Quantification of Liver, Subcutaneous, and Visceral Adipose Tissues by MRI Before and After Bariatric Surgery

Anne Christin Meyer-Gerspach, Ralph Peterli, Michael Moor, Philipp Madörin, Andreas Schötzau, Diana Nabers, Stefan Borgwardt, Christoph Beglinger, Oliver Bieri, Bettina K Wölnerhanssen, Anne Christin Meyer-Gerspach, Ralph Peterli, Michael Moor, Philipp Madörin, Andreas Schötzau, Diana Nabers, Stefan Borgwardt, Christoph Beglinger, Oliver Bieri, Bettina K Wölnerhanssen

Abstract

Background: Morbid obesity is a worldwide epidemic and is increasingly treated by bariatric surgery. Fatty liver is a common finding; almost half of all patients with non-alcoholic steatohepatitis develop steatohepatitis. Bariatric surgery improves steatohepatitis documented by liver biopsy and single voxel magnetic resonance imaging (MRI) techniques.

Objective: To investigate changes before and after bariatric surgery using whole organ MRI quantification of liver, visceral, and subcutaneous fat.

Setting: University of Basel Hospital and St. Clara Research Ltd, Basel, Switzerland.

Methods: Sixteen morbidly obese patients were evaluated by abdominal MRI-scanning before and 3, 6, 12, and 24 months after bariatric surgery to measure percentage liver fat (%-LF), total liver volume (TLV) and visceral and subcutaneous adipose tissues (VAT and SAT). Fasting plasma samples were taken for measurement of glucose, insulin, blood lipids, and liver biomarkers. In a control group of 12 healthy lean volunteers, the liver biomarker was also measured.

Results: The reproducibility of fat quantification by use of MRI was excellent. LF decreased significantly faster than VAT and SAT (%-LF vs. VAT p < 0.001 and %-LF vs. SAT p < 0.001). At certain time points, %-LF, VAT, and SAT were associated with changes in blood lipids and insulin.

Conclusions: MRI quantification offers excellently reproducible results in measurement of liver fat and visceral and subcutaneous adipose tissues. Liver fat decreased significantly faster than visceral or subcutaneous adipose tissue. Decrease in %-LF and VAT is associated with decrease in total cholesterol, LDL, and plasma insulin.

Trial registration: ClinicalTrials.gov NCT02682173.

Keywords: Adipose tissue; Bariatric surgery; Fatty liver; Magnetic resonance imaging; Obesity.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
Time courses of percentage liver fat (%-LF), total liver volume (TLV), visceral adipose tissue (VAT), and subcutaneous adipose tissue (SAT). Time courses of %-LF, TLV, VAT, and SAT before and 3, 6, 12, and 24 months after surgery. N = 16 morbidly obese patients. %-LF percentage liver fat, TLV total liver volume, VAT visceral adipose tissue, SAT subcutaneous adipose tissue

References

    1. Kelly T, Yang W, Chen CS, Reynolds K, He J. Global burden of obesity in 2005 and projections to 2030. Int J Obes. 2008;32(9):1431–1437. doi: 10.1038/ijo.2008.102.
    1. Starley BQ, Calcagno CJ, Harrison SA. Nonalcoholic fatty liver disease and hepatocellular carcinoma: a weighty connection. Hepatology. 2010;51(5):1820–1832. doi: 10.1002/hep.23594.
    1. Katrina Loomis A et al. Body mass index and risk of non-alcoholic fatty liver disease: two electronic health record prospective studies. J Clin Endocrinol Metab. 2015:jc20153444.
    1. Wong RJ, Aguilar M, Cheung R, Perumpail RB, Harrison SA, Younossi ZM, Ahmed A. Nonalcoholic steatohepatitis is the second leading etiology of liver disease among adults awaiting liver transplantation in the United States. Gastroenterology. 2015;148(3):547–555. doi: 10.1053/j.gastro.2014.11.039.
    1. Gonzalez-Cantero J, Martin-Rodriguez JL, Gonzalez-Cantero A, Arrebola JP, Gonzalez-Calvin JL. Insulin resistance in lean and overweight non-diabetic Caucasian adults: study of its relationship with liver triglyceride content, waist circumference and BMI. PLoS One. 2018;13(2):e0192663. doi: 10.1371/journal.pone.0192663.
    1. Korenblat KM, Fabbrini E, Mohammed BS, Klein S. Liver, muscle, and adipose tissue insulin action is directly related to intrahepatic triglyceride content in obese subjects. Gastroenterology. 2008;134(5):1369–1375. doi: 10.1053/j.gastro.2008.01.075.
    1. Stefan N, Kantartzis K, Haring HU. Causes and metabolic consequences of fatty liver. Endocr Rev. 2008;29(7):939–960. doi: 10.1210/er.2008-0009.
    1. Sjostrom L, et al. Effects of bariatric surgery on mortality in Swedish obese subjects. N Engl J Med. 2007;357(8):741–752. doi: 10.1056/NEJMoa066254.
    1. Haufe S, Haas V, Utz W, Birkenfeld AL, Jeran S, Bohnke J, Mahler A, Luft FC, Schulz-Menger J, Boschmann M, Jordan J, Engeli S. Long-lasting improvements in liver fat and metabolism despite body weight regain after dietary weight loss. Diabetes Care. 2013;36(11):3786–3792. doi: 10.2337/dc13-0102.
    1. Joseph AE, et al. Comparison of liver histology with ultrasonography in assessing diffuse parenchymal liver disease. Clin Radiol. 1991;43(1):26–31. doi: 10.1016/S0009-9260(05)80350-2.
    1. Schwenzer NF, Springer F, Schraml C, Stefan N, Machann J, Schick F. Non-invasive assessment and quantification of liver steatosis by ultrasound, computed tomography and magnetic resonance. J Hepatol. 2009;51(3):433–445. doi: 10.1016/j.jhep.2009.05.023.
    1. Mehta SH, Lau B, Afdhal NH, Thomas DL. Exceeding the limits of liver histology markers. J Hepatol. 2009;50(1):36–41. doi: 10.1016/j.jhep.2008.07.039.
    1. Martinez SM, et al. Noninvasive assessment of liver fibrosis. Hepatology. 2011;53(1):325–335. doi: 10.1002/hep.24013.
    1. Rockey DC, Caldwell SH, Goodman ZD, Nelson RC, Smith AD. Liver biopsy. Hepatology. 2009;49(3):1017–1044. doi: 10.1002/hep.22742.
    1. Pooler BD et al. Monitoring fatty liver disease with MRI following bariatric surgery: a prospective, dual-center study. Radiology. 2018:181134.
    1. Wald D, Teucher B, Dinkel J, Kaaks R, Delorme S, Boeing H, Seidensaal K, Meinzer HP, Heimann T. Automatic quantification of subcutaneous and visceral adipose tissue from whole-body magnetic resonance images suitable for large cohort studies. J Magn Reson Imaging. 2012;36(6):1421–1434. doi: 10.1002/jmri.23775.
    1. Wolf I, Vetter M, Wegner I, Böttger T, Nolden M, Schöbinger M, Hastenteufel M, Kunert T, Meinzer HP. The medical imaging interaction toolkit. Med Image Anal. 2005;9(6):594–604. doi: 10.1016/j.media.2005.04.005.
    1. Yushkevich PA, Piven J, Hazlett HC, Smith RG, Ho S, Gee JC, Gerig G. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage. 2006;31(3):1116–1128. doi: 10.1016/j.neuroimage.2006.01.015.
    1. Wildman RP, et al. The obese without cardiometabolic risk factor clustering and the normal weight with cardiometabolic risk factor clustering: prevalence and correlates of 2 phenotypes among the US population (NHANES 1999-2004) Arch Intern Med. 2008;168(15):1617–1624. doi: 10.1001/archinte.168.15.1617.
    1. Otto M, Färber J, Haneder S, Michaely H, Kienle P, Hasenberg T. Postoperative changes in body composition--comparison of bioelectrical impedance analysis and magnetic resonance imaging in bariatric patients. Obes Surg. 2015;25(2):302–309. doi: 10.1007/s11695-014-1382-z.
    1. Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY, Vasan RS, Murabito JM, Meigs JB, Cupples LA, D’Agostino RB, Sr, O’Donnell CJ. Abdominal visceral and subcutaneous adipose tissue compartments: association with metabolic risk factors in the Framingham Heart Study. Circulation. 2007;116(1):39–48. doi: 10.1161/CIRCULATIONAHA.106.675355.
    1. Kaess BM, Pedley A, Massaro JM, Murabito J, Hoffmann U, Fox CS. The ratio of visceral to subcutaneous fat, a metric of body fat distribution, is a unique correlate of cardiometabolic risk. Diabetologia. 2012;55(10):2622–2630. doi: 10.1007/s00125-012-2639-5.
    1. Hedderich DM, Hasenberg T, Haneder S, Schoenberg SO, Kücükoglu Ö, Canbay A, Otto M. Effects of bariatric surgery on non-alcoholic fatty liver disease: magnetic resonance imaging is an effective, non-invasive method to evaluate changes in the liver fat fraction. Obes Surg. 2017;27(7):1755–1762. doi: 10.1007/s11695-016-2531-3.
    1. Luo RB, Suzuki T, Hooker JC, Covarrubias Y, Schlein A, Liu S, Schwimmer JB, Reeder SB, Funk LM, Greenberg JA, Campos GM, Sandler BJ, Horgan S, Sirlin CB, Jacobsen GR. How bariatric surgery affects liver volume and fat density in NAFLD patients. Surg Endosc. 2018;32(4):1675–1682. doi: 10.1007/s00464-017-5846-9.
    1. Friedrich-Rust M, et al. Performance of transient elastography for the staging of liver fibrosis: a meta-analysis. Gastroenterology. 2008;134(4):960–974. doi: 10.1053/j.gastro.2008.01.034.
    1. Stevenson M, Lloyd-Jones M, Morgan MY, Wong R. Non-invasive diagnostic assessment tools for the detection of liver fibrosis in patients with suspected alcohol-related liver disease: a systematic review and economic evaluation. Health Technol Assess. 2012;16(4):1–174. doi: 10.3310/hta16040.
    1. Sandrin L, Fourquet B, Hasquenoph JM, Yon S, Fournier C, Mal F, Christidis C, Ziol M, Poulet B, Kazemi F, Beaugrand M, Palau R. Transient elastography: a new noninvasive method for assessment of hepatic fibrosis. Ultrasound Med Biol. 2003;29(12):1705–1713. doi: 10.1016/j.ultrasmedbio.2003.07.001.
    1. Mottin CC, Moretto M, Padoin AV, Swarowsky AM, Toneto MG, Glock L, Repetto G. The role of ultrasound in the diagnosis of hepatic steatosis in morbidly obese patients. Obes Surg. 2004;14(5):635–637. doi: 10.1381/096089204323093408.
    1. Kuhn JP, et al. Quantitative chemical shift-encoded MRI is an accurate method to quantify hepatic steatosis. J Magn Reson Imaging. 2014;39(6):1494–1501. doi: 10.1002/jmri.24289.
    1. Reeder SB, Cruite I, Hamilton G, Sirlin CB. Quantitative assessment of liver fat with magnetic resonance imaging and spectroscopy. J Magn Reson Imaging. 2011;34(4):729–749. doi: 10.1002/jmri.22580.
    1. Heath ML, Kow L, Slavotinek JP, Valentine R, Toouli J, Thompson CH. Abdominal adiposity and liver fat content 3 and 12 months after gastric banding surgery. Metabolism. 2009;58(6):753–758. doi: 10.1016/j.metabol.2008.05.021.
    1. Gaborit B et al. Ectopic fat storage in the pancreas using H-MRS: importance of diabetic status and modulation with bariatric surgery-induced weight loss. Int J Obes. 2014;
    1. Verras CG, et al. Serum fetuin-A levels are associated with serum triglycerides before and 6 months after bariatric surgery. Hormones (Athens) 2017;16(3):297–305.
    1. Brix JM, Stingl H, Höllerl F, Schernthaner GH, Kopp HP, Schernthaner G. Elevated Fetuin-A concentrations in morbid obesity decrease after dramatic weight loss. J Clin Endocrinol Metab. 2010;95(11):4877–4881. doi: 10.1210/jc.2010-0148.
    1. Yang PJ, Ser KH, Lin MT, Nien HC, Chen CN, Yang WS, Lee WJ. Diabetes associated markers after bariatric surgery: Fetuin-A, but not matrix Metalloproteinase-7, is reduced. Obes Surg. 2015;25(12):2328–2334. doi: 10.1007/s11695-015-1688-5.

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