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Diagnostic Applications of Nuclear Medicine: Pancreatic Cancer

  • Elena TabacchiEmail author
  • Cristina Nanni
  • Irene Bossert
  • Anna Margherita Maffione
  • Stefano Fanti
Living reference work entry

Later version available View entry history

Abstract

Pancreatic cancer can be assessed through a variety of imaging techniques including endoscopic ultrasonography (EUS), computed tomography (CT), endoscopic retrograde cholangiopancreatography (ERCP), magnetic resonance imaging (MRI), and magnetic resonance cholangiopancreatography (MRCP).

These imaging modalities are often effective in the evaluation of pancreatic cancers although sometimes they require the use of radiopharmaceuticals with positron and single-photon emission CT (PET and SPECT) imaging techniques. In this chapter the role of nuclear medicine with various radiolabeled compounds and the rationale for their use in endocrine and nonendocrine pancreatic tumors are discussed.

Keywords

Pancreatic cancer Neuroendocrine tumor Gastroenteropancreatic tumor SPECT/CT PET/CT Somatostatin receptor scintigraphy Somatostatin analogues 111In-pentetreotide [18F]FDG 123I-MIBG 131I-MIBG 18F-DOPA 68Ga-DOTA-peptides Peptide radioreceptor therapy 

Glossary

[18F]FDG

[18F]2-Fluoro-2-deoxyglucose

[18F]FDOPA

L-3,4-Dihydroxy-6-[18F]fluorophenylalanine

11C-5-HTP

11C-5-Hydroxy-L-tryptophan

18F-FLT

18F-Fluoro-thymidine

AJCC

American Joint Cancer Committee

BRCA1

Breast cancer type 1 susceptibility protein

BRCA2

Breast cancer type 2 susceptibility protein

CA 19

Carbohydrate antigen 19

CCK2

Cholecystokinin 2

CRHoma

Neuroendocrine tumor producing adrenocorticotropin-releasing hormone

CT

X-ray computed tomography

DM

Diabetes mellitus

DOTA

1,4,7,10-Tetraazacyclododecane-1,4,7,10-tetraacetic acid

DTPA

Diethylenetriaminepentaacetic acid

EDDA

Ethylenediamine-N,N'-bis(2-hydroxyphenyl)acetic acid

ENETS

European Neuroendocrine Tumor Society

ERCP

Endoscopic retrograde cholangiopancreatography

EUS

Endoscopic ultrasonography

FAMM

Multiple mole melanoma syndrome

FNA

Fine-needle aspiration

G-CSF

Granulocyte colony-stimulating factor

GEP-NET

Gastro-entero-pancreatic neuroendocrine tumor

GHRHoma

Neuroendocrine tumor producing growth hormone-releasing hormone

GI

Gastrointestinal

GLP-1

Exendin

GLP1R

Glucagon-like peptide 1 receptor

GTV

Gross tumor volume

hENT-1

Human equilibrative nucleoside transporter-1

HPF

High-power field

HYNIC

Hydrazidonicotinic acid/hydrazinonicotinamide

IPMN

Intraductal papillary mucinous neoplasm

LAN

Lanreotide

MDCT

Multi-detector row computed tomography

MIBG

Metaiodobenzylguanidine

MRCP

Magnetic resonance cholangiopancreatography

MRI

Magnetic resonance imaging

MTC

Medullary thyroid carcinoma

mTOR

Mammalian target of rapamycin

NCCN

National Comprehensive Cancer Network

NEC

Neuroendocrine carcinoma

NET

Neuroendocrine tumor

NOC

1-Nal3-octreotide

PanIN

Pancreatic intraepithelial neoplasia

PC

Pancreatic cancer

PET

Positron emission tomography

PET/CT

Positron emission tomography/computed tomography

PET/MR

Integrated positron emission tomography/magnetic resonance system

pNEN

Pancreatic neuroendocrine neoplasm

PRRT

Peptide receptor radionuclide therapy

R0

Surgery achieving negative microscopic resection margins

R1

Surgery achieving microscopic positive resection margins

R2

Surgery achieving residual macroscopic disease

RT

Radiation therapy

SPECT

Single-photon emission computed tomography

SPECT/CT

Single-photon emission computed tomography/computed tomography

SRS

Somatostatin receptor scintigraphy

SSA

Somatostatin analogues

SSTR

Somatostatin receptors

SUV

Standardized uptake value

TATE

Octeotate

TNM

AJCC staging system based on parameters “T” (tumor status), “N” (lymph node status) and “M” (distant metastasis status)

TOC

Octreotide

VAP

Vapreotide

VIP

Vasoactive intestinal peptide

WHO

World Health Organization

References

  1. 1.
    Raimondi S, Maisonneuve P, Lowenfels AB. Epidemiology of pancreatic cancer: an overview. Nat Rev Gastroenterol Hepatol. 2009;6:699–708.PubMedCrossRefGoogle Scholar
  2. 2.
    Hariharan D, Saied A, Kocher HM. Analysis of mortality rates for pancreatic cancer across the world. HPB (Oxford). 2008;10:58–62.CrossRefGoogle Scholar
  3. 3.
    Hidalgo M. Pancreatic cancer. N Engl J Med. 2010;362:1605–17.PubMedCrossRefGoogle Scholar
  4. 4.
    Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63:11–30.PubMedCrossRefGoogle Scholar
  5. 5.
    Klinkenbijl JH, Jeekel J, Sahmoud T, van Pel R, Couvreur ML, Veenhof CH, et al. Adjuvant radiotherapy and 5-fluorouracil after curative resection of cancer of the pancreas and periampullary region: phase III trial of the EORTC gastrointestinal tract cancer cooperative group. Ann Surg. 1999;230:776–82.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Klinkenbij JH, Jeekel J, Schmitz PI, Rombout PA, Nix GA, Bruining HA, et al. Carcinoma of the pancreas and periampullary region: palliation versus cure. Br J Surg. 1993;80:1575–8.CrossRefGoogle Scholar
  7. 7.
    Neoptolemos JP, Stocken DD, Friess H, Bassi C, Dunn JA, Hickey H, et al. A randomized trial of chemoradiotherapy and chemotherapy after resection of pancreatic cancer. N Engl J Med. 2004;350:1200–10.PubMedCrossRefGoogle Scholar
  8. 8.
    Oettle H, Post S, Neuhaus P, Gellert K, Langrehr J, Ridwelski K, et al. Adjuvant chemotherapy with gemcitabine vs observation in patients undergoing curative-intent resection of pancreatic cancer: a randomized controlled trial. JAMA. 2007;17(297):267–77.CrossRefGoogle Scholar
  9. 9.
    Sohn TA, Yeo CJ, Cameron JL, Koniaris L, Kaushal S, Abrams R, et al. A Resected adenocarcinoma of the pancreas - 616 patients: results, outcomes, and prognostic indicators. J Gastrointest Surg. 2000;4:567–79.PubMedCrossRefGoogle Scholar
  10. 10.
    Wagner M, Redaelli C, Lietz M, Seiler CA, Friess H, Büchler MW, et al. Curative resection is the single most important factor determining outcome in patients with pancreatic adenocarcinoma. Br J Surg. 2004;91:586–94.PubMedCrossRefGoogle Scholar
  11. 11.
    Hruban RH, Canto MI, Goggins M, Schulick R, Klein AP. Update on familial pancreatic cancer. Adv Surg. 2010;44:293–311.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Goggins M, Canto M, Hruban R. Can we screen high-risk individuals to detect early pancreatic carcinoma? J Surg Oncol. 2000;74:243–8.PubMedCrossRefGoogle Scholar
  13. 13.
    Templeton AW, Brentnall TA. Screening and surgical outcomes of familial pancreatic cancer. Surg Clin North Am. 2013;93:629–45.PubMedCrossRefGoogle Scholar
  14. 14.
    Klein AP, Brune KA, Petersen GM, Goggins M, Tersmette AC, Offerhaus GJ. Prospective risk of pancreatic cancer in familial pancreatic cancer kindreds. Cancer Res. 2004;64:2634–8.PubMedCrossRefGoogle Scholar
  15. 15.
    Lynch SM, Vrieling A, Lubin JH, Kraft P, Mendelsohn JB, Hartge P. Cigarette smoking and pancreatic cancer: a pooled analysis from the pancreatic cancer cohort consortium. Am J Epidemiol. 2009;170:403–13.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Raimondi S, Lowenfels AB, Morselli-Labate AM, Maisonneuve P, Pezzilli R. Pancreatic cancer in chronic pancreatitis; aetiology, incidence, and early detection. Best Pract Res Clin Gastroenterol. 2010;24:349–58.PubMedCrossRefGoogle Scholar
  17. 17.
    Pannala R, Basu A, Petersen GM, Chari ST. New-onset diabetes: a potential clue to the early diagnosis of pancreatic cancer. Lancet Oncol. 2009;10:88–95.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Risch HA, Lu L, Wang J, Zhang W, Ni Q, Gao YT, et al. ABO blood group and risk of pancreatic cancer: a study in Shanghai and meta-analysis. Am J Epidemiol. 2013;177:1326–37.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Chari ST, Kelly K, Hollingsworth MA, Thayer SP, Ahlquist DA, Andersen DK. Early detection of sporadic pancreatic cancer: summative review. Pancreas. 2015;44:693–712.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Takhar AS, Palaniappan P, Dhingsa R, Lobo DN. Recent developments in diagnosis of pancreatic cancer. BMJ. 2004;18(329):668–73.CrossRefGoogle Scholar
  21. 21.
    Saruc M, Pour PM. Diabetes and its relationship to pancreatic carcinoma. Pancreas. 2003;26:381–7.PubMedCrossRefGoogle Scholar
  22. 22.
    Ozkan H, Kaya M, Cengiz A, et al. Comparison of tumour marker CA 242 with CA 19-9 and carcinoembryonic antigen (CEA) in pancreatic cancer. Hepatogastroenterology. 2003;50:1669–74.PubMedGoogle Scholar
  23. 23.
    Willett CG, Daly WJ, Warshaw AL, et al. CA 19-9 is an index of response to neoadjunctive chemoradiation therapy in pancreatic cancer. Am J Surg. 1996;172:350–2.PubMedCrossRefGoogle Scholar
  24. 24.
    Yeo TP, Hruban RH, Leach SD, Wilentz RE, Sohn TA, Kern SE. Pancreatic cancer. Curr Probl Cancer. 2002;26:176–275.PubMedCrossRefGoogle Scholar
  25. 25.
    Karmazanovsky G, Fedorov V, Kubyshkin V, Kotchatkov A, et al. Pancreatic head cancer: accuracy of CT in determination of resectability. Abdom Imaging. 2005;30:488–500.PubMedCrossRefGoogle Scholar
  26. 26.
    Miura F, Takada T, Amano H, Yoshida M, Furui S, Takeshita K. Diagnosis of pancreatic cancer. HPB (Oxford). 2006;8:337–42.CrossRefGoogle Scholar
  27. 27.
    Brennan DD, Zamboni GA, Raptopoulos VD, Kruskal JB, et al. Comprehensive preoperative assessment of pancreatic adenocarcinoma with 64-section volumetric CT. Radiographics. 2007;27:1653–66.PubMedCrossRefGoogle Scholar
  28. 28.
    Morana G, Cancian L, Pozzi Mucelli R, Cugini C. Staging cancer of the pancreas. Cancer Imaging. 2010;10(Spec no A):S137–41.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Appel BL, Tolat P, Evans DB, Tsai S. Current staging systems for pancreatic cancer. Cancer J. 2012;18:539–49.PubMedCrossRefGoogle Scholar
  30. 30.
    Fusaroli P, Kypraios D, Caletti G, Eloubeidi MA. Pancreatico-biliary endoscopic ultrasound: a systematic review of the levels of evidence, performance and outcomes. World J Gastroenterol. 2012;18:4243–56.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Sahani DV, Bonaffini PA, Catalano OA, Guimaraes AR, Blake MA. State-of-the-art PET/CT of the pancreas: current role and emerging indications. Radiographics. 2012;32:1133–58; discussion 1158–60.PubMedCrossRefGoogle Scholar
  32. 32.
    Conrad C, Fernández-Del Castillo C. Preoperative evaluation and management of the pancreatic head mass. J Surg Oncol. 2013;107:23–32.PubMedCrossRefGoogle Scholar
  33. 33.
    Shrikhande SV, Barreto SG, Goel M, Arya S. Multimodality imaging of pancreatic ductal adenocarcinoma: a review of the literature. HPB (Oxford). 2012;14:658–68.CrossRefGoogle Scholar
  34. 34.
    Raman SP, Horton KM, Fishman EK. Multimodality imaging of pancreatic cancer-computed tomography, magnetic resonance imaging, and positron emission tomography. Cancer J. 2012;18:511–22.PubMedCrossRefGoogle Scholar
  35. 35.
    Dibble EH, Karantanis D, Mercier G, Peller PJ, Kachnic LA, Subramaniam RM. PET/CT of cancer patients: part 1, pancreatic neoplasms. AJR Am J Roentgenol. 2012;199:952–67.PubMedCrossRefGoogle Scholar
  36. 36.
    Kinney T. Evidence-based imaging of pancreatic malignancies. Surg Clin North Am. 2010;90:235–49.PubMedCrossRefGoogle Scholar
  37. 37.
    Klimstra DS, Pitman MB, Hruban RH. An algorithmic approach to the diagnosis of pancreatic neoplasms. Arch Pathol Lab Med. 2009;133:454–64.PubMedGoogle Scholar
  38. 38.
    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.CrossRefGoogle Scholar
  39. 39.
    Yao JC, Hassan M, Phan A, Dagohoy C, Leary C, Mares JE. One hundred years after “carcinoid”: epidemiology of and prognostic factors for neuroendocrine tumors in 35,825 cases in the United States. J Clin Oncol. 2008;26:3063–72.PubMedCrossRefGoogle Scholar
  40. 40.
    Zhou J, Enewold L, Stojadinovic A, Clifton GT, Potter JF, Peoples GE. Incidence rates of exocrine and endocrine pancreatic cancers in the United States. Cancer Causes Control. 2010;21:853–61.PubMedCrossRefGoogle Scholar
  41. 41.
    Falconi M, Plockinger U, Kwekkeboom DJ, Manfredi R, Korner M, Kvols L. Well-differentiated pancreatic non-functioning tumors/carcinoma. Neuroendocrinology. 2006;84:196–211.PubMedCrossRefGoogle Scholar
  42. 42.
    O’Toole D, Salazar R, Falconi M, Kaltsas G, Couvelard A, de Herder WW. Rare functioning pancreatic endocrine tumors. Neuroendocrinology. 2006;84:189–95.PubMedCrossRefGoogle Scholar
  43. 43.
    Modlin IM, Moss SF, Gustafsson BI, Lawrence B, Schimmack S, Kidd M. The archaic distinction between functioning and non-functioning neuroendocrine neoplasms is no longer clinically relevant. Langenbecks Arch Surg. 2011;396:1145–56.PubMedCrossRefGoogle Scholar
  44. 44.
    Halfdanarson TR, Rabe KG, Rubin J, Petersen GM. Pancreatic neuroendocrine tumors (PNETs): incidence, prognosis and recent trend toward improved survival. Ann Oncol. 2008;19:1727–33.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Jensen RT, Cadiot G, Brandi ML, de Herder WW, Kaltsas G, Komminoth P, et al. ENETS Consensus Guidelines for the management of patients with digestive neuroendocrine neoplasms: functional pancreatic endocrine tumor syndromes. Neuroendocrinology. 2012;95:98–119.PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Pavel M, Baudin E, Couvelard A, Krenning E, Öberg K, Steinmüller T, et al. 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. 2012;95:157–76.PubMedCrossRefGoogle Scholar
  47. 47.
    Heitz PU, Kommith P, Perren A, Klimstra DS, Dayal Y, Bordi C, et al. Pathology and genetics of tumours of endocrine organs. In: DeLellis DA, Lloyd RV, Heitz PU, editors. WHO classification of tumours. Pancreatic endocrine tumours: introduction. Lyon: IARC Press; 2004. p. 177–82.Google Scholar
  48. 48.
    Schindl M, Kaczirek K, Kaserer K, Niederle B. Is the new classification of neuroendocrine pancreatic tumours of clinical help? World J Surg. 2000;24:1312–8.PubMedCrossRefGoogle Scholar
  49. 49.
    Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A. AJCC cancer staging manual (7th ed.). New York: Springer; 2010.Google Scholar
  50. 50.
    Yeo CJ, Cameron JL, Lillemoe KD, Sitzmann JV, Hruban RH, Goodman SN. Pancreaticoduodenectomy for cancer of the head of the pancreas. 201 patients. Ann Surg. 1995;221:721–31; discussion 731–3.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Conlon KC, Klimstra DS, Brennan MF. Long-term survival after curative resection for pancreatic ductal adenocarcinoma. Clinicopathologic analysis of 5-year survivors. Ann Surg. 1996;223:273–9.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Yeo CJ, Abrams RA, Grochow LB, Sohn TA, Ord SE, Hruban RH, et al. Pancreaticoduodenectomy for pancreatic adenocarcinoma: postoperative adjuvant chemoradiation improves survival. A prospective, single-institution experience. Ann Surg. 1997;225:621–33; discussion 633–6.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Bilimoria KY, Bentrem DJ, Ko CY, Ritchey J, Stewart AK, Winchester DP. Validation of the 6th edition AJCC pancreatic cancer staging system: report from the national cancer database. Cancer. 2007;110:738–44.PubMedCrossRefGoogle Scholar
  54. 54.
    Wasif N, Ko CY, Farrell J, Wainberg Z, Hines OJ, Reber H. Impact of tumor grade on prognosis in pancreatic cancer: should we include grade in AJCC staging? Ann Surg Oncol. 2010;17:2312–20.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Rochefort MM, Ankeny JS, Kadera BE, Donald GW, Isacoff W, Wainberg ZA, et al. Impact of tumor grade on pancreatic cancer prognosis: validation of a novel TNMG staging system. Ann Surg Oncol. 2013;20:4322–9.PubMedCrossRefGoogle Scholar
  56. 56.
    Winter JM, Cameron JL, Campbell KA, Arnold MA, Chang DC, Coleman J. 1423 pancreaticoduodenectomies for pancreatic cancer: a single-institution experience. J Gastrointest Surg. 2006;10:1199–210.PubMedCrossRefGoogle Scholar
  57. 57.
    Erkan M, Michalski CW, Rieder S, Reiser-Erkan C, Abiatari I, Kolb A, et al. The activated stroma index is a novel and independent prognostic marker in pancreatic ductal adenocarcinoma. Clin Gastroenterol Hepatol. 2008;6:1155–61.PubMedCrossRefGoogle Scholar
  58. 58.
    National Comprehensive Cancer Network (NCCN) practice guidelines in oncology. Pancreatic adenocarcinoma (version 1.2014). Available at: http://www.nccn.org/professionals/physician_gls/pdf/pancreatic.pdf.
  59. 59.
    Varadhachary GR, Tamm EP, Abbruzzese JL, Xiong HQ, Crane CH, Wang H, et al. Borderline resectable pancreatic cancer: definitions, management, and role of preoperative therapy. Ann Surg Oncol. 2006;13:1035–46.PubMedCrossRefGoogle Scholar
  60. 60.
    Evans DB, Erickson BA, Ritch P. Borderline resectable pancreatic cancer: definitions and the importance of multimodality therapy. Ann Surg Oncol. 2010;17:2803–5.PubMedCrossRefGoogle Scholar
  61. 61.
    Katz MH, Merchant NB, Brower S, Branda M, Posner MC, William Traverso L, et al. Standardization of surgical and pathologic variables is needed in multicenter trials of adjuvant therapy for pancreatic cancer: results from the ACOSOG Z5031 trial. Ann Surg Oncol. 2011;18:337–44.PubMedCrossRefGoogle Scholar
  62. 62.
    Dalton RR, Sarr MG, van Heerden JA, Colby TV. Carcinoma of the body and tail of the pancreas: is curative resection justified? Surgery. 1992;111:489–94.PubMedGoogle Scholar
  63. 63.
    Brennan MF, Moccia RD, Klimstra D. Management of adenocarcinoma of the body and tail of the pancreas. Ann Surg. 1996;223:506–11; discussion 511–2.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Andersson R, Aho U, Nilsson BI, Peters GJ, Pastor-Anglada M, Rasch W, et al. Gemcitabine chemoresistance in pancreatic cancer: molecular mechanisms and potential solutions. Scand J Gastroenterol. 2009;44:782–6.PubMedCrossRefGoogle Scholar
  65. 65.
    Damaraju VL, Damaraju S, Young JD, Baldwin SA, Mackey J, Sawyer MB. Nucleoside anticancer drugs: the role of nucleoside transporters in resistance to cancer chemotherapy. Oncogene. 2003;22:7524–36.PubMedCrossRefGoogle Scholar
  66. 66.
    Di Marco M, Di Cicilia R, Macchini M, Nobili E, Vecchiarelli S, Brandi G. Metastatic pancreatic cancer: is gemcitabine still the best standard treatment? Oncol Rep. 2010;23:1183–92.PubMedCrossRefGoogle Scholar
  67. 67.
    Sun C, Ansari D, Andersson R, Wu DQ. Does gemcitabine-based combination therapy improve the prognosis of unresectable pancreatic cancer? World J Gastroenterol. 2012;18:4944–58.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Rothenberg ML, Moore MJ, Cripps MC, Andersen JS, Portenoy RK, Burris 3rd HA. A phase II trial of gemcitabine in patients with 5-FU-refractory pancreas cancer. Ann Oncol. 1996;7:347–53.PubMedCrossRefGoogle Scholar
  69. 69.
    Burris 3rd HA, Moore MJ, Andersen J, Green MR, Rothenberg ML, Modiano MR, et al. Improvements in survival and clinical benefit with gemcitabine as firstline therapy for patients with advanced pancreas cancer: a randomized trial. J Clin Oncol. 1997;15:2403–13.PubMedCrossRefGoogle Scholar
  70. 70.
    Storniolo AM, Enas NH, Brown CA, Voi M, Rothenberg ML, Schilsky R. An investigational new drug treatment program for patients with gemcitabine: results for over 3000 patients with pancreatic carcinoma. Cancer. 1999;85:1261–8.PubMedCrossRefGoogle Scholar
  71. 71.
    Kulke MH, Blaszkowsky LS, Ryan DP, Clark JW, Meyerhardt JA, Zhu AX, et al. Capecitabine plus erlotinib in gemcitabine-refractory advanced pancreatic cancer. J Clin Oncol. 2007;25:4787–92.PubMedCrossRefGoogle Scholar
  72. 72.
    Fong ZV, Tan WP, Lavu H, Kennedy EP, Mitchell DG, Koniaris LG, et al. Preoperative imaging for resectable periampullary cancer: clinicopathologic implications of reported radiographic findings. J Gastrointest Surg. 2013;17:1098–106.PubMedCrossRefGoogle Scholar
  73. 73.
    Winter JM, Brennan MF, Tang LH, D’Angelica MI, Dematteo RP, Fong Y, et al. Survival after resection of pancreatic adenocarcinoma: results from a single institution over three decades. Ann Surg Oncol. 2012;19:169–75.PubMedCrossRefGoogle Scholar
  74. 74.
    Bosman FT, Carneiro F, Hruban RH, Theise ND. WHO classification of tumours of the digestive system. 4th ed. Lyon: IARC; 2010.Google Scholar
  75. 75.
    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;104:764–77.PubMedCrossRefGoogle Scholar
  76. 76.
    Caplin ME, Pavel M, Ruszniewski P. Lanreotide in metastatic enteropancreatic neuroendocrine tumors. N Engl J Med. 2014;371:224–33.PubMedCrossRefGoogle Scholar
  77. 77.
    Lee ES, Lee JM. Imaging diagnosis of pancreatic cancer. World J Gastroenterol. 2014;20:7864–77.PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Torigian DA, Zaidi H, Kwee TC, Saboury B, Udupa JK, Cho ZH, et al. PET/MR imaging: technical aspects and potential clinical applications. Radiology. 2013;267:26–44.PubMedCrossRefGoogle Scholar
  79. 79.
    De Gaetano AM, Rufini V, Castaldi P, Gatto AM, Filograna L, Giordano A, et al. Clinical applications of 18F-FDG PET in the management of hepatobiliary and pancreatic tumors. Abdom Imaging. 2012;37:983–1003.PubMedCrossRefGoogle Scholar
  80. 80.
    Izuishi K, Yamamoto Y, Sano T, Takebayashi R, Masaki T, Suzuki Y. Impact of 18-fluorodeoxyglucose positron emission tomography on the management of pancreatic cancer. J Gastrointest Surg. 2010;14:1151–8.PubMedCrossRefGoogle Scholar
  81. 81.
    Lemke AJ, Niehues SM, Hosten N, Amthauer H, Boehmig M, Stroszczynski C, et al. Retrospective digital image fusion of multidetector CT and 18F-FDG PET: clinical value in pancreatic lesions-a prospective study with 104 patients. J Nucl Med. 2004;45:1279–86.PubMedGoogle Scholar
  82. 82.
    Bang S, Chung HW, Park SW, Chung JB, Yun M, Lee JD, et al. The clinical usefulness of 18-fluorodeoxyglucose positron emission tomography in the differential diagnosis, staging, and response evaluation after concurrent chemoradiotherapy for pancreatic cancer. J Clin Gastroenterol. 2006;40:923–9.PubMedCrossRefGoogle Scholar
  83. 83.
    Kauhanen SP, Komar G, Seppänen MP, Dean KI, Minn HR, Kajander SA, et al. A prospective diagnostic accuracy study of 18F-fluorodeoxyglucose positron emission tomography/computed tomography, multidetector row computed tomography, and magnetic resonance imaging in primary diagnosis and staging of pancreatic cancer. Ann Surg. 2009;250:957–63.PubMedCrossRefGoogle Scholar
  84. 84.
    Raman SP, Fishman EK, Lennon AM. Endoscopic ultrasound and pancreatic applications: what the radiologist needs to know. Abdom Imaging. 2013;38:1360–72.PubMedCrossRefGoogle Scholar
  85. 85.
    van Kouwen MC, Jansen JB, van Goor H, de Castro S, Oyen WJ, Drenth JP. FDG-PET is able to detect pancreatic carcinomain chronic pancreatitis. Eur J Nucl Med Mol Imaging. 2005;32:399–404.PubMedCrossRefGoogle Scholar
  86. 86.
    Lee TY, Kim MH, Park DH, Seo DW, Lee SK, Kim JS, et al. Utility of 18F-FDG PET/CT for differentiation of autoimmune pancreatitis with atypical pancreatic imaging findings from pancreatic cancer. AJR Am J Roentgenol. 2009;193:343–8.PubMedCrossRefGoogle Scholar
  87. 87.
    Pakzad F, Groves AM, Ell PJ. The role of positron emission tomography in the management of pancreatic cancer. Semin Nucl Med. 2006;36:248–56.PubMedCrossRefGoogle Scholar
  88. 88.
    Pery C, Meurette G, Ansquer C, Frampas E, Regenet N. Role and limitations of 18F-FDG positron emission tomography (PET) in the management of patients with pancreatic lesions. Gastroenterol Clin Biol. 2010;34:465–74.PubMedCrossRefGoogle Scholar
  89. 89.
    Hong HS, Yun M, Cho A, Choi JY, Kim MJ, Kim KW, et al. The utility of F18 FDG PET/CT in the evaluation of pancreatic intraductal papillary mucinous neoplasm. Clin Nucl Med. 2010;35:776–9.PubMedCrossRefGoogle Scholar
  90. 90.
    Sperti C, Pasquali C, Decet G, Chierichetti F, Liessi G, Pedrazzoli S. F-18-fluorodeoxyglucose positron emission tomography in differentiating malignant from benign pancreatic cysts: a prospective study. J Gastrointest Surg. 2005;9:22–8.PubMedCrossRefGoogle Scholar
  91. 91.
    Fassan M, Pizzi S, Sperti C, Pasquali C, Pedrazzoli S, Chierichetti F, et al. 18F-FDG PET findings and GLUT-1 expression in IPMNs of the pancreas. J Nucl Med. 2008;49:2070.PubMedCrossRefGoogle Scholar
  92. 92.
    Sperti C, Bissoli S, Pasquali C, Frison L, Liessi G, Chierichetti F, et al. 18-Fluorodeoxyglucose positron emission tomography enhances computed tomography diagnosis of malignant intraductal papillary mucinous neoplasms of the pancreas. Ann Surg. 2007;246:932–9.PubMedCrossRefGoogle Scholar
  93. 93.
    Tomimaru Y, Takeda Y, Tatsumi M, Kim T, Kobayashi S, Marubashi S, et al. Utility of 2-[18F]-fluoro-2-deoxy-D-glucose positron emission tomography in differential diagnosis of benign and malignant intraductal papillary mucinous neoplasm of the pancreas. Oncol Rep. 2010;24:613–20.PubMedGoogle Scholar
  94. 94.
    Javery O, Shyn P, Mortele K. FDG PET or PET/CT in patients with pancreatic cancer: when does it add to diagnostic CT or MRI? Clin Imaging. 2013;37:295–301.PubMedCrossRefGoogle Scholar
  95. 95.
    Nishiyama Y, Yamamoto Y, Yokoe K, Monden T, Sasakawa Y, Tsutsui K, et al. Contribution of whole body FDG-PET to the detection of distant metastasis in pancreatic cancer. Ann Nucl Med. 2005;19:491–7.PubMedCrossRefGoogle Scholar
  96. 96.
    Bares R, Klever P, Hauptmann S, Hellwig D, Fass J, Cremerius U, et al. F18-fluorodeoxyglucose PET in vivo evaluation of pancreatic glucose metabolism for detection of pancreatic cancer. Radiology. 1994;192:79–86.PubMedCrossRefGoogle Scholar
  97. 97.
    Zimny M, Bares R, Fass J, Adam G, Cremerius U, Dohmen B, 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;24:678–82.PubMedGoogle Scholar
  98. 98.
    Lytras D, Connor S, Bosonnet L, Jayan R, Evans J, Hughes M, et al. Positron emission tomography does not add to computed tomography for the diagnosis and staging of pancreatic cancer. Dig Surg. 2005;22:55–62.PubMedCrossRefGoogle Scholar
  99. 99.
    Strobel K, Heinrich S, Bhure U, Soyka J, Veit-Haibach P, Pestalozzi BC, et al. Contrast-enhanced 18F-FDG PET/CT: 1-stop-shop imaging for assessing the resectability of pancreatic cancer. J Nucl Med. 2008;49:1408–13.PubMedCrossRefGoogle Scholar
  100. 100.
    Gambhir SS, Czernin J, Schwimmer J, Silverman DH, Coleman RE, Phelps ME. A tabulated summary of the FDG PET literature. J Nucl Med. 2001;42:1S–93.PubMedGoogle Scholar
  101. 101.
    Zafra M, Ayala F, Gonzalez-Billalabeitia E, Vicente E, Gonzalez-Cabezas P, García T, et al. Impact of whole-body 18F-FDG PET on diagnostic and therapeutic management of medical oncology patients. Eur J Cancer. 2008;44:1678–83.PubMedCrossRefGoogle Scholar
  102. 102.
    Topkan E, Parlak C, Yapar AF. FDG-PET/CT-based restaging may alter initial management decisions and clinical outcomes in patients with locally advanced pancreatic carcinoma planned to undergo chemoradiotherapy. Cancer Imaging. 2013;13:423–8.PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Imai H, Doi R, Kanazawa H, Kamo N, Koizumi M, Masui T, et al. Preoperative assessment of para-aortic lymph node metastasis in patients with pancreatic cancer. Int J Clin Oncol. 2010;15:294–300.PubMedCrossRefGoogle Scholar
  104. 104.
    Kuwatani M, Kawakami H, Eto K, Haba S, Shiga T, Tamaki N, et al. Modalities for evaluating chemotherapeutic efficacy and survival time in patients with advanced pancreatic cancer: comparison between FDG-PET, CT, and serum tumor markers. Intern Med. 2009;48:867–75.PubMedCrossRefGoogle Scholar
  105. 105.
    Maisey NR, Webb A, Flux GD, Padhani A, Cunningham DC, Ott RJ, et al. FDG-PET in the prediction of survival of patients with cancer of the pancreas: a pilot study. World J Cancer. 2000;1166:287–93.CrossRefGoogle Scholar
  106. 106.
    Higashi T, Sakahara H, Torizuka T, Nakamoto Y, Kanamori S, Hiraoka M, et al. Evaluation of intraoperative radiation therapy for unresectable pancreatic cancer with FDG PET. J Nucl Med. 1999;40:1424–33.PubMedGoogle Scholar
  107. 107.
    Springett GM, Hoffe SE. Borderline resectable pancreatic cancer: on the edge of survival. Cancer Control. 2008;15:295–307.PubMedGoogle Scholar
  108. 108.
    Higashi T, Fisher SJ, Brown RS, Nakada K, Walter GL, Wahl RL. Evaluation of the early effect of local irradiation on normal rodent bone marrow metabolism using fluorine-18-FDG; preclinical studies for PET. J Nucl Med. 2000;41:2026–35.PubMedGoogle Scholar
  109. 109.
    Ruf J, Lopez Hänninen E, Oettle H, Plotkin M, Pelzer U, Stroszczynski C, et al. Detection of recurrent pancreatic cancer: comparison of FDG-PET with CT/RM. Pancreatology. 2005;5:266–72.PubMedCrossRefGoogle Scholar
  110. 110.
    Urban D, Catane R. Serum tumor markers in oncology. Isr Med Assoc J. 2009;11:103–4.PubMedGoogle Scholar
  111. 111.
    Higashi T, Saga T, Nakamoto Y, Ishimori T, Fujimoto K, Doi R, et al. Diagnosis of pancreatic cancer using fluorine-18 fluorodeoxyglucose positron emission tomography (FDG PET) – usefulness and limitations in “clinical reality”. Ann Nucl Med. 2003;17:261–79.PubMedCrossRefGoogle Scholar
  112. 112.
    [No authors listed]. Radiation therapy combined with Adriamycin or 5-fluorouracil for the treatment of locally unresectable pancreatic carcinoma. Gastrointestinal Tumor Study Group. Cancer. 1985;56:2563–68.Google Scholar
  113. 113.
    Klaassen DJ, MacIntyre JM, Catton GE, Engstrom PF, Moertel CG, et al. Treatment of locally unresectable cancer of the stomach and pancreas: a randomized comparison of 5-fluorouracil alone with radiation plus concurrent and maintenance 5-fluorouracil – an Eastern Cooperative Oncology Group study. J Clin Oncol. 1985;3:373–8.PubMedCrossRefGoogle Scholar
  114. 114.
    Topkan E, Yavuz AA, Aydin M, Onal C, Yapar F, Yavuz MN. Comparison of CT and PET-CT based planning of radiation therapy in locally advanced pancreatic carcinoma. J Exp Clin Cancer Res. 2008;23:27–41.Google Scholar
  115. 115.
    Huguet F, Girard N, Guerche CS, Hennequin C, Mornex F, Azria D. Chemoradiotherapy in the management of locally advanced pancreatic carcinoma: a qualitative systematic review. J Clin Oncol. 2009;27:2269–77.PubMedCrossRefGoogle Scholar
  116. 116.
    Parlak C, Topkan E, Onal C, Reyhan M, Selek U. Prognostic value of gross tumor volume delineated by FDG-PET-CT based radiotherapy treatment planning in patients with locally advanced pancreatic cancer treated with chemoradiotherapy. Radiat Oncol. 2012;7:37.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Kobayashi K, Bhargava P, Raja S, Nasseri F, Al-Balas HA, Smith DD, et al. Image-guided biopsy: what the interventional radiologist needs to know about PET/CT. Radiographics. 2012;32:1483–501.PubMedCrossRefGoogle Scholar
  118. 118.
    Klaeser B, Mueller MD, Schmid RA, Guevara C, Krause T, Wiskirchen J. PET-CT-guided interventions in the management of FDG-positive lesions in patients suffering from solid malignancies: initial experiences. Eur Radiol. 2009;19:1780–5.PubMedCrossRefGoogle Scholar
  119. 119.
    O’Sullivan PJ, Rohren EM, Madewell JE. Positron emission tomography-CT imaging in guiding musculoskeletal biopsy. Radiol Clin N Am. 2008;46:475–86.PubMedCrossRefGoogle Scholar
  120. 120.
    Cerci JJ, Pereira Neto CC, Krauzer C, Sakamoto DG, Vitola JV, et al. The impact of coaxial core biopsy guided by FDG PET/CT in oncological patients. Eur J Nucl Med Mol Imaging. 2013;40:98–103.PubMedCrossRefGoogle Scholar
  121. 121.
    Purandare NC, Kulkarni AV, Kulkarni SS, Roy D, Agrawal A, Shah S, et al. 18F-FDG PET/CT-directed biopsy: does it offer incremental benefit? Nucl Med Commun. 2013;34:203–10.PubMedCrossRefGoogle Scholar
  122. 122.
    Tomozawa Y, Inaba Y, Yamaura H, Sato Y, Kato M, Kanamoto T, et al. Clinical value of CT-guided needle biopsy for retroperitoneal lesions. Korean J Radiol. 2011;12:351–7.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Binderup T, Knigge U, Loft A, Mortensen J, Pfeifer A, Federspiel B, et al. Functional imaging of neuroendocrine tumors: a head-to-head comparison of somatostatin receptors scintigraphy, 123I-MIBG scintigraphy, and 18F-FDG PET. J Nucl Med. 2010;51:704–12.PubMedCrossRefGoogle Scholar
  124. 124.
    Ezziddin S, Logvinski T, Yong-Hing C, Ahmadzadehfar H, Fischer HP, Palmedo H, et al. Factors predicting tracer uptake in somatostatin receptor and MIBG scintigraphy of metastatic gastroenteropancreatic neuroendocrine tumors. J Nucl Med. 2006;47:223–33.PubMedGoogle Scholar
  125. 125.
    Kayani I, Bomanji JB, Groves A, Conway G, Gacinovic S, Win T, Dickson J, et al. Functional imaging of neuroendocrine tumors with combined PET/CT using 68Ga-DOTATATE (DOTA-D-Phe1, Tyr3-octreo-tate) and 18F-FDG. Cancer. 2008;112:2447–55.PubMedCrossRefGoogle Scholar
  126. 126.
    Kauhanen S, Seppänen M, Minn H, Nuutila P. Clinical PET imaging of insulinoma and beta-cell hyperplasia. Curr Pharm Des. 2010;16:1550–60.PubMedCrossRefGoogle Scholar
  127. 127.
    Sundin A, Vullierme MP, Kaltsas G, Plöckinger U, Mallorca Consensus Conference Participants, European Neuroendocrine Tumor Society. ENETS consensus guidelines for the standards of care in neuroendocrine tumors: radiological examinations. Neuroendocrinology. 2009;90:167–83.PubMedCrossRefGoogle Scholar
  128. 128.
    Low MJ. Clinical endocrinology and metabolism: the somatostatin neuroendocrine system – physiology and clinical relevance in gastrointestinal and pancreatic disorders. Best Pract Res Clin Endocrinol Metab. 2004;18:607–22.PubMedCrossRefGoogle Scholar
  129. 129.
    de Herder WW, Hofland LJ, van der Lely AJ, Lamberts SW, et al. Somatostatin receptors in gastroentero-pancreatic neuroendocrine tumours. Endocr Relat Cancer. 2003;10:451–8.PubMedCrossRefGoogle Scholar
  130. 130.
    Veenstra MJ, de Herder WW, Feelders RA, Hofland LJ. Targeting the somatostatin receptor in pituitary and neuroendocrine tumors. Expert Opin Ther Targets. 2013;17:1329–43.PubMedCrossRefGoogle Scholar
  131. 131.
    de Herder WW, Lamberts SW. Somatostatin analog therapy in treatment of gastrointestinal disorders and tumors. Endocrine. 2003;20:285–90.PubMedCrossRefGoogle Scholar
  132. 132.
    Sundin A. Radiological and nuclear medicine imaging of gastroenteropancreatic neuroendocrine tumours. Best Pract Res Clin Gastroenterol. 2012;26:803–18.PubMedCrossRefGoogle Scholar
  133. 133.
    Kwekkeboom DJ, Kam BL, van Essen M, Teunissen JJ, van Eijck CH, Valkema R, et al. Somatostatin-receptor-based imaging and therapy of gastroenteropancreatic neuroendocrine tumors. Endocr Relat Cancer. 2010;17:R53–73.PubMedCrossRefGoogle Scholar
  134. 134.
    de Herder WW, Kwekkeboom DJ, Feelders RA, van Aken MO, Lamberts SW, van der Lely AJ, et al. Somatostatin receptor imaging for neuroendocrine tumors. Pituitary. 2006;9:243–8.PubMedCrossRefGoogle Scholar
  135. 135.
    Oberg K, Kvols L, Caplin M, Delle Fave G, de Herder W, Rindi G, et al. Consensus report on the use of somatostatin analogs for the management of neuroendocrine tumors of the gastroenteropancreatic system. Ann Oncol. 2004;15:966–73.PubMedCrossRefGoogle Scholar
  136. 136.
    Lamberts SW, van der Lely AJ, de Herder WW, Hofland LJ. Octreotide. N Engl J Med. 1996;334:246–54.PubMedCrossRefGoogle Scholar
  137. 137.
    Bodei L, Mueller-Brand J, Baum RP, Pavel ME, Hörsch D, O’Dorisio MS, et al. The joint IAEA, EANM, and SNMMI practical guidance on peptide receptor radionuclide therapy (PRRNT) in neuroendocrine tumours. Eur J Nucl Med Mol Imaging. 2013;40:800–16.PubMedPubMedCentralCrossRefGoogle Scholar
  138. 138.
    Kwekkeboom DJ, Krenning EP, Lebtahi R, Komminoth P, Kos-Kudła B, de Herder WW, et al. ENETS consensus guidelines for the standards of care in neuroendocrine tumors: peptide receptor radionuclide therapy with radiolabeled somatostatin analogs. Neuroendocrinology. 2009;90:220–6.PubMedCrossRefGoogle Scholar
  139. 139.
    Balon HR, Goldsmith SJ, Siegel BA, Silberstein EB, Krenning EP, Lang O, et al. Procedure guideline for somatostatin receptor scintigraphy with 111In-pentetreotide. J Nucl Med. 2001;42:1134–8.PubMedGoogle Scholar
  140. 140.
    de Herder WW, Niederle B, Scoazec JY, Pauwels S, Kloppel G, Falconi M, et al. Well-differentiated pancreatic tumor/carcinoma: insulinoma. Neuroendocrinology. 2006;84:183–8.PubMedCrossRefGoogle Scholar
  141. 141.
    Shah T, Kulakiene I, Quigley AM, Warbey VS, Srirajaskanthan R, Toumpanakis C, et al. The role of 99mTc-depreotide in the management of neuroendocrine tumours. Nucl Med Commun. 2008;29:436–40.PubMedCrossRefGoogle Scholar
  142. 142.
    Heppeler A, Froidevaux S, Eberle AN, Maecke HR, et al. Receptor targeting for tumor localisation and therapy with radiopeptides. Curr Med Chem. 2000;7:971–94.PubMedCrossRefGoogle Scholar
  143. 143.
    Smith-Jones PM, Bischof C, Leimer M, Gludovacz D, Angelberger P, Pangerl T, et al. DOTA-lanreotide: a novel somatostatin analog for tumor diagnosis and therapy. Endocrinology. 1999;140:5136–48.Google Scholar
  144. 144.
    Cwikla JB, Mikolajczak R, Pawlak D, Buscombe JR, Nasierowska-Guttmejer A, Bator A, et al. Initial direct comparison of 99mTc-TOC and 99mTc-TATE in identifying sites of disease in patients with proven GEP NETs. J Nucl Med. 2008;49:1060–5.PubMedCrossRefGoogle Scholar
  145. 145.
    Gabriel M, Muehllechner P, Decristoforo C, von Guggenberg E, Kendler D, Prommegger R, et al. 99mTc-EDDA/HYNIC-Tyr3-octreotide for staging and follow-up of patients with neuroendocrine gastro-entero-pancreatic tumors. Q J Nucl Med Mol Imaging. 2005;49:237–44.PubMedGoogle Scholar
  146. 146.
    Bombardieri E, Aktolun C, Baum RP, Bishof-Delaloye A, Buscombe J, Chatal JF, et al. 131I/123I-metaiodobenzylguanidine (MIBG), scintigraphy: procedure guidelines for tumour imaging. Eur J Nucl Med Mol Imaging. 2003;30:BP132–9.PubMedGoogle Scholar
  147. 147.
    Kaltsas G, Korbonits M, Heintz E, Mukherjee JJ, Jenkins PJ, Chew SL, et al. Comparison of somatostatin analog and meta-iodobenzylguanidine radionuclides in the diagnosis and localization of advanced neuroendocrine tumors. J Clin Endocrinol Metab. 2001;86:895–902.PubMedCrossRefGoogle Scholar
  148. 148.
    Kaltsas G, Rockall A, Papadogias D, Reznek R, Grossman AB, et al. Recent advances in radiological and radionuclide imaging and therapy of neuroendocrine tumours. Eur J Endocrinol. 2004;151:15–27.PubMedCrossRefGoogle Scholar
  149. 149.
    Buscombe JR, Cwikla JB, Caplin ME, Hilson AJ, et al. Long-term efficacy of low activity meta-131Iiodobenzylguanidine therapy in patients with disseminated neuroendocrine tumours depends on initial response. Nucl Med Commun. 2005;26:969–76.PubMedCrossRefGoogle Scholar
  150. 150.
    Taal BG, Zuetenhorst H, Valdés Olmos RA, Hoefnagel CA. 131I-MIBG radionuclide therapy in carcinoid syndrome. Eur J Surg Oncol. 2002;28:243.PubMedCrossRefGoogle Scholar
  151. 151.
    Jacobson AF, Deng H, Lombard J, Lessig HJ, Black RR, et al. 123I-meta-iodobenzylguanidine scintigraphy for the detection of neuroblastoma and pheochromocytoma: results of a meta-analysis. J Clin Endocrinol Metab. 2010;95:2596–606.PubMedCrossRefGoogle Scholar
  152. 152.
    Froberg AC, de Jong M, Nock BA, Breeman WA, Erion JL, Maina T, et al. Comparison of three radiolabelled peptide analogues for CCK-2 receptor scintigraphy in medullary thyroid carcinoma. Eur J Nucl Med Mol Imaging. 2009;36:1265–72.PubMedPubMedCentralCrossRefGoogle Scholar
  153. 153.
    Gotthardt M, Béhé MP, Beuter D, Battmann A, Bauhofer A, Schurrat T, et al. Improved tumour detection by gastrin receptor scintigraphy in patients with metastasised medullary thyroid carcinoma. Eur J Nucl Med Mol Imaging. 2006;33:1273–9.PubMedCrossRefGoogle Scholar
  154. 154.
    Nock BA, Maina T, Béhé M, Nikolopoulou A, Gotthardt M, Schmitt JS, et al. CCK-2/gastrin receptor-targeted tumor imaging with 99mTc-labeled minigastrinanalogs. J Nucl Med. 2005;46:1727–36.PubMedGoogle Scholar
  155. 155.
    Wild D, Christ E, Caplin ME, Kurzawinski TR, Forrer F, Brändle M, et al. Glucagon-like peptide-1 versus somatostatin receptor targeting reveals 2 distinct forms of malignant insulinomas. J Nucl Med. 2011;52:1073–8.PubMedCrossRefGoogle Scholar
  156. 156.
    Wild D, Mäcke H, Christ E, Gloor B, Reubi JC. Glucagon-like peptide 1-receptor scans to localize occult insulinomas. N Engl J Med. 2008;359:766–8.PubMedCrossRefGoogle Scholar
  157. 157.
    Christ E, Wild D, Forrer F, Brändle M, Sahli R, Clerici T, et al. Glucagon-like peptide-1 receptor imaging for localization of insulinomas. J Clin Endocrinol Metab. 2009;94:4398–405.PubMedCrossRefGoogle Scholar
  158. 158.
    Christ E, Wild D, Ederer S, Béhé M, Nicolas G, Caplin ME, et al. Glucagon-like peptide-1 receptor imaging for the localisation of insulinomas: a prospective multicentre imaging study. Lancet Diabetes Endocrinol. 2013;1:115–22.PubMedCrossRefGoogle Scholar
  159. 159.
    Doherty GM, Doppman JL, Shawker TH, Miller DL, Eastman RC, Gorden P, et al. Results of a prospective strategy to diagnose, localize, and resect insulinomas. Surgery. 1991;110:989–96.PubMedGoogle Scholar
  160. 160.
    Pach D, Sowa-Staszczak A, Jabrocka-Hybel A, Stefańska A, Tomaszuk M, Mikołajczak R, et al. Glucagon-like peptide-1 receptor imaging with (Lys40(Ahx-HYNIC-99mTc/EDDA)NH2)–exendin-4 for the diagnosis of recurrence or dissemination of medullary thyroid cancer: a preliminary report. Int J Endocrinol. 2013;2013:384508.PubMedPubMedCentralCrossRefGoogle Scholar
  161. 161.
    Sowa-Staszczak A, Pach D, Mikołajczak R, Mäcke H, Jabrocka-Hybel A, Stefańska A, et al. 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. 2013;40:524–31.PubMedCrossRefGoogle Scholar
  162. 162.
    Brom M, Oyen WJ, Joosten L, Gotthardt M, Boerman OC. 68Ga-labelled exendin-3, a new agent for the detection of insulinomas with PET. Eur J Nucl Med Mol Imaging. 2010;37:1345–55.PubMedPubMedCentralCrossRefGoogle Scholar
  163. 163.
    Hessenius C, Bäder M, Meinhold H, Böhmig M, Faiss S, Reubi JC, et al. Vasoactive intestinal peptide receptor scintigraphy in patients with pancreatic adenocarcinomas or neuroendocrine tumours. Eur J Nucl Med. 2000;27:1684–93.PubMedCrossRefGoogle Scholar
  164. 164.
    Virgolini I, Kurtaran A, Leimer M, Kaserer K, Peck-Radosavljevic M, Angelberger P, et al. Location of a VIPoma by iodine-123-vasoactive intestinal peptide scintigraphy. J Nucl Med. 1998;39:1575–9.PubMedGoogle Scholar
  165. 165.
    Virgolini I, Raderer M, Kurtaran A, Angelberger P, Banyai S, Yang Q, et al. Vasoactive intestinal peptide-receptor imaging for the localization of intestinal adenocarcinomas and endocrine tumors. N Engl J Med. 1994;331:1116–21.PubMedCrossRefGoogle Scholar
  166. 166.
    Wild D, Bomanji JB, Benkert P, Maecke H, Ell PJ, et al. Comparison of 68Ga-DOTANOC and 68Ga-DOTATATE PET/CT within patients with gastroenteropancreatic neuroendocrine tumors. J Nucl Med. 2013;54:364–72.PubMedCrossRefGoogle Scholar
  167. 167.
    Haug AR, Cindea-Drimus R, Auernhammer CJ, Reincke M, Wängler B, et al. The role of 68Ga-DOTATATE PET/CT in suspected neuroendocrine tumors. J Nucl Med. 2012;53:1686–92.PubMedCrossRefGoogle Scholar
  168. 168.
    Schraml C, Schwenzer NF, Sperling O, Aschoff P, Lichy MP, et al. Staging of neuroendocrine tumours: comparison of 68Ga-DOTATOC multiphase PET/CT and whole-body MRI. Cancer Imaging. 2013;13:63–72.PubMedPubMedCentralCrossRefGoogle Scholar
  169. 169.
    Ambrosini V, Campana D, Nanni C, Cambioli S, Tomassetti P, et al. Is 68Ga-DOTA-NOC PET/CT indicated in patients with clinical, biochemical or radiological suspicion of neuroendocrine tumour? Eur J Nucl Med Mol Imaging. 2012;39:1278–83.PubMedCrossRefGoogle Scholar
  170. 170.
    Binderup T, Knigge U, Loft A, Federspiel B, Kjaer A. 18F-fluorodeoxy-glucose positron emission tomography predicts survival of patients with neuroendocrine tumors. Clin Cancer Res. 2010;16:978–85.PubMedCrossRefGoogle Scholar
  171. 171.
    Abgral R, Leboulleux S, Déandreis D, Aupérin A, Lumbroso J, et al. Performance of 18fluorodeoxyglucose-positron emission tomography and somatostatin receptor scintigraphy for high Ki67 (R10%) well-differentiated endocrine carcinoma staging. J Clin Endocrinol Metab. 2011;96:665–71.PubMedCrossRefGoogle Scholar
  172. 172.
    Severi S, Nanni O, Bodei L, Sansovini M, Ianniello A, et al. Role of 18FDG PET/CT in patients treated with 177Lu-DOTATATE for advanced differentiated neuroendocrine tumours. Eur J Nucl Med Mol Imaging. 2013;40:881–8.PubMedCrossRefGoogle Scholar
  173. 173.
    van Essen M, Sundin A, Krenning EP, Kwekkeboom DJ, et al. Neuroendocrine tumours: the role of imaging for diagnosis and therapy. Nat Rev Endocrinol. 2014;10:102–14.PubMedCrossRefGoogle Scholar
  174. 174.
    Rufini V, Baum RP, Castaldi P, Treglia G, De Gaetano AM, et al. Role of PET/CT in the functional imaging of endocrine pancreatic tumors. Abdom Imaging. 2012;37:1004–20.PubMedCrossRefGoogle Scholar
  175. 175.
    Orlefors H, Sundin A, Ahlström H, Bjurling P, Bergström M, Lilja A, et al. Positron emission tomography with 5-hydroxytryptophan in neuroendocrine tumors. J Clin Oncol. 1998;16:2534–41.PubMedCrossRefGoogle Scholar
  176. 176.
    Orlefors H, Sundin A, Garske U, Juhlin C, Oberg K, Skogseid B, et al. Whole-body 11C-5-hydroxytryptophan positron emission tomography as a universal imaging technique for neuroendocrine tumors – comparison with somatostatin receptor scintigraphy and computed tomography. J Clin Endocrinol Metab. 2005;90:3392–400.PubMedCrossRefGoogle Scholar
  177. 177.
    Buck AC, Schirrmeister HH, Guhlmann CA, Diederichs CG, Shen C, Buchmann I, et al. Ki-67 immunostaining in pancreatic cancer and chronic active pancreatitis: does in vivo FDG uptake correlate with proliferative activity? J Nucl Med. 2001;42:721–5.PubMedGoogle Scholar
  178. 178.
    Shields AF, Grierson JR, Dohmen BM, Machulla HJ, Stayanoff JC, Lawhorn-Crews JM, et al. Imaging proliferation in vivo with [F-18]FLT and positron emission tomography. Nat Med. 1998;4:1334–6.PubMedCrossRefGoogle Scholar
  179. 179.
    von Forstner C, Egberts JH, Ammerpohl O, Niedzielska D, Buchert R, Mikecz P, et al. Gene expression patterns and tumor uptake of 18F-FDG, 18FFLT, and 18F-FEC in PET/MRI of an orthotopic mouse xenotransplantation model of pancreatic cancer. J Nucl Med. 2008;49:1362–70.CrossRefGoogle Scholar
  180. 180.
    Wang X, Fani M, Schulz S, Rivier J, Reubi JC, Maecke HR. Comprehensive evaluation of a somatostatin-based radiolabelled antagonist for diagnostic imaging and radionuclide therapy. Eur J Nucl Med Mol Imaging. 2012;39:1876–85.PubMedCrossRefGoogle Scholar
  181. 181.
    Marsouvanidis PJ, Maina T, Sallegger W, Krenning EP, de Jong M, Nock BA. 99mTc radiotracers based on human GRP(18–27): synthesis and comparative evaluation. J Nucl Med. 2013;54:1797–803.PubMedCrossRefGoogle Scholar
  182. 182.
    Richter S, Wuest M, Krieger SS, Rogers BE, Friebe M, Bergmann R, et al. Synthesis and radiopharmacological evaluation of a high-affinity and metabolically stabilized 18F-labeled bombesin analogue for molecular imaging of gastrin-releasing peptide receptor-expressing prostate cancer. Nucl Med Biol. 2013;40:1025–34.PubMedCrossRefGoogle Scholar
  183. 183.
    Varasteh Z, Aberg O, Velikyan I, Lindeberg G, Sörensen J, Larhed M, et al. In vitro and in vivo evaluation of a18F-labeled high affinity NOTA conjugated bombesin antagonist as a PET ligand for GRPR-targeted tumor imaging. PLoS ONE. 2013;8, e81932.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Elena Tabacchi
    • 1
    Email author
  • Cristina Nanni
    • 1
  • Irene Bossert
    • 1
    • 3
  • Anna Margherita Maffione
    • 2
  • Stefano Fanti
    • 1
  1. 1.Nuclear Medicine Unit“S. Orsola-Malpighi” University HospitalBolognaItaly
  2. 2.Nuclear Medicine UnitOspedale Santa Maria della MisericordiaRovigoItaly
  3. 3.Nuclear Medicine Service“Fondazione Salvatore Maugeri” IRCCSPaviaItaly

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