Vascular neoplasm is the most common primary neoplasm
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1 Splenic hamartoma is a rare, benign vascular proliferation that is often found incidentally while working up other complaints or at autopsy. Women more commonly present with symptoms related to mass effect than men. Histologic findings consist of unorganized vascular channels of varying width, with intervening red pulp like disorganized stroma with or without lymphoid follicles. The endothelial cells are similar to those of normal splenic sinuses. Although rendering a diagnosis can be difficult, endothelial cells that are positive for CD8 are a key feature that differentiate hamartoma from other vascular lesions of the spleen. Clinical, radiologic, and histologic correlation is essential to ensure this benign lesion is not mistaken for malignancy. (Arch Pathol Lab Med. 2009;133: ) Vascular neoplasm is the most common primary neoplasm of the spleen. 1 Of the various vascular tumors of the spleen, splenic hamartoma and littoral cell angioma occur only in the spleen. 2 Since the first report in 1861 by Rokitansky, 3 splenic hamartomas have also been called splenomas, spleen within a spleen, hemangiomas, posttraumatic scars, fibrotic nodules, tumorlike congenital malformations, and hyperplastic nodules. 4 6 Splenic hamartomas are very rare with only 3 described in splenectomies at a medical center during a 17-year period 7 and an incidence of 0.024% to 0.13% in a review of autopsies. 8 More than 150 cases of splenic hamartoma have been documented in the literature to date. 9 Improvements in imaging techniques have led to increased detection of this entity and a secondary rise in incidence. 5 Although hamartomas are benign and usually asymptomatic, it is important to distinguish this benign lesion from malignancy. CLINICAL HISTORY A 29-year-old woman, with no significant medical history, presented with persistent right-sided abdominal pain. No organomegaly was noted in the abdomen on physical examination. Ultrasound of the abdomen demonstrated a homogeneous, hypoechoic, 3.9-cm mass of the spleen, without internal color Doppler flow. Computed tomography displayed a hypoenhancing and hypodense le- Accepted for publication May 16, From the Department of Pathology and Laboratory Medicine, Henry Ford Hospital, Detroit, Mich. The authors have no relevant financial interest in the products or companies described in this article. Reprints: Hwajeong Lee, MD, Department of Pathology and Laboratory Medicine, Henry Ford Hospital, 2799 W Grand Blvd, Detroit, MI ( hlee1@hfhs.org). Hamartoma of the Spleen Hwajeong Lee, MD; Koichi Maeda, MD sion (Figure 1, A). Magnetic resonance imaging revealed a mildly hypointense and hypovascular lesion on T1- and T2-weighed images (Figure 1, B). Subsequently, the lesion demonstrated heterogeneous enhancement, becoming mildly hyperintense to the spleen. Differential diagnoses included inflammatory pseudotumor, lymphoma, and atypical hemangioma. On further evaluation, the patient was found to have biliary dyskinesia and underwent a laparoscopic cholecystectomy and splenectomy for tissue diagnosis. The resected 200-g spleen contained a 3-cm, well-circumscribed solid mass (Figure 2). Histology of the mass showed partially solid and cystic areas, containing a mixture of unorganized vascular channels lined by plump endothelial cells (Figures 3 and 4). No areas of cytologic atypia, mitosis, or necrosis were identified (Figure 5). Immunostain for CD8 was positive for lining cells (Figure 6). CD68 was diffusely positive in macrophages and focally positive in lining cells, and CD34 was positive in lining cells; CD31 was diffusely positive, and CD21 was negative. The combined morphologic and immunohistochemical profile supported a diagnosis of splenic hamartoma. CLINICAL FEATURES Splenic hamartomas occur in any age group (11 months to 86 years), 5 with equal occurrence in males and females, usually without symptoms. 6,8,10 The average size of the lesion is reported 1 to be larger in females, suggesting hormonal influence. Hence, clinical manifestations associated with larger lesions, such as splenomegaly, palpable mass, or spontaneous rupture, are more common in women. 11 Some reported cases were associated with hypersplenism, such as thrombocytopenia, anemia, and pancytopenia, or hematologic conditions, including malignancy. 4 6,12 Although even rarer in the pediatric population, the percentage of affected children who are symptomatic is higher than that of adult patients. 4,5 Rare cases of splenic hamartoma associated with tuberous sclerosis have also been reported. 4,13,14 Most splenic hamartomas are hyperechoic solid masses, with or without cystic changes in ultrasonogram, and are hypervascular in both color Doppler ultrasound and angiogram. On computed tomography, hamartomas appear as isodense or hypodense solid masses and demonstrate heterogeneous contrast enhancement relative to adjacent normal parenchyma 6,11 (Figure 1). Most of the lesions are isointense in T1-weighed magnetic resonance images and heterogeneously hyperintense in T2-weighed magnetic resonance images. 11,15 Although splenic hamartoma may be suggested by radiologic findings, definitive diagnosis Arch Pathol Lab Med Vol 133, January 2009 Hamartoma of the Spleen Lee & Maeda 147
2 Figure 1. Incidentally found splenic hamartoma in a 29-year-old woman. A, Contrast-enhanced computed tomography scan showing hypodense lesion (arrow) in the dome of the spleen. B, The lesion (arrow) is mildly hypointense on a T1-weighed image. Figure 2. Photograph of the cut surface of the resected spleen illustrating well-circumscribed solid mass (arrow) (10% buffered formalin-fixed). Figure 3. Scanning view of the mass without malpighian corpuscles (left field), in contrast to the adjacent normal splenic parenchyma with white pulp (right field) (hematoxylin-eosin, original magnification 40). requires tissue examination. Tissue examination can also exclude malignancy and, in some cases, relieve symptoms. Fine-needle aspiration of hamartomas has been performed in a limited number of cases. 2,12,16 Splenectomy is curative for rare symptomatic hamartomas, but a partial splenectomy may be sufficient in some cases. 6,17 PATHOLOGIC FEATURES Hamartomas are solitary or multiple, round, well-circumscribed, unencapsulated bulging nodules compressing the adjacent normal splenic parenchyma (Figure 2). Focal fibrosis and cystic areas can be seen. The color is usually dark red to grayish white. The size ranges from a few millimeters to centimeters, with a median size of 5 cm, but lesions as large as 20 cm have been reported. 6,10 Histologic findings reveal disorganized vascular channels lined by slightly plump endothelial cells without atypia, mixed with intervening splenic red pulp like stroma with or without white pulp 11,18 (Figures 3 through 5). Organized lymphoid follicles (malpighian corpuscles) are not present. 11 Four cases of splenic hamartoma with large, atypical stromal cells have been described recently. 19,20 The bizarre stromal cells expressed desmin and keratin, suggestive of immunophenotype similar to that of accessory reticulin cells. Laskin et al 19 interpreted this immunophenotypic modulation as a response to pathologic stimuli and emphasized that the presence of bizarre stromal cells should not be misinterpreted as malignancy. Additionally, 148 Arch Pathol Lab Med Vol 133, January 2009 Hamartoma of the Spleen Lee & Maeda
3 Figure 4. The lesion containing a mixture of unorganized vascular channels (arrow) and fibrotic cords of splenic red pulp like area (hematoxylin-eosin, original magnification 200). Figure 5. Higher magnification of the lesion reveals no cytologic atypia, mitosis, or necrosis (hematoxylin-eosin, original magnification 600). Figure 6. CD8 immunostain is positive in the lining cells (arrow) and scattered lymphocytes (original magnification 200). plasmacytosis, extramedullary hematopoiesis, and increased numbers of macrophages, eosinophils, and mast cells can be seen. 7,10 A key immunohistochemical feature is CD8 positivity of the lining cells of the vascular channels 21 (Figure 6). The cells are also positive for CD31, factor VIII related antigen, and vimentin. 2,9,12,18,22 Immunostaining results for the lining cells with CD34 have been inconsistent, 2,9,12,18,20,22 and the endothelial cells are negative for CD21. CD68 is positive in scattered stromal macrophages but negative in the lining cells of the vascular channels. The endothelial nature of the lining cells with Weibel-Palade bodies has been confirmed by ultrastructural studies. 2,5 PATHOGENESIS The pathogenesis of hamartoma is controversial. Some consider hamartomas congenital malformation of the splenic red pulp, a neoplasm, excessive and disorganized growth of abnormally formed red pulp, or a reactive lesion to prior trauma. 2,7 With documented cases associated with hematologic malignancy, others believe hamartoma is an acquired proliferative process. 11 DIFFERENTIAL DIAGNOSIS Splenic hamartomas must be differentiated from other vascular tumors of the spleen, including hemangioma, littoral cell angioma, lymphangioma, hemangioendothelioma, sclerosing angiomatoid nodular transformation of the spleen and angiosarcoma (Table). Solid mass forming lesions of the spleen, such as inflammatory myofibroblastic tumor, lymphoma, metastatic disease, disseminated fungal or mycobacterial infections, and sarcoidosis are also included in the radiologic differential diagnosis. 23 Splenic hemangiomas are the most common benign neoplasm arising from sinusoidal epithelial cells. Usually, hemangiomas are asymptomatic, measuring less than 2 cm in diameter. However, there is a risk of a spontaneous rupture with a large lesion. 15 The cavernous type is more common than the capillary type, and diffuse angiomatosis replacing the whole spleen has been documented. Histologically, hemangioma is composed of proliferating vascular channels, which are lined by flat endothelial cells and separated by thin fibrous septa or red pulps. 11 The vascular channels are filled with red blood cells. Larger lesions may show thrombosis, infarction, fibrosis, and pseudocystic degeneration. 11 The flat endothelial cells are positive for endothelial markers including CD31 and CD34 and are negative for CD8, CD21, and CD68. Littoral cell angioma is a vascular tumor arising form littoral cells originating from splenic sinuses. Littoral cells are characterized by their expression of both endothelial and histiocytic markers. This rare entity was first described in and 2 cases with malignant histology have been reported. 25,26 One-third of previously reported littoral cell angioma cases were associated with visceral tumors. 23 Littoral cell angiomas are frequently associated with splenomegaly and appear as low attenuating lesions in contrast-enhanced computed tomography. 11 Histologic examination demonstrates anastomosing vascular channels lined by tall columnar cells, which often show hemophagocytosis. 2 The lining cells are positive for both endothelial and histiocytic markers, CD31 and CD68. 11,23 CD21, which is the C3d complement receptor and also the Epstein-Barr virus receptor of B lymphocytes, is reported to be exclusively positive in littoral cell angioma. 18 Unlike Arch Pathol Lab Med Vol 133, January 2009 Hamartoma of the Spleen Lee & Maeda 149
4 Hamartoma Hemangioma Differential Diagnoses of Splenic Hamartoma Entity Histologic Findings Immunomarkers Clinical Outcomes Littoral cell angioma Lymphangioma Hemangioendothelioma Sclerosing angiomatoid nodular transformation Angiosarcoma Disorganized vascular channels mixed with red pulp like stroma Vascular channels separated by thin fibrous septa or red pulps Anastomosing vascular channels lined by tall columnar cells; occasional papillary fronds Honeycomb of cystic spaces filled with proteinaceous fluids Vascular channels lined by mildly to moderately atypical cells Multiple confluent vascular nodules surrounded by concentric fibrous rims Anastomosing vascular channels lined by markedly atypical cells CD8, CD21, CD34 variable, CD68 CD8 CD21 CD31 CD34 CD68 CD8 CD21 CD34 CD68 CD8 CD21 CD31 CD31, factor VIII related antigen, CD34 variable Sinusoids: CD34 CD31 CD8 ; capillaries: CD34 CD31 CD8 ; small veins: CD34 CD31 CD8 CD31, factor VIII related antigen, CD34, CD68 Benign, occasional mass effect Benign, possible splenic rupture Splenomegaly, unknown biological behavior Benign Intermediate between benign and malignant Benign Malignant splenic hamartoma, littoral cell angioma is negative for CD8 and CD34 in the lining cells. 18 Occasional papillary fronds are present, and the periphery of the lesion displays normal splenic sinuses. Because the biological behavior of this tumor has not been established, close followup is recommended for a patient diagnosed with littoral cell angioma. 23 Lymphangioma is an uncommon, benign tumor of the spleen manifesting as a solitary subcapsular nodule or as diffuse lymphangiomatosis in young patients. 15 Cystic lymphangioma is more common than capillary or cavernous types. Microscopic examination shows a honeycomb of cystic spaces containing proteinaceous, lymphlike, clear fluids. Occasional epithelial papillary projections of the cystic spaces are seen. Endothelial cells lining the cystic spaces are positive for CD31, focally positive or negative for CD34, and negative for CD21 and CD8. Hemangioendothelioma is a rare and controversial entity of the spleen. 27 It is considered a lesion of intermediate histology between benign hemangioma and angiosarcoma. 11 Epithelioid, spindle, and a combination of the 2 patterns have been described. 28,29 The lining cells of the vascular channels show mild to moderate atypia with similar immunohistochemical staining patterns to littoral cell angioma, with positive immunostaining for endothelial and histiocytic markers. The lining cells are usually positive for CD31 and factor VIII related antigen, and variably positive for CD34 and cytokeratin. Sclerosing angiomatoid nodular transformation of the spleen, also known as multinodular hemangioma, is altered red pulp entrapped by nonneoplastic stromal proliferation. 27 Microscopically, the lesion is composed of multiple confluent vascular nodules surrounded by concentric collagen fibers or fibrinoid rims. The central portion of the nodules consists of vascular channels of varying caliber lined by plump endothelial cells interspersed with ovoid or spindle cells. There are numerous red blood cells, and intervening stroma is fibrosclerotic or myxoid with scattered myofibroblasts, siderophages, and inflammatory cell infiltrates. Immunostaining of the vascular area reveals 3 types of blood vessels: CD34 CD31 CD8 sinusoids, CD34 CD31 CD8 capillaries, and CD34 CD31 CD8 small veins. Scattered macrophages are positive for CD68, and CD21 immunostaining is negative in the lining endothelial cells. 27,30 Despite its similarity with splenic hamartoma in composition, sclerosing angiomatoid nodular transformation is a mixture of 3 types of blood vessels, whereas hamartoma consists of only sinusoid-type vessels. Angiosarcoma is the most common nonlymphoid malignant primary tumor of the spleen. 11 Although CD8 positivity of the lining cells in angiosarcoma of the spleen has been reported, 18 the presence of irregular, anastomosing vascular channels associated with marked cellular atypia, frequent mitoses, and invasion of surrounding organs can aid in making a diagnosis. The lining cells are positive for endothelial cell markers, including CD31, CD34, factor VIII related antigen, and the histiocytic marker CD68. Angiosarcoma is highly aggressive with a poor prognosis. 15 CONCLUSION With the rapid advancement of imaging modalities, smaller asymptomatic lesions of the spleen are being identified. Splenic hamartoma is a benign vascular proliferation characterized by CD8 immunophenotype of the lining endothelial cells. We should be aware of this rare, benign entity and interpret histologic features in the context of clinical and radiologic findings to render a diagnosis and differentiate it from malignancy. References 1. Garvin DF, King FM. Cysts and nonlymphomatous tumors of the spleen. Pathol Annu. 1981;16: Ramdall RB, Alasio TM, Cai G, Yang GC. Primary vascular neoplasms unique to the spleen: littoral cell angioma and splenic hamartoma diagnosis by fine-needle aspiration biopsy. Diagn Cytopathol. 2007;35: Rokitansky K. Über splenoma. Lehrbuch der Pathol Anat. 1861;3:9. 4. Abramowsky C, Alvarado C, Wyly JB, Ricketts R. Hamartoma of the spleen (splenoma) in children. Pediatr Dev Pathol. 2004;7: Hayes TC, Britton HA, Mewborne EB, Troyer DA, Saldivar VA, Ratner LA. Symptomatic splenic hamartoma: case report and literature review. Pediatrics. 1998;101:10E. 6. Wirbel RJ, Uhlig U, Futterer KM. Case report: splenic hamartoma with hematologic disorders. Am J Med Sci. 1996;311: Silverman ML, LiVolsi VA. Splenic hamartoma. Ann J Clin Pathol. 1978;70: Lam KY, Yip KH, Peh WC. Splenic vascular lesions: unusual features and a review of the literature. Aust N Z J Surg. 1999;69: Conlon S, Royston D, Murphy P. Splenic hamartoma. Cytopathology. 2007; 18: Falk S, Stutte HJ. Hamartomas of the spleen: a study of 20 biopsy cases. Histopathology. 1989;14: Abbott RM, Levy AD, Aguilera NS, Gorospe L, Thompson WM. From the archives of the AFIP: primary vascular neoplasms of the spleen: radiologic-pathologic correlation. Radiographics. 2004;24: Lee SH. Fine-needle aspiration cytology of splenic hamartoma. Diagn Cytopathol. 2003;28: Darden JW, Teeslink R, Parrish A. Hamartoma of the spleen: a manifestation of tuberous sclerosis. Am Surgeon. 1975;41: Arch Pathol Lab Med Vol 133, January 2009 Hamartoma of the Spleen Lee & Maeda
5 14. van Heerden JA, Longo MF, Cardoza F, Farrow GM. The abdominal mass in patients with tuberous sclerosis: surgical implications and report of a case. Arch Surg. 1967;95: Giovagnoni A, Giorgi C, Goteri G. Tumours of the spleen. Cancer Imaging. 2005;25: Kumar PV. Splenic hamartoma: a diagnostic problem on fine needle aspiration cytology. Acta Cytol. 1995;39: Havlik RJ, Touloukian RJ, Markowitz RI, Buckley P. Partial splenectomy for symptomatic splenic hamartoma. J Pediatr Surg. 1990;25: Arber DA, Strickler JG, Chen YY, Weiss LM. Splenic vascular tumors: a histologic, immunophenotypic, and virologic study [comment on: Am J Surg Pathol. 2000;24: ]. Am J Surg Pathol. 1997;21: Laskin WB, Alasadi R, Variakojis D. Splenic hamartoma [comment on: Am J Surg Pathol. 2005;29: ]. Am J Surg Pathol. 2005;29: Cheuk W, Lee AK, Arora N, Ben-Arie Y, Chan JK. Splenic hamartoma with bizarre stromal cells [comment in: Am J Surg Pathol. 2005;29: ]. Am J Surg Pathol. 2005;29: Zujerberg LR, Kaynor BL, Silverman ML, Harris NL. Splenic hamartoma and capillary hemangioma are distinct entities: immunohistochemical analysis of CD8 expression by endothelial cells. Hum Pathol. 1991;22: Ali TZ, Beyer G, Taylor M, Volpe C, Papadimitriou JC. Splenic hamartoma: immunohistochemical and ultrastructural profile of two cases. Int J Surg Pathol. 2005;13: Cosme A, Tejada A, Bujanda L, et al. Littoral-cell angioma of the spleen: a case report. World J Gastroenterol. 2007;13: Falk S, Stutte HJ, Frizzera G. Littoral cell angioma: a novel splenic vascular lesion demonstrating histiocytic differentiation. Am J Surg Pathol. 1991;15: Rosso R, Paulli M, Gianelli U, Bovert E, Stella G, Magrini U. Littoral cell angiosarcoma of the spleen: case report with immunohistochemical and ultrastructural analysis. Am J Surg Pathol. 1995;19: Ben-Lzhak O, Bejar J, Ben-Eliezer S, Vlodavsky E. Splenic littoral cell hemangioendothelioma: a new low-grade variant of malignant littoral cell tumor. Histopathology. 2001;39: Awamleh AA, Perez-Ordonez B. Sclerosing angiomatoid nodular transformation of the spleen. Arch Pathol Lab Med. 2007;131: Suster S. Epithelioid and spindle-cell hemangioendothelioma of the spleen: report of a distinctive splenic vascular neoplasm of childhood. Am J Surg Pathol. 1992;16: Budke HL, Breitfeld PP, Neiman RS. Functional hyposplenism due to a primary epithelioid hemangioendothelioma of the spleen. Arch Pathol Lab Med. 1995;119: Martel M, Cheuk W, Lombardi L, Lifschitz-Mercer B, Chan JK, Rosai J. Sclerosing angiomatoid nodular transformation (SANT): report of 25 cases of a distinctive benign splenic lesion. Am J Surg Pathol. 2004;28: Arch Pathol Lab Med Vol 133, January 2009 Hamartoma of the Spleen Lee & Maeda 151
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