Skip to main content
SpringerLink
Log in

MRI characterization of brown adipose tissue in obese and normal-weight children

  • Original Article
  • Published:
Pediatric Radiology Aims and scope Submit manuscript

Abstract

Background

Brown adipose tissue (BAT) is identified in mammals as an adaptive thermogenic organ for modulation of energy expenditure and heat generation. Human BAT may be primarily composed of brown-in-white (BRITE) adipocytes and stimulation of BRITE may serve as a potential target for obesity interventions. Current imaging studies of BAT detection and characterization have been mainly limited to PET/CT. MRI is an emerging application for BAT characterization in healthy children.

Objective

To exploit Dixon and diffusion-weighted MRI methods to characterize cervical-supraclavicular BAT/BRITE properties in normal-weight and obese children while accounting for pubertal status.

Materials and methods

Twenty-eight healthy children (9–15 years old) with a normal or obese body mass index participated. MRI exams were performed to characterize supraclavicular adipose tissues by measuring tissue fat percentage, T2*, tissue water mobility, and microvasculature properties. We used multivariate linear regression models to compare tissue properties between normal-weight and obese groups while accounting for pubertal status.

Results

MRI measurements of BAT/BRITE tissues in obese children showed higher fat percentage (P < 0.0001), higher T2* (P < 0.0001), and lower diffusion coefficient (P = 0.015) compared with normal-weight children. Pubertal status was a significant covariate for the T2* measurement, with higher T2* (P = 0.0087) in pubertal children compared to prepubertal children. Perfusion measurements varied by pubertal status. Compared to normal-weight children, obese prepubertal children had lower perfusion fraction (P = 0.003) and pseudo-perfusion coefficient (P = 0.048); however, obese pubertal children had higher perfusion fraction (P = 0.02) and pseudo-perfusion coefficient (P = 0.028).

Conclusion

This study utilized chemical-shift Dixon MRI and diffusion-weighted MRI methods to characterize supraclavicular BAT/BRITE tissue properties. The multi-parametric evaluation revealed evidence of morphological differences in brown adipose tissues between obese and normal-weight children.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. National Heart, Lung and Blood Institute (1998) Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults — the evidence report. National Institutes of Health. Obes Res 2:51S–209S

  2. Van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM et al (2009) Cold-activated brown adipose tissue in healthy men. N Engl J Med 360:1500–1508

    Article  PubMed  Google Scholar 

  3. Saito M, Okamatsu-Ogura Y, Matsushita M et al (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58:1526–1531

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Saito M (2013) Brown adipose tissue as a regulator of energy expenditure and body fat in humans. Diabetes Metab J 37:22–29

    Article  PubMed Central  PubMed  Google Scholar 

  5. Lee P, Zhao JT, Swarbrick MM et al (2011) High prevalence of brown adipose tissue in adult humans. J Clin Endocrinol Metab 96:2450–2455

    Article  CAS  PubMed  Google Scholar 

  6. Virtanen KA, Lidell ME, Orava J et al (2009) Functional brown adipose tissue in healthy adults. N Engl J Med 360:1518–1525

    Article  CAS  PubMed  Google Scholar 

  7. Lee P, Greenfield JR, Ho KK et al (2010) A critical appraisal of the prevalence and metabolic significance of brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab 299:E601–606

    Article  CAS  PubMed  Google Scholar 

  8. Yoneshiro T, Aita S, Matsushita M et al (2011) Brown adipose tissue, whole-body energy expenditure, and thermogenesis in healthy adult men. Obesity 19:13–16

    Article  PubMed  Google Scholar 

  9. Vijgen GH, Bouvy ND, Teule GJ et al (2011) Brown adipose tissue in morbidly obese subjects. PLoS One 6, e17247

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Vosselman MJ, Brans B, van der Lans AA et al (2013) Brown adipose tissue activity after a high-calorie meal in humans. Am J Clin Nutr 98:57–64

    Article  CAS  PubMed  Google Scholar 

  11. Van der Lans AA, Hoeks J, Brans B et al (2013) Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J Clin Invest 123:3395–3403

    Article  PubMed Central  PubMed  Google Scholar 

  12. Chondronikola M, Volpi E, Borsheim E et al (2014) Brown adipose tissue improves whole-body glucose homeostasis and insulin sensitivity in humans. Diabetes 63:4089–4099

    Article  CAS  PubMed  Google Scholar 

  13. Lee P, Smith S, Linderman J et al (2014) Temperature-acclimated brown adipose tissue modulates insulin sensitivity in humans. Diabetes 63:3686–3698

    Article  CAS  PubMed  Google Scholar 

  14. Cypess AM, Lehman S, Williams G et al (2009) Identification and importance of brown adipose tissue in adult humans. N Engl J Med 360:1509–1517

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Sharp LZ, Shinoda K, Ohno H et al (2012) Human BAT possesses molecular signatures that resemble beige/brite cells. PLoS One 7, e49452

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Lidell ME, Betz MJ, Dahlqvist Leinhard O et al (2013) Evidence for two types of brown adipose tissue in humans. Nat Med 19:631–634

    Article  CAS  PubMed  Google Scholar 

  17. Giralt M, Villarroya F (2013) White, brown, beige/brite: different adipose cells for different functions? Endocrinology 154:2992–3000

    Article  CAS  PubMed  Google Scholar 

  18. Beranger GE, Karbiener M, Barquissau V et al (2013) In vitro brown and “brite”/”beige” [sic] adipogenesis: human cellular models and molecular aspects. Biochim Biophys Acta 1831:905–914

    Article  CAS  PubMed  Google Scholar 

  19. Gelfand MJ, O’Hara SM, Curtwright LA et al (2005) Pre-medication to block [(18)F]FDG uptake in the brown adipose tissue of pediatric and adolescent patients. Pediatr Radiol 35:984–990

    Article  PubMed  Google Scholar 

  20. Bar-Sever Z, Keidar Z, Ben-Barak A et al (2007) The incremental value of 18F-FDG PET/CT in paediatric malignancies. Eur J Nucl Med Mol Imaging 34:630–637

    Article  PubMed  Google Scholar 

  21. Drubach LA, Palmer EL 3rd, Connolly LP et al (2011) Pediatric brown adipose tissue: detection, epidemiology, and differences from adults. J Pediatr 159:939–944

    Article  CAS  PubMed  Google Scholar 

  22. Gilsanz V, Smith ML, Goodarzian F et al (2012) Changes in brown adipose tissue in boys and girls during childhood and puberty. J Pediatr 160:604–609

    Article  PubMed Central  PubMed  Google Scholar 

  23. Ponrartana S, Hu HH, Gilsanz V (2013) On the relevance of brown adipose tissue in children. Ann N Y Acad Sci 1302:24–29

    Article  PubMed  Google Scholar 

  24. Hu HH, Perkins TG, Chia JM et al (2013) Characterization of human brown adipose tissue by chemical-shift water-fat MRI. AJR Am J Roentgenol 200:177–183

    Article  PubMed Central  PubMed  Google Scholar 

  25. Hu HH, Smith DL Jr, Nayak KS et al (2010) Identification of brown adipose tissue in mice with fat-water IDEAL-MRI. J Magn Reson Imaging 31:1195–1202

    Article  PubMed Central  PubMed  Google Scholar 

  26. Hu HH, Tovar JP, Pavlova Z et al (2012) Unequivocal identification of brown adipose tissue in a human infant. J Magn Reson Imaging 35:938–942

    Article  PubMed Central  PubMed  Google Scholar 

  27. Hu HH, Yin L, Aggabao PC et al (2013) Comparison of brown and white adipose tissues in infants and children with chemical-shift-encoded water-fat MRI. J Magn Reson Imaging 38:885–896

    Article  PubMed Central  PubMed  Google Scholar 

  28. Rasmussen JM, Entringer S, Nguyen A et al (2013) Brown adipose tissue quantification in human neonates using water-fat separated MRI. PLoS One 8, e77907

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Le Bihan D (2008) Intravoxel incoherent motion perfusion MR imaging: a wake-up call. Radiology 249:748–752

    Article  PubMed  Google Scholar 

  30. Marshall WA, Tanner JM (1969) Variations in pattern of pubertal changes in girls. Arch Dis Child 44:291–303

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  31. Marshall WA, Tanner JM (1970) Variations in the pattern of pubertal changes in boys. Arch Dis Child 45:13–23

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Deng J, Miller FH, Salem R et al (2006) Multishot diffusion-weighted PROPELLER magnetic resonance imaging of the abdomen. Invest Radiol 41:769–775

    Article  PubMed  Google Scholar 

  33. Ren J, Dimitrov I, Sherry AD et al (2008) Composition of adipose tissue and marrow fat in humans by 1H NMR at 7 tesla. J Lipid Res 49:2055–2062

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Deng J, Fishbein MH, Rigsby CK et al (2014) Quantitative MRI for hepatic fat fraction and T2* measurement in pediatric patients with non-alcoholic fatty liver disease. Pediatr Radiol 44:1379–1387

    Article  PubMed  Google Scholar 

  35. Patel J, Sigmund EE, Rusinek H et al (2010) Diagnosis of cirrhosis with intravoxel incoherent motion diffusion MRI and dynamic contrast-enhanced MRI alone and in combination: preliminary experience. J Magn Reson Imaging 31:589–600

    Article  PubMed  Google Scholar 

  36. Weber DR, Moore RH, Leonard MB et al (2013) Fat and lean BMI reference curves in children and adolescents and their utility in identifying excess adiposity compared with BMI and percentage body fat. Am J Clin Nutr 98:49–56

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  37. Hu HH, Hines CD, Smith DL Jr et al (2012) Variations in T(2)* and fat content of murine brown and white adipose tissues by chemical-shift MRI. Magn Reson Imaging 30:323–329

    Article  PubMed Central  PubMed  Google Scholar 

  38. Van Rooijen BD, van der Lans AA, Brans B et al (2013) Imaging cold-activated brown adipose tissue using dynamic T2*-weighted magnetic resonance imaging and 2-deoxy-2-[18F]fluoro-D-glucose positron emission tomography. Invest Radiol 48:708–714

    Article  PubMed  Google Scholar 

  39. Padhani AR, Liu G, Koh DM et al (2009) Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. Neoplasia 11:102–125

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Bogner W, Pinker-Domenig K, Bickel H et al (2012) Readout-segmented echo-planar imaging improves the diagnostic performance of diffusion-weighted MR breast examinations at 3.0T. Radiology 263:64–76

    Article  PubMed  Google Scholar 

  41. Jeong EK, Kim SE, Guo J et al (2005) High-resolution DTI with 2D interleaved multislice reduced FOV single-shot diffusion-weighted EPI (2D ss-rFOV-DWEPI). Magn Reson Med 54:1575–1579

    Article  PubMed  Google Scholar 

  42. Wilm BJ, Svensson J, Henning A et al (2007) Reduced field-of-view MRI using outer volume suppression for spinal cord diffusion imaging. Magn Reson Med 57:625–630

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This project was supported through a cooperative research agreement between Ann & Robert H. Lurie Children’s Hospital of Chicago and the Williams Heart Foundation.

Dr. J. L. Josefson is supported by Grant Number K12 HD055884 from the Eunice Kennedy Shriver National Institute of Child Health & Human Development.

Conflicts of interest

None

Author information

Authors and Affiliations

  1. Department of Medical Imaging, Ann & Robert H. Lurie Children’s Hospital of Chicago, 225 E. Chicago Ave., Box 9, Chicago, IL, 60611-2605, USA

    Jie Deng, Samantha E. Schoeneman, Cynthia K. Rigsby & Richard M. Shore

  2. Collaborative Research Unit, John H. Stroger, Jr. Hospital of Cook County, Chicago, IL, USA

    Huiyuan Zhang

  3. Stanley Manne Children’s Research Institute, Ann & Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL, USA

    Soyang Kwon

  4. Division of Endocrinology, Ann & Robert H. Lurie Children’s Hospital of Chicago, Chicago, IL, USA

    Jami L. Josefson

  5. Department of Radiology, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA

    Jie Deng, Cynthia K. Rigsby & Richard M. Shore

  6. Department of Pediatrics, Feinberg School of Medicine, Northwestern University, Chicago, IL, USA

    Soyang Kwon & Jami L. Josefson

Authors
  1. Jie Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Samantha E. Schoeneman
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Huiyuan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Soyang Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cynthia K. Rigsby
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Richard M. Shore
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jami L. Josefson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jie Deng.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deng, J., Schoeneman, S.E., Zhang, H. et al. MRI characterization of brown adipose tissue in obese and normal-weight children. Pediatr Radiol 45, 1682–1689 (2015). https://doi.org/10.1007/s00247-015-3391-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00247-015-3391-z

Keywords

Search

Navigation