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Published in: European Radiology 2/2019

01-02-2019 | Magnetic Resonance

Observed changes in brown, white, hepatic and pancreatic fat after bariatric surgery: Evaluation with MRI

Authors: Steve C. N. Hui, Simon K. H. Wong, Qiyong Ai, David K. W. Yeung, Enders K. W. Ng, Winnie C. W. Chu

Published in: European Radiology | Issue 2/2019

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Abstract

Objectives

To study the change in brown and white adipose tissue (BAT and WAT), as well as fat content in the liver and pancreas, in patients with morbid obesity before and after bariatric surgery.

Methods

Twelve patients with morbid obesity (F=8, M=4, age: 45.4 years (38.4–51.2), BMI: 35.2 kg/m2 (32.5–38.6)) underwent pre-op MRI at baseline and two post-op scans at 6-month and 12-month intervals after bariatric surgery. Co-registered water, fat, fat-fraction and T2* image series were acquired. Supraclavicular BAT and abdominal WAT were measured using in-house algorithms. Intrahepatic triglyceride (IHTG) was measured using MR spectroscopy and pancreatic fat was measured using a region-of-interest approach. Fat contents were compared between baseline and the first and second 6-month intervals using non-parametric analysis of Friedman’s test and Wilcoxon’s signed-rank test. Level of significance was selected at p=0.017 (0.05/3). Threshold of non-alcoholic fatty liver disease was set at 5.56%.

Results

Results indicated that BMI (p=0.005), IHTG (p=0.005), and subcutaneous (p=0.005) and visceral adipose tissues (p=0.005) were significantly reduced 6 months after surgery. Pancreatic fat (p=0.009) was significantly reduced at 12 months. Most reduction became stable between the 6-month and 12-month interval. No significant difference was observed in BAT volume, fat-fraction and T2* values.

Conclusion

The results of this study suggest that bariatric surgery effectively reduced weight, mainly as a result of the reduction of abdominal WAT. Liver and pancreatic fat were deceased below the threshold possibly due to the reduction of free fatty acid. BAT volume, fat-fraction and T2* showed no significant changes, probably because surgery itself might not have altered the metabolic profile of the patients.

Key Points

• No significant changes were observed in fat-fraction, T2* and volume of brown adipose tissue after bariatric surgery.
• Non-alcoholic fatty liver disease was resolved after surgery.
• Abdominal white fat and liver fat were significantly reduced 6 months after surgery and become stable between 6 and 12 months while pancreatic fat was significantly reduced between 0 and 12 months.
Literature
1.
go back to reference McFarlane SI, Banerji M, Sowers JR (2001) Insulin resistance and cardiovascular disease. J Clin Endocrinol Metab 86:713–718PubMed McFarlane SI, Banerji M, Sowers JR (2001) Insulin resistance and cardiovascular disease. J Clin Endocrinol Metab 86:713–718PubMed
3.
go back to reference Enerbäck S (2010) Brown adipose tissue in humans. Int J Obes (Lond) 34(Suppl 1):S43–S46CrossRef Enerbäck S (2010) Brown adipose tissue in humans. Int J Obes (Lond) 34(Suppl 1):S43–S46CrossRef
4.
5.
go back to reference van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM et al (2009) Cold-activated brown adipose tissue in healthy men. N Engl J Med 360:1500–1508CrossRefPubMed van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM et al (2009) Cold-activated brown adipose tissue in healthy men. N Engl J Med 360:1500–1508CrossRefPubMed
6.
go back to reference Ricquier D (2011) Uncoupling protein 1 of brown adipocytes, the only uncoupler: a historical perspective. Front Endocrinol (Lausanne) 2:85CrossRef Ricquier D (2011) Uncoupling protein 1 of brown adipocytes, the only uncoupler: a historical perspective. Front Endocrinol (Lausanne) 2:85CrossRef
7.
go back to reference Goodpaster BH, Delany JP, Otto AD et al (2010) Effects of diet and physical activity interventions on weight loss and cardiometabolic risk factors in severely obese adults: a randomized trial. JAMA 304:1795–1802CrossRefPubMedPubMedCentral Goodpaster BH, Delany JP, Otto AD et al (2010) Effects of diet and physical activity interventions on weight loss and cardiometabolic risk factors in severely obese adults: a randomized trial. JAMA 304:1795–1802CrossRefPubMedPubMedCentral
8.
go back to reference Unick JL, Beavers D, Jakicic JM et al (2011) Effectiveness of lifestyle interventions for individuals with severe obesity and type 2 diabetes: results from the Look AHEAD trial. Diabetes Care 34:2152–2157CrossRefPubMedPubMedCentral Unick JL, Beavers D, Jakicic JM et al (2011) Effectiveness of lifestyle interventions for individuals with severe obesity and type 2 diabetes: results from the Look AHEAD trial. Diabetes Care 34:2152–2157CrossRefPubMedPubMedCentral
9.
go back to reference Wadden TA, Webb VL, Moran CH, Bailer BA (2012) Lifestyle modification for obesity: new developments in diet, physical activity, and behavior therapy. Circulation 125:1157–1170CrossRefPubMedPubMedCentral Wadden TA, Webb VL, Moran CH, Bailer BA (2012) Lifestyle modification for obesity: new developments in diet, physical activity, and behavior therapy. Circulation 125:1157–1170CrossRefPubMedPubMedCentral
10.
go back to reference Karlsson J, Taft C, Rydén A, Sjöström L, Sullivan M (2007) Ten-year trends in health-related quality of life after surgical and conventional treatment for severe obesity: the SOS intervention study. Int J Obes (Lond) 31:1248–1261CrossRef Karlsson J, Taft C, Rydén A, Sjöström L, Sullivan M (2007) Ten-year trends in health-related quality of life after surgical and conventional treatment for severe obesity: the SOS intervention study. Int J Obes (Lond) 31:1248–1261CrossRef
11.
go back to reference Liu SY, Wong SK, Lam CC, Yung MY, Kong AP, Ng EK (2015) Long-term Results on Weight Loss and Diabetes Remission after Laparoscopic Sleeve Gastrectomy for A Morbidly Obese Chinese Population. Obes Surg 25:1901–1908CrossRefPubMed Liu SY, Wong SK, Lam CC, Yung MY, Kong AP, Ng EK (2015) Long-term Results on Weight Loss and Diabetes Remission after Laparoscopic Sleeve Gastrectomy for A Morbidly Obese Chinese Population. Obes Surg 25:1901–1908CrossRefPubMed
12.
go back to reference Karmali S, Schauer P, Birch D, Sharma AM, Sherman V (2010) Laparoscopic sleeve gastrectomy: an innovative new tool in the battle against the obesity epidemic in Canada. Can J Surg 53:126–132PubMedPubMedCentral Karmali S, Schauer P, Birch D, Sharma AM, Sherman V (2010) Laparoscopic sleeve gastrectomy: an innovative new tool in the battle against the obesity epidemic in Canada. Can J Surg 53:126–132PubMedPubMedCentral
13.
go back to reference Hui SCN, Ko JKL, Zhang T et al (2017) Quantification of brown and white adipose tissue based on Gaussian mixture model using water-fat and T2* MRI in adolescents. J Magn Reson Imaging 46:758–768CrossRefPubMed Hui SCN, Ko JKL, Zhang T et al (2017) Quantification of brown and white adipose tissue based on Gaussian mixture model using water-fat and T2* MRI in adolescents. J Magn Reson Imaging 46:758–768CrossRefPubMed
14.
go back to reference Hu HH, Perkins TG, Chia JM, Gilsanz V (2013) Characterization of human brown adipose tissue by chemical-shift water-fat MRI. AJR Am J Roentgenol 200:177–183CrossRefPubMedPubMedCentral Hu HH, Perkins TG, Chia JM, Gilsanz V (2013) Characterization of human brown adipose tissue by chemical-shift water-fat MRI. AJR Am J Roentgenol 200:177–183CrossRefPubMedPubMedCentral
15.
go back to reference Hu HH, Smith DL Jr, Nayak KS, Goran MI, Nagy TR (2010) Identification of brown adipose tissue in mice with fat-water IDEAL-MRI. J Magn Reson Imaging 31:1195–1202CrossRefPubMedPubMedCentral Hu HH, Smith DL Jr, Nayak KS, Goran MI, Nagy TR (2010) Identification of brown adipose tissue in mice with fat-water IDEAL-MRI. J Magn Reson Imaging 31:1195–1202CrossRefPubMedPubMedCentral
16.
go back to reference Koskensalo K, Raiko J, Saari T et al (2017) Human Brown Adipose Tissue Temperature and Fat Fraction Are Related to Its Metabolic Activity. J Clin Endocrinol Metab 102:1200–1207CrossRefPubMed Koskensalo K, Raiko J, Saari T et al (2017) Human Brown Adipose Tissue Temperature and Fat Fraction Are Related to Its Metabolic Activity. J Clin Endocrinol Metab 102:1200–1207CrossRefPubMed
17.
go back to reference Hui SCN, Zhang T, Shi L, Wang D, Ip CB, Chu WCW (2017) Automated segmentation of abdominal subcutaneous adipose tissue and visceral adipose tissue in obese adolescent in MRI. Magn Reson Imaging 45:97–104CrossRefPubMed Hui SCN, Zhang T, Shi L, Wang D, Ip CB, Chu WCW (2017) Automated segmentation of abdominal subcutaneous adipose tissue and visceral adipose tissue in obese adolescent in MRI. Magn Reson Imaging 45:97–104CrossRefPubMed
18.
go back to reference Stefan D, Cesare FD, Andrasescu A et al (2009) Quantitation of magnetic resonance spectroscopy signals: the jMRUI software package. Meas Sci Technol 20:104035–104044CrossRef Stefan D, Cesare FD, Andrasescu A et al (2009) Quantitation of magnetic resonance spectroscopy signals: the jMRUI software package. Meas Sci Technol 20:104035–104044CrossRef
19.
go back to reference van Werven JR, Hoogduin JM, Nederveen AJ et al (2009) Reproducibility of 3.0 Tesla magnetic resonance spectroscopy for measuring hepatic fat content. J Magn Reson Imaging 30:444–448CrossRefPubMed van Werven JR, Hoogduin JM, Nederveen AJ et al (2009) Reproducibility of 3.0 Tesla magnetic resonance spectroscopy for measuring hepatic fat content. J Magn Reson Imaging 30:444–448CrossRefPubMed
20.
go back to reference Szczepaniak LS, Nurenberg P, Leonard D et al (2005) Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 288:E462–E468CrossRefPubMed Szczepaniak LS, Nurenberg P, Leonard D et al (2005) Magnetic resonance spectroscopy to measure hepatic triglyceride content: prevalence of hepatic steatosis in the general population. Am J Physiol Endocrinol Metab 288:E462–E468CrossRefPubMed
21.
go back to reference Fabbrini E, Sullivan S, Klein S (2010) Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 51:679–689CrossRefPubMed Fabbrini E, Sullivan S, Klein S (2010) Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 51:679–689CrossRefPubMed
22.
go back to reference Chalasani N, Younossi Z, Lavine JE et al (2012) The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 55:2005–2023CrossRefPubMed Chalasani N, Younossi Z, Lavine JE et al (2012) The diagnosis and management of non-alcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 55:2005–2023CrossRefPubMed
23.
go back to reference European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD) & European Association for the Study of Obesity (EASO) (2016) EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. Diabetologia 59(6):1121–1140 European Association for the Study of the Liver (EASL), European Association for the Study of Diabetes (EASD) & European Association for the Study of Obesity (EASO) (2016) EASL-EASD-EASO Clinical Practice Guidelines for the management of non-alcoholic fatty liver disease. Diabetologia 59(6):1121–1140
24.
go back to reference Wong VW, Wong GL, Yeung DK et al (2014) Fatty pancreas, insulin resistance, and beta-cell function: a population study using fat-water magnetic resonance imaging. Am J Gastroenterol 109:589–597CrossRefPubMed Wong VW, Wong GL, Yeung DK et al (2014) Fatty pancreas, insulin resistance, and beta-cell function: a population study using fat-water magnetic resonance imaging. Am J Gastroenterol 109:589–597CrossRefPubMed
25.
go back to reference Cicchetti DV (1994) Guidelines, Criteria, and Rules of Thumb for Evaluating Normed and Standardized Assessment Instruments in Psychology. Psychological Assessment 6:284–290CrossRef Cicchetti DV (1994) Guidelines, Criteria, and Rules of Thumb for Evaluating Normed and Standardized Assessment Instruments in Psychology. Psychological Assessment 6:284–290CrossRef
26.
go back to reference Karamanakos SN, Vagenas K, Kalfarentzos F, Alexandrides TK (2008) Weight loss, appetite suppression, and changes in fasting and postprandial ghrelin and peptide-YY levels after Roux-en-Y gastric bypass and sleeve gastrectomy: a prospective, double blind study. Ann Surg 247:401–407CrossRefPubMed Karamanakos SN, Vagenas K, Kalfarentzos F, Alexandrides TK (2008) Weight loss, appetite suppression, and changes in fasting and postprandial ghrelin and peptide-YY levels after Roux-en-Y gastric bypass and sleeve gastrectomy: a prospective, double blind study. Ann Surg 247:401–407CrossRefPubMed
27.
go back to reference Cummings DE, Weigle DS, Frayo RS et al (2002) Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N Engl J Med 346:1623–1630CrossRefPubMed Cummings DE, Weigle DS, Frayo RS et al (2002) Plasma ghrelin levels after diet-induced weight loss or gastric bypass surgery. N Engl J Med 346:1623–1630CrossRefPubMed
28.
go back to reference Taitano AA, Markow M, Finan JE, Wheeler DE, Gonzalvo JP, Murr MM (2015) Bariatric surgery improves histological features of nonalcoholic fatty liver disease and liver fibrosis. J Gastrointest Surg 19:429–437CrossRefPubMed Taitano AA, Markow M, Finan JE, Wheeler DE, Gonzalvo JP, Murr MM (2015) Bariatric surgery improves histological features of nonalcoholic fatty liver disease and liver fibrosis. J Gastrointest Surg 19:429–437CrossRefPubMed
29.
go back to reference Bower G, Toma T, Harling L et al (2015) Bariatric Surgery and Non-Alcoholic Fatty Liver Disease: a systematic review of liver biochemistry and histology. Obes Surg 25:2280–2289CrossRefPubMed Bower G, Toma T, Harling L et al (2015) Bariatric Surgery and Non-Alcoholic Fatty Liver Disease: a systematic review of liver biochemistry and histology. Obes Surg 25:2280–2289CrossRefPubMed
30.
go back to reference Luo RB, Suzuki T, Hooker JC et al (2018) How bariatric surgery affects liver volume and fat density in NAFLD patients. Surg Endosc 32:1675–1682CrossRefPubMed Luo RB, Suzuki T, Hooker JC et al (2018) How bariatric surgery affects liver volume and fat density in NAFLD patients. Surg Endosc 32:1675–1682CrossRefPubMed
31.
go back to reference Immonen H, Hannukainen JC, Kudomi N et al (2018) Increased Liver Fatty Acid Uptake Is Partly Reversed and Liver Fat Content Normalized After Bariatric Surgery. Diabetes Care 41:368–371CrossRefPubMed Immonen H, Hannukainen JC, Kudomi N et al (2018) Increased Liver Fatty Acid Uptake Is Partly Reversed and Liver Fat Content Normalized After Bariatric Surgery. Diabetes Care 41:368–371CrossRefPubMed
32.
go back to reference Zhang J, Zhao Y, Xu C et al (2014) Association between serum free fatty acid levels and nonalcoholic fatty liver disease: a cross-sectional study. Sci Rep 4:5832CrossRefPubMedPubMedCentral Zhang J, Zhao Y, Xu C et al (2014) Association between serum free fatty acid levels and nonalcoholic fatty liver disease: a cross-sectional study. Sci Rep 4:5832CrossRefPubMedPubMedCentral
33.
go back to reference Honka H, Koffert J, Hannukainen JC et al (2015) The effects of bariatric surgery on pancreatic lipid metabolism and blood flow. J Clin Endocrinol Metab 100:2015–2023CrossRefPubMed Honka H, Koffert J, Hannukainen JC et al (2015) The effects of bariatric surgery on pancreatic lipid metabolism and blood flow. J Clin Endocrinol Metab 100:2015–2023CrossRefPubMed
34.
go back to reference Vijgen GH, Bouvy ND, Teule GJ, Brans B, Schrauwen P, van Marken Lichtenbelt WD (2011) Brown adipose tissue in morbidly obese subjects. PLoS One 6:e17247CrossRefPubMedPubMedCentral Vijgen GH, Bouvy ND, Teule GJ, Brans B, Schrauwen P, van Marken Lichtenbelt WD (2011) Brown adipose tissue in morbidly obese subjects. PLoS One 6:e17247CrossRefPubMedPubMedCentral
35.
go back to reference Vijgen GH, Bouvy ND, Teule GJ et al (2012) Increase in brown adipose tissue activity after weight loss in morbidly obese subjects. J Clin Endocrinol Metab 97:E1229–E1233CrossRefPubMed Vijgen GH, Bouvy ND, Teule GJ et al (2012) Increase in brown adipose tissue activity after weight loss in morbidly obese subjects. J Clin Endocrinol Metab 97:E1229–E1233CrossRefPubMed
37.
38.
go back to reference Martínez-Sánchez N, Moreno-Navarrete JM, Contreras C et al (2017) Thyroid hormones induce browning of white fat. J Endocrinol 232:351–362CrossRefPubMed Martínez-Sánchez N, Moreno-Navarrete JM, Contreras C et al (2017) Thyroid hormones induce browning of white fat. J Endocrinol 232:351–362CrossRefPubMed
39.
go back to reference Sampath SC, Bredella MA, Cypess AM, Torriani M (2016) Imaging of Brown Adipose Tissue: State of the Art. Radiology 280:4–19CrossRefPubMed Sampath SC, Bredella MA, Cypess AM, Torriani M (2016) Imaging of Brown Adipose Tissue: State of the Art. Radiology 280:4–19CrossRefPubMed
40.
go back to reference Bartelt A, Heeren J (2014) Adipose tissue browning and metabolic health. Nat Rev Endocrinol 10:24–36CrossRefPubMed Bartelt A, Heeren J (2014) Adipose tissue browning and metabolic health. Nat Rev Endocrinol 10:24–36CrossRefPubMed
Metadata
Title
Observed changes in brown, white, hepatic and pancreatic fat after bariatric surgery: Evaluation with MRI
Authors
Steve C. N. Hui
Simon K. H. Wong
Qiyong Ai
David K. W. Yeung
Enders K. W. Ng
Winnie C. W. Chu
Publication date
01-02-2019
Publisher
Springer Berlin Heidelberg
Published in
European Radiology / Issue 2/2019
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-018-5611-z

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