Neuroendocrine Carcinomas (Carcinoid Tumor) of the Testis A Clinicopathologic and Immunohistochemical Study of Ten Cases
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1 Anatomic Pathology / NEUROENDOCRINE CARCINOMAS OF THE TESTIS Neuroendocrine Carcinomas (Carcinoid Tumor) of the Testis A Clinicopathologic and Immunohistochemical Study of Ten Cases Adriana Reyes, MD, 1 Cesar A. Moran, MD, 1 Saul Suster, MD, 2 Michal Michal, MD, 3 and Hugo Dominguez, MD 4 Key Words: Carcinoid; Testis; Neuroendocrine; Carcinoma; Immunohistochemistry Abstract We studied 10 cases of primary pure testicular neuroendocrine carcinoma. Patients were between 16 and 48 years old and had testicular swelling with pain or a painless testicular mass and no history of neuroendocrine carcinoma or other malignant neoplasm. All underwent orchiectomy. The tumors were low (n = 9) and intermediate (n = 1) grades with a variegated histologic appearance characterized by a nesting pattern, cords of neoplastic cells with rosettes, or sheets of neoplastic cells. Mitotic activity was lacking in 9 cases. In 1 case, mitotic figures ranged from 7 to 8 per 10 high-power fields, and cellular atypia and comedo-like necrosis were present. Immunohistochemical studies using a keratin cocktail, chromogranin, synaptophysin, epidermal growth factor, p53, placentallike alkaline phosphatase, and CD117 (c-kit) were performed in all cases. Keratin, chromogranin, and synaptophysin were positive in all tumors. Clinical follow-up information was obtained for 6 patients (range, months): 5 with low-grade tumors were alive 24 to 60 months after diagnosis; 1 with an intermediate-grade tumor died of tumor 12 months after initial diagnosis. The behavior of these tumors, while in the testicular region, correlates well with the histologic grade. We propose replacing the term testicular carcinoid with neuroendocrine carcinoma, which better reflects the nature of these neoplasms. Neuroendocrine neoplasms of the testis are unusual tumors, which are represented mainly by carcinoid tumors. It has been estimated that testicular carcinoid tumors represent no more than 1% of all testicular tumors. 1 The current terminology and criteria for diagnosis have been drawn essentially from the criteria established for similar tumors in the respiratory tract, namely the lung. However, the diagnostic criteria to classify these neoplasms have been revised during the last few years. 2 Even though neuroendocrine neoplasms (carcinoids) represent a small group of testicular tumors, the course that these tumors follow may be indolent or aggressive. Thus, it is important to separate them into low- and intermediate-grade tumors. The cases presented herein constitute the largest series of these neoplasms and highlight the importance of careful histologic study and differentiating them from other more common testicular tumors. Based on our experience, we consider that the designation neuroendocrine carcinoma is justified for these tumors. Materials and Methods Ten cases of primary pure testicular neuroendocrine carcinomas (carcinoid) represent the basis of this report. The cases were identified from the files of the departments of pathology at M.D. Anderson Cancer Center, Houston, TX; the Ohio State University, Columbus; Pilsen, Czech Republic; and the Cancer Institute of Mexico, Mexico City, during the previous 10 years (none of the cases presented herein has been reported previously). H&E-stained sections were available for review for all cases studied. The tumors 182 Am J Clin Pathol 2003;120: Downloaded 182 from
2 Anatomic Pathology / ORIGINAL ARTICLE were separated into 2 groups according to the following morphologic criteria: (1) low-grade (well-differentiated) neuroendocrine carcinoma: mitotic figures, fewer than 3 per 10 high-power fields (HPF), mild cellular atypia, including nuclear enlargement with prominent nucleoli; (2) intermediate-grade (moderately differentiated) neuroendocrine carcinoma: mitotic figures, more than 3 per 10 HPF, prominent necrosis, moderate cellular atypia, including nuclear enlargement with prominent nucleoli, and an abnormal nuclear/ cytoplasmic ratio. The scheme followed in separating these tumors into low- and intermediate-grade categories is the one proposed by the World Health Organization for the classification of carcinoid tumors in the lung. 2 For immunohistochemical studies, representative formalin-fixed, paraffin-embedded tissue sections were available for all 10 cases. Thin sections were incubated with antibodies against a broad-spectrum keratin cocktail (DAKO, Carpinteria, CA), chromogranin (dilution, 1:4,000; Chemicon, Temecula, CA), synaptophysin (dilution, 1:50; BioGenex, San Ramon, CA), epidermal growth factor receptor (EGFR; dilution, 1:50; Zymed, San Francisco, CA), p53 (dilution, 1:100; DAKO), placental-like alkaline phosphatase (PLAP; dilution, 1:25; Neomarkers, Fremont, CA), and CD117 (c-kit; dilution, 1:100; DAKO) by the avidinbiotin peroxidase complex technique. Nonimmune rabbit and mouse serum were substituted for negative controls. Appropriate positive tissue controls were run concurrently. For clinical follow-up, all clinical charts were reviewed and physicians contacted. Results Clinical Features The patients were 10 males aged 16 to 48 years (mean age, 39.5 years) who sought care because of tender swelling of the testicle (4 patients) or because of a painless mass of the testicle (6 patients). The tumor was located in the right testicle in 6 patients and in the left testicle in 4 patients. None of the patients had a history of neuroendocrine tumor elsewhere, nor did they show paraneoplastic syndrome. All patients underwent orchiectomy. According to the American Joint Committee on Cancer classification, all the patients were in stage IA Table 1. Gross Features The tumors were described as solid, light brown to tan, and well circumscribed but not encapsulated. The cut surface was homogeneous, light brown Image 1. In 1 case, focal areas of necrosis and hemorrhage were seen. The tumors measured from 2.0 to 4.8 cm in greatest dimension. Histopathologic Features The tumors were divided according to their histopathologic features into 2 categories: low-grade (well-differentiated) and intermediate-grade (moderately differentiated) tumors. Low-Grade (Well-Differentiated) Neuroendocrine Carcinoma The low-power magnification showed well-defined tumors obliterating normal testicular parenchyma. Even though the tumors were well defined, none showed encapsulation Image 2. The neoplastic cells were arranged in a prominent nesting pattern separated by thin, fibroconnective tissue Image 3. At higher magnification, the tumor cells showed pale eosinophilic cytoplasm with round to oval nuclei and inconspicuous nucleoli Image 4. Rosettes were seen commonly. In 2 cases, low-power magnification revealed a pseudoglandular pattern composed of ribbons of cells forming gland-like structures Image 5. Higher magnification showed similar characteristics, namely cells with pale eosinophilic cytoplasm, round to oval nuclei, and inconspicuous nucleoli. None of the cases showed mitotic activity, areas of necrosis, or Table 1 Clinical Features of Ten Patients With Primary Neuroendocrine Carcinomas (Carcinoids) of the Testis Keratin, p53, Histologic Chromogranin, EGFR, c-kit, Case No./Age (y) Clinical History Tumor Size (cm) Grade and Synaptophysin and PLAP Follow-up 1/44 Painless mass, right testicle 2.1 Low + Alive and well, 5 y 2/16 Tender swelling, right testicle 4.5 Low + Alive and well, 5 y 3/42 Painless mass, left testicle 3.2 Low + Lost to follow-up 4/48 Tender swelling, right testicle 4.0 Intermediate + Died, 1 y 5/39 Painless mass, right testicle 3.5 Low + Alive and well, 2 y 6/43 Painless mass, right testicle 3.0 Low + Lost to follow-up 7/40 Painless mass, right testicle 4.1 Low + Alive and well, 2 y 8/37 Painless mass, left testicle 3.5 Low + Alive and well, 2 y 9/41 Tender swelling, left testicle 2.0 Low + Lost to follow-up 10/45 Tender swelling, left testicle 2.0 Low + Lost to follow-up EGFR, epidermal growth factor receptor; PLAP, placental-like alkaline phosphatase. Downloaded from Am J Clin Pathol 2003;120:
3 Reyes et al / NEUROENDOCRINE CARCINOMAS OF THE TESTIS Image 1 Gross specimen of a testicle containing a welldemarcated but not encapsulated tumor. The tumor shows a homogeneous surface without necrosis or hemorrhage. Image 2 Neuroendocrine carcinoma of the testicle showing a well-demarcated tumor mass. No evidence of intratubular germ cell neoplasia is present (H&E, 25). Image 3 Testicular neuroendocrine carcinoma showing the characteristic nesting pattern (H&E, 60). Image 4 Higher magnification of a neuroendocrine carcinoma of the testicle showing a cellular proliferation characterized by bland nuclei without evidence of marked cytologic atypia or mitotic activity (H&E, 75). hemorrhage. In 1 case, focal areas of microcalcifications were present. No evidence of vascular invasion or intratubular germ cell neoplasia was identified in any of the cases. Intermediate-Grade (Moderately Differentiated) Neuroendocrine Carcinoma One case was categorized as belonging to this histologic grade. At low power, the tumor was shown as well circumscribed; however, in addition to nesting areas, tumor cells were displayed in a more haphazard arrangement. At higher magnification, areas of comedo-like necrosis were found easily, cellular atypia (nuclear irregularity, prominent nucleoli, and nuclear pleomorphism) was prominent, and mitotic figures were encountered in a range from 7 to 8 per 10 HPF Image 6. No evidence of vascular invasion or intratubular germ cell neoplasia was identified. Immunohistochemical Features The 10 cases were studied using a panel of antibodies on formalin-fixed, paraffin-embedded tissue samples, including a 184 Am J Clin Pathol 2003;120: Downloaded 184 from
4 Anatomic Pathology / ORIGINAL ARTICLE years). Five patients were alive and well 2 to 5 years after surgery (low-grade tumors), while 1 patient (with intermediate-grade neuroendocrine carcinoma) died of tumor within 1 year after surgery. No autopsy was performed to assess metastatic disease. Four patients were lost to follow-up. Discussion Image 5 Testicular neuroendocrine carcinoma showing a pseudoglandular growth pattern (H&E, 60). broad-spectrum keratin cocktail, chromogranin, synaptophysin, p53, EGFR, PLAP, and CD117. Results for the keratin cocktail, chromogranin, and synaptophysin were positive in all cases, while p53, EGFR, PLAP, and CD117 were negative. The positive staining for neuroendocrine markers was strong and diffuse in all tumors. In addition, histochemical stains for periodic acid Schiff with and without diastase and mucicarmine were negative for the presence of intracellular mucin. Clinical Follow-up Clinical information was obtained for 6 patients (60%), with follow-up ranging from 1 to 5 years (mean follow-up, 3 Obendorfer and Frankfurt 3 introduced the term carcinoid in 1907 to separate a group of tumors in the small intestine that behave less aggressively than conventional carcinomas. Years later, Gosset and Masson 4 suggested that these tumors derived from Kulchitsky cells by demonstrating argentaffin granules in the cells. Williams and Sandler 5 presented their classification based on embryologic divisions of the gut and divided them into foregut, midgut, and hindgut with their specific hormonal association. However, controversy has always existed regarding the best way to predict prognosis. In 1972, Arrigoni et al 6 introduced the term atypical carcinoid to designate a group of tumors characterized by increased mitotic activity in the presence of a recognizable carcinoid pattern (1 mitosis per 1-2 HPF = 5-10 mitoses per 10 HPF), pleomorphism, and irregularity of the nuclei with prominent nucleoli, hyperchromatism, increased cellularity with disorganization of the architecture, and tumor necrosis. Despite these criteria for atypical carcinoid, numerous publications on the subject have used different histopathologic criteria, which have confused the proper classification of these neoplasms. More recently, the histopathologic criteria for the diagnosis of atypical carcinoid have changed, namely in the mitotic count, which has been lowered to more than 2 per 10 HPF. 2 A B Image 6 A, Moderately differentiated neuroendocrine carcinoma of the testicle showing prominent comedo-like necrosis (H&E, 60). B, Moderately differentiated neuroendocrine carcinoma showing nuclear atypia and mitotic activity (H&E, 75). Downloaded from Am J Clin Pathol 2003;120:
5 Reyes et al / NEUROENDOCRINE CARCINOMAS OF THE TESTIS While the vast majority of neuroendocrine carcinomas (carcinoids) occur in the intestine, current nomenclatures have been made by assessing pulmonary neoplasms. Interestingly, owing to the rarity of these tumors in the genitourinary system, namely the testicle, it has been difficult to analyze these tumors using more modern classifications. Neuroendocrine carcinomas in the testicular region have been recognized for some time in the literature; however, for the most part, reports have been of single cases Thus, it is difficult to determine from the literature whether the tumors described can be categorized today as well-differentiated or moderately differentiated tumors. Clinically, the cases presented herein shared some similarities with those previously described in the literature. The age group in our cases spans from young males to adults (mean age, 39.5 years). The patients may have a painless tumor mass, tender swelling of the testicle, or other symptoms, including carcinoid syndrome. In our cases, none of the patients had an associated carcinoid syndrome. All patients have undergone orchiectomy. In about 10% of the cases, metastatic disease has been described. It has been stated that testicular neuroendocrine tumors may be encountered in 3 clinical settings: (1) as a component of a teratomatous tumor, (2) as a metastatic lesion, and (3) as a de novo neuroendocrine neoplasm. The first 2 clinical settings are relatively easy to explain; however, the third is a challenge because the presence of neuroendocrine cells or Kulchitsky cells has not been described in the testicle. One is left to assume that there may be neuroendocrine rests that in due time are capable of forming a tumor mass. Berdjis and Mostofi 34 in 1977 presented a series of 10 cases of what they called carcinoid tumors of the testis; 2 of the patients died in a period of 4 to 6 years. Although one of them had clinically evident metastatic disease to the posterior abdominal wall, no autopsy was performed on either patient. On the other hand, in at least 2 of the cases described, the gross description casts some doubt about whether the tumors were pure neuroendocrine carcinomas. One tumor was described as a seminecrotic mass and the other as a hard cartilaginous mass (cases 1 and 2). It is possible that both of these cases may have been part of a teratomatous tumor. Both patients received radiation therapy. One survived for 16 years, while no follow-up was recorded for the second case. Nevertheless, it is apparent that at least 20% of the tumors in that series of cases followed an aggressive course. Unfortunately, the microscopic description for the cases was not sufficiently detailed to assign the cases to a low- or an intermediate-grade category. In a more recent article, Zavala-Pompa et al 35 described 3 cases, including a case previously recorded in the literature. Two of the cases described can be categorized as low-grade (well-differentiated) tumors, while 1 case likely corresponds to an intermediate-grade (moderately differentiated) tumor. Unfortunately, for the latter case, no meaningful follow-up was obtained to assess tumor behavior. In some respects, our cases share features similar to those reported in the literature. However, when we used current criteria to separate these tumors into low and intermediate grades of malignancy, we noted an important difference. In 1 of our cases, which was categorized as intermediate grade, the patient died within 1 year after surgery, while in 5 additional patients in whom the tumor was categorized as low grade, the behavior was that of a low-grade neoplasm (patients alive and well 2-4 years later). We can safely assume that current criteria to separate neuroendocrine tumors seem to correlate with clinical behavior. In our experience, 1 case had a fatal outcome (10% of the 10 cases studied). On the other hand, our immunohistochemical results correlate with the neuroendocrine nature of the neoplasm by showing a strong, diffuse, positive reaction for neuroendocrine markers such as chromogranin and synaptophysin. None of our cases showed a positive reaction for other markers, which have been used to predict behavior (p53, CD117, EGFR). In regard to the treatment of these tumors, it seems that for the low-grade tumors, surgical resection in the form of orchiectomy with close follow-up is the treatment of choice. Whether patients with intermediate-grade tumors should receive additional therapy remains a choice based on an individual clinical analysis, which also should include clinical staging. We did not identify any cases of high-grade neuroendocrine carcinoma with either small cell or large cell histologic features. Although theoretically, pure high-grade neuroendocrine carcinoma (small cell carcinoma or large cell neuroendocrine carcinoma) may occur as a primary testicular tumor, we did not find examples of such cases, nor are we aware of such descriptions in the literature. Nevertheless, as we noted earlier, metastatic tumors, namely metastatic small cell carcinomas to the testis, have been reported. 36 Although the diagnosis of neuroendocrine carcinoma in the testis is rather straightforward, there are some testicular tumors that may enter into the differential diagnosis. Sertoli cell tumors at low-power magnification may give a neuroendocrine-like pattern; however, these tumors would not show positive staining for neuroendocrine markers. Another tumor that may pose a problem is granulosa cell tumor. In this setting, the presence of Call-Exner bodies may be confused with rosette formation. Interestingly, 2 of the cases described herein initially were misinterpreted as those particular entities. Once again, the use of immunohistochemical studies, including neuroendocrine markers, will lead to the correct interpretation. We have presented 10 cases of primary testicular neuroendocrine carcinomas. We believe that the term carcinoid should be abandoned and that these tumors should be 186 Am J Clin Pathol 2003;120: Downloaded 186 from
6 Anatomic Pathology / ORIGINAL ARTICLE divided into specific grades of histologic differentiation. In our experience and in that reported in the literature, in at least 10% of the patients, the tumor followed an aggressive course. The use of immunohistochemical studies may be helpful in difficult cases in which one needs to separate these tumors from other more common testicular neoplasms. Neuroendocrine carcinomas should be included in the differential diagnosis of testicular tumors. From the Departments of Pathology, 1 M.D. Anderson Cancer Center, Houston, TX; 2 Ohio State University, Columbus; 3 Pilsen, Czech Republic; and 4 Cancer Institute of Mexico, Mexico City. Address reprint requests to Dr Moran: Dept of Pathology, M.D. Anderson Cancer Center, Box 85, Houston, TX References 1. Ulbright TM, Amin MB, Young RH. Tumors of the Testis, Adnexa, Spermatic Cord, and Scrotum. Washington, DC: Armed Forces Institute of Pathology; 1999:161. 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Primary carcinoid tumor of the testis: case report, ultrastructure and review of the literature. Cancer. 1978;42: Magyar E, Talerman A. Primary carcinoid tumor of testis. Urology. 1977;6: Weitzner S, Robison JR. Primary carcinoid of testis. J Urol. 1976;116: Saxena A, Watkin SW. Bilateral malignant testicular carcinoid. Br J Urol. 1990;65: Umeda T, Tokuda H, Hara T, et al. Primary testicular carcinoid tumor in a 19-year-old boy. Eur Urol. 1987;13: Bates RJ, Perrone TL, Parkhurst EC. Insular carcinoid arising in a mature teratoma of the testis. J Urol. 1981;126: Ordoñez NG, Ayala AG, Sneige N, et al. Immunohistochemical demonstration of multiple neurohormonal polypeptides in a case of pure testicular carcinoid. Am J Clin Pathol. 1982;78: Finci R, Gunhan O, Celasun B, et al. Carcinoid tumor of undescended testis. J Urol. 1987;137: Terhune DW, Manson AL, Jordon GH, et al. Pure primary testicular carcinoid: a case report and discussion. J Urol. 1988;139: Walker AN, White CR, Erickson DJ, et al. Primary carcinoid tumor of the testis. South Med J. 1988;81: Sullivan JL, Packer JT, Bryant M. Primary malignant carcinoid of the testis. Arch Pathol Lab Med. 1981;105: Hosking DH, Bowman DM, McMorris SL, et al. Primary carcinoid of the testis with metastases. J Urol. 1981;125: Kaufman JJ, Waisman J. Primary carcinoid tumor of testis with metastasis. Urology. 1985;25: Glazier DB, Murphy DP, Barnard N, et al. Primary carcinoid tumour of the testis. Br J Urol. 1983;1: Rosenberg JW, Yang M. Carcinoid tumor of the testicle. N J Med. 1989;86: Danikas D, Sachs R, Dressner RM, et al. Testicular metastasis from ileal carcinoid: report of a case. Dis Colon Rectum. 2001;44: Hayashi T, Iida S, Taguchi J, et al. Primary carcinoid of the testis associated with carcinoid syndrome. Int J Urol. 2001;8: Singer AJ, Anders KH. Primary carcinoid of the testis 25 years after contralateral testicular seminoma. Urology. 2001;57: Frank RG, Gerard PS, Anselmo MT, et al. Primary carcinoid tumor of the testis. Urol Radiol. 1991;12: Miliauskas JR. Carcinoid tumor occurring in a mature testicular teratoma. Pathology. 1991;23: Kim HJ, Cho MY, Park YN, et al. Primary carcinoid tumor of the testis: immunohistochemical, ultrastructural and DNA flow cytometric study of two cases. J Korean Med Sci. 1999;14: Sutherland RS, Wettlaufer JN, Miller GJ. Primary carcinoid tumor of the testicle: a case report and management schema. J Urol. 1992;148: Grunshaw ND, Gopichandran TD. Case report: primary carcinoid tumour of the testis: ultrasound appearances. Clin Radiol. 1993;47: Lodato RF, Zentner GJ, Gomez CA, et al. Scrotal carcinoid: presenting manifestation of multiple lesions in the small intestine. Am J Clin Pathol. 1991;96: Leake J, Levitt G, Ramani P. Primary carcinoid of the testis in a 10-year-old boy. Histopathology. 1991;19: Berdjis CC, Mostofi FK. Carcinoid tumors of the testis. J Urol. 1977;118: Zavala-Pompa A, Ro JY, El-Naggar A, et al. Primary carcinoid tumor of testis. Cancer. 1993;72: Rosser CJ, Gerrard E. Metastatic small cell carcinoma to the testis. South Med J. 2000;93: Downloaded from Am J Clin Pathol 2003;120:
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