Resident Short Review. Solid Pseudopapillary Neoplasm of the Pancreas. A Rare Entity With Unique Features. Peyman Dinarvand, MD; Jinping Lai, MD, PhD
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1 Resident Short Review Solid Pseudopapillary Neoplasm of the Pancreas Solid pseudopapillary neoplasm of the pancreas is a rare entity with low malignant potential and excellent overall prognosis. It has nonspecific clinical presentations such as abdominal pain and nausea, with vague radiologic features. Histologic features of this neoplasm are usually specific. The tumor shows minimally cohesive, uniform, monotonous cells lining delicate capillary-sized blood vessels, described as pseudopapillary architecture. Other features including hyaline globules, cytoplasmic vacuoles, and nuclear grooving are frequently present. Use of a select panel of immunostains always helps pathologists to differentiate this tumor from other circumscribed tumors of the pancreas. Recently, b-catenin, CD10, and E-cadherin have been shown to be very important in the diagnosis of solid pseudopapillary neoplasm. Nuclear staining of tumor cells by b-catenin and membranous presentation of CD10 is seen in almost 100% of cases. Tumor cells can be partially positive for synaptophysin and chromogranin. This tumor has a low malignant potential, and definite treatment is surgical resection. (Arch Pathol Lab Med. 2017;141: ; doi: / arpa rs) A Rare Entity With Unique Features Peyman Dinarvand, MD; Jinping Lai, MD, PhD because of its low incidence, its clinical and pathologic features have not been extensively studied. Solid pseudopapillary neoplasm primarily affects young females with a mean age of 22 years. 6 In 2 separate studies, Papavramidis and Papavramidis 2 and Lam et al 7 have reported its occurrence in men at 3.9% and 6.6%, respectively. Most tumors are located in the pancreatic body and tail. 3,5 The purpose of this short review is to cover the important aspects of SPN with focus on histologic features and differential diagnosis. CLINICAL FEATURES The tumor does not exclude any group of patients and has been noted to affect the pediatric population. 2 Abdominal pain or mass is the most common presenting clinical symptom or sign. Nonspecific symptoms such as nausea, vomiting, fever, weight loss, and jaundice are other clinical symptoms; most of them are caused by tumor compression to normal pancreas. However, a considerable percentage of patient populations are asymptomatic and the neoplasm can be incidentally detected. About 15% of the patients are asymptomatic before clinical detection. Solid pseudopapillary neoplasm (SPN), an uncommon IMAGING entity first described by Frantz in 1959, 1 reportedly Solid pseudopapillary neoplasm can be detected by accounts for between 2% and 3% of pancreatic neoplasms ultrasonography, computed tomography, magnetic resonance imaging, and positron emission tomography. Plain and 0.9% to 2.7% of exocrine pancreatic neoplasms. 2,3 This neoplasm, which has had a variety of names such as solid radiography (X-ray) does not have value but to show and papillary epithelial neoplasm, papillary cystic neoplasm, possible calcifications in the neoplasm. Computed tomography scan of the neoplasm demonstrates solid and cystic and solid and cystic papillary epithelial neoplasm, was designated as solid pseudopapillary neoplasm by the World features with regions of hemorrhage and/or cystic degeneration. Calcifications and enhancing solid areas may be Health Organization in Terms other than solid pseudopapillary neoplasm should no longer be used in present at the periphery of the mass. 8 Magnetic resonance pathology reports. imaging basically shows a well-circumscribed lesion with a Solid pseudopapillary neoplasm is being recognized with mixture of high- and low-signal intensity on T1- and T2- increasing frequency as having low malignant potential weighted images. 9 Typically, SPNs are well-circumscribed owing to extensive use of imaging techniques, along with a masses that demonstrate variable degrees of internal better understanding of the neoplasm itself. 5 However, hemorrhage and cystic degeneration, and may be associated with calcifications. When these features are encountered in a Accepted for publication October 12, young female patient, this neoplasm should be considered From the Department of Pathology, School of Medicine, Saint as an important differential diagnosis. Lee et al 10 reported Louis University, Saint Louis, Missouri. that solid pseudopapillary carcinoma may be differentiated The authors have no relevant financial interest in the products or from benign SPN in radiologic imaging by its aggressive companies described in this article. Reprints: Jinping Lai, MD, PhD, Department of Pathology, School behavior, such as pancreatic duct dilation and vessel of Medicine, Saint Louis University, 1402 S Grand Blvd, Saint Louis, invasion, either with or without metastases. If such imaging MO ( jinpinglai@slu.edu). features are present, aggressive surgical approach is 990 Arch Pathol Lab Med Vol 141, July 2017 Solid Pseudopapillary Neoplasm Dinarvand & Lai
2 Figure 1. Cytologic and histologic features of solid pseudopapillary neoplasm (SPN) of the pancreas. A, Fine-needle aspiration of SPN shows multibranching capillaries surrounded by numerous neoplastic cells in low and high (inset) magnifications. B, Discohesive neoplastic cells with pleomorphic nuclei, nuclear grooves (arrows), and fair amount of cytoplasm. Cercariform cells (arrowheads) are shown in the inset. C, Characteristic histologic features of SPN are pseudopapillae surrounded by discohesive neoplastic cells (arrow), with clusters of foamy histiocytes (arrowhead). D, Characteristic amorphous intracytoplasmic and extracytoplasmic eosinophilic globules (arrows), along with numerous foamy histiocytes (arrowheads) (Diff-Quick, original magnifications 3100 [A] and 3400 [inset A]; Papanicolaou stain, original magnification 3400 [B and inset B]; hematoxylin-eosin, original magnifications 3100 [C] and 3400 [D]). mandatory, and an intensive follow-up is highly recommended. CYTOLOGY AND HISTOLOGY Cytology Endoscopic ultrasound-guided fine-needle aspiration is the standard procedure for solid and cystic pancreatic lesions and one of the major modalities to obtain preoperative diagnosis for solid and cystic pancreatic lesions. Definite and quick diagnosis of SPN by evaluating cytologic features before an aggressive surgery is vital for the patient; therefore, close interaction with cytopathology colleagues is critical in improving patient care and diagnostic yield. 11 Smears demonstrate branching capillaries surrounded by numerous neoplastic cells (Figure 1, A). Characteristic myxoid clear material that surrounds the delicate papillae is an important observation for diagnosis of this entity on fine-needle aspiration. Numerous tumor cells show ill-defined granular cytoplasm with cytoplasmic elongations and on occasion, nuclear grooves (Figure 1, B). 11 Samad et al 12 recently demonstrated the presence of cercariform cells (Figure 1, B, inset); moreover, large cytoplasmic vacuoles in SPN are very useful clues in challenging cases, and also for differentiating SPN from other pancreatic tumors. Since distinguishing SPN from neuroendocrine tumor can be difficult in some cases, using a selected panel of immunostains including b-catenin, CD10, synaptophysin, and chromogranin is highly recommended for the definite diagnosis. 11 Gross Examination These tumors are widely variable in size. They measure between 0.5 cm to 34.5 cm with a mean of 9.3 cm. 7 This neoplasm is usually a round, circumscribed mass that is separated from pancreas parenchyma by a pseudocapsule. It shows variable appearance with solid, cystic, hemorrhagic, and necrotic areas. Incomplete capsules during gross examination are highly suggestive of a malignant SPN. Arch Pathol Lab Med Vol 141, July 2017 Solid Pseudopapillary Neoplasm Dinarvand & Lai 991
3 Figure 2. Applying immunostains to solid-pseudopapillary neoplasm (SPN). A, Characteristic nuclear staining of b-catenin in tumor (T) cells. This stain shows membranous pattern in normal (N) pancreatic cells. B, Membranous staining of CD10 is another important stain for SPN in tumor (T) cells, which does not show up in normal (N) pancreatic cells. C, Synaptophysin is an important strong stain, characteristic for neuroendocrine tumor of the pancreas. Synaptophysin shows negativity (or minimal positivity) in tumor (T) cells. Inset compares a hematoxylin-eosin section of the tissue including both tumor (T) cells and normal (N) pancreatic cells with the abovementioned stains (b-catenin, CD10, and synaptophysin) (original magnification 3400 [A through C]; hematoxylin-eosin, original magnification 3400 [inset C]). The larger the tumor, the greater the cystic component that the tumor contains. 11 Microscopy The typical histopathologic appearance of an SPN is shown in Figure 1, C and D. The microscopic features represent the solid and cystic nature of this neoplasm. The SPNs show a combination of solid components that consist of pseudopapillae with vascular stalks and cystic components with hemorrhage, a characteristic architecture. The tumor cells are uniform with round and small nuclei lining a delicate capillary-sized vessel (Figure 1, C and D). 13 The nuclei are round or oval, and they are located within the cell center and exhibit grooves. The nuclei do not have salt-and-pepper features, which are seen in neuroendocrine tumors. The neoplastic cells usually have a moderate amount of amphophilic cytoplasm with focal aggregation of intracytoplasmic and extracytoplasmic hyaline globules (Figure 1, C and D). 1 These globules are typically periodic acid Schiff positive and diastase resistant and highly characteristic for diagnosis of SPN. Foam cells (macrophages) and foreign-body giant cells are usually observed adjacent to the cystic spaces (Figure 1, C and D). Mitotic activity is either absent or very low. 13 Malignant types of SPN can be dangerous and fatal. Tang et al 14 reported fatal cases of SPN with unusual microscopic features including diffuse growth pattern in the solid areas of tumor with minimal supporting fibrovascular stroma; tumor necrosis in either a diffuse, geographic, or punctate pattern; increased nuclear to cytoplasmic ratio with hyperchromasia; and a high mitotic rate (up to 70 mitoses per 50 high-power fields). In another case report, Reindl et al 5 described an aggressive SPN with similar histologic features such as prominent nuclear atypia, increased proliferative index around 50%, and extensive necrosis. LYMPH NODE INVOLVEMENT Lymph node metastasis is rare in SPN, and it has been reported in only 5 cases. 5,13 15 Reindl et al 5 found 7 lymph nodes in an aggressive form of SPN, but none of them were positive for tumor. However, Tang et al 14 reported a case of fast-growing SPN with liver metastasis and lymph node metastasis. Searching for lymph nodes should be promptly considered in SPN with atypical cellular features, increased proliferative index, and extensive necrosis. Solid pseudopapillary neoplasms are classified as low-grade malignant neoplasms with good prognosis, so finding positive lymph nodes is very uncommon in this entity. ANCILLARY STUDIES The tumor cells demonstrate a wide range of immunophenotypes with variable degrees of heterogeneity. The cells of SPNs demonstrate strong positive staining for b-catenin, CD10, vimentin, a-1-antitrypsin, a-1-antichymotrypsin, neuron-specific enolase, and cyclin D1 (Figure 2, A through C). 5,16 Neoplastic cells harbor somatic point mutations in exon 3 of CTNNB1, the gene encoding b-catenin in Wnt signaling pathway, resulting in nuclear condensation of b- catenin and cyclin D1, and also loss of E-cadherin receptors on cellular membranes. 16 These changes will be detected by strong nuclear staining of b-catenin (Figure 2, A) and cyclin D1, and by loss of E-cadherin membranous staining in these tumor cells. 17,18 CD10 shows membranous positivity in almost all cases (Figure 2, B). 11 a-1-antitrypsin and a-1- antichymotrypsin have typically intense staining but only involve small cell clusters. 5 Some cases of SPN exhibit neuroendocrine differentiation by consistent staining with CD56 and occasional focal reactivity for synaptophysin (Figure 2, C). 3 Although there is a distinct female preponderance for SPN, estrogen receptor-a positivity is very uncommon, and most series report absence of 992 Arch Pathol Lab Med Vol 141, July 2017 Solid Pseudopapillary Neoplasm Dinarvand & Lai
4 immunoreactivity. On the other hand, progesterone receptor positivity is seen in almost all cases of SPN, irrespective of sex. Keratin expression is noted in 30% to 70% of cases. 5 Several investigators have demonstrated expression of neuron-specific enolase in SPN. 19 Kosmahl et al 20 demonstrated that 93% of the examined cases show staining with antibodies to neuron-specific enolase. Synaptophysin and chromogranin A are more specific for neuroendocrine tumors. Staining for synaptophysin, usually weak and focal, is reported in as many as 44% of SPNs. 19,21 The SPN cells are weakly positive for antibodies directed against chromogranin A in 38% of cases in some reports. 19,21 Electron Microscopy The tumor cells have many vacuoles in the cytoplasm with scattered organelles. Organelles such as mitochondria dissolve and form vacuoles. The tumor cells contain variable amounts of corpuscles, around 8 to 1.2 mm in diameter, which are covered by bound membranes. 16 Nuclear indentation and cleaving can be identified. 13 Molecular Pathway Despite numerous investigations, the origin of this neoplasm remains unclear. Distinctive molecular alterations such as the presence of CTNNB1 mutations are demonstrated in almost all cases; however, other genetic alterations found in ductal adenocarcinoma, such as KRAS, TP53, and SMAD4, are not involved in SPNs, demonstrating its different nature from other pancreatic neoplasms. Recent investigations on cellular signaling pathways have successfully demonstrated that activation of the Wnt/b-catenin pathway in these tumors is associated with the upregulation of genes required in Notch, Hedgehog, and androgen receptor signaling pathways. 22 The activation of the Wnt/bcatenin pathway in SPN has 2 main consequences. First, E- cadherin expression changes from a membranous to an intracytoplasmic localization. Second, GLUL expression is highly correlated with Wnt/b-catenin activation, demonstrating its faithfulness as a Wnt target gene. 23 Park et al 24 recently demonstrated the existence of new molecules involved in SPN. They analyzed 1686 (1119 upregulated and 567 down-regulated) genes differentially expressed in SPN, revealing that the Wnt/b-catenin, Hedgehog, and androgen receptor signaling pathways, as well as genes involved in epithelial mesenchymal transition, are activated in SPNs. They validated these results experimentally by assessing the expression of b-catenin, WIF-1, GLI2, androgen receptor, and epithelial-mesenchymal transition related markers with Western blot and immunohistochemistry. Their analysis also revealed 17 micrornas, especially the mir-200 family and mir-192/ 215, that were closely associated with the upregulated genes associated with the 3 pathways activated in SPN and epithelial-mesenchymal transition. 24 Role of mutational testing in diagnosis of SPN has not been extensively investigated yet, and future studies are needed in the current era of genomic pathology to characterize specific, clinically related mutations for this entity. DIFFERENTIAL DIAGNOSIS Diagnosis of SPN may be challenging, but careful interpretation of the histologic and/or cytologic features and staining patterns usually allows pathologists to make the diagnosis for this uncommon tumor. Distinguishing histologic characteristics of lesions commonly present in the differential diagnosis and steps needed to make a correct diagnosis, are outlined below and summarized in Figure 3. Immunostain panels to differentiate these entities are also described in Figure 3. Histologic features of pancreatic neuroendocrine neoplasms are very similar to SPNs, and it is often difficult for a pathologist to diagnose either one on the basis only of histology or cytology. 11 However, multiple architectural and cellular features, such as presence of pseudopapillae, hyaline globules, foamy histiocytes, and nuclear grooving, help us to favor SPN. 1 Presence of speckled (salt-and-pepper) chromatin favors neuroendocrine tumor. Immunohistochemistry panel is recommended by most investigators to differentiate these 2 entities. 5 Histologically, acinar cell carcinoma consists of acinar, trabecular, or solid proliferations of uniform tumor cells with diffuse granular cytoplasm. The nuclei are irregularly sized and maintain cytoplasmic polarity. 25 Observing cohesive clusters of acinic cells with granular cytoplasm, and with abundant acinar formation, is the key for the diagnosis of acinar cell carcinoma. 25 Pancreatoblastoma is a rare pancreatic tumor that primarily occurs in children, and histologically it is composed of epithelial cells surrounded by a fibrous stroma. The epithelial component consists of cells arranged in acini, sheets, and squamoid corpuscles. Fine-needle aspiration cytology reveals cohesive epithelial cells with both acinar and neuroendocrine features. 26 Squamoid corpuscles with intracellular accumulation of biotin, which make the characteristic nuclear clearing, is specific for pancreatoblastoma. Another differential diagnosis of SPN is serous cystadenoma. It is a circumscribed nodule, which consists of cystic spaces lined by cuboidal cells with clear cytoplasm (glycogen). The myoepithelial layer is present and cell islets are present between lobules, making a radiating pattern with central scar. 27 CURRENT TREATMENT Complete surgical excision is the treatment of choice for SPN. Reddy et al 28 successfully demonstrated that surgery was safe and associated with long-term survival. Depending on tumor location, different procedures are performed. In another report, SPNs with metastasis and vascular invasion were also successfully treated with surgery, and patients had a good outcome. 29 PROGNOSIS Solid pseudopapillary neoplasm is considered as a neoplasm of low malignant potential because of its low probability of metastasis and vascular invasion. 13 Local invasion to the adjacent structures or metastasis to other organs has been reported with 15% to 20% of SPNs. 2 The patients who have SPN usually have very good prognosis after surgery, even with local invasion or multiple metastasis. More than 95% of patients with SPN limited to the pancreas are cured by complete surgical excision. Resection is not contraindicated in the case of limited metastasis or local invasion. 1 Five-year survival rate is as high as 95% to 97%, with an estimated 10-year survival rate of approximately 93%. 19 Solid pseudopapillary neoplasms with treated liver metastases are usually associated with a lower survival rate Arch Pathol Lab Med Vol 141, July 2017 Solid Pseudopapillary Neoplasm Dinarvand & Lai 993
5 Figure 3. A step-by-step algorithm is a helpful tool for diagnosis of solid pseudopapillary neoplasm of the pancreas and differentiates it from other circumscribed tumors in the pancreas. Abbreviations: CEA, carcinoembryonic antigen; CK, cytokeratin; EMA, epithelial membrane antigen; N, nuclear; PAS, periodic acid Schiff; þ, positive. of 5 years. 30 Owing to its rare recurrence, statistically significant risk factors have not been established yet. 19 Multiple follow-ups are required for patients whose tumors have malignant potential, and active management is needed for patients with tumor recurrence. 5,19 CONCLUSIONS It is essential for a pathologist to know that SPN of the pancreas is an uncommon tumor with unknown origin, and with low malignant potential. Being familiar with its unique microscopic features, immunohistochemical panel, and how to differentiate it from other circumscribed pancreatic neoplasms, in particular neuroendocrine tumor, is critical knowledge. References 1. Chakhachiro ZI, Zaatari G. Solid-pseudopapillary neoplasm: a pancreatic enigma. Arch Pathol Lab Med. 2009;133(12): Papavramidis T, Papavramidis S. Solid pseudopapillary tumors of the pancreas: review of 718 patients reported in English literature. J Am Coll Surg. 2005;200(6): Santini D, Poli F, Lega S. Solid-papillary tumors of the pancreas: histopathology. JOP. 2006;7(1): Bosman FT, Carneiro F, Hruban RH, Theise ND. WHO Classification of Tumours of the Digestive System. Lyon, France: IARC Press; World Health Organization Classification of Tumours; vol Reindl BA, Lynch DW, Jassim AD. Aggressive variant of a solid pseudopapillary neoplasm: a case report and literature review. Arch Pathol Lab Med. 2014;138(7): Yan SX, Adair CF, Balani J, Mansour JC, Gokaslan ST. Solid pseudopapillary neoplasm collides with a well-differentiated pancreatic endocrine neoplasm in an adult man. Am J Clin Pathol. 2015;143(2): Lam KY, Lo CY, Fan ST. Pancreatic solid-cystic-papillary tumor: clinicopathologic features in eight patients from Hong Kong and review of the literature. World J Surg. 1999;23(10): Kawamoto S, Scudiere J, Hruban RH, Wolfgang CL, Cameron JL, Fishman EK. Solid-pseudopapillary neoplasm of the pancreas: spectrum of findings on multidetector CT. Clin Imaging. 2011;35(1): Guerrache Y, Soyer P, Dohan A, et al. Solid-pseudopapillary tumor of the pancreas: MR imaging findings in 21 patients. Clin Imaging. 2014;38(4): Lee J, Yu J-S, Kim H, et al. Solid pseudopapillary carcinoma of the pancreas: differentiation from benign solid pseudopapillary tumour using CT and MRI. Clin Radiol. 2008;63(9): Lai J-P, Fan X, Guindi M, Balzer B, Rutgers JK. Endoscopic ultrasound guided-fine needle aspiration (EUS-FNA), in comparison with gross and histologic diagnoses of pancreatic lesions. Am J Digest Dis. 2014;1(2): Samad A, Shah AA, Stelow EB, Alsharif M, Cameron SE, Pambuccian SE. Cercariform cells: another cytologic feature distinguishing solid pseudopapillary neoplasms from pancreatic endocrine neoplasms and acinar cell carcinomas in endoscopic ultrasound-guided fine-needle aspirates. Cancer Cytopathol. 2013; 121(6): Klimstra DS, Wenig BM, Heffess CS. Solid-pseudopapillary tumor of the pancreas: a typically cystic carcinoma of low malignant potential. Semin Diagn Pathol. 2000;17(1): Tang LH, Aydin H, Brennan MF, Klimstra DS. Clinically aggressive solid pseudopapillary tumors of the pancreas: a report of two cases with components of undifferentiated carcinoma and a comparative clinicopathologic analysis of 34 conventional cases. Am J Surg Pathol. 2005;29(4): Martin RC, Klimstra DS, Brennan MF, Conlon KC. Solid-pseudopapillary tumor of the pancreas: a surgical enigma? Ann Surg Oncol. 2002;9(1): Ye J, Ma M, Cheng D, et al. Solid-pseudopapillary tumor of the pancreas: clinical features, pathological characteristics, and origin. J Surg Oncol. 2012; 106(6): Arch Pathol Lab Med Vol 141, July 2017 Solid Pseudopapillary Neoplasm Dinarvand & Lai
6 17. Tiemann K, Heitling U, Kosmahl M, Klöppel G. Solid pseudopapillary neoplasms of the pancreas show an interruption of the Wnt-signaling pathway and express gene products of 11q. Mod Pathol. 2007;20(9): Tang WW, Stelter AA, French S, et al. Loss of cell-adhesion molecule complexes in solid pseudopapillary tumor of pancreas. Mod Pathol. 2007;20(5): Adams AL, Siegal GP, Jhala NC. Solid pseudopapillary tumor of the pancreas: a review of salient clinical and pathologic features. Adv Anat Pathol. 2008;15(1): Kosmahl M, Seada LS, Jänig U, Harms D, Klöppel G. Solid pseudopapillary tumor of the pancreas: its origin revisited. Virchows Arch. 2000;436(5): Burford H, Baloch Z, Liu X, Jhala D, Siegal GP, Jhala N. E-cadherin/bcatenin and CD10. Am J Clin Pathol. 2009;132(6): Terris B, Cavard C. Diagnosis and molecular aspects of solid-pseudopapillary neoplasms of the pancreas. Semin Diagn Pathol. 2014;31(6): Audard V, Cavard C, Richa H, et al. Impaired E-cadherin expression and glutamine synthetase overexpression in solid pseudopapillary neoplasm of the pancreas. Pancreas. 2008;36(1): Park M, Kim M, Hwang D, et al. Characterization of gene expression and activated signaling pathways in solid-pseudopapillary neoplasm of pancreas. Mod Pathol. 2014;27(4): Singhi AD, Norwood S, Liu T-C, et al. Acinar cell cystadenoma of the pancreas: a benign neoplasm or non-neoplastic ballooning of acinar and ductal epithelium? Am J Surg Pathol. 2013;37(9): Hammer ST, Owens SR. Pancreatoblastoma: a rare, adult pancreatic tumor with many faces. Arch Pathol Lab Med. 2013;137(9): Panarelli NC, Park KJ, Hruban RH, Klimstra DS. Microcystic serous cystadenoma of the pancreas with subtotal cystic degeneration: another neoplastic mimic of pancreatic pseudocyst. Am J Surg Pathol. 2012;36(5): Reddy S, Cameron JL, Scudiere J, et al. Surgical management of solidpseudopapillary neoplasms of the pancreas (Franz or Hamoudi tumors): a large single-institutional series. J Am Coll Surg. 2009;208(5): Cai H, Zhou M, Hu Y, et al. Solid-pseudopapillary neoplasms of the pancreas: clinical and pathological features of 33 cases. Surg Today. 2013;43(2): Yu P-F, Hu Z-H, Wang X-B, et al. Solid pseudopapillary tumor of the pancreas: a review of 553 cases in Chinese literature. World J Gastroenterol. 2010;16(10): Arch Pathol Lab Med Vol 141, July 2017 Solid Pseudopapillary Neoplasm Dinarvand & Lai 995
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