Skip to main content
Top
Published in: Acta Diabetologica 10/2019

Open Access 01-10-2019 | Magnetic Resonance Imaging | Original Article

Pancreatic perfusion and its response to glucose as measured by simultaneous PET/MRI

Authors: Daniel Espes, Elin Manell, Anneli Rydén, Lina Carlbom, Jan Weis, Marianne Jensen-Waern, Leif Jansson, Olof Eriksson

Published in: Acta Diabetologica | Issue 10/2019

Login to get access

Abstract

Aims

Perfusion of the pancreas and the islets of Langerhans is sensitive to physiological stimuli and is dysregulated in metabolic disease. Pancreatic perfusion can be assessed by both positron emission tomography (PET) and magnetic resonance imaging (MRI), but the methods have not been directly compared or benchmarked against the gold-standard microsphere technique.

Methods

Pigs (n = 4) were examined by [15O]H2O PET and intravoxel incoherent motion (IVIM) MRI technique simultaneously using a hybrid PET/MRI scanner. The pancreatic perfusion was measured both at basal conditions and after intravenous (IV) administration of up to 0.5 g/kg glucose.

Results

Pancreatic perfusion increased by 35%, 157%, and 29% after IV 0.5 g/kg glucose compared to during basal conditions, as assessed by [15O]H2O PET, IVIM MRI, and microspheres, respectively. There was a correlation between pancreatic perfusion as assessed by [15O]H2O PET and IVIM MRI (r = 0.81, R2 = 0.65, p < 0.01). The absolute quantification of pancreatic perfusion (ml/min/g) by [15O]H2O PET was within a 15% error of margin of the microsphere technique.

Conclusion

Pancreatic perfusion by [15O]H2O PET was in agreement with the microsphere technique assessment. The IVIM MRI method has the potential to replace [15O]H2O PET if the pancreatic perfusion is sufficiently large, but not when absolute quantitation is required.
Literature
1.
go back to reference Lifson N, Kramlinger KG, Mayrand RR, Lender EJ (1980) Blood flow to the rabbit pancreas with special reference to the islets of Langerhans. Gastroenterology 79(3):466–473CrossRefPubMed Lifson N, Kramlinger KG, Mayrand RR, Lender EJ (1980) Blood flow to the rabbit pancreas with special reference to the islets of Langerhans. Gastroenterology 79(3):466–473CrossRefPubMed
2.
go back to reference Jansson L, Barbu A, Bodin B, Drott CJ, Espes D, Gao X, Grapensparr L, Källskog Ö, Lau J, Liljebäck H, Palm F, Quach M, Sandberg M, Strömberg V, Ullsten S, Carlsson PO (2016) Pancreatic islet blood flow and its measurement. Ups J Med Sci 121(2):81–95CrossRefPubMedPubMedCentral Jansson L, Barbu A, Bodin B, Drott CJ, Espes D, Gao X, Grapensparr L, Källskog Ö, Lau J, Liljebäck H, Palm F, Quach M, Sandberg M, Strömberg V, Ullsten S, Carlsson PO (2016) Pancreatic islet blood flow and its measurement. Ups J Med Sci 121(2):81–95CrossRefPubMedPubMedCentral
3.
go back to reference Jansson L, Hellerström C (1983) Stimulation by glucose of the blood flow to the pancreatic islets of the rat. Diabetologia 25(1):45–50CrossRefPubMed Jansson L, Hellerström C (1983) Stimulation by glucose of the blood flow to the pancreatic islets of the rat. Diabetologia 25(1):45–50CrossRefPubMed
4.
go back to reference Nyman LR, Ford E, Powers AC, Piston DW (2010) Glucose-dependent blood flow dynamics in murine pancreatic islets in vivo. Am J Physiol Endocrinol Metab 298(4):E807–E814CrossRefPubMedPubMedCentral Nyman LR, Ford E, Powers AC, Piston DW (2010) Glucose-dependent blood flow dynamics in murine pancreatic islets in vivo. Am J Physiol Endocrinol Metab 298(4):E807–E814CrossRefPubMedPubMedCentral
5.
go back to reference Jansson L, Andersson A, Bodin B, Kallskog O (2007) Pancreatic islet blood flow during euglycaemic, hyperinsulinaemic clamp in anaesthetized rats. Acta Physiol 189:319–324CrossRef Jansson L, Andersson A, Bodin B, Kallskog O (2007) Pancreatic islet blood flow during euglycaemic, hyperinsulinaemic clamp in anaesthetized rats. Acta Physiol 189:319–324CrossRef
6.
go back to reference Carlbom L, Espes D, Lubberink M, Eriksson O, Johansson L, Jansson L, Korsgren O, Ahlström H, Carlsson PO (2016) Pancreatic perfusion and subsequent response to glucose in healthy individuals and patients with type 1 diabetes. Diabetologia 59:1968–1972CrossRefPubMed Carlbom L, Espes D, Lubberink M, Eriksson O, Johansson L, Jansson L, Korsgren O, Ahlström H, Carlsson PO (2016) Pancreatic perfusion and subsequent response to glucose in healthy individuals and patients with type 1 diabetes. Diabetologia 59:1968–1972CrossRefPubMed
7.
go back to reference Eriksson O, Espes D, Selvaraju RK, Jansson E, Antoni G, Sörensen J, Lubberink M, Biglarnia A, Eriksson JW, Sundin A, Ahlström H, Eriksson B, Johansson L, Carlsson PO, Korsgren O (2014) The positron emission tomography ligand [11C]5-hydroxy-tryptophan can be used as a surrogate marker for the human endocrine pancreas. Diabetes 63:3428–3437CrossRefPubMed Eriksson O, Espes D, Selvaraju RK, Jansson E, Antoni G, Sörensen J, Lubberink M, Biglarnia A, Eriksson JW, Sundin A, Ahlström H, Eriksson B, Johansson L, Carlsson PO, Korsgren O (2014) The positron emission tomography ligand [11C]5-hydroxy-tryptophan can be used as a surrogate marker for the human endocrine pancreas. Diabetes 63:3428–3437CrossRefPubMed
8.
go back to reference Koffert J, Honka H, Teuho J, Kauhanen S, Hurme S, Parkkola R, Oikonen V, Mari A, Lindqvist A, Wierup N, Groop L, Nuutila P (2017) Effects of meal and incretins in the regulation of splanchnic blood flow. Endocr Connect 6(3):179–187CrossRefPubMedPubMedCentral Koffert J, Honka H, Teuho J, Kauhanen S, Hurme S, Parkkola R, Oikonen V, Mari A, Lindqvist A, Wierup N, Groop L, Nuutila P (2017) Effects of meal and incretins in the regulation of splanchnic blood flow. Endocr Connect 6(3):179–187CrossRefPubMedPubMedCentral
9.
go back to reference Honka H, Hannukainen JC, Tarkia M, Karlsson H, Saunavaara V, Salminen P, Soinio M, Mikkola K, Kudomi N, Oikonen V, Haaparanta-Solin M, Roivainen A, Parkkola R, Iozzo P, Nuutila P (2014) Pancreatic metabolism, blood flow, and β-cell function in obese humans. J Clin Endocrinol Metab 99(6):E981–E990CrossRefPubMed Honka H, Hannukainen JC, Tarkia M, Karlsson H, Saunavaara V, Salminen P, Soinio M, Mikkola K, Kudomi N, Oikonen V, Haaparanta-Solin M, Roivainen A, Parkkola R, Iozzo P, Nuutila P (2014) Pancreatic metabolism, blood flow, and β-cell function in obese humans. J Clin Endocrinol Metab 99(6):E981–E990CrossRefPubMed
10.
go back to reference Carlbom L, Espes D, Lubberink M, Martinell M, Johansson L, Ahlström H, Carlsson PO, Korsgren O, Eriksson O (2017) [11C]5-Hydroxy-tryptophan PET for assessment of islet mass during progression of type 2 diabetes. Diabetes 66(5):1286–1292CrossRefPubMed Carlbom L, Espes D, Lubberink M, Martinell M, Johansson L, Ahlström H, Carlsson PO, Korsgren O, Eriksson O (2017) [11C]5-Hydroxy-tryptophan PET for assessment of islet mass during progression of type 2 diabetes. Diabetes 66(5):1286–1292CrossRefPubMed
11.
go back to reference Honka H, Koffert J, Kauhanen S, Teuho J, Hurme S, Mari A, Lindqvist A, Wierup N, Groop L, Nuutila P (2017) Bariatric surgery enhances splanchnic vascular responses in patients with type 2 diabetes. Diabetes 66(4):880–885CrossRefPubMed Honka H, Koffert J, Kauhanen S, Teuho J, Hurme S, Mari A, Lindqvist A, Wierup N, Groop L, Nuutila P (2017) Bariatric surgery enhances splanchnic vascular responses in patients with type 2 diabetes. Diabetes 66(4):880–885CrossRefPubMed
12.
go back to reference Eriksson O, Johnström P, Cselenyi Z, Jahan M, Selvaraju RK, Jensen-Waern M, Sörhede-Winzell M, Halldin C, Skrtic S, Korsgren O (2018) In vivo visualization of beta cells by targeting of GPR44. Diabetes 67(2):182–192CrossRefPubMed Eriksson O, Johnström P, Cselenyi Z, Jahan M, Selvaraju RK, Jensen-Waern M, Sörhede-Winzell M, Halldin C, Skrtic S, Korsgren O (2018) In vivo visualization of beta cells by targeting of GPR44. Diabetes 67(2):182–192CrossRefPubMed
13.
go back to reference Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505CrossRefPubMed Le Bihan D, Breton E, Lallemand D, Aubin ML, Vignaud J, Laval-Jeantet M (1988) Separation of diffusion and perfusion in intravoxel incoherent motion MR imaging. Radiology 168:497–505CrossRefPubMed
14.
go back to reference Yipintsoi T, Dobbs WA, Scanlon PD, Knopp TJ, Bassingthwaighte JB (1973) Regional distribution of diffusible tracers and carbonized microspheres in the left ventricle of isolated dog hearts. Circ Res 33:573–587CrossRefPubMedPubMedCentral Yipintsoi T, Dobbs WA, Scanlon PD, Knopp TJ, Bassingthwaighte JB (1973) Regional distribution of diffusible tracers and carbonized microspheres in the left ventricle of isolated dog hearts. Circ Res 33:573–587CrossRefPubMedPubMedCentral
15.
go back to reference Bol A, Melin JA, Vanoverschelde JL, Baudhuin T, Vogelaers D, De Pauw M, Michel C, Luxen A, Labar D, Cogneau M (1993) Direct comparison of [13N]ammonia and [15O]water estimates of perfusion with quantification of regional myocardial blood flow by microspheres. Circulation 87:512–525CrossRefPubMed Bol A, Melin JA, Vanoverschelde JL, Baudhuin T, Vogelaers D, De Pauw M, Michel C, Luxen A, Labar D, Cogneau M (1993) Direct comparison of [13N]ammonia and [15O]water estimates of perfusion with quantification of regional myocardial blood flow by microspheres. Circulation 87:512–525CrossRefPubMed
17.
go back to reference Esposito A, Palmisano A, Maffi P, Malosio ML, Nano R, Canu T, De Cobelli F, Piemonti L, Ironi G, Secchi A, Del Maschio A (2014) Liver perfusion changes occurring during pancreatic islet engraftment: a dynamic contrast-enhanced magnetic resonance study. Am J Transplant 14(1):202–209. https://doi.org/10.1111/ajt.12501 (Epub 2013 Nov 12) CrossRefPubMed Esposito A, Palmisano A, Maffi P, Malosio ML, Nano R, Canu T, De Cobelli F, Piemonti L, Ironi G, Secchi A, Del Maschio A (2014) Liver perfusion changes occurring during pancreatic islet engraftment: a dynamic contrast-enhanced magnetic resonance study. Am J Transplant 14(1):202–209. https://​doi.​org/​10.​1111/​ajt.​12501 (Epub 2013 Nov 12) CrossRefPubMed
18.
go back to reference Nalin L, Selvaraju RK, Velikyan I, Berglund M, Andréasson S, Wikstrand A, Rydén A, Lubberink M, Kandeel F, Nyman G, Korsgren O, Eriksson O, Jensen-Waern M (2014) Positron emission tomography imaging of the glucagon like peptide-1 receptor in healthy and streptozotocin-induced diabetic pigs. Eur J Nucl Med Mol Imaging 41:1800–1810CrossRefPubMed Nalin L, Selvaraju RK, Velikyan I, Berglund M, Andréasson S, Wikstrand A, Rydén A, Lubberink M, Kandeel F, Nyman G, Korsgren O, Eriksson O, Jensen-Waern M (2014) Positron emission tomography imaging of the glucagon like peptide-1 receptor in healthy and streptozotocin-induced diabetic pigs. Eur J Nucl Med Mol Imaging 41:1800–1810CrossRefPubMed
19.
go back to reference Schindler TH (2015) Positron-emitting myocardial blood flow tracers and clinical potential. Prog Cardiovasc Dis 57(6):588–606CrossRefPubMed Schindler TH (2015) Positron-emitting myocardial blood flow tracers and clinical potential. Prog Cardiovasc Dis 57(6):588–606CrossRefPubMed
20.
go back to reference Murthy VL, Naya M, Foster CR, Hainer J, Gaber M, Di Carli G, Blankstein R, Dorbala S, Sitek A, Pencina MJ, Di Carli MF (2011) Improved cardiac risk assessment with noninvasive measures of coronary flow reserve. Circulation 124(20):2215–2224CrossRefPubMedPubMedCentral Murthy VL, Naya M, Foster CR, Hainer J, Gaber M, Di Carli G, Blankstein R, Dorbala S, Sitek A, Pencina MJ, Di Carli MF (2011) Improved cardiac risk assessment with noninvasive measures of coronary flow reserve. Circulation 124(20):2215–2224CrossRefPubMedPubMedCentral
Metadata
Title
Pancreatic perfusion and its response to glucose as measured by simultaneous PET/MRI
Authors
Daniel Espes
Elin Manell
Anneli Rydén
Lina Carlbom
Jan Weis
Marianne Jensen-Waern
Leif Jansson
Olof Eriksson
Publication date
01-10-2019
Publisher
Springer Milan
Published in
Acta Diabetologica / Issue 10/2019
Print ISSN: 0940-5429
Electronic ISSN: 1432-5233
DOI
https://doi.org/10.1007/s00592-019-01353-2

Other articles of this Issue 10/2019

Acta Diabetologica 10/2019 Go to the issue