Skip to main content
Top
Published in: Obesity Surgery 10/2008

01-10-2008 | Research Article

Lipid Mobilization Following Roux-en-Y Gastric Bypass Examined by Magnetic Resonance Imaging and Spectroscopy

Authors: L. Johansson, M. Roos, J. Kullberg, J. Weis, H. Ahlström, M. Sundbom, B. Edén Engström, F. A. Karlsson

Published in: Obesity Surgery | Issue 10/2008

Login to get access

Abstract

Background

Recent developments of magnetic resonance imaging (MRI) and spectroscopy have made it possible to quantify lipid deposited in different tissues. To what extent an improvement of glucose tolerance shortly after Roux-en-Y gastric bypass surgery (RYGBP) is reflected in lipid levels in liver and skeletal muscle, markers of insulin resistance, has not been clarified.

Methods

Whole-body MRI and MR spectroscopy (MRS) of liver and muscle and measurements of biochemical markers of glucose and lipid metabolism were performed at baseline and 1, 6, and 12 months following surgery in seven morbidly obese women. Volumes of adipose tissue depots and liver and muscle lipids were assessed from the MRI/MRS data.

Results

At 1 month postoperatively, body mass index and visceral and subcutaneous adipose tissues were reduced by 9%, 26%, and 10%, respectively, whereas no reductions in intrahepatocellular or skeletal intramyocellular lipid concentrations were found. Free fatty acid and beta-hydroxybutyrate levels were elevated two- and sixfold, respectively; glucose and insulin levels were lowered, indicating increased insulin sensitivity. Further weight loss up to 1 year was associated with reductions in all investigated lipid depots investigated, with the exception of the intramyocellular compartment.

Conclusion

RYGBP causes rapid lipid mobilization from visceral and subcutaneous adipose depots and enhanced free fatty acid flux to the liver. An exceptional disconnection between liver fat and insulin sensitivity occurs in the early dynamic phase after surgery. However, in the late phase, the energy restriction imposed by the surgical procedure also reduces the liver lipids, but not the intramyocellular lipids.
Literature
1.
go back to reference Sjöström L, Lindroos AK, Peltonen M, et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med. 2004;351:2683–93.PubMedCrossRef Sjöström L, Lindroos AK, Peltonen M, et al. Lifestyle, diabetes, and cardiovascular risk factors 10 years after bariatric surgery. N Engl J Med. 2004;351:2683–93.PubMedCrossRef
2.
go back to reference Wickremesekera K, Miller G, Naotunne TD, et al. Loss of insulin resistance after Roux-en-Y gastric bypass surgery: a time course study. Obes Surg. 2005;15:474–81.PubMedCrossRef Wickremesekera K, Miller G, Naotunne TD, et al. Loss of insulin resistance after Roux-en-Y gastric bypass surgery: a time course study. Obes Surg. 2005;15:474–81.PubMedCrossRef
3.
go back to reference Mari A, Manco M, Guidone C, et al. Restoration of normal glucose tolerance in severely obese patients after bilio-pancreatic diversion: role of insulin sensitivity and beta cell function. Diabetologia. 2006;49:2136–43.PubMedCrossRef Mari A, Manco M, Guidone C, et al. Restoration of normal glucose tolerance in severely obese patients after bilio-pancreatic diversion: role of insulin sensitivity and beta cell function. Diabetologia. 2006;49:2136–43.PubMedCrossRef
4.
go back to reference Guidone C, Manco M, Valera-Mora E, et al. Mechanisms of recovery from type 2 diabetes after malabsorptive bariatric surgery. Diabetes. 2006;55:2025–31.PubMedCrossRef Guidone C, Manco M, Valera-Mora E, et al. Mechanisms of recovery from type 2 diabetes after malabsorptive bariatric surgery. Diabetes. 2006;55:2025–31.PubMedCrossRef
5.
go back to reference Rubino F, Forgione A, Cummings DE, et al. The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes. Ann Surg. 2006;244:741–9.PubMedCrossRef Rubino F, Forgione A, Cummings DE, et al. The mechanism of diabetes control after gastrointestinal bypass surgery reveals a role of the proximal small intestine in the pathophysiology of type 2 diabetes. Ann Surg. 2006;244:741–9.PubMedCrossRef
6.
go back to reference Arner P. Human fat cell lipolysis: biochemistry, regulation and clinical role. Best Pract Res Clin Endocrinol Metab. 2005;19:471–82.PubMedCrossRef Arner P. Human fat cell lipolysis: biochemistry, regulation and clinical role. Best Pract Res Clin Endocrinol Metab. 2005;19:471–82.PubMedCrossRef
7.
go back to reference McGarry JD. Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes. 2002;51:7–18.PubMedCrossRef McGarry JD. Banting lecture 2001: dysregulation of fatty acid metabolism in the etiology of type 2 diabetes. Diabetes. 2002;51:7–18.PubMedCrossRef
8.
go back to reference Nielsen S, Guo Z, Johnson CM, et al. Splanchnic lipolysis in human obesity. J Clin Invest. 2004;113:1582–8.PubMed Nielsen S, Guo Z, Johnson CM, et al. Splanchnic lipolysis in human obesity. J Clin Invest. 2004;113:1582–8.PubMed
9.
go back to reference Yki-Järvinen H, Westerbacka J. The fatty liver and insulin resistance. Curr Mol Med. 2005;5:287–95.PubMedCrossRef Yki-Järvinen H, Westerbacka J. The fatty liver and insulin resistance. Curr Mol Med. 2005;5:287–95.PubMedCrossRef
10.
go back to reference Kelley DE, Goodpaster BH, Storlien L. Muscle triglyceride and insulin resistance. Annu Rev Nutr. 2002;22:325–46.PubMedCrossRef Kelley DE, Goodpaster BH, Storlien L. Muscle triglyceride and insulin resistance. Annu Rev Nutr. 2002;22:325–46.PubMedCrossRef
11.
go back to reference Sinha R, Dufour S, Petersen KF, et al. Assessment of skeletal muscle triglyceride content by (1)H nuclear magnetic resonance spectroscopy in lean and obese adolescents: relationships to insulin sensitivity, total body fat, and central adiposity. Diabetes. 2002;51:1022–7.PubMedCrossRef Sinha R, Dufour S, Petersen KF, et al. Assessment of skeletal muscle triglyceride content by (1)H nuclear magnetic resonance spectroscopy in lean and obese adolescents: relationships to insulin sensitivity, total body fat, and central adiposity. Diabetes. 2002;51:1022–7.PubMedCrossRef
12.
go back to reference Kelley DE, McKolanis TM, Hegazi RA, et al. Fatty liver in type 2 diabetes mellitus: relation to regional adiposity, fatty acids, and insulin resistance. Am J Physiol Endocrinol Metab. 2003;285:E906–16.PubMed Kelley DE, McKolanis TM, Hegazi RA, et al. Fatty liver in type 2 diabetes mellitus: relation to regional adiposity, fatty acids, and insulin resistance. Am J Physiol Endocrinol Metab. 2003;285:E906–16.PubMed
13.
go back to reference Sundbom M, Gustavsson S. Randomized clinical trial of hand-assisted laparoscopic versus open Roux-en-Y gastric bypass for the treatment of morbid obesity. Br J Surg. 2004;91:418–23.PubMedCrossRef Sundbom M, Gustavsson S. Randomized clinical trial of hand-assisted laparoscopic versus open Roux-en-Y gastric bypass for the treatment of morbid obesity. Br J Surg. 2004;91:418–23.PubMedCrossRef
14.
go back to reference Wildenhoff KE. A micro-method for the enzymatic determination of acetoacetate and 3-hydroxybutyrate in blood and urine. Scand J Clin Lab Invest. 1970;25:171–9.PubMedCrossRef Wildenhoff KE. A micro-method for the enzymatic determination of acetoacetate and 3-hydroxybutyrate in blood and urine. Scand J Clin Lab Invest. 1970;25:171–9.PubMedCrossRef
15.
go back to reference Holdstock C, Edén Engström B, Öhrvall M, et al. Ghrelin and adipose tissue regulatory peptides: effect of gastric bypass surgery in obese humans. J Clin Endocrinol Metab. 2003;88:3177–83.PubMedCrossRef Holdstock C, Edén Engström B, Öhrvall M, et al. Ghrelin and adipose tissue regulatory peptides: effect of gastric bypass surgery in obese humans. J Clin Endocrinol Metab. 2003;88:3177–83.PubMedCrossRef
16.
go back to reference Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–9.PubMedCrossRef Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28:412–9.PubMedCrossRef
17.
go back to reference Kullberg J, Angelhed JE, Lönn L, et al. Whole-body T1 mapping improves the definition of adipose tissue: consequences for automated image analysis. J Magn Reson Imaging. 2006;24:394–401.PubMedCrossRef Kullberg J, Angelhed JE, Lönn L, et al. Whole-body T1 mapping improves the definition of adipose tissue: consequences for automated image analysis. J Magn Reson Imaging. 2006;24:394–401.PubMedCrossRef
18.
go back to reference Naressi A, Couturier C, Devos JM, et al. Java-based graphical user interface for the MRUI quantitation package. MAGMA. 2001;12:141–52.PubMedCrossRef Naressi A, Couturier C, Devos JM, et al. Java-based graphical user interface for the MRUI quantitation package. MAGMA. 2001;12:141–52.PubMedCrossRef
19.
go back to reference Weis J, Johansson L, Courivaud F, et al. Quantification of intramyocellular lipids in obese subjects using spectroscopic imaging with high spatial resolution. Magn Reson Med. 2007;57:22–8.PubMedCrossRef Weis J, Johansson L, Courivaud F, et al. Quantification of intramyocellular lipids in obese subjects using spectroscopic imaging with high spatial resolution. Magn Reson Med. 2007;57:22–8.PubMedCrossRef
20.
go back to reference Lind L, Berne C, Lithell H. Prevalence of insulin resistance in essential hypertension. J Hypertens. 1995;13:1457–62.PubMed Lind L, Berne C, Lithell H. Prevalence of insulin resistance in essential hypertension. J Hypertens. 1995;13:1457–62.PubMed
21.
go back to reference Westerbacka J, Lammi K, Häkkinen AM, et al. Dietary fat content modifies liver fat in overweight nondiabetic subjects. J Clin Endocrinol Metab. 2005;90:2804–9.PubMedCrossRef Westerbacka J, Lammi K, Häkkinen AM, et al. Dietary fat content modifies liver fat in overweight nondiabetic subjects. J Clin Endocrinol Metab. 2005;90:2804–9.PubMedCrossRef
22.
go back to reference Westerbacka J, Cornér A, Tiikkainen M, et al. Women and men have similar amounts of liver and intra-abdominal fat, despite more subcutaneous fat in women: implications for sex differences in markers of cardiovascular risk. Diabetologia. 2004;47:1360–9.PubMedCrossRef Westerbacka J, Cornér A, Tiikkainen M, et al. Women and men have similar amounts of liver and intra-abdominal fat, despite more subcutaneous fat in women: implications for sex differences in markers of cardiovascular risk. Diabetologia. 2004;47:1360–9.PubMedCrossRef
24.
go back to reference Sato F, Tamura Y, Watada H, et al. Effects of diet-induced moderate weight reduction on intrahepatic and intramyocellular triglycerides and glucose metabolism in obese subjects. J Clin Endocrinol Metab. 2007;92:3326–9.PubMedCrossRef Sato F, Tamura Y, Watada H, et al. Effects of diet-induced moderate weight reduction on intrahepatic and intramyocellular triglycerides and glucose metabolism in obese subjects. J Clin Endocrinol Metab. 2007;92:3326–9.PubMedCrossRef
25.
go back to reference Larson-Meyer DE, Heilbronn LK, Redman LM, et al. Effect of calorie restriction with or without exercise on insulin sensitivity, β-cell function, fat cell size, and ectopic lipid in overweight subjects. Diabetes Care. 2006;29:1337–44.PubMedCrossRef Larson-Meyer DE, Heilbronn LK, Redman LM, et al. Effect of calorie restriction with or without exercise on insulin sensitivity, β-cell function, fat cell size, and ectopic lipid in overweight subjects. Diabetes Care. 2006;29:1337–44.PubMedCrossRef
26.
go back to reference Tiikkainen M, Bergholm R, Vehkavaara S, et al. Effects of identical weight loss on body composition and features of insulin resistance in obese women with high and low liver fat content. Diabetes. 2003;52:701–7.PubMedCrossRef Tiikkainen M, Bergholm R, Vehkavaara S, et al. Effects of identical weight loss on body composition and features of insulin resistance in obese women with high and low liver fat content. Diabetes. 2003;52:701–7.PubMedCrossRef
27.
go back to reference Petersen KF, Dufour S, Befroy D, et al. Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes. 2005;54:603–8.PubMedCrossRef Petersen KF, Dufour S, Befroy D, et al. Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes. 2005;54:603–8.PubMedCrossRef
28.
go back to reference Alami RS, Morton JM, Schuster R, et al. Is there a benefit to preoperative weight loss in gastric bypass patients? A prospective randomized trial. Surg Obes Relat Dis. 2007;3:141–5.PubMedCrossRef Alami RS, Morton JM, Schuster R, et al. Is there a benefit to preoperative weight loss in gastric bypass patients? A prospective randomized trial. Surg Obes Relat Dis. 2007;3:141–5.PubMedCrossRef
29.
go back to reference Alvarado R, Alami RS, Hsu G, et al. The impact of preoperative weight loss in patients undergoing laparoscopic Roux-en-Y gastric bypass. Obes Surg. 2005;15:1282–6.PubMedCrossRef Alvarado R, Alami RS, Hsu G, et al. The impact of preoperative weight loss in patients undergoing laparoscopic Roux-en-Y gastric bypass. Obes Surg. 2005;15:1282–6.PubMedCrossRef
30.
go back to reference Liu RC, Sabnis AA, Forsyth C, et al. The effects of acute preoperative weight loss on laparoscopic Roux-en-Y gastric bypass. Obes Surg. 2005;15:1396–402.PubMedCrossRef Liu RC, Sabnis AA, Forsyth C, et al. The effects of acute preoperative weight loss on laparoscopic Roux-en-Y gastric bypass. Obes Surg. 2005;15:1396–402.PubMedCrossRef
31.
32.
go back to reference Lewis MC, Phillips ML, Slavotinek JP, et al. Change in liver size and fat content after treatment with Optifast very low calorie diet. Obes Surg. 2006;16:697–701.PubMedCrossRef Lewis MC, Phillips ML, Slavotinek JP, et al. Change in liver size and fat content after treatment with Optifast very low calorie diet. Obes Surg. 2006;16:697–701.PubMedCrossRef
33.
go back to reference Colles SL, Dixon JB, Marks P, et al. Preoperative weight loss with a very-low-energy diet: quantitation of changes in liver and abdominal fat by serial imaging. Am J Clin Nutr. 2006;84:304–11.PubMed Colles SL, Dixon JB, Marks P, et al. Preoperative weight loss with a very-low-energy diet: quantitation of changes in liver and abdominal fat by serial imaging. Am J Clin Nutr. 2006;84:304–11.PubMed
34.
go back to reference Busetto L, Tregnaghi A, De Marchi F, et al. Liver volume and visceral obesity in women with hepatic steatosis undergoing gastric banding. Obes Res. 2002;10:408–11.PubMedCrossRef Busetto L, Tregnaghi A, De Marchi F, et al. Liver volume and visceral obesity in women with hepatic steatosis undergoing gastric banding. Obes Res. 2002;10:408–11.PubMedCrossRef
35.
go back to reference Krssak M, Falk Petersen K, Dresner A, et al. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia. 1999;42:113–6.PubMedCrossRef Krssak M, Falk Petersen K, Dresner A, et al. Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia. 1999;42:113–6.PubMedCrossRef
36.
go back to reference Stannard SR, Thompson MW, Fairbairn K, et al. Fasting for 72 h increases intramyocellular lipid content in nondiabetic, physically fit men. Am J Physiol Endocrinol Metab. 2002;283:E1185–91.PubMed Stannard SR, Thompson MW, Fairbairn K, et al. Fasting for 72 h increases intramyocellular lipid content in nondiabetic, physically fit men. Am J Physiol Endocrinol Metab. 2002;283:E1185–91.PubMed
37.
go back to reference Johnson NA, Stannard SR, Rowlands DS, et al. Short-term suppression of plasma free fatty acids fails to improve insulin sensitivity when intramyocellular lipid is elevated. Diabet Med. 2006;23:1061–8.PubMedCrossRef Johnson NA, Stannard SR, Rowlands DS, et al. Short-term suppression of plasma free fatty acids fails to improve insulin sensitivity when intramyocellular lipid is elevated. Diabet Med. 2006;23:1061–8.PubMedCrossRef
38.
go back to reference Greco AV, Mingrone G, Giancaterini A, et al. Insulin resistance in morbid obesity: reversal with intramyocellular fat depletion. Diabetes. 2002;51:144–51.PubMedCrossRef Greco AV, Mingrone G, Giancaterini A, et al. Insulin resistance in morbid obesity: reversal with intramyocellular fat depletion. Diabetes. 2002;51:144–51.PubMedCrossRef
39.
go back to reference Borg CM, le Roux CW, Ghatei MA, et al. Progressive rise in gut hormone levels after Roux-en-Y gastric bypass suggests gut adaptation and explains altered satiety. Br J Surg. 2006;93:210–5.PubMedCrossRef Borg CM, le Roux CW, Ghatei MA, et al. Progressive rise in gut hormone levels after Roux-en-Y gastric bypass suggests gut adaptation and explains altered satiety. Br J Surg. 2006;93:210–5.PubMedCrossRef
40.
go back to reference Morinigo R, Moize V, Musri M, et al. Glucagon-like peptide-1, peptide YY, hunger, and satiety after gastric bypass surgery in morbidly obese subjects. J Clin Endocrinol Metab. 2006;91:1735–40.PubMedCrossRef Morinigo R, Moize V, Musri M, et al. Glucagon-like peptide-1, peptide YY, hunger, and satiety after gastric bypass surgery in morbidly obese subjects. J Clin Endocrinol Metab. 2006;91:1735–40.PubMedCrossRef
Metadata
Title
Lipid Mobilization Following Roux-en-Y Gastric Bypass Examined by Magnetic Resonance Imaging and Spectroscopy
Authors
L. Johansson
M. Roos
J. Kullberg
J. Weis
H. Ahlström
M. Sundbom
B. Edén Engström
F. A. Karlsson
Publication date
01-10-2008
Publisher
Springer-Verlag
Published in
Obesity Surgery / Issue 10/2008
Print ISSN: 0960-8923
Electronic ISSN: 1708-0428
DOI
https://doi.org/10.1007/s11695-008-9484-0

Other articles of this Issue 10/2008

Obesity Surgery 10/2008 Go to the issue