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The role of multimodal imaging in guiding resectability and cytoreduction in pancreatic neuroendocrine tumors: focus on PET and MRI

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Abstract

Pancreatic neuroendocrine tumors (pNETs) are rare neoplasms that secrete peptides and neuro-amines. pNETs can be sporadic or hereditary, syndromic or non-syndromic with different clinical presentations and prognoses. The role of medical imaging includes locating the tumor, assessing its extent, and evaluating the feasibility of curative surgery or cytoreduction. Pancreatic NETs have very distinctive phenotypes on CT, MRI, and PET. PET have been demonstrated to be very sensitive to detect either well-differentiated pNETs using 68Gallium somatostatin receptor (SSTR) radiotracers, or more aggressive undifferentiated pNETS using 18F-FDG. A comprehensive interpretation of multimodal imaging guides resectability and cytoreduction in pNETs. The imaging phenotype provides information on the differentiation and proliferation of pNETs, as well as the spatial and temporal heterogeneity of tumors with prognostic and therapeutic implications. This review provides a structured approach for standardized reading and reporting of medical imaging studies with a focus on PET and MR techniques. It explains which imaging approach should be used for different subtypes of pNET and what a radiologist should be looking for and reporting when interpreting these studies.

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Abbreviations

ADC:

Apparent diffusion coefficient

AJCC:

American Joint Committee on Cancer

APUD:

Amine precursor uptake and decarboxylation

CEUS:

Contrast-enhanced ultra sound examination

CT:

Computed tomography

DOPA:

Dihydroxyphenylalanine

DOTATOC:

DOTA0-Phe1-Tyr3 octreotide

DWI:

Diffusion-weighted imaging

ENETs:

European Neuroendocrine Tumor Society

EUS:

Endoscopic ultrasound examination

18F-FDG:

18Fluoro-Fluorodeoxyglucose

68Ga:

Gallium-68

99mTc:

Technetium 99m

GLP-1:

Glucagon-like peptide 1

IACIG:

Intra-arterial injection of calcium

IOUS:

Intraoperative ultrasound examination

LM:

Liver metastases

MEN:

Multiple endocrine neoplasia syndrome

MRI:

Magnetic resonance imaging

NANETS:

North American Neuroendocrine Tumor Society

NF:

Neurofibromatosis

NET:

Neuroendocrine tumors

OS:

Overall survival

PDAC:

Pancreatic ductal adenocarcinoma

pNET:

Pancreatic tumor

SSTR:

Somatostatin receptor

SSTR-PET:

Somatostatin receptor PET

SSTR scintigraphy:

Somatostatin receptor scintigraphy

SUV:

Standard uptake value

TSC:

Tuberous sclerosis complex

US:

Ultrasound examination

VHL:

Von Hippel–Lindau syndrome

WHO:

World Health Organization

References

  1. Canellas R, Lo G, Bhowmik S, Ferrone C, Sahani D (2018) Pancreatic neuroendocrine tumor: Correlations between MRI features, tumor biology, and clinical outcome after surgery. J Magn Reson Imaging 47 (2):425-432. https://doi.org/10.1002/jmri.25756

    Article  PubMed  Google Scholar 

  2. Smith JK, Ng SC, Hill JS, Simons JP, Arous EJ, Shah SA, Tseng JF, McDade TP (2010) Complications after pancreatectomy for neuroendocrine tumors: a national study. J Surg Res 163 (1):63-68. https://doi.org/10.1016/j.jss.2010.04.017

    Article  PubMed  Google Scholar 

  3. Falconi M, Eriksson B, Kaltsas G, Bartsch DK, Capdevila J, Caplin M, Kos-Kudla B, Kwekkeboom D, Rindi G, Klöppel G, Reed N, Kianmanesh R, Jensen RT, Participants aoVCC (2016) ENETS Consensus Guidelines Update for the Management of Patients with Functional Pancreatic Neuroendocrine Tumors and Non-Functional Pancreatic Neuroendocrine Tumors. Neuroendocrinology 103 (2):153-171. https://doi.org/10.1159/000443171

    Article  CAS  PubMed  Google Scholar 

  4. Vagefi PA, Razo O, Deshpande V, McGrath DJ, Lauwers GY, Thayer SP, Warshaw AL, Fernández-del Castillo C (2007) Evolving patterns in the detection and outcomes of pancreatic neuroendocrine neoplasms: the Massachusetts General Hospital experience from 1977 to 2005. Archives of Surgery 142 (4):347-354

    Article  PubMed  Google Scholar 

  5. Ellison TA, Wolfgang CL, Shi C, Cameron JL, Murakami P, Mun LJ, Singhi AD, Cornish TC, Olino K, Meriden Z, Choti M, Diaz LA, Pawlik TM, Schulick RD, Hruban RH, Edil BH (2014) A single institution’s 26-year experience with nonfunctional pancreatic neuroendocrine tumors: a validation of current staging systems and a new prognostic nomogram. Ann Surg 259 (2):204-212. https://doi.org/10.1097/sla.0b013e31828f3174

    Article  PubMed  Google Scholar 

  6. Siegel RL, Miller KD, Jemal A (2017) Cancer Statistics, 2017. CA Cancer J Clin 67 (1):7-30. https://doi.org/10.3322/caac.21387

    Article  PubMed  Google Scholar 

  7. Halfdanarson TR, Rabe KG, Rubin J, Petersen GM (2008) Pancreatic neuroendocrine tumors (PNETs): incidence, prognosis and recent trend toward improved survival. Ann Oncol 19 (10):1727-1733. https://doi.org/10.1093/annonc/mdn351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Ambe CM, Nguyen P, Centeno BA, Choi J, Strosberg J, Kvols L, Hodul P, Hoffe S, Malafa MP (2017) Multimodality Management of “Borderline Resectable” Pancreatic Neuroendocrine Tumors: Report of a Single-Institution Experience. Cancer Control 24 (5):1073274817729076. https://doi.org/10.1177/1073274817729076

    Article  PubMed  PubMed Central  Google Scholar 

  9. van Essen M, Sundin A, Krenning EP, Kwekkeboom DJ (2014) Neuroendocrine tumours: the role of imaging for diagnosis and therapy. Nat Rev Endocrinol 10 (2):102-114. https://doi.org/10.1038/nrendo.2013.246

    Article  CAS  PubMed  Google Scholar 

  10. Halfdanarson TR, Rabe KG, Rubin J, Petersen GM (2008) Pancreatic neuroendocrine tumors (PNETs): incidence, prognosis and recent trend toward improved survival. Annals of Oncology 19 (10):1727-1733. https://doi.org/10.1093/annonc/mdn351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Bozkurt MF, Virgolini I, Balogova S, Beheshti M, Rubello D, Decristoforo C, Ambrosini V, Kjaer A, Delgado-Bolton R, Kunikowska J, Oyen WJG, Chiti A, Giammarile F, Fanti S (2017) Guideline for PET/CT imaging of neuroendocrine neoplasms with (68)Ga-DOTA-conjugated somatostatin receptor targeting peptides and (18)F-DOPA. Eur J Nucl Med Mol Imaging 44 (9):1588-1601. https://doi.org/10.1007/s00259-017-3728-y

    Article  CAS  PubMed  Google Scholar 

  12. Gouya H, Vignaux O, Augui J, Dousset B, Palazzo L, Louvel A, Chaussade S, Legmann P (2003) CT, Endoscopic Sonography, and a Combined Protocol for Preoperative Evaluation of Pancreatic Insulinomas. American Journal of Roentgenology 181 (4):987-992. https://doi.org/10.2214/ajr.181.4.1810987

    Article  PubMed  Google Scholar 

  13. Berends FJ, Cuesta MA, Kazemier G, van Eijck CH, de Herder WW, van Muiswinkel JM, Bruining HA, Bonjer HJ (2000) Laparoscopic detection and resection of insulinomas. Surgery 128 (3):386-391. https://doi.org/10.1067/msy.2000.107413

    Article  CAS  PubMed  Google Scholar 

  14. Klöppel G, Klimstra DS, Hruban RH, Adsay V, Capella C, Couvelard A, Komminoth P, La Rosa S, Ohike N, Osamura RY, Perren A, Scoazec J-Y, Rindi G (2017) Pancreatic Neuroendocrine Tumors: Update on the New World Health Organization Classification. AJSP: Reviews & Reports 22 (5)

  15. Tang LH, Basturk O, Sue JJ, Klimstra DS (2016) A Practical Approach to the Classification of WHO Grade 3 (G3) Well Differentiated Neuroendocrine Tumor (WD-NET) and Poorly Differentiated Neuroendocrine Carcinoma (PD-NEC) of the Pancreas. The American journal of surgical pathology 40 (9):1192-1202. https://doi.org/10.1097/pas.0000000000000662

    Article  PubMed  PubMed Central  Google Scholar 

  16. Dasari A, Shen C, Halperin D, et al. (2017) Trends in the incidence, prevalence, and survival outcomes in patients with neuroendocrine tumors in the united states. JAMA Oncol 3 (10):1335-1342. https://doi.org/10.1001/jamaoncol.2017.0589

    Article  PubMed  PubMed Central  Google Scholar 

  17. Sho S, Court CM, Winograd P, Toste PA, Pisegna JR, Lewis M, Donahue TR, Hines OJ, Reber HA, Dawson DW, Tomlinson JS (2018) A Prognostic Scoring System for the Prediction of Metastatic Recurrence Following Curative Resection of Pancreatic Neuroendocrine Tumors. J Gastrointest Surg. https://doi.org/10.1007/s11605-018-4011-7

  18. Jensen RT, Cadiot G, Brandi ML, de Herder WW, Kaltsas G, Komminoth P, Scoazec J-Y, Salazar R, Sauvanet A, Kianmanesh R (2012) ENETS Consensus Guidelines for the Management of Patients with Digestive Neuroendocrine Neoplasms: Functional Pancreatic Endocrine Tumor Syndromes. Neuroendocrinology 95 (2):98-119. https://doi.org/10.1159/000335591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Sadowski SM, Neychev V, Millo C, Shih J, Nilubol N, Herscovitch P, Pacak K, Marx SJ, Kebebew E (2016) Prospective Study of 68Ga-DOTATATE Positron Emission Tomography/Computed Tomography for Detecting Gastro-Entero-Pancreatic Neuroendocrine Tumors and Unknown Primary Sites. J Clin Oncol 34 (6):588-596. https://doi.org/10.1200/jco.2015.64.0987

    Article  CAS  PubMed  Google Scholar 

  20. Buchmann I, Henze M, Engelbrecht S, Eisenhut M, Runz A, Schafer M, Schilling T, Haufe S, Herrmann T, Haberkorn U (2007) Comparison of 68Ga-DOTATOC PET and 111In-DTPAOC (Octreoscan) SPECT in patients with neuroendocrine tumours. Eur J Nucl Med Mol Imaging 34 (10):1617-1626. https://doi.org/10.1007/s00259-007-0450-1

    Article  CAS  PubMed  Google Scholar 

  21. Oberndorfer S (1907) Karzinoide tumoren des dunndarms. Frankfurt Z Path 1:426-432

    Google Scholar 

  22. Öberg KE (2010) Gastrointestinal neuroendocrine tumors. Annals of Oncology 21 (suppl_7):vii72-vii80

  23. Triponez F, Dosseh D, Goudet P, Cougard P, Bauters C, Murat A, Cadiot G, Niccoli-Sire P, Chayvialle JA, Calender A, Proye CA (2006) Epidemiology data on 108 MEN 1 patients from the GTE with isolated nonfunctioning tumors of the pancreas. Ann Surg 243 (2):265-272. https://doi.org/10.1097/01.sla.0000197715.96762.68

    Article  PubMed  PubMed Central  Google Scholar 

  24. Corrias G, Monti S, Horvat N, Tang L, Basturk O, Saba L, Mannelli L (2018) Imaging features of malignant abdominal neuroendocrine tumors with rare presentation. Clin Imaging 51:59-64. https://doi.org/10.1016/j.clinimag.2018.02.004

    Article  PubMed  PubMed Central  Google Scholar 

  25. Owen N, Sohaib S, Peppercorn P, Monson J, Grossman A, Besser G, Reznek R (2001) MRI of pancreatic neuroendocrine tumours. The British journal of radiology 74 (886):968-973

    Article  CAS  PubMed  Google Scholar 

  26. Kim JH, Eun HW, Kim YJ, Han JK, Choi BI (2013) Staging accuracy of MR for pancreatic neuroendocrine tumor and imaging findings according to the tumor grade. Abdominal imaging 38 (5):1106-1114

    Article  PubMed  Google Scholar 

  27. Metz DC, Jensen RT (2008) Gastrointestinal neuroendocrine tumors: pancreatic endocrine tumors. Gastroenterology 135 (5):1469-1492

    Article  CAS  PubMed  Google Scholar 

  28. Guo J, Zhao J, Bi X, Li Z, Huang Z, Zhang Y, Cai J, Zhao H (2017) Should surgery be conducted for small nonfunctioning pancreatic neuroendocrine tumors: a systematic review. Oncotarget 8 (21):35368-35375. https://doi.org/10.18632/oncotarget.15685

    Article  PubMed  PubMed Central  Google Scholar 

  29. Raman SP, Hruban RH, Cameron JL, Wolfgang CL, Fishman EK (2012) Pancreatic imaging mimics: part 2, pancreatic neuroendocrine tumors and their mimics. AJR Am J Roentgenol 199 (2):309-318. https://doi.org/10.2214/ajr.12.8627

    Article  PubMed  Google Scholar 

  30. Foster DS, Jensen R, Norton JA (2018) Management of liver neuroendocrine tumors in 2018. JAMA Oncol. https://doi.org/10.1001/jamaoncol.2018.3035

  31. Ito T, Igarashi H, Uehara H, Berna MJ, Jensen RT (2013) Causes of death and prognostic factors in multiple endocrine neoplasia type 1: a prospective study: comparison of 106 MEN1/Zollinger-Ellison syndrome patients with 1613 literature MEN1 patients with or without pancreatic endocrine tumors. Medicine (Baltimore) 92 (3):135-181. https://doi.org/10.1097/md.0b013e3182954af1

    Article  CAS  Google Scholar 

  32. Reznek RH (2006) CT/MRI of neuroendocrine tumours. Cancer Imaging 6 (Spec No A):S163-S177. https://doi.org/10.1102/1470-7330.2006.9037

  33. Lipinski M, Rydzewska G, Foltyn W, Andrysiak-Mamos E, Baldys-Waligorska A, Bednarczuk T, Blicharz-Dorniak J, Bolanowski M, Boratyn-Nowicka A, Borowska M, Cichocki A, Cwikla JB, Falconi M, Handkiewicz-Junak D, Hubalewska-Dydejczyk A, Jarzab B, Junik R, Kajdaniuk D, Kaminski G, Kolasinska-Cwikla A, Kowalska A, Krol R, Krolicki L, Kunikowska J, Kusnierz K, Lampe P, Lange D, Lewczuk-Myslicka A, Lewinski A, Londzin-Olesik M, Marek B, Nasierowska-Guttmejer A, Nowakowska-Dulawa E, Pilch-Kowalczyk J, Poczkaj K, Rosiek V, Ruchala M, Sieminska L, Sowa-Staszczak A, Starzynska T, Steinhof-Radwanska K, Strzelczyk J, Sworczak K, Syrenicz A, Szawlowski A, Szczepkowski M, Wachula E, Zajecki W, Zemczak A, Zgliczynski W, Kos-Kudla B (2017) Gastroduodenal neuroendocrine neoplasms, including gastrinoma - management guidelines (recommended by the Polish Network of Neuroendocrine Tumours). Endokrynol Pol 68 (2):138-153. https://doi.org/10.5603/ep.2017.0016

    Article  CAS  PubMed  Google Scholar 

  34. O’Toole D, Salazar R, Falconi M, Kaltsas G, Couvelard A, de Herder WW, Hyrdel R, Nikou G, Krenning E, Vullierme M-P (2006) Rare functioning pancreatic endocrine tumors. Neuroendocrinology 84 (3):189-195

    Article  PubMed  Google Scholar 

  35. Lo GC, Kambadakone A (2018) MR Imaging of Pancreatic Neuroendocrine Tumors. Magn Reson Imaging Clin N Am 26 (3):391-403. https://doi.org/10.1016/j.mric.2018.03.010

    Article  PubMed  Google Scholar 

  36. Lee NJ, Hruban RH, Fishman EK (2018) Pancreatic neuroendocrine tumor: review of heterogeneous spectrum of CT appearance. Abdom Radiol (NY) 43 (11):3025-3034. https://doi.org/10.1007/s00261-018-1574-4

    Article  Google Scholar 

  37. Bushnell DL, Baum RP (2011) Standard imaging techniques for neuroendocrine tumors. Endocrinol Metab Clin North Am 40 (1):153-162, ix. https://doi.org/10.1016/j.ecl.2010.12.002

  38. Sundin A, Garske U, Örlefors H Nuclear imaging of neuroendocrine tumours. Best Practice & Research Clinical Endocrinology & Metabolism 21 (1):69-85. https://doi.org/10.1016/j.beem.2006.12.003

  39. Sun H, Zhou J, Liu K, Shen T, Wang X, Wang X (2018) Pancreatic neuroendocrine tumors: MR imaging features preoperatively predict lymph node metastasis. Abdom Radiol (NY). https://doi.org/10.1007/s00261-018-1863-y

  40. Dromain C, Deandreis D, Scoazec JY, Goere D, Ducreux M, Baudin E, Tselikas L (2016) Imaging of neuroendocrine tumors of the pancreas. Diagn Interv Imaging 97 (12):1241-1257. https://doi.org/10.1016/j.diii.2016.07.012

    Article  CAS  PubMed  Google Scholar 

  41. Boninsegna L, Partelli S, D’Innocenzio MM, Capelli P, Scarpa A, Bassi C, Pederzoli P, Falconi M (2010) Pancreatic cystic endocrine tumors: a different morphological entity associated with a less aggressive behavior. Neuroendocrinology 92 (4):246-251. https://doi.org/10.1159/000318771

    Article  CAS  PubMed  Google Scholar 

  42. Singhi AD, Chu LC, Tatsas AD, Shi C, Ellison TA, Fishman EK, Kawamoto S, Schulick RD, Wolfgang CL, Hruban RH, Edil BH (2012) Cystic Pancreatic Neuroendocrine Tumors: A Clinicopathologic Study. The American Journal of Surgical Pathology 36 (11):1666-1673. https://doi.org/10.1097/pas.0b013e31826a0048

    Article  PubMed  Google Scholar 

  43. De Robertis R, Maris B, Cardobi N, Tinazzi Martini P, Gobbo S, Capelli P, Ortolani S, Cingarlini S, Paiella S, Landoni L, Butturini G, Regi P, Scarpa A, Tortora G, D’Onofrio M (2018) Can histogram analysis of MR images predict aggressiveness in pancreatic neuroendocrine tumors? Eur Radiol. https://doi.org/10.1007/s00330-017-5236-7

  44. Buetow PC, Buck JL, Pantongrag-Brown L, Beck KG, Ros PR, Adair CF (1996) Solid and papillary epithelial neoplasm of the pancreas: imaging-pathologic correlation on 56 cases. Radiology 199 (3):707-711

    Article  CAS  PubMed  Google Scholar 

  45. Semelka RC, Ascher SM (1993) MR imaging of the pancreas. Radiology 188 (3):593-602

    Article  CAS  PubMed  Google Scholar 

  46. Sureka B, Meena V, Khera PS (2018) Differential diagnosis of pancreatic calcifications. American Journal of Roentgenology 210 (1):W43-W43

    Article  PubMed  Google Scholar 

  47. Javadi S, Menias CO, Korivi BR, Shaaban AM, Patnana M, Alhalabi K, Elsayes KM (2017) Pancreatic calcifications and calcified pancreatic masses: pattern recognition approach on CT. American Journal of Roentgenology 209 (1):77-87

    Article  PubMed  Google Scholar 

  48. Singh R, Calhoun S, Shin M, Katz R (2008) Pancreatic Neuroendocrine Tumor with Atypical Radiologic Presentation. Radiol Case Rep 3 (3):162. https://doi.org/10.2484/rcr.v3i3.162

    Article  PubMed  Google Scholar 

  49. Cescato R, Schulz S, Waser B, Eltschinger V, Rivier JE, Wester HJ, Culler M, Ginj M, Liu Q, Schonbrunn A, Reubi JC (2006) Internalization of sst2, sst3, and sst5 receptors: effects of somatostatin agonists and antagonists. J Nucl Med 47 (3):502-511

    CAS  PubMed  Google Scholar 

  50. Graham MM, Gu X, Ginader T, Breheny P, Sunderland JJ (2017) (68)Ga-DOTATOC Imaging of Neuroendocrine Tumors: A Systematic Review and Metaanalysis. J Nucl Med 58 (9):1452-1458. https://doi.org/10.2967/jnumed.117.191197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Reubi JC, Waser B, Friess H, Büchler M, Laissue J (1998) Neurotensin receptors: a new marker for human ductal pancreatic adenocarcinoma. Gut 42 (4):546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Stabin MG, Kooij PP, Bakker WH, Inoue T, Endo K, Coveney J, de Jong R, Minegishi A (1997) Radiation dosimetry for indium-111-pentetreotide. J Nucl Med 38 (12):1919-1922

    CAS  PubMed  Google Scholar 

  53. Sandstrom M, Velikyan I, Garske-Roman U, Sorensen J, Eriksson B, Granberg D, Lundqvist H, Sundin A, Lubberink M (2013) Comparative biodistribution and radiation dosimetry of 68Ga-DOTATOC and 68Ga-DOTATATE in patients with neuroendocrine tumors. J Nucl Med 54 (10):1755-1759. https://doi.org/10.2967/jnumed.113.120600

    Article  CAS  PubMed  Google Scholar 

  54. Werner RA, Bluemel C, Allen-Auerbach MS, Higuchi T, Herrmann K (2015) 68 Gallium-and 90 Yttrium-/177 Lutetium:“theranostic twins” for diagnosis and treatment of NETs. Annals of nuclear medicine 29 (1):1-7

    Article  CAS  PubMed  Google Scholar 

  55. Kabasakal L, Demirci E, Ocak M, Decristoforo C, Araman A, Ozsoy Y, Uslu I, Kanmaz B (2012) Comparison of (6)(8)Ga-DOTATATE and (6)(8)Ga-DOTANOC PET/CT imaging in the same patient group with neuroendocrine tumours. Eur J Nucl Med Mol Imaging 39 (8):1271-1277. https://doi.org/10.1007/s00259-012-2123-y

    Article  PubMed  Google Scholar 

  56. Fani M, Nicolas GP, Wild D (2017) Somatostatin receptor antagonists for imaging and therapy. J Nucl Med 58 (Suppl 2):61S-66S

    Article  CAS  PubMed  Google Scholar 

  57. Kauhanen S, Seppanen M, Nuutila P (2008) Premedication with carbidopa masks positive finding of insulinoma and beta-cell hyperplasia in [(18)F]-dihydroxy-phenyl-alanine positron emission tomography. J Clin Oncol 26 (32):5307-5308; author reply 5308-5309. https://doi.org/10.1200/jco.2008.18.8581

  58. Halbrook CJ, Lyssiotis CA (2017) Employing Metabolism to Improve the Diagnosis and Treatment of Pancreatic Cancer. Cancer Cell 31 (1):5-19. https://doi.org/10.1016/j.ccell.2016.12.006

    Article  CAS  PubMed  Google Scholar 

  59. Vander Heiden MG, Cantley LC, Thompson CB (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324 (5930):1029-1033. https://doi.org/10.1126/science.1160809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Binderup T, Knigge U, Loft A, Federspiel B, Kjaer A (2010) 18F-fluorodeoxyglucose positron emission tomography predicts survival of patients with neuroendocrine tumors. Clin Cancer Res 16 (3):978-985. https://doi.org/10.1158/1078-0432.ccr-09-1759

    Article  CAS  PubMed  Google Scholar 

  61. Hindie E (2017) The NETPET Score: Combining FDG and Somatostatin Receptor Imaging for Optimal Management of Patients with Metastatic Well-Differentiated Neuroendocrine Tumors. Theranostics 7 (5):1159-1163. https://doi.org/10.7150/thno.19588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Bucau M, Laurent-Bellue A, Poté N, Hentic O, Cros J, Mikail N, Rebours V, Ruszniewski P, Lebtahi R, Couvelard A (2018) 18F-FDG Uptake in Well-Differentiated Neuroendocrine Tumors Correlates with Both Ki-67 and VHL Pathway Inactivation. Neuroendocrinology 106 (3):274-282

    Article  CAS  PubMed  Google Scholar 

  63. Zimny M, Bares R, Fass J, Adam G, Cremerius U, Dohmen B, Klever P, Sabri O, Schumpelick V, Buell U (1997) Fluorine-18 fluorodeoxyglucose positron emission tomography in the differential diagnosis of pancreatic carcinoma: a report of 106 cases. European journal of nuclear medicine 24 (6):678-682

    Article  CAS  PubMed  Google Scholar 

  64. Korner M, Stockli M, Waser B, Reubi JC (2007) GLP-1 receptor expression in human tumors and human normal tissues: potential for in vivo targeting. J Nucl Med 48 (5):736-743. https://doi.org/10.2967/jnumed.106.038679

    Article  CAS  PubMed  Google Scholar 

  65. Sowa-Staszczak A, Pach D, Mikolajczak R, Macke H, Jabrocka-Hybel A, Stefanska A, Tomaszuk M, Janota B, Gilis-Januszewska A, Malecki M, Kaminski G, Kowalska A, Kulig J, Matyja A, Osuch C, Hubalewska-Dydejczyk A (2013) Glucagon-like peptide-1 receptor imaging with [Lys40(Ahx-HYNIC- 99mTc/EDDA)NH2]-exendin-4 for the detection of insulinoma. Eur J Nucl Med Mol Imaging 40 (4):524-531. https://doi.org/10.1007/s00259-012-2299-1

    Article  CAS  PubMed  Google Scholar 

  66. Sowa-Staszczak A, Trofimiuk-Müldner M, Stefańska A, Tomaszuk M, Buziak-Bereza M, Gilis-Januszewska A, Jabrocka-Hybel A, Głowa B, Małecki M, Bednarczuk T (2016) 99mTc labeled glucagon-like peptide-1-analogue (99mTc-GLP1) scintigraphy in the management of patients with occult insulinoma. PloS one 11 (8):e0160714

    Article  PubMed  PubMed Central  Google Scholar 

  67. Christ E, Wild D, Ederer S, Béhé M, Nicolas G, Caplin ME, Brändle M, Clerici T, Fischli S, Stettler C (2013) Glucagon-like peptide-1 receptor imaging for the localisation of insulinomas: a prospective multicentre imaging study. The Lancet Diabetes & Endocrinology 1 (2):115-122

    Article  CAS  Google Scholar 

  68. Doppman JL, Miller DL, Chang R, Shawker TH, Gorden P, Norton JA (1991) Insulinomas: localization with selective intraarterial injection of calcium. Radiology 178 (1):237-241

    Article  CAS  PubMed  Google Scholar 

  69. Braatvedt G, Jennison E, Holdaway IM (2014) Comparison of two low-dose calcium infusion schedules for localization of insulinomas by selective pancreatic arterial injection with hepatic venous sampling for insulin. Clinical endocrinology 80 (1):80-84

    Article  CAS  PubMed  Google Scholar 

  70. Kato M, Doi R, Imamura M, Furutani M, Hosotani R, Shimada Y (1997) Calcium-evoked insulin release from insulinoma cells is mediated via calcium-sensing receptor. Surgery 122 (6):1203-1211

  71. Itami A, Kato M, Komoto I, Doi R, Hosotani R, Shimada Y, Imamura M (2001) Human gastrinoma cells express calcium-sensing receptor. Life Sciences 70 (2):119-129. https://doi.org/10.1016/s0024-3205(01)01380-7

  72. Morganstein D, Lewis D, Jackson J, Isla A, Lynn J, Devendra D, Meeran K, Todd J (2009) The role of arterial stimulation and simultaneous venous sampling in addition to cross-sectional imaging for localisation of biochemically proven insulinoma. Eur Radiol 19 (10):2467-2473

    Article  CAS  PubMed  Google Scholar 

  73. Yeh R, Dercle L, Garg I, Wang ZJ, Hough DM, Goenka AH (2018) The Role of 18F-FDG PET/CT and PET/MRI in Pancreatic Ductal Adenocarcinoma. Abdominal Radiology 43 (2):415-434

    Article  PubMed  Google Scholar 

  74. Attenberger U, Catana C, Chandarana H, Catalano OA, Friedman K, Schonberg SA, Thrall J, Salvatore M, Rosen BR, Guimaraes AR (2015) Whole-body FDG PET-MR oncologic imaging: pitfalls in clinical interpretation related to inaccurate MR-based attenuation correction. Abdominal Imaging 40 (6):1374-1386. https://doi.org/10.1007/s00261-015-0455-3

    Article  PubMed  Google Scholar 

  75. Kamisawa T, Takum K, Anjiki H, Egawa N, Kurata M, Honda G, Tsuruta K (2010) FDG-PET/CT findings of autoimmune pancreatitis. Hepato-gastroenterology 57 (99-100):447-450

    PubMed  Google Scholar 

  76. Kato K, Nihashi T, Ikeda M, Abe S, Iwano S, Itoh S, Shimamoto K, Naganawa S (2013) Limited Efficacy of 18F-FDG PET/CT for Differentiation Between Metastasis-Free Pancreatic Cancer and Mass-Forming Pancreatitis. Clinical Nuclear Medicine 38 (6):417. https://doi.org/10.1097/rlu.0b013e3182817d9d

    Article  PubMed  Google Scholar 

  77. Matsumoto I, Shirakawa S, Shinzeki M, Asari S, Goto T, Ajiki T, Fukumoto T, Kitajima K, Ku Y (2013) 18-Fluorodeoxyglucose Positron Emission Tomography Does Not Aid in Diagnosis of Pancreatic Ductal Adenocarcinoma. Clinical Gastroenterology and Hepatology 11 (6):712-718. https://doi.org/10.1016/j.cgh.2012.12.033

    Article  PubMed  Google Scholar 

  78. Rijkers AP, Valkema R, Duivenvoorden HJ, van Eijck CHJ (2014) Usefulness of F-18-fluorodeoxyglucose positron emission tomography to confirm suspected pancreatic cancer: A meta-analysis. European Journal of Surgical Oncology (EJSO) 40 (7):794-804. https://doi.org/10.1016/j.ejso.2014.03.016

    Article  CAS  Google Scholar 

  79. Beiderwellen K, Geraldo L, Ruhlmann V, Heusch P, Gomez B, Nensa F, Umutlu L, Lauenstein TC (2015) Accuracy of [18F]FDG PET/MRI for the Detection of Liver Metastases. PLoS One 10 (9):e0137285. https://doi.org/10.1371/journal.pone.0137285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Joo I, Lee JM, Lee DH, Lee ES, Paeng JC, Lee SJ, Jang JY, Kim SW, Ryu JK, Lee KB (2017) Preoperative Assessment of Pancreatic Cancer with FDG PET/MR Imaging versus FDG PET/CT Plus Contrast-enhanced Multidetector CT: A Prospective Preliminary Study. Radiology 282 (1):149-159. https://doi.org/10.1148/radiol.2016152798

    Article  PubMed  Google Scholar 

  81. Schaarschmidt BM, Grueneisen J, Heusch P, Gomez B, Umutlu L, Ruhlmann V, Rosenbaum-Krumme S, Antoch G, Buchbender C (2015) Does 18F-FDG PET/MRI reduce the number of indeterminate abdominal incidentalomas compared with 18F-FDG PET/CT? Nucl Med Commun 36 (6):588-595. https://doi.org/10.1097/mnm.0000000000000298

    Article  CAS  PubMed  Google Scholar 

  82. Chen BB, Tien YW, Chang MC, Cheng MF, Chang YT, Yang SH, Wu CH, Kuo TC, Shih IL, Yen RF, Shih TT (2018) Multiparametric PET/MR imaging biomarkers are associated with overall survival in patients with pancreatic cancer. Eur J Nucl Med Mol Imaging 45 (7):1205-1217. https://doi.org/10.1007/s00259-018-3960-0

    Article  CAS  PubMed  Google Scholar 

  83. Dercle L, Deandreis D, Terroir M, Leboulleux S, Lumbroso J, Schlumberger M (2016) Evaluation of 124 I PET/CT and 124 I PET/MRI in the management of patients with differentiated thyroid cancer. European journal of nuclear medicine and molecular imaging 43 (6):1006-1010

    Article  PubMed  Google Scholar 

  84. Kolbitsch C, Neji R, Fenchel M, Mallia A, Marsden P, Schaeffter T (2018) Fully integrated 3D high-resolution multicontrast abdominal PET-MR with high scan efficiency. Magn Reson Med 79 (2):900-911. https://doi.org/10.1002/mrm.26757

    Article  PubMed  Google Scholar 

  85. Fuin N, Catalano OA, Scipioni M, Canjels LPW, Izquierdo-Garcia D, Pedemonte S, Catana C (2018) Concurrent Respiratory Motion Correction of Abdominal PET and Dynamic Contrast-Enhanced-MRI Using a Compressed Sensing Approach. J Nucl Med 59 (9):1474-1479. https://doi.org/10.2967/jnumed.117.203943

    Article  PubMed  PubMed Central  Google Scholar 

  86. Yang J, Liu J, Wiesinger F, Menini A, Zhu X, Hope TA, Seo Y, Larson PEZ (2018) Developing an efficient phase-matched attenuation correction method for quiescent period PET in abdominal PET/MRI. Phys Med Biol 63 (18):185002. https://doi.org/10.1088/1361-6560/aada26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Wagenknecht G, Kaiser HJ, Mottaghy FM, Herzog H (2013) MRI for attenuation correction in PET: methods and challenges. MAGMA 26 (1):99-113. https://doi.org/10.1007/s10334-012-0353-4

    Article  PubMed  Google Scholar 

  88. Keereman V, Mollet P, Berker Y, Schulz V, Vandenberghe S (2013) Challenges and current methods for attenuation correction in PET/MR. MAGMA 26 (1):81-98. https://doi.org/10.1007/s10334-012-0334-7

    Article  PubMed  Google Scholar 

  89. Visvikis D, Monnier F, Bert J, Hatt M, Fayad H (2014) PET/MR attenuation correction: where have we come from and where are we going? Eur J Nucl Med Mol Imaging 41 (6):1172-1175. https://doi.org/10.1007/s00259-014-2748-0

    Article  PubMed  Google Scholar 

  90. Attenberger U, Catana C, Chandarana H, Catalano OA, Friedman K, Schonberg SA, Thrall J, Salvatore M, Rosen BR, Guimaraes AR (2015) Whole-body FDG PET-MR oncologic imaging: pitfalls in clinical interpretation related to inaccurate MR-based attenuation correction. Abdom Imaging 40 (6):1374-1386. https://doi.org/10.1007/s00261-015-0455-3

    Article  PubMed  Google Scholar 

  91. Martinez-Moller A, Souvatzoglou M, Delso G, Bundschuh RA, Chefd’hotel C, Ziegler SI, Navab N, Schwaiger M, Nekolla SG (2009) Tissue classification as a potential approach for attenuation correction in whole-body PET/MRI: evaluation with PET/CT data. J Nucl Med 50 (4):520-526. https://doi.org/10.2967/jnumed.108.054726

    Article  PubMed  Google Scholar 

  92. Jeong JH, Cho IH, Kong EJ, Chun KA (2014) Evaluation of Dixon Sequence on Hybrid PET/MR Compared with Contrast-Enhanced PET/CT for PET-Positive Lesions. Nucl Med Mol Imaging 48 (1):26-32. https://doi.org/10.1007/s13139-013-0240-6

    Article  PubMed  Google Scholar 

  93. Dercle L, Lu L, Lichtenstein P, Yang H, Wang D, Zhu J, Wu F, Piessevaux H, Schwartz LH, Zhao B (2017) Impact of Variability in Portal Venous Phase Acquisition Timing in Tumor Density Measurement and Treatment Response Assessment: Metastatic Colorectal Cancer as a Paradigm. JCO Clinical Cancer Informatics (1):1-8. https://doi.org/10.1200/cci.17.00108

    Article  PubMed  Google Scholar 

  94. Dercle L, Chisin R, Ammari S, Gillebert Q, Ouali M, Jaudet C, Delord JP, Dierickx L, Zerdoud S, Schlumberger M, Courbon F (2014) Nonsurgical giant cell tumour of the tendon sheath or of the diffuse type: Are MRI or F-FDG PET/CT able to provide an accurate prediction of long-term outcome? Eur J Nucl Med Mol Imaging. https://doi.org/10.1007/s00259-014-2938-9

  95. Dercle L, Ammari S, Bateson M, Durand PB, Haspinger E, Massard C, Jaudet C, Varga A, Deutsch E, Soria JC, Ferte C (2017) Limits of radiomic-based entropy as a surrogate of tumor heterogeneity: ROI-area, acquisition protocol and tissue site exert substantial influence. Sci Rep 7 (1):7952. https://doi.org/10.1038/s41598-017-08310-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Dierickx LO, Dercle L, Chaltiel L, Caselles O, Brillouet S, Zerdoud S, Courbon F (2017) Evaluation of 2 diuretic 18Fluorine-Fluorodeoxyglucose positron emission tomography/computed tomography imaging protocols for intra-pelvic cancer. Q J Nucl Med Mol Imaging. https://doi.org/10.23736/s1824-4785.17.02912-0

  97. Sun R, Limkin EJ, Dercle L, Reuze S, Zacharaki EI, Chargari C, Schernberg A, Dirand AS, Alexis A, Paragios N, Deutsch E, Ferte C, Robert C (2017) [Computational medical imaging (radiomics) and potential for immuno-oncology]. Cancer Radiother 21 (6-7):648-654. https://doi.org/10.1016/j.canrad.2017.07.035

    Article  CAS  PubMed  Google Scholar 

  98. Dercle L, Hartl D, Rozenblum-Beddok L, Mokrane FZ, Seban RD, Yeh R, Bidault F, Ammari S (2018) Diagnostic and prognostic value of 18F-FDG PET, CT, and MRI in perineural spread of head and neck malignancies. Eur Radiol 28 (4):1761-1770. https://doi.org/10.1007/s00330-017-5063-x

    Article  PubMed  Google Scholar 

  99. Chi W, Warner RRP, Chan DL, Singh S, Segelov E, Strosberg J, Wisnivesky J, Kim MK (2018) Long-term Outcomes of Gastroenteropancreatic Neuroendocrine Tumors. Pancreas 47 (3):321. https://doi.org/10.1097/mpa.0000000000001005

    Article  PubMed  Google Scholar 

  100. Patel BN, Olcott E, Jeffrey RB (2018) Extrapancreatic perineural invasion in pancreatic adenocarcinoma. Abdom Radiol (NY) 43 (2):323-331. https://doi.org/10.1007/s00261-017-1343-9

    Article  Google Scholar 

  101. De Robertis R, Paiella S, Cardobi N, Landoni L, Tinazzi Martini P, Ortolani S, De Marchi G, Gobbo S, Giardino A, Butturini G, Tortora G, Bassi C, D’Onofrio M (2018) Tumor thrombosis: a peculiar finding associated with pancreatic neuroendocrine neoplasms. A pictorial essay. Abdom Radiol (NY) 43 (3):613-619. https://doi.org/10.1007/s00261-017-1243-z

    Article  Google Scholar 

  102. Kulke MH, Anthony LB, Bushnell DL, De Herder WW, Goldsmith SJ, Klimstra DS, Marx SJ, Pasieka JL, Pommier RF, Yao JC (2010) NANETS treatment guidelines: well-differentiated neuroendocrine tumors of the stomach and pancreas. Pancreas 39 (6):735

    Article  PubMed  PubMed Central  Google Scholar 

  103. Sundin A, Arnold R, Baudin E, Cwikla JB, Eriksson B, Fanti S, Fazio N, Giammarile F, Hicks RJ, Kjaer A, Krenning E, Kwekkeboom D, Lombard-Bohas C, O’Connor JM, O’Toole D, Rockall A, Wiedenmann B, Valle JW, Vullierme M-P, all other Antibes Consensus Conference p (2017) ENETS Consensus Guidelines for the Standards of Care in Neuroendocrine Tumors: Radiological, Nuclear Medicine and Hybrid Imaging. Neuroendocrinology 105 (3):212-244. https://doi.org/10.1159/000471879

    Article  CAS  PubMed  Google Scholar 

  104. Schraml C, Schwenzer NF, Sperling O, Aschoff P, Lichy MP, Muller M, Brendle C, Werner MK, Claussen CD, Pfannenberg C (2013) Staging of neuroendocrine tumours: comparison of [(6)(8)Ga]DOTATOC multiphase PET/CT and whole-body MRI. Cancer Imaging 13:63-72. https://doi.org/10.1102/1470-7330.2013.0007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Yu F, Venzon DJ, Serrano J, Goebel SU, Doppman JL, Gibril F, Jensen RT (1999) Prospective study of the clinical course, prognostic factors, causes of death, and survival in patients with long-standing Zollinger-Ellison syndrome. J Clin Oncol 17 (2):615-630. https://doi.org/10.1200/jco.1999.17.2.615

    Article  CAS  PubMed  Google Scholar 

  106. Jensen RT, Niederle B, Mitry E, Ramage JK, Steinmuller T, Lewington V, Scarpa A, Sundin A, Perren A, Gross D, O’Connor JM, Pauwels S, Kloppel G, Frascati Consensus C, European Neuroendocrine Tumor S (2006) Gastrinoma (duodenal and pancreatic). Neuroendocrinology 84 (3):173-182. https://doi.org/10.1159/000098009

    Article  CAS  PubMed  Google Scholar 

  107. Ellison EC, Johnson JA (2009) The Zollinger-Ellison syndrome: a comprehensive review of historical, scientific, and clinical considerations. Current problems in surgery 46 (1):13-106

    Article  PubMed  Google Scholar 

  108. d’Assignies G, Fina P, Bruno O, Vullierme MP, Tubach F, Paradis V, Sauvanet A, Ruszniewski P, Vilgrain V (2013) High sensitivity of diffusion-weighted MR imaging for the detection of liver metastases from neuroendocrine tumors: comparison with T2-weighted and dynamic gadolinium-enhanced MR imaging. Radiology 268 (2):390-399. https://doi.org/10.1148/radiol.13121628

    Article  PubMed  Google Scholar 

  109. Pavel M, Baudin E, Couvelard A, Krenning E, Oberg K, Steinmuller T, Anlauf M, Wiedenmann B, Salazar R, Barcelona Consensus Conference p (2012) ENETS Consensus Guidelines for the management of patients with liver and other distant metastases from neuroendocrine neoplasms of foregut, midgut, hindgut, and unknown primary. Neuroendocrinology 95 (2):157-176. https://doi.org/10.1159/000335597

    Article  CAS  PubMed  Google Scholar 

  110. Hope TA, Bergsland EK, Bozkurt MF, Graham M, Heaney AP, Herrmann K, Howe JR, Kulke MH, Kunz PL, Mailman J, May L, Metz DC, Millo C, O’Dorisio S, Reidy-Lagunes DL, Soulen MC, Strosberg JR (2018) Appropriate Use Criteria for Somatostatin Receptor PET Imaging in Neuroendocrine Tumors. J Nucl Med 59 (1):66-74. https://doi.org/10.2967/jnumed.117.202275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Orditura M, Petrillo A, Ventriglia J, Diana A, Laterza MM, Fabozzi A, Savastano B, Franzese E, Conzo G, Santini L, Ciardiello F, De Vita F (2016) Pancreatic neuroendocrine tumors: Nosography, management and treatment. Int J Surg 28 Suppl 1:S156-162. https://doi.org/10.1016/j.ijsu.2015.12.052

    Article  PubMed  Google Scholar 

  112. Dromain C, de Baere T, Lumbroso J, Caillet H, Laplanche A, Boige V, Ducreux M, Duvillard P, Elias D, Schlumberger M, Sigal R, Baudin E (2005) Detection of liver metastases from endocrine tumors: a prospective comparison of somatostatin receptor scintigraphy, computed tomography, and magnetic resonance imaging. J Clin Oncol 23 (1):70-78. https://doi.org/10.1200/jco.2005.01.013

    Article  PubMed  Google Scholar 

  113. de Baère T, Aupérin A, Deschamps F, Chevallier P, Gaubert Y, Boige V, Fonck M, Escudier B, Palussiére J (2015) Radiofrequency ablation is a valid treatment option for lung metastases: experience in 566 patients with 1037 metastases. Annals of Oncology 26 (5):987-991. https://doi.org/10.1093/annonc/mdv037

    Article  PubMed  PubMed Central  Google Scholar 

  114. Eriksson J, Stålberg P, Nilsson A, Krause J, Lundberg C, Skogseid B, Granberg D, Eriksson B, Åkerström G, Hellman P (2008) Surgery and Radiofrequency Ablation for Treatment of Liver Metastases from Midgut and Foregut Carcinoids and Endocrine Pancreatic Tumors. World J Surg 32 (5):930-938. https://doi.org/10.1007/s00268-008-9510-3

    Article  PubMed  Google Scholar 

  115. de Baere T, Palussiere J, Auperin A, Hakime A, Abdel-Rehim M, Kind M, Dromain C, Ravaud A, Tebboune N, Boige V, Malka D, Lafont C, Ducreux M (2006) Midterm local efficacy and survival after radiofrequency ablation of lung tumors with minimum follow-up of 1 year: prospective evaluation. Radiology 240 (2):587-596. https://doi.org/10.1148/radiol.2402050807

    Article  PubMed  Google Scholar 

  116. Kennedy A, Bester L, Salem R, Sharma RA, Parks RW, Ruszniewski P (2015) Role of hepatic intra-arterial therapies in metastatic neuroendocrine tumours (NET): guidelines from the NET-Liver-Metastases Consensus Conference. HPB (Oxford) 17 (1):29-37. https://doi.org/10.1111/hpb.12326

    Article  Google Scholar 

  117. Vogl TJ, Gruber T, Naguib NNN, Hammerstingl R, Nour-Eldin N-EA (2009) Liver metastases of neuroendocrine tumors: treatment with hepatic transarterial chemotherapy using two therapeutic protocols. American Journal of Roentgenology 193 (4):941-947

    Article  PubMed  Google Scholar 

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L Dercle’s work was funded by a grant from Fondation Philanthropia, Geneva, Switzerland, and the Fondation Nuovo-Soldati.

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Rozenblum, L., Mokrane, FZ., Yeh, R. et al. The role of multimodal imaging in guiding resectability and cytoreduction in pancreatic neuroendocrine tumors: focus on PET and MRI. Abdom Radiol 44, 2474–2493 (2019). https://doi.org/10.1007/s00261-019-01994-5

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