Fine-Needle Aspiration of Intrapancreatic Accessory Spleen, Mimic of Pancreatic Neoplasms
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1 Fine-Needle Aspiration of Intrapancreatic Accessory Spleen, Mimic of Pancreatic Neoplasms Jingmei Lin, MD, PhD; Xin Jing, MD N Intrapancreatic accessory spleen (IPAS) is a congenital abnormality, which mimics neoplasm. Distinguishing IPAS from pancreatic neoplasm/malignancy is extremely important from a treatment perspective. We report the case of a 67-year-old asymptomatic man who had a 1.3-cm, incidentally detected, pancreatic tail mass. The mass was round, well-circumscribed, and hypervascular with uniform enhancement. The image findings were highly suggestive of a pancreatic endocrine neoplasm. An endoscopic ultrasound-guided fine-needle aspiration was performed. Conventional smears revealed a polymorphous population of lymphocytes admixed with a subset of other inflammatory cells. Hematoxylin-eosin stained cell block sections showed conspicuous thin-walled blood vessels in addition to inflammatory cells. Immunostaining for CD8 demonstrated strong positivity in endothelial cells of the thin-walled vessels. By correlating the cytologic findings with the result of immunostaining, we rendered the diagnosis of IPAS. Our experience supports the view that endoscopic ultrasoundguided fine-needle aspiration may enable a reliable, preoperative diagnosis of IPAS and thus prevent unnecessary surgery. (Arch Pathol Lab Med. 2010;134: ) stained with Diff-Quik stain (StatLab, McKinney, Texas) for onsite rapid assessment. The other smear was quickly fixed with Spray Fix (Surgipath Medical Industries, Inc, Richmond, Illinois) and stained with Papanicolaou stain before final evaluation. The on-site review of the Diff-Quik stained smears revealed a polymorphous population of lymphocytes admixed with a subset of other inflammatory cells that included neutrophils, monocytes, plasma cells, and a few eosinophils. In addition, the presence of lymphoglandular bodies in the background was appreciated (Figure 1, A). The latter finding is compatible with a lesion of lymphoid origin. After confirming correct placement of the needle into the mass and the similarity of signal intensity between the mass and the spleen, a preliminary diagnosis of intrapancreatic accessory spleen (IPAS) was rendered. Review of the Papanicolaou-stained smears (Figure 1, B) showed cellular components that were identical to those of the Diff-Quik stained smears. Further, the hematoxylin-eosin stained cell block sections showed conspicuous thin-walled blood vessels in addition to the mixtures of lymphocytes and other inflammatory cells. Immunostaining with antibody against CD8 (Novocastra, Newcastle Upon Tyne, United Kingdom) was performed and showed strong positivity in endothelial cells of the thin-walled vessels (Figure 1, C). This immunoprofile was consistent with the origin of splenic sinuses. Overall, the cytologic findings and the result of immnuostaining supported a final diagnosis of IPAS, which was in agreement with the preliminary interpretation. COMMENT REPORT OF A CASE Accessory spleen is a congenital abnormality with The patient was a 67-year-old asymptomatic man who had a normal pancreatic tissue in ectopic sites due to the fusion 1.3-cm pancreatic tail mass incidentally detected by computed failure of splenic anlage. 1,2 It is estimated to occur in tomography. The mass was round, well-circumscribed, hypervascular with uniform enhancement. The image findings were approximately 10% to 15% of the general population. 3 Most accessory spleens (80%) are located at the splenic highly suggestive of a pancreatic endocrine neoplasm. Other differential diagnoses included acinar cell carcinoma, solid hilum, while fewer than 20% are in the pancreatic tail. pseudopapillary neoplasm, and, less likely, adenocarcinoma or Other uncommon sites have also been reported, such as lymphoma. To further classify the mass, the patient underwent the wall of the jejunum, mesentery, and pelvis. The endoscopic ultrasound (EUS) guided transgastric fine-needle aspiration (FNA) and a total of 7 passes were performed. Two patients are usually asymptomatic and have an incidental, image-detected mass during an unrelated workup. Computed tomography and/or magnetic resonance imaging direct smears were made from each pass and the needle was then rinsed in CytoLyt solution (Cytyc Corporation, Marlborough, commonly identify the lesion as a round to oval, Massachusetts) for a cell block. One smear was air dried and hypervascular mass with sharp borders and homogenous intensity. The enhancement pattern is similar to that of the Accepted for publication June 10, From the Department of Pathology, University of Michigan Health spleen on contrast computed tomography and/or magnetic resonance imaging. However, radiographic features System, Ann Arbor. Dr Lin is now located at the Department of Anatomic Pathology, The Cleveland Clinic, Ohio. of accessory spleens are not specific and similar features The authors have no relevant financial interest in the products or may be observed in many neoplasms. 4,5 Review of the companies described in this article. literature by Uchiyama et al 6 revealed that, among 11 cases Presented at New Frontiers in Pathology: An Update for Practicing Pathologists, University of Michigan, Ann Arbor, Michigan, October 9, of surgically removed IPAS, only 1 case was correctly Reprints: Xin Jing, MD, Department of Pathology, University of diagnosed preoperatively owing to the presentation of Michigan Health System, 1500 E Medical Center Dr, Rm 2G332, Ann idiopathic thrombocytopenic purpura. On the contrary, Arbor, MI ( xinjing@umich.edu). the remaining 10 cases were misdiagnosed as pancreatic 1474 Arch Pathol Lab Med Vol 134, October 2010 FNA of Intrapancreatic Accessory Spleen Lin & Jing
2 Figure 1. Fine-needle aspiration of intrapancreatic accessory spleen. A and B, Conventional smears reveal polymorphous population of lymphocytes admixed with other inflammatory cells, including neutrophils, monocytes, plasma cells, and a few eosinophils. C, Positive immunostaining for CD8 highlights endothelial cells of splenic sinus in cell block (Diff-Quik, original magnification 3400 [A]; Papanicolau, original magnification 3600 [B]; original magnification 3400 [C]). endocrine neoplasms and patients therefore underwent surgical resection. 6 Currently, there are no clinical or radiographic criteria to distinguish IPAS from pancreatic neoplasms. What About the Role of EUS-Guided FNA in the Diagnosis of IPAS? There are a few case reports of thoracic splenosis diagnosed by FNA cytology. 7,8 Schreiner et al 9 recently reported the first series of IPAS diagnosed by EUS-guided FNA. Accordingly, the cytologic features of IPAS were nonspecific and included predominantly small lymphocytes with a subset of histiocytes, conspicuous eosinophils, and plasma cells. The cell block sections showed conspicuous thin-walled blood vessels. Immunocytochemical staining of CD8 specifically highlighted endothelial cells of the thin-walled blood vessels. The authors stated that the latter findings were characteristic of splenic sinuses, as immunostaining of CD8 is negative in systemic endothelial cells and hemangioma. 9,10 Overall, EUS-guided FNA with the aid of CD8 immunostaining may make it possible to diagnose IPAS preoperatively and thus avoid unnecessary surgery. Cytologic Differential Diagnoses of IPAS Neoplasms mimicking IPAS include pancreatic endocrine neoplasm (PEN), acinar cell carcinoma (ACC), solid pseudopapillary neoplasm, well-differentiated adenocarcinoma, as well as lymphoma. Among these entities, PEN is the most common mimic of IPAS. 6 Pancreatic endocrine neoplasm is uncommon and represents 2% of pancreatic neoplasms. 11 There is no sex predilection. The tumor commonly occurs in older adults, although it may affect individuals in a broad age range. It may be associated with hereditary syndromes such as multiple endocrine neoplasia type I and von Hippel-Lindau syndrome. Pancreatic endocrine neoplasm often involves the pancreatic tail and is identified incidentally by radiologic imaging. A specimen of PEN prepared from FNA is hypercellular with single and loosely cohesive groups of cells. Some groups may exhibit a configuration of pseudorosettes. Commonly, the tumor cells appear relatively uniform with a round, polygonal, or plasmacytoid shape, although other cell types, that is, clear, oncocytic, and spindled, may be seen. Some cells may show binucleation or multinucleation. Classic salt-and-pepper chromatin pattern is easily appreciated and nucleoli may be conspicuous (Figure 2, A and B). Acinar cell carcinoma is a rare malignant exocrine pancreatic neoplasm, which accounts for less than 2% of pancreatic malignancy. 12 Acinar cell carcinoma occurs in older adults, with a male predominance. It commonly involves the head of the pancreas. Smears of ACC prepared from FNA are cellular with tumor cells and naked nuclei in a clean background. The cells are arranged either singly or in loose clusters with acinar formation. The cytoplasmic borders are indistinct and cytoplasm is abundant, with granular, clear, or vacuolated appearance. The nuclei are either centrally or eccentrically located and prominent nucleoli are appreciated (Figure 3, A through C). Solid pseudopapillary neoplasms compose 1% to 2% of pancreatic tumors. It is a disease of young women, with uncertain cellular differentiation. 13 Fine-needle aspiration smears are hypercellular with single and/or loose clusters of cells, as well as branching papillary fronds with central fibrovascular cores surrounded by 1 to several layers of cells. The cells appear monotonous and bland with scant to moderate amount of delicate cytoplasm and mildly Arch Pathol Lab Med Vol 134, October 2010 FNA of Intrapancreatic Accessory Spleen Lin & Jing 1475
3 Figure 2. Fine-needle aspiration of pancreatic endocrine neoplasm. A and B, Conventional smears show cellular aspirates with single cells and clusters of cells. Some cells have a plasmacytoid appearance. Saltand-pepper chromatin and conspicuous nucleoli are appreciated (DiffQuik, original magnification 3600 [A]; Papanicolau, original magnification 3600 [B]). atypical nuclei. The chromatin is granular with indistinct nucleoli. Intranuclear grooves are commonly identified (Figure 4, A and B). Myxoid, metachromatic stroma, and hyaline globules may be present. Rarely, necrotic debris may be seen when cystic degeneration occurs in the tumor. Adenocarcinoma is the fifth leading cause for cancerrelated death in the United States, with a 5-year survival rate of 5% despite the progress of chemotherapy regimens and the increased success rate of pancreatoduodenectomy. Adenocarcinoma accounts for up to 85% to 90% of all pancreatic neoplasms. It is a disease of older adults with a male predominance. More than 50% occur in the head of the pancreas, 15% in the body, 5% in the tail, and the remaining 20% are multifocal. Although FNA cytologic diagnosis of moderately or poorly differentiated adenocarcinoma of pancreas is commonly straightforward, welldifferentiated adenocarcinoma may present a diagnostic dilemma owing to the subtle, atypical features. With regard to the latter, the aspirates are hypercellular, with numerous, large, 2-dimensional sheets of neoplastic cells with well- to ill-defined cytoplasmic borders. The nuclei are unevenly distributed within the sheets and thus 1476 Arch Pathol Lab Med Vol 134, October 2010 Figure 3. Fine-needle aspiration of acinar cell carcinoma. A, Conventional smear shows hypercellularity with a clean background. B and C, The neoplastic cells have abundant granular cytoplasm with indistinct cell borders and centrally or eccentrically located nuclei with prominent nucleoli. Many naked nuclei are seen (Diff-Quik, original magnifications 3100 [A] and 3400 [B]; Papanicolaou, original magnification 3600 [C]). present a drunken honeycomb appearance. Nuclear atypia varies from mild to severe and N/C ratios range from low to high (Figure 5, A and B). It is not uncommon to see scattered, isolated cells with severe atypia. FNA of Intrapancreatic Accessory Spleen Lin & Jing
4 Figure 4. Fine-needle aspiration of solid pseudopapillary tumor. A and B, Conventional smears are cellular. Branching papillary fronds have 1 to several layers of uniform polygonal cells surrounding the fibrovascular cores. The cells appear monotonous and bland with scant to moderate amount of delicate cytoplasm and mildly atypical nuclei. The chromatin is granular with indistinct nucleoli. Intranuclear grooves (indicated by arrows) are seen (Diff-Quik, original magnifications 3100 [A] and 3400 [B]). Figure 5. Well-differentiated ductal adenocarcinoma. A and B, Conventional smears show large, 2-dimensional sheets of neoplastic cells. Normal honeycombing pattern is altered. The nuclei are unevenly distributed, showing overlapping and crowding, and give an appearance of drunken honeycomb (Diff-Quik, original magnification 3400 [A]; Papanicolaou stain, original magnification 3400 [B]). It is noteworthy to mention that distinguishing welldifferentiated pancreatic adenocarcinoma from chronic pancreatitis may be extremely difficult not only for clinicians and radiologists but also for pathologists. Reports 14,15 indicate that chronic pancreatitis accounts for up to 75.9% of false-positive diagnoses. Cellularity of smears prepared from FNA of patients with chronic pancreatitis is variable. Fibrotic stromal fragments, along with variable amount of acinar tissue and mixed inflammatory infiltrates, may be seen. The background may contain prominent chalky calcific debris. Despite the cytologic atypia, normal architecture of honeycombing is maintained. Moreover, the lack of single atypical cells makes the diagnosis of adenocarcinoma less likely. The role of ancillary studies, such as immunostaining, in establishing a definitive diagnosis of pancreatic epithelial neoplasms has been previously discussed. 11 In this regard, PEN is positive for pancytokeratin as well as neuroendocrine markers such as chromogranin and synaptophysin. The presence of diastase-resistant, periodic acid-schiff positive zymogen granules is characteristic of ACC. Acinar cell carcinoma is also immunoreactive for the antibody to cytokeratin, as well as enzymes such as trypsin, lipase, chymotrypsin, and a 1 -antitrypsin. 11 Solid pseudopapillary neoplasm reacts variably with neuroendocrine markers, cytokeratin, and pancreatic enzymes. In addition, nuclear staining of b-catenin is characteristic for solid pseudopapillary neoplasm. 16 Last but not least, the neoplastic entity that needs to be differentiated from IPAS is lymphoma. Like the smears of IPAS, those prepared from aspirations of lymphoma may contain a lymphoglandular bodies in the background. However, aspirates of non-hodgkin lymphoma commonly contain monomorphous population of lymphocytes. On the other hand, identification of rare atypical cells resembling Reed-Sternberg cells, with a background polymorphous population of lymphocytes, should raise concerns for Hodgkin lymphoma. When in doubt during Arch Pathol Lab Med Vol 134, October 2010 FNA of Intrapancreatic Accessory Spleen Lin & Jing 1477
5 the on-site rapid assessment of FNA, collecting additional material for ancillary studies, such as flow cytometry and/or immunostaining, is highly recommended. Epidermoid cysts may occur in IPAS, 5,6,17 which raises concerns for distinguishing IPAS from lymphoepithelial cyst, a nonneoplastic pancreatic lesion of unknown etiology. Aspirates of lymphoepithelial cyst reveal squamous cells, keratinous materials, lymphocytes, histiocytes, and cholesterol crystals. CONCLUSIONS Most patients with IPAS do not require surgical treatment unless IPAS becomes symptomatic owing to torsion, spontaneous rupture, or hemorrhage or causes hematologic disorders such as idiopathic thrombocytopenic purpura. 18 In contrast, virtually all pancreatic neoplasm/malignancies require surgery if the lesions are resectable. Therefore, the distinction between IPAS and pancreatic neoplasm/malignancy is extremely important. The use of EUS-guided FNA may provide a reliable diagnosis, thus preventing unnecessary surgery. References 1. Dodds WJ, Taylor AJ, Erickson SJ, Stewart ET, Lawson TL. Radiologic imaging of splenic anomalies. AJR Am J Roentgenol. 1990;155(4): Chin S, Isomoto H, Mizuta Y, Wen CY, Shikuwa S, Kohno S. Enlarged accessory spleen presenting stomach submucosal tumor. World J Gastroenterol. 2007;13(11): Halpert B, Alden ZA. Accessory spleens in or at the tail of the pancreas: a survey of 2,700 additional necropsies. Arch Pathol. 1964;77: Spencer LA, Spizarny DL, Williams TR. Imaging features of intrapancreatic accessory spleen [published online ahead of print August 18, 2009]. Br J Radiol. doi: /bjr/ Kim SH, Lee JM, Han JK, et al. Intrapancreatic accessory spleen: findings on MR Imaging, CT, US and scintigraphy, and the pathologic analysis. Korean J Radiol. 2008;9(2): Uchiyama S, Chijiiwa K, Hiyoshi M, et al. Intrapancreatic accessory spleen mimicking endocrine tumor of the pancreas: case report and review of the literature. J Gastrointest Surg. 2008;12(8): Syed S, Zaharopoulos P. Thoracic splenosis diagnosed by fine-needle aspiration cytology: a case report. Diagn Cytopathol. 2001;25(5): Carlson BR, McQueen S, Kimbrell F, Humphreys S, Gentry HL, Esbenshade A. Thoracic splenosis: diagnosis of a case by fine needle aspiration cytology. Acta Cytol. 1988; 32(1): Schreiner AM, Mansoor A, Faigel DO, Morgan TK. Intrapancreatic accessory spleen: mimic of pancreatic endocrine tumor diagnosed by endoscopic ultrasound-guided fine-needle aspiration biopsy. Diagn Cytopathol. 2008;36(4): Kraus MD. Splenic histology and histopathology: an update. Semin Diagn Pathol. 2003;20(2): Chhieng DC, Stelow EB. Pancreatic Cytopathology (Essentials in Cytopathology). 1st ed. New York, NY: Springer; Klimstra DS, Heffess CS, Oertel JE, Rosai J. Acinar cell carcinoma of the pancreas: a clinicopathologic study of 28 cases. Am J Surg Pathol. 1992;16(9): Kissane J. Pancreatoblastoma and solid and cystic papillary tumor: two tumors related to pancreatic ontogeny. Semin Diagn Pathol. 1994;11(2): Smith CD, Behrns KE, van Heerden JA, Sarr MG. Radical pancreatoduodenectomy for misdiagnosed pancreatic mass. Br J Surg. 1994;81(4): Kennedy T, Preczewski L, Stocker SJ, et al. Incidence of benign inflammatory disease in patients undergoing Whipple procedure for clinically suspected carcinoma: a single-institution experience Am J Surg. 2006;191(3): Tanaka Y, Notohara K, Kato K, et al. Usefulness of beta-catenin immunostaining for the differential diagnosis of solid-pseudopapillary neoplasm of the pancreas. Am J Surg Pathol. 2002;26(6): Itano O, Chiba N, Wada T, et al. Laparoscopic resection of an epidermoid cyst originating from an intrapancreatic accessory spleen: report of a case. Surg Today. 2010;40(1): Arkadopoulos N, Athanasopoulos P, Stafyla V, et al. Intrapancreatic accessory spleen issues: diagnostic and therapeutic challenges. JOP. 2009;10(4): Arch Pathol Lab Med Vol 134, October 2010 FNA of Intrapancreatic Accessory Spleen Lin & Jing
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