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Right arrow Sentinel lymph node
Annals of Surgical Oncology 8:682-686 (2001)
© 2001 Society of Surgical Oncology

ORIGINAL ARTICLES

Localization of the Sentinel Node in Breast Cancer: Identical Results With Same-Day and Day-Before Isotope Injection

Martin D. McCarter, MD, Henry Yeung, MD, Samuel Yeh, MD, Jane Fey, MPH, Patrick I. Borgen, MD and Hiram S. Cody III, MD

From The Breast Service, Department of Surgery (MDM, JF, PIB, HSC), and the Department of Nuclear Medicine (HY, SY), Memorial Sloan-Kettering Cancer Center, New York, New York.

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


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Although the technique of sentinel lymph node (SLN) biopsy in breast cancer is not fully standardized, an increasing number of centers map the SLN by using radioisotope supplemented by blue dye, and most have injected isotope on the day of surgery. Here we directly compare the results of same-day and day-before isotope injection in a large series of breast cancer patients having SLN biopsy with our mature technique.

Methods: Starting with our 961st SLN procedure for breast cancer, 1320 consecutive patients had SLN biopsy after the injection of unfiltered 99mTc-labeled sulfur colloid given as a single-site, low-volume (0.05 ml) intradermal injection: 933 on the day of surgery (1-day protocol) and 387 on the day before (2-day protocol). All had intraparenchymal injection of blue dye.

Results: The two groups were comparable in age, tumor location, histopathologic characteristics, and number of SLNs identified. LSG taken at 2 hours in the 2-day protocol was positive more often than LSG performed at 30 minutes in the 1-day protocol, and nonaxillary sites of lymphatic drainage were seen in <1% of each group. Absolute isotope counts and the ratio of SLN to axillary background counts were similar. Isotope localization of the SLN succeeded in a comparable fraction of patients, as did SLN identification overall.

Conclusions: The results of SLN mapping with same-day and day-before injection of radioisotope are virtually identical. The logistical advantages of day-before injection do not compromise the success of the procedure.

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


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Sentinel lymph node (SLN) biopsy is a new standard of care for patients with operable breast cancer. Forty-one clinical series of SLN biopsy (1993–1999)1 validated by a backup axillary node dissection confirm that the SLN can be found in at least 90% of cases and suggest that isotope (used in conjunction with blue dye) is an essential technical element of the procedure. Although the technique of blue dye mapping, as first described for breast cancer by Giuliano et al.,2 is straightforward, that of isotope mapping is not. Although all authors have used 99mTc, there is wide variation in the carrier particle (sulfur colloid, colloidal albumin, antimony, or dextran), dose (0.1–10 mCi), route (intraparenchymal, subdermal, intradermal, and subareolar), volume (0.05–16 ml), and timing of injection, with many European centers using a day-before and most North American programs a same-day methodology.

As our volume of SLN biopsy procedures grew, same-day isotope injection became increasingly cumbersome and the logistical advantages of day-before injection increasingly attractive. Patients could have isotope injection the afternoon before surgery, with lymphoscintigraphy (LSG) performed free of time pressure from the operating room. SLN procedures the following day could be scheduled as first case, eliminating OR downtime as a result of delays from same-day LSG. Encouraged by favorable reports of day-before mapping from European centers,3–7 and in collaboration with our Department of Nuclear Medicine, we initiated this study, directly comparing the results of same-day and day-before isotope mapping for our mature technique of SLN biopsy.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
This series encompasses 1320 consecutive patients having SLN biopsy for breast cancer at Memorial Sloan-Kettering Cancer Center between January 1, 1999, and June 30, 2000, beginning with the 961st patient in our overall experience. The technique and results of our first 60,8 500,9 and 100010,11 procedures have previously been presented in detail. This study reflects our mature technique of SLN biopsy and is free of learning curve artifacts.

All patients had a single-site low-volume (0.05-ml) intradermal injection of unfiltered 99mTc-labeled sulfur colloid, given directly over the tumor or just cephalad to the biopsy scar. Same-day patients received a dose of 0.1 mCi (3.7 MBq), and day-before patients received 0.5 mCi (18.5 MBq). The latter dose was estimated, on the basis of the 6-hour half-life of 99mTc, to give equivalent counts at the time of surgery the following day. Static LSG images were obtained at 30 minutes after injection in the 1-day group (dictated by the demands of the operating room schedule) and 2 hours after injection in the 2-day group. Four to five milliliters of isosulfan blue dye was injected into the breast parenchyma around the tumor site at the beginning of the surgery.

Most nonpalpable lesions requiring needle localization had same-day isotope injection guided by the localizing wire, on the basis of our concern that the isotope be injected precisely in the right place; this concern may have been unfounded, because we and others have since learned that most of the lymphatic drainage of the breast is probably to the same few SLNs and that a variety of injection sites identify the SLN with equal success.

Successful SLN localization by blue dye required the identification of a blue node or a contiguous blue lymphatic vessel, and success by isotope required that the ex vivo counts of the SLN exceed the postexcision axillary background by a ratio of 4 or greater. All blue or hot nodes were removed. An SLN site was defined during surgery by the surgeon as a specimen thought to consist of a single SLN; the number of SLN is that identified by the surgical pathologist. All SLNs that proved negative on intraoperative frozen section underwent enhanced pathologic analysis with serial sections, and both hematoxylin and eosin and immunohistochemical staining for cytokeratins.

This is a nonrandomized observational trial, with patients allocated to same-day or day-before isotope injection on the basis of their own preference, and also on the availability of operating room time. End points for comparison included LSG findings, number of SLN sites found at surgery, isotope counts in the SLN (expressed both as absolute counts and as the ratio of SLN to postexcision axillary background), and the success of SLN mapping, both by isotope and overall (i.e., by isotope, blue dye, or both). The significance of differences between groups was tested (where appropriate) by {chi}2, Wilcoxon rank-sum, and Student’s t-test.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Of the 1320 patients, 387 (30%) elected the 2-day protocol, and the remainder had same-day injection. Patient and tumor characteristics between the two groups were strikingly similar (Table 1). In general, patients with nonpalpable lesions were allocated to the 1-day group and had isotope injection immediately after needle localization on the morning of surgery. Therefore, a larger proportion of the 1-day patients had nonpalpable and/or T1 cancers.


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  		TABLE 1. Patient and tumor characteristics
 
With the benefit of 2-hour images (which were not taken in the 1-day group), the SLN was imaged more often overall in the 2-day group: 83% vs. 66% (Table 2). Nonaxillary sites of lymphatic drainage were demonstrated for a comparably small fraction of patients in each group (<1%).


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  		TABLE 2. Results of preoperative lymphoscintigraphy
 
The mean and median number of SLNs found was slightly higher in the 2-day than in the 1-day group (3.1 vs. 2.7, 3 vs. 2, P < .05), and the range in number of SLNs found was comparable (0–14 vs. 0–12). A comparable proportion of each group had SLNs identified at 1, 2, 3, 4, 5, or >5 sites (Table 3). SLNs were identified equally often by isotope in each group, whether measured by the absolute level of counts in the SLN (Table 4) or by the ratio of SLN to postexcision axillary background counts (Table 5). An apparent trend toward higher absolute levels of counts in the 2-day group (Table 4) disappeared when expressed as a ratio of SLN to postexcision background counts (Table 5). By using our standard definition of isotope success (SLN counts >=4 times those of the postexcision axillary background), the levels of isotope are virtually identical in both groups. The mean level of counts (Table 4) and the mean count ratios (Table 5) were remarkably comparable at the site of injection, at the first SLN found, and (for patients with more than one SLN site) at sites 2, 3, 4, and 5.


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  		TABLE 3. Number of SLN sites found at surgery
 

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  		TABLE 4. Absolute counts for injection site, each SLN site, and postexcision axillary bed
 

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  		TABLE 5. Ex vivo SLN to postexcision axillary bed count ratios for each SLN site
 
Overall isotope success for the 1- and 2-day groups was 93% and 96%, respectively (Table 6). Within each group, isotope succeeded significantly more often than blue dye (P < .0001), and the overall success rate of SLN identification (by isotope, blue dye, or both) was identical between groups (98%).


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  		TABLE 6. Successful SLN mapping by method
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The methodology of SLN biopsy for breast cancer is not standardized. Our own technique evolved over our first 1000 procedures.10 In a logical sequence of studies, we have previously demonstrated (1) the complementarity of isotope and blue dye,8–11 (2) the superiority of unfiltered over 220 nm filtered 99mTc-labeled sulfur colloid,12 (3) the advantage of intradermal over intraparenchymal isotope injection,13,14 and (4) an overall success in identifying the SLN, which continued to increase over our first 500 procedures.15 We also demonstrated (5) that false negative results were most common in the early experience of each surgeon.15

Our current mature technique of SLN biopsy, described in detail previously,10 involves (1) a single-site, low-dose, low-volume intradermal injection of 99mTc-labeled sulfur colloid directly over the tumor site at least 1 to 2 hours before surgery, (2) intraparenchymal injection of isosulfan blue dye in the operating room at the start of surgery, (3) the removal of all blue nodes and of all nodes containing isotope counts at least 4 times those of the axillary background, and (4) enhanced pathologic analysis whenever the SLNs prove negative on frozen section. Isotope mapping remains an indispensable element in our algorithm for SLN biopsy. Here we seek to improve the scheduling logistics of the procedure by directly comparing same-day and day-before isotope injection in a large series of contemporaneous cases in which the timing (and dosage) of isotope injection are the only variables.

Morton and Bostick ("Will the true sentinel node please stand?")16 have argued that blue dye is the gold standard that defines the true SLN and that isotope has the theoretical potential to pass beyond this true SLN and identify numerous second-echelon lymph nodes, i.e., non-SLNs that are irrelevant to the staging of the node basin. Here we demonstrate that this concern, although logical, is unfounded. Although day-before isotope injection resulted in a marginal increase in the mean number of SLNs found by the pathologist (3.1 vs. 2.7), the same-day and day-before groups were comparable in most other aspects: number of SLN sites found at surgery, proportion of patients with SLNs at one or more than one site, absolute SLN isotope counts, SLN-to-background count ratios, and proportion of positive SLNs.

Indeed, neither isotope nor blue dye by itself constitutes a gold standard, and each has the potential to miss positive SLNs. Among our first 1000 SLN procedures,11 8% of positive SLNs were missed by isotope and 14% were missed by blue dye. Because all of our SLN procedures were performed with both isotope and dye, we cannot eliminate the possibility of a bias in which one modality affected the results of the other. However, the most persuasive support for a combined approach comes from the landmark multi-institutional trial of McMasters et al.17 This large study of SLN biopsy (uniformly validated by a backup axillary node dissection) allowed the 99 university- and community-based participant surgeons to perform SLN biopsy using isotope only, dye only, or an isotope-dye combination, and it confirmed that false-negative results are twice as common with single-agent as with dual-agent mapping (12% vs. 6%). We continue to strongly support combined isotope-dye mapping.

An advantage of day-before mapping is the removal of time constraints from the nuclear medicine team. A previous report of our experience by Yeung et al.18 has demonstrated identical LSG success at 30 minutes in the 1- and 2-day groups. The increased LSG success we observe in the 2-day group (Table 2) is a result of the delayed images taken at 2 hours; of note, most of these delayed images identified only a single SLN and did not identify additional second echelon nodes. Nonaxillary sites were seen in a very small fraction of both groups, a finding also consistent with our earlier studies of intradermal isotope injection. Other groups, most notably Jansen et al.19 from the Netherlands Cancer Institute, demonstrate nonaxillary drainage in as many as 20% of cases after intraparenchymal isotope injection. The clinical significance of these nonaxillary sites remains undefined. A negative LSG does not preclude successful isotope mapping at surgery, because the hand-held gamma probe is far more sensitive than the full-field-of-view gamma camera. Among our patients whose preoperative LSG was negative, isotope localization still succeeded in 82%.11

Our 2-day protocol required a larger dose of isotope, 0.5 mCi, as opposed to 0.1 mCi for the 1-day group. Of note, the dosages reported by other investigators (ranging from 0.3 to 1.6 mCi) are much higher.20 In our experience, large doses of isotope (or high-volume injection) are not required to achieve a high rate of successful mapping. Although one might argue that even an increase from 0.1 to 0.5 mCi raises issues of radiation safety, we demonstrate here that intraoperative absolute count levels and SLN-to-background count ratios are comparable in both groups. 99mTc has a 6-hour half-life, and our day-before isotope injection allows the radioactivity levels to equalize. Further, 0.5 mCi is itself a trivial dose, only 2% of that given for a standard bone scan (25 mCi), for which no isolation procedures are required. Miner et al.,21 in a careful study of radiation exposures during SLN biopsy, demonstrate that one would have to perform approximately 500 SLN biopsy procedures annually to achieve an exposure of the surgeon’s hands sufficient to require a radiation safety badge and approximately 5000 procedures to reach the statutory dosage limit. By using a different method, Stratmann et al.22 estimate an allowable operating time of 2190 hours/year before the surgeon’s hand exposure exceeds the dosage limit. The level of radiation exposure under our current protocol, whether 1- or 2-day, is inconsequential.

For both the 1- and 2-day groups, we found the SLN in an identical proportion of cases: 98%. This result is concordant with earlier reports from Italy3,4 and Holland,5–7 in which the authors report successful isotope mapping in 69% to 99% of cases. Winchester et al.23 were the first American group to advocate day-before isotope injection (by using filtered 99mTc-labeled sulfur colloid) for SLN biopsy in breast cancer. They substantially increased their isotope success rate from 50% (with same-day injection) to 96% (with day-before injection) and actually obtained fewer SLNs in the day-before group, suggesting that a longer delay between isotope injection and surgery allows washout of isotope from additional non-SLNs. We found comparable numbers of SLNs in both the 1- and 2-day groups, perhaps as a result of using an unfiltered isotope preparation with a larger particle size. In our own study of filtered isotope,12 approximately one fourth of the isotope mappings failed because the axilla was diffusely hot, suggesting extensive migration of the smaller isotope particles beyond the SLN.

Day-before isotope injection involves no compromise whatever in the outcome of SLN biopsy, and the advantages of day-before isotope injection are many. Patients have their LSG in a calmer setting, do not have to be NPO, and can avoid waiting between same-day injection and surgery. Nuclear medicine physicians are free to take whatever delayed images are required to further investigate LSG findings of interest. Surgeons can schedule their SLN procedures as the first case the following day. Finally, hospital administrators can achieve more efficient and cost-effective utilization; the operating room is a very expensive asset if kept idle by scheduling delays.

SLN biopsy is a new standard of care for the patient with operable breast cancer. Our previous experience demonstrates the value of combined isotope-dye mapping, the superiority of unfiltered 99mTc-labeled sulfur colloid, and the value of low-dose, low-volume intradermal isotope injection. This mature technique identifies the SLN in 98% of cases overall. The results of SLN mapping are identical whether 0.5 mCi of isotope is injected the day before, or 0.1 mCi is injected the morning of surgery. SLN biopsy can be scheduled for the convenience both of the patient and the hospital staff, without compromising the success of the procedure.


   Acknowledgments
 
Supported by philanthropic grants from the Tow Foundation.


   Footnotes
 
Presented at the 54th Annual Meeting of the Society of Surgical Oncology, Washington, DC, March 15–18, 2001.

Received for publication March 16, 2001. Accepted for publication June 15, 2001.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  1. Cody HS. Clinical aspects of sentinel node biopsy. Breast Cancer Res 2001; 3: 104–8.[CrossRef][Medline]
  2. Giuliano AE, Kirgan DM, Guenther JM, Morton DL. Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 1994; 220: 391–401.[Medline]
  3. Veronesi U, Paganelli G, Galimberti V, et al. Sentinel node biopsy to avoid axillary dissection in breast cancer with clinically negative lymph-nodes. Lancet 1997; 349: 1864–7.[CrossRef][Medline]
  4. 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]
  5. 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]
  6. Pijpers R, Meijer S, Hoekstra OS, et al. Impact of lymphoscintigraphy on sentinel node identification with technetium-99m-colloidal albumin in breast cancer. J Nucl Med 1997; 38: 366–8.[Abstract/Free Full Text]
  7. Roumen RMH, Valkenburg JGM, Geuskens LM. Lymphoscintigraphy and feasibility of sentinel node biopsy in 83 patients with primary breast cancer. Eur J Surg Oncol 1997; 23: 495–502.[CrossRef][Medline]
  8. 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]
  9. 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]
  10. 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]
  11. 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]
  12. 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]
  13. 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]
  14. Boolbol SK, Fey J, Borgen PI, et al. Intradermal isotope injection: a highly accurate method of lymphatic mapping in breast carcinoma. Ann Surg Oncol 2001; 8: 20–4.[Abstract/Free Full Text]
  15. 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]
  16. Morton DL, Bostick PJ. Will the true sentinel node please stand? Ann Surg Oncol 1999; 6: 12–4.[CrossRef][Medline]
  17. 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]
  18. 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]
  19. Jansen L, Doting MH, Rutgers EJ, de Vries J, Olmos RA, Nieweg OE. Clinical relevance of sentinel lymph nodes outside the axilla in patients with breast cancer. Br J Surg 2000; 87: 920–5.[CrossRef][Medline]
  20. Liberman L, Cody HS, Hill ADK, et al. Sentinel lymph node biopsy after percutaneous diagnosis of nonpalpable breast cancer. Radiology 1999; 211: 835–44.[Abstract/Free Full Text]
  21. Miner TJ, Shriver CD, Flicek PR, et al. Guidelines for the safe use of radioactive materials during localization and resection of the sentinel lymph node. Ann Surg Oncol 1999; 6: 75–82.[Abstract]
  22. Stratmann SL, McCarty TM, Kuhn JA. Radiation safety with breast sentinel node biopsy. Am J Surg 1999; 178: 454–7.[CrossRef][Medline]
  23. Winchester DJ, Sener SF, Winchester DP, et al. Sentinel lymphadenectomy for breast cancer: experience with 180 consecutive patients: efficacy of filtered technetium 99m sulphur colloid with overnight migration time. J Am Coll Surg 1999; 188: 597–603.[CrossRef][Medline]



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