Korean Journal of Radiology

The Korean Society of Radiology (대한영상의학회)
권호 표지
DOI QR코드

DOI QR Code

What Is New in the 2017 World Health Organization Classification and 8th American Joint Committee on Cancer Staging System for Pancreatic Neuroendocrine Neoplasms?

  • Jooae Choe (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Kyung Won Kim (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Hyoung Jung Kim (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Dong Wook Kim (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Kyu Pyo Kim (Department of Oncology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Seung-Mo Hong (Department of Pathology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Jin-Sook Ryu (Department of Nuclear Medicine, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Sree Harsha Tirumani (Department of Imaging, Dana-Farber Cancer Institute, Brigham and Women's Hospital, Harvard Medical School) ;
  • Katherine Krajewski (Department of Imaging, Dana-Farber Cancer Institute, Brigham and Women's Hospital, Harvard Medical School) ;
  • Nikhil Ramaiya (Department of Imaging, UH Cleveland Medical Center, Case Western Reserve University)
  • Received : 2018.01.14
  • Accepted : 2018.07.09
  • Published : 2019.01.01
Download PDF
⟨ Previous Next ⟩

Abstract

The diagnosis and management of pancreatic neuroendocrine neoplasms (NENs) have evolved significantly in recent years. There are several diagnostic and therapeutic challenges and controversies regarding the management of these lesions. In this review, we focus on the recent significant changes and controversial issues regarding the diagnosis and management of NENs and discuss the role of imaging in the multidisciplinary team approach.

Keywords

Acknowledgement

This study was supported by the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (No. HI18C1216) and a grant from the Asan Institute for Life Sciences, Asan Medical Center (No. 2015-0636).

References

  1. Singhi AD, Klimstra DS. Well-differentiated pancreatic neuroendocrine tumours (PanNETs) and poorly differentiated pancreatic neuroendocrine carcinomas (PanNECs): concepts, issues and a practical diagnostic approach to high-grade (G3) cases. Histopathology 2018;72:168-177 https://doi.org/10.1111/his.13408
  2. Lawrence B, Gustafsson BI, Chan A, Svejda B, Kidd M, Modlin IM. The epidemiology of gastroenteropancreatic neuroendocrine tumors. Endocrinol Metab Clin N Am 2011;40:1-18 https://doi.org/10.1016/j.ecl.2010.12.005
  3. Bosman FT, Carneiro F, Hruban RH, Theise ND. WHO classification of tumours of the digestive system, 4th ed. Lyon: International Agency for Research on Cancer, 2010
  4. Klimstra DS, Modlin IR, Coppola D, Lloyd RV, Suster S. The pathologic classification of neuroendocrine tumors: a review of nomenclature, grading, and staging systems. Pancreas 2010;39:707-712 https://doi.org/10.1097/MPA.0b013e3181ec124e
  5. Edge S, Byrd DR, Compton CC, Fritz AG, Greene F, Trotti A. AJCC cancer staging manual, 7th ed. New York, NY: Springer, 2010:181-190
  6. Rindi G, Kloppel G, Alhman H, Caplin M, Couvelard A, de Herder WW, et al.; all other Frascati Consensus Conference participants; European Neuroendocrine Tumor Society (ENETS). TNM staging of foregut (neuro)endocrine tumors: a consensus proposal including a grading system. Virchows Arch 2006;449:395-401 https://doi.org/10.1007/s00428-006-0250-1
  7. Klimstra DS, Modlin IR, Adsay NV, Chetty R, Deshpande V, Gonen M, et al. Pathology reporting of neuroendocrine tumors: application of the Delphic consensus process to the development of a minimum pathology data set. Am J Surg Pathol 2010;34:300-313 https://doi.org/10.1097/PAS.0b013e3181ce1447
  8. Kloppel G, Couvelard A, Perren A, Komminoth P, McNicol AM, Nilsson O, et al.; Mallorca Consensus Conference participants; European Neuroendocrine Tumor Society. ENETS consensus guidelines for the standards of care in neuroendocrine tumors: towards a standardized approach to the diagnosis of gastroenteropancreatic neuroendocrine tumors and their prognostic stratification. Neuroendocrinology 2009;90:162-166 https://doi.org/10.1159/000182196
  9. NCCN clinical practice guidelines in oncology. Neuroendocrine tumors. Version 3. National Comprehensive Cancer Network Web site. https://www.nccn.org/professionals/physician_gls/pdf/neuroendocrine.pdf. Published June 13, 2017. Accessed December 16, 2017
  10. Lloyd RV, Osamura RY, Kloppel G, Rosai J. WHO classification of tumours of endocrine organs, 4th ed. Lyon: International Agency for Research on Cancer, 2017:209-240
  11. Basturk O, Yang Z, Tang LH, Hruban RH, Adsay V, McCall CM, et al. The high-grade (WHO G3) pancreatic neuroendocrine tumor category is morphologically and biologically heterogenous and includes both well differentiated and poorly differentiated neoplasms. Am J Surg Pathol 2015;39:683-690 https://doi.org/10.1097/PAS.0000000000000408
  12. Adsay NV, Bagci P, Tajiri T, Oliva I, Ohike N, Balci S, et al. Pathologic staging of pancreatic, ampullary, biliary, and gallbladder cancers: pitfalls and practical limitations of the current AJCC/UICC TNM staging system and opportunities for improvement. Semin Diagn Pathol 2012;29:127-141 https://doi.org/10.1053/j.semdp.2012.08.010
  13. Rindi G, Falconi M, Klersy C, Albarello L, Boninsegna L, Buchler MW, et al. TNM staging of neoplasms of the endocrine pancreas: results from a large international cohort study. J Natl Cancer Inst 2012;104:764-777 https://doi.org/10.1093/jnci/djs208
  14. Li X, Gou S, Liu Z, Ye Z, Wang C. Assessment of the American Joint Commission on Cancer 8th Edition Staging System for patients with pancreatic neuroendocrine tumors: a surveillance, epidemiology, and end results analysis. Cancer Med 2018;7:626-634 https://doi.org/10.1002/cam4.1336
  15. Luo G, Javed A, Strosberg JR, Jin K, Zhang Y, Liu C, et al. Modified staging classification for pancreatic neuroendocrine tumors on the basis of the American Joint Committee on Cancer and European Neuroendocrine Tumor Society systems. J Clin Oncol 2017;35:274-280 https://doi.org/10.1200/JCO.2016.67.8193
  16. Bushnell DL Jr, O'Dorisio TM, O'Dorisio MS, Menda Y, Hicks RJ, Van Cutsem E, et al. 90Y-edotreotide for metastatic carcinoid refractory to octreotide. J Clin Oncol 2010;28:1652-1659 https://doi.org/10.1200/JCO.2009.22.8585
  17. Ramage JK, Ahmed A, Ardill J, Bax N, Breen DJ, Caplin ME, et al.; UK and Ireland Neuroendocrine Tumour Society. Guidelines for the management of gastroenteropancreatic neuroendocrine (including carcinoid) tumours (NETs). Gut 2012;61:6-32 https://doi.org/10.1136/gutjnl-2011-300831
  18. Reid MD, Balci S, Saka B, Adsay NV. Neuroendocrine tumors of the pancreas: current concepts and controversies. Endocr Pathol 2014;25:65-79 https://doi.org/10.1007/s12022-013-9295-2
  19. Raj N, Valentino E, Capanu M, Tang LH, Basturk O, Untch BR, et al. Treatment response and outcomes of grade 3 pancreatic neuroendocrine neoplasms based on morphology: well differentiated versus poorly differentiated. Pancreas 2017;46:296-301 https://doi.org/10.1097/MPA.0000000000000735
  20. Burns WR, Edil BH. Neuroendocrine pancreatic tumors: guidelines for management and update. Curr Treat Options Oncol 2012;13:24-34 https://doi.org/10.1007/s11864-011-0172-2
  21. Parekh JR, Wang SC, Bergsland EK, Venook AP, Warren RS, Kim GE, et al. Lymph node sampling rates and predictors of nodal metastasis in pancreatic neuroendocrine tumor resections: the UCSF experience with 149 patients. Pancreas 2012;41:840-844 https://doi.org/10.1097/MPA.0b013e31823cdaa0
  22. Hill JS, McPhee JT, McDade TP, Zhou Z, Sullivan ME, Whalen GF, et al. Pancreatic neuroendocrine tumors: the impact of surgical resection on survival. Cancer 2009;115:741-751 https://doi.org/10.1002/cncr.24065
  23. Kim KW, Krajewski KM, Nishino M, Jagannathan JP, Shinagare AB, Tirumani SH, et al. Update on the management of gastroenteropancreatic neuroendocrine tumors with emphasis on the role of imaging. AJR Am J Roentgenol 2013;201:811-824 https://doi.org/10.2214/AJR.12.10240
  24. Strosberg J, El-Haddad G, Wolin E, Hendifar A, Yao J, Chasen B, et al.; NETTER-1 Trial Investigators. Phase 3 trial of 177Ludotatate for midgut neuroendocrine tumors. N Engl J Med 2017;376:125-135 https://doi.org/10.1056/NEJMoa1607427
  25. Villard L, Romer A, Marincek N, Brunner P, Koller MT, Schindler C, et al. Cohort study of somatostatin-based radiopeptide therapy with [(90)Y-DOTA]-TOC versus [(90)Y-DOTA]-TOC plus [(177)Lu-DOTA]-TOC in neuroendocrine cancers. J Clin Oncol 2012;30:1100-1106 https://doi.org/10.1200/JCO.2011.37.2151
  26. Terashima T, Morizane C, Hiraoka N, Tsuda H, Tamura T, Shimada Y, et al. Comparison of chemotherapeutic treatment outcomes of advanced extrapulmonary neuroendocrine carcinomas and advanced small-cell lung carcinoma. Neuroendocrinology 2012;96:324-332 https://doi.org/10.1159/000338794
  27. Sundstrom S, Bremnes RM, Kaasa S, Aasebo U, Hatlevoll R, Dahle R, et al.; Norwegian Lung Cancer Study Group. Cisplatin and etoposide regimen is superior to cyclophosphamide, epirubicin, and vincristine regimen in small-cell lung cancer: results from a randomized phase III trial with 5 years' followup. J Clin Oncol 2002;20:4665-4672 https://doi.org/10.1200/JCO.2002.12.111
  28. Kim DW, Kim HJ, Kim KW, Byun JH, Song KB, Kim JH, 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;25:1375-1383 https://doi.org/10.1007/s00330-014-3532-z
  29. Takumi K, Fukukura Y, Higashi M, Ideue J, Umanodan T, Hakamada H, et al. Pancreatic neuroendocrine tumors: correlation between the contrast-enhanced computed tomography features and the pathological tumor grade. Eur J Radiol 2015;84:1436-1443 https://doi.org/10.1016/j.ejrad.2015.05.005
  30. Kim C, Byun JH, Hong SM, An S, Kim JH, Lee SS, et al. A comparison of enhancement patterns on dynamic enhanced CT and survival between patients with pancreatic neuroendocrine tumors with and without intratumoral fibrosis. Abdom Radiol (NY) 2017;42:2835-2842 https://doi.org/10.1007/s00261-017-1212-6
  31. Cappelli C, Boggi U, Mazzeo S, Cervelli R, Campani D, Funel N, et al. Contrast enhancement pattern on multidetector CT predicts malignancy in pancreatic endocrine tumours. Eur Radiol 2015;25:751-759 https://doi.org/10.1007/s00330-014-3485-2
  32. Rust E, Hubele F, Marzano E, Goichot B, Pessaux P, Kurtz JE, et al. Nuclear medicine imaging of gastro-entero-pancreatic neuroendocrine tumors. The key role of cellular differentiation and tumor grade: from theory to clinical practice. Cancer Imaging 2012;12:173-184
  33. Lewis RB, Lattin GE Jr, Paal E. Pancreatic endocrine tumors: radiologic-clinicopathologic correlation. Radiographics 2010;30:1445-1464 https://doi.org/10.1148/rg.306105523
  34. Gabriel M, Decristoforo C, Kendler D, Dobrozemsky G, Heute D, Uprimny C, et al. 68Ga-DOTA-Tyr3-octreotide PET in neuroendocrine tumors: comparison with somatostatin receptor scintigraphy and CT. J Nucl Med 2007;48:508-518 https://doi.org/10.2967/jnumed.106.035667
  35. Haug AR, Auernhammer CJ, Wangler B, Schmidt GP, Uebleis C, Goke B, et al. 68Ga-DOTATATE PET/CT for the early prediction of response to somatostatin receptor-mediated radionuclide therapy in patients with well-differentiated neuroendocrine tumors. J Nucl Med 2010;51:1349-1356 https://doi.org/10.2967/jnumed.110.075002
  36. Sharma P, Singh H, Bal C, Kumar R. PET/CT imaging of neuroendocrine tumors with (68)Gallium-labeled somatostatin analogues: an overview and single institutional experience from India. Indian J Nucl Med 2014;29:2-12 https://doi.org/10.4103/0972-3919.125760
  37. Gallotti A, Johnston RP, Bonaffini PA, Ingkakul T, Deshpande V, Fernandez-del Castillo C, et al. Incidental neuroendocrine tumors of the pancreas: MDCT findings and features of malignancy. AJR Am J Roentgenol 2013;200:355-362 https://doi.org/10.2214/AJR.11.8037
  38. Singhi AD, Chu LC, Tatsas AD, Shi C, Ellison TA, Fishman EK, et al. Cystic pancreatic neuroendocrine tumors: a clinicopathologic study. Am J Surg Pathol 2012;36:1666-1673 https://doi.org/10.1097/PAS.0b013e31826a0048
  39. Lee JH, Byun JH, Kim JH, Lee SS, Kim HJ, Lee MG. Solid pancreatic tumors with unilocular cyst-like appearance on CT: differentiation from unilocular cystic tumors using CT. Korean J Radiol 2014;15:704-711 https://doi.org/10.3348/kjr.2014.15.6.704
  40. Shi C, Siegelman SS, Kawamoto S, Wolfgang CL, Schulick RD, Maitra A, et al. Pancreatic duct stenosis secondary to small endocrine neoplasms: a manifestation of serotonin production? Radiology 2010;257:107-114 https://doi.org/10.1148/radiol.10100046
  41. Lam KY, Lo CY. Pancreatic endocrine tumour: a 22-year clinico-pathological experience with morphological, immunohistochemical observation and a review of the literature. Eur J Surg Oncol 1997;23:36-42 https://doi.org/10.1016/S0748-7983(97)80140-0
  42. Volante M, Righi L, Berruti A, Rindi G, Papotti M. The pathological diagnosis of neuroendocrine tumors: common questions and tentative answers. Virchows Arch 2011;458:393-402 https://doi.org/10.1007/s00428-011-1060-7
  43. Balachandran A, Tamm EP, Bhosale PR, Katz MH, Fleming JB, Yao JC, et al. Venous tumor thrombus in nonfunctional pancreatic neuroendocrine tumors. AJR Am J Roentgenol 2012;199:602-608 https://doi.org/10.2214/AJR.11.7058
  44. Kulke MH, Siu LL, Tepper JE, Fisher G, Jaffe D, Haller DG, et al. Future directions in the treatment of neuroendocrine tumors: consensus report of the National Cancer Institute neuroendocrine tumor clinical trials planning meeting. J Clin Oncol 2011;29:934-943 https://doi.org/10.1200/JCO.2010.33.2056
  45. Oberg K, Casanovas O, Castano JP, Chung D, Delle Fave G, Denefle P, et al. Molecular pathogenesis of neuroendocrine tumors: implications for current and future therapeutic approaches. Clin Cancer Res 2013;19:2842-2849 https://doi.org/10.1158/1078-0432.CCR-12-3458
  46. Kim JH, Lee JM, Park JH, Kim SC, Joo I, Han JK, et al. Solid pancreatic lesions: characterization by using timing bolus dynamic contrast-enhanced MR imaging assessment--a preliminary study. Radiology 2013;266:185-196 https://doi.org/10.1148/radiol.12120111
  47. Bali MA, Metens T, Denolin V, Delhaye M, Demetter P, Closset J, et al. Tumoral and nontumoral pancreas: correlation between quantitative dynamic contrast-enhanced MR imaging and histopathologic parameters. Radiology 2011;261:456-466 https://doi.org/10.1148/radiol.11103515
  48. Hwang EJ, Lee JM, Yoon JH, Kim JH, Han JK, Choi BI, et al. Intravoxel incoherent motion diffusion-weighted imaging of pancreatic neuroendocrine tumors: prediction of the histologic grade using pure diffusion coefficient and tumor size. Invest Radiol 2014;49:396-402 https://doi.org/10.1097/RLI.0000000000000028
  49. Koh DM, Collins DJ, Orton MR. Intravoxel incoherent motion in body diffusion-weighted MRI: reality and challenges. AJR Am J Roentgenol 2011;196:1351-1361 https://doi.org/10.2214/AJR.10.5515
  50. De Cecco CN, Darnell A, Rengo M, Muscogiuri G, Bellini D, Ayuso C, et al. Dual-energy CT: oncologic applications. AJR Am J Roentgenol 2012;199(5 Suppl):S98-S105 https://doi.org/10.2214/AJR.12.9207
  51. Kartalis N, Mucelli RM, Sundin A. Recent developments in imaging of pancreatic neuroendocrine tumors. Ann Gastroenterol 2015;28:193-202