RADIOLOGICAL IMAGING METHODSIN PANCREATIC NEUROENDOCRINE TUMORS

Sezer Nil Yılmazer Zorlu

Mamak State Hospital, Department of Radiology, Ankara, Türkiye

Yılmazer Zorlu SN. Radiological Imaging Methods in Pancreatic Neuroendocrine Tumors. In: Gönüllü E, Karaman K, editors. Modern Approaches and Recent Advances in Neuroendocrine Tumors. 1st ed. Ankara: Türkiye Klinikleri; 2025. p.67-78.

ABSTRACT

Radiological imaging plays a crucial role in the detection, characterization, and staging of pancreatic neuroendocrine neoplasms (panNENs). Ultrasound (US), computed tomography (CT), and magnetic resonance imaging (MRI) are the primary anatomical imaging modalities used for the evaluation of these tumors. PanNENs typically appear as well-defined, hypervascular lesions on contrast-enhanced imaging. On US, they are detected as hypoechoic masses with hypervascularity on Doppler studies. In contrast-enhanced CT and MRI, they frequently demonstrate arterial-phase hyperenhancement due to their rich capillary network, with mild hyperattenuation in the portal venous phase. However, atypical imaging features may be encountered, including hypoenhancing lesions, cystic or calcified variants, and intraductal extension, which can mimic other pancreatic tumors such as pancreatic ductal adenocarcinoma. In the differential diagnosis, imaging features such as the clarity of tumor margins, as well as associated findings like ductal dilatation and pancreatic parenchymal atrophy, should be carefully evaluated. Imaging characteristics vary depending on the functional status and histological grade of the tumor. Functioning panNENs, such as insulinomas and gastrinomas, tend to be smaller and hypervascular, whereas non-functioning tumors are often larger, heterogeneous, and more likely to exhibit necrosis. Higher-grade tumors demonstrate aggressive imaging features, including larger size, poorly defined margins, lower apparent diffusion coefficient (ADC) values, low-to-intermediate signal intensity on T2-weighted images, heterogeneous enhancement on contrast-enhanced series, as well as accompanying bile duct dilatation and vascular invasion. Identifying these imaging features indicative of tumor aggressiveness is crucial for prognostic assessment. Beyond its role in the diagnosis of the primary tumor, radiological assessment is also essential for detecting metastatic disease, with the liver and lymph nodes being the most common metastatic sites. PanNEN liver metastases are typically hypervascular on arterial-phase imaging, whereas atypical metastases may present as isoor hypoattenuating lesions. Overall, radiological imaging remains a cornerstone in the diagnosis and management of panNENs. Recognizing both typical and atypical imaging characteristics, along with variations related to tumor functionality and histological grade, is crucial for accurate diagnosis, prognostic assessment, and therapeutic decision-making.

Keywords: Gastro-enteropancreatic neuroendocrine tumor; Pancreatic neoplasms; Neuroendocrine tumors; Radiology; Ultrasonography; Multidetector computed tomography; Magnetic resonance imaging

Referanslar

  1. Cives M, Strosberg JR. Gastroenteropancreatic neuroendocrine tumors. CA: a cancer journal for clinicians 2018;68(6):471-487. [Crossref]  [PubMed]
  2. Sahani DV, Bonaffini PA, Fernández-Del Castillo C, Blake MA. Gastroenteropancreatic neuroendocrine tumors: role of imaging in diagnosis and management. Radiology 2013;266(1):38-61. [Crossref]  [PubMed]
  3. Półtorak-Szymczak G, Budlewski T, Furmanek MI, et al. Radiological imaging of gastro-entero-pancreatic neuroendocrine tumors. The review of current literature emphasizing the diagnostic value of chosen imaging methods. Frontiers in Oncology 2021;11:670233. [Crossref]  [PubMed]  [PMC]
  4. Ciaravino V, De Robertis R, Tinazzi Martini P, et al. Imaging presentation of pancreatic neuroendocrine neoplasms. Insights into imaging 2018;9:943-953. [Crossref]  [PubMed]  [PMC]
  5. Lewis RB, Lattin Jr M, Grant E, Paal E. Pancreatic endocrine tumors: radiologic-clinicopathologic correlation. Radiographics 2010;30(6):1445-1464. [Crossref]  [PubMed]
  6. Melita G, Pallio S, Tortora A, Crinò SF, Macrì A, Dionigi G. Diagnostic and interventional role of endoscopic ultrasonography for the management of pancreatic neuroendocrine neoplasms. Journal of clinical medicine 2021;10(12):2638. [Crossref]  [PubMed]  [PMC]
  7. Sun MR, Brennan DD, Kruskal JB, Kane RA. Intraoperative ultrasonography of the pancreas. Radiographics 2010;30(7):1935-1953. [Crossref]  [PubMed]
  8. Tamm EP, Bhosale P, Lee JH, Rohren E. State-of-the-art imaging of pancreatic neuroendocrine tumors. Surgical oncology clinics of North America 2016;25(2):375. [Crossref]  [PubMed]  [PMC]
  9. Khanna L, Prasad SR, Sunnapwar A, et al. Pancreatic neuro endocrine neoplasms: 2020 update on pathologic and imaging findings and classification. Radiographics 2020;40(5):12401262. [Crossref]  [PubMed]
  10. Rockall AG, Reznek RH. Imaging of neuroendocrine tumours (CT/MR/US). Best practice & research Clinical endocrinology & metabolism 2007;21(1):43-68. [Crossref]  [PubMed]
  11. Singh A, Hines JJ, Friedman B. Multimodality imaging of the pancreatic neuroendocrine tumors. Seminars in Ultrasound, CT and MRI: Elsevier; 2019:469-482. [Crossref]  [PubMed]
  12. Garbino N, Brancato V, Salvatore M, Cavaliere C. A systematic review on the role of the perfusion computed tomography in abdominal cancer. Dose-Response 2021;19(4):15593258211056199. [Crossref]  [PubMed]  [PMC]
  13. Mastrodicasa D, Pizzi AD, Patel BN. Dual-energy CT of the pancreas. Seminars in Ultrasound, CT and MRI: Elsevier; 2019:509-514. [Crossref]  [PubMed]
  14. Wan Y, Hao H, Meng S, et al. Application of low dose pancreas perfusion CT combined with enhancement scanning in diagnosis of pancreatic neuroendocrine tumors. Pancreatology 2021;21(1):240-245. [Crossref]  [PubMed]
  15. Wan Y, Hao H, Chen Y, Zhang Y, Yue Q, Li Z. Application of spectral CT combined with perfusion scan in diagnosis of pancreatic neuroendocrine tumors. Insights into Imaging 2022;13(1):145. [Crossref]  [PubMed]  [PMC]
  16. Fang JM, Shi J. A clinicopathologic and molecular update of pancreatic neuroendocrine neoplasms with a focus on the new World Health Organization classification. Archives of pathology & laboratory medicine 2019;143(11):1317-1326. [Crossref]  [PubMed]  [PMC]
  17. Frizziero M, Chakrabarty B, Nagy B, et al. Mixed neuroendocrine non-neuroendocrine neoplasms: a systematic review of a controversial and underestimated diagnosis. Journal of clinical medicine 2020;9(1):273. [Crossref]  [PubMed]  [PMC]
  18. Lee L, Ito T, Jensen RT. Imaging of pancreatic neuroendocrine tumors: recent advances, current status, and controversies. Expert review of anticancer therapy 2018;18(9):837860. [Crossref]  [PubMed]  [PMC]
  19. Kulali F, Semiz-Oysu A, Demir M, Segmen-Yilmaz M, Bukte Y. Role of diffusion-weighted MR imaging in predicting the grade of nonfunctional pancreatic neuroendocrine tumors. Diagnostic and interventional imaging 2018;99(5):301-309. [Crossref]  [PubMed]
  20. Nakashima Y, Ohtsuka T, Nakamura S, et al. Clinicopathological characteristics of non-functioning cystic pancreatic neuroendocrine tumors. Pancreatology 2019;19(1):50-56. [Crossref]  [PubMed]
  21. Makris EA, Cannon JGD, Norton JA, et al. Calcifications and cystic morphology on preoperative imaging predict survival after resection of pancreatic neuroendocrine tumors. Annals of surgical oncology 2023;30(4):2424-2430. [Crossref]  [PubMed]
  22. Choe J, Kim KW, Kim HJ, et al. What is new in the 2017 World Health Organization classification and 8th American Joint Committee on Cancer staging system for pancreatic neuroendocrine neoplasms? Korean journal of radiology 2019;20(1):5-17. [Crossref]  [PubMed]  [PMC]
  23. Cappelli C, Boggi U, Mazzeo S, et al. Contrast enhancement pattern on multidetector CT predicts malignancy in pancreatic endocrine tumours. European radiology 2015;25:751-759. [Crossref]  [PubMed]
  24. Zhao W, Quan Z, Huang X, et al. Grading of pancreatic neuroendocrine neoplasms using pharmacokinetic parameters derived from dynamic contrast-enhanced MRI. Oncology Letters 2018;15(6):8349-8356. [Crossref]  [PubMed]  [PMC]
  25. Daskalakis K. Functioning and nonfunctioning pNENs. Current Opinion in Endocrine and Metabolic Research 2021;18:284-290. [Crossref]
  26. Bicci E, Cozzi D, Ferrari R, Grazzini G, Pradella S, Miele V. Pancreatic neuroendocrine tumours: spectrum of imaging findings. Gland Surgery 2020;9(6):2215. [Crossref]  [PubMed]  [PMC]
  27. D'Onofrio M, De Robertis R, Capelli P, et al. Uncommon presentations of common pancreatic neoplasms: a pictorial essay. Abdominal imaging 2015;40:1629-1644. [Crossref]  [PubMed]
  28. Jeon SK, Lee JM, Joo I, et al. Nonhypervascular pancreatic neuroendocrine tumors: differential diagnosis from pancreatic ductal adenocarcinomas at MR imaging-retrospective cross-sectional study. Radiology 2017;284(1):77-87. [Crossref]  [PubMed]
  29. Saleh M, Bhosale PR, Yano M, et al. New frontiers in imaging including radiomics updates for pancreatic neuroendocrine neoplasms. Abdominal Radiology 2020:1-23. [Crossref]  [PubMed]
  30. Guo C, Zhuge X, Wang Q, et al. The differentiation of pancreatic neuroendocrine carcinoma from pancreatic ductal adenocarcinoma: the values of CT imaging features and texture analysis. Cancer Imaging 2018;18:1-6. [Crossref]  [PubMed]  [PMC]
  31. Li J, Lu J, Liang P, et al. Differentiation of atypical pancreatic neuroendocrine tumors from pancreatic ductal adenocarcinomas: Using whole-tumor CT texture analysis as quantitative biomarkers. Cancer medicine 2018;7(10):4924-4931. [Crossref]  [PubMed]  [PMC]
  32. Kim B, Lee SS, Sung YS, et al. Intravoxel incoherent motion diffusion-weighted imaging of the pancreas: characterization of benign and malignant pancreatic pathologies. Journal of Magnetic Resonance Imaging 2017;45(1):260-269. [Crossref]  [PubMed]
  33. Ma W, Wei M, Han Z, et al. The added value of intravoxel incoherent motion diffusion weighted imaging parameters in differentiating high-grade pancreatic neuroendocrine neoplasms from pancreatic ductal adenocarcinoma. Oncology letters 2019;18(5):5448-5458. [Crossref]  [PubMed]  [PMC]
  34. Chetty R, El-Shinnawy I. Intraductal pancreatic neuroendocrine tumor. Endocrine pathology 2009;20:262-266. [Crossref]  [PubMed]
  35. Shi C, Siegelman SS, Kawamoto S, et al. Pancreatic duct stenosis secondary to small endocrine neoplasms: a manifestation of serotonin production? Radiology 2010;257(1):107-114. [Crossref]  [PubMed]  [PMC]
  36. De Robertis R, Paiella S, Cardobi N, et al. Tumor thrombosis: a peculiar finding associated with pancreatic neuroendocrine neoplasms. A pictorial essay. Abdominal Radiology 2018;43(3):613-619. [Crossref]  [PubMed]
  37. Caglia P, Cannizzaro MT, Tracia A, et al. Cystic pancreatic neuroendocrine tumors: To date a diagnostic challenge. International Journal of Surgery 2015;21:S44-S49. [Crossref]  [PubMed]
  38. Raman SP, Hruban RH, Cameron JL, Wolfgang CL, Fishman EK. Pancreatic imaging mimics: part 2, pancreatic neuroendocrine tumors and their mimics. American Journal of Roentgenology 2012;199(2):309-318. [Crossref]  [PubMed]
  39. Prosperi D, Gentiloni Silveri G, Panzuto F, et al. Nuclear medicine and radiological imaging of pancreatic neuroendocrine neoplasms: a multidisciplinary update. Journal of Clinical Medicine 2022;11(22):6836. [Crossref]  [PubMed]  [PMC]
  40. Dromain C, de Baere T, Baudin E, et al. MR imaging of hepatic metastases caused by neuroendocrine tumors: comparing four techniques. American Journal of Roentgenology 2003;180(1):121-128. [Crossref]  [PubMed]
  41. Altieri B, Di Dato C, Martini C, et al. Bone metastases in neuroendocrine neoplasms: from pathogenesis to clinical management. Cancers 2019;11(9):1332. [Crossref]  [PubMed]  [PMC]