The impact of Roux-en-Y gastric bypass surgery on normal metabolism in a porcine model

Andreas Lindqvist; Mikael Ekelund; Eliana Garcia-Vaz; Marcus Ståhlman; Stefan Pierzynowski; Maria F Gomez; Jens F Rehfeld; Leif Groop; Jan Hedenbro; Nils Wierup; Peter Spégel

doi:10.1371/journal.pone.0173137

The impact of Roux-en-Y gastric bypass surgery on normal metabolism in a porcine model

Andreas Lindqvist, Mikael Ekelund, Eliana Garcia-Vaz, Marcus Ståhlman, Stefan Pierzynowski, Maria F Gomez, Jens F Rehfeld, Leif Groop, Jan Hedenbro, Nils Wierup, Peter Spégel

Department of Clinical Medicine

8 Citations (Scopus)

53 Downloads (Pure)

Abstract

BACKGROUND: A growing body of literature on Roux-en-Y gastric bypass surgery (RYGB) has generated inconclusive results on the mechanism underlying the beneficial effects on weight loss and glycaemia, partially due to the problems of designing clinical studies with the appropriate controls. Moreover, RYGB is only performed in obese individuals, in whom metabolism is perturbed and not completely understood.

METHODS: In an attempt to isolate the effects of RYGB and its effects on normal metabolism, we investigated the effect of RYGB in lean pigs, using sham-operated pair-fed pigs as controls. Two weeks post-surgery, pigs were subjected to an intravenous glucose tolerance test (IVGTT) and circulating metabolites, hormones and lipids measured. Bile acid composition was profiled after extraction from blood, faeces and the gallbladder.

RESULTS: A similar weight development in both groups of pigs validated our experimental model. Despite similar changes in fasting insulin, RYGB-pigs had lower fasting glucose levels. During an IVGTT RYGB-pigs had higher insulin and lower glucose levels. VLDL and IDL were lower in RYGB- than in sham-pigs. RYGB-pigs had increased levels of most amino acids, including branched-chain amino acids, but these were more efficiently suppressed by glucose. Levels of bile acids in the gallbladder were higher, whereas plasma and faecal bile acid levels were lower in RYGB- than in sham-pigs.

CONCLUSION: In a lean model RYGB caused lower plasma lipid and bile acid levels, which were compensated for by increased plasma amino acids, suggesting a switch from lipid to protein metabolism during fasting in the immediate postoperative period.

Original language	English
Article number	e0173137
Journal	PLOS ONE
Volume	12
Issue number	3
Number of pages	15
ISSN	1932-6203
DOIs	https://doi.org/10.1371/journal.pone.0173137
Publication status	Published - Mar 2017

Keywords

Animals
Blood Glucose
Disease Models, Animal
Fasting/blood
Gastric Bypass/adverse effects
Glucose/metabolism
Glucose Tolerance Test
Humans
Insulin/metabolism
Insulin Resistance/physiology
Obesity/blood
Swine
Weight Loss/physiology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1371/journal.pone.0173137Licence: CC BY

The impact of Roux-en-Y gastric bypass surgery on normal metabolism in a porcine modelFinal published version, 2.08 MBLicence: CC BY

Cite this

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title = "The impact of Roux-en-Y gastric bypass surgery on normal metabolism in a porcine model",

abstract = "BACKGROUND: A growing body of literature on Roux-en-Y gastric bypass surgery (RYGB) has generated inconclusive results on the mechanism underlying the beneficial effects on weight loss and glycaemia, partially due to the problems of designing clinical studies with the appropriate controls. Moreover, RYGB is only performed in obese individuals, in whom metabolism is perturbed and not completely understood.METHODS: In an attempt to isolate the effects of RYGB and its effects on normal metabolism, we investigated the effect of RYGB in lean pigs, using sham-operated pair-fed pigs as controls. Two weeks post-surgery, pigs were subjected to an intravenous glucose tolerance test (IVGTT) and circulating metabolites, hormones and lipids measured. Bile acid composition was profiled after extraction from blood, faeces and the gallbladder.RESULTS: A similar weight development in both groups of pigs validated our experimental model. Despite similar changes in fasting insulin, RYGB-pigs had lower fasting glucose levels. During an IVGTT RYGB-pigs had higher insulin and lower glucose levels. VLDL and IDL were lower in RYGB- than in sham-pigs. RYGB-pigs had increased levels of most amino acids, including branched-chain amino acids, but these were more efficiently suppressed by glucose. Levels of bile acids in the gallbladder were higher, whereas plasma and faecal bile acid levels were lower in RYGB- than in sham-pigs.CONCLUSION: In a lean model RYGB caused lower plasma lipid and bile acid levels, which were compensated for by increased plasma amino acids, suggesting a switch from lipid to protein metabolism during fasting in the immediate postoperative period.",

keywords = "Animals, Blood Glucose, Disease Models, Animal, Fasting/blood, Gastric Bypass/adverse effects, Glucose/metabolism, Glucose Tolerance Test, Humans, Insulin/metabolism, Insulin Resistance/physiology, Obesity/blood, Swine, Weight Loss/physiology",

author = "Andreas Lindqvist and Mikael Ekelund and Eliana Garcia-Vaz and Marcus St{\aa}hlman and Stefan Pierzynowski and Gomez, {Maria F} and Rehfeld, {Jens F} and Leif Groop and Jan Hedenbro and Nils Wierup and Peter Sp{\'e}gel",

year = "2017",

month = mar,

doi = "10.1371/journal.pone.0173137",

language = "English",

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T1 - The impact of Roux-en-Y gastric bypass surgery on normal metabolism in a porcine model

AU - Lindqvist, Andreas

AU - Ekelund, Mikael

AU - Garcia-Vaz, Eliana

AU - Ståhlman, Marcus

AU - Pierzynowski, Stefan

AU - Gomez, Maria F

AU - Rehfeld, Jens F

AU - Groop, Leif

AU - Hedenbro, Jan

AU - Wierup, Nils

AU - Spégel, Peter

PY - 2017/3

Y1 - 2017/3

N2 - BACKGROUND: A growing body of literature on Roux-en-Y gastric bypass surgery (RYGB) has generated inconclusive results on the mechanism underlying the beneficial effects on weight loss and glycaemia, partially due to the problems of designing clinical studies with the appropriate controls. Moreover, RYGB is only performed in obese individuals, in whom metabolism is perturbed and not completely understood.METHODS: In an attempt to isolate the effects of RYGB and its effects on normal metabolism, we investigated the effect of RYGB in lean pigs, using sham-operated pair-fed pigs as controls. Two weeks post-surgery, pigs were subjected to an intravenous glucose tolerance test (IVGTT) and circulating metabolites, hormones and lipids measured. Bile acid composition was profiled after extraction from blood, faeces and the gallbladder.RESULTS: A similar weight development in both groups of pigs validated our experimental model. Despite similar changes in fasting insulin, RYGB-pigs had lower fasting glucose levels. During an IVGTT RYGB-pigs had higher insulin and lower glucose levels. VLDL and IDL were lower in RYGB- than in sham-pigs. RYGB-pigs had increased levels of most amino acids, including branched-chain amino acids, but these were more efficiently suppressed by glucose. Levels of bile acids in the gallbladder were higher, whereas plasma and faecal bile acid levels were lower in RYGB- than in sham-pigs.CONCLUSION: In a lean model RYGB caused lower plasma lipid and bile acid levels, which were compensated for by increased plasma amino acids, suggesting a switch from lipid to protein metabolism during fasting in the immediate postoperative period.

AB - BACKGROUND: A growing body of literature on Roux-en-Y gastric bypass surgery (RYGB) has generated inconclusive results on the mechanism underlying the beneficial effects on weight loss and glycaemia, partially due to the problems of designing clinical studies with the appropriate controls. Moreover, RYGB is only performed in obese individuals, in whom metabolism is perturbed and not completely understood.METHODS: In an attempt to isolate the effects of RYGB and its effects on normal metabolism, we investigated the effect of RYGB in lean pigs, using sham-operated pair-fed pigs as controls. Two weeks post-surgery, pigs were subjected to an intravenous glucose tolerance test (IVGTT) and circulating metabolites, hormones and lipids measured. Bile acid composition was profiled after extraction from blood, faeces and the gallbladder.RESULTS: A similar weight development in both groups of pigs validated our experimental model. Despite similar changes in fasting insulin, RYGB-pigs had lower fasting glucose levels. During an IVGTT RYGB-pigs had higher insulin and lower glucose levels. VLDL and IDL were lower in RYGB- than in sham-pigs. RYGB-pigs had increased levels of most amino acids, including branched-chain amino acids, but these were more efficiently suppressed by glucose. Levels of bile acids in the gallbladder were higher, whereas plasma and faecal bile acid levels were lower in RYGB- than in sham-pigs.CONCLUSION: In a lean model RYGB caused lower plasma lipid and bile acid levels, which were compensated for by increased plasma amino acids, suggesting a switch from lipid to protein metabolism during fasting in the immediate postoperative period.

KW - Animals

KW - Blood Glucose

KW - Disease Models, Animal

KW - Fasting/blood

KW - Gastric Bypass/adverse effects

KW - Glucose/metabolism

KW - Glucose Tolerance Test

KW - Humans

KW - Insulin/metabolism

KW - Insulin Resistance/physiology

KW - Obesity/blood

KW - Swine

KW - Weight Loss/physiology

U2 - 10.1371/journal.pone.0173137

DO - 10.1371/journal.pone.0173137

M3 - Journal article

C2 - 28257455

SN - 1932-6203

VL - 12

JO - PLoS Computational Biology

JF - PLoS Computational Biology

IS - 3

M1 - e0173137

ER -

The impact of Roux-en-Y gastric bypass surgery on normal metabolism in a porcine model

Abstract

Keywords

UN SDGs

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