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Right arrow Sentinel lymph node
Annals of Surgical Oncology 8:592-597 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Highest Isotope Count Does Not Predict Sentinel Node Positivity in All Breast Cancer Patients

Robert C.G. Martin, MD, Jane Fey, MPH, Henry Yeung, MD, Patrick I. Borgen, MD and Hiram S. Cody III, MD

From The Breast Service, Department of Surgery (RCGM, JF, PIB, HSC) and the Department of Nuclear Medicine (HY), 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, New York, NY 10021; Fax: 212-794-5812; E-mail: codyh{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Background: Radioisotope mapping is an essential technical component of sentinel lymph node (SLN) biopsy, and most authors define isotope success by an arbitrary threshold SLN-to-background ratio. Few studies have examined the degree to which the relative level of SLN counts correlates with the presence of metastasis. Having removed the SLN with the highest counts, how far should the surgeon persist in removing additional SLN which contain much lower levels of isotope?

Methods: We performed SLN biopsy, using both radioisotope and blue dye, in 2285 consecutive patients with stage I-II breast cancer. Successful isotope localization was defined as an ex vivo SLN-to-axillary background count ratio of at least 4:1, and enhanced pathologic analysis (serial sections and immunohistochemistry) was used throughout.

Results: Among the 1566 patients with more than one SLN site identified, the SLN contained metastasis in 463 (30%). In 369 (80%) of these SLN-positive cases, the SLN with the highest count contained tumor, but in 94 (20%) it was benign. Among these 94: (1) the counts of the hottest benign SLN exceeded those of the histologically positive SLN by a ratio of at least 10:1 in 31% (29 of 94) of cases, (2) the counts of the positive SLN were < 4:1 those of the axillary background in 16% (15 of 94) of cases, and (3) blue dye failed to identify 27% of positive SLN. No optimum ratio of SLN-to-SLN or SLN-to-background counts identified the positive SLN in all cases.

Conclusion: Although the SLN with the highest counts is positive in 80% of breast cancer patients with multiple SLN, neither a relatively high isotope count nor the presence of blue dye consistently predict SLN positivity in all breast cancer patients. For maximum accuracy, SLN biopsy requires (1) the removal of all nodes containing isotope regardless of the relative magnitude of counts, (2) the concurrent use of blue dye to salvage those procedures in which isotope fails, and (3) the removal of all clinically suspicious non-SLN.

Key Words: Sentinel node biopsy • Breast cancer • Lymph node metastasis • Lymphoscintigraphy


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
Sentinel lymph node (SLN) biopsy represents a new standard of care for axillary node staging in patients with breast cancer. More than 40 clinical studies of SLN biopsy validated by a backup axillary dissection confirm that the SLN can be found in at least 90% of cases and that it predicts the axillary node status with an accuracy of 97%.1 The optimal technique of SLN mapping remains a matter of debate. Since the first reports of radioisotope mapping by Krag in 1993,2 blue dye mapping by Giuliano in 1994,3 and combined isotope-dye mapping by Albertini in 1996,4 a number of large observational studies (both academic and community-based)5–8 and an emerging international consensus increasingly support the use of isotope and dye in combination.

A successful SLN mapping by blue dye, defined as the identification of a blue node or a blue lymphatic leading to a non-blue node, is straightforward and unambiguous. In contrast, there is no standard definition of isotope success. Some authors use node counts alone to define the SLN, and others use one of three ratios: SLN to postexcision axillary background, SLN to hottest SLN, or SLN to non-SLN. While each method seems to work well, the derivation of the exact count levels or ratios defining the SLN has been largely empirical and arbitrary.

Here we aim to determine, among patients with more than one SLN found at surgery, the patterns of SLN metastasis and whether there is indeed a threshold level of isotope counts which could ensure the identification of all positive SLN.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 
At Memorial Sloan-Kettering Cancer Center between September 1996 and June 2000, 2285 patients with clinical stage I-II invasive breast cancer underwent SLN biopsy. The technique and results of the first 60, 9 500,10 and 10005,11 procedures have previously been reported in detail. All patients had SLN mapping using a combination of radioisotope (Tc-99m sulfur colloid) and isosulfan blue dye. Our first 60 procedures9 were performed by three surgeons under an IRB (institutional review board) protocol in which a planned backup axillary node dissection (ALND) validated all SLN biopsies. Subsequent to this, five additional surgeons began to perform SLN biopsy, validating their initial experience with a backup ALND as well. The point at which each surgeon made the transition from SLN biopsy with backup ALND to SLN biopsy alone was variable. Within the present cohort, 303 patients had SLN biopsy with a backup ALND planned in advance.

All patients had intraparenchymal injection of isosulfan blue dye, with 4–5 cc injected adjacent to the breast tumor or biopsy cavity. In 525 patients, the isotope was given as an intraparenchymal injection (0.3 mCi in 4–6 cc of saline at multiple sites around the tumor or biopsy cavity) and in 1750 as an intradermal injection (0.1 mCi in 0.05 cc of saline at a single site directly over the tumor or just cephalad to the biopsy scar); 200 of these patients were part of a previous study12 comparing intraparenchymal and intradermal isotope injection. All patients had preoperative lymphoscintigraphy.

Successful blue dye localization was defined as the identification of a lymph node with visible blue dye staining, a directly contiguous blue-stained afferent lymphatic, or both. Successful isotope SLN localization required the ratio of 10-second ex vivo SLN counts to exceed the postexcision axillary background count by 4 times or greater. A threshold count ratio of 4 was chosen arbitrarily to be as inclusive as possible and seemed to correlate well with the surgeon’s subjective impression of isotope success. In general, we removed all blue and all hot SLN, regardless of count ratios, until no focally hot spots remained and then measured counts of the postexcision axillary background, taking care to direct the probe away from the isotope injection site in the breaSt. The operation on the breast (excision, re-excision, or mastectomy) was done after the SLN biopsy.

Pathologic analysis of the SLN in the first 60 cases consisted of a single hematoxylin-eosin (H&E) stained section. Thereafter, all SLN were serially sectioned and stained with H&E and immunohistochemical (IHC) stains for cytokeratins (CAM5.1 and AE1:AE3). An average of three H&E and two IHC-stained sections were examined per SLN. Nonsentinel nodes from the axillary dissection specimens were examined routinely with a single H&E stained section per node.

An SLN site was defined as a surgical specimen submitted by the surgeon intraoperatively as a single SLN (some sites proved on final pathologic analysis to contain more than one SLN). Palpable, suspicious axillary nodes that did not contain isotope or dye were not considered to be SLN, and were submitted as non-SLN. The success rate was defined as the proportion of all procedures in which SLN were identified and the false-negative rate as the proportion of axillary node-positive cases in which the SLN was negative.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSION
 REFERENCES
 
Patient demographics are presented in Table 1 and, aside from small tumor size, are those of the breast cancer population in general. Fifty-nine percent were diagnosed by a prior surgical biopsy and 74% chose breast conservation. Ninety-seven percent were mapped using unfiltered isotope, but 3% were part of a pilot study comparing filtered and unfiltered Tc-99m sulfur colloid.13 Eighty-three percent had same-day isotope injection, and 17% had day-before isotope injection as part of a study comparing the two methods.14


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  		TABLE 1. Patient characteristics
 
SLN were identified in 97% of patients, with 13% of SLN identified by isotope alone and 6% by blue dye alone (Table 2). Twenty-eight percent of patients (626 of 2215) were node positive overall, ranging from 10% for T1a to 80% for T3 tumors. The median number of SLN sites removed was 2, with a range of 1–15. There was no difference between filtered (median, 1; range, 1–4) and unfiltered (median, 2; range, 1–15) isotope, or between same-day (median, 2; range, 2–15) and day-before (median, 2; range, 2–15) isotope injection.


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  		TABLE 2. Method of SLN detection and frequency of nodal metastasis
 
Seventy-one percent (1566 of 2285) of patients had more than one SLN site identified. In 369 (80%) of these, the SLN with the highest counts contained tumor and in 94 (20%) patients it was benign (Table 3). Among these 94, the counts of the benign hottest SLN exceeded those of the histologically positive SLN by a ratio of at least 10:1 in 31% of cases (29 of 94) (Table 4A). In addition, the counts of the positive SLN relative to the axillary background were < 4:1 in 16% of cases (15 of 94) (Table 4B). Using either SLN-to-SLN ratios or SLN-to-background ratios, there was no threshold value which identified all positive SLN. Finally, while blue dye identified the SLN in all 15 of the isotope failures (defined by an SLN-to-background ratio of < 4:1) (Table 4B), dye failed to identify the positive SLN in 27% (25 of 94) of the 94 patients whose hottest SLN was benign. Among these 94, the positive SLN was found within the first three sites sampled in 92% of cases and was found at sites 4 or greater in the remaining 8% (Table 5). Sampling only the first two SLN sites (the median number of SLN obtained overall) would have missed 22% of positive SLN.


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  		TABLE 3. Frequency, number, and positivity of multiple SLN
 

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  		TABLE 4. Count ratios in the 94 SLN-positive patients whose hottest SLN was benign
 

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  		TABLE 5. Site of positive SLN in 94 patients with hottest SLN benign
 
As part of our validation protocol, 303 of the 2285 patients had SLN biopsy with a planned backup ALND (Table 6). Removal of only the hottest SLN would have resulted in a false-negative rate of 12.1%, while removing all focally hot SLN, all blue SLN, and all suspicious, palpable non-SLN yielded the 4% false-negative rate we actually observed.


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  		TABLE 6. SLN biopsy with backup ALND in 303 patients
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSION
 REFERENCES
 
Despite increasing worldwide acceptance of the procedure1 and convincing validation of the SLN hypothesis,15 the optimum technique of SLN biopsy remains a matter of debate. Individual investigators report excellent results with single-modality SLN mapping. For example, Giuliano et al.16 with blue dye alone found the SLN in 93.5% of patients, and Veronesi et al.17 had 98.7% success with isotope alone. The collective literature for single modality mapping is less encouraging, with blue dye alone succeeding in 81% (714 of 886 patients in 11 series) and isotope alone in 92% (2112 of 2292 patients in 16 series) of SLN biopsy procedures.1 An emerging international consensus supports the use of dye and isotope in combination, as does our own experience,5,10 and that of other large series from both academic and community settings.6–8 In the present study, 6% of SLN were found by dye alone and 13% by isotope alone, and among our first 1000 SLN biopsy procedures,11 10%–11% of positive SLN were found by dye or isotope alone and presumably would have been missed by reliance on single-modality mapping.

While the identification of a blue SLN is usually unequivocal, there are, to date, no standard criteria which define successful SLN identification by isotope. Some authors report the absolute level of counts in the SLN, with the definition of success ranging from 25 counts (taken percutaneously or ex vivo)18 to as high as 2000.19 Because of wide variation in the absolute level of counts, most authors have chosen to use one of three count ratios to define the SLN: SLN-to-background, SLN-to-non-SLN, or SLN-to-hottest SLN. Using a ratio of SLN-to-background, we have arbitrarily defined success as a ratio of at least 4:1;9 other definitions range from 2:120 to 10:1.21 Using a ratio of SLN-to-non-SLN, Cox et al.22 define success as a ratio of 10:1. Using a ratio of SLN-to-hottest SLN, McMasters et al.6 apply a 10% rule, defining a SLN as any node containing counts at least 10% of the hottest SLN, while Borgstein et al.23 require that the SLN contain counts at least 50% of the hottest SLN.

There is, in fact, some scientific precedent for defining isotope success. Nathanson et al.24 have used a mouse model to determine that 2%–10% of injected radiocolloid traverses the SLN and lodges in adjacent non-SLN. Based on these results, McMasters et al.6 of the University of Louisville Breast Cancer Study Group devised their 10% rule, described above, and are the only investigators to date who have made a correlation between count ratios and histopathology of the SLN. In a remarkable prospective multi-institutional trial,25 they demonstrate a reduction in the potential SLN false-negative rate from 13% (if only the hottest SLN was removed) to 5.8% (by following the 10% rule and removing all SLN with counts at least 10% those of the hottest). No other studies to date have validated this concept or given a convincing rationale for another definition of isotope success.

Here we draw on an experience of 2285 procedures to demonstrate that there is no single count ratio which reliably identifies the positive SLN in all patients. Among SLN positive patients, the hottest SLN indeed proved positive in 80% of cases, but no single ratio of counts reliably identified the remaining 20% of SLN-positive patients whose hottest SLN was benign.

Using the ratio of SLN-to-hottest SLN (Table 4A), patients were equally distributed in all categories. Had we used the 10% rule, 31% (29 of 94) of SLN-positive patients in this subset (or 4.6% of all node-positive patients) would have been missed. Under an even more inclusive 2% rule, 20% (19 of 94) of SLN-positive cases still would have been missed. Using a ratio of SLN-to-background (Table 4B), a similar outcome is apparent. Requiring the SLN to exceed the axillary background by a ratio of at least 10:1 would miss 37% (35 of 94) of positive SLN in this subset (or 5.6% of all node-positive patients). Our own more inclusive threshold value of 4:1 still missed 16% (15 of 94), all of which were fortunately identified by blue dye. While most positive SLN were identified by blue dye regardless of isotope count ratios, blue dye also failed to identify a substantial proportion (27%) of positive SLN among these 94 patients.

We have previously shown that, over our entire experience, 98% of positive SLN are identified within the first three sites sampled.26 In parallel to that observation, we here demonstrate that in the smaller SLN-positive subset in which the hottest SLN was benign, the positive SLN was found at the first, second, or third site sampled in 92% of the 94 patients (Table 5). Stopping after the first three sites would have missed 8% of positive SLN. As for count ratios, there was no threshold number of SLN sites which identified all SLN-positive cases. In one extreme case (subsequent to this series) the first positive SLN was found at the 13th site examined!

In a memorable editorial ("Will the true sentinel node please stand?"), Morton27 argues that the first node to receive lymphatic drainage from the tumor site is best identified by blue dye and that a flaw of isotope mapping is its tendency to identify additional second echelon nodes which are not true SLN. Our data show that the distinction between the true SLN and second echelon lymph nodes is not clear-cut. While we agree with Morton that the presence of a blue lymphatic leading to a blue node is without question a SLN, we question whether a blue SLN is really the gold standard. Among our 94 SLN-positive patients in whom the hottest SLN was benign, blue dye failed to identify 27% of positive SLN.

Neither the presence of blue dye nor isotope count ratios of any particular threshold level consistently identified the positive SLN in all patients.

The most rigorous assessment of SLN biopsy requires the performance of a backup ALND to establish with certainty the false-negative rate of the procedure. Among our 2285 SLN biopsy procedures, 303 had an ALND planned in advance to validate our early experience (Table 6). We have previously audited our learning curve, showing that false-negative results occur less often with experience, and that, when the SLN is falsely negative, grossly suspicious nodes are identified at surgery in a majority of cases;10,28 careful intraoperative palpation is an essential part of SLN biopsy, and ALND should be done when grossly suspicious nodes are found. By removing all focally hot SLN, all blue nodes, and excluding 10 patients with grossly suspicious nodes identified at surgery, we observed a false-negative rate of 4%. Had we removed only the blue SLN, only the hottest SLN, or set a specific threshold count ratio to define the SLN, our false-negative rate would have been higher.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
REFERENCES
 
SLN biopsy is a highly accurate test, if not a perfect one, and is performed within a biologic system which itself is subject to variation. We would argue that the challenge for the surgeon is to maximize the accuracy of the procedure with a technique which can reliably encompass this biologic variation. We conclude that isotope is an essential technical element of SLN mapping, and that it complements blue dye, but find that there is no particular isotope count ratio which identifies the positive SLN in all patients.


   Acknowledgments
 
The authors are grateful to the Tow Foundation for philanthropic grants supporting the sentinel node programs at Memorial Sloan-Kettering Cancer Center.

Received for publication February 21, 2001. Accepted for publication May 8, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSION
 REFERENCES
 

  1. Cody HS. Clinical aspects of sentinel node biopsy. Breast Cancer Res 2001; 3: 104–8.[CrossRef][Medline]
  2. Krag DN, Weaver DL, Alex JC, Fairbank JT. Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol 1993; 2: 335–40.[CrossRef][Medline]
  3. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 1994; 220: 391–401.[Medline]
  4. Albertini JJ, Lyman GH, Cox C, et al. Lymphatic mapping and sentinel node biopsy in the patient with breast cancer. JAMA 1996; 276: 1818–22.[Abstract]
  5. Cody HS, Fey J, Akhurst T, et al. Complementarity of blue dye and isotope in sentinel node localization for breast cancer: Univariate and multivariate analysis of 966 procedures. Ann Surg Oncol 2001; 8: 13–9.[Abstract/Free Full Text]
  6. McMasters KM, Tuttle TM, Carlson DJ, et al. Sentinel lymph node biopsy for breast cancer: A suitable alternative to routine axillary dissection in multi-institutional practice when optimal technique is used. J Clin Oncol 2000; 18: 2560–6.[Abstract/Free Full Text]
  7. Tafra LC, Lannin DR, Swanson MS, et al. Multicenter trial of sentinel node biopsy for breast cancer using both technetium sulfur colloid and isosulfan blue dye. Ann Surg 2001; 233: 51–9.[CrossRef][Medline]
  8. Bass SS, Cox CE, Ku NN, Berman C, Reintgen DS. The role of sentinel lymph node biopsy in breast cancer. J Am Coll Surg 1999; 189: 183–94.[CrossRef][Medline]
  9. O’Hea BJ, Hill ADK, El-Shirbiny A, et al. Sentinel lymph node biopsy in breast cancer: Initial experience at Memorial Sloan-Kettering Cancer Center. J Am Coll Surg 1998; 186: 423–7.[CrossRef][Medline]
  10. Hill ADK, Tran KN, Akhurst T, et al. Lessons learned from 500 cases of lymphatic mapping for breast cancer. Ann Surg 1999; 229: 528–35.[CrossRef][Medline]
  11. Cody HS, Borgen PI. State-of-the-art approaches to sentinel node biopsy for breast cancer: Study design, patient selection, technique, and quality control at Memorial Sloan-Kettering Cancer Center. Surg Oncol 1999; 8: 85–91.[CrossRef][Medline]
  12. Linehan DC, Hill ADK, Akhurst T, Tran KN, Borgen PI, Cody HS. Intradermal radiocolloid and intraparenchymal blue dye injection optimize sentinel node identification in breast cancer patients. Ann Surg Oncol 1999; 6: 450–4.[Abstract]
  13. Linehan DC, Hill ADK, Tran KN, et al. Sentinel lymph node biopsy in breast cancer: Unfiltered radioisotope is superior to filtered. J Am Coll Surg 1999; 188: 377–81.[CrossRef][Medline]
  14. Yeung HWD, Cody HS, Turlakow A, et al. Lymphoscintigraphy and sentinel node localization in breast cancer patients: A comparison between one-day and two-day protocols. J Nucl Med 2001; 42: 420–3.[Abstract/Free Full Text]
  15. Turner RR, Ollila DW, Krasne DL, Giuliano AE. Histologic validation of the sentinel lymph node hypothesis for breast carcinoma. Ann Surg 1997; 226: 271–8.[CrossRef][Medline]
  16. Giuliano AE, Jones RC, Brennan M, Statman R. Sentinel lymphadenectomy in breast cancer. J Clin Oncol 1997; 15: 2345–50.[Abstract/Free Full Text]
  17. Veronesi U, Paganelli G, Viale G, et al. Sentinel lymph node biopsy and axillary dissection in breast cancer: Results in a large series. J Natl Cancer Inst 1999; 91: 368–73.[Abstract/Free Full Text]
  18. 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]
  19. Galimberti V, Zurrida S, Zucali P, Luini A. Can sentinel node biopsy avoid axillary dissection in clinically node-negative breast cancer patients? Breast 1998; 7: 8–10.[CrossRef]
  20. Krag DN, Meijer SJ, Weaver DL, et al. Minimal-access surgery for staging of malignant melanoma. Arch Surg 1995; 130: 654–8.[Abstract]
  21. Klimberg VS, Rubio IT, Henry R, Cowan C, Colvert M, Kourourian S. Subareolar versus peritumoral injection for location of the sentinel lymph node. Ann Surg 1999; 229: 860–5.[CrossRef][Medline]
  22. Cox CE, Pendas S, Cox JM, et al. Guidelines for sentinel node biopsy and lymphatic mapping of patients with breast cancer. Ann Surg 1998; 5: 645–53.
  23. Borgstein PJ, Pijpers R, Comans EF, van Diest PJ, Boom RP, Meijer S. Sentinel lymph node biopsy in breast cancer: Guidelines and pitfalls of lymphoscintigraphy and gamma probe detection. J Am Coll Surg 1998; 186: 275–83.[CrossRef][Medline]
  24. Nathanson SD, Anaya P, Karvelis KC, Eck L, Havstad S. Sentinel lymph node uptake of two different technetium-labeled radiocolloids. Ann Surg Oncol 1997; 4: 104–10.[Abstract]
  25. Martin RCII, 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]
  26. McCarter MD, Yeung H, Fey J, Borgen PI, Cody HS. The breast cancer patient with multiple sentinel nodes: When to stop? J Am Coll Surg 2001; 192: 692–7.[CrossRef][Medline]
  27. Morton DL, Bostick PJ. Will the true sentinel node please stand? Ann Surg Oncol 1999; 6: 12–14.[CrossRef][Medline]
  28. Cody HS, Hill ADK, Tran KN, Brennan MF, Borgen PI. Credentialing for breast lymphatic mapping - how many cases are enough? Ann Surg 1999; 229: 723–8.[CrossRef][Medline]



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