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10.1245/s10434-006-9046-4
Annals of Surgical Oncology 13:1682-1689 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Ultrasound-guided Fine Needle Aspiration Cytology prior to Sentinel Lymph Node Biopsy in Melanoma Patients

Christiane Voit, MD1, Martina Kron, PhD2, Gregor Schäfer, MD1, Alfred Schoengen, MD3, Heike Audring1, Ansgar Lukowsky1, Markus Schwürzer-Voit, MD1, Wolfram Sterry, MD1, Helmut Winter, MD1 and Jürgen Rademaker, MD4

1 Department of Dermatology of the Charité , Humboldt University, Berlin, Germany
2 Department of Biometry and Medical Documentation, University of Ulm, Ulm, Germany
3 Department of Medical Oncology, Armed Forces Hospital, University of Ulm, Ulm, Germany
4 Department of Radiology, Memorial Sloan-Kettering Cancer Center, New York, New York, USA

Correspondence: Address correspondence and reprint requests to: Christiane Voit, MD; E-mail: christiane.voit{at}charite.de


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Sentinel lymph node biopsy (SLNB) allows early detection of metastases, thereby enabling early treatment in melanoma patients likely to benefit from adjuvant therapies. This prospective study analyzes the possible benefits of additional ultrasound (US) and fine needle aspiration cytology (FNAC) of sentinel nodes (SN) prior to SLNB.

Method: Over a 2-year period 127 melanoma patients with 151 SN were scheduled for SLNB. All SN were initially identified with lymphoscintigraphy, then identified and evaluated by US and the cells aspirated for cytology (FNAC). US findings and FNAC results were compared to surgical findings.

Results: Of 127 patients, 114 had one SN each, 12 had two, and one had three. In vivo US achieved a sensitivity of 79% (95% CI: 62–91%) and a specificity of 72% (95% CI: 62–81%). FNAC showed a sensitivity of 59% (95% CI: 41–76%) and a specificity of 100% (95% CI: 95–100%). The combination of these two in vivo methods achieved an overall sensitivity of 82% (95% CI: 65–93%) and an overall specificity of 72% [95% CI: 62–81%].

Conclusion: Combined US and FNAC provides important information prior to SLNB in that both procedures identify metastases in the lymph nodes (sensitivity > 80%). Patients with positive FNAC may proceed directly to complete lymph node dissection (cLND) instead of having initial SLNB. Thus, combined US and FNAC may prevent unnecessary anesthesia and surgical management as well reduce costs. In our study 16% (19/121) fewer SLNB procedures were carried out, subsequently replaced by cLND. For patients with a negative combination of in vivo US and FNAC, SLNB remains the best diagnostic option.

Key Words: Sentinel lymph node biopsy • Fine needle aspiration cytology • Ultrasound • Melanoma


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In recent years, both the incidence of and the mortality rate from melanoma have increased despite great efforts to achieve early diagnosis.1 The involvement of loco-regional lymph nodes is the most important predictive factor for overall survival.2 A "diagnostic" sentinel lymph node biopsy (SLNB) provides early identification of metastases in the excised lymph node;3 this in turn justifies the "therapeutic," and more aggressive, complete lymph node dissection (cLND).

A detection rate of approximately 97% for sentinel nodes (SN) is achieved by combining techniques of radio-colloidal technetium-99m application, blue-dye-mapping, and intraoperative gamma-probe.4–6 Ultrasound (US) and fine needle aspiration cytology (FNAC) has been shown to identify local regional metastases earlier than physical examination with a high sensitivity and specificity during the follow-up of melanoma patients.7,8 FNAC has been proven to be a potent diagnostic tool with high sensitivity and even higher specificity,7,9–12 but it is only applied in specialized medical centers.13

The purpose of this prospective study was to analyze the possible advantages of US and FNAC prior to SLNB for patients with melanoma. More specifically, our aim was to assess the sensitivity and reliability of identifying sentinel lymph nodes with US and the ability to identify positive–involved–sentinel lymph nodes with US and FNAC. As part of this process, we investigated whether the SN identified by lymphoscintigraphy was the same one as that identified by US and whether the site of the SN indicated by US was identical to the site apparent following lymphoscintigraphy. Sentinel lymph nodes were examined with US and FNAC and the findings were compared with the surgical findings from SLNB. A high diagnostic accuracy of US and FNAC would justify the use of both procedures before SLNB and thereby allow some patients to proceed directly to the therapeutic cLND without undergoing SNLD.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
Our prospective study included 127 consecutive patients who were scheduled for SLNB after the excision of suspected melanoma between July 2001 and August 2003. The institutional ethical review board approved the study, and informed consent was obtained from all patients enrolled. At the time of enrolment, the new version of the American Joint Committee on Cancer (AJCC) staging system for melanoma was applied to our patient population. Patients’s tumor data were not known in all cases prior to the in vivo examination, but in cases of primary melanoma with a tumor depth of less than 1 mm and without ulceration and/or regression, patients were excluded from the study. Figure 1Go summarizes the order of the examinations and interventions in our study. Table 1Go summarizes the patients’s clinical data.


Figure 1
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  		FIG. 1. Flowchart of the procedures and interventions carried out in this study. US, Ultrasonography; SN, sentinel node; FNAC, fine needle aspiration cytology; SNLB, sentinel lymph node biopsy.

 

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  		TABLE 1. Summary of the clinical data
 
Methods
All patients were scheduled for SLNB and examined by US in the B-Mode and Power Doppler in vivo before and also after lymphoscintigraphy in order to identify the location that had been proposed for the SN by lymphoscintigraphy. Our aim in using US was to clearly depict the location of the suspected SN prior to surgical treatment. Since patients with truncal, head, or neck melanoma commonly drain to more than one basin and marking with lymphoscintigraphy proved to be helpful, FNAC material was only aspirated during the second sonographic examination after lymphoscintigraphy. The US findings were passed on to the surgeon. Repeated FNAC took place to aspirate material from the suspected in vivo SN prior to SLNB. In addition, the excised SN–detected intraoperatively by a combination of lymphoscintigraphy and blue-dye mapping as standard procedure–was sonographically examined between two gel stand-off pads following surgery and before histology. This was carried out in order to compare the sonographic shape and measurements of the ex vivo SN with the sonographic shape and measurements of the in vivo SN. See Fig. 1Go.

Classification via Ultrasound
Pre-operatively we performed a high-resolution US examination of the lymphatic basin and the lymphatic drainage of the tumor. All US examinations were performed using the high-end device Technos (ESAOTE, Italy) equipped with three transducers of between 3.5 and 14 MHz (B-mode, 30 pictures per second, color Doppler, Power Mode). The lymph node was measured, classified as benign (b), suspect for benignity (sfb), suspect for malignancy (sfm) or malignant (m). The region was always examined in comparison to the contralateral side.

Fine Needle Aspiration in Detail
FNAC was performed with a hand-held "Binder"-valve, which provides an especially short distance between the button for initiation of aspiration and the region of interest. This makes it possible to aspirate even very small targets without losing contact with the lesion in the process. US-guided FNAC uses an alcoholic fluid as a conductor medium, thus minimizing the danger of infection. The fine needle for superficial lymph nodes has a diameter of approximately 0.4 mm (26G). For deeper lymph nodes (depth > 25 mm) a 22 G lumbar puncture needle is used. The negative pressure for aspiration is performed with a 20-ml syringe by fixing the plunger at the 10 ml position, thereby creating an approximate negative pressure of about –300 cm H2O. We performed numerous aspirations under sonographic guidance to receive multiple smears for cytodiagnostic evaluation. A smear was considered to be technically efficient if it contained approximately 100 cells. FNAC procedures performed in small targets, such as intranodal areas within a sentinel node, with a needle diameter of only 0.4 mm often obtain a smaller number of cells and thus tend to give ‘unrepresentative’ results. In order to deliver representative results, multiple and repeated FNAC procedures must be performed.

Postsurgical Evaluation (Post-SLNB)
Directly after SLNB the excised node was studied by US between two gel-pads of 10-mm thickness to achieve a high focus within the lymph node (Fig. 1Go). Again we documented the diameter and volume and compared the structure of the parenchyma to that shown in the in vivo pictures. The malignancy was assessed and classified again in vitro as b, sfb, sfm, or m (see above). As a result we were able to determine whether the excised SN coincided with the one seen and punctured in vivo (Fig. 2Go). The SN was then sliced into 1-mm thick sections and evaluated histologically. Standard techniques, including those for HMB-45 and Melan-A, were performed.


Figure 2
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  		FIG. 2. Technical arrangement of the ex vivo ultrasound of the sentinel node. The excised SN and adjacent tissue are shown between stand-off gel pads directly after excision and before ex vivo US examination.

 
Patterns in Ultrasound
To estimate criteria for the SN we evaluated the node’s size and shape in the expected lymphatic basin in comparison to circumjacent nodes. A more symmetrical broadening of the parenchymal periphery, a cap-like structure where the afferent lymphatic vessels enter, and a certain pattern of vascularization (rather central) as described elsewhere have been found to be relatively typical patterns for the SN.14,15 Our experience suggests that involved SN show a more asymmetrical broadening of the periphery (often hump-like) with a localized hypervascularization in the periphery and/or echo-free islands within the node and/or a slight increase in vascularization. The non-sentinel lymph nodes in the depth of the subcutaneous tissue usually present an iso-echoic structure, so that they only rarely can be discriminated from the surrounding fatty tissue. In most cases a non-malignant lymph node has a Vasallo-index > 2.16,17

Statistics
To assess diagnostic value separately for US and FNAC, sensitivity, specificity, positive and negative predictive values with corresponding 95% confidence intervals (95% CI) were calculated. Additionally, sensitivity, specificity, and predictive values were calculated for the combination of US and FNAC by defining a positive test as a test that is positive in at least one of the two methods. The statistical analyses were performed with the Statistical Analysis System Version 8.2 (SAS Institute, Cary, N.C.).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Median tumor Breslow depth was 2.1 mm, and most patients had Clark level III (39%) or IV (51%) (Table 1Go). One hundred forty-one SN were evaluated in 127 patients; of these, 114 patients each had one sentinel lymph node evaluated, 12 patients had two, and 1 patient had three. Three patients presented with palpable regional lymph nodes. In 121 of the 141 sentinel nodes evaluated ex vivo we found that the in vivo and ex vivo sonographic examinations matched. In one case, neither the US nor surgery was able to detect any lymph node, leading to a unique matching result. Five SN were not seen on the in vivo US, or were post-sentinels, i.e. second-echelon lymph nodes with no signs of malignancy and therefore were not subject to further evaluation. For an additional 14 SN, the in vivo and ex vivo sonographic examinations did not match, but none of these SN was histologically malignant.

Certain patterns on US, such as asymmetrical broadening of the parenchymal periphery (often hump-like), a cap-like structure, and a certain pattern of vascularization, are considered to be typical for metastasis in sentinel lymph nodes14,18 (Fig. 3Go). When we compared the in vivo US evaluation with the histological one (Table 2Go), 34 of the 121 in vivo and ex vivo matching nodes were histologically malignant or suspicious for malignancy (30 m, 4 sfm, respectively). For those SN classified as merely suspicious for malignancy based on histology, very few cells (< 10) could be detected by histopathology. Of these 34 nodes, 27 had already been evaluated as malignant or suspicious for malignancy based on the in vivo US examination, indicating that in vivo US had a sensitivity of 79% (95% CI: 62–91%). Six of the 34 nodes were classified as "possibly benign" (sfb) based on the US, and four were histologically classified as being merely suspicious for malignancy, meaning that very few cells (< 10) could be detected by histopathology. Of the 121 lymph nodes with matching in vivo and ex vivo US results, 87 were histologically negative (87 benign and 0 sfb). In 63 of 87 cases, the US examinations had already classified the lymph nodes as uninvolved (37 benign and 26 sfb), resulting in a specificity of 72% (95% CI: 62–81). The positive predictive value was 53% (95% CI: 38–67%), and the negative predictive values was 90% (95% CI:80–96%).


Figure 3
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  		FIG. 3. Comparison between the patterns of the in vivo and ex vivo SN. (Two cases, surgically confirmed).

 

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  		TABLE 2. Sensitivity and specificity of US and FNAC in combination
 
The results of in vivo cytology were found to be valuable, i.e. an adequate specimen could be obtained in 105 of the 121 nodes (Table 2Go). The remaining cytological smears were not valuable due to a limited number of cells or non-representative cells. Histology of the SN was negative in 73 of 105 cases (73 benign and 0 sfb), of which 73 had already been proven to be negative by the cytological analysis, thereby reflecting a specificity of 100% (95% CI: 95–100%) for in vivo cytology when an adequate specimen was obtained. Sensitivity was only 59% (95% CI: 41–76%) for in vivo cytology. Of the 32 SN found to be positive by histological evaluation (28 malignant and 4 sfm), 19 were also identified as being positive by in vivo cytology (FNAC). The positive predictive value was 100% (95% CI: 82–100%), and the negative predictive value was 85% (95% CI: 76–92%).

The combination of US and FNAC of in vivo SN correctly classified 28 of the 34 histologically proven malignant/sfm cases as being positive, thus achieving a sensitivity of 82% (95% CI: 65–93%) (Table 2Go). This combination of US and FNAC also correctly identified 63 of 87 histologically proven benign SN as not involved, reflecting a specificity of 72% (95% CI: 62–81%). The positive predictive value was 54% (95% CI: 39–68%), and the negative predictive value was 91% (95% CI: 82–97%).

By restricting our analysis to all histologically clearly malignant SN and taking all suspect US findings (sfb, sfm, and the malignant findings) together as one group, we would achieve a sensitivity of 100% (30 nodes; 95% CI: 88–100%) but only gain a worse specificity of 41% (37 of 90; 95% CI: 31–52%). Only one histologically sfm SN was classified as sonographically benign. We did not see bleeding or infection or any other adverse side effects from the FNAC, and the procedure was well tolerated by the patients. To date, we have not observed any spreading of tumor cells along the fine needle tract and have not found any recurrences related to the FNAC procedure. The median volume of SN in vivo was 842 mm3, while that of SN ex vivo was 714 mm3. Volume measurements of lymph nodes tend to be greater when taken in vivo because the surrounding fatty tissue is more often included in the measurement, thus artificially augmenting the numbers.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
To our knowledge, the study reported here is the first prospective study to include in vivo examinations of the SN in melanoma patients. Malignant melanoma of the skin primarily metastasizes to the regional lymph nodes.19 It is therefore important to have accurate tools for detecting relapse as early as possible. Once a lymph node is involved, the 5- or 10-year survival rate drops dramatically.2,20

It has been shown that the status of the SN after SLNB is the most important single prognostic factor.21

For physicians unfamiliar with ultrasound, it may be difficult to imagine that the SN could show a different sonographic-morphologic pattern, as was demonstrated in another study.14 During immunologic processes such as infection or peripheral tumor growth, a lymph node loses its inactive structure and proceeds to a reactive state. This transformation tends to be reversible as long as no neovascularization or (micro-) metastases exist within the node. The shape of the SN tends to be oval, and it lays down an echo-poor peripheral band, much like the pulp around the stone of a cherry. The hilum reveals increased echoes. An increase in blood perfusion throughout the whole node and partial hypervascularization within the periphery in the power mode may be identified, and should be taken signaling the location of a process in the parenchyma that is suspicious for a malignancy. A balloon-shaped parenchyma is always highly suspicious for malignancy, especially if it contains the above-mentioned local hyper-perfusion. The maximum asymmetrical cortex thickness, as shown in a recent breast cancer study,22 combined with irregular hypervascularization has turned out to be the most important feature for predicting sentinel node involvement. There is no correlation between size and assessment of malignancy of a lymph node.8

Due to the fact that melanoma cells are scattered in a disconnected fashion within the lymph node, these cells are best suited for the aspiration process, and an amazingly high specificity has been achieved so far. The specificity of FNAC is 100%, which indicates that the probability of producing false positive findings is nearly zero. False positive results were not produced, even when nests of nevus cells within the lymph node were found (in 9/141 excised SN).7,23–27 The relatively low sensitivity of FNAC can be explained by the small size of our targets, which sometimes measure only about 3 x 3 mm. Not only the entire sentinel but sometimes a small area within the node is the ‘region of interest.’ In order to be able to examine the cells within such small areas, we performed FNAC repeatedly.

In four cases histology revealed only a very small number of melanoma cells, or even just one melanoma cell. We documented these cases under the histologically positive sentinels, and the patients were scheduled for cLND.

US is very useful in treatment planning as it provides the surgeon with information about surrounding structures, blood vessels, and suspicious findings in additional lymph nodes. It is best if the surgeon schedules the US examination directly prior to SLNB as this will provide information on the in vivo conditions and the extent of agreement with the skin marking of the scintigraphy. If the SN reveals a positive cytology, the SLNB can be replaced by a LND, thus saving a surgical procedure as well as time.

US cannot and has never been intended to replace the established method of SN identification with a combination of lymphoscintigraphy and blue-dye mapping, since it is not able to achieve as high as sensitivity.28 Furthermore, it was not our intention to suggest replacing SLNB with FNAC. The important point we wish to make–based on the results of this study–is the potential of high-resolution US and FNA for identifying a subgroup of patients who do not need to undergo surgical SN biopsy but can instead undergo high-resolution US and fine needle aspiration. Our data only show that in a selected number of patients it is justified to proceed directly from FNAC to cLND. In our study, 16% (19/121) of the SLNB procedures could be omitted; these were immediately replaced by LNDs. At our institution (Charite, Berlin), US and FNAC are now performed as regular staging procedures before SLNB, and patients with positive FNAC directly undergo therapeutic LND. Using the gamma probe during in vivo US could be helpful and will be tested in further studies.


Figure 4
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  		FIG. 4. Typical patterns of the lymph node suspected to be an involved SN (two different cases, surgically confirmed). The nodes reveal asymmetrical broadening of the parenchyma, asymmetrical hypervascularization, and partial loss of the hilum.

 

   ACKNOWLEDGMENTS
 
Supported by Deutsche Krebshilfe (grant: 70-2791-Vo I).


   FOOTNOTES
 
Part of this work was presented in May 2003 at the Melanoma session of the 39th Annual Meeting of the American Society of Clinical Oncology in Chicago, Illinois, and at the Oral Melanoma Poster Discussion session of the 40th Annual Meeting of the American Society of Clinical Oncology in New Orleans, Louisiana.

Received for publication June 8, 2005. Accepted for publication January 23, 2006.


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TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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