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Published online before print June 20, 2003, 10.1148/radiol.2282020651
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(Radiology 2003;228:546-551.)
© RSNA, 2003

Breast Imaging

Lymphatic Mapping in Patients with Breast Carcinoma: Reproducibility of Lymphoscintigraphic Results1

Pieter J. Tanis, MD, PhD, Renato A. Valdés Olmos, MD, PhD, Saar H. Muller, PhD and Omgo E. Nieweg, MD, PhD

1 From the Departments of Surgery (P.J.T., O.E.N.) and Nuclear Medicine (R.A.V.O., S.H.M.), Netherlands Cancer Institute, Amsterdam. Received May 28, 2002; revision requested July 18; final revision received November 18; accepted December 10. Address correspondence to P.J.T., Department of Surgery, St Lucas Andreas Hospital, Jan Tooropstraat 164, 1006 AE Amsterdam, the Netherlands (e-mail: p.tanis@slaz.nl).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
PURPOSE: To evaluate the reproducibility of lymphoscintigraphic results in assessment of the location and number of sentinel nodes in patients with breast cancer.

MATERIALS AND METHODS: Twenty-five patients with breast cancer were prospectively enrolled in this study. Lymphoscintigraphy was performed after intratumoral injection of about 130 MBq of technetium 99m nanocolloid. Anterior and lateral images were obtained 20 minutes and 2 and 4 hours after injection. The following day, scintigraphy was repeated after a second injection of the radiolabeled colloid in an identical fashion and was preceded by acquisition of a starting image. Two observers evaluated the paired images independently, and count rates were calculated from the images. Correlation coefficient and Bland-Altman methods were used to analyze the paired count rates.

RESULTS: At least one sentinel node was visualized at lymphoscintigraphy in all 25 patients. Drainage to the axilla was observed in 17 patients; drainage to the axilla and extraaxillary basins, in seven patients; and drainage exclusively to extraaxillary sentinel nodes, in one patient. The second scintigraphic study revealed the same drainage pattern in all 25 patients (reproducibility, 100%; 95% CI: 86%, 100%). The Pearson correlation coefficient of the paired count rates was 0.54 (P < .001). Count rates at repeat scintigraphy were 23%–417% of the count rates at first scintigraphy in 95% of cases.

CONCLUSION: Results of lymphoscintigraphy for lymphatic mapping in breast cancer are highly reproducible for assessment of the number of sentinel nodes.

© RSNA, 2003

Index terms: Breast neoplasms, radionuclide studies, 08.12166 • Lymphatic system, radionuclide studies, 997.12974 • Radionuclide imaging, in diagnosis of neoplasms


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Lymphatic mapping reveals the draining regional lymph node basin(s) of a primary tumor and the number and exact location of sentinel nodes. The use of a radiolabeled colloid at preoperative lymphoscintigraphy and intraoperative detection with a gamma-ray detection probe have recently been incorporated into the traditional blue dye protocol for lymphatic mapping to optimize the visualization of all lymph nodes on a direct drainage pathway (1). Lymphoscintigraphy enables identification of unexpected drainage routes and is helpful in determining the exact number of sentinel nodes and in distinguishing first- from second-tier nodes. Although sensitivity of and interobserver variability at lymphoscintigraphy are reported to be favorable, various other aspects also determine the accuracy of an imaging technique (2).

Lymphoscintigraphy with technetium 99m (99mTc) nanocolloid for lymphatic mapping in patients with melanoma does not always reveal the complete drainage pattern (3). In three (12%) of 25 patients, the exact number of sentinel nodes could not be reproduced at repeat examination (3). One should not assume that results of a study of melanoma can be extrapolated to breast cancer. There are many other factors that influence lymphoscintigraphy in breast cancer: The tumor is still in place, a different type of injection is used, and the lymphatic drainage of the breast is complex. Because scintigraphy is a crucial part of lymphatic mapping, establishing the reproducibility of its results in patients with breast cancer is important. Thus, the purpose of our study was to evaluate the reproducibility of lymphoscintigraphic results in the assessment of the location and number of sentinel nodes in patients with breast cancer.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From November 2000 to October 2001, 25 patients with a clinical diagnosis of T1N0 or T2N0 breast cancer who met the inclusion criteria and signed informed consent forms were prospectively included in this study. Patients who had previously undergone excisional biopsy and patients with a nonpalpable breast carcinoma were not eligible. The mean age of the patients was 54 years (range, 36–84 years).

A preoperative diagnosis was obtained with the aid of physical examination, mammography, ultrasonography, and fine-needle aspiration cytology or core biopsy. The tumor was situated in the upper outer quadrant in 13 patients, the lower outer quadrant in two, the upper inner quadrant in five, the lower inner quadrant in four, and in the central part of the breast in one. The clinical stage was T1 in 19 women and T2 in six women. The histologic diagnosis of the primary tumor was ductal carcinoma in 21 patients, lobular carcinoma in two, mucinous carcinoma in one, and medullary carcinoma in one. Informed consent was obtained from all patients, and the protocol of investigation was approved by the ethical committee of our institution.

Imaging
The first lymphoscintigraphic examination was routinely performed (R.A.V.O.) the day before surgery. Nanocolloid (Nanocoll; Amersham Cygne, Eindhoven, the Netherlands) with a particle size of less than 80 nm was labeled with 99mTc by using a labeling dilution volume of 2.0 mL. The average net administered dose was 131 MBq (range, 111–156 MBq). The tumor was fixed between two fingers, and the overlying skin was stretched. A 25-gauge needle was inserted into the center of the lesion. The radioactive tracer was injected slowly into the tumor to an average volume of 0.2 mL. Anterior and prone lateral (ie, "hanging breast") planar images were obtained 20 minutes and 2 and 4 hours after injection with an acquisition time of 5 minutes. Simultaneous transmission scanning with a cobalt 57 (57Co) flood source was used to facilitate orientation. Images were produced by using a dual-head gamma camera (ADAC, Milpitas, Calif) with low-energy high-spatial-resolution collimators. The location of the sentinel node was marked on the skin by using a 57Co pen.

On the day of surgery, a 5-minute static image was obtained early in the morning as a point of reference for the second injection. Subsequently, the procedure described above was repeated in an identical fashion by the same investigator. The mean time between the first and second injections of the radiolabeled colloid was 23 hours (range, 22–24 hours). The mean radioactivity dose of the second injection, calculated on the basis of net administered doses, was 133 MBq (range, 117–156 MBq). To reduce the workload, the 2-hour image was omitted during repeat lymphoscintigraphy. Sequential imaging on the second day was thought to be less important, because our main purpose was to compare the lymphatic drainage patterns rather than to determine the dynamics of lymph flow. The timing of the last image was sometimes influenced by the operating room schedule, resulting in small differences with regard to the time between injection and acquisition of the last image at the second scintigraphic examination compared with the first scintigraphic examination.

Just before surgery, patent blue dye (Blue Patenté V; Laboratoire Guerbet, Aulnay-sous-Bois, France) was injected into the tumor to a volume of 1.0 mL. The sentinel node was identified and harvested after careful dissection of blue lymphatic vessels and detection of radioactivity with a gamma-ray detection probe (Neoprobe; Johnson & Johnson Medical, Hamburg, Germany). Sentinel nodes were fixed in formalin, bisected, embedded in paraffin, and cut at a minimum of six levels in 50–100-µm intervals. Paraffin sections were stained with hematoxylin-eosin and an immunohistochemical stain (CAM5.2; Becton Dickinson, San Jose, Calif).

Data Interpretation and Statistical Analysis
Images were evaluated with regard to similarity of depiction of draining lymph node basin and location and number of sentinel nodes. Two observers (P.J.T., R.A.V.O.) independently evaluated the paired images. In case of disagreement, a definitive outcome was reached by consensus. A hot spot was defined as a sentinel node on the basis of one or more of the following criteria: visualization of an afferent lymphatic channel, the appearance of this hot spot as the first in a sequential series of hot spots, or the appearance of a single hot spot in a particular lymph node basin. The 95% CI of the calculated reproducibility was determined by using the binomial distribution.

Radioactive count rates for the visualized sentinel nodes were measured on 5-minute anterior images by using the region-of-interest software linked to the gamma camera on images acquired at three points in time: the last image acquired at routine lymphoscintigraphy, the starting image acquired before the second injection, and the last image acquired at repeat scintigraphy. Count rates were calculated as the number of counts per pixel. The count rate for hot spots visualized during the second scintigraphic examination was corrected for differences in the time between injection and acquisition of the last image, differences in net administered radioactivity dose, and residual radioactivity. The paired count rates for each hot spot were plotted to determine the variability of lymphatic flow and tracer uptake. The correlation coefficient between the two sets of scintigraphic results was calculated. P < .05 was considered to indicate a statistically significant difference. In addition, the Bland-Altman method was used to determine the amount of agreement between the count rates at the two scintigraphic examinations (4). A logarithmic data transformation was performed because the differences were proportional to the mean count rate. Analyses were performed with Statistical Package for the Social Sciences software (SPSS, Chicago, Ill).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The visualization rate at routine preoperative lymphoscintigraphy was 100% (ie, at least one sentinel node was visualized in 25 of 25 patients). A total of 50 sentinel nodes were depicted in 34 basins, with a mean number of 2.0 nodes (range, 1.0–5.0 nodes) per patient and a mean number of 1.5 nodes (range, 1.0–3.0 nodes) per basin. The lateral image was of additional value in eight (32%) of 25 patients. Lymphatic drainage exclusively to the axilla was observed in 17 patients. Seven patients had drainage to both the axilla and nonaxillary basins: to the internal mammary chain in five patients, to the infraclavicular fossa in one, and to the internal mammary chain and the infraclavicular fossa in one. One patient had drainage exclusively to nonaxillary sentinel nodes (Fig 1).



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  		Figure 1. Anterior lymphoscintigraphic images in a 51-year-old woman show drainage from a tumor (T) in the upper inner quadrant of the right breast to two paramammary nodes (solid arrows) and internal mammary chain nodes (open arrow). Compared with A, the late image acquired at initial lymphoscintigraphy, B, the late image acquired at repeat lymphoscintigraphy shows an identical drainage pattern, with a slightly changed distribution of radioactive tracer uptake by the lymph nodes.

 
The second scintigraphic study revealed the same drainage pattern in all 25 patients; the same number of nodal basins and the same number of sentinel nodes were visualized at identical locations (Table 1, Fig 2). This resulted in a reproducibility of 100% with a lower 95% confidence limit of 86%.


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  		TABLE 1. Patient Characteristics and Scintigraphic Findings

 


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  		Figure 2. Three paired sets of late anterior scintigraphic images show lymphatic drainage from a primary tumor (T) to identical nodal basins and the same number of sentinel nodes. A and B (obtained in a 37-year-old woman) show drainage to a single axillary sentinel node (arrow in A), C and D (obtained in a 48-year-old woman) show drainage to two axillary (solid arrows in C) and two internal mammary chain (open arrows in C) sentinel nodes, and E and F (obtained in a 52-year-old woman) show drainage to one axillary (solid arrow in E) and two internal mammary chain (open arrows in E) sentinel nodes. Beside the two internal mammary nodes with high radiocolloid uptake (interpreted as being sentinel nodes) in E and F, three lymph nodes with less intensity and three nodes with very faint uptake are visualized in both images. The second hot spot in the axilla observed on F, an image obtained during the second scintigraphic examination, was also seen during the first scintigraphic examination, especially on the lateral image (not supplied). The variability in lymphatic flow and lymph node uptake is nicely illustrated in C and D.

 
Measurements could be obtained in 43 hot spots representing 50 sentinel nodes (some sentinel nodes were located too close to each other to allow us to measure each node separately). All 43 hot spots visualized during routine lymphoscintigraphy showed an increase in radioactivity content after the second injection of radiolabeled colloid (Fig 3). The paired count rates for each hot spot are displayed in Figure 4. The Pearson correlation coefficient for the count rates at the first and the second scintigraphic examinations was 0.54 (P < .001). The differences in count rates between the first and second scintigraphic examinations were plotted against their means after logarithmic transformation according to the Bland-Altman method (Fig 5). The mean difference was -0.024, and the SD was 0.74 on the log scale. The 95% limits of agreement were -1.48 and 1.43 for these values. The antilogs of -1.48 and 1.43 are 0.23 and 4.17, indicating that count rates at repeat scintigraphy were 23%–417% of the count rates at initial scintigraphy in 95% of cases.



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  		Figure 3. Graph shows the count rate for each hot spot (n = 43), as measured on 5-minute images obtained at three points in time: (1) the late image obtained at initial scintigraphy, (2) the starting image obtained just before the second radiocolloid injection, and (3) the late image obtained at repeat scintigraphy.

 


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  		Figure 4. Scatterplot shows correlation between the count rates of each sentinel node, as measured on the late image of the first and second lymphoscintigraphic examinations (Pearson r = 0.54, P < .001). Count rates were corrected for differences in administered dose, for differences in time between injection and acquisition of the late image, and for residual radioactivity that was still present during the second study. The relatively low correlation between the paired count rates demonstrates the intraindividual variability in radiocolloid uptake.

 


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  		Figure 5. Scatterplot depicts agreement of sentinel node count rates at two lymphoscintigraphic examinations, as calculated with the Bland-Altman method after logarithmic data transformation. The mean difference in log count rate between the first and second scintigraphic examinations is illustrated by the middle dotted line, and the upper and lower 95% confidence limits, respectively, are illustrated by the upper and lower dotted lines. This analysis quantifies the difference in lymph node radiocolloid uptake during the second scintigraphic examination; uptake at the second scintigraphic examination ranged between four times lower and four times higher than that observed at the first scintigraphic examination.

 
All visualized hot spots in the axilla, internal mammary chain, and infraclavicular fossa could be localized by using the handheld gamma-ray detection probe. Two internal mammary sentinel nodes, however, were located behind a rib and were not harvested. The paramammary sentinel nodes could not be measured separately from the injection site because they were too close to the site to be identified. In two patients, an additional axillary sentinel node was found only by using blue dye. Metastasis was found in an axillary sentinel node in 13 (52%) of the 25 patients. In one additional patient, a firm lymph node without radioactive tracer uptake or blue discoloration was excised. This lymph node was positive for carcinoma, while the sentinel node was negative for carcinoma. Two additional nodal metastases were found at subsequent axillary dissection in this patient. All nonaxillary sentinel nodes were negative for carcinoma.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In our study, each hot spot visualized during lymphoscintigraphy showed an increase in radioactivity after repeat injection of 99mTc nanocolloid into a breast carcinoma. The high reproducibility of lymphoscintigraphic results for lymphatic mapping in breast cancer observed in the present study is in contrast to observations in studies of melanoma. Table 2 presents a review of studies in which the reproducibility of lymphoscintigraphic results was assessed. Only two investigators performed lymphoscintigraphy twice in an identical fashion, resulting in reproducibility rates of 85% and 88% (3,5).


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  		TABLE 2. Review of Studies of Reproducibility of Lymphoscintigraphic Findings

 
Four possible explanations for limited reproducibility of lymphoscintigraphic results were considered in a study of melanoma (3). The first explanation was the existence of inevitable small variations in the site of injection and in the injected volume. The former explanation was studied by Rettenbacher and colleagues (9). Expanding the injection site–to-tumor distance from 2–5 to 10 mm resulted in an increase in the visualization rate (from 93% to 100%) and visualization of additional sentinel nodes in 16% of patients (9). One may question whether this resulted in higher accuracy (12). A second explanation was related to characteristics of the radioactive tracer such as particle size. A third explanation consisted of patient-related factors such as previous exertion, body hydration, and variation in oncotic and hydrostatic pressure of blood that may play a role (13). Finally, it was thought that the time between the two examinations could result in discordance (13). The wound healing process after primary excision of the melanoma may alter lymphatic drainage patterns.

By taking these explanations into account, the high reproducibility of lymphoscintigraphic results for sentinel node identification in breast cancer compared with that of lymphoscintigraphic results in melanoma could have been predicted. A single intratumoral injection in a volume ranging between 0.18 and 0.22 mL may be less liable to variation compared with the four injections at a certain distance from the primary excision scar that are typically performed in scintigraphy of melanoma. The reason we used a small injection volume is that we did not want to disturb the normal physiology of the lymphatic system. Patients with breast cancer who had previously undergone surgical treatment were not eligible for enrollment in our study because of our intratumoral injection technique. The existence of lymphatics in a tumor and their role in lymphangiogenesis is the theoretical basis for this route of administration, which probably reflects lymphatic drainage from the primary tumor better than injection at a certain distance.

Because we excluded patients who had undergone excisional biopsy, we eliminated the likelihood that patients in whom lymphatic drainage was disturbed owing to replacement of granulation tissue by more dense and compact fibrous tissue after surgical intervention would be included in this study. Several authors have concluded that previous excisional biopsy of breast cancer has no effect on the results of lymphatic mapping, but only secondary end points were used in these studies (14,15). It would be interesting to compare results of paired lymphoscintigraphic examinations performed before and after excision of a breast carcinoma.

Some investigators have studied the effect of different radiopharmaceuticals on lymphoscintigraphic results (16–18). Three groups of investigators evaluated paired scintigraphic studies of melanoma in which 99mTc human serum albumin and 99mTc sulfur colloid were used (6–8). Human serum albumin is a nonparticulate tracer with rapid drainage. Sulfur colloid has a relatively large particle size and is characterized by slow flow and prolonged nodal retention. Furthermore, it has been reported that sulfur colloid particle size increases after approximately 5 hours (19). After studies in melanoma, Wong et al (7) reported no discernible differences in sentinel node localization between these two tracers, and Tonakie et al (8) attributed a few observed discrepancies to a reduced tracer dose.

The importance of a sufficient tracer dose is in agreement with findings in breast lymphoscintigraphy (20,21). Variation in the composition of the tracer in terms of particle size may have repercussions for the reproducibility of the results of the procedure, although the role of variation in particle size seems to be minimal, given the findings in the previously mentioned studies. The particles of 99mTc nanocolloid we used are less than 80 nm in size, which meets the criteria for optimal inert colloids for interstitial lymphoscintigraphy (19). Further investigation of different agents may be needed to exclude unfavorable characteristics that can cause variable outcomes.

Variability in lymphatic drainage patterns is theoretically one of the explanations for false-negative results of sentinel node procedures. The 100% concordance for nodal basins, number of sentinel nodes, and sentinel node location in the present study reduces the likelihood of this explanation, despite the fact that intraindividual variability in radiocolloid uptake by the sentinel node was quite high. However, discrepancies with the blue dye method occur fairly frequently (22–24). This may be caused by the characteristics of the two tracers, the site of injection, and the injected volume. Blue dye can enable visualization of an afferent lymphatic vessel leading to a sentinel node without having to be phagocytosed by that lymph node. In general, different physicians perform injection of the radiolabeled colloid and blue dye, resulting in differences in injection technique. The injected volume of blue dye is often greater than the volume of the radioisotope. But even with the use of blue dye, some sentinel nodes remain undetected, with the risk that some nodal metastases are missed. One of the primary reasons for this phenomenon is probably that a sentinel node is completely filled with a metastasis, so the inflow and uptake of tracers are prohibited (25–27); this phenomenon was observed in one of the patients in our study.

In conclusion, accuracy of lymphatic mapping is of utmost importance now that axillary node dissection is usually not performed in patients who have breast cancer but negative sentinel nodes. We believed there was a need to learn more about the reproducibility of lymphoscintigraphic results because lymphoscintigraphy is one of the cornerstones of lymphatic mapping. The results of the present study indicate that lymphoscintigraphic results were reproducible in the assessment of axillary and nonaxillary drainage in all 25 patients. Our data suggest that intraindividual variability in lymphatic drainage is an unlikely explanation for false-negative results of sentinel node procedures, but further study is needed to confirm this.


   ACKNOWLEDGMENTS
 
We thank Emiel J. T. Rutgers, MD, PhD, surgeon, Cornelis A. Hoefnagel, MD, PhD, head of the Department of Nuclear Medicine, and Bin B. R. Kroon, MD, PhD, head of the Department of Surgery, for their support of this study and their critical review of the manuscript.


   FOOTNOTES
 
See also the editorial by Liberman in this issue.

Author contributions: Guarantor of integrity of entire study, O.E.N.; study concepts and design, all authors; literature research, clinical studies, and data acquisition, P.J.T., R.A.V.O.; data analysis/interpretation, all authors; statistical analysis, P.J.T., S.H.M.; manuscript preparation and definition of intellectual content, all authors; manuscript editing, P.J.T., O.E.N.; manuscript revision/review and final version approval, all authors


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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