Abdominal Radiology

, Volume 44, Issue 9, pp 3107–3114 | Cite as

Relationship between abdominal fat stores and liver fat, pancreatic fat, and metabolic comorbidities in a pediatric population with non-alcoholic fatty liver disease

  • Andrew T. TroutEmail author
  • David E. Hunte
  • Marialena Mouzaki
  • Stavra A. Xanthakos
  • Weizhe Su
  • Bin Zhang
  • Jonathan R. Dillman



To define the relationship between compartmental abdominal fat stores, liver and pancreatic fat fractions, and type 2 diabetes mellitus (T2DM) in children with non-alcoholic fatty liver disease (NAFLD).


This was a retrospective study of patients with NAFLD who underwent abdominal MRI between August 2015 and July 2017. Using an axial multi-echo Dixon-based sequence, liver fat fraction (LFF) and pancreatic fat fraction (PFF) were measured. The fat image was used to quantify abdominal fat depots (thickness, cross-sectional area) at the L2 vertebral level. Multivariable models with stepwise selection were created for prediction of LFF, PFF, and T2DM status based upon variables of clinical interest.


86 patients (70% male, 25% Hispanic, 58% Caucasian, 11% African American) with a mean age of 14.2 ± 3.2 years were included. 19 (22%) patients were pre-diabetic or diabetic. Only ethnicity was a predictor of LFF (P = 0.0023) with Hispanic ethnicity associated with the highest LFF. Depending on the model, either total abdominal fat area (P = 0.0003) or patient weight (P = 0.008) were the only predictors of PFF. No patient variable predicted T2DM status.


In our population, there was an association between ethnicity and LFF, with the highest LFF in Hispanics. The presence or severity of hepatic steatosis could not be predicted based on patient size or the distribution of abdominal fat in our cohort. Neither LFF nor PFF were predictive of T2DM.


NAFLD Steatosis Pancreas Diabetes MRI PDFF 


Compliance with ethical standards

Conflict of interest

None relevant to this article. Dr. Trout receives unrelated grant support from Siemens Medical Solutions and Canon Medical Systems for ultrasound research. Dr. Trout also receives royalties for authorship from Reed Elsevier and Wolters Kluwer. Dr. Dillman receives unrelated grant support from Siemens Medical Solutions and Bracco.


  1. 1.
    Tariq H, Nayudu S, Akella S, Glandt M, Chilimuri S (2016) Non-Alcoholic Fatty Pancreatic Disease: A Review of Literature. Gastroenterology Res 9 (6):87-91. CrossRefGoogle Scholar
  2. 2.
    Welsh JA, Karpen S, Vos MB (2013) Increasing prevalence of nonalcoholic fatty liver disease among United States adolescents, 1988-1994 to 2007-2010. J Pediatr 162 (3):496-500 e491.
  3. 3.
    Temple JL, Cordero P, Li J, Nguyen V, Oben JA (2016) A Guide to Non-Alcoholic Fatty Liver Disease in Childhood and Adolescence. Int J Mol Sci 17 (6).
  4. 4.
    Jakobsen MU, Berentzen T, Sorensen TI, Overvad K (2007) Abdominal obesity and fatty liver. Epidemiol Rev 29:77-87. CrossRefGoogle Scholar
  5. 5.
    Goran MI, Figueroa R, McGloin A, Nguyen V, Treuth MS, Nagy TR (1995) Obesity in children: recent advances in energy metabolism and body composition. Obes Res 3 (3):277-289CrossRefGoogle Scholar
  6. 6.
    Schwimmer JB, Middleton MS, Behling C, Newton KP, Awai HI, Paiz MN, Lam J, Hooker JC, Hamilton G, Fontanesi J, Sirlin CB (2015) Magnetic resonance imaging and liver histology as biomarkers of hepatic steatosis in children with nonalcoholic fatty liver disease. Hepatology 61 (6):1887-1895. CrossRefGoogle Scholar
  7. 7.
    Middleton MS, Heba ER, Hooker CA, Bashir MR, Fowler KJ, Sandrasegaran K, Brunt EM, Kleiner DE, Doo E, Van Natta ML, Lavine JE, Neuschwander-Tetri BA, Sanyal A, Loomba R, Sirlin CB, Network NCR (2017) Agreement Between Magnetic Resonance Imaging Proton Density Fat Fraction Measurements and Pathologist-Assigned Steatosis Grades of Liver Biopsies From Adults With Nonalcoholic Steatohepatitis. Gastroenterology 153 (3):753-761. CrossRefGoogle Scholar
  8. 8.
    Middleton MS, Van Natta ML, Heba ER, Alazraki A, Trout AT, Masand P, Brunt EM, Kleiner DE, Doo E, Tonascia J, Lavine JE, Shen W, Hamilton G, Schwimmer JB, Sirlin CB, Network NCR (2018) Diagnostic accuracy of magnetic resonance imaging hepatic proton density fat fraction in pediatric nonalcoholic fatty liver disease. Hepatology 67 (3):858-872. CrossRefGoogle Scholar
  9. 9.
    Mouzaki M, Trout AT, Arce-Clachar AC, Bramlage K, Kuhnell P, Dillman JR, Xanthakos S (2018) Assessment of Nonalcoholic Fatty Liver Disease Progression in Children Using Magnetic Resonance Imaging. J Pediatr.
  10. 10.
    DeFronzo RA, Ferrannini E (1991) Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care 14 (3):173-194Google Scholar
  11. 11.
    Lindsay RS, Howard BV (2004) Cardiovascular risk associated with the metabolic syndrome. Curr Diab Rep 4 (1):63-68CrossRefGoogle Scholar
  12. 12.
    Mantatzis M, Milousis T, Katergari S, Delistamatis A, Papachristou DN, Prassopoulos P (2014) Abdominal adipose tissue distribution on MRI and diabetes. Acad Radiol 21 (5):667-674. CrossRefGoogle Scholar
  13. 13.
    Wang CY, Ou HY, Chen MF, Chang TC, Chang CJ (2014) Enigmatic ectopic fat: prevalence of nonalcoholic fatty pancreas disease and its associated factors in a Chinese population. J Am Heart Assoc 3 (1):e000297. CrossRefGoogle Scholar
  14. 14.
    van Geenen EJ, Smits MM, Schreuder TC, van der Peet DL, Bloemena E, Mulder CJ (2010) Nonalcoholic fatty liver disease is related to nonalcoholic fatty pancreas disease. Pancreas 39 (8):1185-1190. CrossRefGoogle Scholar
  15. 15.
    Wong VW, Wong GL, Yeung DK, Abrigo JM, Kong AP, Chan RS, Chim AM, Shen J, Ho CS, Woo J, Chu WC, Chan HL (2014) Fatty pancreas, insulin resistance, and beta-cell function: a population study using fat-water magnetic resonance imaging. Am J Gastroenterol 109 (4):589-597. CrossRefGoogle Scholar
  16. 16.
    Joshi M, Dillman JR, Towbin AJ, Serai SD, Trout AT (2017) MR elastography: high rate of technical success in pediatric and young adult patients. Pediatr Radiol 47 (7):838-843. CrossRefGoogle Scholar
  17. 17.
    Ridler TW, Calvard S (1978) Picture Thresholding Using an Iterative Selection Method. Ieee T Syst Man Cyb 8 (8):630-632CrossRefGoogle Scholar
  18. 18.
    American Diabetes A (2014) Standards of medical care in diabetes–2014. Diabetes Care 37 Suppl 1:S14-80. CrossRefGoogle Scholar
  19. 19.
    Le KA, Ventura EE, Fisher JQ, Davis JN, Weigensberg MJ, Punyanitya M, Hu HH, Nayak KS, Goran MI (2011) Ethnic differences in pancreatic fat accumulation and its relationship with other fat depots and inflammatory markers. Diabetes Care 34 (2):485-490. CrossRefGoogle Scholar
  20. 20.
    Yaskolka Meir A, Tene L, Cohen N, Shelef I, Schwarzfuchs D, Gepner Y, Zelicha H, Rein M, Bril N, Serfaty D, Kenigsbuch S, Chassidim Y, Sarusy B, Dicker D, Thiery J, Ceglarek U, Stumvoll M, Bluher M, Stampfer MJ, Rudich A, Shai I (2017) Intrahepatic fat, abdominal adipose tissues, and metabolic state: magnetic resonance imaging study. Diabetes Metab Res Rev 33 (5).
  21. 21.
    Parente DB, Oliveira Neto JA, Brasil P, Paiva FF, Ravani JPR, Gomes MB, Lanzoni V, Campos CFF, Machado-Silva L, Perez RM, Rodrigues RS (2018) Preperitoneal fat as a non-invasive marker of increased risk of severe non-alcoholic fatty liver disease in patients with type 2 diabetes. J Gastroenterol Hepatol 33 (2):511-517. CrossRefGoogle Scholar
  22. 22.
    Toledo-Corral CM, Alderete TL, Hu HH, Nayak K, Esplana S, Liu T, Goran MI, Weigensberg MJ (2013) Ectopic fat deposition in prediabetic overweight and obese minority adolescents. J Clin Endocrinol Metab 98 (3):1115-1121. CrossRefGoogle Scholar
  23. 23.
    Nazare JA, Smith JD, Borel AL, Haffner SM, Balkau B, Ross R, Massien C, Almeras N, Despres JP (2012) Ethnic influences on the relations between abdominal subcutaneous and visceral adiposity, liver fat, and cardiometabolic risk profile: the International Study of Prediction of Intra-Abdominal Adiposity and Its Relationship With Cardiometabolic Risk/Intra-Abdominal Adiposity. Am J Clin Nutr 96 (4):714-726. CrossRefGoogle Scholar
  24. 24.
    Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, Grundy SM, Hobbs HH (2004) Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 40 (6):1387-1395. CrossRefGoogle Scholar
  25. 25.
    de Mutsert R, Gast K, Widya R, de Koning E, Jazet I, Lamb H, le Cessie S, de Roos A, Smit J, Rosendaal F, den Heijer M (2018) Associations of Abdominal Subcutaneous and Visceral Fat with Insulin Resistance and Secretion Differ Between Men and Women: The Netherlands Epidemiology of Obesity Study. Metab Syndr Relat Disord 16 (1):54-63. CrossRefGoogle Scholar
  26. 26.
    McLaughlin T, Lamendola C, Liu A, Abbasi F (2011) Preferential fat deposition in subcutaneous versus visceral depots is associated with insulin sensitivity. J Clin Endocrinol Metab 96 (11):E1756-1760. CrossRefGoogle Scholar
  27. 27.
    Pacifico L, Di Martino M, Anania C, Andreoli GM, Bezzi M, Catalano C, Chiesa C (2015) Pancreatic fat and beta-cell function in overweight/obese children with nonalcoholic fatty liver disease. World J Gastroenterol 21 (15):4688-4695. CrossRefGoogle Scholar
  28. 28.
    van der Zijl NJ, Goossens GH, Moors CC, van Raalte DH, Muskiet MH, Pouwels PJ, Blaak EE, Diamant M (2011) Ectopic fat storage in the pancreas, liver, and abdominal fat depots: impact on beta-cell function in individuals with impaired glucose metabolism. J Clin Endocrinol Metab 96 (2):459-467. CrossRefGoogle Scholar
  29. 29.
    Maggio AB, Mueller P, Wacker J, Viallon M, Belli DC, Beghetti M, Farpour-Lambert NJ, McLin VA (2012) Increased pancreatic fat fraction is present in obese adolescents with metabolic syndrome. J Pediatr Gastroenterol Nutr 54 (6):720-726. CrossRefGoogle Scholar
  30. 30.
    Staaf J, Labmayr V, Paulmichl K, Manell H, Cen J, Ciba I, Dahlbom M, Roomp K, Anderwald CH, Meissnitzer M, Schneider R, Forslund A, Widhalm K, Bergquist J, Ahlstrom H, Bergsten P, Weghuber D, Kullberg J (2017) Pancreatic Fat Is Associated With Metabolic Syndrome and Visceral Fat but Not Beta-Cell Function or Body Mass Index in Pediatric Obesity. Pancreas 46 (3):358-365. CrossRefGoogle Scholar
  31. 31.
    Joshi M, Dillman JR, Singh K, Serai SD, Towbin AJ, Xanthakos S, Zhang B, Su W, Trout AT (2018) Quantitative MRI of fatty liver disease in a large pediatric cohort: correlation between liver fat fraction, stiffness, volume, and patient-specific factors. Abdom Radiol (NY) 43 (5):1168-1179. CrossRefGoogle Scholar
  32. 32.
    Maislin G, Ahmed MM, Gooneratne N, Thorne-Fitzgerald M, Kim C, Teff K, Arnardottir ES, Benediktsdottir B, Einarsdottir H, Juliusson S, Pack AI, Gislason T, Schwab RJ (2012) Single slice vs. volumetric MR assessment of visceral adipose tissue: reliability and validity among the overweight and obese. Obesity (Silver Spring) 20 (10):2124-2132.

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of RadiologyCincinnati Children’s Hospital Medical CenterCincinnatiUSA
  2. 2.Department of RadiologyUniversity of Cincinnati Medical CenterCincinnatiUSA
  3. 3.Department of PediatricsUniversity of Cincinnati College of MedicineCincinnatiUSA
  4. 4.Division of Gastroenterology, Hepatology and NutritionCincinnati Children’s Hospital Medical CenterCincinnatiUSA
  5. 5.Department of Mathematical SciencesUniversity of CincinnatiCincinnatiUSA
  6. 6.Division of Biostatistics and EpidemiologyCincinnati Children’s Hospital Medical CenterCincinnatiUSA

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