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10.1245/s10434-006-9313-4
Annals of Surgical Oncology 14:1629-1637 (2007)
© 2007 Society of Surgical Oncology
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Original Article

Breast Cancer Sentinel Lymph Node Identification Rates: The Influence of Radiocolloid Mapping, Case Volume, and the Place of the Procedure

S. David Nathanson, MD1, Jennifer K. Grogan, MD1, Deborah DeBruyn, BS4, Alissa Kapke, MS2 and Kastytis Karvelis, MD3

1 Department of Surgery, Henry Ford Health System, 2799 W Grand Boulevard, Detroit, MI 48202, USA
2 Department of Biostatistics and Epidemiology, Henry Ford Health System, 2799 W Grand Boulevard, Detroit, MI 48202, USA
3 Department of Radiology, Henry Ford Health System, 2799 W Grand Boulevard, Detroit, MI 48202, USA
4 The Josephine Ford Cancer Center Clinical Trials Office, Henry Ford Health System, 2799 W Grand Boulevard, Detroit, MI 48202, USA

Correspondence: Address correspondence and reprint requests to: S. David Nathanson, MD; E-mail: dnathan1{at}hfhs.org


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: We hypothesized that high-volume surgeons performing sentinel lymph node (SLN) biopsy at an academic medical center (AMC) would have the same identification rates at suburban surgical centers (SSCs).

Methods: Twenty-one surgeons performed 1199 SLN biopsies in 1187 clinically node-negative patients with an intraoperative gamma probe (IOGP) plus blue dye (at AMC) or blue dye alone (at SSCs). Demographic, radiologic, and pathological data were analyzed by generalized estimating equations logistic regression models.

Results: Four surgeons (group 1) performed 877 procedures (361, 247, 152, and 117 cases each), 426 with and 451 without IOGP. Seventeen surgeons (group 2) performed 322 procedures (2–92 cases each), 173 with and 149 without IOGP. Group 1 found 411 SLNs (96.5%) with and 419 (92.9%) without IOGP (P = .024). Group 2 found 163 (94.2%) with and 117 (78.5%) without IOGP (P < .0001). The odds of finding the SLN was 2.9 times higher with IOGP (95% confidence interval [95% CI], 1.8, 4.7; P < .001) and 2.7 times higher by group 1 than group 2 surgeons (95% CI, 1.7, 4.3; P < .001), controlling for tumor size and surgery type.

Conclusions: High-volume surgeons identified more SLNs with IOGP (at the AMC) than without (at the SSCs). They also were more efficient than low-volume surgeons when blue dye alone was used. Low-volume surgeons were almost as efficient as high-volume surgeons when they used IOGP. Optimal identification of SLNs requires nuclear medicine facilities.

Key Words: Sentinel lymph nodes • Breast cancer • Radiocolloid • Case volume


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Sentinel lymph node biopsy (SLNB) has become a popular technique for evaluating the axillary nodes in breast cancer.1,2 Yet the techniques for identifying the correct lymph node draining the breast tumor vary.36 The procedure, first developed in specialized centers,68 is increasingly performed in less specialized centers.9 The absence of a credentialing method for SLNB makes it necessary to establish quality control measures to determine whether individual variations in different locations adversely affect the identification rates. This is particularly true when patients are treated in suburban locations in small surgical centers geographically and academically separated from larger institutions, where multidisciplinary protocols have been established.

SLNB requires cooperation between patients, surgeons, pathologists, operating room personnel, nurses, and radiologists who provide expertise in radiocolloid injection and gamma imaging. A breakdown in any of the components decreases the quality and accuracy of the procedure. The anatomic site of radiocolloid injection does not seem to affect the identification rate much.1012 Intraparenchymal, subareolar, or intradermal injections seem to drain to the same axillary sentinel lymph node (SLN).3,5,7,10,11 The type of radiocolloid seems to have little impact on the accuracy of the technique as well.13 Modern gamma probes all function well in the operating room, and the learning curve for surgeons1,2,5,79,1416 may be quite rapid when gamma probes are used. The necessity of the use of lymphophilic blue dye is debated because of the rare anaphylactic reaction.2 However, the use of intraoperative blue dye injections is relatively cheap and accurate and can be performed even when radiocolloid is not available.

Surgeons continue to debate the advantages of the use of a combination of radiocolloid (usually injected by a radiologist) and blue dye (injected by the surgeon in the operating room).2 In some centers, blue dye alone is thought to provide as accurate an identification of the SLN as a combination technique.17 The learning curve for surgeons in those centers seems quite lengthy, and the result is a relatively conservative approach to quality control and accreditation issues.

The ideal method to establish whether blue dye techniques alone are as accurate as a combination of radiocolloid and blue dye would be a prospective study in which patients would be randomized to one or the other technique performed by the same surgeons. This same experiment would be a good way to establish how many SLNBs an inexperienced surgeon would have to perform to achieve the optimum quality. Our practice environment allowed us to do an experiment similar to the ideal because surgeons operate at both an urban academic medical center (AMC), where high-quality nuclear medicine facilities are available, and suburban surgical centers (SSCs), where intraoperative radiocolloid mapping with an intraoperative gamma probe (IOGP) is not available. We describe the identification rates at the two different practice facilities. We also have a unique situation with regard to teaching board-certified surgeons and surgical residents the SLN technique. Surgeons previously unlearned in the technique learned the SLNB procedure at the urban facility, where the mature technique had been established by the senior author. Monitoring their progress allowed us to evaluate how quickly it was possible for surgeons to learn SLNB.


    METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Patients
All the patients in this study were diagnosed and managed by salaried, full-time physicians in a vertically integrated academic health system. The Surgery Department of the main AMC, situated in Detroit, is serviced by senior surgical staff, residents, medical students, and allied staff. It is the main referral center for complex tertiary cases. Three large suburban satellite clinics (SSCs) in Wayne, Oakland, and Macomb counties, with six fully equipped and staffed operating rooms apiece, are part of the Henry Ford Health System. Six of the surgeons operating at the SSCs also operated at the AMC.

All cases treated at the AMC used both radiocolloid injections plus blue dye, whereas all cases treated at the SSCs used blue dye only. The diagnosis of breast cancer was made at either the AMC or the SSCs by core needle biopsy by a surgeon in the clinic, by excision biopsy in the operating room (for non-palpable masses), or by a radiologist in the mammography suite by image-guided (x-ray or ultrasound) needle biopsy techniques. Two of the patients received neoadjuvant systemic therapy. All patients were discussed at a breast cancer tumor board meeting by surgeons, medical oncologists, radiation oncologists, radiologists, and pathologists at the AMC. Some patients were seen in a Multidisciplinary Breast Cancer Clinic and treatment options, including SLNB, were presented and discussed.

The study we present here includes a prospective nonrandomized evaluation of 1187 clinically node-negative patients undergoing 1199 SLNBs from April 1995 through December 2005, although most of the procedures were performed after January 1997. We have previously reported some of these patients in other studies,10,18 evaluating other questions in the management of breast cancer, and the database continues to be updated as more patients from our breast cancer population are added.

Radiocolloid Injection and Lymphoscintigraphy
Filtered Tc-99m sulfur colloid was used for IOGP. This technique was available at the AMC and not at the three SSCs. Tc-99m sulfur colloid was prepared to optimize the abundance of smaller particles which are most suitable for lymphoscintigraphy. A Sulfur Colloid kit (CIS-US, Bedford, MA) was prepared with ~100 mCi of Tc-99m pertechnetate (Technelite, Bristol Myers Squibb, Billerica, MA) in a small volume (approximately .25 mL). After boiling and buffering, 1 mL of the final preparation was diluted to 2 mL with .9% sodium chloride and aseptically transferred to a sterile vial through a Millex GP .22-µ m filter unit (Millipore, Bedford, MA). Five hundred microcuries of this filtered modified sulfur colloid were administered intradermally in a volume of .3 to .4 mL with a 26-gauge needle. A total of 500 µ Ci was injected in three intradermal injections superficial to the breast lesion (or, if nonpalpable, in the periareolar region of the quadrant containing the lesion) on the day of the surgical procedure. The skin was marked with an indelible surgical marker to denote the location of injection. The effective radiation dose was estimated to be .0071 mrem/mCi.19

Imaging was performed with a large-field-of-view gamma camera (Siemens, Hoffman Estates, IL) with a low-energy all-purpose collimator. Injections sites were shielded with flexible lead disks, and imaging of the radiotracer flow to the nodal bed or beds was performed with serial static images of 5 minutes each. An identified node was marked on the overlying skin with a permanent ink marker. Beginning in July of 2003, to avoid delays in the operating room, most of the patients received the radiocolloid injection but were not imaged with gamma cameras.

Techniques in the Operating Room
The technique of SLNB used for patients with melanoma with 100% discovery rate (unpublished results) was adapted for use in patients with breast cancer by the senior author in the operating room in 1994. An in-house protocol, approved by the Institutional Review Board, was developed for breast cancer and followed rigorously. The identification rate for the first 60 patients was documented during a learning phase when an additional complete axillary lymphadenectomy (ALND) was performed at the time of the SLNB. The SLN was identified during surgery in 39 patients (65%). The difficulty in identifying the other 21 cases was ascribable to the technique of technetium-labeled sulfur colloid injection. In the initial cases, radiocolloid was injected into the breast parenchyma adjacent to the primary breast tumor and did not always drain to the SLN on gamma camera imaging. There was no radioactive node identified intraoperatively in 21 patients. We evolved at that time to our current technique of injecting radiocolloid intradermally superficial to the tumor immediately before surgery.

Twenty additional board-certified surgeons were trained in house to do SLNB. There was no credentialing body for this new technique. None of the surgeons attended any of the lymphatic mapping courses offered in the United States. The quality of the technique was monitored continuously by the senior author and a research nurse. Criteria for the in-house accreditation of surgeons were based on published national and international criteria.2,19 We looked for >90% identification rate and <5% false-negative rate. We initially aimed at a minimum of 30 learning cases to determine quality. Four surgeons (group 1) continued to regularly perform the procedure. Of the other 17 surgeons (group 2), 6 did at least 20 cases, and the remaining 11 surgeons did less than 5 cases each. Group 2 surgeons occasionally operated at the SSCs. After 300 cases, where both the SLNB and ALND were performed on every case, the discovery rate exceeded 90%, and the false-negative rate was 2.6%. We developed an institutional policy in 1999 that allowed all surgeons with expertise in SLNB to perform this procedure without ALND.

Initially, all SLNBs were performed at the AMC, where lymphoscintigraphy was available. In all cases treated at the AMC, isosulfan blue dye injection was also used. All four surgeons in group 1 also consistently operated at SSCs, where IOGP was not available, and blue dye alone was used to identify the SLN. Because group 1 surgeons did most of the cases, the results we report here constitute a comparison between the successes of the same surgeons operating at the AMC versus the SSCs. Group 2 surgeons were also evaluated even though most did not do 30 cases.

Technique of SLN Identification After Blue Dye Injection
All surgeries were performed by the operating surgeon after appropriate consent was obtained from the patient. The consent process included a detailed discussion about the experimental nature of SLNB. A small number of our eligible patients with breast cancer elected to undergo ALND without SLNB, and their data are excluded from this study.

The intraoperative technique we used for SLNB was described previously.10,12,18 In summary, general endotracheal anesthesia was used in all cases. Intra-operative lymphatic mapping was performed after injection of 5 mL of 1% isosulfan blue into the breast parenchyma adjacent to the breast cancer and into the subareolar plexus in the "clock" position of the tumor. If the tumor in the breast had previously been removed, care was taken to avoid injection into the lumpectomy cavity. The breast was massaged for 5 to 6 minutes. The axilla was explored through a transverse skin incision just below the lowest axillary hair follicles. Careful fine dissection was used to find a blue lymphatic and trace it to a blue lymph node. We tried to find the blue lymphatic first in every case, but this was not always possible. In some cases a blue lymph node was found without first identifying a blue lymphatic; we attempted to identify the afferent lymphatic entering the node and trace it anatomically. Occasionally a dilated blue lymphatic was seen ending abruptly at the surface of a lymph node completely replaced by tumor; the node itself may not be blue or may have a very faint tinge of blue in one small area. When the blue dye was the only agent used, we assessed the correct SLN by the description of one blue lymph node, with a blue lymphatic entering. It has been rare for us to find more than one blue lymph node, although surgeons sometimes found a nonblue lymph node adjacent to the blue node and removed that node as well.

At the AMC we used a gamma probe to confirm that the blue node was also radioactive ("hot"). In 6% of cases in a prior study,9 the blue and the hot nodes were two different nodes, usually adjacent to each other. Additional hot nodes were removed, occasionally yielding more than one SLN. In all cases where a SLN was not identified, a full axillary lymph node dissection (ALND) was performed.

The primary breast tumor was excised by mastectomy or breast-conserving surgery using standard techniques. The terms lumpectomy, partial mastectomy, quadrantectomy, and wide excision were used interchangeably.

Pathologic Evaluation
All primary tumors and axillary lymph nodes were subjected to expert pathologic evaluation by a breast pathologist as previously reported.18 Lymph nodes were fixed in 10% buffered formalin and embedded in paraffin. Five-micron slices were placed on glass slides and standard hematoxylin and eosin staining performed. The SLN was cut in half along the equator of the node, four to six 4-µ m slices cut at various depths, and stained on glass slides. Cytokeratin immunohistochemistry was deliberately avoided except in cases where a few suspicious cells were identified in the node and the pathologist wished to confirm that these were tumor cells. An axillary node was classified as positive (containing metastatic tumor cells) according to current American Joint Commission on Cancer guidelines.

Data Retrieval, Collection, and Abstracting
All patient information was available on an electronic medical record system, updated daily. There were paper medical records available, but they were not necessary for this study. Demographic, clinical, operative, radiological, and pathological information was carefully abstracted by the staff in the Clinical Trials Office in consultation with the principal investigator (S.D.N.) and recorded in an Excel database. Criteria for appropriate abstracting of the SLN identification were established. The operative report was required to include a statement from the surgeon that verified the blue lymphatic and the blue lymph node after appropriate injection of blue dye. The radiology report from the nuclear medicine department confirmed that radiocolloid was injected for those patients operated on at the AMC. The intraoperative gamma counts were recorded, and the surgeon stated that he or she found the node. When the SLN contained tumor, further confirmation of the correct node was the evaluation of the pathology report after the subsequent ALND (when performed), showing that additional nodes did not contain tumor. If additional nodes contained tumor, we relied on the surgeons’ intraoperative notes to confirm the pedigree of the SLN. Regular meetings were conducted to discuss data input. The database was periodically updated and searched for errors, which were corrected. The database was used for analysis by a biostatistician (A.K.) in consultation with the senior author.

Statistical Methods
A total of 1199 SLN results were analyzed from 1187 patients. Surgeons were divided into two groups: four who performed more than 100 SLNBs (high volume) and those (n = 17) who performed less than 100 surgeries (low volume). Comparisons between groups 1 and 2 included whether the SLN was found (yes/no), SLN positive (yes/no), use of IOGP (yes/no), patient age, side of tumor, quadrant of the tumor (upper inner quadrant [UIQ], lower inner quadrant [LIQ], upper outer quadrant [UOQ], and lower outer quadrant [LOQ]), primary tumor size (<1, 1–2, or >2 cm), number of nodes found, and type of surgery (mastectomy vs. lumpectomy). For binary outcomes, generalized estimating equations (GEE) logistic regression models20 were used. Otherwise, comparisons between surgeon groups were made by {chi} 2 tests.

GEE logistic regression modeling also was used to determine a final multivariable model for prediction of SLN identification. Univariate GEE models were run to determine individual predictors of SLN discovery rate. Variables with an individual effect (P < .20) were included in the first multivariable model. The backward model selection method was used to determine a final multivariable model. Two-way or three-way variable interactions were considered only if there were individual variable effects or variable interactions. The final model included variables with P < .05, or interactions with P < .10.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The four surgeons in group 1 performed a total of 877 surgeries, and those in group 2 completed 322 surgeries. Table 1Go lists SLN discovery rate by surgeon group. All four surgeons in group 1 operated at the AMC (where IOGP was available) and the SSCs (where IOGP was not available). Results from the GEE model indicated that the odds of finding SLNs was 2.6 times greater among surgeon group 1 compared with surgeon group 2 (95% confidence interval [95% CI], 1.7, 4.1; P < .0001). Also, in surgeon group 1, the SLN discovery rate was highest (95.8%) for the surgeon who performed the most surgeries and was lowest for the surgeon who performed the least number of surgeries in this group (88.9%). In 1997 the SLN procedure was performed an average of 4.5 cases per month. The numbers progressively increased to 17.8 per month in 2004, dropping to 16 per month in 2005.


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TABLE 1. SLN identification rate by surgeon groupa
 
Table 2Go lists the SLN discovery rate by procedure (IOGP or no IOGP) and surgeon group. Percents are reported within surgeon group by IOGP category. The highest SLN discovery rate was seen among surgeons who used IOGP in surgeon group 1 (96.5%), and was lowest among the group 2 surgeons who did not use IOGP (78.5%). There was no statistically significant difference in the percentage of IOGP procedures between surgeon groups (P = .109). Among surgeons in group 1, the odds of finding the SLN was 2.0 times higher if IOGP was used compared with the use of blue dye alone at the SSCs (95% CI, 1.09, 3.78; P = .024). When SLN biopsy was performed at the AMC (N = 599) and IOGP was available, surgeon group 1 had a slightly higher SLN discovery rate than group 2 (96.5% vs. 94.2%), but this difference was not statistically significant (P = .277). Group 2 surgeons were able to find the SLNB at their first attempt with the gamma probe and blue dye when proctored by the senior author, when the established multidisciplinary protocol was followed. They continued to find the SLN when operating without the senior author even when they had treated only two cases as long as they used a gamma probe intraoperatively. However, there were statistically significant differences for both group 1 and 2 surgeons when IOGP was not performed.


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TABLE 2. SLN identification rate by IOGP and surgeon group
 
Table 3Go reports statistical analyses of SLN discovery rates according to selected clinical, anatomical, pathological, and surgical variables. These variables were chosen because of published reports of their possible effects on the likelihood of SLN identification.21 SLNs were found much more often by group 1 surgeons, when IOGP was used, when the primary breast tumor was smaller, when less SLNs were removed, and when a lumpectomy was performed (compared with a mastectomy). SLN discovery rates were not affected by the side or quadrant of the primary tumor, or by the age of the patient.


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TABLE 3. Generalized estimating equations logistic regression univariate results for SLN discovery rate
 
The SLN was found in 204 (93.6%) of 218 UIQ, 154 (92.2%) of 167 LIQ, 606 (92.1%) of 658 UOQ, and 136 (93.8%) of 145 LOQ tumors. In 8 of 877 group 1 cases and 3 of 322 group 2, cases the exact quadrant could not be allocated; the tumors were probably central.

For analysis purposes, tumor size was divided into three categories: <1, 1–2, and >2 cm. There were three cases where tumor size could not be measured by the pathologist because the tumors were so small that the needle biopsy had removed the entire tumor. There were 293 cases where the tumor size was <1 cm. The SLN was found in 283 of these cases (96.6%). Among cases with tumor sizes ≥ 1 cm, the SLN discovery rate was 91%.

The number of SLNs found (1.73 ± 0.9 (S.D)) was divided into two categories: fewer than two tumors, and two or more tumors. In 1039 patients in whom fewer than two SLN were removed, the actual discovery rate was 969 (93.3%) when we used our modified criteria.

Mastectomy was performed in 303 (25.3%) of 1199 cases. In these cases, the SLN was found in 269 (88.8%), whereas the identification rate in 896 lumpectomy/partial mastectomy cases was 841 (93.9%; P = .01).

Patients operated by group 1 surgeons and summarized in Table 4Go were compared according to the use of IOGP. There were no statistically significant differences in the distribution of any of the variables studied.


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TABLE 4. Comparison of anatomic, pathologic, demographic, and surgical variables in patients, with and without IOGP, treated by four high-volume surgeons
 
The final multivariable model included IOGP, surgeon group, tumor size, and mastectomy. Table 5Go lists the odds ratios and 95% CIs derived from this model. Results showed that after adjusting for all other variables in the model, the odds of finding the SLN was 2.9 when IOGP was used compared with when blue dye alone was used (95% CI, 1.8, 4.7; P < .001). Surgeon group 1 was 2.7 times more likely than surgeon group 2 to find the SLN (95% CI, 1.7, 4.3; P < .001). The odds of finding the SLN was approximately 60% lower among tumor sizes 1–2 cm compared with tumor size <1 cm (95% CI, .19, .79; P = .008). Finally, the odds of finding the SLN among cases where mastectomy was performed was approximately 50% lower compared with patients who did not have a mastectomy (OR = .51, 95% CI, .31, .82; P = .013).


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TABLE 5. Generalized estimating equations logistic regression multivariable model results for sentinel lymph node discovery rate
 
Of the 830 SLNs found by group 1 surgeons, 177 had tumor metastasis (21.3%). Seventy-three of the 280 SLNs found by group 2 surgeons had a positive node (26%; P = .099). In the 47 of 877 and the 42 of 322 patients (group 1 and group 2, respectively) in whom the SLN was not found, none was found by ALND to have tumor metastasis.

As soon as we had the multidisciplinary protocol in place in 1997, the identification rate over time for individual group 1 surgeons ranged slightly upward over time. Each of these surgeons had a 90% to 100% discovery rate when radioguided techniques were used in the operating room.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The sentinel lymph node identification rate in 1187 patients with breast cancer undergoing 1199 biopsies (SLNBs) was far higher when combined radiocolloid and blue dye techniques were used compared with blue dye as the only technique. Individual surgeons’ identification rates could be easily compared in our academic practice because each of the four highest-volume surgeons operated at both the AMC and the SSCs (where IOGP was not available and only the blue dye technique was possible). The success of finding the SLN was much less when the procedure was performed by the same surgeons at SSCs. The success of the technique partly depended on the experience of the surgeon doing the procedure, but the high identification rate was rapidly and easily accomplished by surgeons new to this procedure, provided they used established multidisciplinary protocols developed at the AMC. Identification of the SLN was better when the primary breast tumor was small, and when a lumpectomy was used to treat the primary tumor compared with mastectomy. The age of the patient and the quadrant of the tumor did not seem to affect the identification of the node.

There is still no consensus regarding the optimal lymphatic mapping technique (blue dye alone, or a combination of blue dye and radiocolloid, or radio-colloid alone)2,19 or the optimal learning phase for each of these techniques.1,39,11,1417 Yet our study confirms others15,22 that found that intraoperative identification of the SLN is more successful when accomplished with the aid of a gamma probe after injection of an appropriate lymphophilic radioactive solution.19 Unlike the radiocolloid particles, which are retained in the SLN by phagocytic cells,23 blue dye is not phagocytosed as it traverses the node and is likely to be washed out relatively quickly. Blue dye and radiocolloid usually flow to the same SLN.10 The data show that high-volume surgeons were consistently capable of identifying the SLN at the SSCs, almost as well as their success at the AMC. Low-volume surgeons were much less adept at identifying the SLN when blue dye alone was used, suggesting a need for intraoperative radiocolloid mapping and justifying an attempt to establish this capability in suburban or rural SSCs.

A direct comparison between the sites where the procedures were performed raises questions about the quality of the operating room facilities at the AMC and SSCs. Fortunately, the variable of surgical expertise, identified as important in identification of the SLN,15 was not an issue for group 1 surgeons in our study because the same surgeons operated in both places. Other variables, such as the presence of surgical residents and medical students at the AMC but not always at the SSCs, cannot be assessed in our study. There are no apparent differences in the operating room conditions, and although it is possible that hidden differences may have influenced the quality of the procedure performed at the SSCs, we think that this is unlikely.

Identification of the correct SLN requires a coordinated team of interested and knowledgeable radiologists, surgeons, nurses, and allied health care professionals. A breakdown in any one of these disciplines can undermine the success of the procedure. There are variables in each of the disciplines. The techniques in nuclear medicine departments have matured over the decade that breast SLN has been performed, and it is clear that variations in type of radiocolloid, site, time and dose of injection, the use of lymphoscintigraphy, and the type of gamma probe do not seem to greatly alter the quality of the technical accuracy.19 Handling of tissues in the operating room is an art that can be partially taught by a more senior surgical teacher, but even experienced surgeons may not attain perfection in identification of the SLN.24

The term lymphatic mapping, originally applied to SLNB of melanoma,25 may have a different meaning in breast SLNB because different parts of the breast seem to drain to the same SLN in the axilla;10 in melanoma, different areas of skin drain to different nodes. During the learning phase in our institution, a key learning issue was the friability of the main afferent lymphatic coursing toward the SLN. The thin walled lymphatic trunk, usually no more than 100 µ m in diameter,26 is easily disrupted by cautery, by overly aggressive blunt dissection techniques, or by sharp instruments. Interruption of the main lymphatic trunk is often disastrous when blue dye is used alone, but not when radiocolloid has been injected before surgery. Relatively inexperienced surgeons can rely on gamma probe identification, but the learning curve for blue dye is a much longer process.6,9,15,16

Breast cancers in this series, as in others,27 were most often in the UOQ on either side. As reported previously, we had four cases in which lower inner quadrant radiocolloid injections drained to the internal mammary nodes and not to the axilla. However, the identification rate did not depend on the quadrant of the tumor. This finding confirms the experimental findings that the predominant lymphatic drainage of the breast, irrespective of quadrant, is to the axilla.

Smaller tumors have far higher identification rates. There is no obvious reason for this finding, although it is tempting to speculate that it may be related to the incidence of SLN metastasis. Primary tumor size in the breast is directly related to the likelihood of SLN metastasis.18 Macroscopic tumor in the SLN may alter the pressure in the node,28 which could in turn change the direction of flow in the main lymphatic trunk or trunks toward adjacent (nonsentinel) nodes. In our study, the only way that this could have been observed would have been when full ALNDs were performed in our early experience with SLNB, and a false-negative result obtained.

Discussions with surgeons about their comfort level and confidence in performing SLNB speak to the learning curve in a nonquantitative way. High-volume surgeons (group 1) soon became adept at the technique when radioguidance was used in the operating room, but they took a little longer to attain >90% identification rates when blue dye was used alone. Although hard to quantify in a retrospective analysis, there were anecdotal cases for each of the four surgeons in this group in whom the SLN was not found because there was no visible blue dye in the axilla. Over time, the surgeons have become more astute at seeing subtle signs of the SLN (such as an almost ethereal greenish tinge in the fat) that aided in pursuit of the node. Other tricks may be learned by trial and error over time, such as the realization that the SLN is often closely associated with the lateral thoracic vein and artery, and that we are often a little too high in the axilla when we cannot find the blue lymphatic. Each of the surgeons became more confident more quickly after doing their first 30 cases aided by radioguidance. Even low-volume surgeons were able to immediately function like high-volume surgeons when IOGP was available. The learning curve may be a phenomenon of the blue dye technique, but it does not seem to apply when a gamma probe is used intraoperatively.

There is no reason why SLN identification rates were higher when a lumpectomy was performed rather than a mastectomy. This difference was not seen at the AMC, and it may be related to the site of axillary incision when a mastectomy was performed when IOGP was not available. Some surgeons did not extend their mastectomy incisions into the axilla when immediate breast reconstruction was not performed. It is possible that this simple difference of not following the usual incision in the axilla may have adversely affected the discovery rates because the site of the node was away from the closest incision. Our practice of performing skin-sparing mastectomies during immediate reconstruction should not be a reason, because most surgeons make a second skin incision in the axilla during this procedure.

Older age has been reported to make it more difficult to find the SLN.21 This may be related to the presumed slower lymphatic flow in older women or to the progressive replacement of nodes by fat. Neither of these proposed mechanisms has been proven, and our data do not support the concept.

The data suggest that sentinel node procedures should be performed where nuclear medicine facilities are available. Implementation of radiocolloid injection in suburban ambulatory surgery centers outside of specialized academic centers needs a nuclear medicine facility and quality control through a radiation safety team. This requires space, personnel, and resources, all precious commodities in an economically constrained health care environment. As such, it is neither reasonable nor cost effective. An alternative option would be to inject the radio-colloid the day before surgery at a high-quality, approved nuclear medicine facility. The patient could have her surgery the next day at the SSC, where it would be reasonable to have a permanently available IOGP.

There is still controversy regarding the optimal learning curve for the sentinel node technique in breast cancer.2 Individual surgeon volume plays a role, as in many other specialized surgical procedures.29 Our experience suggests that we were able to accelerate the rate of identification in previously naive surgeons by providing an established multidisciplinary technique and supervision by an experienced surgeon.


    ACKNOWLEDGMENTS
 
Supported in part by the Nathanson/Rands Chair for Breast Cancer Research, awarded to S.D.N.


    FOOTNOTES
 
Presented in part at the 59th Annual Cancer Symposium of the Society of Surgical Oncology, San Diego, CA, March 25, 2006.

Received for publication March 17, 2006. Accepted for publication October 18, 2006.


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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S. D. Nathanson, M. Burke, R. Slater, and A. Kapke
Preoperative Identification of the Sentinel Lymph Node in Breast Cancer
Ann. Surg. Oncol., November 1, 2007; 14(11): 3102 - 3110.
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