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10.1245/s10434-006-9142-5
Annals of Surgical Oncology 13:1664-1670 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Sentinel Lymph Node Biopsy for Atypical Melanocytic Lesions with Spitzoid Features

T. Clark Gamblin, MD1,2,7, Howard Edington, MD1,3,4, John M. Kirkwood, MD5 and Uma N. M. Rao, MD6

1 Division of Surgical Oncology, Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
2 Division of Transplantation, Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
3 Division of Plastic Surgery, Department of Surgery, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
4 Division of Dermatology, Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
5 Divison of Hematology/Oncology, Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
6 Department of Pathology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
7 Liver Cancer Center, UPMC Montefiore Hospital, 3459 Fifth Avenue, 7 South, Pittsburgh, PA 15213, USA

Correspondence: Address correspondence and reprint requests to: T. Clark Gamblin, MD; E-mail: gamblintc{at}upmc.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Introduction: Sentinel lymph node biopsy (SLNB) is routinely used as a staging procedure for melanomas, however may also assist in understanding the biology of atypical and controversial spitzoid melanocytic skin lesions.

Methods: Five hundred and forty-nine sentinal lymph node excisions were performed over a 5-year period. Fourteen patients with controversial melanocytic lesions were identified and of these ten underwent SLNB. The histology of the primary skin lesion and corresponding sentinal lymph nodes were evaluated and correlated with outcome.

Results: Thickness of the primary melanocytic lesion ranged from 1.22 to 4 mm. Fifty percent of patients were less than 17 years of age. Ten patients underwent SLNB and three cases (30%) displayed metastatic disease in the SLNB specimen. All three patients were under 17 years of age and all underwent completion axillary dissection. One completion axillary dissection had an additional node with metastasis on routine H&E and immunohistochemical staining. No capsular invasion was seen. All three cases with metastatic disease received adjuvant systemic therapy and remain disease free at 29, 49 and 57 months follow-up. All patients with a negative SLNB remain disease free at mean follow-up of 28.1 months (range: 13–40 months).

Conclusion: Our results confirm that some of these spitzoid lesions metastasize to regional lymph nodes and SLNB is a valuable adjunct tool in staging these lesions. However, molecular studies and a prolonged follow-up are needed to determine whether these lesions, especially those occurring in children are comparable to stage matched overt melanoma in adults.

Key Words: Sentinel lymph node biopsy • Spitzoid lesion • Atypical skin lesion • Pediatric melanoma


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The clinical and pathological differentiation between benign Spitz nevus and the potentially fatal melanoma can be difficult. An error in diagnosis may lead to under-treatment with potentially catastrophic outcome. Several years ago we embarked upon an aggressive approach to the management of these enigmatic cutaneous lesions. We used sentinel node mapping and biopsy as both a staging and diagnostic adjunct. We present the results and rationale for this approach. We believe that identification and pathological examination of the sentinel node in patients having "spitzoid" lesions with atypia is reasonable and appropriate.

Sophie Spitz first reported a series of melanocytic lesions previously referred to as juvenile melanoma and noted the difficulties differentiating them from adult-type nodular malignant melanomas.1 These typically occur before puberty but may also occur in adults. Spitz nevus is however generally a lesion of childhood and highly unlikely in a patient >50 years of age.2–10 The typical benign Spitz nevus has characteristic histological features that in most instances are diagnostic, especially when they occur in children and are considered to have a benign course.11 Atypical variants of Spitz nevi and other atypical melanocytic lesions with uncertain biologic behavior may be almost impossible to distinguish from melanoma in the adult population.12–16

Many terms have been used to identify these diagnostically difficult melanocytic lesions and very often, these cases are reviewed by two or more pathologists with expertise in this area.12,17–26 The North America Melanoma Pathology Study Group reported considerable lack of consensus among pathologist diagnosing lesions termed "atypical Spitz tumors". Some lesions diagnosed as benign proved to be malignant with clinical follow up.3 In one study, a review of a group of atypical Spitz nevi/tumors that included cases of Spitz nevi/tumors that had metastasized, a panel of experts illustrated a lack of objective criteria for distinction of Spitz nevi from melanoma and their relationship to melanoma outside of semantics remained unresolved.12 Conflicting second opinions may results in confusion and anxiety for the patients as well as the physician, given the current "standard of care" management recommendation. Melanoma in children is rare and accounts for 1.3% of all cancers in patients less than 20 years of age and 7% of all cancers in ages between 15 and 19 years. Very often the diagnosis is made retrospectively after metastases have occurred.27

Lymph node assessment has become an important tool for staging cancer patients, particularly patients having melanoma or breast cancer. Routine pathologic staging of regional lymph nodes was not performed until the introduction of lymphatic mapping (LM) and sentinel lymph node biopsy (SLNB).28,29 Lymphatic mapping (LM) and sentinel lymph node biopsy (SLNB) have provided a method for early detection of metastatic disease through the lymphatic system with minimal morbidity.30–32 Although SLNB is typically used for staging, if metastases are detected, it can also provide information that would assist in the definitive diagnosis of a difficult primary lesion.33

In this study, we analyze the treatment and clinical outcome in a group of patients for whom the diagnosis of atypical melanocytic lesion/neoplasm of uncertain malignant potential/atypical Spitzoid lesions has been considered and will here refer to them collectively as controversial melanocytic neoplasms for discussion.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
After obtaining approval from the University of Pittsburgh Institutional Review Board, case records of patients having a diagnosis of atypical melanocytic lesions and those with atypical and spitzoid features that underwent sentinel node biopsy were retrieved from a database of the University of Pittsburgh Medical Center (UPMC). Clinical data and histopathologic material from primary lesions sentinel lymph nodes and completion lymphadenectomy specimens (when applicable) were retrospectively reviewed.

Clinical data obtained included patient age, gender, race, location of the primary lesion, number of sentinel nodes obtained, and site of lymphadenectomy. Histologic parameters of the primary lesion that were assessed included tumor thickness, Clark level of invasion, presence or absence of ulceration; mitotic rate, especially in the deeper portion of the lesion, presence or absence of maturation, pattern of growth of dermal melanocyte and atypical features such as prominent radial growth phase. All cases were reviewed by the pathologist (UNMR). About 50% of cases had been previously reviewed by more than one consultant when they were referred to this institute. Follow-up status, months to progression and systemic treatment administered were also obtained from the database. The procedure for LM and SLNB used in our institution is similar to that previously described in the literature by Morton et al.29 A combination of preoperative lymphoscintigraphy with unfiltered 99m TC-sulfur colloid and intraoperative lymphatic mapping using both a gamma detector and vital blue dye (Lymphazurin 1%; Hirsch Industuries, Richmond, VA, USA) was used to identify the SLN in all patients. The protocol for pathological evaluation of SLN at our institutions is essentially similar to that previously described with some modifications as follows.34,35 A maximum of two lymph nodes were designated as sentinal nodes according to blue dye uptake and increased counts of isotope. These were processed for the sentinal node protocol. Intraoperative frozen section evaluation is not recommended or pursued at this center, since small metastatic foci with few tumor cells are identified on permanent sections more accurately than on frozen sections. The size of the lymph node and presence or absence of blue dye is recorded, then the lymph node(s) are bisected, fixed in 10% buffered formalin, and processed in the routine fashion and paraffin blocks obtained. Eighteen serial sections are cut at 4 µm intervals levels 1, 4 and 6 are stained with routine hematoxylin and eosin stains and sections in between, are stained with standard immunohistochemical techniques with S100, HMB45, Melan A, tyrosinase and CD68 (DAKO, Carpentaria, CA, USA). A red chromogen is used instead of diaminobenzidine (DAB) to facilitate identification of pigment containing cells. CD68 was added to the panel to distinguish pigmented tumor cells from melanopeges. Level 17 was used for the negative control and appropriate positive controls were used for the individual antibodies. In some cases, if deemed necessary by the reviewing pathologist, additional sections were obtained for routine stains and immunohistochemistry. When there were more than two sentinel nodes from the same anatomical site, the additional nodes were bisected and entire node(s) were processed in the usual fashion, deeper levels and additional immunostains were obtained only if needed. Where as there is debate as to the exact number of serial sections to be examined from each sentinel lymph node, at UPMC, the sentinel lymph node protocol for melanoma cases is standardized, and a maximum of 20 sections are obtained for practical purposes and economic constraints. The surgically excised primary melanocytic lesion is fixed in formalin after the surgical margins are inked appropriately, and sectioned at 1 mm intervals with a sharp scalpel blade and the lesion is submitted entirely for pathological evaluation.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
We identified 14 patients from our database where the diagnosis varied from atypical melanocytic neoplasm, dermal melanocytic neoplasm compatible with atypical Spitz nevus, melanocytic neoplasm with marked dysplasia and atypical Spitz nevus. The probability of melanoma was raised in all cases. The majority of the cases had been reviewed by two pathologists and about one third had been reviewed by extramural consultants with expertise in melanocytic lesions. The histological quality of the sections was optimal in all cases. The lesions were noted to be dome shaped when the lesion had been removed in its entirety and on histological examination were found to be asymmetrical, meaning all had a junctional proliferation of atypical melanocytes in a lentigenous and nested fashion, beyond the dermal component. Pagetoid spread was also noted in the shoulder of the lesions (Fig. 1Go), and presence of maturation could not be determined with certainty in the cases that had superficial biopsies. The thickness of the melanocytic neoplasms ranged from 1.22 to 12 mm. Some had sectioning artifacts therefore the measured thickness was not accurate. Six lesions had a peripheral non-brisk lymphocytic infiltrate. At least one abnormal mitotic figure was found in the deeper part of the lesion. Proliferation marker Ki 67 was positive in five cases (≥ 15% of the dermal melanocytes). Some of these were again difficult to quantitate in the presence of lymphocytic infiltrates.


Figure 1
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  		FIG. 1. Primary lesion displaying features of Spitz nevus with epithelioid cells displaying prominent nucleoli (a) and an edematous papillary dermis and an area showing lack of maturation and a solitary mitotic figure (arrow) (b). Magnification: 20x.

 
The data was incomplete in three patients and in one case the slides were not reviewed at this institute. Of these three cases, none had tumor in their sentinel lymph node and are not included in Table 1Go due to missing data. Six patients were female, and eight patients were male. Their age at the time of diagnosis ranged from 7 to 47 years (mean age, 22 years). The lesions were predominantly in the extremities. Six patients were under 17 years of age, pediatric age range 7–17 years. Ten patients underwent sentinel node excision. Three patients had microscopic foci of metastatic melanoma in sentinel nodes on routine Hematoxylin and Eosin stains, confirmed by immunohistochemical stains, and subsequently underwent completion lymph node dissection (Fig. 2Go). In the completion dissection specimen, pathological examination revealed a total of 17, 22 and 47 lymph nodes, respectively. One of these patients was found to have an additional node with metastasis on completion dissection. The metastatic foci measured less than 5 mm in maximum diameter. They were both sub-capsular and parenchymal in location. None demonstrated extracapsular spread. Of these lymph node positive patients, one was 6 years old and the others were 10 and 11 years of age at diagnosis.


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  		TABLE 1. Patients with atypical melanocytic lesion with spitzoid features and sentinal node assessment
 

Figure 2
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  		FIG. 2. Hematoxylin and eosin stain (a) and S100 immunohistochemistry (b) of metastatic lymph node. Magnification: 20x.

 
Based on evidence of nodal disease all three patients received one month of high dose IFN therapy followed by eleven months of low dose IFN. At follow-up 29, 49 and 57 months all patients are alive with no evidence of disease. Patients were followed with clinical exam, CXR and blood work as we follow our routine melanoma patients. The remaining eleven patients remain without evidence of disease at routine follow-up (13–40 months, mean 28.1).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Spitz nevus is generally a lesion of childhood and highly unlikely in a patient >50 years of age. Spitz nevi and variants of other nevi can mimic melanoma and pose problems in histological diagnosis.36 Typically a Spitz nevus is a dome shaped non-ulcerated lesion, that histologically may be composed of spindle and epitheliod cells with distinct cell borders. The lesion may contain both junctional and dermal component, or may be either entirely junctional or intradermal.11 Mitosis can occur in superficial portions of the dermal component and this together with other cytological features such as prominent red nucleoli, can be mistaken for melanoma. However those that cause concern tend to display a prominent junctional melanocytic proliferation beyond the dermal component (i.e. shoulder). They can be deep and predominantly epitheliod. There are no consistent immunohistochemical staining characteristics with S100, HMB45 or other markers that distinguish these lesions from melanoma. A low proliferative index determined by immunostaining with Ki 67 can be seen in both Spitz nevi and some melanoma. There is agreement amongst most pathologists that lack of maturation and abnormal mitosis in deeper portions of the lesion favors a diagnosis of melanoma. Some ancillary molecular techniques like comparative genomic hybridization have demonstrated copy number changes of chromosome 11 that are thought to be specific for Spitz nevi. However such techniques are not widely available, and routine histological evaluation still remains the gold standard.37

The diagnostic problems of these lesions are compounded in children because melanoma is uncommon in this age group, and very often the diagnosis is made in retrospect after development of regional lymph node metastases.38 In our cases, the diagnosis of atypical melanocytic neoplasm was made with great caution and after deliberation with other pathologists and surgical colleagues about the feasibility of reexcision and sentinel node mapping. The diagnostic uncertainty as well as management options should be clearly discussed with all patients and their family, especially the younger patients. As seen from our own experience, although melanoma is rare in children, it does occur and aggressive treatment is warranted.

We agree with Kelley et al.33 that in select patients, SLNB is a useful adjunct in the management of histologically difficult melanocytic lesions because the status of the regional lymph node basin is the most powerful predictor of survival for patient with melanoma. The SLNB technique allows one to assess the regional basin with minimal morbidity. Historically the SLN technique has been a staging tool, however with these challenging lesions the technique may assist with the diagnosis of the primary lesion. The concept of "benign metastases" should be revisited, and a location of such cellular elements in portions of the parenchyma of the node apart from the capsule adds concern.39–41 Benign nevus cells in the lymph node capsule can be mistaken for metastatic melanoma especially when they occur within fibrous septae of the capsule, however they are distinct from the metastasis that are found in the subcapsular sinus.42 In our cases, the metastatic foci clearly resembled the primary lesions, were present in the lymph node parenchyma and subcapsular sinus which are the expected sites of metastases. Further molecular studies are needed to determine whether the metastases derived from controversial lesions are distinct from the usual type of cutaneous melanoma in order to justify a separate prognostic category for these patients.

Attempting to use a published grading system to predict behavior of atypical spitzoid melanocytic tumor, we found none of the previously described parameters such as presence of mitotic figures, maturation, or pleomorphism individually correlated with lymphatic metastasis.43 Thickness of the primary lesion appeared to correlated but the number of cases reported are too few for statistical significance.

Patients with positive SLNB may be treated as a melanoma with adjuvant interventions such as interferon however some treating physicians may choose a "watch and wait" approach especially in the pediatric population. Although a negative SLNB does not exclude the diagnosis of melanoma, one can reassure the patient that appropriate staging and management has been performed. Patients with an atypical melanocytic lesion should undergo close surveillance.

The frequency of sentinel node metastasis observed in our study (30%) is less than previously reported in two other series.44,45 Melanomas that range 2–4 mm in thickness are estimated to have occult metastasis in 40–50% of cases. In summary, the pathological and clinical diagnosis in patients having atypical melanocytic lesions with spitzoid features is challenging and controversial especially in the pediatric age group. Acquired melanocytic lesions, especially those categorized as severely atypical spitzoid lesions, pose a diagnostic and therapeutic dilemma. In this group of patients, sentinel node mapping and biopsy should be considered for both staging and diagnostic purposes. Understanding the biologic nature of these atypical melanocytic lesions will require long-term surveillance of patients and use of evolving molecular techniques. Primary cutaneous lesions with metastasis to the SLN should be considered as melanoma and treated accordingly.


Figure 3
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  		FIG. 3. Photomicrograph of metastatic foci in sentinel lymph node displaying pigment. Magnification: 20x.

 

Figure 4
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  		FIG. 4. Photomicrograph of additional case with S100 positive spindle cells in the lymph node parenchyma; hematoxylin and eosin (a) and immunohistochemical for S100 (b). Magnification: 20x.

 

   ACKNOWLEDGMENTS
 
Special thanks to Hiedi Gianella for providing assistance as an Honest Broker.

Received for publication December 9, 2005. Accepted for publication April 3, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Sentinel Lymph Node Biopsy in Histologically Ambiguous Melanocytic Tumors With Spitzoid Features (So-Called Atypical Spitzoid Tumors)
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