinel lymph nodes
J. Clin. Pathol., January 1, 2004; 57(1): 64 - 67.
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B. R. Krynyckyi, C. K. Kim, M. R. Goyenechea, P. T. Chan, Z.-Y. Zhang, and J. Machac
Clinical Breast Lymphoscintigraphy: Optimal Techniques for Performing Studies, Image Atlas, and Analysis of Images
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Lymphoscintigraphy for Lymphatic Mapping in Breast Carcinoma
Radiology, August 1, 2003; 228(2): 313 - 315.
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J. Sprung, M. J. Tully, and A. Ziser
Anaphylactic Reactions to Isosulfan Blue Dye During Sentinel Node Lymphadenectomy for Breast Cancer
Anesth. Analg., April 1, 2003; 96(4): 1051 - 1053.
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C. M. Balch, M. S. Roh, K. I. Bland, M. F. Brennan, E. M. Copeland III, D. L. Morton, J. E. Niederhuber, and R. E. Pollock
Annals of Surgical Oncology Impact Factor/Rating Has Dramatically Increased
Ann. Surg. Oncol., January 1, 2003; 10(1): 1 - 3.
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J. Bonnema and C. J. H. van de Velde
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Ann. Onc., October 1, 2002; 13(10): 1531 - 1537.
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Isosulfan Blue Dye Reactions During Sentinel Lymph Node Mapping for Breast Cancer
Anesth. Analg., August 1, 2002; 95(2): 385 - 388.
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K. I. Bland
Utilization of Sentinel Lymph Node Mapping to Determine Pathologic Outcomes for Patients Receiving Neoadjuvant Chemotherapy for Locally Advanced Breast Cancer
Ann. Surg. Oncol., April 1, 2002; 9(3): 217 - 219.
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A. R. Miller, V. E. Thomason, I-T. Yeh, A. Alrahwan, F. E. Sharkey, J. Stauffer, P. M. Otto, C. McKay, M. S. Kahlenberg, W. T. Phillips, et al.
Analysis of Sentinel Lymph Node Mapping With Immediate Pathologic Review in Patients Receiving Preoperative Chemotherapy for Breast Carcinoma
Ann. Surg. Oncol., April 1, 2002; 9(3): 243 - 247.
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Ann. Surg. Oncol., December 1, 2001; 8(10): 837 - 843.
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M. D. McCarter, H. Yeung, S. Yeh, J. Fey, P. I. Borgen, and H. S. Cody III
Localization of the Sentinel Node in Breast Cancer: Identical Results With Same-Day and Day-Before Isotope Injection
Ann. Surg. Oncol., September 1, 2001; 8(8): 682 - 686.
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R. C.G. Martin, J. Fey, H. Yeung, P. I. Borgen, and H. S. Cody III
Highest Isotope Count Does Not Predict Sentinel Node Positivity in All Breast Cancer Patients
Ann. Surg. Oncol., August 1, 2001; 8(7): 592 - 597.
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