Neuroendocrine Neoplasms of the Mediastinum

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1 Neuroendocrine Neoplasms of the Mediastinum Saul Suster, MD, 1 and Cesar A. Moran, MD 2 Key Words: Neuroendocrine carcinoma; Carcinoid; Paraganglioma; Parathyroid adenoma Abstract Neuroendocrine neoplasms of the mediastinum form part of a family of tumors characterized by genotypic, immunophenotypic, and functional properties of neuroendocrine differentiation. Although rare, these tumors have been the source of much attention and controversy in the literature. Their nomenclature and classification, in particular, have continued to evolve over the years. Such tumors comprise lesions derived from neuroendocrine elements within the thymus, from paraganglionic rests, or from misplaced embryonal structures within the mediastinum. The most common neuroendocrine neoplasms of this anatomic region, however, correspond to neuroendocrine carcinomas of the thymus. The light microscopic, immunohistochemical, and ultrastructural features of these tumors are reviewed along with the advances in our understanding of these lesions and current trends in nomenclature and terminology. Neuroendocrine neoplasms of the mediastinum are relatively rare tumors that have been the source of much controversy in the literature. These tumors may originate from the thymus proper or from paraganglionic structures within the mediastinum, or they may be the result of neoplastic transformation in misplaced embryonal rests within the mediastinum. These tumors can often also be the source of hormone secretion and, thus, come to the attention of the clinician owing to metabolic abnormalities. The exact nosologic classification of these tumors has been a subject of debate for many years. The most common neuroendocrine neoplasms in the mediastinum are thymic neuroendocrine carcinomas (so-called thymic carcinoid in the older literature). More rarely, the mediastinum also can be the seat of tumors derived from aorticopulmonary or aorticosympathetic paraganglia or from ectopic or supernumerary parathyroid glands. Neuroendocrine Carcinomas of the Thymus Primary neuroendocrine carcinomas of the thymus (formerly known as thymic carcinoids) are unusual tumors that account for less than 5% of all anterior mediastinal neoplasms. 1 The first to recognize these tumors in this location were Rosai and Higa, 2 who called attention to their association with the multiple endocrine neoplasia (MEN) syndrome. 3 It was noted in the older literature that thymic carcinoids differed substantially from their other foregut counterparts in that the mediastinal tumors often followed a significantly more aggressive clinical course. Thus, thymic carcinoids were found to behave in a malignant fashion in approximately 82% of cases, as opposed to bronchial carcinoids, which exhibit malignant behavior in only about 26% of cases. 4 S17

2 Suster and Moran / NEUROENDOCRINE NEOPLASMS OF THE MEDIASTINUM Thymic neuroendocrine carcinomas generally manifest as anterosuperior mediastinal masses with a male predilection (male/female ratio, 3:1). 5 The disease most often affects middle-aged adults (median age, 43 years). The patients may be asymptomatic or have signs and symptoms related to a rapidly growing mediastinal mass, ie, cough, chest pain, and the superior vena cava syndrome. About a third of the patients may have endocrine symptoms. There is a strong clinical association with endocrine abnormalities, particularly the MEN-type 1 syndrome, 3,6-8 and other conditions such as polyarthropathy, proximal myopathy, peripheral neuropathy, 9 hyperparathyroidism, 10 inappropriate antidiuretic hormone secretion, Eaton-Lambert syndrome, and hypertrophic osteoarthropathy. 11 Wick et al 12 noted that approximately half of thymic carcinoids were functionally active or associated with the MEN syndrome. It has been estimated that these tumors also may be associated with the secretion of ectopic corticotropin in approximately 38% of cases. 13 Thymic neuroendocrine carcinomas, however, are not associated with myasthenia gravis, hypogammaglobulinemia, or the carcinoid syndrome. Classification and Nomenclature The term carcinoid was introduced in the literature in 1907 by Obendorfer 14 to designate a group of tumors in the small intestine that had a better prognosis than conventional carcinomas. Gosset and Masson 15 postulated an origin from neuroendocrine cells by demonstrating the presence of argentaffin granules in the tumor cells. Since then the term carcinoid became ingrained in the literature and was widely applied to all tumors displaying similar histologic and histochemical features throughout the body. The terminology for these tumors in the mediastinum, however, has been controversial. Some authors have proposed designating all mediastinal tumors of this type as atypical carcinoid, 16 owing to their close resemblance to similar tumors described by Arrigoni et al 17 in the lung. Rosai et al 18 proposed separating these tumors into carcinoid grade I (equivalent to conventional carcinoid), carcinoid grade II (equivalent to atypical carcinoid), and carcinoid grade III (equivalent to oat cell carcinoma). Interestingly, Wick and Rosai 11 subsequently stated that the terms carcinoid and atypical carcinoid had become outmoded and should be replaced by the generic designation of neuroendocrine carcinoma. Other authors have since supported this view. Montpreville et al, 19 in their study of neuroendocrine tumors of the thymus, also concluded that these tumors should be considered as belonging in the spectrum of neuroendocrine carcinomas. We recently had the opportunity to evaluate a large series of primary thymic neuroendocrine neoplasms from the files of the Armed Forces Institute of Pathology, Washington, DC. 20 Based on our observations, we also agree that such tumors should be regarded as part of a single spectrum of differentiation ranging from well to moderately well to poorly differentiated neuroendocrine neoplasms Table 1. We support abandoning the term carcinoid as a designation for these tumors because the term may imply a misleadingly benign or extremely low-grade neoplasm, whereas most thymic carcinoids are actually very aggressive tumors. Also, the designation of neuroendocrine carcinoma is histogenetically more accurate. As such, we have proposed the following classification scheme for primary neuroendocrine neoplasms 20 : 1. Well-differentiated neuroendocrine carcinoma: tumors showing 3 or fewer mitotic figures per 10 high-power fields (HPF), minimal cytologic atypia, small foci of necrosis, and good preservation of the classic organoid growth pattern 2. Moderately differentiated neuroendocrine carcinoma: tumors showing loss of organoid architecture with increased mitotic activity (4-10 mitoses per 10 HPF), areas of necrosis, and moderate cytologic atypia 3. Poorly differentiated neuroendocrine carcinoma: tumors showing high mitotic activity (>10 mitoses per 10 HPF), extensive areas of necrosis, marked nuclear atypia, loss of organoid architecture, and/or evidence of areas showing features of small cell carcinoma Neuroendocrine carcinomas of the thymus are usually large, bulky tumors with an average diameter of 10 cm. The tumors are often infiltrative and invade adjacent structures such as lung, pleura, and pericardium, but also may be encapsulated and well-circumscribed. The cut surface usually shows tan-white, homogeneous rubbery tissue with frequent areas of hemorrhage and necrosis. Foci of microcalcifications are common and account for the gritty texture of these tumors on the cut surface. Histologically, the tumors recapitulate the features of similar neoplasms at other locations. However, when arising in the thymus, they often can adopt unusual morphologic appearances. Table 1 Comparison of Proposed Terms for Primary Thymic Neuroendocrine Neoplasms Conventional Terminology Rosai et al 18 Moran and Suster 20 Carcinoid Carcinoid type I Well-differentiated neuroendocrine carcinoma Atypical carcinoid Carcinoid type II Moderately differentiated neuroendocrine carcinoma Small cell carcinoma Carcinoid type III Poorly differentiated neuroendocrine carcinoma S18

3 Well-Differentiated Thymic Neuroendocrine Carcinomas Well-differentiated thymic neuroendocrine carcinomas are characterized by a well-developed neuroendocrine (organoid) growth pattern with mild to minimal cytologic atypia. The most frequent growth pattern observed in these tumors is the nested (Zellballen) pattern characterized by rounded nests of monotonous tumor cells surrounded by thin fibrovascular septa Image 1. Another distinctive growth pattern is the trabecular pattern characterized by the formation of ribbons or festoons of monotonous tumor cells separated by edematous or hyalinized stroma Image 2. The tumor cells usually contain small round nuclei with coarse clumping of chromatin surrounded by abundant cytoplasm, but usually will display at least focally subtle cytologic features of atypia such as enlarged, hyperchromatic nuclei with prominent nucleoli and scattered mitoses (usually 3 or fewer mitoses per 10 HPF). Discrete foci of necrosis with dystrophic calcifications also may be seen. A series of unusual growth patterns has been described in these tumors, which may display cytologic features of atypia ranging from well to moderately differentiated. The oncocytic variant of neuroendocrine carcinoma of the thymus is characterized by a neoplastic cell population containing abundant eosinophilic cytoplasm Image In most cases, such tumors display, at least focally, a prominent neuroendocrine growth pattern that will facilitate their proper identification. In many cases, however, the tumor may grow as solid sheets of oncocytic tumor cells, raising the possibility of conditions other than a neuroendocrine neoplasm in the differential diagnosis. Neuroendocrine carcinomas may adopt a prominent spindle cell appearance that can closely simulate other types of spindle cell tumors of this region Image 4. 22,23 The clue to the diagnosis lies in identifying, by scanning magnification, the subtle organoid pattern of growth, which is composed of vaguely formed nests of spindle tumor cells separated by thin fibrovascular septa. Transitions with areas showing some of the more conventional features of these tumors also may be helpful for diagnosis. The pigmented variant of neuroendocrine carcinoma of the thymus is characterized by deposition of melanin pigment in an intracellular or an extracellular location, raising the possibility of metastasis from a melanocytic neoplasm. 24,25 Neuroendocrine carcinomas with prominent mucinous stroma also have been described in the mediastinum. 26 Such tumors are characterized by prominent stromal deposition of strongly sulfated acid mucopolysaccharides that stain with hyaluronic acid following pretreatment with hyaluronidase, indicating the presence of connective tissue mucin rather than epithelial mucin. Histologically, the tumors show islands, strands, or small clusters of monotonous tumor cells embedded in pools of lightly staining mucinous matrix Image 5. Distinction from a metastatic mucin-secreting (so-called colloid) carcinoma can be extremely difficult and may require the use of appropriate special stains. A histologic variant characterized by a prominent pseudoangiomatous appearance has been described that may be mistaken for a vascular neoplasm. 27 Such tumors show dilated spaces filled with pools of blood reminiscent of cavernous hemangiomas Image 6. Higher magnification, Image 1 Well-differentiated neuroendocrine carcinoma of the thymus showing characteristic organoid pattern (Zellballen) (H&E, 100). Image 2 Well-differentiated neuroendocrine carcinoma of the thymus displaying prominent trabecular pattern of growth (H&E, 100). S19

4 Suster and Moran / NEUROENDOCRINE NEOPLASMS OF THE MEDIASTINUM Image 3 Oncocytic variant of neuroendocrine carcinoma of the thymus showing large cells with abundant granular cytoplasm (H&E, 200). Image 4 Spindle cell neuroendocrine carcinoma of the thymus (H&E, 200). however, reveals round neoplastic cells with the cytologic characteristics of neuroendocrine cells lining the dilated spaces. Another variant is one that closely resembles medullary carcinoma of the thyroid and is characterized by displaying a prominent amyloid-like stroma Image 7. Because calcitonin has been recognized in some cases of neuroendocrine carcinomas of the thymus, such tumors may pose a difficult problem for differential diagnosis from a thyroid primary tumor. Close clinicopathologic correlation to rule out the possibility of a primary tumor in the thyroid is necessary to arrive at a definitive diagnosis in such instances. Moderately Differentiated Thymic Neuroendocrine Carcinoma Although the growth pattern of these tumors may be similar to those of the well-differentiated group, there is a greater tendency to form sheets of tumor cells, and cytologic atypia and necrosis are more prominent. The tumor cells are characterized by increased nuclear size with large, prominent Image 5 Neuroendocrine carcinoma of the thymus with prominent mucinous stroma simulating metastatic mucinsecreting carcinoma (H&E, 200). Image 6 Neuroendocrine carcinoma of the thymus with pseudoangiomatous pattern (H&E, 40). S20

5 Image 7 Neuroendocrine carcinoma of the thymus with amyloid-like stroma simulating medullary carcinoma of thyroid (H&E, 100). Image 8 Moderately differentiated neuroendocrine carcinoma of the thymus showing moderate nuclear atypia and mitotic figures (H&E, 200). nucleoli, coarse chromatin pattern, and frequent mitotic figures (4-10 mitoses per 10 HPF) Image 8. Vascular invasion is also frequent. A characteristic finding is the formation of large balls of tumor cells with central comedo-like areas of necrosis and foci of dystrophic calcification Image 9. These tumor balls frequently display a prominent clefting artifact from the surrounding tumor cells and usually are composed of atypical cells with frequent mitotic figures. Another distinctive feature of these tumors is the formation of small acinar or rosette-like structures with central empty lumens Image 10. Moderately differentiated neuroendocrine carcinomas also frequently show a tendency to grow in a diffuse, sheet-like pattern that may closely resemble a malignant lymphoma Image Attention to the nuclear morphologic features and identification of other areas displaying the more typical neuroendocrine pattern of growth may point toward the correct diagnosis. Image 9 Moderately differentiated neuroendocrine carcinoma of the thymus showing balls of tumor cells with central comedo-like areas of necrosis and foci of dystrophic calcification (H&E, 100). Image 10 Moderately differentiated neuroendocrine carcinoma of the thymus with numerous microacinar, rosette-like structures (H&E, 100). S21

6 Suster and Moran / NEUROENDOCRINE NEOPLASMS OF THE MEDIASTINUM Image 11 Moderately differentiated neuroendocrine carcinoma of the thymus showing diffuse growth pattern reminiscent of malignant lymphoma (H&E, 200). Poorly Differentiated Thymic Neuroendocrine Carcinoma These tumors are defined by their high-grade nuclear features, high mitotic activity, and extensive areas of necrosis. The tumors most often grow as sheets or cords of highly atypical tumor cells with almost total loss of the organoid growth pattern, extensive areas of necrosis, marked cellular atypia, and high mitotic index (>10 mitoses per 10 HPF) Image 12. Tumors in this category essentially overlap and are synonymous with the neuroendocrine or small cell variant of thymic carcinoma. 28 Not all tumors in this category are composed of small round blue cells. A large cell form also has been described. 29 Tumors showing features associated with conventional carcinoids, such as nests, trabeculae, and rosettes, but that already display high-grade nuclear morphologic features, more than 10 mitoses per 10 HPF, and extensive and confluent areas of necrosis also belong in the poorly differentiated neuroendocrine carcinoma category. 20 Tumors showing clear transitions between conventional carcinoid and small cell carcinoma have been well-documented, supporting the premise that all of these lesions are closely related and form part of a continuous spectrum of differentiation Image ,31 The most common manifestation, however, for poorly differentiated neuroendocrine carcinoma of the thymus is that of a small cell (oat cell) carcinoma indistinguishable from those found in the lung and other organs. 28 It should be pointed out, however, that the diagnosis of primary small cell neuroendocrine carcinoma of the thymus is one of exclusion and can rarely be made a priori. The possibility of metastasis from an occult lung primary tumor needs to be ruled out first by clinical, radiographic, and other means. Rare cases of neuroendocrine carcinomas in association with other thymic carcinomas or mesenchymal neoplasms also have been described. 28,32,33 The use of immunohistochemical stains with antibodies against neuroendocrine markers is of great value for confirming the diagnosis of neuroendocrine carcinomas. In general, chromogranin seems to be the most reliable neuroendocrine marker for these tumors. 20 In a recent study Image 12 Poorly differentiated neuroendocrine carcinoma of the thymus, small cell type (H&E, 200). Image 13 Transitions between moderately differentiated neuroendocrine carcinoma and poorly differentiated neuroendocrine carcinoma of the thymus with small cell features (H&E, 100). S22

7 on a large series of cases, we observed positivity for chromogranin in 75% of cases and for synaptophysin in 72%. 20 Not all cases that were positive for chromogranin stained with synaptophysin, and vice versa; only 60% of cases showed both chromogranin and synaptophysin positivity. Thus, we recommended always using both markers in the panel of immunohistochemical stains when looking for the possibility of a neuroendocrine carcinoma. 20 All cases in our study were positive for CAM 5.2 low-molecular-weight cytokeratin (Becton Dickinson, San Jose, CA); broad-spectrum cytokeratin, however, stained only 88% of the cases, and in some tumors, staining was patchy and weak. Leu-7 (CD57), another neuroendocrine-associated marker, was positive in 68% of the tumors. Neuron-specific enolase also has been used successfully for the identification of neuroendocrine tumors of the thymus. 34,35 This marker, however, is not as specific for neuroendocrine cells as is chromogranin and may cross-react with a wide variety of other cell types and tissues (including thymoma), thus limiting its reliability. A variety of other peptides also have been identified in thymic neuroendocrine neoplasms, such as corticotropin, 36 calcitonin, cholecystokinin, gastrin, somatostatin, and beta-endorphin. 31,35,37,38 The latter, however, may be of limited value for diagnosis. Electron microscopic examination may also be very valuable for diagnosis in equivocal cases. Ultrastructural features observed in thymic neuroendocrine tumors include closely apposed cell membranes with immature cell junctions and round, membrane-bound dense-core neurosecretory granules in the cytoplasm. 26,39,40 Neuroendocrine carcinomas of the thymus as a group generally follow an aggressive clinical course. In a recent large study, the overall survival rate was 28% at 5 years and 10% at 10 years; however, biologic behavior was directly related to grade and degree of differentiation. 20 Clinical follow-up in a group of 50 patients in that study showed that 32% of patients with low-grade (well-differentiated) carcinoma died of tumor, as did 48% with intermediate-grade (moderately differentiated) carcinoma and 91% with highgrade (poorly differentiated) carcinoma. Recurrences were documented in 18 of 50 patients and metastases in 20. The most frequent metastatic sites (in decreasing order) were regional lymph nodes, lungs, bone, esophagus, chest wall, and liver. Metastases sometimes can occur after a long disease-free interval. Complete excision is probably the best treatment of choice for neuroendocrine carcinoma of the thymus. 41 The roles of radiation and chemotherapy in the treatment of these tumors has not been well defined. Some studies seem to indicate that these tumors may not be radiosensitive. 9 The role of chemotherapy also remains to be more clearly elucidated. High-grade, poorly differentiated neuroendocrine carcinomas of the thymus, particularly of the small cell type, are refractory to any form of therapy and usually follow an extremely aggressive clinical course with a median survival of 15 months irrespective of the modality of treatment. 28 Mediastinal Paraganglioma Paragangliomas originate from aorticopulmonary paraganglia, a specialized type of neural crest cell associated with autonomic ganglia, which are distributed in the superior and middle mediastinum or in aorticosympathetic paraganglia in the posterior mediastinum. 42 Some paraganglia in aorticopulmonary areas have a chemoreceptor function, hence the term chemodectoma sometimes applied to these tumors in the older literature. Mediastinal paragangliomas are extremely rare neoplasms that account for fewer than 10% of all mediastinal neuroendocrine tumors. 43 Some authors divide paragangliomas based on their location within the mediastinum and seem to believe that significant clinical differences exist between those arising from the distribution of aortic bodies in the anterior and middle mediastinum ( aortic body paragangliomas) and those in the posterior compartment ( paravertebral paragangliomas). Thus, aortic body paragangliomas have been found to occur in older people (mean age, 46 years), are rarely functional, and may be associated with aggressive behavior and metastases in up to 15% of cases, whereas paravertebral paragangliomas tend to occur in younger people (mean age, 29 years), may be functional in up to half of cases, and will have a tendency to show an indolent behavior Because morphologically the 2 types are indistinguishable and clinical behavior is more often a function of size and symptoms rather than location, this distinction may be of limited practical value. Paragangliomas arising in the anterior and middle mediastinum are more often asymptomatic and discovered incidentally on routine chest radiographs. 43,45,46 Symptoms, when present, such as cough, chest pain, and shortness of breath, are associated with compression of local structures due to large growth of the tumor. 43 Paragangliomas arising in the posterior mediastinum frequently manifest with symptoms related to release of catecholamines by the tumor, such as sweating, headaches, tachycardia, palpitations, dyspnea, nausea, and hypertension. 45 The symptoms usually disappear following removal of the tumor. Functioning mediastinal paragangliomas may occur as part of Carney syndrome (together with epithelioid gastric stromal sarcoma and pulmonary chondroma). 47,48 Paragangliomas may be multiple. About 10% of patients with mediastinal paraganglioma have similar tumors at other body sites such as the head and neck or retroperitoneum. In the study by Gallivan et al, 45 23% of patients with paravertebral paraganglioma had associated multiple tumors, S23

8 Suster and Moran / NEUROENDOCRINE NEOPLASMS OF THE MEDIASTINUM including extra-adrenal abdominal paraganglioma, carotid body paraganglioma, and pheochromocytoma. Making the distinction between a multifocal paraganglioma and a metastasis may be quite difficult. In general, when the tumors are found in locations where extra-adrenal paragangliomas are frequently encountered, they are assumed to represent separate primary tumors rather than metastases. Gross examination reveals that paragangliomas tend to be well-circumscribed, lobulated masses that range from 2 to 12 cm in greatest diameter. The larger tumors tend to be invasive and may be firmly attached to adjacent structures, making complete surgical removal difficult. The cut section usually shows soft, homogeneous, tan-white tissue with focal areas of hemorrhage, but rarely displays evidence of necrosis. Paragangliomas are characterized by a well-developed neuroendocrine (organoid) pattern of growth. The tumor cells grow forming discrete nests or Zellballen that are separated by well-formed fibrovascular septa Image 14. Unlike other low-grade neuroendocrine neoplasms, paragangliomas are characterized at the cytologic level by a more pronounced degree of atypia, with enlarged nuclei and prominent nucleoli. In fact, a distinguishing feature of paraganglioma is the presence of nucleomegaly with often bizarre, multinucleated tumor cells, in the absence of significant mitotic activity or other features of malignancy. 43 Mitoses are usually sparse, and atypical mitoses are seen rarely. The cells may be of 2 types: (1) clear cells characterized by abundant optically clear cytoplasm and (2) eosinophilic cells that contain abundant lightly eosinophilic cytoplasm Image 15. The tumor may be composed of a Image 14 Mediastinal paraganglioma showing prominent organoid pattern (Zellballen) with focal cytomegaly (H&E, 200). single cell type; more often, admixtures of the two can be observed within a single tumor. Unusual histologic variants of mediastinal paraganglioma include tumors with cells displaying abundant oncocytic granular cytoplasm, tumors with prominent spindling of the cells, and pigmented paragangliomas. 43,49 The main differential diagnosis for these tumors is with well-differentiated neuroendocrine carcinoma of the thymus (thymic carcinoid). Unlike the latter, paragangliomas do not form ribbons or festoons, nor do they display a microacinar or rosette-like growth pattern. In addition, paragangliomas seldom display the degree of cytologic atypia, mitotic activity, or necrosis commonly associated with thymic carcinoids. Histochemical stains can be useful in the diagnosis of mediastinal paraganglioma. The modified Grimelius stain usually brings out the argyrophilic neurosecretory granules in the cytoplasm. Periodic acid Schiff stains are usually negative in the tumor cells. Immunohistochemical stains also can be of great value for the diagnosis of these tumors. Neuroendocrine markers, such as chromogranin, synaptophysin, and neuron-specific enolase, are usually positive in the tumor cells. 42,43 Immunoreactivity for vimentin, corticotropin, glucagon, somatostatin, and calcitonin also has been described. 50 S-100 protein stains usually will highlight a distinct population of sustentacular cells surrounding the nests of tumor cells Image A very important feature of mediastinal paraganglioma is the complete absence of reactivity for low-molecular-weight cytokeratin (such as CAM 5.2). 43 The latter feature may serve as a helpful clue to the differential diagnosis from thymic carcinoid in equivocal cases. At the ultrastructural level, the tumors are characterized by the presence of numerous dense-core neurosecretory granules. The granules tend to be larger than those seen in carcinoid tumors and show marked variation in their size and shape, sometimes assuming a dumbbell configuration. 40,42,46,51 Mediastinal paragangliomas as a group behave as very low-grade, indolent neoplasms. Approximately 10% of cases are associated with metastases. The most significant prognostic factor for the evaluation of clinical behavior in these tumors is the staging at the time of diagnosis. In a study by Moran et al, 43 tumors that were invasive at the time of diagnosis were the only ones associated with aggressive clinical behavior. Invasive tumors tended to also be associated with evidence of vascular invasion; however, histologic features in general (eg, atypia, mitoses) showed no correlation with prognosis. In a review of the literature of posterior mediastinal paragangliomas, local invasion and metastases also were shown to represent the most significant factors associated with aggressive behavior. 52 The most common S24

9 A B Image 15 A, Mediastinal paraganglioma composed of clear cells. B, Mediastinal paraganglioma composed of eosinophilic cells. (H&E, 200) metastatic sites include bone, lung, and lymph nodes Complete surgical excision is the treatment of choice for these tumors. Ectopic Parathyroid Tumors Ectopic parathyroid adenomas may be present in the mediastinum in about 15% of cases of hyperparathyroidism. 53,54 The majority are located in the anterosuperior mediastinum, in proximity to or within the thymus. Most of Image 16 Mediastinal paraganglioma. S-100 protein stain highlights a population of sustentacular cells surrounding the cell nests ( 100). these tumors are believed to arise from the inferior parathyroid glands, which develop in close association with the thymus during embryogenesis. However, about 20% may originate from supernumerary parathyroid glands. 55,56 Parathyroid adenomas of the mediastinum occur in patients between 40 and 70 years of age and show a female predilection (male/female ratio, 1:3). 54 Patients usually have symptoms of hyperparathyroidism, including skeletal abnormalities, renal stones, peptic ulcer, pancreatitis, mental changes, and hypercalcemia; however, rare nonfunctional cases also have been described. 57 Histologically, mediastinal parathyroid adenomas are indistinguishable from their head and neck counterparts. The tumors are composed of sheets of monotonous round or polygonal tumor cells with small central nuclei surrounded by abundant lightly eosinophilic cytoplasm Image 17. An admixture of clear cells with smaller chief cells or oxyphilic cells is frequently present. Some tumors may display focal nucleomegaly with very large, hyperchromatic cells; however, mitotic activity will be absent or inconspicuous. The tumors are usually surrounded by a fibrous capsule, and scanning magnification will show a nodular or acinar pattern. Occasional tumors may show a prominent mature adipose tissue component; such tumors have been designated as lipoadenoma. 58 Rare cases of parathyroid carcinomas ectopically arising in the anterior mediastinum also have been described. 57,59 Numerous mitoses, capsular penetration, and vascular invasion are features associated with malignancy in such lesions. The differential diagnosis for these tumors includes neuroendocrine carcinoma of the thymus, paraganglioma, clear cell thymic carcinoma, and metastases from clear cell S25

10 Suster and Moran / NEUROENDOCRINE NEOPLASMS OF THE MEDIASTINUM Image 17 Mediastinal parathyroid adenoma (H&E, 40). carcinomas of internal organs. Since most of these tumors are associated with functional hyperparathyroidism and are encountered during the course of exploration for parathyroid adenoma, there are seldom difficulties associated with their histologic diagnosis. Problems may arise, however, with nonsecretory tumors. Immunohistochemical stains for parathyroid hormone may be of help for determining a definitive diagnosis in such instances. 57 From the Departments of Pathology, 1 The Ohio State University, Columbus, OH, and the 2 University of Alabama at Birmingham. Address reprint requests to Dr Suster: Dept of Pathology, The Ohio State University, E-411 Doan Hall, 410 W 10th Ave, Columbus, OH References 1. Klemm KM, Moran CA. Primary neuroendocrine carcinomas of the thymus. Semin Diagn Pathol. 1999;16: Rosai J, Higa E. Mediastinal endocrine neoplasm of probably thymic origin related to carcinoid tumor. Cancer. 1972; 29: Rosai J, Higa E, Davie J. Mediastinal endocrine neoplasm in patients with multiple endocrine adenomatosis: a previously unrecognized association. Cancer. 1972;29: Duh QY, Hybarger CP, Geist R, et al. Carcinoids associated with multiple endocrine neoplasia syndromes. Am J Surg. 1987;154: Viebahn R, Hiddemann W, Klinke F, et al. Thymus carcinoid. Pathol Res Pract. 1985;180: Manes JL, Taylor HB. Thymic carcinoid in familial multiple endocrine adenomatosis. Arch Pathol Lab Med. 1976;100: Marchevsky AM, Dikman SH. Mediastinal carcinoid with an incomplete Sipple s syndrome. Cancer. 1979;43: Floros D, Dosios T, Tsourdis A, et al. Carcinoid tumor of the thymus with multiple endocrine adenomatosis. Pathol Res Pract. 1982;175: Lowenthal RM, Gumpel JM, Kreel L, et al. Carcinoid tumor of the thymus with systemic manifestations: a radiological and pathological study. Thorax. 1974;92: Lokich JJ, Li F. Carcinoid of the thymus with hereditary hyperparathyroidism. Ann Intern Med. 1978;89: Wick MR, Rosai J. Neuroendocrine neoplasms of the thymus. Pathol Res Pract. 1988;183: Wick MR, Scott RE, Li YC, et al. Carcinoid tumor of the thymus: a clinicopathologic report of seven cases with a review of the literature. Mayo Clin Proc. 1980;55: Brown LR, Aughenbaugh GL, Wick MR, et al. Roentgenologic diagnosis of primary corticotropin-producing carcinoid tumors of the mediastinum. Radiology. 1982;142: Obendorfer S. Karzinoide Tumoren des Duenndarns. Frankfurt Z Pathol. 1907;1: Gosset A, Masson P. Tumeurs endocrines de l appendice. Presse Med. 1914;22: Valli M, Fabris GA, Dewar A, et al. Atypical carcinoid tumour of the thymus: a study of 8 cases. Histopathology. 1994;24: Arrigoni MG, Woolner LB, Bernatz PE. Atypical carcinoid tumors of the lung. J Thorac Cardiovasc Surg. 1972;64: Rosai J, Levine G, Weber R, et al. Carcinoid tumors and oat cell carcinomas of the thymus. Pathol Annu. 1977;2: Montpreville VT, Machiarini P, Dulmet E. Thymic neuroendocrine carcinoma (carcinoid): a clinicopathologic study of 14 cases. J Thorac Cardiovasc Surg. 1996;111: Moran CA, Suster S. Neuroendocrine carcinoma (carcinoid tumor) of the thymus: a clinicopathologic analysis of 80 cases. Am J Clin Pathol. 2000;114: Moran CA, Suster S. Primary neuroendocrine carcinoma (carcinoid) of the thymus with prominent oncocytic features: clinicopathologic study of 22 cases. Mod Pathol. 2000;13: Moran CA, Suster S. Spindle cell neuroendocrine carcinomas of the thymus (spindle cell thymic carcinoid): a clinicopathologic and immunohistochemical study of seven cases. Mod Pathol. 1999;12: Levine GD, Rosai J. A spindle cell variant of thymic carcinoid tumor. Arch Pathol Lab Med. 1976;100: Lagrange W, Dahm H-H, Karstens J, et al. Melanocytic neuroendocrine carcinoma of the thymus. Cancer. 1987;59: Klemm KM, Moran CA, Suster S. Pigmented thymic carcinoids: a clinicopathological and immunohistochemical study of two cases. Mod Pathol. 1999;12: Suster S, Moran CA. Thymic carcinoid with prominent mucinous stroma: report of a distinctive morphologic variant of thymic neuroendocrine neoplasm. Am J Surg Pathol. 1995;19: Moran CA, Suster S. Angiomatous neuroendocrine carcinoma of the thymus: report of a distinctive morphological variant of neuroendocrine tumor of the thymus resembling a vascular neoplasm. Hum Pathol. 1999;30: Suster S, Rosai J. Thymic carcinoma: clinicopathologic study of 60 cases. Cancer. 1991;67: S26

11 29. Chetty R, Batitang S, Govender D. Large cell neuroendocrine carcinoma of the thymus. Histopathology. 1997;11: Moran CA, Suster S. Thymic neuroendocrine carcinomas with combined features ranging from well-differentiated (carcinoid) to small cell carcinoma: a clinicopathologic and immunohistochemical study of 11 cases. Am J Clin Pathol. 2000;113: Wick MR, Scheithauer BW. Oat-cell carcinoma of the thymus. Cancer. 1982;49: Kuo TT. Carcinoid tumor of the thymus with divergent sarcomatoid differentiation: report of a case with histogenetic considerations. Hum Pathol. 1994;25: Snover DC, Levine GD, Rosai J. Thymic carcinoma: five distinctive histological variants. Am J Surg Pathol. 1982;6: Wick MR, Scheithauer BW, Kovacs K. Neuron-specific enolase in neuroendocrine tumors of the thymus, bronchus and skin. Am J Clin Pathol. 1983;79: Herbst WM, Kummer W, Hofmann W, et al. Carcinoid tumors of the thymus: an immunohistochemical study. Cancer. 1987;60: Wick MR, Carney JA, Bernatz PE, et al. Primary mediastinal carcinoid tumors. Am J Surg Pathol. 1982;6: Pullan PT, Clement-Jones V, Corder R, et al. Ectopic production of methionine enkephalin and beta-endorphin. Br Med J. 1980;280: DeLellis RA, Wolfe HJ. Calcitonin in spindle cell thymic carcinoid tumors [letter]. Arch Pathol Lab Med. 1976;100: Wick MR, Scheithauer BW. Thymic carcinoid: a histologic, immunohistochemical and ultrastructural study of 12 cases. Cancer. 1984;53: Wick MR, Rosai J. Neuroendocrine neoplasms of the mediastinum. Semin Diagn Pathol. 1991;8: Economopoulus GC, Lewis JW Jr, Lee MW, et al. Carcinoid tumors of the thymus. Ann Thorac Surg. 1990;50: Kliewer KE, Cochran AJ. A review of the histology, ultrastructure, immunohistology and molecular biology of extra-adrenal paragangliomas. Arch Pathol Lab Med. 1989;113: Moran CA, Suster S, Fishback N, et al. Mediastinal paragangliomas: a clinicopathologic and immunohistochemical study of 16 cases. Cancer. 1993;72: Olson JL, Salyer WR. Mediastinal paragangliomas (aortic body tumor): a report of four cases and a review of the literature. Cancer. 1978;41: Gallivan MVE, Chun B, Rowden G, et al. Intrathoracic paravertebral malignant paraganglioma. Arch Pathol Lab Med. 1980;104: Lack EE, Stillinger RA, Colvin DB, et al. Aortico-pulmonary paraganglioma: report of a case with ultrastructural study and review of the literature. Cancer. 1979;43: Herrera MF, van Heerden JA, Puga FJ, et al. Mediastinal paraganglioma: a surgical experience. Ann Thorac Surg. 1993;56: Carney JA. The triad of gastric epithelioid leiomyosarcoma, functioning extraadrenal paraganglioma, and pulmonary chondroma. Cancer. 1979;43: Moran CA, Albores-Saavedra J, Wenig B, et al. Pigmented extraadrenal paragangliomas: a clinicopathologic and immunohistochemical study of five cases. Cancer. 1997;79: Assaf HM, Al-Momen AA, Martin JG. Aorticopulmonary paraganglioma: a case report with immunohistochemical studies and literature review. Arch Pathol Lab Med. 1992;116: Kliewer KF, Wen D-R, Cancilla PA, et al. Paragangliomas: assessment of prognosis by histologic, immunohistochemical, and ultrastructural techniques. Hum Pathol. 1989;20: Odze R, Begin LR. Malignant paraganglioma of the posterior mediastinum: a case report and review of the literature. Cancer. 1990;65: Conn JM, Goncalves MA, Mansour KA, et al. The mediastinal parathyroid. Am Surg. 1991;57: Nathaniels EK, Nathaniels AM, Wang CA. Mediastinal parathyroid tumors: a clinical and pathological study of 84 cases. Ann Surg. 1970;171: Russel CF, Edis AJ, Scholz DA, et al. Mediastinal parathyroid tumors: experience with 38 tumors requiring mediastinotomy for removal. Ann Surg. 1981;193: Wang C, Mahaffey JE, Axelrod L, et al. Hyperfunctioning supernumerary parathyroid glands. Surg Gynecol Obstet. 1979;148: Murphy MN, Glennon PG, Diocee MS, et al. Nonsecretory parathyroid carcinoma of the mediastinum: light microscopic, immunocytochemical and ultrastructural features of a case, and review of the literature. Cancer. 1986;58: Wolff M, Goodman EN. Functioning lipoadenoma of a supernumerary parathyroid. Head Neck Surg. 1980;2: Putnam JB, Schantz SP, Pugh WC, et al. Extended en bloc resection of a primary mediastinal parathyroid carcinoma. Ann Thorac Surg. 1990;50: S27

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