ORIGINAL ARTICLE. Cutaneous Sebaceous Neoplasms With a Focal Glandular Pattern (Seboapocrine Lesions): A Clinicopathological Study of Three Cases
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1 ORIGINAL ARTICLE Cutaneous Sebaceous Neoplasms With a Focal Glandular Pattern (Seboapocrine Lesions): A Clinicopathological Study of Three Cases Dmitry V. Kazakov, MD, PhD,* Eduardo Calonje, MD, Dip RCPath, Arno Rütten, MD, Kathrin Glatz, MD, and Michal Michal, MD* Abstract: Presented here are three cutaneous sebaceous tumors (one carcinoma and two sebaceomas), each demonstrating a focal glandular pattern representing apocrine differentiation. The patients, two males and one female, each clinically presented with a small solitary nodule or tumor on the scalp. None of the patients had features of Muir Torre syndrome. Surgical removal of the lesions was performed in all cases. None of the patients developed recurrence or metastasis after surgery (follow-up ranged from 18 to 24 months). The glandular areas represented a minor but significant component of the lesions and appeared as glands of various complexity, mostly as simple round or elongated tubular structures lined by a row of cuboidal to columnar cells with eosinophilic cytoplasm and round nuclei, with or without a distinct nucleolus. Decapitation secretion was evident but not prominent. In both sebaceomas, at least a portion of the glands had a peripheral small-cell layer that appeared similar to the basal/myoepithelial cells of normal eccrine and apocrine ducts. In some glands, the basal/myoepithelial cells seemed to have undergone hyperplasia, resulting in two or more rows of cells that even formed small islands, with an overall appearance reminiscent of basal cell hyperplasia in the prostate, arising in the basal layer of the prostatic glands. The descriptive terms seboapocrine carcinoma or seboapocrine sebaceoma are proposed for such lesions. These tumors may be viewed as rare histopathological variants of sebaceous carcinoma and sebaceoma, with a second type of differentiation along the lines of the folliculosebaceous apocrine unit. Key Words: adnexal tumors, sebaceous neoplasms, apocrine differentiation, multidirectional differentiation, myoepithelial cells (Am J Dermatopathol 2007;29: ) Sebaceous tumors of the skin are most commonly classified into carcinoma (ocular and extraocular), sebaceoma, and sebaceous adenoma. 1 These show different degrees of From the *Sikl s Department of Pathology, Charles University, Medical Faculty Hospital, Pilsen, Czech Republic (D.V.K., M.M.); Department of Dermatopathology, St John s Institute of Dermatology, St Thomas s Hospital, London, England, UK (E.C.); Dermatohistopathologische Gemeinschaftspraxis, Friedrichshafen, Germany (A.R.); and Institute of Pathology, University of Basel, Basel, Switzerland (K.G.). Reprints: Dmitry V. Kazakov, MD, PhD, Sikl s Department of Pathology, Charles University Medical Faculty Hospital, Alej Svobody 80, PILSEN, Czech Republic ( kazakov@medima.cz). Copyright Ó 2007 by Lippincott Williams & Wilkins sebaceous differentiation and different architectural and cytological features, usually allowing clear histopathological separation, although some histopathological overlap exists. The tumor cells in these sebaceous neoplasms grow mainly in a cohesive fashion, although rare tumors manifest distinctive growth patterns such as the rippled, labyrinthine/sinusoidal, and carcinoid-like ones that are apparently specific for lesions with sebaceous differentiation and are encountered either singly or in combination in cutaneous tumors with sebaceous differentiation. 2 6 So-called adenoid and acinar patterns have been recorded in some examples of ocular sebaceus carcinoma, 7 and rare sebaceous neoplasms have been reported to focally exhibit apocrine differentiation. 8,9 Presented here are three further cutaneous sebaceous tumors with a focal glandular pattern representing apocrine differentiation. MATERIALS AND METHODS Histological slides from approximately 200 malignant and benign cutaneous sebaceous tumors (ocular and extraocular carcinomas, sebaceomas, sebaceous adenomas, basal cell carcinoma with sebaceous differentiation, cystic sebaceous tumor 10 ), including those associated with the Muir Torre syndrome, 11 were evaluated. Cases of organoid nevus (nevus sebaceus of Jadassohn) and secondary tumors arising in it were not studied and, when recognized histologically as such, were excluded. Eight sebaceous tumors manifesting a glandular pattern were found. The term glandular is used to describe structures containing lumina surrounded by epithelial cells, with or without evidence of decapitation secretion. Multiple sections were reviewed to exclude the possibility that these glandular areas might represent preexisting ducts or represent a pseudoglandular pattern attributable to various causes (holocrine secretion, cell discohesive arrangement attributable to necrosis, acantholysis, or myxoid degeneration), as was the case in five tumors that were subsequently excluded from the study. Clinical information and follow-up on the three included cases were obtained from pathology reports, submitting pathologists, patients, and their clinicians. Paraffin blocks or reserved unstained slides were available in two cases for immunohistochemical study. Immunohistochemical stains were performed on 5-mM-thick, formalin-fixed, paraffin-embedded tissue sections, and appropriate controls were applied using the monoclonal and polyclonal antisera listed in Table 1. The avidin biotin complex or Am J Dermatopathol Volume 29, Number 4, August
2 Kazakov et al Am J Dermatopathol Volume 29, Number 4, August 2007 TABLE 1. Antibodies Used for Immunohistochemical Study Antibody Specificity Clone Dilution Source CK7 OV-TL 12/30 1:200 DakoCytomation CK 14 Ll002 1:1000 NeoMarkers EMA E29 1:700 DakoCytomation CK 8 &18 CAM5.2 1:200 Becton Dickinson ASMA 1A4 1:200 DakoCytomation MSA HHF-35 1:5000 DakoCytomation GCDFP-15 BRST-2 1:1000 Signet Laboratories p63 4A4 1:500 Biotex CK, cytokeratin; EMA, epithelial membrane antigen; ASMA, a-smooth muscle actin; MSA, muscle-specific actin; GCDFP-15, gross cystic disease fluid protein-15. streptavidin biotin complex, labeled with peroxidase or alkaline phosphatase, were employed as the detection systems. Automated immunostaining employing the Lab Vision automatic stainer was used. RESULTS Clinical Data The patients, two males and one female, each clinically presented with a small solitary nodule or tumor on the scalp (Table 2). Ulceration was seen in case 1, which represented sebaceous carcinoma. None of the patients had features of Muir Torre syndrome. Surgical removal of the lesions was performed in all cases. None of the patients developed recurrence or metastasis after surgery (follow-up ranged from 18 to 24 months). Histopathological Findings One case was classified as sebaceous carcinoma because of the presence of architectural (asymmetry, infiltrative growth) and cytological atypia (cellular and nuclear pleomorphism, cell necrosis, atypical mitoses; Fig. 1A D). Two lesions were classified as sebaceomas (Fig. 2A C). All three neoplasms manifested a multinodular architecture and were predominantly composed of basaloid cells and cells with vacuolated cytoplasm and scalloped nuclei. The neoplasm cells grew mainly in a cohesive fashion, but in both sebaceomas, labyrinthine/sinusoidal, poorly developed carcinoidlike, and rippled patterns, as previously reported, 2 4 were identified (Fig. 2B). The glandular areas represented a minor but significant component of the lesions; they appeared as glands of various complexity, mostly as simple round or elongated tubular structures lined by rows of cuboidal to columnar cells with eosinophilic cytoplasm and round nuclei, with or without a distinct nucleolus (Fig. 1E and F and Fig. 2D F). Decapitation secretion was evident but not prominent (Fig. 2E). In one sebaceoma (case 3), the cytoplasm of the luminal cells in glandular structures contained zymogen granules (Fig. 2F). In both sebaceomas, at least a portion of the glands had a peripheral small-cell layer that seemed similar to the basal/ myoepithelial cells of normal eccrine and apocrine ducts. The gland structures were numerous and were distributed somewhat haphazardly. In some glands, the basal/myoepithelial cells seemed to have undergone hyperplasia, resulting in two or more rows of cells that even formed small islands, with an overall appearance reminiscent of basal cell hyperplasia in the prostate, arising in the basal layer of the prostatic glands. (Fig. 2G). Glands with basal/myoepithelilal cells and those lacking them were intermingled. In one sebaceoma (case 2), there were foci of immature squamous metaplasia and areas composed of basaloid cells, devoid of sebaceous differentiation, that housed scattered lymphocytes, with the resulting picture vaguely resembling a spiradenoma. In both sebaceomas, differentiation toward sebaceous ducts was seen. No other metaplastic phenomena or adnexal-type differentiations were observed, nor were there any recognizable microscopic features of nevus sebaceus of Jadassohn. Immunohistochemical Findings Immunohistochemical studies were performed on the sebaceomas. The glandular areas were positive for CAM5.2 and CK7 (Fig. 2H). Stains for CK7 also highlighted sebocytes with multivacuolated cytoplasm, as did the stains for EMA (Fig. 2I). CK14 stained the entire tumors, including the glandular parts and basaloid cells; GCDFP-15 was tested in case 3 and proved positive in the glandular luminal cells. The peripheral basal/myoepithelial-like cells in the glandular areas were positive for p63 in both cases; they tested negative for actins in case 3. DISCUSSION We have presented three sebaceous cutaneous neoplasms with a focal glandular pattern. The detection of this feature in an otherwise typical sebaceous tumor seems to have no clinical or prognostic implication, but this microscopic finding may be confusing. Two of the presented cases were consultations, and the submitting pathologists specifically TABLE 2. The Main Clinical Features of Patients With Seboapocrine Carcinoma (Case 1) and Seboapocrine Sebaceomas (Cases 2 and 3) Case Sex Age Location Clinical Presentation Size (cm) Treatment Follow-Up MTS Case 1 Female 76 Scalp Solitary tumor Excision NED at 29 months No Case 2 Male 36 Scalp Solitary grey nodule Excision NED at 18 months No Atheroma? Fibroma? Case 3 Male 84 Scalp Solitary tumor. BCC? Excision NED at 24 months No NED, no evidence of disease; MTS, Muir Torre syndrome; BCC, basal cell carcinoma. 360 q 2007 Lippincott Williams & Wilkins
3 Am J Dermatopathol Volume 29, Number 4, August 2007 Seboapocrine Skin Tumors FIGURE 1. Sebaceous carcinoma. A and B, Asymmetric multinodular neoplasm with an infiltrative growth pattern. C and D, Cytological details: cohesive growth of cells with pleomorphic round nuclei and prominent nucleolus. The cytoplasm of some cells contained tiny vacuoles and a mature sebocyte can be seen in the center. Note atypical mitotic figures. E and F, A glandular structure with decapitation secretion. asked for the meaning of this feature and the precise classification of the lesions. We suggest that the descriptive terms seboapocrine carcinoma, seboapocrine sebaceoma, or sebaceous carcinoma (or sebaceoma) with focal apocrine differentiation can be used in such situations. The term seboapocrine sebaceoma should not be mistaken for the term sebocrine adenoma, which has been used by Zaim 8 to describe two lesions that were regarded later as apocrine poroma. Conjoint apocrine, sebaceous and follicular differentiation in a cutaneous appendageal tumor, is not an unexpected finding given the embryological derivation of the apocrine gland, sebaceous gland, and hair follicle from the common folliculosebaceous apocrine unit The simultaneous occurrence of two or three types of differentiation along the lines of the folliculosebaceous apocrine unit in cutaneous adnexal tumors is not rare; it may, in fact, be underrecognized. Combined folliculosebaceous apocrine differentiation is quite often seen in apocrine mixed tumors 12,24 26 and nevus sebaceus of Jadassohn In the classification of cutaneous adnexal neoplasms proposed by McCalmont, 32 the lesions that are reported herein can be added to the apocrine sebaceous category to join apocrine poroma and may be viewed as examples of adnexal tumors with divergent (multidirectional) differentiation. 32,38 40 Parenthetically, a sebaceoma in one of our patients manifested small areas resembling those seen in a spiradenoma, the entity that some authorities now consider an apocrine neoplasm. 12,41 Evidence supporting this issue is provided by the reported cases of spiradenoma associated with areas of sebaceous and/or follicular differentiation in adnexal lesions or simultaneous occurrence of spiradenoma and other follicular, sebaceous, or apocrine neoplasms in patients with Brooke Spiegler syndrome, or q 2007 Lippincott Williams & Wilkins 361
4 Kazakov et al Am J Dermatopathol Volume 29, Number 4, August 2007 FIGURE 2. Sebaceoma. A, Whole-mount view of the vertically oriented multinodular lesion. B, Labyrinth-like /sinusoidal pattern. C, Cytological detail: monomorphous basaloid cells admixed with mature sebocytes. D G, Glandular areas. Numerous elongated tubules and small round lumens can be seen (D). Note rare vacuolated sebocytes in the adjacent areas (D, lower left). Glands of more complex architecture surrounded by a distinct peripheral basal/myoepithelial cell layer and decapitation secretion in the luminal cells (E). Zymogen granules in the luminal cells of the glands (F). In some glands, the basal/myoepithelial cell layer appears hyperplastic resulting in two or more rows of cells that even form small islands (G, arrows). This appearance can be linked to basal cell hyperplasia in the prostate. H and I, Immunohistochemical staining. The glandular structures are positive for CAM5.2, whereas the rest of the tumor reacted negatively (H). Both scattered sebocytes with vacuolated cytoplasm and glandular structures are positive for CK7 (I). 362 q 2007 Lippincott Williams & Wilkins
5 Am J Dermatopathol Volume 29, Number 4, August 2007 Seboapocrine Skin Tumors folliculosebaceous apocrine tumors manifesting spiradenomatous areas. 12,40,42 51 The glandular patterns described above should be distinguished from a pseudoglandular pattern, in which the formation of structures resembling glands is caused by the loss of integrity of solid epithelial structures attributable to cell necrosis, acantholysis, or myxoid degeneration. Holocrine secretion may sometimes impart a pseudoglandular appearance to a sebaceous tumor. Further, small aggregations of neoplastic sebaceous cells with vacuolated cytoplasm may produce cleftlike spaces resembling tubules. Glandular patterns, especially simple, small, round, tubular ones, should also be distinguished from preexisting adnexal structures that became entrapped by the tumor. Clues to the latter situation include a small number of tubular elements in the lesion, the location of tubular/ductal structures near the preexisting hair follicle, or a traceable vertical arrangement suggesting involved excretory ducts. The glands in both sebaceomas in our series were numerous exceeding the number that one would expect to see with the preexisting ducts and were haphazardly distributed. Still, we had the impression that the neoplastic tubules may have indeed originated from the preexisting ducts, because some glands were surrounded in part by a preserved basal/myoepithelial layer. On the other hand, one cannot fully discard the fact that the ducts with basal/myoepithelial cells may represent newly formed neoplastic ducts. Three lines of evidence may indirectly support this preposition. First, the glands containing a peripheral basal/myoepithelial cell layer and those lacking it were intermingled, as if they belonged to the same origin. Second, they showed decapitation secretion, which is normally seen only in the secretory part, and never in the ducts (hence, apocrine and eccrine ducts cannot be distinguished morphologically). Third, some glands showed focal hyperplasia of cells comprising the peripheral layer, resulting in an appearance reminiscent of basal cell hyperplasia of the prostate. To our knowledge, this feature has not been described in normal eccrine or apocrine ducts, but we have seen a similar phenomenon in rare examples of cutaneous tubular adenoma and syringocystadenoma papilliferum (Kazakov et al, unpublished observations, 2006). In summary, we have described three sebaceous cutaneous neoplasms with a focal glandular pattern, for which the descriptive terms seboapocrine carcinoma or seboapocrine sebaceoma are proposed. These cases most probably do not represent separate entities; instead, they may be viewed as rare, histopathological variants of sebaceous carcinoma and sebaceoma, with a second type of differentiation along the lines of the folliculosebaceous apocrine unit. REFERENCES 1. LeBoit PE, Burg G, Weedon D, et al. World Health Organization Classification of Tumours. Pathology and Genetics of Skin Tumours. Lyon; France: IARC Press; Ackerman AB, Ball E, Guo Y. Labyrinthine/sinusoidal pattern in sebaceoma. Dermatopathol Pract Conc. [serial online]. 2002;8. Available at: BookTextView/136403;cs¼pr. Accessed October Ohata C, Ackerman AB. Ripple pattern in a neoplasm signifies sebaceous differentiation [sebaceoma (not trichoblastoma or trichomatricoma) if benign and sebaceous carcinoma if malignant]. Dermatopathol Pract Conc. [serial online]. 2001;7: Available at: com/dynaweb/resources/dpc/130926/@generic_booktextview/130926; cs¼pr. Accessed October Kazakov DV, Kutzner H, Rutten A, et al. 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