J Cutan Pathol 2014: 41: 686–691 doi: 10.1111/cup.12347 John Wiley & Sons. Printed in Singapore

© 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Journal of Cutaneous Pathology

Recurrent primary cutaneous mucinous carcinoma with neuroendocrine differentiation: case report and review of the literature We report the case of a 60-year-old woman presenting with primary cutaneous mucinous carcinoma (PCMC) with neuroendocrine differentiation, revealed by neuroendocrine tumor lymph node metastasis 7 years before identification of the skin tumor. Only five cases of PCMC with neuroendocrine differentiation have been reported to date. The frequency of this neuroendocrine component may be underestimated, as it can require immunohistochemistry for identification, rather than being obvious on initial histopathologic examination. In the case presented here, the prominent neuroendocrine component displayed the morphological features of a well-differentiated neuroendocrine tumor with expression of common neuroendocrine markers, strong expression of estrogen and progesterone receptors and low Ki67 proliferation index (5%). This case shows that not all primary cutaneous neuroendocrine carcinomas are Merkel cell carcinomas (MCCs). In addition to rare primary cutaneous carcinoid tumors, the diagnosis of PCMC with neuroendocrine differentiation must be considered, particularly when confronted by a mucinous tumor or lymph node metastases of neuroendocrine carcinoma of unknown origin. On the basis of this case, identification of a neuroendocrine component in a PCMC might be an adverse prognostic indicator of recurrence or of lymph node metastasis and should support wider excision margins of the tumor. Keywords: cutaneous metastasis, mucinous carcinoma, neuroendocrine differentiation, sweat gland carcinoma Standley E, Dujardin F, Arbion F, Touzé A, Machet L, Velut S, Guyétant S. Recurrent primary cutaneous mucinous carcinoma with neuroendocrine differentiation: case report and review of the literature. J Cutan Pathol 2014; 41: 686–691. © 2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Primary cutaneous mucinous carcinoma (PCMC) is a rare low-grade skin carcinoma,1 reputedly developing from sweat glands and preferentially affecting men between 50 and 70 years of age.2 – 4 The main site of involvement


Elodie MiquelestorenaStandley1,2 , Fanny Dujardin1 , Flavie Arbion1 , Antoine Touzé3 , Laurent Machet2,4 , Stéphane Velut2,5 and Serge Guyétant1,2 1

CHRU de Tours, Laboratoire d’anatomie et cytologie pathologiques, Tours, France, 2 Université François-Rabelais de Tours, PRES Centre-Val de Loire Université, Tours, France, 3 INRA, UR 1282, Infectiologie animale et Santé Publique, Nouzilly, France, 4 CHRU de Tours, Service de dermatologie, Tours, France, and 5 CHRU de Tours, Service de neurochirurgie, Tours, France

Elodie Miquelestorena-Standley Service d’anatomie et cytologie pathologiques, CHRU de Tours, Hôpital Trousseau, 37044 Tours Cedex 09, France Tel: +33 247478112 Fax: +33 247474622 e-mail: [email protected] Accepted for publication March 16, 2014

is the head, particularly the eyelids.2,3 Although the clinical presentation is non-specific, the pathologic pattern of mucinous carcinoma is quite characteristic, with islands of basaloid cells surrounded by pools of mucin and separated by

Mucinous neuroendocrine carcinoma delicate fibrovascular trabeculae.2,4 Rare cases of mucinous carcinoma have been reported with neuroendocrine differentiation. Such neuroendocrine differentiation may cause diagnostic confusion, particularly when it is predominant or identified in a metastatic site of the disease. Mucinous carcinoma of the skin shares similarities with its mammary counterpart, especially in what some authors have described as a continuum from benign eccrine lesions to invasive carcinoma.5,6 Distinguishing primary cutaneous carcinoma from metastases of mammary or digestive origin may be challenging. A full metastatic workup is therefore recommended before reaching a conclusion of primary cutaneous carcinoma. Case report A healthy post-menopausal 60-year-old woman presented with a spinal cervical lymph node, measuring about 1 cm. Histopathology showed a lymph node widely infiltrated by a monotonous highly cellular carcinomatous proliferation of neuroendocrine appearance, consisting of cords and lobules separated by fibrous septae. Pseudorosettes are observed in some areas (Fig. 1). The proliferation comprised mid-sized cells with moderate amounts of cytoplasm. The nuclei were round with fine granular chromatin, small nucleoli and rare mitosis. Necrosis and intracytoplasmic or extracellular mucin were not observed. Immunohistochemical analysis showed that the tumor cells expressed epithelial membrane antigen (EMA), chromogranin and synaptophysin but not neurofilament. No primary tumor was identified. We concluded that this was a lymph node metastasis of a well-differentiated neuroendocrine carcinoma of unknown origin, and the patient was followed up with no other treatment. Over 7 years later, clinical examination revealed a painless infiltrated lesion of the scalp measuring 2 cm which had not previously been noticed (Fig. 2). Microscopic examination showed a tumor infiltrating the dermis and subcutis, consisting of nests or cribriform islands separated by thin fibrous septae (Fig. 3). Nests and islands were composed of epithelial cells embedded in pools of mucin (Fig. 3). Except for mucin production, the tumor morphology and immunophenotype were similar to the previously excised lymph node metastasis, and no in situ component was identified. Occasional cytoplasmic mucin-filled vacuoles were found. Immunohistochemistry staining was

Fig. 1. Lymph node metastasis is depicted with hematoxylin– phloxine–saffron staining. There is a well-differentiated neuroendocrine proliferation consisting of cords and lobules separated by fibrous septa.

Fig. 2. Histopathologic findings with hematoxylin–phloxine– saffron staining. The tumor consists of cell nests embedded in mucin pools separated by thin fibrous septa with infiltration of the dermis and subcutis.

positive for cytokeratin (CK) 7, chromogranin and synaptophysin, estrogen receptor (ER) and progesterone receptor (PR) (Fig. 4). The tumor expressed neither p63 nor CK5/6. Tumor cells were not labeled with CK20 antibody and polymerase chain reaction (PCR) using primer pairs in VP1 and large T (LT) antigen coding regions did not identify Merkel cell virus DNA in the tumor.7 As the excision margins were narrow, a complementary excision was performed. Complete clinical examination and extensive radiological investigations, including mammary examination, mammography, computed tomography (CT) scan and positron emission tomography (PET) scan were performed, with no evidence of a primary tumor. We therefore diagnosed a PCMC with neuroendocrine differentiation revealed by neuroendocrine lymph node metastasis 7 years before.


Standley et al.

Fig. 3. Histopathologic findings. Left panel: hematoxylin–phloxine–saffron staining; right panel: alcian blue staining. Nests and islands composed of epithelial cells embedded in pools of mucin are depicted.

Fig. 4. Immunohistochemical findings. Note the expression of CK7 (A), chromogranin (C) and estrogen receptor (D) and the absence of expression of CK20 (B).

Several local recurrences and regional lymph node metastases were identified over the 4 years following this diagnosis. Each one was removed, frequently with insufficient margins. The patient received cervical radiotherapy after the last intervention because of narrow margins. There has been no recurrence during the last 3 years of follow-up. Discussion We report the case of a 60-year-old woman presenting with PCMC with prominent neuroendocrine differentiation. Only five cases of this very rare cutaneous tumor have been published to date, none of them revealed by neuroendocrine tumor lymph node metastasis. In addition to this very particular diagnostic circumstance, this case provided the opportunity to review the diagnostic challenges presented by cutaneous mucinous carcinoma and to discuss the place of this rare tumor in the spectrum of neuroendocrine skin tumors – most of which


are Merkel cell carcinomas (MCCs) – and the prognostic role of this particular component. First described in 1952 by Lennox et al.,8 PCMC is a rare skin carcinoma, with fewer than 200 cases described in the literature.1 Certain histochemical and ultrastructural findings support eccrine differentiation,9 whereas other authors have reported apocrine differentiation,10 and thus an eccrine or apocrine origin remains a matter of debate. Mucinous carcinoma of the skin with neuroendocrine differentiation was first reported by Rahilly et al.11 in 1995 and to our knowledge only four other cases have been published since this initial report.1,2,11,12 PCMC more often affects men (58.8%) than women (41.2%) (mean age: 62.6 years).2,3,13 The clinical appearance of PCMC is non-specific. The most common site of involvement is the head and neck.3,14 Hematoxylin and eosin-stained sections of cutaneous mucinous carcinoma show a nodular tumor involving the dermis without connection to the epidermis. The tumor consists of solid, cystic or cribriform nests ‘floating’ in pools of mucin, separated by thin fibrous septae.2 Tumor cells present a low degree of atypia and mitotic figures are uncommon.3,14 Immunohistochemically, tumor cells show positive staining for CK7, EMA and hormone receptors and negativity for CK20.15,16 When present, neuroendocrine differentiation is emphasized by neuroendocrine markers such as chromogranin, synaptophysin or neuron-specific enolase, the expression of which is variable and sometimes focal.1,2,11,12 In 1997, Flieder et al.5 described a cutaneous tumor so-called endocrine mucin-producing sweat gland carcinoma (EMPSGC) which presented similarities with endocrine ductal carcinoma in situ (EDCIS) of the breast. EMPSGC is a well-circumscribed lesion arising in the dermis and consisting of solid or partially cystic nodules of cells with intracellular mucin production. Expression of neuroendocrine markers, which may be focal, is required to establish the diagnosis. Several findings suggest that EMPSGC might be a precursor of invasive mucinous carcinoma of the skin, in the same manner that EDCIS, a low-grade in situ breast carcinoma characterized by comparable aspects to those seen in EMPSGC, is frequently associated with invasive mucinous carcinoma of the breast.5 In 2005, following this report, Kazakov et al.15 carried out a study of 37 cases of PCMC and reported the presence of tumors with simultaneous sweat gland duct

Mucinous neuroendocrine carcinoma hyperplasia, atypical duct hyperplasia and ductal carcinoma in situ, as seen in breast carcinomas. The same year, Zembowicz et al.6 reviewed 12 cases of EMPSGC and showed that this tumor was frequently associated with benign sweat duct cysts, atypical epithelial cell proliferation and invasive mucinous eccrine carcinoma. In addition to comparable microscopic features, both mammary and sweat gland mucinous carcinomas express hormone receptors, as found in our case. However, hormone receptor expression is not specific of mucinous carcinoma as such expression sometimes occurs in other skin tumors.16 Our case supports the close relationship between the EMPSGC and PCMC. Even though these two tumors have never been observed together in any of all recurrences, the absence of other primitive carcinoma identified and the presence of neuroendocrine component in both lymph node and cutaneous tumors are supplementary arguments in favor of the hypothesis highlighted by Zembowicz et al. PCMC can be indistinguishable from metastatic mucinous carcinoma, particularly when metastasized from breast carcinoma. It can be difficult, or even impossible, to differentiate a mammary metastasis from a primary skin tumor on hematoxylin and eosin-stained sections. Furthermore, immuhistochemistry can be misleading (CK7 and hormone receptors are expressed in both instances). The identification of neuroendocrine differentiation is not helpful, as it can be found in both tumors. Mucinous carcinoma from other organs can metastasize to the skin, including gastrointestinal tract, lung, ovary, pancreatic–biliary tract, prostate and salivary gland tumors. A complete metastatic workup is therefore required before establishing a diagnosis of PCMC, even when its presentation is slightly different. Indeed, the primary tumor is often already diagnosed at the time of excision as cutaneous metastases are most frequently observed in advanced stages. Moreover, cutaneous metastases from other sites show a strong predilection for the trunk or axillae and display more atypical cells with more mitosis.13 The World Health Organization (WHO) classification of the skin4 offers certain histopathologic criteria to identify metastasis: larger clusters of cohesive neoplastic cells, smaller quantity of mucin and absence of fibrous septa surrounding pools of mucin. In terms of differential diagnosis from a metastasis of gastrointestinal origin, the latter frequently displays dirty necrosis often associated with goblet cells, CK20 positivity and CK7 negativity, in contrast

to cutaneous carcinomas.15,17 Immunoreactivity with transcription factor CDX2 may be an additional argument indicating a primary colorectal tumor. According to Kazakov et al.,15 the presence of an in situ component surrounded by myoepithelial cells highlighted by p63 and CK5/6 at the periphery of the tumor17 may be an additional criterion on which to make the diagnosis of primary carcinoma. However, the absence of an in situ component does not imply extracutaneous origin.17,18 The neuroendocrine differentiation observed in our case raised the possibility of a primary or metastatic neuroendocrine tumor. Although it is a rare tumor, MCC is by far the most frequent primary cutaneous neuroendocrine tumor7 and displays high grade features.4 An important advance in the understanding of this malignancy has been the recent discovery of a new polyomavirus (Merkel cell polyomavirus), which has been identified in most Merkel cell carcinomas.19,20 Low-grade primary cutaneous neuroendocrine tumors are exceedingly rare: MCC is the only neuroendocrine neoplasm described in the WHO ‘blue book’ of skin tumors4 and only four cases of primary cutaneous carcinoid tumors and one case of a primary cutaneous atypical carcinoid tumor have been described in the literature.21 Most cutaneous neuroendocrine tumors are therefore high grade tumors and consist of either MCC or metastases of non-cutaneous neuroendocrine carcinomas, particularly small cell lung carcinomas. In our case, the tumor was growing slowly and displayed low or intermediate grade features such as no mitotic activity, no necrosis and Ki67 index proliferation evaluated at 5%, clearly indicating a low-grade neuroendocrine component. In addition, the prominent mucinous differentiation of the tumor and the absence of CK 20 expression by tumor cells were strong arguments against MCC. Moreover, PCR analysis for Merkel cell polyomavirus performed on the cutaneous tumor was negative. In addition to this uncommon neuroendocrine differentiation, the singularity of our observation is the revealing of the disease by a lymph node metastasis 7 years before the identification of the primary cutaneous tumor. This lymph node metastasis contained only the neuroendocrine component of the tumor without any mucin pool, as did each local recurrence and subsequent lymph node metastases. The hypothesis of a primary cutaneous tumor was therefore unpredictable. To our knowledge, no


Standley et al. other case with such a presentation has been reported to date. Although PCMC is a low-grade carcinoma, local aggressive behavior and recurrence have been reported and attributed to infiltrative growth.13 Local recurrence is frequent (20–30%)3,13,22,23 while lymph node and distant metastases are uncommon (11% and 3–11%, respectively).3,13,22,23 Only two cases with fatal outcome because of metastatic spread have been reported.24,25 The natural history of our case suggests that the neuroendocrine component, identified in every lymph node metastasis and recurrence, was mainly responsible for the aggressiveness of the tumor. This differs from what has been reported in breast mucinous carcinomas, in which neuroendocrine differentiation is associated with a better prognosis because of more favorable microscopic and immunohistochemical parameters, and moreover it affects older patients.26 Our case suggests that in the context of PCMC with neuroendocrine differentiation, the latter component should alert the physician to the possibility of recurrence and lymph node metastasis and may necessitate more extensive local resection of the tumor. In spite of this, PCMC with neuroendocrine differentiation remains a low-grade skin carcinoma, since more than 10 years have elapsed from the first identification of the tumor, and the patient has not presented any recurrence or metastases since receiving local radiotherapy 3 years ago. Owing to the unpredictable risk of clinical spread, wide surgical excision represents the reference treatment for PCMC. For the same reason, long term annual follow-up with detailed systemic examination is recommended, with particular attention to regional lymph nodes.1

PCMC is usually resistant to chemotherapy and radiotherapy, and as a consequence surgical treatment with wide margins remains the gold standard.1,14 In our case, the patient presented several recurrences and regional lymph node metastases, most of them because of positive or narrow margins. Moreover, she received radiotherapy after the fourth local recurrence of the tumor, which has not recurred since that time (3 years follow-up). This may indicate a possible role for radiotherapy, at least for tumors with a prominent neuroendocrine component. Conclusion PCMC is a rare, low-grade cutaneous tumor in which neuroendocrine differentiation may uncommonly occur. When identifying a mucinous carcinoma on a skin specimen, pathologists should be aware of the possibility of cutaneous metastasis, which has a worse prognosis. A full metastatic workup and long term follow-up is therefore recommended in such cases before asserting the primary nature of the tumor. Diffuse neuroendocrine differentiation, as seen in our patient, has rarely been reported in mucinous skin carcinomas. Its frequency may be underestimated, as it requires specific immunohistochemistry in order to identify the neuroendocrine component, which may be focal. In our case, the natural history of the tumor, revealed by lymph node metastasis of the neuroendocrine component, was particularly misleading. In cases of lymph node metastasis of a low-grade neuroendocrine tumor with no identified primary tumor, the rare possibility of low-grade cutaneous neuroendocrine tumors, including PCMC with neuroendocrine differentiation, should be borne in mind.

References 1. Han S-E, Lim SY, Lim HS. Neuroendocrine differentiation of primary mucinous carcinoma of the cheek skin. Arch Plast Surg 2013; 40: 159. 2. Kim J-B, Choi J-H, Kim J-H, et al. A case of primary cutaneous mucinous carcinoma with neuroendocrine differentiation. Ann Dermatol 2010; 22: 472. 3. Scilletta A, Soma PF, Grasso G, et al. Primary cutaneous mucinous carcinoma of the cheek. Case report. G Chir 2011; 32: 323. 4. Requena L, Kutzner H, Hurt MA, Santa Cruz DJ, Mehregan DA, Mehregan DR, Mengesha YM, Kohler S, Argenyi ZB, McNiff J, Rudolph P, Sangüeza OP. Malignant tumors with apocrine and eccrine


differentiation. In: LeBoit PE, Burg G, Weedon D, Sarasain A, eds. World Health Organization classification of tumors. Pathology and genetics of skin tumors. Lyon: IARC Press, 2006; 131. 5. Flieder A, Koerner FC, Pilch BZ, Maluf HM. Endocrine mucin-producing sweat gland carcinoma: a cutaneous neoplasm analogous to solid papillary carcinoma of breast. Am J Surg Pathol 1997; 21: 1501. 6. Zembowicz A, Garcia CF, Tannous ZS, Mihm MC, Koerner F, Pilch BZ. Endocrine mucin-producing sweat gland carcinoma: twelve new cases suggest that it is a precursor of some invasive mucinous carcinomas. Am J Surg Pathol 2005; 29: 1330.

7. Touzé A, Le Bidre E, Laude H, et al. High levels of antibodies against merkel cell polyomavirus identify a subset of patients with merkel cell carcinoma with better clinical outcome. J Clin Oncol 2011; 29: 1612. 8. Lennox B, Pearse AG, Symmers WS. The frequency and significance of mucin in sweat gland tumours. Br J Cancer 1952; 6: 363. 9. Wright JD, Font RL. Mucinous sweat gland adenocarcinoma of eyelid: a clinicopathologic study of 21 cases with histochemical and electron microscopic observations. Cancer 1979; 44: 1757. 10. Yeung KY, Stinson JC. Mucinous (adenocystic) carcinoma of sweat glands with

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widespread metastasis. Case report with ultrastructural study. Cancer 1977; 39: 2556. Rahilly MA, Beattie GJ, Lessells AM. Mucinous eccrine carcinoma of the vulva with neuroendocrine differentiation (abstract). Histopathology 1995; 27: 82. Bellezza G, Sidoni A, Bucciarelli E. Primary mucinous carcinoma of the skin(abstract). Am J Dermatopathol 2000; 22: 166. Scholz IM, Hartschuh W. Primary mucinous eccrine carcinoma of the skin-a rare clinical tumor with many differential diagnoses. J Dtsch Dermatol Ges 2010; 8: 446. Karimipour DJ, Johnson TM, Kang S, Wang TS, Lowe L. Mucinous carcinoma of the skin. J Am Acad Dermatol 1997; 36: 323. Kazakov DV, Suster S, LeBoit PE, et al. Mucinous carcinoma of the skin, primary, and secondary: a clinicopathologic study of 63 cases with emphasis on the morphologic spectrum of primary cutaneous forms: homologies with mucinous lesions in the breast. Am J Surg Pathol 2005; 29: 764.

16. Kwatra KS, Prabhakar BR, Jain S. Oestrogen and progesterone receptors in primary mucinous carcinoma of skin. Australas J Dermatol 2005; 46: 246. 17. Levy G, Finkelstein A, McNiff JM. Immunohistochemical techniques to compare primary vs. metastatic mucinous carcinoma of the skin. J Cutan Pathol 2010; 37: 411. 18. Ivan D, Nash JW, Prieto VG, et al. Use of p63 expression in distinguishing primary and metastatic cutaneous adnexal neoplasms from metastatic adenocarcinoma to skin. J Cutan Pathol 2007; 34: 474. 19. Touzé A, Gaitan J, Maruani A, et al. Merkel cell polyomavirus strains in patients with merkel cell carcinoma. Emerg Infect Dis 2009; 15: 960. 20. Feng H, Shuda M, Chang Y, Moore PS. Clonal integration of a polyomavirus in human Merkel cell carcinoma. Science 2008; 319: 1096. 21. Terada T. Primary cutaneous neuroendocrine tumor (atypical carcinoid) expressing KIT and PDGFRA with myoepithelial differentiation: a case report with immunohistochemical and molecular






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Recurrent primary cutaneous mucinous carcinoma with neuroendocrine differentiation: case report and review of the literature.

We report the case of a 60-year-old woman presenting with primary cutaneous mucinous carcinoma (PCMC) with neuroendocrine differentiation, revealed by...
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