Superficial Spreading Malignant Melanoma with Neurosarcomatous Metastasis
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1 Vol. 82 No. 1 CASE REPORT Haynes BF, Metzgar RS, Minna JD, Bunn PA: Phenotypic characterization of cutaneous T-cell lymphoma use of monoclonal antibodies to compare with other malignant T-cells. N Engl J Med 1981; 304: Haynes BF, Hensley LL, Jegasothy BV: Phenotypic characterization of skin-infiltrating T cells in cutaneous T-cell lymphoma: Comparison with benign cutaneous T-cell infiltrates. Blood 1982; 60: Holden CA, Morgan EW, MacDonald DM: The cell population in the cutaneous infiltrate of mycosis fungoides: In situ studies using monoclonal antiserum. Br J Dermatol 1982; 106: Hopper JE, Haren JM: Studies on a Sezary lymphocyte population with T-suppressor activity suppression of Ig synthesis of normal peripheral blood lymphocytes. Clin Immunol Immunopathol 1980; 17: Jensen JR, Thestrup-Pedersen K: Subpopulations of T lymphocytes in a patient with fulminant mycosis fungoides. Acta Derm Venerolo (Stockh) 1980; 60: Kansu E, Hauptman SP: Suppressor cell population in Sezary syndrome. Clin Immunol Immunopathol 1979; 12: Kung PC, Berger CL, Goldstein G, LoGerfo P, Edelson RL: Cutaneous T-cell lymphoma: Characterization by monoclonal antibodies. Blood 1981; 57: Lennert K: Malignant lymphomas other than Hodgkin's diseasehistology, cytology, ultrastructure and immunology. New York, Springer-Verlag, 1978, pp Long JC, Mihm MC: Mycosis fungoides with extracutaneous dissemination: A distinct clinicopathologic entity. Cancer 1974; 34: Lutzner M, Edelson R, Schein P, Green I, Kirkpatrick C, Ahmed A: Cutaneous T-cell lymphomas: The Sezary syndrome, mycosis fungoides and related disorders. Ann Intern Med 1975; 83: Rappaport H, Thomas TB: Mycosis fungoides: The pathology of extracutaneous involvement. Cancer 1974; 34: Schmitt D, Souteyrand P, Brochier J, Czernielewski J, Thivolet J: Phenotype of cells involved in mycosis fungoides and Sezary syndrome (blood and skin lesions): Immunomorphological study with monoclonal antibodies. Acta Derm Venerolo (Stockh) 1982; 62: Superficial Spreading Malignant Melanoma with Neurosarcomatous Metastasis DAVID J. DABBS, M.D. AND JOHN W. BOLEN, M.D. Metastatic malignant melanoma often poses a difficult light and ultrastructural diagnostic challenge. A superficial spreading malignant melanoma without desmoplasia displayed neurosarcomatous light and electron microscopic features in metastatic sites. The ultrastructure displayed some Schwann cell features and strong-s-100 immunostaining. Metastatic melanoma with Schwannian differentiation in metastatic sites without lesional desmoplasia is rare and must be included in the differential diagnosis of spindled neoplasms involving lymph nodes. The evolution of this lesion illustrates the spectrum of melanocytic differentiation, i.e., pigment synthesis, adaptive fibroplasia and Schwannian differentiation. (Key words: Superficial spreading melanoma; Neurosarcomatous; S-100 protein; ABC immunoperoxidase) Am J Clin Pathol 1984; 82: THE HISTOLOGIC APPEARANCE of metastatic malignant melanoma exhibits such a wide spectrum that one often is confronted with excluding such a lesion as part of a differential diagnostic study. The desmoplastic variants of malignant melanoma require special recognition, for they present as a spindled cell component in association with the superficial spreading melanoma or lentigo melanoma, sometimes with neuroid qualities. The histogenesis of the spindled component and the spectrum of neuroid patterns recently have been subjects of debate, Received August 25, 1983; received revised manuscript and accepted for publication December 28, Addressreprintrequests to Dr. Dabbs: Pitt County Memorial Hospital, Department of Clinical Pathology and Diagnostic Medicine, Greenville, North Carolina Department of Pathology, University of Washington, Seattle, Washington with most authors favoring a transformed melanocyte, with sheath-forming properties, to account for the desmoplasia seen in these lesions. Reported here is the evolution of a superficial spreading malignant melanoma arising in a dermal nevus, the metastasis of which displayed predominant neurosarcomatous features. Report of a Case A 33-year-old white man presented to University Hospital for evaluation of arightgroin mass. The patient had figuration of a wart from his right anterior thigh in Subsequently, a flat thickened lesion appeared at the same site and began to increase in size in 1977, which bled on minor trauma, with healing. In December 1978, the lesion was excised and interpreted as malignant melanoma, Clark level III, arising in an intradermal nevus. Widere-excisionfailed to reveal residual tumor. In January 1980, a right superficial inguinal node dissection was performed, yielding four lymph nodes positive for metastasis. The patient was asymptomatic until December 1981, when a mass was excised from the iliac fossa, superior and contiguous to the previous surgery. Materials and Methods The initial thigh lesion, re-excision specimen and superficial inguinal node dissection were performed elsewhere and were reviewed in consultation. Tissue from
2 DABBS AND BOLEN A.J.C.P. July 1984 FIG. 1. A (upper). Pagetoid pattern of superficial spreading melanoma. B (inset). Cytology of melanoma cells in original thigh lesion. C (lower). Sample of associated intradermal nevus. Hematoxylin and eoxin (A, XlOO; B, X400, C, X250).
3 CASE REPORT Vol. 82 No The first superficial inguinal node dissection included four lymph nodes, infiltrated by a population of gently curved fascicles of small bland cells, insinuating throughout the lymph sinuses and extensively permeating the perinodal connective tissues (Fig. 2). The nuclei of spindle cells were oval without atypia or mitosis, and cellular borders were indistinct. Focally within the node were collections of epithelioid and dendritic cells, the cytoplasms of which were packed with Fontana-positive, finely granular, golden-brown granules. Some of these cells also assumed the spindled configuration and merged with nonpigment-containing spindled cells. Reticulin stains highlighted individual reticulin fibers about spindle cells. The third operation yielded a 4.0 X 3.0 X 1.5 cm gritty, firm, unencapsulated, grayish-white mass, which centrally contained residual lymph node. Light microscopy was virtually identical to the previous lymph node dissection. Ultrastructural examination revealed elongate cells with numerous cell processes, which were, in part, invested by basal lamina (Fig. 3). There was some tendency for the cells to form nests, but well-formed cell junctions were not identified. Nuclei exhibited irregular contours with finely dispersed chromatin and inconspicuous, compact nucleoli. Cytoplasms contained small amounts of rough the iliac fossa was fixed in Millonig's buffered formalin for light and electron microscopy. For electron microscopy, tissue was postfixed in osmium tetroxide, cut at 60 to 90 nm, and stained with uranyl acetate and lead citrate. Antibody to S-100 protein was obtained from Dako Co. Formalin-fixed sections were deparaffinized and rehydrated and then overlaid with antibodies to S-100 antibody in a 1:600 dilution. The ABC-immunoperoxidase system then was employed.10 Results The thigh lesion (Fig. 1) was composed of regions exhibiting an intradermal nevocytic nevus. This component exhibited bland nevus cells in theques and cords extending into reticular dermis without cytologic atypia, mitosis, or prominent pigmentation. Adjacentfieldsrevealed considerable cytologic atypia of nevus cells with prominent nucleoli, enlarged irregular nuclei, and prominent patchy pigmentation throughout cords and theques. Host response was not present, and upward extension at the epidermis was evident. The melanoma component was classified Clark level III, 1.5 mm. Serial sections failed to reveal any lesional desmoplasia. w& &; *; ^L*% - v. V - Bt'.T-ft '-'' a??'\. * ' >., *;'.-' *» atr*',.-- ** f. >:..» - * t - v.'i» v *<*. v " --,Mn *tk ' "L & --.TV. ^- Safe ^yuz^ FIG. 2 A. Perinodal and intranodal spindle tumor. B (inset). Intranodal deposit of pigment bearing epithelioid cells. Hematoxylin and eosin (A, X100; B, X400).
4 112 A.J.C.P. July 1984 DABBS AND BOLEN»** '"^^L f^^'^ FIG. 3. Tumor cells in connective tissue space display features of mesenchymal cells with segments of external lamina (arrows). Note elongate cell processes in cross section (X28.080). endoplasmic reticulum, small Golgi complexes, and few mitochondria. Peripheral dense bodies were not seen, and careful examination for premelanosomes was negative. Immunoperoxidase methods (Fig. 4) revealed strong positive uniform cellular reactions for S-100 protein in the tumor cells. Discussion It generally is accepted that Schwann cells and melanocytes are derived from related precursors as neural crest derivatives.924 Abundant morphologic evidence exists that illustrate the overlapping spectrum of differentiation among melanocytic and Schwannian lines. Such cases include the melanotic Schwannoma, pigmented neurofibroma, dermatofibrosarcoma protuberans, desmoplastic malignant melanoma, and the common cutaneous nevi, in which progressive dermal "neurotization" is the normal sequence of lesional maturation. Each of these lesions presents distinct light microscopic appearances and, often, characteristic electron microscopic appearances. Melanotic Schwannomas 1516 display cytoarchitectural features of Schwann cells and contain melanosomes, while Bednars group of neurofibromas illustrated typical patterns of neurofibromas, yet had tumor cells with melanin pigment.2 Histogenetic studies by Hashimoto, 8 Smith, 19 and Alguacil-Garcia1 suggest a modified fibroblastic cell with sheath-forming abilities, simulating perineural cells as the characteristic cell of dermatofibrosarcoma protuberans. In the dermatofibrosarcoma protruberans spectrum, Smith identified tumor melanosomes, while Alguacil-Garcia found dendritic melanocytes containing melanosomes among the tumor cell population. The desmoplastic malignant melanoma initially described by Conley and associates4 usually presents as a clinically innocuous pigmented lesion, often associated
5 Vol. 82 No. I CASE REPORT 113 FlG. 4. A (left). Spindled neurosarcomatous pattern in perinodal soft tissue. B (center). S-100 protein immunoperoxidase result with neurosarcoma pattern. C (right). Low magnification S-100 protein reveals mode of nodal tissue penetration. Hematoxylin and eosin (A, X160). Immunoperoxidase, methyl green counterstain (B, XI60, and C, X64). with an underlying ill-defined mass and has a considerable tendency for local recurrence as well as widespread metastasis. In most series including Conley's, the histopathology of the lesions consisted usually of lentigo malignant melanoma or superficial spreading malignant melanoma. The dermis in such lesions revealed marked stromal desmoplasia with ill-defined populations of spindled cells diffusely infiltrating the stroma and adnexal structures, including nerves, in a fibromatosis-like fashion. The spindle cells typically revealed long attenuated hyperchromatic nuclei without conspicuous mitoses, cell borders, or areas of necrosis. Electron microscopic studies performed by Conley indicated that the spindle cells infiltrated perineural spaces, and he described a solitary melanosome in a tumor cell. Valensi21 viewed the desmoplastic condition as dedifferentiated malignant melanoma cells, exhibiting macular desmosomes, dilated endoplasmic reticulum, and an overall fibroblast-like structure, without interdigitating cell processes, melanosomes, or basal lamina. He previously had suggested that the finding of a lymph node metastasis of the desmoplastic variant bearing pigmented spindled cells would resolve the dilemma of whether they were differentiated melanoma cells or were merely a peculiar local fibroblastic response to invasive melanoma cells, as Labrecque'2 suggested. Frolow6 and others reported a case of desmoplastic malignant melanoma with regional metastasis eliciting an amelanotic spindled tumor, but electron microscopy was not performed. Reed and Leonard18 Warner and associates22 reported a series of desmoplastic melanoma, subclassified as "neurotropic," since the predominant growth pattern was of traumatic neuroma-like quality. Like the lesions described by Conley, the majority were associated with a superficial melanocyte lesion with some arising de novo in the lip. Clinically, the lesions were identical to Conley's series and did not reveal the neuroma-like growth pattern in metastatic sites but did show the desmoplastic and usual epithelioid patterns. Unlike Conley's lesions, the neurotropic lesions were composed of gently curved fascicles of spindled cells with pale cytoplasm and oval nuclei, with neuroma-like fascicles separated by a fibrous matrix. Preliminary electron microscopic studies described by Reed suggested Schwann cell characteristics of the neurotropic variant. It appears that the major difference between a neurotropic melanoma and a desmoplastic melanoma is essentially qualitative in terms of the prominence of the "neuroma-like" growth patterns. One other difference is the de nov lip lesions in Reed series, in which the lesions may in fact represent malignant neuroma. The diagnostic difficulty in this case became apparent when, upon review of the original melanoma excision, no spindled or desmoplastic component could be found even on serial sectioning. In fact, the evolution of this lesion strikingly displays the histogenetic links alluded to by Valensi, by exhibiting a superficial malignant melanoma arising in an intradermal nevus, with Schwannian and pigmented epithelioid differentiation in metastatic sites. Only one case of neurosarcomatous metastatic melanoma without lesional desmoplasia, described by DiMaio and associates5 has been reported, although spindled and neurosarcomatous features are well described for metastatic melanoma.13,23'25 One must be aware of the patient with the clinical history of melanoma and be careful to
6 114 DABBS AND BOLEN A.J.C.P. July 1984 exclude lesions such as malignant nerve sheath tumors, 37 ' 20 melanocyte Schwannoma, nevus cell inclusions in lymph nodes, 14 cellular Schwannoma, neurofibroma, spindled carcinoma, and fibromatosis when confronted with melanotic neuroid lesions in unusual sites such as lymph nodes. It is unlikely that the lesions in this patient represented de novo Schwannian lesions in the lymph node, as the lesions were multiple, contiguous, and in the lymphatic drainage sector of a previously excised melanoma. Immunohistochemical study with the S-100 protein, in the context of a well-studied conventional histologic section and electron microscopy, is extremely valuable in the evaluation of neural crest derived neoplasms, 117 as ultrastructure alone offers no specific features for neurosarcomatous lesions. S-100 staining tends to be correlated inversely with the tumor content of melanin for melanoma, while there tends to be a decline in staining with decreasing differentiation in nerve sheath tumors. The intensity of S-100 staining in this case is more suggestive of origin from melanoma. From these observations and those of others, it is clear that one should anticipate the spectrum of pigment synthesis, collagen synthesis, and Schwannian differentiation in the desmoplastic patterns of malignant melanoma. These may vary from deceptively infiltrating hyperchromatic spindled cells in primary lesions, through the spectrum of neuroma-like patterns to isolated metastasis showing frank Schwannian features without primary lesional desmoplasia. Histogenetically, one may draw a parallel relationship between the normal sequence of intradermal nevus saturation ("neurotization") and the variable recapitulation of this process observed in the malignant counterparts. References 1. Alguacil-Garcia A, Uiani K, Goellner J: Histogenesis of dermatofibrosarcoma protuberans, An ultrastructural study. Am J Clin Pathol 1978; 69: Bednar B: Storiform neurofibroma of the skin, Pigmented and nonpigmented. Cancer 1957; 10: Chen K, Latorraca R, Fabich D, et al: Malignant schwannoma, A light microscopic and ultrastructural study. Cancer 1980; 45: Conley J, Lattes R, Orr W: Desmoplastic malignant melanoma, A rare variant of spindle cell melanoma. Cancer 1971; 28: Dimaio S, MacKay B, Smith L, et al: Neurosarcomatous transformation in malignant melanoma. An ultrastructural study. Cancer 1982; 50: Frolow G, Shapiro L, Brownstein M: Desmoplastic malignant melanoma. Arch Dermatol 1975; 111: Ghosh BC, Ghosh L, Huvos AJ, et al: Malignant schwannoma. A clinicopathologic study. Cancer 1973; 31: Hashimoto K, Brownstein M, Jakobrec F: Dermatofibrosarcoma protuberans, A tumor with perineural and endoneural cell features. Arch Dermatol 1974; 110: Horstadius S: The neural crest, Its properties and derivatives in the light of experimental research. London, Oxford University Press, Hsu SM, Raine L, Fanger H: Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 1981; 29:577, Kahn HJ, Marks A, Thom H, Baumal R: Role of antibody to S-100 protein in diagnostic pathology. Am J Clin Pathol 1983; 79: Labrecque P, Hong C, Winkelman RK: On the nature of desmoplastic melanoma. Cancer 1976; 38: Mazur M, Katzenstein AL: Metastatic melanoma: The spectrum of ultrastructural morphology. Ultrastructural Pathology 1980; 1: McCarthy SW, Palmer AA, Bale P: Nevus cells in lymph nodes. Pathology 1974;6: McGauran WL, Sypert G, Ballinger W: Melanotic schwannoma. Neurosurgery 1978; 2: Mennenmeyer RP, Hammar S, Tytus J, et al: Melanotic schwannoma. Am J Surg Pathol 1979; 3: Nakajima P, Watanabe S, Sato Y, et al: An immunoperoxidase study of S-100 protein distribution in normal and neoplastic tissues. Am J Surg Pathol 1982; 6: Reed R, Leonard D: Neurotropic melanoma, A variant of desmoplastic melanoma. Am J Surg Pathol 1979; 3: Smith JL: Tumors of the corium, The skin. Edited by EB Helwig, FK Mostofi. Baltimore, Williams and Wilkins, 1971, pp Taxy JB, Battifora H, Trujillo Y: Electron microscopy in the diagnosis of malignant schwannoma. Cancer 1981; 48: Valensi Q: Desmoplastic malignant melanoma, A light and electron microscopic study of two cases. Cancer 1979; 43: Warner T, Hafez R, Buehler D: Neurotropic melanoma of the vulva. Cancer 1982; 49: Warner T, Hafez G, Finch R, Bradenberg J: Schwann cell features in neurotropic melanoma. J Cutan Pathol 1981; 8: Weston RP: The migration and differentiation of neural crest cells. Adv Morphogenesis 1970; 8: Yannopoulos K: Desmoplastic malignant melanoma, Progress in surgical pathology, vol 2. New York, Masson, 1980, pp
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