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Sentinel Node Biopsy for High-Risk Nonmelanoma Cutaneous Malignancy
Jeffrey D. Wagner, MD;
David Z. Evdokimow, MD;
Edward Weisberger;
David Moore, MD;
Tsu-Yi Chuang, MD, MPH;
Stacie Wenck, RNP;
John J. Coleman III, MD
Arch Dermatol. 2004;140:75-79.
ABSTRACT
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Objective To evaluate the feasibility of sentinel node staging for detection of occult regional lymph node metastasis in high-risk cutaneous nonmelanoma malignancies.
Design Consecutive clinical case series.
Setting Referral university medical center.
Patients A consecutive sample of patients with a variety of high-risk nonmelanoma cutaneous malignancies without evidence of regional lymph node metastases.
Intervention Sentinel node biopsies were performed using preoperative lymphoscintigraphy, blue dye, and intraoperative radiolocalization.
Main Outcome Measure Sensitivity, determined by comparing the results of biopsy specimen evaluation with those of completion lymphadenectomy and/or clinical follow-up.
Results Twenty-four patients underwent sentinel node biopsy for the staging of 29 nodal basins identified by lymphoscintigraphy. Primary diagnoses were squamous cell carcinoma (n = 17), Merkel cell carcinoma (n = 5), and adenocarcinoma (n = 2). Seven patients (29%) had a tumor-positive sentinel node. Sentinel node biopsy followed by complete lymphadenectomy was performed in 12 patients and sentinel node biopsy alone in 12 patients. Tumor-positive lymph nodes were noted in 8 patients, 7 of whom also had positive sentinel nodes. There was 1 false-positive result (1/8 [12%]), in a patient with recurrent squamous cell carcinoma of the scalp. At a median follow-up of 10 months, no recurrences in a sentinel node–negative basin have been noted. Compared with all information, the sensitivity of sentinel node staging was 88% and the negative predictive value was 0.94.
Conclusions Sentinel node biopsy is a minimally invasive staging procedure useful in identifying occult regional lymph node disease in selected patients with nonmelanoma cutaneous malignancies. Further studies to verify these findings and develop formal guidelines are indicated.
INTRODUCTION
The presence of regional lymph node metastasis is the most powerful prognostic factor for predicting recurrence and survival in patients with most solid tumors. Identification of patients with occult metastasis is vitally important for staging and treatment planning. Lymphatic mapping and sentinel node biopsy have become the standard of care for melanoma at most major melanoma centers and university melanoma programs.1-3
There is currently no adequate noninvasive means for detection of occult metastases in regional nodes in most malignancies.4 The trend toward less invasive surgical methods to stage regional lymph nodes has led to the gradual replacement of radical lymph node dissection procedures by limited, selective procedures. The rationale for less invasive staging procedures is that they can provide prognostic information pertinent to treatment planning and therefore lower morbidity and cost. Sentinel node biopsy, the most recent chapter of this minimally invasive revolution, has increasingly become the staging procedure of choice for patients with clinically node-negative breast cancer.5-6 Several reports on sentinel node staging for squamous cell malignancy of the male and female genitalia7-8 and Merkel cell carcinoma9-11 suggest that lymphatic mapping and sentinel lymph node biopsy may be used for a variety of nonmelanoma cutaneous malignancies.
We postulated that the stepwise progression of early lymphatic metastases might occur in certain nonmelanoma cutaneous malignancies with a high risk of nodal metastases. The false-negative rate of histologic sentinel node evaluation in this population is unknown. The objective of this study was to investigate the feasibility of sentinel node biopsy in selected high-risk skin cancers by determining the false-negative rate and sensitivity of this procedure for detection of occult regional lymph node metastases.
METHODS
We reviewed our cumulative experience with sentinel node staging in nonmelanoma cutaneous malignancies in a consecutive series of clinically node-negative patients who underwent this procedure between 1997 and 2002. The study protocol was reviewed and approved by the institutional review board of Indiana University–Purdue University and all patients signed informed consent to participate in the study. The 6 inclusion criteria were primary squamous cell carcinoma (SCC) at least 4 cm in diameter or invasive of deep connective, skeletal, or muscular structures; locally recurrent SCC; SCC at least 1 cm in diameter on the genitalia; SCC at least 2 cm in diameter in immunosuppressed patients; Merkel cell carcinoma; and primary cutaneous adenocarcinoma. The 3 exclusion criteria were lymph node metastases or adenopathy; prior wide excision greater than 2 cm or lymphatic surgery; and if the patient was pregnant or breastfeeding. There were 2 groups of patients (Figure 1). Group 1 consisted of 9 patients who participated in a prospective nonrandomized clinical pilot study designed to test the preliminary feasibility of sentinel node staging in selected high-risk cutaneous malignancies. Group 1 patients underwent sentinel node biopsy, followed by complete lymphadenectomy for all basins identified by lymphoscintigraphy.
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Study schema. SNB indicates sentinel node biopsy; LND, complete lymphadenectomy.
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Group 2 consisted of a consecutive series of 15 patients to whom the sentinel node procedure was offered as a clinical adjunct or an alternative to staging lymph node dissection because they had high-risk cutaneous malignancies. All patients in this group also had clinically negative, ie, nonpalpable regional lymph nodes. Patient and tumor characteristics were similar in group 1 and group 2. Sentinel node–positive patients in group 2 were offered complete lymphadenectomy or definitive radiation therapy. Sentinel node–negative patients were followed up clinically without further therapy or underwent complete planned lymphadenectomy after harvesting of the sentinel node or nodes.
All patients underwent preoperative dermatolymphoscintigraphy 1 to 2 hours prior to surgery with unfiltered technetium Tc 99m-labeled sulfur colloid injected intradermally at several points around the tumor or biopsy scar. Imaging was performed for up to 2 hours using a gamma camera with a wide field of view to identify focal accumulations of tracer in regional lymph node basins. Intraoperative radiolocalization was performed with a handheld Neoprobe (Neoprobe Corporation, Dublin, Ohio) or C-track (Care Wise Medical Products, Morgan Hill, Calif) gamma probe detector. The radiolocalization was combined with intradermal injection of 1 to 2 mL of isosulfan blue to aid in visual localization of the sentinel nodes.
All basins identified by lymphoscintigraphy were explored through limited incisions directed by the gamma probe and skin markings. The primary criterion for sentinel node status was blue coloration. All blue nodes were identified and removed as sentinel nodes. Ex vivo sentinel node to residual lymph node basin radioactivity ratios were determined after removal of the blue nodes. If this ratio was at least 10:1, the procedure was terminated. If the ratio was less than 10:1, the gamma probe was used to identify and remove additional radioactive lymph nodes until the ratio was at least 10:1.
The sentinel nodes were step sectioned at 1-mm intervals and analyzed by light microscopy using hematoxylin-eosin stain. Any lymph node with at least 1 positive section was counted as positive for metastasis. All nonsentinel nodes were sent for standard histologic analysis.
The sensitivity of the procedure was determined by comparing the incidence of micrometastasis in the sentinel node with the histologic findings of the complete lymphadenectomy in 12 patients. The 12 patients who underwent sentinel lymph node biopsy as the sole procedure had a follow-up physical examination of the residual basins in which biopsies were performed.
RESULTS
Characteristics of the study population are shown in Table 1. Twenty-four patients (15 men and 9 women; mean age, 61.4 years [range, 32-93 years]) underwent lymphatic mapping and sentinel node biopsy. The histologic diagnoses were squamous cell carcinoma (n = 17), Merkel cell carcinoma (n = 5), and adenocarcinoma (n = 2). Tumor locations were the head/neck (n = 6), extremities (n = 11), trunk (n = 1), and genitalia (n = 6). Twenty-nine lymph node basins were identified by lymphoscintigraphy and staged by sentinel node biopsy, and 55 sentinel nodes were removed (mean number of sentinel nodes per basin, 1.9 [range, 1-4]).
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Table 1. Patient and Tumor Characteristics
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Seven of 24 patients had at least 1 tumor-positive sentinel node (29%). Sentinel node biopsy findings by tumor type are shown in Table 2. Twelve patients had completion lymphadenectomy to remove all nodes in the basin where a biopsy was performed. Additional tumor-containing nonsentinel lymph nodes were noted in 3 (43%) of the 7 sentinel node–positive patients. One sentinel node–negative patient had a positive nonsentinel lymph node in a lymphadenectomy specimen. This false-negative sentinel node biopsy finding occurred in patient 9 (Table 1) who had locally recurrent squamous cell carcinoma of the scalp and had undergone prior resection and radiation.
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Table 2. Sentinel Node Biopsy Findings by Tumor Type
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Sentinel lymph node biopsy without complete lymphadenectomy was performed in 12 patients. Biopsy findings revealed positive sentinel nodes in the cervical lymph nodes of 2 (17%) of these patients who were then offered radiation therapy. The median clinical follow-up for 10 sentinel node–negative patients was 11 months (range, 4-41 months). No nodal recurrences were noted in any sentinel node–negative basin. Compared with all clinical information, the sensitivity of the sentinel node procedure was 88% (7/8), its specificity was 100% (16/16), its positive predictive value was 1.0 (7/7), and its negative predictive value was 0.94 (16/17).
COMMENT
Nonmelanoma skin cancer is the leading cause of cancer in the United States, with more than 1 million new cases diagnosed annually.12-16 Basal cell carcinoma, which very rarely metastasizes, accounts for most nonmelanoma cutaneous carcinomas17 while SCC, which accounts for about 20% of nonmelanoma cutaneous carcinomas, is increasing in incidence.13-16,18 Approximately 80% of initial treatment failures in cutaneous SCC occur in regional lymph nodes.19-20 The overall incidence of regional nodal metastases is relatively low (only about 0.5%) in all cutaneous SCCs, but the presence of metastasis carries a poor prognosis.19-20 Merkel cell carcinoma and primary cutaneous adenocarcinomas are uncommon skin malignancies, with a relatively poor prognosis and a significant chance of regional node metastases.9-11,21 The 5-year survival rate for stage III disease is approximately 25% to 35%, depending on histologic findings and tumor burden.19-22
The optimal approach to occult nodal metastases in patients with high-risk cutaneous nonmelanoma malignancies has not been standardized by prospective randomized clinical trials. Elective surgical lymphadenectomy or nodal irradiation are frequently considered in the treatment planning for these malignancies. Nodal staging may contribute prognostic information useful in preventing unnecessary surgery or other therapies.
The present study demonstrates the usefulness of sentinel node biopsy for the staging of clinically node-negative patients with several high-risk skin malignancies. These results parallel our larger experience with treatment of melanoma23 and suggest a clinical role for minimally invasive staging in selected nonmelanoma cutaneous malignancies. The study's small size and limited follow-up time preclude definitive conclusions regarding the sensitivity and false-negative rates to be expected from the procedure. Nonetheless, it appears reasonable to offer the procedure to selected patients as an alternative to observation or to elective complete lymphadenectomy.
The false-negative rate in this series was 12%, which is considerably higher than rates reported for large series of patients with melanoma.23 It is likely due to the small size of this series, and would likely be lower with larger numbers and more precise patient selection for the procedure. The patient with the false-negative result of sentinel node biopsy had a relatively large recurrent scalp SCC after excision and radiation therapy. Lymphatic mapping is known to be somewhat less reliable when the normal lymphatic drainage has been altered, eg, after previous wide excisions, flap reconstruction, and lymphadenectomy. The effect of radiation on the reliability of lymphatic mapping is not known, but is likely similar. And although sentinel node biopsy is generally accepted in the management of melanomas in the head and neck region, it is more difficult owing to complex lymphatic drainage patterns. These factors may have contributed to the single false-negative observation.
Because of the rarity of high-risk nonmelanoma cutaneous tumors, experience with sentinel node biopsy is limited and large clinical trials may not be feasible. Lymphatic mapping has been investigated in SCC of the vulva. Early experiences using only blue dye showed a relatively low sensitivity,24 but more recent reports using the combined techniques of blue dye and radiolocalization have been highly accurate in establishing the pathological status of the inguinofemoral node.8 Good results have also been achieved in the staging of early penile cancer.7 There are several reports of successful sentinel node biopsy for Merkel cell carcinoma and the procedure seems to be applicable to this rare malignancy.9-11 Early reports suggest that sentinel node biopsy may have an emerging role for staging of head and neck mucosal cancer.25-26
To date, only very small or anecdotal reports of sentinel node staging for cutaneous SCC exist.27-28 The frequency of regional nodal metastases varies with anatomic site, histologic features such as increasing tumor thickness and histologic dedifferentiation, tumor size, host immune competency, perineural invasion, and prior treatment.19, 28-35 Squamous cell tumors arising in nonglabrous mucocutaneous sites such as the lip, vulva, penis, and perianal area are also more likely to metastasize than those involving other areas of the skin.29 Squamous cell carcinoma arising in areas of chronic inflammation, nonhealing wounds, chronic osteomyelitis, and in irradiated fields are known to be particularly aggressive, with rates of nodal metastases between 18% and 30%.31-34 Immunosuppressed patients also have a higher incidence of nonmelanoma skin cancer metastases. The presence of perineural infiltration is another recognized determinant of metastatic potential.22, 34
Based on this series and the prognostic factors in the literature, it is possible to formulate rational recommendations for nodal staging in patients with nonmelanoma cutaneous malignancies. Sentinel node biopsy should be considered in all patients with Merkel cell carcinoma clinically localized to the skin. We also advocate considering sentinel node staging for cutaneous SCC in patients with a primary tumor greater than 2 cm in diameter, any tumor invasive of underlying skeletal structures, and any SCC in a chronic wound, with perineural invasion, or a thickness greater than 4 mm. Squamous cell carcinomas that are less than 2 cm in diameter that are poorly differentiated, develop on the genitalia, recur after therapy, and develop in immunocompromised patients may also be considered for nodal staging with sentinel node biopsy. The rarity and clinical diversity of primary cutaneous adenocarcinomas and the small size of this series prevent any meaningful conclusions. However, sebaceous carcinomas, malignancies of eccrine origin, and extramammary Paget disease have the potential to metastasize to regional lymph nodes and may be considered for sentinel node staging. These preliminary recommendations are empiric and await confirmation in larger numbers of patients.
Sentinel node biopsy has the potential to improve the clinical management of selected patients with nonmelanoma cutaneous malignancies. Sentinel node staging theoretically could spare node-negative patients the morbidity of complete lymphadenectomy—or empiric radiotherapy. Because observation of clinically negative regional lymph nodes is an accepted management option, patients without disease in sentinel nodes could be selected for close monitoring without further therapy. Conversely, patients with micrometastatic disease in lymph nodes could be appropriately treated with lymphadenectomy or radiation therapy. Finally, more accurate staging information permits more precise design and analysis of clinical trial results.
In conclusion, minimally invasive staging of clinically node-negative regional lymphatic basins with sentinel node biopsy is applicable to a variety of nonmelanoma cutaneous malignancies. Further studies are indicated to verify these findings and refine guidelines for sentinel node staging in nonmelanoma skin malignancies.
AUTHOR INFORMATION
Corresponding author: Jeffrey D. Wagner, MD, RT 471, 535 Barnhill Dr, Indianapolis, IN 46202 (e-mail: jdwagner{at}iupui.edu).
Accepted for publication September 24, 2003.
From the Division of Plastic Surgery, Department of Surgery (Drs Wagner, Evdokimow, and Coleman, and Ms Wenck), and the Departments of Otolaryngology/Head and Neck Surgery (Mr Weisberger), Gynecology and Oncology (Dr Moore), and Dermatology (Dr Chuang), Indiana University School of Medicine, Indianapolis. The authors have no relevant financial interest in this article.
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