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.	Kl?ppel 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, Kl?ppel 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.	錢清富, 陳志奎, 張秀娟, 等. 胰腺神經內分泌腫瘤的超聲診斷分析. 中國超聲醫學雜志, 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.	楊道輝, 張琪, 于凌云, 等. 超聲造影診斷胰腺神經內分泌腫瘤的臨床應用價值. 腫瘤影像學, 2018, 27(3): 145-149.
18.	宋茜, 王化, 孫琳, 等. 胰腺神經內分泌腫瘤的多層螺旋 CT 表現及與不同病理分級的相關性. 中國醫學影像學雜志, 2017, 25(11): 807-810, 816.
19.	劉黎明, 唐艷華, 王海屹, 等. 多層 CT 對胰腺神經內分泌腫瘤病理分級的可行性. 中華放射學雜志, 2016, 50(2): 105-109.
20.	陳曉姍, 周建軍, 曾蒙蘇. 動態增強 CT 在胰腺神經內分泌腫瘤病理分級中的可行性研究. 放射學實踐, 2018, 33(2): 166-171.
21.	王齊艷, 黃子星, 吳明蓬, 等. 胰腺神經內分泌腫瘤的多層螺旋 CT 表現與其病理分級的關系. 中國普外基礎與臨床雜志, 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.	張永嫦, 于浩鵬, 李謀, 等. CT 圖像紋理分析鑒別乏血供胰腺神經內分泌腫瘤與胰腺導管腺癌. 中國普外基礎與臨床雜志, 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.	劉曦嬌, 王威亞, 黃子星, 等. 胰腺神經內分泌癌的影像學表現. 中國普外基礎與臨床雜志, 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. Kl?ppel 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, Kl?ppel 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. 錢清富, 陳志奎, 張秀娟, 等. 胰腺神經內分泌腫瘤的超聲診斷分析. 中國超聲醫學雜志, 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. 楊道輝, 張琪, 于凌云, 等. 超聲造影診斷胰腺神經內分泌腫瘤的臨床應用價值. 腫瘤影像學, 2018, 27(3): 145-149.
18. 宋茜, 王化, 孫琳, 等. 胰腺神經內分泌腫瘤的多層螺旋 CT 表現及與不同病理分級的相關性. 中國醫學影像學雜志, 2017, 25(11): 807-810, 816.
19. 劉黎明, 唐艷華, 王海屹, 等. 多層 CT 對胰腺神經內分泌腫瘤病理分級的可行性. 中華放射學雜志, 2016, 50(2): 105-109.
20. 陳曉姍, 周建軍, 曾蒙蘇. 動態增強 CT 在胰腺神經內分泌腫瘤病理分級中的可行性研究. 放射學實踐, 2018, 33(2): 166-171.
21. 王齊艷, 黃子星, 吳明蓬, 等. 胰腺神經內分泌腫瘤的多層螺旋 CT 表現與其病理分級的關系. 中國普外基礎與臨床雜志, 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. 張永嫦, 于浩鵬, 李謀, 等. CT 圖像紋理分析鑒別乏血供胰腺神經內分泌腫瘤與胰腺導管腺癌. 中國普外基礎與臨床雜志, 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. 劉曦嬌, 王威亞, 黃子星, 等. 胰腺神經內分泌癌的影像學表現. 中國普外基礎與臨床雜志, 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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