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Review Article| Volume 18, ISSUE 2, P267-286, April 2023

Neuroendocrine Tumor Therapy Response Assessment

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      References

        • Strosberg J.
        • El-Haddad G.
        • Wolin E.
        • et al.
        Phase 3 trial of (177)Lu-DOTATATE for midgut neuroendocrine tumors.
        N Engl J Med. 2017; 376: 125-135
        • Strosberg J.R.
        • Caplin M.E.
        • Kunz P.L.
        • et al.
        (177)Lu-DOTATATE plus long-acting octreotide versus high-dose long-acting octreotide in patients with midgut neuroendocrine tumours (NETTER-1): final overall survival and long-term safety results from an open-label, randomised, controlled, phase 3 trial.
        Lancet Oncol. 2021; 22: 1752-1763
        • Krenning E.P.
        • de Jong M.
        • Kooij P.P.
        • et al.
        Radiolabelled somatostatin analogue(s) for peptide receptor scintigraphy and radionuclide therapy.
        Ann Oncol. 1999; 10: S23-S29
        • Bodei L.
        • Mueller-Brand J.
        • Baum R.P.
        • 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: 800-816
        • Bodei L.
        • Cremonesi M.
        • Grana C.
        • et al.
        Receptor radionuclide therapy with 90Y-[DOTA]0-Tyr3-octreotide (90Y-DOTATOC) in neuroendocrine tumours.
        Eur J Nucl Med Mol Imaging. 2004; 31: 1038-1046
        • de Jong M.
        • Breeman W.A.
        • Bernard B.F.
        • et al.
        [177Lu-DOTA(0),Tyr3] octreotate for somatostatin receptor-targeted radionuclide therapy.
        Int J Cancer. 2001; 92: 628-633
        • Kwekkeboom D.J.
        • Bakker W.H.
        • Kam B.L.
        • et al.
        Treatment of patients with gastro-entero-pancreatic (GEP) tumours with the novel radiolabelled somatostatin analogue [177Lu-DOTA(0),Tyr3]octreotate.
        Eur J Nucl Med Mol Imaging. 2003; 30: 417-422
        • Strosberg J.
        • Wolin E.
        • Chasen B.
        • et al.
        Health-related quality of life in patients with progressive midgut neuroendocrine tumors treated with (177)Lu-DOTATATE in the phase III NETTER-1 trial.
        J Clin Oncol. 2018; 36: 2578-2584
        • Strosberg J.
        • Kunz P.L.
        • Hendifar A.
        • et al.
        Impact of liver tumour burden, alkaline phosphatase elevation, and target lesion size on treatment outcomes with (177)Lu-DOTATATE: an analysis of the NETTER-1 study.
        Eur J Nucl Med Mol Imaging. 2020; 47: 2372-2382
        • Mariniello A.
        • Bodei L.
        • Tinelli C.
        • et al.
        Long-term results of PRRT in advanced bronchopulmonary carcinoid.
        Eur J Nucl Med Mol Imaging. 2016; 43: 441-452
        • Pavel M.E.
        • Rinke A.
        • Baum R.P.
        1335TiP - COMPETE trial: peptide receptor radionuclide therapy (PRRT) with 177Lu-edotreotide vs. everolimus in progressive GEP-NET.
        Ann Oncol. 2018; 29: viii478
        • Jungels C.
        • Deleporte A.
        State of the art and future directions in the systemic treatment of neuroendocrine neoplasms.
        Curr Opin Oncol. 2021; 33: 378-385
        • Halfdanarson T.R.
        • Reidy D.L.
        • Vijayvergia N.
        • et al.
        Pivotal phase III COMPOSE trial will compare 177Lu-edotreotide with best standard of care for well-differentiated aggressive grade 2 and grade 3 gastroenteropancreatic neuroendocrine tumors.
        J Clin Oncol. 2022; 40: TPS514-TPS
        • Kratochwil C.
        • Apostolidis L.
        • Rathke H.
        • et al.
        Dosing (225)Ac-DOTATOC in patients with somatostatin-receptor-positive solid tumors: 5-year follow-up of hematological and renal toxicity.
        Eur J Nucl Med Mol Imaging. 2021; 49: 54-63
        • Bruchertseifer F.
        • Kellerbauer A.
        • Malmbeck R.
        • et al.
        Targeted alpha therapy with bismuth-213 and actinium-225: meeting future demand.
        J Labelled Comp Radiopharm. 2019; 62: 794-802
        • Cazzato R.L.
        • Hubelé F.
        • De Marini P.
        • et al.
        Liver-directed therapy for neuroendocrine metastases: from interventional radiology to nuclear medicine procedures.
        Cancers (Basel). 2021; 13: 6368
        • Rudisile S.
        • Gosewisch A.
        • Wenter V.
        • et al.
        Salvage PRRT with (177)Lu-DOTA-octreotate in extensively pretreated patients with metastatic neuroendocrine tumor (NET): dosimetry, toxicity, efficacy, and survival.
        BMC Cancer. 2019; 19: 788
        • Bodei L.
        • Kidd M.
        • Paganelli G.
        • et al.
        Long-term tolerability of PRRT in 807 patients with neuroendocrine tumours: the value and limitations of clinical factors.
        Eur J Nucl Med Mol Imaging. 2015; 42: 5-19
        • Sabet A.
        • Ezziddin K.
        • Pape U.F.
        • et al.
        Long-term hematotoxicity after peptide receptor radionuclide therapy with 177Lu-octreotate.
        J Nucl Med. 2013; 54: 1857-1861
        • Kwekkeboom D.J.
        • Kam B.L.
        • van Essen M.
        • et al.
        Somatostatin-receptor-based imaging and therapy of gastroenteropancreatic neuroendocrine tumors.
        Endocr Relat Cancer. 2010; 17: R53-R73
        • Singh S.
        • Granberg D.
        • Wolin E.
        • et al.
        Patient-reported burden of a neuroendocrine tumor (NET) diagnosis: results from the first global survey of patients with NETs.
        J Glob Oncol. 2017; 3: 43-53
        • Halperin D.M.
        • Huynh L.
        • Beaumont J.L.
        • et al.
        Assessment of change in quality of life, carcinoid syndrome symptoms and healthcare resource utilization in patients with carcinoid syndrome.
        BMC Cancer. 2019; 19: 274
        • Warsame R.
        • D'Souza A.
        Patient reported outcomes have arrived: a practical overview for clinicians in using patient reported outcomes in oncology.
        Mayo Clin Proc. 2019; 94: 2291-2301
        • Barcaccia B.
        • Esposito G.
        • Matarese M.
        • et al.
        Defining quality of life: a wild-goose chase?.
        Eur J Psychol. 2013; 9: 185-203
        • Basch E.
        • Deal A.M.
        • Kris M.G.
        • et al.
        Symptom monitoring with patient-reported outcomes during routine cancer treatment: a randomized controlled trial.
        J Clin Oncol. 2016; 34: 557-565
        • Chau I.
        • Casciano R.
        • Willet J.
        • et al.
        Quality of life, resource utilisation and health economics assessment in advanced neuroendocrine tumours: a systematic review.
        Eur J Cancer Care (Engl). 2013; 22: 714-725
        • Oken M.M.
        • Creech R.H.
        • Tormey D.C.
        • et al.
        Toxicity and response criteria of the Eastern Cooperative Oncology Group.
        Am J Clin Oncol. 1982; 5: 649-655
        • Aaronson N.K.
        • Ahmedzai S.
        • Bergman B.
        • et al.
        The European Organization for Research and Treatment of Cancer QLQ-C30: a quality-of-life instrument for use in international clinical trials in oncology.
        J Natl Cancer Inst. 1993; 85: 365-376
        • Cella D.F.
        • Tulsky D.S.
        • Gray G.
        • et al.
        The functional assessment of cancer therapy scale: development and validation of the general measure.
        J Clin Oncol. 1993; 11: 570-579
        • Yadegarfar G.
        • Friend L.
        • Jones L.
        • et al.
        Validation of the EORTC QLQ-GINET21 questionnaire for assessing quality of life of patients with gastrointestinal neuroendocrine tumours.
        Br J Cancer. 2013; 108: 301-310
        • Vinik E.
        • Carlton C.A.
        • Silva M.P.
        • et al.
        Development of the Norfolk quality of life tool for assessing patients with neuroendocrine tumors.
        Pancreas. 2009; 38: e87-e95
        • Kwekkeboom D.J.
        • de Herder W.W.
        • Kam B.L.
        • et al.
        Treatment with the radiolabeled somatostatin analog [177 Lu-DOTA 0,Tyr3]octreotate: toxicity, efficacy, and survival.
        J Clin Oncol. 2008; 26: 2124-2130
        • Marinova M.
        • Mücke M.
        • Mahlberg L.
        • et al.
        Improving quality of life in patients with pancreatic neuroendocrine tumor following peptide receptor radionuclide therapy assessed by EORTC QLQ-C30.
        Eur J Nucl Med Mol Imaging. 2018; 45: 38-46
        • Khan S.
        • Krenning E.P.
        • van Essen M.
        • et al.
        Quality of life in 265 patients with gastroenteropancreatic or bronchial neuroendocrine tumors treated with [177Lu-DOTA0,Tyr3]Octreotate.
        J Nucl Med. 2011; 52: 1361
        • Ma Z.Y.
        • Gong Y.F.
        • Zhuang H.K.
        • et al.
        Pancreatic neuroendocrine tumors: a review of serum biomarkers, staging, and management.
        World J Gastroenterol. 2020; 26: 2305-2322
        • Oberg K.
        • Modlin I.M.
        • De Herder W.
        • et al.
        Consensus on biomarkers for neuroendocrine tumour disease.
        Lancet Oncol. 2015; 16: e435-e446
        • Feldman S.A.
        • Eiden L.E.
        The chromogranins: their roles in secretion from neuroendocrine cells and as markers for neuroendocrine neoplasia.
        Endocr Pathol. 2003; 14: 3-23
        • Kidd M.
        • Bodei L.
        • Modlin I.M.
        Chromogranin A: any relevance in neuroendocrine tumors?.
        Curr Opin Endocrinol Diabetes Obes. 2016; 23: 28-37
        • Brabander T.
        • van der Zwan W.A.
        • Teunissen J.J.M.
        • et al.
        Pitfalls in the response evaluation after peptide receptor radionuclide therapy with [(177)Lu-DOTA(0),Tyr(3)]octreotate.
        Endocr Relat Cancer. 2017; 24: 243-251
        • Zissimopoulos A.
        • Vradelis S.
        • Konialis M.
        • et al.
        Chromogranin A as a biomarker of disease activity and biologic therapy in inflammatory bowel disease: a prospective observational study.
        Scand J Gastroenterol. 2014; 49: 942-949
        • Biondi A.
        • Malaguarnera G.
        • Vacante M.
        • et al.
        Elevated serum levels of chromogranin A in hepatocellular carcinoma.
        BMC Surg. 2012; 12: S7
        • Hong P.
        • Guo R.Q.
        • Song G.
        • et al.
        Prognostic role of chromogranin A in castration-resistant prostate cancer: a meta-analysis.
        Asian J Androl. 2018; 20: 561-566
        • Hong L.
        • Wang Y.
        • Zhang T.
        • et al.
        Chromogranin A: a valuable serum diagnostic marker for non-insulinoma neuroendocrine tumors of the pancreas in a Chinese population.
        Med Sci Monit. 2020; 26: e926635
        • Oberg K.
        • Jelic S.O.
        Neuroendocrine gastroenteropancreatic tumors: ESMO clinical recommendation for diagnosis, treatment and follow-up.
        Ann Oncol. 2009; 20: iv150-iv153
        • Burghuber O.C.
        • Worofka B.
        • Schernthaner G.
        • et al.
        Serum neuron-specific enolase is a useful tumor marker for small cell lung cancer.
        Cancer. 1990; 65: 1386-1390
        • Gambichler T.
        • Abu Rached N.
        • Susok L.
        • et al.
        Serum neuron-specific enolase independently predicts outcomes of patients with Merkel cell carcinoma.
        Br J Dermatol. 2022; 187: 806-808
        • Nobels F.R.
        • Kwekkeboom D.J.
        • Coopmans W.
        • et al.
        Chromogranin A as serum marker for neuroendocrine neoplasia: comparison with neuron-specific enolase and the alpha-subunit of glycoprotein hormones.
        J Clin Endocrinol Metab. 1997; 82: 2622-2628
        • Tirosh A.
        • Nilubol N.
        • Patel D.
        • et al.
        Prognostic utility of 24-hour urinary 5-HIAA doubling time in patients with neuroendocrine tumors.
        Endocr Pract. 2018; 24: 710-717
        • Feldman J.M.
        • O'Dorisio T.M.
        Role of neuropeptides and serotonin in the diagnosis of carcinoid tumors.
        Am J Med. 1986; 81: 41-48
        • Adaway J.E.
        • Dobson R.
        • Walsh J.
        • et al.
        Serum and plasma 5-hydroxyindoleacetic acid as an alternative to 24-h urine 5-hydroxyindoleacetic acid measurement.
        Ann Clin Biochem. 2016; 53: 554-560
        • Oberg K.
        • Couvelard A.
        • Delle Fave G.
        • et al.
        ENETS consensus guidelines for standard of care in neuroendocrine tumours: biochemical markers.
        Neuroendocrinology. 2017; 105: 201-211
        • Janson E.T.
        • Holmberg L.
        • Stridsberg M.
        • et al.
        Carcinoid tumors: analysis of prognostic factors and survival in 301 patients from a referral center.
        Ann Oncol. 1997; 8: 685-690
        • Huizing D.M.V.
        • Aalbersberg E.A.
        • Versleijen M.W.J.
        • et al.
        Early response assessment and prediction of overall survival after peptide receptor radionuclide therapy.
        Cancer Imaging. 2020; 20: 57
        • Kidd M.
        • Drozdov I.
        • Modlin I.
        Blood and tissue neuroendocrine tumor gene cluster analysis correlate, define hallmarks and predict disease status.
        Endocr Relat Cancer. 2015; 22: 561-575
        • Sang M.
        • Wu X.
        • Fan X.
        • et al.
        Multiple MAGE-A genes as surveillance marker for the detection of circulating tumor cells in patients with ovarian cancer.
        Biomarkers. 2014; 19: 34-42
        • Barrera-Saldaña H.A.
        • Fernández-Garza L.E.
        • Barrera-Barrera S.A.
        Liquid biopsy in chronic liver disease.
        Ann Hepatol. 2021; 20: 100197
        • Bodei L.
        • Kidd M.S.
        • Singh A.
        • et al.
        PRRT neuroendocrine tumor response monitored using circulating transcript analysis: the NETest.
        Eur J Nucl Med Mol Imaging. 2020; 47: 895-906
        • Modlin I.M.
        • Kidd M.
        • Malczewska A.
        • et al.
        The NETest: the clinical utility of multigene blood analysis in the diagnosis and management of neuroendocrine tumors.
        Endocrinol Metab Clin North Am. 2018; 47: 485-504
        • Modlin I.M.
        • Drozdov I.
        • Kidd M.
        The identification of gut neuroendocrine tumor disease by multiple synchronous transcript analysis in blood.
        PLoS One. 2013; 8: e63364
        • Liu E.
        • Paulson S.
        • Gulati A.
        • et al.
        Assessment of NETest clinical utility in a U.S. Registry-based study.
        Oncologist. 2019; 24: 783-790
        • Malczewska A.
        • Oberg K.
        • Bodei L.
        • et al.
        NETest liquid biopsy is diagnostic of lung neuroendocrine tumors and Identifies progressive disease.
        Neuroendocrinology. 2019; 108: 219-231
        • Bodei L.
        • Kidd M.S.
        • Singh A.
        • et al.
        PRRT genomic signature in blood for prediction of (177)Lu-octreotate efficacy.
        Eur J Nucl Med Mol Imaging. 2018; 45: 1155-1169
        • Schueller G.
        • Schima W.
        • Schueller-Weidekamm C.
        • et al.
        Multidetector CT of pancreas: effects of contrast material flow rate and individualized scan delay on enhancement of pancreas and tumor contrast.
        Radiology. 2006; 241: 441-448
        • Eisenhauer E.A.
        • Therasse P.
        • Bogaerts J.
        • et al.
        New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1).
        Eur J Cancer. 2009; 45: 228-247
        • de Mestier L.
        • Dromain C.
        • d'Assignies G.
        • et al.
        Evaluating digestive neuroendocrine tumor progression and therapeutic responses in the era of targeted therapies: state of the art.
        Endocr Relat Cancer. 2014; 21: R105-R120
        • Luo Y.
        • Chen J.
        • Huang K.
        • et al.
        Early evaluation of sunitinib for the treatment of advanced gastroenteropancreatic neuroendocrine neoplasms via CT imaging: RECIST 1.1 or Choi Criteria?.
        BMC Cancer. 2017; 17: 154
        • Solis-Hernandez M.P.
        • Fernandez Del Valle A.
        • Carmona-Bayonas A.
        • et al.
        Evaluating radiological response in pancreatic neuroendocrine tumours treated with sunitinib: comparison of Choi versus RECIST criteria (CRIPNET_ GETNE1504 study).
        Br J Cancer. 2019; 121: 537-544
        • Zwirtz K.
        • Hardt J.
        • Acker G.
        • et al.
        Comparison of CHOI, RECIST and somatostatin receptor PET/CT based criteria for the evaluation of response and response prediction to PRRT.
        Pharmaceutics. 2022; 14: 1278
        • Das S.
        • Pineda G.
        • Berlin J.
        • et al.
        Hidden figures: occult intra-cardiac metastases in asymptomatic neuroendocrine tumor patients.
        J Oncol Cancer Res. 2018; 2: 23-27
        • Blažević A.
        • Zandee W.T.
        • Franssen G.J.H.
        • et al.
        Mesenteric fibrosis and palliative surgery in small intestinal neuroendocrine tumours.
        Endocr Relat Cancer. 2018; 25: 245-254
        • Blažević A.
        • Brabander T.
        • Zandee W.T.
        • et al.
        Evolution of the mesenteric mass in small intestinal neuroendocrine tumours.
        Cancers (Basel). 2021; 13: 443
        • Choi H.
        • Charnsangavej C.
        • de Castro Faria S.
        • et al.
        CT evaluation of the response of gastrointestinal stromal tumors after imatinib mesylate treatment: a quantitative analysis correlated with FDG PET findings.
        AJR Am J Roentgenol. 2004; 183: 1619-1628
        • Chen M.Y.
        • Bechtold R.E.
        • Savage P.D.
        Cystic changes in hepatic metastases from gastrointestinal stromal tumors (GISTs) treated with Gleevec (imatinib mesylate).
        AJR Am J Roentgenol. 2002; 179: 1059-1062
        • Grimaldi S.
        • Terroir M.
        • Caramella C.
        Advances in oncological treatment: limitations of RECIST 1.1 criteria.
        Q J Nucl Med Mol Imaging. 2018; 62: 129-139
        • Choi H.
        • Charnsangavej C.
        • Faria S.C.
        • et al.
        Correlation of computed tomography and positron emission tomography in patients with metastatic gastrointestinal stromal tumor treated at a single Institution with imatinib mesylate: proposal of new computed tomography response criteria.
        J Clin Oncol. 2007; 25: 1753-1759
        • Oberg K.
        • Krenning E.
        • Sundin A.
        • et al.
        A delphic consensus assessment: imaging and biomarkers in gastroenteropancreatic neuroendocrine tumor disease management.
        Endocr Connect. 2016; 5: 174-187
        • Rodallec M.
        • Vilgrain V.
        • Couvelard A.
        • et al.
        Endocrine pancreatic tumours and helical ct: contrast enhancement is correlated with microvascular density, histoprognostic factors and survival.
        Pancreatology. 2006; 6: 77-85
        • Arai T.
        • Kobayashi A.
        • Fujinaga Y.
        • et al.
        Contrast-enhancement ratio on multiphase enhanced computed tomography predicts recurrence of pancreatic neuroendocrine tumor after curative resection.
        Pancreatology. 2016; 16: 397-402
        • Pettersson O.
        • Fröss-Baron K.
        • Crona J.
        • et al.
        Tumor contrast-enhancement for monitoring of PRRT (177)Lu-DOTATATE in pancreatic neuroendocrine tumor patients.
        Front Oncol. 2020; 10: 193
        • Yao J.
        • Phan A.
        • Fogleman D.
        • et al.
        Randomized run-in study of bevacizumab (B) and everolimus (E) in low-to intermediate-grade neuroendocrine tumors (LGNETs) using perfusion CT as functional biomarker.
        J Clin Oncol. 2010; 28: 4002
        • Ng C.S.
        • Charnsangavej C.
        • Wei W.
        • et al.
        Perfusion CT findings in patients with metastatic carcinoid tumors undergoing bevacizumab and interferon therapy.
        Am J Roentgenol. 2011; 196: 569-576
        • Weikert T.
        • Maas O.C.
        • Haas T.
        • et al.
        Early prediction of treatment response of neuroendocrine hepatic metastases after peptide receptor radionuclide therapy with (90)Y-DOTATOC using diffusion weighted and dynamic contrast-enhanced MRI.
        Contrast Media Mol Imaging. 2019; 2019: 1517208
        • Miyazaki K.
        • Orton M.R.
        • Davidson R.L.
        • et al.
        Neuroendocrine tumor liver metastases: use of dynamic contrast-enhanced MR imaging to monitor and predict radiolabeled octreotide therapy response.
        Radiology. 2012; 263: 139-148
        • Werner R.A.
        • Solnes L.B.
        • Javadi M.S.
        • et al.
        SSTR-RADS version 1.0 as a reporting system for SSTR PET imaging and selection of potential PRRT candidates: a proposed standardization framework.
        J Nucl Med. 2018; 59: 1085-1091
        • Zidan L.
        • Iravani A.
        • Oleinikov K.
        • et al.
        Efficacy and safety of (177)Lu-DOTATATE in lung neuroendocrine tumors: a bicenter study.
        J Nucl Med. 2022; 63: 218-225
        • Ambrosini V.
        • Campana D.
        • Polverari G.
        • et al.
        Prognostic value of 68Ga-DOTANOC PET/CT SUVmax in patients with neuroendocrine tumors of the pancreas.
        J Nucl Med. 2015; 56: 1843-1848
        • Kratochwil C.
        • Stefanova M.
        • Mavriopoulou E.
        • et al.
        SUV of [68Ga]DOTATOC-PET/CT predicts response probability of PRRT in neuroendocrine tumors.
        Mol Imaging Biol. 2015; 17: 313-318
        • Durmo R.
        • Filice A.
        • Fioroni F.
        • et al.
        Predictive and prognostic role of pre-therapy and interim 68Ga-DOTATOC PET/CT parameters in metastatic advanced neuroendocrine tumor patients treated with PRRT.
        Cancers (Basel). 2022; 14: 592
        • Sharma R.
        • Wang W.M.
        • Yusuf S.
        • et al.
        68)Ga-DOTATATE PET/CT parameters predict response to peptide receptor radionuclide therapy in neuroendocrine tumours.
        Radiother Oncol. 2019; 141: 108-115
        • Ortega C.
        • Wong R.K.S.
        • Schaefferkoetter J.
        • et al.
        Quantitative (68)Ga-DOTATATE PET/CT parameters for the prediction of therapy response in patients with progressive metastatic neuroendocrine tumors treated with (177)Lu-DOTATATE.
        J Nucl Med. 2021; 62: 1406-1414
        • Mahajan S.
        • O’Donoghue J.
        • Weber W.
        • et al.
        Integrating early rapid post-peptide receptor radionuclide therapy quality assurance scan into the outpatient setting.
        J Nucl Med Radiat Ther. 2019; 10: 395
        • Aalbersberg E.A.
        • de Vries-Huizing D.M.V.
        • Tesselaar M.E.T.
        • et al.
        Post-PRRT scans: which scans to make and what to look for.
        Cancer Imaging. 2022; 22: 29
        • Bozkurt M.F.
        • Virgolini I.
        • Balogova S.
        • et al.
        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. 2017; 44: 1588-1601
        • Shah M.H.
        • Goldner W.S.
        • Benson A.B.
        • et al.
        Neuroendocrine and adrenal tumors, version 2.2021, NCCN clinical practice guidelines in oncology.
        J Natl Compr Canc Netw. 2021; 19: 839-868
        • Hofman M.S.
        • Lau W.F.
        • Hicks R.J.
        Somatostatin receptor imaging with 68Ga DOTATATE PET/CT: clinical utility, normal patterns, pearls, and pitfalls in interpretation.
        Radiographics. 2015; 35: 500-516
        • Cherk M.H.
        • Kong G.
        • Hicks R.J.
        • et al.
        Changes in biodistribution on (68)Ga-DOTA-Octreotate PET/CT after long acting somatostatin analogue therapy in neuroendocrine tumour patients may result in pseudoprogression.
        Cancer Imaging. 2018; 18: 3
        • Beauregard J.M.
        • Hofman M.S.
        • Kong G.
        • et al.
        The tumour sink effect on the biodistribution of 68Ga-DOTA-octreotate: implications for peptide receptor radionuclide therapy.
        Eur J Nucl Med Mol Imaging. 2012; 39: 50-56
        • Basu S.
        • Ranade R.
        • Abhyankar A.
        "Tumour sink effect" on the diagnostic or posttreatment radioiodine scan due to sequestration into large-volume functioning metastasis of differentiated thyroid carcinoma influencing uptake in smaller metastatic sites or remnant thyroid tissue: an uncommon but possible phenomenon in thyroid cancer practice.
        World J Nucl Med. 2020; 19: 141-143
        • Severi S.
        • Nanni O.
        • Bodei L.
        • 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: 881-888
        • Thapa P.
        • Ranade R.
        • Ostwal V.
        • et al.
        Performance of 177Lu-DOTATATE-based peptide receptor radionuclide therapy in metastatic gastroenteropancreatic neuroendocrine tumor: a multiparametric response evaluation correlating with primary tumor site, tumor proliferation index, and dual tracer imaging characteristics.
        Nucl Med Commun. 2016; 37: 1030-1037
        • Alevroudis E.
        • Spei M.E.
        • Chatziioannou S.N.
        • et al.
        Clinical utility of (18)F-FDG PET in neuroendocrine tumors prior to peptide receptor radionuclide therapy: a systematic review and meta-analysis.
        Cancers (Basel). 2021; 13: 1813
        • Pape U.F.
        • Berndt U.
        • Müller-Nordhorn J.
        • et al.
        Prognostic factors of long-term outcome in gastroenteropancreatic neuroendocrine tumours.
        Endocr Relat Cancer. 2008; 15: 1083-1097
        • Rindi G.
        • D'Adda T.
        • Froio E.
        • et al.
        Prognostic factors in gastrointestinal endocrine tumors.
        Endocr Pathol. 2007; 18: 145-149
        • Frilling A.
        • Modlin I.M.
        • Kidd M.
        • et al.
        Recommendations for management of patients with neuroendocrine liver metastases.
        Lancet Oncol. 2014; 15: e8-e21
        • Fiore F.
        • Del Prete M.
        • Franco R.
        • et al.
        Transarterial embolization (TAE) is equally effective and slightly safer than transarterial chemoembolization (TACE) to manage liver metastases in neuroendocrine tumors.
        Endocrine. 2014; 47: 177-182
        • Paprottka P.M.
        • Hoffmann R.T.
        • Haug A.
        • et al.
        Radioembolization of symptomatic, unresectable neuroendocrine hepatic metastases using yttrium-90 microspheres.
        Cardiovasc Intervent Radiol. 2012; 35: 334-342
        • Dermine S.
        • Palmieri L.J.
        • Lavolé J.
        • et al.
        Non-pharmacological therapeutic options for liver metastases in advanced neuroendocrine tumors.
        J Clin Med. 2019; 8: 1907
        • Guibal A.
        • Lefort T.
        • Chardon L.
        • et al.
        Contrast-enhanced ultrasound after devascularisation of neuroendocrine liver metastases: functional and morphological evaluation.
        Eur Radiol. 2013; 23: 805-815
        • Fowler K.J.
        • Maughan N.M.
        • Laforest R.
        • et al.
        PET/MRI of hepatic 90Y microsphere Deposition Determines individual tumor response.
        Cardiovasc Intervent Radiol. 2016; 39: 855-864
        • Staal F.C.R.
        • Aalbersberg E.A.
        • van der Velden D.
        • et al.
        GEP-NET radiomics: a systematic review and radiomics quality score assessment.
        Eur Radiol. 2022; 32: 7278-7294