Skip to main content
Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging 4/2014

01.04.2014 | Review Article

Molecular imaging of brown adipose tissue in health and disease

verfasst von: Matthias Bauwens, Roel Wierts, Bart van Royen, Jan Bucerius, Walter Backes, Felix Mottaghy, Boudewijn Brans

Erschienen in: European Journal of Nuclear Medicine and Molecular Imaging | Ausgabe 4/2014

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Brown adipose tissue (BAT) has transformed from an interfering tissue in oncological 18F-fluorodeoxyglucose (FDG) positron emission tomography (PET) to an independent imaging research field. This review takes the perspective from the imaging methodology on which human BAT research has come to rely on heavily.

Methods

This review analyses relevant PubMed-indexed publications that discuss molecular imaging methods of BAT. In addition, reported links between BAT and human diseases such as obesity are discussed, and the possibilities for imaging in these fields are highlighted. Radiopharmaceuticals aiming at several different biological mechanisms of BAT are discussed and evaluated.

Results

Prospective, dedicated studies allow visualization of BAT function in a high percentage of human subjects. BAT dysfunction has been implicated in obesity, linked with diabetes and associated with cachexia and atherosclerosis. Presently, 18F-FDG PET/CT is the most useful tool for evaluating therapies aiming at BAT activity. In addition to 18F-FDG, other radiopharmaceuticals such as 99mTc-sestamibi, 123I-metaiodobenzylguanidine (MIBG), 18F-fluorodopa and 18F-14(R,S)-[18F]fluoro-6-thia-heptadecanoic acid (FTHA) may have a potential for visualizing other aspects of BAT activity. MRI methods are under continuous development and provide the prospect of functional imaging without ionizing radiation.

Conclusion

Molecular imaging of BAT can be used to quantitatively assess different aspects of BAT metabolic activity.
Literatur
1.
Zurück zum Zitat Barrington SF, Maisey MN. Skeletal muscle uptake of fluorine-18-FDG: effect of oral diazepam. J Nucl Med. 1996;37:1127–9.PubMed Barrington SF, Maisey MN. Skeletal muscle uptake of fluorine-18-FDG: effect of oral diazepam. J Nucl Med. 1996;37:1127–9.PubMed
2.
3.
Zurück zum Zitat Hany TF, Gharehpapagh E, Kamel EM, Buck A, Himms-Hagen J, von Schulthess GK. Brown adipose tissue: a factor to consider in symmetrical tracer uptake in the neck and upper chest region. Eur J Nucl Med Mol Imaging. 2002;29:1393–8. doi:10.1007/s00259-002-0902-6.PubMed Hany TF, Gharehpapagh E, Kamel EM, Buck A, Himms-Hagen J, von Schulthess GK. Brown adipose tissue: a factor to consider in symmetrical tracer uptake in the neck and upper chest region. Eur J Nucl Med Mol Imaging. 2002;29:1393–8. doi:10.​1007/​s00259-002-0902-6.PubMed
4.
Zurück zum Zitat Cohade C, Mourtzikos KA, Wahl RL. "USA-Fat": prevalence is related to ambient outdoor temperature-evaluation with 18F-FDG PET/CT. J Nucl Med. 2003;44:1267–70.PubMed Cohade C, Mourtzikos KA, Wahl RL. "USA-Fat": prevalence is related to ambient outdoor temperature-evaluation with 18F-FDG PET/CT. J Nucl Med. 2003;44:1267–70.PubMed
5.
Zurück zum Zitat Cohade C, Osman M, Pannu HK, Wahl RL. Uptake in supraclavicular area fat (“USA-Fat”): description on 18F-FDG PET/CT. J Nucl Med. 2003;44:170–6.PubMed Cohade C, Osman M, Pannu HK, Wahl RL. Uptake in supraclavicular area fat (“USA-Fat”): description on 18F-FDG PET/CT. J Nucl Med. 2003;44:170–6.PubMed
8.
Zurück zum Zitat van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009;360:1500–8. doi:10.1056/NEJMoa0808718.PubMed van Marken Lichtenbelt WD, Vanhommerig JW, Smulders NM, Drossaerts JM, Kemerink GJ, Bouvy ND, et al. Cold-activated brown adipose tissue in healthy men. N Engl J Med. 2009;360:1500–8. doi:10.​1056/​NEJMoa0808718.PubMed
9.
Zurück zum Zitat Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, et al. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360:1518–25. doi:10.1056/NEJMoa0808949.PubMed Virtanen KA, Lidell ME, Orava J, Heglind M, Westergren R, Niemi T, et al. Functional brown adipose tissue in healthy adults. N Engl J Med. 2009;360:1518–25. doi:10.​1056/​NEJMoa0808949.PubMed
10.
Zurück zum Zitat Zingaretti MC, Crosta F, Vitali A, Guerrieri M, Frontini A, Cannon B, et al. The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J. 2009;23:3113–20. doi:10.1096/fj.09-133546.PubMed Zingaretti MC, Crosta F, Vitali A, Guerrieri M, Frontini A, Cannon B, et al. The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J. 2009;23:3113–20. doi:10.​1096/​fj.​09-133546.PubMed
11.
Zurück zum Zitat Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, et al. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes. 2009;58:1526–31. doi:10.2337/db09-0530.PubMedCentralPubMed Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, et al. High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes. 2009;58:1526–31. doi:10.​2337/​db09-0530.PubMedCentralPubMed
12.
Zurück zum Zitat Yeung HW, Grewal RK, Gonen M, Schöder H, Larson SM. Patterns of (18)F-FDG uptake in adipose tissue and muscle: a potential source of false-positives for PET. J Nucl Med. 2003;44:1789–96.PubMed Yeung HW, Grewal RK, Gonen M, Schöder H, Larson SM. Patterns of (18)F-FDG uptake in adipose tissue and muscle: a potential source of false-positives for PET. J Nucl Med. 2003;44:1789–96.PubMed
13.
Zurück zum Zitat Truong MT, Erasmus JJ, Munden RF, Marom EM, Sabloff BS, Gladish GW, et al. Focal FDG uptake in mediastinal brown fat mimicking malignancy: a potential pitfall resolved on PET/CT. AJR Am J Roentgenol. 2004;183:1127–32. doi:10.2214/ajr.183.4.1831127.PubMed Truong MT, Erasmus JJ, Munden RF, Marom EM, Sabloff BS, Gladish GW, et al. Focal FDG uptake in mediastinal brown fat mimicking malignancy: a potential pitfall resolved on PET/CT. AJR Am J Roentgenol. 2004;183:1127–32. doi:10.​2214/​ajr.​183.​4.​1831127.PubMed
14.
Zurück zum Zitat Kim S, Krynyckyi BR, Machac J, Kim CK. Temporal relation between temperature change and FDG uptake in brown adipose tissue. Eur J Nucl Med Mol Imaging. 2008;35:984–9. doi:10.1007/s00259-007-0670-4.PubMed Kim S, Krynyckyi BR, Machac J, Kim CK. Temporal relation between temperature change and FDG uptake in brown adipose tissue. Eur J Nucl Med Mol Imaging. 2008;35:984–9. doi:10.​1007/​s00259-007-0670-4.PubMed
15.
16.
Zurück zum Zitat Cheng WY, Zhu ZH, Ouyang M. Patterns and characteristics of brown adipose tissue uptake of 18F-FDG positron emission tomograph/computed tomography imaging. Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 2009;31:370–3.PubMed Cheng WY, Zhu ZH, Ouyang M. Patterns and characteristics of brown adipose tissue uptake of 18F-FDG positron emission tomograph/computed tomography imaging. Zhongguo Yi Xue Ke Xue Yuan Xue Bao. 2009;31:370–3.PubMed
17.
Zurück zum Zitat Stefan N, Pfannenberg C, Häring HU. The importance of brown adipose tissue. N Engl J Med. 2009;361:416–7. author reply 8–21.PubMed Stefan N, Pfannenberg C, Häring HU. The importance of brown adipose tissue. N Engl J Med. 2009;361:416–7. author reply 8–21.PubMed
19.
Zurück zum Zitat Lee P, Greenfield JR, Ho KK, Fulham MJ. A critical appraisal of the prevalence and metabolic significance of brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab. 2010;299:E601–6. doi:10.1152/ajpendo.00298.2010.PubMed Lee P, Greenfield JR, Ho KK, Fulham MJ. A critical appraisal of the prevalence and metabolic significance of brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab. 2010;299:E601–6. doi:10.​1152/​ajpendo.​00298.​2010.PubMed
20.
Zurück zum Zitat Pace L, Nicolai E, D’Amico D, Ibello F, Della Morte AM, Salvatore B, et al. Determinants of physiologic 18F-FDG uptake in brown adipose tissue in sequential PET/CT examinations. Mol Imaging Biol. 2011;13:1029–35. doi:10.1007/s11307-010-0431-9.PubMed Pace L, Nicolai E, D’Amico D, Ibello F, Della Morte AM, Salvatore B, et al. Determinants of physiologic 18F-FDG uptake in brown adipose tissue in sequential PET/CT examinations. Mol Imaging Biol. 2011;13:1029–35. doi:10.​1007/​s11307-010-0431-9.PubMed
21.
Zurück zum Zitat Ouellet V, Routhier-Labadie A, Bellemare W, Lakhal-Chaieb L, Turcotte E, Carpentier AC, et al. Outdoor temperature, age, sex, body mass index, and diabetic status determine the prevalence, mass, and glucose-uptake activity of 18F-FDG-detected BAT in humans. J Clin Endocrinol Metab. 2011;96:192–9. doi:10.1210/jc.2010-0989.PubMed Ouellet V, Routhier-Labadie A, Bellemare W, Lakhal-Chaieb L, Turcotte E, Carpentier AC, et al. Outdoor temperature, age, sex, body mass index, and diabetic status determine the prevalence, mass, and glucose-uptake activity of 18F-FDG-detected BAT in humans. J Clin Endocrinol Metab. 2011;96:192–9. doi:10.​1210/​jc.​2010-0989.PubMed
22.
Zurück zum Zitat Jacene HA, Cohade CC, Zhang Z, Wahl RL. The relationship between patients’ serum glucose levels and metabolically active brown adipose tissue detected by PET/CT. Mol Imaging Biol. 2011;13:1278–83. doi:10.1007/s11307-010-0379-9. Jacene HA, Cohade CC, Zhang Z, Wahl RL. The relationship between patients’ serum glucose levels and metabolically active brown adipose tissue detected by PET/CT. Mol Imaging Biol. 2011;13:1278–83. doi:10.​1007/​s11307-010-0379-9.
23.
24.
26.
Zurück zum Zitat Vrieze A, Schopman JE, Admiraal WM, Soeters MR, Nieuwdorp M, Verberne HJ, et al. Fasting and postprandial activity of brown adipose tissue in healthy men. J Nucl Med. 2012;53:1407–10. doi:10.2967/jnumed.111.100701.PubMed Vrieze A, Schopman JE, Admiraal WM, Soeters MR, Nieuwdorp M, Verberne HJ, et al. Fasting and postprandial activity of brown adipose tissue in healthy men. J Nucl Med. 2012;53:1407–10. doi:10.​2967/​jnumed.​111.​100701.PubMed
27.
Zurück zum Zitat Admiraal WM, Holleman F, Bahler L, Soeters MR, Hoekstra JB, Verberne HJ. Combining 123I-metaiodobenzylguanidine SPECT/CT and 18F-FDG PET/CT for the assessment of brown adipose tissue activity in humans during cold exposure. J Nucl Med. 2013;54:208–12. doi:10.2967/jnumed.112.111849.PubMed Admiraal WM, Holleman F, Bahler L, Soeters MR, Hoekstra JB, Verberne HJ. Combining 123I-metaiodobenzylguanidine SPECT/CT and 18F-FDG PET/CT for the assessment of brown adipose tissue activity in humans during cold exposure. J Nucl Med. 2013;54:208–12. doi:10.​2967/​jnumed.​112.​111849.PubMed
28.
Zurück zum Zitat Vijgen GH, Bouvy ND, Teule GJ, Brans B, Hoeks J, Schrauwen P, et al. Increase in brown adipose tissue activity after weight loss in morbidly obese subjects. J Clin Endocrinol Metab. 2012;97:E1229–33. doi:10.1210/jc.2012-1289.PubMed Vijgen GH, Bouvy ND, Teule GJ, Brans B, Hoeks J, Schrauwen P, et al. Increase in brown adipose tissue activity after weight loss in morbidly obese subjects. J Clin Endocrinol Metab. 2012;97:E1229–33. doi:10.​1210/​jc.​2012-1289.PubMed
29.
Zurück zum Zitat Pfannenberg C, Werner MK, Ripkens S, Stef I, Deckert A, Schmadl M, et al. Impact of age on the relationships of brown adipose tissue with sex and adiposity in humans. Diabetes. 2010;59:1789–93. doi:10.2337/db10-0004.PubMedCentralPubMed Pfannenberg C, Werner MK, Ripkens S, Stef I, Deckert A, Schmadl M, et al. Impact of age on the relationships of brown adipose tissue with sex and adiposity in humans. Diabetes. 2010;59:1789–93. doi:10.​2337/​db10-0004.PubMedCentralPubMed
30.
Zurück zum Zitat Yoneshiro T, Aita S, Matsushita M, Kameya T, Nakada K, Kawai Y, et al. Brown adipose tissue, whole-body energy expenditure, and thermogenesis in healthy adult men. Obesity (Silver Spring). 2011;19:13–6. doi:10.1038/oby.2010.105. Yoneshiro T, Aita S, Matsushita M, Kameya T, Nakada K, Kawai Y, et al. Brown adipose tissue, whole-body energy expenditure, and thermogenesis in healthy adult men. Obesity (Silver Spring). 2011;19:13–6. doi:10.​1038/​oby.​2010.​105.
31.
Zurück zum Zitat Perkins AC, Mshelia DS, Symonds ME, Sathekge M. Prevalence and pattern of brown adipose tissue distribution of 18F-FDG in patients undergoing PET-CT in a subtropical climatic zone. Nucl Med Commun. 2013;34:168–74. doi:10.1097/MNM.0b013e32835bbbf0.PubMed Perkins AC, Mshelia DS, Symonds ME, Sathekge M. Prevalence and pattern of brown adipose tissue distribution of 18F-FDG in patients undergoing PET-CT in a subtropical climatic zone. Nucl Med Commun. 2013;34:168–74. doi:10.​1097/​MNM.​0b013e32835bbbf0​.PubMed
32.
Zurück zum Zitat Cronin CG, Prakash P, Daniels GH, Boland GW, Kalra MK, Halpern EF, et al. Brown fat at PET/CT: correlation with patient characteristics. Radiology. 2012;263:836–42. doi:10.1148/radiol.12100683.PubMed Cronin CG, Prakash P, Daniels GH, Boland GW, Kalra MK, Halpern EF, et al. Brown fat at PET/CT: correlation with patient characteristics. Radiology. 2012;263:836–42. doi:10.​1148/​radiol.​12100683.PubMed
33.
Zurück zum Zitat Zukotynski KA, Fahey FH, Laffin S, Davis R, Treves ST, Grant FD, et al. Seasonal variation in the effect of constant ambient temperature of 24 degrees C in reducing FDG uptake by brown adipose tissue in children. Eur J Nucl Med Mol Imaging. 2010;37:1854–60. doi:10.1007/s00259-010-1485-2.PubMed Zukotynski KA, Fahey FH, Laffin S, Davis R, Treves ST, Grant FD, et al. Seasonal variation in the effect of constant ambient temperature of 24 degrees C in reducing FDG uptake by brown adipose tissue in children. Eur J Nucl Med Mol Imaging. 2010;37:1854–60. doi:10.​1007/​s00259-010-1485-2.PubMed
34.
Zurück zum Zitat Zukotynski KA, Fahey FH, Laffin S, Davis R, Treves ST, Grant FD, et al. Constant ambient temperature of 24 degrees C significantly reduces FDG uptake by brown adipose tissue in children scanned during the winter. Eur J Nucl Med Mol Imaging. 2009;36:602–6. doi:10.1007/s00259-008-0983-y.PubMed Zukotynski KA, Fahey FH, Laffin S, Davis R, Treves ST, Grant FD, et al. Constant ambient temperature of 24 degrees C significantly reduces FDG uptake by brown adipose tissue in children scanned during the winter. Eur J Nucl Med Mol Imaging. 2009;36:602–6. doi:10.​1007/​s00259-008-0983-y.PubMed
35.
Zurück zum Zitat Ouellet V, Labbé SM, Blondin DP, Phoenix S, Guérin B, Haman F, et al. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest. 2012;122:545–52. doi:10.1172/JCI60433.PubMedCentralPubMed Ouellet V, Labbé SM, Blondin DP, Phoenix S, Guérin B, Haman F, et al. Brown adipose tissue oxidative metabolism contributes to energy expenditure during acute cold exposure in humans. J Clin Invest. 2012;122:545–52. doi:10.​1172/​JCI60433.PubMedCentralPubMed
36.
Zurück zum Zitat Vogel WV, Valdés Olmos RA, Tijs TJ, Gillies MF, van Elswijk G, Vogt J. Intervention to lower anxiety of 18F-FDG PET/CT patients by use of audiovisual imagery during the uptake phase before imaging. J Nucl Med Technol. 2012;40:92–8. doi:10.2967/jnmt.111.097964.PubMed Vogel WV, Valdés Olmos RA, Tijs TJ, Gillies MF, van Elswijk G, Vogt J. Intervention to lower anxiety of 18F-FDG PET/CT patients by use of audiovisual imagery during the uptake phase before imaging. J Nucl Med Technol. 2012;40:92–8. doi:10.​2967/​jnmt.​111.​097964.PubMed
40.
Zurück zum Zitat Yoneshiro T, Aita S, Matsushita M, Kayahara T, Kameya T, Kawai Y, et al. Recruited brown adipose tissue as an antiobesity agent in humans. J Clin Invest. 2013;123:3404–8. doi: 10.1172/JCI67803. Yoneshiro T, Aita S, Matsushita M, Kayahara T, Kameya T, Kawai Y, et al. Recruited brown adipose tissue as an antiobesity agent in humans. J Clin Invest. 2013;123:3404–8. doi: 10.​1172/​JCI67803.
41.
Zurück zum Zitat van der Lans AA, Hoeks J, Brans B, Vijgen GH, Visser MG, Vosselman MJ, et al. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J Clin Invest. 2013;123:3395–403. doi: 10.1172/JCI68993. van der Lans AA, Hoeks J, Brans B, Vijgen GH, Visser MG, Vosselman MJ, et al. Cold acclimation recruits human brown fat and increases nonshivering thermogenesis. J Clin Invest. 2013;123:3395–403. doi: 10.​1172/​JCI68993.
42.
Zurück zum Zitat van der Veen DR, Shao J, Chapman S, Leevy WM, Duffield GE. A diurnal rhythm in glucose uptake in brown adipose tissue revealed by in vivo PET-FDG imaging. Obesity (Silver Spring). 2012;20:1527–9. doi:10.1038/oby.2012.78. van der Veen DR, Shao J, Chapman S, Leevy WM, Duffield GE. A diurnal rhythm in glucose uptake in brown adipose tissue revealed by in vivo PET-FDG imaging. Obesity (Silver Spring). 2012;20:1527–9. doi:10.​1038/​oby.​2012.​78.
43.
44.
Zurück zum Zitat Jezek P, Garlid KD. Mammalian mitochondrial uncoupling proteins. Int J Biochem Cell Biol. 1998;30:1163–8.PubMed Jezek P, Garlid KD. Mammalian mitochondrial uncoupling proteins. Int J Biochem Cell Biol. 1998;30:1163–8.PubMed
45.
Zurück zum Zitat Rousset S, Alves-Guerra MC, Mozo J, Miroux B, Cassard-Doulcier AM, Bouillaud F, et al. The biology of mitochondrial uncoupling proteins. Diabetes. 2004;53 Suppl 1:S130–5.PubMed Rousset S, Alves-Guerra MC, Mozo J, Miroux B, Cassard-Doulcier AM, Bouillaud F, et al. The biology of mitochondrial uncoupling proteins. Diabetes. 2004;53 Suppl 1:S130–5.PubMed
47.
Zurück zum Zitat Jastroch M, Withers K, Klingenspor M. Uncoupling protein 2 and 3 in marsupials: identification, phylogeny, and gene expression in response to cold and fasting in Antechinus flavipes. Physiol Genomics. 2004;17:130–9. doi:10.1152/physiolgenomics.00165.2003.PubMed Jastroch M, Withers K, Klingenspor M. Uncoupling protein 2 and 3 in marsupials: identification, phylogeny, and gene expression in response to cold and fasting in Antechinus flavipes. Physiol Genomics. 2004;17:130–9. doi:10.​1152/​physiolgenomics.​00165.​2003.PubMed
48.
50.
Zurück zum Zitat Baba S, Jacene HA, Engles JM, Honda H, Wahl RL. CT Hounsfield units of brown adipose tissue increase with activation: preclinical and clinical studies. J Nucl Med. 2010;51:246–50. doi:10.2967/jnumed.109.068775.PubMed Baba S, Jacene HA, Engles JM, Honda H, Wahl RL. CT Hounsfield units of brown adipose tissue increase with activation: preclinical and clinical studies. J Nucl Med. 2010;51:246–50. doi:10.​2967/​jnumed.​109.​068775.PubMed
51.
Zurück zum Zitat Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, et al. Brown adipose tissue activity controls triglyceride clearance. Nat Med. 2011;17:200–5. doi:10.1038/nm.2297.PubMed Bartelt A, Bruns OT, Reimer R, Hohenberg H, Ittrich H, Peldschus K, et al. Brown adipose tissue activity controls triglyceride clearance. Nat Med. 2011;17:200–5. doi:10.​1038/​nm.​2297.PubMed
53.
Zurück zum Zitat Lidell ME, Betz MJ, Dahlqvist Leinhard O, Heglind M, Elander L, Slawik M, et al. Evidence for two types of brown adipose tissue in humans. Nat Med. 2013;19:631–4. doi:10.1038/nm.3017.PubMed Lidell ME, Betz MJ, Dahlqvist Leinhard O, Heglind M, Elander L, Slawik M, et al. Evidence for two types of brown adipose tissue in humans. Nat Med. 2013;19:631–4. doi:10.​1038/​nm.​3017.PubMed
55.
Zurück zum Zitat Jespersen NZ, Larsen TJ, Peijs L, Daugaard S, Homøe P, Loft A, et al. A classical brown adipose tissue mRNA signature partly overlaps with brite in the supraclavicular region of adult humans. Cell Metab. 2013;17:798–805. doi:10.1016/j.cmet.2013.04.011.PubMed Jespersen NZ, Larsen TJ, Peijs L, Daugaard S, Homøe P, Loft A, et al. A classical brown adipose tissue mRNA signature partly overlaps with brite in the supraclavicular region of adult humans. Cell Metab. 2013;17:798–805. doi:10.​1016/​j.​cmet.​2013.​04.​011.PubMed
56.
Zurück zum Zitat van der Lans AA, Hoeks J, Brans B, Vijgen G, Visser M, Vosselman MJ, et al. Cold acclimation recruits BAT and increases non-shivering thermogenesis in humans. J Clin Invest. 2013. Accepted for publication. van der Lans AA, Hoeks J, Brans B, Vijgen G, Visser M, Vosselman MJ, et al. Cold acclimation recruits BAT and increases non-shivering thermogenesis in humans. J Clin Invest. 2013. Accepted for publication.
57.
59.
Zurück zum Zitat Guerra C, Navarro P, Valverde AM, Arribas M, Brüning J, Kozak LP, et al. Brown adipose tissue-specific insulin receptor knockout shows diabetic phenotype without insulin resistance. J Clin Invest. 2001;108:1205–13. doi:10.1172/JCI13103.PubMedCentralPubMed Guerra C, Navarro P, Valverde AM, Arribas M, Brüning J, Kozak LP, et al. Brown adipose tissue-specific insulin receptor knockout shows diabetic phenotype without insulin resistance. J Clin Invest. 2001;108:1205–13. doi:10.​1172/​JCI13103.PubMedCentralPubMed
60.
61.
Zurück zum Zitat Moreno-Navarrete JM, Ortega F, Serrano M, Guerra E, Pardo G, Tinahones F, et al. Irisin is expressed and produced by human muscle and adipose tissue in association with obesity and insulin resistance. J Clin Endocrinol Metab. 2013;98:E769–78. doi:10.1210/jc.2012-2749.PubMed Moreno-Navarrete JM, Ortega F, Serrano M, Guerra E, Pardo G, Tinahones F, et al. Irisin is expressed and produced by human muscle and adipose tissue in association with obesity and insulin resistance. J Clin Endocrinol Metab. 2013;98:E769–78. doi:10.​1210/​jc.​2012-2749.PubMed
62.
Zurück zum Zitat Sakamoto T, Takahashi N, Sawaragi Y, Naknukool S, Yu R, Goto T, et al. Inflammation induced by RAW macrophages suppresses UCP1 mRNA induction via ERK activation in 10T1/2 adipocytes. Am J Physiol Cell Physiol. 2013;304:C729–38. doi:10.1152/ajpcell.00312.2012.PubMed Sakamoto T, Takahashi N, Sawaragi Y, Naknukool S, Yu R, Goto T, et al. Inflammation induced by RAW macrophages suppresses UCP1 mRNA induction via ERK activation in 10T1/2 adipocytes. Am J Physiol Cell Physiol. 2013;304:C729–38. doi:10.​1152/​ajpcell.​00312.​2012.PubMed
63.
Zurück zum Zitat Parinandi NL, Magalang UJ. Avatars of adipose tissue: the saga of transformation of white fat, the villain into brown fat, the protector. Focus on “inflammation induced by RAW macrophages suppresses the UCP1 mRNA induction via ERK activation in 10T1/2 adipocytes”. Am J Physiol Cell Physiol. 2013;304:C715–6.PubMed Parinandi NL, Magalang UJ. Avatars of adipose tissue: the saga of transformation of white fat, the villain into brown fat, the protector. Focus on “inflammation induced by RAW macrophages suppresses the UCP1 mRNA induction via ERK activation in 10T1/2 adipocytes”. Am J Physiol Cell Physiol. 2013;304:C715–6.PubMed
64.
Zurück zum Zitat Pasanisi F, Pace L, Fonti R, Marra M, Sgambati D, De Caprio C, et al. Evidence of brown fat activity in constitutional leanness. J Clin Endocrinol Metab. 2013;98:1214–8. doi:10.1210/jc.2012-2981.PubMed Pasanisi F, Pace L, Fonti R, Marra M, Sgambati D, De Caprio C, et al. Evidence of brown fat activity in constitutional leanness. J Clin Endocrinol Metab. 2013;98:1214–8. doi:10.​1210/​jc.​2012-2981.PubMed
65.
Zurück zum Zitat Kosmiski LA, Sage-El A, Kealey EH, Bessesen DH. Brown fat activity is not apparent in subjects with HIV lipodystrophy and increased resting energy expenditure. Obesity (Silver Spring). 2011;19:2096–8. doi:10.1038/oby.2011.231. Kosmiski LA, Sage-El A, Kealey EH, Bessesen DH. Brown fat activity is not apparent in subjects with HIV lipodystrophy and increased resting energy expenditure. Obesity (Silver Spring). 2011;19:2096–8. doi:10.​1038/​oby.​2011.​231.
66.
Zurück zum Zitat Torriani M, Zanni MV, Fitch K, Stavrou E, Bredella MA, Lim R, et al. Increased FDG uptake in association with reduced extremity fat in HIV patients. Antivir Ther. 2013;18:243–8. doi:10.3851/IMP2420.PubMedCentralPubMed Torriani M, Zanni MV, Fitch K, Stavrou E, Bredella MA, Lim R, et al. Increased FDG uptake in association with reduced extremity fat in HIV patients. Antivir Ther. 2013;18:243–8. doi:10.​3851/​IMP2420.PubMedCentralPubMed
68.
Zurück zum Zitat Fatemi A, Item C, Stöckler-Ipsiroglu S, Ipsiroglu O, Sperl W, Patsch W, et al. Sudden infant death: no evidence for linkage to common polymorphisms in the uncoupling protein-1 and the beta3-adrenergic receptor genes. Eur J Pediatr. 2002;161:337–9. doi:10.1007/s00431-002-0940-x.PubMed Fatemi A, Item C, Stöckler-Ipsiroglu S, Ipsiroglu O, Sperl W, Patsch W, et al. Sudden infant death: no evidence for linkage to common polymorphisms in the uncoupling protein-1 and the beta3-adrenergic receptor genes. Eur J Pediatr. 2002;161:337–9. doi:10.​1007/​s00431-002-0940-x.PubMed
69.
Zurück zum Zitat Vijgen G, van Marken LW, Lichtenbelt W. Brown adipose tissue: clinical impact of a re-discovered thermogenic organ. Front Biosci (Elite Ed). 2013;5:823–33. Vijgen G, van Marken LW, Lichtenbelt W. Brown adipose tissue: clinical impact of a re-discovered thermogenic organ. Front Biosci (Elite Ed). 2013;5:823–33.
70.
Zurück zum Zitat Ichimiya H, Arakawa S, Sato T, Shimada T, Chiba M, Soma Y, et al. Involvement of brown adipose tissue in subcutaneous fat necrosis of the newborn. Dermatology. 2011;223:207–10. doi:10.1159/000331810.PubMed Ichimiya H, Arakawa S, Sato T, Shimada T, Chiba M, Soma Y, et al. Involvement of brown adipose tissue in subcutaneous fat necrosis of the newborn. Dermatology. 2011;223:207–10. doi:10.​1159/​000331810.PubMed
71.
Zurück zum Zitat Svacina S. Treatment of obese diabetics. Adv Exp Med Biol. 2012;771:459–64.PubMed Svacina S. Treatment of obese diabetics. Adv Exp Med Biol. 2012;771:459–64.PubMed
72.
Zurück zum Zitat Schwartz S, Fabricatore AN, Diamond A. Weight reduction in diabetes. Adv Exp Med Biol. 2012;771:438–58.PubMed Schwartz S, Fabricatore AN, Diamond A. Weight reduction in diabetes. Adv Exp Med Biol. 2012;771:438–58.PubMed
73.
Zurück zum Zitat Muzik O, Mangner TJ, Leonard WR, Kumar A, Janisse J, Granneman JG. 15O PET measurement of blood flow and oxygen consumption in cold-activated human brown fat. J Nucl Med. 2013;54:523–31. doi:10.2967/jnumed.112.111336.PubMed Muzik O, Mangner TJ, Leonard WR, Kumar A, Janisse J, Granneman JG. 15O PET measurement of blood flow and oxygen consumption in cold-activated human brown fat. J Nucl Med. 2013;54:523–31. doi:10.​2967/​jnumed.​112.​111336.PubMed
74.
Zurück zum Zitat Stock MJ. Thermogenesis and brown fat: relevance to human obesity. Infusionstherapie. 1989;16:282–4.PubMed Stock MJ. Thermogenesis and brown fat: relevance to human obesity. Infusionstherapie. 1989;16:282–4.PubMed
76.
Zurück zum Zitat Rothwell NJ, Stock MJ. A role for brown adipose tissue in diet-induced thermogenesis. Nature. 1979;281:31–5.PubMed Rothwell NJ, Stock MJ. A role for brown adipose tissue in diet-induced thermogenesis. Nature. 1979;281:31–5.PubMed
77.
Zurück zum Zitat Rothwell NJ, Stock MJ. Luxuskonsumption, diet-induced thermogenesis and brown fat: the case in favour. Clin Sci (Lond). 1983;64:19–23. Rothwell NJ, Stock MJ. Luxuskonsumption, diet-induced thermogenesis and brown fat: the case in favour. Clin Sci (Lond). 1983;64:19–23.
78.
Zurück zum Zitat Kim JY, Lee SS. The effects of uncoupling protein 1 and beta3-adrenergic receptor gene polymorphisms on weight loss and lipid profiles in obese women. Int J Vitam Nutr Res. 2010;80:87–96. doi:10.1024/0300-9831/a000009.PubMed Kim JY, Lee SS. The effects of uncoupling protein 1 and beta3-adrenergic receptor gene polymorphisms on weight loss and lipid profiles in obese women. Int J Vitam Nutr Res. 2010;80:87–96. doi:10.​1024/​0300-9831/​a000009.PubMed
79.
Zurück zum Zitat Kurokawa N. Association of BMI with the beta3 adrenergic receptor gene mutation: a meta-analysis. Nihon Eiseigaku Zasshi. 2011;66:42–6.PubMed Kurokawa N. Association of BMI with the beta3 adrenergic receptor gene mutation: a meta-analysis. Nihon Eiseigaku Zasshi. 2011;66:42–6.PubMed
80.
Zurück zum Zitat Feldmann HM, Golozoubova V, Cannon B, Nedergaard J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 2009;9:203–9. doi:10.1016/j.cmet.2008.12.014.PubMed Feldmann HM, Golozoubova V, Cannon B, Nedergaard J. UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 2009;9:203–9. doi:10.​1016/​j.​cmet.​2008.​12.​014.PubMed
81.
Zurück zum Zitat Lowell BB, S-Susulic V, Hamann A, Lawitts JA, Himms-Hagen J, Boyer BB, et al. Development of obesity in transgenic mice after genetic ablation of brown adipose tissue. Nature. 1993;366:740–2. doi:10.1038/366740a0. Lowell BB, S-Susulic V, Hamann A, Lawitts JA, Himms-Hagen J, Boyer BB, et al. Development of obesity in transgenic mice after genetic ablation of brown adipose tissue. Nature. 1993;366:740–2. doi:10.​1038/​366740a0.
82.
Zurück zum Zitat Bachman ES, Dhillon H, Zhang CY, Cinti S, Bianco AC, Kobilka BK, et al. betaAR signaling required for diet-induced thermogenesis and obesity resistance. Science. 2002;297:843–5. doi:10.1126/science.1073160.PubMed Bachman ES, Dhillon H, Zhang CY, Cinti S, Bianco AC, Kobilka BK, et al. betaAR signaling required for diet-induced thermogenesis and obesity resistance. Science. 2002;297:843–5. doi:10.​1126/​science.​1073160.PubMed
83.
84.
Zurück zum Zitat Kopecky J, Clarke G, Enerbäck S, Spiegelman B, Kozak LP. Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J Clin Invest. 1995;96:2914–23. doi:10.1172/JCI118363.PubMedCentralPubMed Kopecky J, Clarke G, Enerbäck S, Spiegelman B, Kozak LP. Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J Clin Invest. 1995;96:2914–23. doi:10.​1172/​JCI118363.PubMedCentralPubMed
85.
Zurück zum Zitat Ghorbani M, Claus TH, Himms-Hagen J. Hypertrophy of brown adipocytes in brown and white adipose tissues and reversal of diet-induced obesity in rats treated with a beta3-adrenoceptor agonist. Biochem Pharmacol. 1997;54:121–31.PubMed Ghorbani M, Claus TH, Himms-Hagen J. Hypertrophy of brown adipocytes in brown and white adipose tissues and reversal of diet-induced obesity in rats treated with a beta3-adrenoceptor agonist. Biochem Pharmacol. 1997;54:121–31.PubMed
86.
Zurück zum Zitat Ghorbani M, Himms-Hagen J. Appearance of brown adipocytes in white adipose tissue during CL 316,243-induced reversal of obesity and diabetes in Zucker fa/fa rats. Int J Obes Relat Metab Disord. 1997;21:465–75.PubMed Ghorbani M, Himms-Hagen J. Appearance of brown adipocytes in white adipose tissue during CL 316,243-induced reversal of obesity and diabetes in Zucker fa/fa rats. Int J Obes Relat Metab Disord. 1997;21:465–75.PubMed
88.
Zurück zum Zitat Stanford KI, Middelbeek RJ, Townsend KL, An D, Nygaard EB, Hitchcox KM, et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest. 2012;123:215–23. doi:10.1172/JCI62308.PubMedCentralPubMed Stanford KI, Middelbeek RJ, Townsend KL, An D, Nygaard EB, Hitchcox KM, et al. Brown adipose tissue regulates glucose homeostasis and insulin sensitivity. J Clin Invest. 2012;123:215–23. doi:10.​1172/​JCI62308.PubMedCentralPubMed
89.
Zurück zum Zitat Lee P, Zhao JT, Swarbrick MM, Gracie G, Bova R, Greenfield JR, et al. High prevalence of brown adipose tissue in adult humans. J Clin Endocrinol Metab. 2011;96:2450–5. doi:10.1210/jc.2011-0487.PubMed Lee P, Zhao JT, Swarbrick MM, Gracie G, Bova R, Greenfield JR, et al. High prevalence of brown adipose tissue in adult humans. J Clin Endocrinol Metab. 2011;96:2450–5. doi:10.​1210/​jc.​2011-0487.PubMed
90.
Zurück zum Zitat Orava J, Nuutila P, Noponen T, Parkkola R, Viljanen T, Enerbäck S, et al. Blunted metabolic responses to cold and insulin stimulation in brown adipose tissue of obese humans. Obesity (Silver Spring). 2013. doi:10.1002/oby.20456. Orava J, Nuutila P, Noponen T, Parkkola R, Viljanen T, Enerbäck S, et al. Blunted metabolic responses to cold and insulin stimulation in brown adipose tissue of obese humans. Obesity (Silver Spring). 2013. doi:10.​1002/​oby.​20456.
91.
Zurück zum Zitat Ma SW, Foster DO. Uptake of glucose and release of fatty acids and glycerol by rat brown adipose tissue in vivo. Can J Physiol Pharmacol. 1986;64:609–14.PubMed Ma SW, Foster DO. Uptake of glucose and release of fatty acids and glycerol by rat brown adipose tissue in vivo. Can J Physiol Pharmacol. 1986;64:609–14.PubMed
92.
Zurück zum Zitat Orava J, Nuutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T, et al. Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab. 2011;14:272–9. doi:10.1016/j.cmet.2011.06.012.PubMed Orava J, Nuutila P, Lidell ME, Oikonen V, Noponen T, Viljanen T, et al. Different metabolic responses of human brown adipose tissue to activation by cold and insulin. Cell Metab. 2011;14:272–9. doi:10.​1016/​j.​cmet.​2011.​06.​012.PubMed
93.
Zurück zum Zitat Lean ME, Murgatroyd PR, Rothnie I, Reid IW, Harvey R. Metabolic and thyroidal responses to mild cold are abnormal in obese diabetic women. Clin Endocrinol (Oxf). 1988;28:665–73. Lean ME, Murgatroyd PR, Rothnie I, Reid IW, Harvey R. Metabolic and thyroidal responses to mild cold are abnormal in obese diabetic women. Clin Endocrinol (Oxf). 1988;28:665–73.
94.
Zurück zum Zitat Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, et al. Definition and classification of cancer cachexia: an international consensus. Lancet Oncol. 2011;12:489–95. doi:10.1016/S1470-2045(10)70218-7.PubMed Fearon K, Strasser F, Anker SD, Bosaeus I, Bruera E, Fainsinger RL, et al. Definition and classification of cancer cachexia: an international consensus. Lancet Oncol. 2011;12:489–95. doi:10.​1016/​S1470-2045(10)70218-7.PubMed
95.
Zurück zum Zitat Martin L, Birdsell L, Macdonald N, Reiman T, Clandinin MT, McCargar LJ, et al. Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol. 2013;31:1539–47. doi:10.1200/JCO.2012.45.2722.PubMed Martin L, Birdsell L, Macdonald N, Reiman T, Clandinin MT, McCargar LJ, et al. Cancer cachexia in the age of obesity: skeletal muscle depletion is a powerful prognostic factor, independent of body mass index. J Clin Oncol. 2013;31:1539–47. doi:10.​1200/​JCO.​2012.​45.​2722.PubMed
96.
Zurück zum Zitat Shellock FG, Riedinger MS, Fishbein MC. Brown adipose tissue in cancer patients: possible cause of cancer-induced cachexia. J Cancer Res Clin Oncol. 1986;111:82–5.PubMed Shellock FG, Riedinger MS, Fishbein MC. Brown adipose tissue in cancer patients: possible cause of cancer-induced cachexia. J Cancer Res Clin Oncol. 1986;111:82–5.PubMed
97.
Zurück zum Zitat Bancroft LW, Kransdorf MJ, Peterson JJ, O’Connor MI. Benign fatty tumors: classification, clinical course, imaging appearance, and treatment. Skeletal Radiol. 2006;35:719–33. doi:10.1007/s00256-006-0189-y.PubMed Bancroft LW, Kransdorf MJ, Peterson JJ, O’Connor MI. Benign fatty tumors: classification, clinical course, imaging appearance, and treatment. Skeletal Radiol. 2006;35:719–33. doi:10.​1007/​s00256-006-0189-y.PubMed
98.
Zurück zum Zitat Craig WD, Fanburg-Smith JC, Henry LR, Guerrero R, Barton JH. Fat-containing lesions of the retroperitoneum: radiologic-pathologic correlation. Radiographics. 2009;29:261–90. doi:10.1148/rg.291085203.PubMed Craig WD, Fanburg-Smith JC, Henry LR, Guerrero R, Barton JH. Fat-containing lesions of the retroperitoneum: radiologic-pathologic correlation. Radiographics. 2009;29:261–90. doi:10.​1148/​rg.​291085203.PubMed
99.
Zurück zum Zitat Essadel A, Bensaid Alaoui S, Mssrouri R, Mohammadine E, Benamr S, Taghy A, et al. Hibernoma: a rare case of massive weight loss. Ann Chir. 2002;127:215–7.PubMed Essadel A, Bensaid Alaoui S, Mssrouri R, Mohammadine E, Benamr S, Taghy A, et al. Hibernoma: a rare case of massive weight loss. Ann Chir. 2002;127:215–7.PubMed
101.
Zurück zum Zitat Muliawati Y, Haroen H, Rotty LW. Cancer anorexia - cachexia syndrome. Acta Med Indones. 2012;44:154–62.PubMed Muliawati Y, Haroen H, Rotty LW. Cancer anorexia - cachexia syndrome. Acta Med Indones. 2012;44:154–62.PubMed
102.
Zurück zum Zitat Baracos VE, Reiman T, Mourtzakis M, Gioulbasanis I, Antoun S. Body composition in patients with non-small cell lung cancer: a contemporary view of cancer cachexia with the use of computed tomography image analysis. Am J Clin Nutr. 2010;91:1133S–7S. doi:10.3945/ajcn.2010.28608C.PubMed Baracos VE, Reiman T, Mourtzakis M, Gioulbasanis I, Antoun S. Body composition in patients with non-small cell lung cancer: a contemporary view of cancer cachexia with the use of computed tomography image analysis. Am J Clin Nutr. 2010;91:1133S–7S. doi:10.​3945/​ajcn.​2010.​28608C.PubMed
104.
Zurück zum Zitat Bachmann J, Ketterer K, Marsch C, Fechtner K, Krakowski-Roosen H, Büchler MW, et al. Pancreatic cancer related cachexia: influence on metabolism and correlation to weight loss and pulmonary function. BMC Cancer. 2009;9:255. doi:10.1186/1471-2407-9-255.PubMedCentralPubMed Bachmann J, Ketterer K, Marsch C, Fechtner K, Krakowski-Roosen H, Büchler MW, et al. Pancreatic cancer related cachexia: influence on metabolism and correlation to weight loss and pulmonary function. BMC Cancer. 2009;9:255. doi:10.​1186/​1471-2407-9-255.PubMedCentralPubMed
106.
Zurück zum Zitat George J, Cannon T, Lai V, Richey L, Zanation A, Hayes DN, et al. Cancer cachexia syndrome in head and neck cancer patients: part II. Pathophysiology. Head Neck. 2007;29:497–507. doi:10.1002/hed.20630.PubMed George J, Cannon T, Lai V, Richey L, Zanation A, Hayes DN, et al. Cancer cachexia syndrome in head and neck cancer patients: part II. Pathophysiology. Head Neck. 2007;29:497–507. doi:10.​1002/​hed.​20630.PubMed
107.
Zurück zum Zitat Petrák O, Haluzíková D, Kaválková P, Štrauch B, Rosa J, Holaj R, et al. Changes in energy metabolism in pheochromocytoma. J Clin Endocrinol Metab. 2013;98:1651–8. doi:10.1210/jc.2012-3625.PubMed Petrák O, Haluzíková D, Kaválková P, Štrauch B, Rosa J, Holaj R, et al. Changes in energy metabolism in pheochromocytoma. J Clin Endocrinol Metab. 2013;98:1651–8. doi:10.​1210/​jc.​2012-3625.PubMed
108.
Zurück zum Zitat Nguyen-Martin MA, Hammer GD. Pheochromocytoma: an update on risk groups, diagnosis, and management. Hosp Physician. 2006;42:17–24. Nguyen-Martin MA, Hammer GD. Pheochromocytoma: an update on risk groups, diagnosis, and management. Hosp Physician. 2006;42:17–24.
109.
Zurück zum Zitat Salpeter SR, Malter DS, Luo EJ, Lin AY, Stuart B. Systematic review of cancer presentations with a median survival of six months or less. J Palliat Med. 2011;15:175–85. doi:10.1089/jpm.2011.0192.PubMed Salpeter SR, Malter DS, Luo EJ, Lin AY, Stuart B. Systematic review of cancer presentations with a median survival of six months or less. J Palliat Med. 2011;15:175–85. doi:10.​1089/​jpm.​2011.​0192.PubMed
110.
Zurück zum Zitat Gilsanz V, Hu HH, Smith ML, Goodarzian F, Carcich SL, Warburton NM, et al. The depiction of brown adipose tissue is related to disease status in pediatric patients with lymphoma. AJR Am J Roentgenol. 2012;198:909–13. doi:10.2214/AJR.11.7488.PubMed Gilsanz V, Hu HH, Smith ML, Goodarzian F, Carcich SL, Warburton NM, et al. The depiction of brown adipose tissue is related to disease status in pediatric patients with lymphoma. AJR Am J Roentgenol. 2012;198:909–13. doi:10.​2214/​AJR.​11.​7488.PubMed
111.
Zurück zum Zitat Vijgen GH, Bouvy ND, Smidt M, Kooreman L, Schaart G, van Marken Lichtenbelt W. Hibernoma with metabolic impact? BMJ Case Rep. 2012;2012. doi: 10.1136/bcr-2012-006325. Vijgen GH, Bouvy ND, Smidt M, Kooreman L, Schaart G, van Marken Lichtenbelt W. Hibernoma with metabolic impact? BMJ Case Rep. 2012;2012. doi: 10.​1136/​bcr-2012-006325.
113.
Zurück zum Zitat Lean ME, James WP, Jennings G, Trayhurn P. Brown adipose tissue in patients with phaeochromocytoma. Int J Obes. 1986;10:219–27.PubMed Lean ME, James WP, Jennings G, Trayhurn P. Brown adipose tissue in patients with phaeochromocytoma. Int J Obes. 1986;10:219–27.PubMed
114.
Zurück zum Zitat Chalfant JS, Smith ML, Hu HH, Dorey FJ, Goodarzian F, Fu CH, et al. Inverse association between brown adipose tissue activation and white adipose tissue accumulation in successfully treated pediatric malignancy. Am J Clin Nutr. 2012;95:1144–9. doi:10.3945/ajcn.111.030650.PubMedCentralPubMed Chalfant JS, Smith ML, Hu HH, Dorey FJ, Goodarzian F, Fu CH, et al. Inverse association between brown adipose tissue activation and white adipose tissue accumulation in successfully treated pediatric malignancy. Am J Clin Nutr. 2012;95:1144–9. doi:10.​3945/​ajcn.​111.​030650.PubMedCentralPubMed
115.
Zurück zum Zitat Beijer E, Schoenmakers J, Vijgen G, Kessels F, Dingemans A, Schrauwen P, et al. A role of active brown adipose tissue in cancer cachexia? Oncol Rev. 2012;6:88–94. Beijer E, Schoenmakers J, Vijgen G, Kessels F, Dingemans A, Schrauwen P, et al. A role of active brown adipose tissue in cancer cachexia? Oncol Rev. 2012;6:88–94.
116.
Zurück zum Zitat Kortelainen ML. Association between cardiac pathology and fat tissue distribution in an autopsy series of men without premortem evidence of cardiovascular disease. Int J Obes Relat Metab Disord. 1996;20:245–52.PubMed Kortelainen ML. Association between cardiac pathology and fat tissue distribution in an autopsy series of men without premortem evidence of cardiovascular disease. Int J Obes Relat Metab Disord. 1996;20:245–52.PubMed
117.
Zurück zum Zitat Chang L, Milton H, Eitzman DT, Chen YE. Paradoxical roles of perivascular adipose tissue in atherosclerosis and hypertension. Circ J. 2012;77:11–8.PubMed Chang L, Milton H, Eitzman DT, Chen YE. Paradoxical roles of perivascular adipose tissue in atherosclerosis and hypertension. Circ J. 2012;77:11–8.PubMed
118.
Zurück zum Zitat Tewson TJ, Welch MJ, Raichle ME. [18F]-labeled 3-deoxy-3-fluoro-D-glucose: synthesis and preliminary biodistribution data. J Nucl Med. 1978;19:1339–45.PubMed Tewson TJ, Welch MJ, Raichle ME. [18F]-labeled 3-deoxy-3-fluoro-D-glucose: synthesis and preliminary biodistribution data. J Nucl Med. 1978;19:1339–45.PubMed
120.
Zurück zum Zitat Antar MA. Radiopharmaceuticals for studying cardiac metabolism. Int J Rad Appl Instrum B. 1990;17:103–28.PubMed Antar MA. Radiopharmaceuticals for studying cardiac metabolism. Int J Rad Appl Instrum B. 1990;17:103–28.PubMed
121.
Zurück zum Zitat Kaiser KP, Geuting B, Grossmann K, Vester E, Lösse B, Antar MA, et al. Tracer kinetics of 15-(ortho-123/131I-phenyl)-pentadecanoic acid (oPPA) and 15-(para-123/131I-phenyl)-pentadecanoic acid (pPPA) in animals and man. J Nucl Med. 1990;31:1608–16.PubMed Kaiser KP, Geuting B, Grossmann K, Vester E, Lösse B, Antar MA, et al. Tracer kinetics of 15-(ortho-123/131I-phenyl)-pentadecanoic acid (oPPA) and 15-(para-123/131I-phenyl)-pentadecanoic acid (pPPA) in animals and man. J Nucl Med. 1990;31:1608–16.PubMed
123.
Zurück zum Zitat DeGrado TR, Coenen HH, Stocklin G. 14(R,S)-[18F]fluoro-6-thia-heptadecanoic acid (FTHA): evaluation in mouse of a new probe of myocardial utilization of long chain fatty acids. J Nucl Med. 1991;32:1888–96.PubMed DeGrado TR, Coenen HH, Stocklin G. 14(R,S)-[18F]fluoro-6-thia-heptadecanoic acid (FTHA): evaluation in mouse of a new probe of myocardial utilization of long chain fatty acids. J Nucl Med. 1991;32:1888–96.PubMed
124.
Zurück zum Zitat Ci X, Frisch F, Lavoie F, Germain P, Lecomte R, van Lier JE, et al. The effect of insulin on the intracellular distribution of 14(R,S)-[18F]fluoro-6-thia-heptadecanoic acid in rats. Mol Imaging Biol. 2006;8:237–44. doi:10.1007/s11307-006-0042-7.PubMed Ci X, Frisch F, Lavoie F, Germain P, Lecomte R, van Lier JE, et al. The effect of insulin on the intracellular distribution of 14(R,S)-[18F]fluoro-6-thia-heptadecanoic acid in rats. Mol Imaging Biol. 2006;8:237–44. doi:10.​1007/​s11307-006-0042-7.PubMed
128.
Zurück zum Zitat Sun KT, Yeatman LA, Buxton DB, Chen K, Johnson JA, Huang SC, et al. Simultaneous measurement of myocardial oxygen consumption and blood flow using [1-carbon-11]acetate. J Nucl Med. 1998;39:272–80.PubMed Sun KT, Yeatman LA, Buxton DB, Chen K, Johnson JA, Huang SC, et al. Simultaneous measurement of myocardial oxygen consumption and blood flow using [1-carbon-11]acetate. J Nucl Med. 1998;39:272–80.PubMed
129.
Zurück zum Zitat Czernin J, Porenta G, Brunken R, Krivokapich J, Chen K, Bennett R, et al. Regional blood flow, oxidative metabolism, and glucose utilization in patients with recent myocardial infarction. Circulation. 1993;88:884–95.PubMed Czernin J, Porenta G, Brunken R, Krivokapich J, Chen K, Bennett R, et al. Regional blood flow, oxidative metabolism, and glucose utilization in patients with recent myocardial infarction. Circulation. 1993;88:884–95.PubMed
131.
134.
Zurück zum Zitat Fukuchi K, Ono Y, Nakahata Y, Okada Y, Hayashida K, Ishida Y. Visualization of interscapular brown adipose tissue using (99m)Tc-tetrofosmin in pediatric patients. J Nucl Med. 2003;44:1582–5.PubMed Fukuchi K, Ono Y, Nakahata Y, Okada Y, Hayashida K, Ishida Y. Visualization of interscapular brown adipose tissue using (99m)Tc-tetrofosmin in pediatric patients. J Nucl Med. 2003;44:1582–5.PubMed
135.
Zurück zum Zitat Baba S, Engles JM, Huso DL, Ishimori T, Wahl RL. Comparison of uptake of multiple clinical radiotracers into brown adipose tissue under cold-stimulated and nonstimulated conditions. J Nucl Med. 2007;48:1715–23. doi:10.2967/jnumed.107.041715.PubMed Baba S, Engles JM, Huso DL, Ishimori T, Wahl RL. Comparison of uptake of multiple clinical radiotracers into brown adipose tissue under cold-stimulated and nonstimulated conditions. J Nucl Med. 2007;48:1715–23. doi:10.​2967/​jnumed.​107.​041715.PubMed
136.
Zurück zum Zitat Kyparos D, Arsos G, Georga S, Petridou A, Kyparos A, Papageorgiou E, et al. Assessment of brown adipose tissue activity in rats by 99mTc-sestamibi uptake. Physiol Res. 2006;55:653–9.PubMed Kyparos D, Arsos G, Georga S, Petridou A, Kyparos A, Papageorgiou E, et al. Assessment of brown adipose tissue activity in rats by 99mTc-sestamibi uptake. Physiol Res. 2006;55:653–9.PubMed
137.
138.
Zurück zum Zitat Madar I, Ravert H, Dipaula A, Du Y, Dannals RF, Becker L. Assessment of severity of coronary artery stenosis in a canine model using the PET agent 18F-fluorobenzyl triphenyl phosphonium: comparison with 99mTc-tetrofosmin. J Nucl Med. 2007;48:1021–30. doi:10.2967/jnumed.106.038778.PubMed Madar I, Ravert H, Dipaula A, Du Y, Dannals RF, Becker L. Assessment of severity of coronary artery stenosis in a canine model using the PET agent 18F-fluorobenzyl triphenyl phosphonium: comparison with 99mTc-tetrofosmin. J Nucl Med. 2007;48:1021–30. doi:10.​2967/​jnumed.​106.​038778.PubMed
139.
Zurück zum Zitat Madar I, Ravert H, Nelkin B, Abro M, Pomper M, Dannals R, et al. Characterization of membrane potential-dependent uptake of the novel PET tracer 18F-fluorobenzyl triphenylphosphonium cation. Eur J Nucl Med Mol Imaging. 2007;34:2057–65. doi:10.1007/s00259-007-0500-8.PubMed Madar I, Ravert H, Nelkin B, Abro M, Pomper M, Dannals R, et al. Characterization of membrane potential-dependent uptake of the novel PET tracer 18F-fluorobenzyl triphenylphosphonium cation. Eur J Nucl Med Mol Imaging. 2007;34:2057–65. doi:10.​1007/​s00259-007-0500-8.PubMed
140.
Zurück zum Zitat Hadi M, Chen CC, Whatley M, Pacak K, Carrasquillo JA. Brown fat imaging with (18)F-6-fluorodopamine PET/CT, (18)F-FDG PET/CT, and (123)I-MIBG SPECT: a study of patients being evaluated for pheochromocytoma. J Nucl Med. 2007;48:1077–83. doi:10.2967/jnumed.106.035915.PubMed Hadi M, Chen CC, Whatley M, Pacak K, Carrasquillo JA. Brown fat imaging with (18)F-6-fluorodopamine PET/CT, (18)F-FDG PET/CT, and (123)I-MIBG SPECT: a study of patients being evaluated for pheochromocytoma. J Nucl Med. 2007;48:1077–83. doi:10.​2967/​jnumed.​106.​035915.PubMed
141.
Zurück zum Zitat Okuyama C, Sakane N, Yoshida T, Shima K, Kurosawa H, Kumamoto K, et al. (123)I- or (125)I-metaiodobenzylguanidine visualization of brown adipose tissue. J Nucl Med. 2002;43:1234–40.PubMed Okuyama C, Sakane N, Yoshida T, Shima K, Kurosawa H, Kumamoto K, et al. (123)I- or (125)I-metaiodobenzylguanidine visualization of brown adipose tissue. J Nucl Med. 2002;43:1234–40.PubMed
142.
Zurück zum Zitat Okuyama C, Ushijima Y, Kubota T, Yoshida T, Nakai T, Kobayashi K, et al. 123I-Metaiodobenzylguanidine uptake in the nape of the neck of children: likely visualization of brown adipose tissue. J Nucl Med. 2003;44:1421–5.PubMed Okuyama C, Ushijima Y, Kubota T, Yoshida T, Nakai T, Kobayashi K, et al. 123I-Metaiodobenzylguanidine uptake in the nape of the neck of children: likely visualization of brown adipose tissue. J Nucl Med. 2003;44:1421–5.PubMed
143.
Zurück zum Zitat Vosselman MJ, van der Lans AA, Brans B, Wierts R, van Baak MA, Schrauwen P, et al. Systemic beta-adrenergic stimulation of thermogenesis is not accompanied by brown adipose tissue activity in humans. Diabetes. 2012;61:3106–13. doi:10.2337/db12-0288.PubMedCentralPubMed Vosselman MJ, van der Lans AA, Brans B, Wierts R, van Baak MA, Schrauwen P, et al. Systemic beta-adrenergic stimulation of thermogenesis is not accompanied by brown adipose tissue activity in humans. Diabetes. 2012;61:3106–13. doi:10.​2337/​db12-0288.PubMedCentralPubMed
144.
Zurück zum Zitat Osculati F, Leclercq F, Sbarbati A, Zancanaro C, Cinti S, Antonakis K. Morphological identification of brown adipose tissue by magnetic resonance imaging in the rat. Eur J Radiol. 1989;9:112–4.PubMed Osculati F, Leclercq F, Sbarbati A, Zancanaro C, Cinti S, Antonakis K. Morphological identification of brown adipose tissue by magnetic resonance imaging in the rat. Eur J Radiol. 1989;9:112–4.PubMed
145.
Zurück zum Zitat Osculati F, Sbarbati A, Leclercq F, Zancanaro C, Accordini C, Antonakis K, et al. The correlation between magnetic resonance imaging and ultrastructural patterns of brown adipose tissue. J Submicrosc Cytol Pathol. 1991;23:167–74.PubMed Osculati F, Sbarbati A, Leclercq F, Zancanaro C, Accordini C, Antonakis K, et al. The correlation between magnetic resonance imaging and ultrastructural patterns of brown adipose tissue. J Submicrosc Cytol Pathol. 1991;23:167–74.PubMed
146.
Zurück zum Zitat Sbarbati A, Baldassarri AM, Zancanaro C, Boicelli A, Osculati F. In vivo morphometry and functional morphology of brown adipose tissue by magnetic resonance imaging. Anat Rec. 1991;231:293–7. doi:10.1002/ar.1092310302.PubMed Sbarbati A, Baldassarri AM, Zancanaro C, Boicelli A, Osculati F. In vivo morphometry and functional morphology of brown adipose tissue by magnetic resonance imaging. Anat Rec. 1991;231:293–7. doi:10.​1002/​ar.​1092310302.PubMed
147.
Zurück zum Zitat Lunati E, Marzola P, Nicolato E, Fedrigo M, Villa M, Sbarbati A. In vivo quantitative lipidic map of brown adipose tissue by chemical shift imaging at 4.7 Tesla. J Lipid Res. 1999;40:1395–400.PubMed Lunati E, Marzola P, Nicolato E, Fedrigo M, Villa M, Sbarbati A. In vivo quantitative lipidic map of brown adipose tissue by chemical shift imaging at 4.7 Tesla. J Lipid Res. 1999;40:1395–400.PubMed
148.
Zurück zum Zitat Sbarbati A, Guerrini U, Marzola P, Asperio R, Osculati F. Chemical shift imaging at 4.7 tesla of brown adipose tissue. J Lipid Res. 1997;38:343–7.PubMed Sbarbati A, Guerrini U, Marzola P, Asperio R, Osculati F. Chemical shift imaging at 4.7 tesla of brown adipose tissue. J Lipid Res. 1997;38:343–7.PubMed
151.
Zurück zum Zitat Peng XG, Ju S, Fang F, Wang Y, Fang K, Cui X, et al. Comparison of brown and white adipose tissue fat fractions in ob, seipin, and Fsp27 gene knockout mice by chemical shift-selective imaging and (1)H-MR spectroscopy. Am J Physiol Endocrinol Metab. 2013;304:E160–7. doi:10.1152/ajpendo.00401.2012.PubMed Peng XG, Ju S, Fang F, Wang Y, Fang K, Cui X, et al. Comparison of brown and white adipose tissue fat fractions in ob, seipin, and Fsp27 gene knockout mice by chemical shift-selective imaging and (1)H-MR spectroscopy. Am J Physiol Endocrinol Metab. 2013;304:E160–7. doi:10.​1152/​ajpendo.​00401.​2012.PubMed
152.
Zurück zum Zitat van Rooijen BD, van der Lans AA, Brans B, Wildberger JE, Mottaghy FM, Schrauwen P, et al. 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. 2013;48:708–14. doi:10.1097/RLI.0b013e31829363b8. van Rooijen BD, van der Lans AA, Brans B, Wildberger JE, Mottaghy FM, Schrauwen P, et al. 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. 2013;48:708–14. doi:10.​1097/​RLI.​0b013e31829363b8​.
153.
Zurück zum Zitat Foster DO, Frydman ML. Tissue distribution of cold-induced thermogenesis in conscious warm- or cold-acclimated rats reevaluated from changes in tissue blood flow: the dominant role of brown adipose tissue in the replacement of shivering by nonshivering thermogenesis. Can J Physiol Pharmacol. 1979;57:257–70.PubMed Foster DO, Frydman ML. Tissue distribution of cold-induced thermogenesis in conscious warm- or cold-acclimated rats reevaluated from changes in tissue blood flow: the dominant role of brown adipose tissue in the replacement of shivering by nonshivering thermogenesis. Can J Physiol Pharmacol. 1979;57:257–70.PubMed
154.
Zurück zum Zitat Chen YI, Cypess AM, Sass CA, Brownell AL, Jokivarsi KT, Kahn CR, et al. Anatomical and functional assessment of brown adipose tissue by magnetic resonance imaging. Obesity (Silver Spring). 2012;20:1519–26. doi:10.1038/oby.2012.22. Chen YI, Cypess AM, Sass CA, Brownell AL, Jokivarsi KT, Kahn CR, et al. Anatomical and functional assessment of brown adipose tissue by magnetic resonance imaging. Obesity (Silver Spring). 2012;20:1519–26. doi:10.​1038/​oby.​2012.​22.
157.
Zurück zum Zitat Hu HH, Gilsanz V. Developments in the imaging of brown adipose tissue and its associations with muscle, puberty, and health in children. Front Endocrinol (Lausanne). 2011;2:33. doi:10.3389/fendo.2011.00033. Hu HH, Gilsanz V. Developments in the imaging of brown adipose tissue and its associations with muscle, puberty, and health in children. Front Endocrinol (Lausanne). 2011;2:33. doi:10.​3389/​fendo.​2011.​00033.
159.
Zurück zum Zitat Ruth M, Wellman T, Mercier G, Szabo T, Apovian C. An automated algorithm to identify and quantify brown adipose tissue in human (18)F-FDG-PET/CT scans. Obesity (Silver Spring). 2013;21:1554–60. doi:10.1002/oby.20315. Ruth M, Wellman T, Mercier G, Szabo T, Apovian C. An automated algorithm to identify and quantify brown adipose tissue in human (18)F-FDG-PET/CT scans. Obesity (Silver Spring). 2013;21:1554–60. doi:10.​1002/​oby.​20315.
161.
Zurück zum Zitat Patlak CS, Blasberg RG. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. Generalizations. J Cereb Blood Flow Metab. 1985;5:584–90. doi:10.1038/jcbfm.1985.87.PubMed Patlak CS, Blasberg RG. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. Generalizations. J Cereb Blood Flow Metab. 1985;5:584–90. doi:10.​1038/​jcbfm.​1985.​87.PubMed
162.
Zurück zum Zitat Sundaram SK, Freedman NM, Carrasquillo JA, Carson JM, Whatley M, Libutti SK, et al. Simplified kinetic analysis of tumor 18F-FDG uptake: a dynamic approach. J Nucl Med. 2004;45:1328–33.PubMed Sundaram SK, Freedman NM, Carrasquillo JA, Carson JM, Whatley M, Libutti SK, et al. Simplified kinetic analysis of tumor 18F-FDG uptake: a dynamic approach. J Nucl Med. 2004;45:1328–33.PubMed
163.
Zurück zum Zitat Fox PT, Raichle ME, Mintun MA, Dence C. Nonoxidative glucose consumption during focal physiologic neural activity. Science. 1988;241:462–4.PubMed Fox PT, Raichle ME, Mintun MA, Dence C. Nonoxidative glucose consumption during focal physiologic neural activity. Science. 1988;241:462–4.PubMed
164.
165.
Zurück zum Zitat Mintun MA, Raichle ME, Martin WR, Herscovitch P. Brain oxygen utilization measured with O-15 radiotracers and positron emission tomography. J Nucl Med. 1984;25:177–87.PubMed Mintun MA, Raichle ME, Martin WR, Herscovitch P. Brain oxygen utilization measured with O-15 radiotracers and positron emission tomography. J Nucl Med. 1984;25:177–87.PubMed
166.
Zurück zum Zitat Hattori N, Bergsneider M, Wu HM, Glenn TC, Vespa PM, Hovda DA, et al. Accuracy of a method using short inhalation of (15)O-O(2) for measuring cerebral oxygen extraction fraction with PET in healthy humans. J Nucl Med. 2004;45:765–70.PubMed Hattori N, Bergsneider M, Wu HM, Glenn TC, Vespa PM, Hovda DA, et al. Accuracy of a method using short inhalation of (15)O-O(2) for measuring cerebral oxygen extraction fraction with PET in healthy humans. J Nucl Med. 2004;45:765–70.PubMed
167.
168.
Zurück zum Zitat Raichle ME, Welch MJ, Grubb Jr RL, Higgins CS, Ter-Pogossian MM, Larson KB. Measurement of regional substrate utilization rates by emission tomography. Science. 1978;199:986–7.PubMed Raichle ME, Welch MJ, Grubb Jr RL, Higgins CS, Ter-Pogossian MM, Larson KB. Measurement of regional substrate utilization rates by emission tomography. Science. 1978;199:986–7.PubMed
Metadaten
Titel
Molecular imaging of brown adipose tissue in health and disease
verfasst von
Matthias Bauwens
Roel Wierts
Bart van Royen
Jan Bucerius
Walter Backes
Felix Mottaghy
Boudewijn Brans
Publikationsdatum
01.04.2014
Verlag
Springer Berlin Heidelberg
Erschienen in
European Journal of Nuclear Medicine and Molecular Imaging / Ausgabe 4/2014
Print ISSN: 1619-7070
Elektronische ISSN: 1619-7089
DOI
https://doi.org/10.1007/s00259-013-2611-8

Weitere Artikel der Ausgabe 4/2014

European Journal of Nuclear Medicine and Molecular Imaging 4/2014 Zur Ausgabe