Pancreatic neuroendocrine neoplasm: current status and advancement in imaging_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

CHENG Yue , HUANG Zixing ,  SONG Bin

Department of Radiology, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

SONG Bin, Email: cjr.songbin@vip.163.com

Keywords：

pancreas neuroendocrine neoplasm; imaging; pathological grade; CT; MRI; ultrasound; PET-CT

DOI：

10.7507/1007-9424.202001070

Video：

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Objective To summarize the status and progress of imaging studies of pancreatic neuroendocrine neoplasms (pNENs).Method The relevant literatures published recently at domestic and abroad about the imaging of pNENs were collected and reviewed.Results Due to poor visibility of pancreatic body and tail, the application of ultrasound (US) was limited. Compared with US, endoscopic ultrasound (EUS) and contrast-enhanced ultrasound (CEUS) could improve the detection rate of pNENs. The ability of plain CT scans to differentiate pathological grades was still controversial, but the value of enhanced scan was higher. CT texture analysis was feasible in the discrimination of nonhypervascular pNENs and pancreatic ductal adenocarcinoma (PDAC). Teta2 was the parameter with the highest diagnostic performance. The enhanced features of MRI were similar to CT. Combined with the apparent diffusion coefficient (ADC) value, the diagnostic and classification capabilities of MRI were improved, and the sensitivity and specificity of different ADC thresholds were also different. ⁶⁸Ga-tetraazacyclododecane tetraacetic acid (⁶⁸Ga-DOTA) peptide PET-CT had good preliminary diagnostic value for well-differentiated pNENs, and ¹⁸Fluoro-fluorodeoxyglucose (¹⁸F-FDG) PET-CT had limited diagnostic value.Conclusions Somatostatin receptor imaging is of high diagnostic value and can guide clinical treatment and predict prognosis, but it has not been widely used in China. Conventional morphological images have advantages in the diagnosis and classification of pNENs. Therefore, it is important to choose a proper image inspection method.

Citation： CHENG Yue, HUANG Zixing, SONG Bin. Pancreatic neuroendocrine neoplasm: current status and advancement in imaging. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(4): 489-493. doi: 10.7507/1007-9424.202001070 Copy

1.	Fesinmeyer MD, Austin MA, Li CI, et al. Differences in survival by histologic type of pancreatic cancer. Cancer Epidemiol Biomarkers Prev, 2005, 14(7): 1766-1773.
2.	Klöppel G. Classification and pathology of gastroenteropancreatic neuroendocrine neoplasms. Endocr Relat Cancer, 2011, 18(Suppl 1): S1-S16.
3.	Tan EH, Tan CH. Imaging of gastroenteropancreatic neuroendocrine tumors. World J Clin Oncol, 2011, 2(1): 28-43.
4.	Lloyd RV, Osamura RY, Klöppel G, et al. WHO classification of tumours of endocrine organs. 4^th ed. Lyon: IARC press, 2017: 1-355.
5.	Pitre J, Soubrane O, Palazzo L, et al. Endoscopic ultrasonography for the preoperative localization of insulinomas. Pancreas, 1996, 13(1): 55-60.
6.	Buetow PC, Miller DL, Parrino TV, et al. Islet cell tumors of the pancreas: clinical, radiologic, and pathologic correlation in diagnosis and localization. Radiographics, 1997, 17(2): 453-472.
7.	Fidler JL, Fletcher JG, Reading CC, et al. Preoperative detection of pancreatic insulinomas on multiphasic helical CT. AJR Am J Roentgenol, 2003, 181(3): 775-780.
8.	Mansour JC, Chen H. Pancreatic endocrine tumors. J Surg Res, 2004, 120: 139-161.
9.	钱清富, 陈志奎, 张秀娟, 等. 胰腺神经内分泌肿瘤的超声诊断分析. 中国超声医学杂志, 2019, 35(6): 524-527.
10.	Kulke MH, Anthony LB, Bushnell DL, et al. NANETS treatment guidelines: well-differentiated neuroendocrine tumors of the stomach and pancreas. Pancreas, 2010, 39(6): 735-752.
11.	Gouya H, Vignaux O, Augui J, et al. CT, endoscopic sonography, and a combined protocol for preoperative evaluation of pancreatic insulinomas. AJR Am J Roentgenol, 2003, 181(4): 987-992.
12.	Anderson MA, Carpenter S, Thompson NW, et al. Endoscopic ultrasound is highly accurate and directs management in patients with neuroendocrine tumors of the pancreas. Am J Gastroenterol, 2000, 95(9): 2271-2277.
13.	McAuley G, Delaney H, Colville J, et al. Multimodality preoperative imaging of pancreatic insulinomas. Clin Radiol, 2005, 60(10): 1039-1050.
14.	Zimmer T, Scherübl H, Faiss S, et al. Endoscopic ultrasonography of neuroendocrine tumours. Digestion, 2000, 62(Suppl 1): 45-50.
15.	Chen CH, Yang CC, Yeh YH, et al. Contrast-enhanced power Doppler sonography of ductal pancreatic adenocarcinomas: correlation with digital subtraction angiography findings. J Clin Ultrasound, 2004, 32(4): 179-185.
16.	D’Onofrio M, Malagò R, Zamboni G, et al. Contrast-enhanced ultrasonography better identifies pancreatic tumor vascularization than helical CT. Pancreatology, 2005, 5(4-5): 398-402.
17.	杨道辉, 张琪, 于凌云, 等. 超声造影诊断胰腺神经内分泌肿瘤的临床应用价值. 肿瘤影像学, 2018, 27(3): 145-149.
18.	宋茜, 王化, 孙琳, 等. 胰腺神经内分泌肿瘤的多层螺旋 CT 表现及与不同病理分级的相关性. 中国医学影像学杂志, 2017, 25(11): 807-810, 816.
19.	刘黎明, 唐艳华, 王海屹, 等. 多层 CT 对胰腺神经内分泌肿瘤病理分级的可行性. 中华放射学杂志, 2016, 50(2): 105-109.
20.	陈晓姗, 周建军, 曾蒙苏. 动态增强 CT 在胰腺神经内分泌肿瘤病理分级中的可行性研究. 放射学实践, 2018, 33(2): 166-171.
21.	王齐艳, 黄子星, 吴明蓬, 等. 胰腺神经内分泌肿瘤的多层螺旋 CT 表现与其病理分级的关系. 中国普外基础与临床杂志, 2016, 23(2): 243-247.
22.	Kim DW, Kim HJ, Kim KW, et al. Neuroendocrine neoplasms of the pancreas at dynamic enhanced CT: comparison between grade 3 neuroendocrine carcinoma and grade 1/2 neuroendocrine tumour. Eur Radiol, 2015, 25(5): 1375-1383.
23.	Humphrey PE, Alessandrino F, Bellizzi AM, et al. Non-hyperfunctioning pancreatic endocrine tumors: multimodality imaging features with histopathological correlation. Abdom Imaging, 2015, 40(7): 2398-2410.
24.	张永嫦, 于浩鹏, 李谋, 等. CT 图像纹理分析鉴别乏血供胰腺神经内分泌肿瘤与胰腺导管腺癌. 中国普外基础与临床杂志, 2018, 25(6): 748-753.
25.	Guo C, Zhuge X, Wang Z, et al. Textural analysis on contrast-enhanced CT in pancreatic neuroendocrine neoplasms: association with WHO grade. Abdom Radiol (NY), 2019, 44(2): 576-585.
26.	D’Onofrio M, Ciaravino V, Cardobi N, et al. CT Enhancement and 3D texture analysis of pancreatic neuroendocrine neoplasms. Sci Rep, 2019, 9(1): 2176.
27.	刘曦娇, 王威亚, 黄子星, 等. 胰腺神经内分泌癌的影像学表现. 中国普外基础与临床杂志, 2012, 19(10): 1126-1129.
28.	Owen NJ, Sohaib SA, Peppercorn PD, et al. MRI of pancreatic neuroendocrine tumours. Br J Radiol, 2001, 74(886): 968-973.
29.	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.
30.	Wang Y, Chen ZE, Yaghmai V, et al. Diffusion-weighted MR imaging in pancreatic endocrine tumors correlated with histopathologic characteristics. J Magn Reson Imaging, 2011, 33(5): 1071-1079.
31.	Jang KM, Kim SH, Lee SJ, et al. The value of gadoxetic acid-enhanced and diffusion-weighted MRI for prediction of grading of pancreatic neuroendocrine tumors. Acta Radiol, 2014, 55(2): 140-148.
32.	Guo C, Chen X, Xiao W, et al. Pancreatic neuroendocrine neo-plasms at magnetic resonance imaging: comparison between grade 3 and grade 1/2 tumors. Onco Targets Ther, 2017, 10: 1465-1474.
33.	Kim JH, Eun HW, Kim YJ, et al. Staging accuracy of MR for pancreatic neuroendocrine tumor and imaging findings according to the tumor grade. Abdom Imaging, 2013, 38(5): 1106-1114.
34.	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. Oncol Lett, 2019, 18(5): 5448-5458.
35.	Papotti M, Bongiovanni M, Volante M, et al. Expression of somatostatin receptor types 1-5 in 81 cases of gastrointestinal and pancreatic endocrine tumors. A correlative immunohistochemical and reverse-transcriptase polymerase chain reaction analysis. Virchows Arch, 2002, 440(5): 461-475.
36.	Modlin IM, Oberg K, Chung DC, et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol, 2008, 9(1): 61-72.
37.	Geijer H, Breimer LH. Somatostatin receptor PET/CT in neuroendocrine tumours: update on systematic review and meta-analysis. Eur J Nucl Med Mol Imaging, 2013, 40(11): 1770-1780.
38.	Kumar R, Sharma P, Garg P, et al. Role of (68)Ga-DOTATOC PET-CT in the diagnosis and staging of pancreatic neuroendocrine tumours. Eur Radiol, 2011, 21(11): 2408-2416.
39.	Wild D, Bomanji JB, Benkert P, et al. Comparison of ⁶⁸Ga-DOTANOC and ⁶⁸Ga-DOTATATE PET/CT within patients with gastroenteropancreatic neuroendocrine tumors. J Nucl Med, 2013, 54(3): 364-372.
40.	Yang J, Kan Y, Ge BH, et al. Diagnostic role of Gallium-68 DOTATOC and Gallium-68 DOTATATE PET in patients with neuroendocrine tumors: a meta-analysis. Acta Radiol, 2014, 55(4): 389-398.
41.	Schmid-Tannwald C, Schmid-Tannwald CM, Morelli JN, et al. Comparison of abdominal MRI with diffusion-weighted imaging to ⁶⁸Ga-DOTATATE PET/CT in detection of neuroendocrine tumors of the pancreas. Eur J Nucl Med Mol Imaging, 2013, 40(6): 897-907.
42.	Hindié E. The NETPET score: combining FDG and somatostatin receptor imaging for optimal management of patients with metastatic well-differentiated neuroendocrine tumors. Theranostics, 2017, 7(5): 1159-1163.
43.	Bucau M, Laurent-Bellue A, Poté N, et al. ¹⁸F-FDG uptake in well-differentiated neuroendocrine tumors correlates with both Ki-67 and VHL pathway inactivation. Neuroendocrinology, 2018, 106(3): 274-282.
44.	Zimny M, Bares R, Fass J, et al. Fluorine-18 fluorodeoxyglucose positron emission tomography in the differential diagnosis of pancreatic carcinoma: a report of 106 cases. Eur J Nucl Med, 1997, 24(6): 678-682.

1. Fesinmeyer MD, Austin MA, Li CI, et al. Differences in survival by histologic type of pancreatic cancer. Cancer Epidemiol Biomarkers Prev, 2005, 14(7): 1766-1773.
2. Klöppel G. Classification and pathology of gastroenteropancreatic neuroendocrine neoplasms. Endocr Relat Cancer, 2011, 18(Suppl 1): S1-S16.
3. Tan EH, Tan CH. Imaging of gastroenteropancreatic neuroendocrine tumors. World J Clin Oncol, 2011, 2(1): 28-43.
4. Lloyd RV, Osamura RY, Klöppel G, et al. WHO classification of tumours of endocrine organs. 4^th ed. Lyon: IARC press, 2017: 1-355.
5. Pitre J, Soubrane O, Palazzo L, et al. Endoscopic ultrasonography for the preoperative localization of insulinomas. Pancreas, 1996, 13(1): 55-60.
6. Buetow PC, Miller DL, Parrino TV, et al. Islet cell tumors of the pancreas: clinical, radiologic, and pathologic correlation in diagnosis and localization. Radiographics, 1997, 17(2): 453-472.
7. Fidler JL, Fletcher JG, Reading CC, et al. Preoperative detection of pancreatic insulinomas on multiphasic helical CT. AJR Am J Roentgenol, 2003, 181(3): 775-780.
8. Mansour JC, Chen H. Pancreatic endocrine tumors. J Surg Res, 2004, 120: 139-161.
9. 钱清富, 陈志奎, 张秀娟, 等. 胰腺神经内分泌肿瘤的超声诊断分析. 中国超声医学杂志, 2019, 35(6): 524-527.
10. Kulke MH, Anthony LB, Bushnell DL, et al. NANETS treatment guidelines: well-differentiated neuroendocrine tumors of the stomach and pancreas. Pancreas, 2010, 39(6): 735-752.
11. Gouya H, Vignaux O, Augui J, et al. CT, endoscopic sonography, and a combined protocol for preoperative evaluation of pancreatic insulinomas. AJR Am J Roentgenol, 2003, 181(4): 987-992.
12. Anderson MA, Carpenter S, Thompson NW, et al. Endoscopic ultrasound is highly accurate and directs management in patients with neuroendocrine tumors of the pancreas. Am J Gastroenterol, 2000, 95(9): 2271-2277.
13. McAuley G, Delaney H, Colville J, et al. Multimodality preoperative imaging of pancreatic insulinomas. Clin Radiol, 2005, 60(10): 1039-1050.
14. Zimmer T, Scherübl H, Faiss S, et al. Endoscopic ultrasonography of neuroendocrine tumours. Digestion, 2000, 62(Suppl 1): 45-50.
15. Chen CH, Yang CC, Yeh YH, et al. Contrast-enhanced power Doppler sonography of ductal pancreatic adenocarcinomas: correlation with digital subtraction angiography findings. J Clin Ultrasound, 2004, 32(4): 179-185.
16. D’Onofrio M, Malagò R, Zamboni G, et al. Contrast-enhanced ultrasonography better identifies pancreatic tumor vascularization than helical CT. Pancreatology, 2005, 5(4-5): 398-402.
17. 杨道辉, 张琪, 于凌云, 等. 超声造影诊断胰腺神经内分泌肿瘤的临床应用价值. 肿瘤影像学, 2018, 27(3): 145-149.
18. 宋茜, 王化, 孙琳, 等. 胰腺神经内分泌肿瘤的多层螺旋 CT 表现及与不同病理分级的相关性. 中国医学影像学杂志, 2017, 25(11): 807-810, 816.
19. 刘黎明, 唐艳华, 王海屹, 等. 多层 CT 对胰腺神经内分泌肿瘤病理分级的可行性. 中华放射学杂志, 2016, 50(2): 105-109.
20. 陈晓姗, 周建军, 曾蒙苏. 动态增强 CT 在胰腺神经内分泌肿瘤病理分级中的可行性研究. 放射学实践, 2018, 33(2): 166-171.
21. 王齐艳, 黄子星, 吴明蓬, 等. 胰腺神经内分泌肿瘤的多层螺旋 CT 表现与其病理分级的关系. 中国普外基础与临床杂志, 2016, 23(2): 243-247.
22. Kim DW, Kim HJ, Kim KW, et al. Neuroendocrine neoplasms of the pancreas at dynamic enhanced CT: comparison between grade 3 neuroendocrine carcinoma and grade 1/2 neuroendocrine tumour. Eur Radiol, 2015, 25(5): 1375-1383.
23. Humphrey PE, Alessandrino F, Bellizzi AM, et al. Non-hyperfunctioning pancreatic endocrine tumors: multimodality imaging features with histopathological correlation. Abdom Imaging, 2015, 40(7): 2398-2410.
24. 张永嫦, 于浩鹏, 李谋, 等. CT 图像纹理分析鉴别乏血供胰腺神经内分泌肿瘤与胰腺导管腺癌. 中国普外基础与临床杂志, 2018, 25(6): 748-753.
25. Guo C, Zhuge X, Wang Z, et al. Textural analysis on contrast-enhanced CT in pancreatic neuroendocrine neoplasms: association with WHO grade. Abdom Radiol (NY), 2019, 44(2): 576-585.
26. D’Onofrio M, Ciaravino V, Cardobi N, et al. CT Enhancement and 3D texture analysis of pancreatic neuroendocrine neoplasms. Sci Rep, 2019, 9(1): 2176.
27. 刘曦娇, 王威亚, 黄子星, 等. 胰腺神经内分泌癌的影像学表现. 中国普外基础与临床杂志, 2012, 19(10): 1126-1129.
28. Owen NJ, Sohaib SA, Peppercorn PD, et al. MRI of pancreatic neuroendocrine tumours. Br J Radiol, 2001, 74(886): 968-973.
29. 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.
30. Wang Y, Chen ZE, Yaghmai V, et al. Diffusion-weighted MR imaging in pancreatic endocrine tumors correlated with histopathologic characteristics. J Magn Reson Imaging, 2011, 33(5): 1071-1079.
31. Jang KM, Kim SH, Lee SJ, et al. The value of gadoxetic acid-enhanced and diffusion-weighted MRI for prediction of grading of pancreatic neuroendocrine tumors. Acta Radiol, 2014, 55(2): 140-148.
32. Guo C, Chen X, Xiao W, et al. Pancreatic neuroendocrine neo-plasms at magnetic resonance imaging: comparison between grade 3 and grade 1/2 tumors. Onco Targets Ther, 2017, 10: 1465-1474.
33. Kim JH, Eun HW, Kim YJ, et al. Staging accuracy of MR for pancreatic neuroendocrine tumor and imaging findings according to the tumor grade. Abdom Imaging, 2013, 38(5): 1106-1114.
34. 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. Oncol Lett, 2019, 18(5): 5448-5458.
35. Papotti M, Bongiovanni M, Volante M, et al. Expression of somatostatin receptor types 1-5 in 81 cases of gastrointestinal and pancreatic endocrine tumors. A correlative immunohistochemical and reverse-transcriptase polymerase chain reaction analysis. Virchows Arch, 2002, 440(5): 461-475.
36. Modlin IM, Oberg K, Chung DC, et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol, 2008, 9(1): 61-72.
37. Geijer H, Breimer LH. Somatostatin receptor PET/CT in neuroendocrine tumours: update on systematic review and meta-analysis. Eur J Nucl Med Mol Imaging, 2013, 40(11): 1770-1780.
38. Kumar R, Sharma P, Garg P, et al. Role of (68)Ga-DOTATOC PET-CT in the diagnosis and staging of pancreatic neuroendocrine tumours. Eur Radiol, 2011, 21(11): 2408-2416.
39. Wild D, Bomanji JB, Benkert P, et al. Comparison of ⁶⁸Ga-DOTANOC and ⁶⁸Ga-DOTATATE PET/CT within patients with gastroenteropancreatic neuroendocrine tumors. J Nucl Med, 2013, 54(3): 364-372.
40. Yang J, Kan Y, Ge BH, et al. Diagnostic role of Gallium-68 DOTATOC and Gallium-68 DOTATATE PET in patients with neuroendocrine tumors: a meta-analysis. Acta Radiol, 2014, 55(4): 389-398.
41. Schmid-Tannwald C, Schmid-Tannwald CM, Morelli JN, et al. Comparison of abdominal MRI with diffusion-weighted imaging to ⁶⁸Ga-DOTATATE PET/CT in detection of neuroendocrine tumors of the pancreas. Eur J Nucl Med Mol Imaging, 2013, 40(6): 897-907.
42. Hindié E. The NETPET score: combining FDG and somatostatin receptor imaging for optimal management of patients with metastatic well-differentiated neuroendocrine tumors. Theranostics, 2017, 7(5): 1159-1163.
43. Bucau M, Laurent-Bellue A, Poté N, et al. ¹⁸F-FDG uptake in well-differentiated neuroendocrine tumors correlates with both Ki-67 and VHL pathway inactivation. Neuroendocrinology, 2018, 106(3): 274-282.
44. Zimny M, Bares R, Fass J, et al. Fluorine-18 fluorodeoxyglucose positron emission tomography in the differential diagnosis of pancreatic carcinoma: a report of 106 cases. Eur J Nucl Med, 1997, 24(6): 678-682.

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Pancreatic neuroendocrine neoplasm: current status and advancement in imaging

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