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Regional Variation in Skeletal Muscle and Adipose Tissue FDG Uptake Using PET/CT and Their Relation to BMI

Rationale and Objectives

Skeletal muscle metabolism is a primary contributor to whole-body energy expenditure. Currently, methods to measure changes in skeletal muscle metabolism in vivo are limited. Our objectives were to characterize the regional variation in skeletal muscle and adipose tissue (AT) FDG uptake as a surrogate for glycolytic metabolism using 18 F-2-fluorodeoxyglucose (FDG)-positron emission tomography (PET)/computed tomography (CT) in healthy men and to correlate these findings to body mass index (BMI).

Materials and Methods

Eighteen healthy men were enrolled and underwent FDG-PET/CT. The mean standardized uptake value of 14 skeletal muscles and two AT regions was measured and linear regression analysis was performed to identify metabolic predictors of BMI.

Results

FDG-PET/CT reliably detected changes in skeletal muscle and AT depot metabolic activity based on location. The most metabolically active muscles were those used for posture and breathing, which have the highest percentage of reported type I muscle myofiber content. Visceral AT tended to have a higher FDG uptake than subcutaneous AT. The mean standardized uptake value of VAT, pectoralis major, and gluteus maximus muscles accounted for 64% of the variance in BMI.

Conclusions

FDG-PET/CT can be used to quantify the regional variation in glucose metabolism of multiple skeletal muscle groups and AT depots.

Introduction

Body mass is maintained by balancing changes in energy intake with energy expenditure. Skeletal muscle is a primary contributor to energy expenditure because of the substantial amount of energy used to maintain posture and to mediate locomotion. For example, skeletal muscle can account for up to 90% of the whole-body energy usage during physical activity . Skeletal muscle generates energy to power muscle contraction mostly via oxidation of glucose. Slow twitch (type I) muscle fibers are rich in mitochondria, rely on oxidative metabolism, and are resistant to fatigue, whereas fast twitch (type II) fibers more readily fatigue and contain more glycolytic enzymes.

Skeletal muscle metabolism is difficult to measure in vivo. Estimates can be made using blood gas exchange, indirect calorimetry, or serum metabolites such as glucose and lactate, but direct nutrient uptake is not routinely measured. Muscle biopsies can be done; however, these biopsies are invasive and only one skeletal muscle is usually assessed (most commonly the vastus lateralis [VL]).

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Materials and Methods

Study Sample

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FDG-PET/CT Image Acquisition

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FDG-PET/CT Image Analysis

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Figure 1, Representative axial low-dose computed tomography images from positron emission tomography/computed tomography showing specific muscles and adipose tissues that were assessed in this study. The SM, PM, Int, SA, ES, PS, RA, IO, GM, RF, AM, VL, S, and MG muscles, as well as the anterior abdominal SAT and the retroperitoneal VAT are depicted. AM, adductor magnus; ES, erector spinae; GM, gluteus maximus; Int, intercostal; IO, internal oblique; MG, medial gastrocnemius; PM, pectoralis major; PS, psoas; RA, rectus abdominis; RF, rectus femoris; S, soleus; SA, serratus anterior; SAT, subcutaneous adipose tissue; SM, sternocleidomastoid; VAT, visceral adipose tissue; VL, vastus lateralis.

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Data Analysis

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Results

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TABLE 1

Variation in Skeletal Muscle and Adipose SUV mean

SUV mean P Value Int 0.68 ± 0.02 — SM 0.67 ± 0.02 0.824 ES 0.67 ± 0.02 0.824 S 0.66 ± 0.03 0.606 SA 0.63 ± 0.02 0.029 GM 0.59 ± 0.02 0.005 IO 0.57 ± 0.02 0.000 MG 0.57 ± 0.03 0.002 PS 0.56 ± 0.02 0.000 PM 0.51 ± 0.02 0.000 RF 0.51 ± 0.02 0.000 AM 0.49 ± 0.02 0.000 VL 0.48 ± 0.02 0.000 RA 0.46 ± 0.02 0.000 SAT 0.24 ± 0.03 — VAT 0.30 ± 0.02 0.058

AM, adductor magnus; ES, erector spinae; GM, gluteus maximus; Int, intercostal; IO, internal oblique; MG, medial gastrocnemius; PM, pectoralis major; PS, psoas; RA, rectus abdominis; RF, rectus femoris; S, soleus; SA, serratus anterior; SAT, subcutaneous adipose tissue; SEM, standard error of the mean; SM, sternocleidomastoid; SUV mean , standardized uptake value; VAT, visceral adipose tissue; VL, vastus lateralis.

Data are mean SUV mean ± SEM for Int, SM, ES, S, SA, GM, IO, MG, PS, PM, RF, AM, VL, and RA muscles, as well as for SAT and VAT. Comparisons were made by Student t test using Int as a reference for muscles and SAT as a reference for adipose tissue depots.

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Figure 2, Skeletal muscle metabolism in terms of mean standardized uptake value measured on 18 F-2-fluorodeoxyglucose-positron emission tomography/computed tomography vs skeletal muscle fiber composition reported as the percentage of type I fibers. The RF, VL, MG, RA, GM, ES, and S muscles are displayed because fiber composition data were freely available. The Pearson r correlation value and the two-tailed P value are presented on the graph. ES, erector spinae; GM, gluteus maximus; MG, medial gastrocnemius; RA, rectus abdominis; RF, rectus femoris; S, soleus; VL, vastus lateralis.

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TABLE 2

Relationship of BMI to FDG-PET Tissue Metabolic Activity

Variable Pearson r Correlation β_b_ PM GM VAT BMI PM 0.149 −0.214 0.596 ** 15.198 ** 0.472 GM −0.331 0.517 * 8.922 0.332 VAT −0.556 * −7.749 −0.344 Intercept = 9.065R 2 = 0.64 **

BMI, body mass index; FDG, 18 F-2-fluorodeoxyglucose; GM, gluteus maximus; PET, positron emission tomography; PM, pectoralis major; VAT, visceral adipose tissue.

Pearson correlation values from a univariate analysis among independent and dependent variables (left) and the results of multivariate linear regression (right) for BMI based on independent variables: PM, GM, and VAT. Pearson r correlation values, unstandardized (β) regression coefficients, and standardized ( b ) regression coefficients are presented. Two-tailed P values were P < 0.05 and P < 0.01.

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Discussion

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Conclusions

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References

  • 1. Zurlo F., Larson K., Bogardus C., et. al.: Skeletal muscle metabolism is a major determinant of resting energy expenditure. J Clin Invest 1990; 86: pp. 1423-1427.

  • 2. Kelley D.E., Price J.C., Cobelli C.: Assessing skeletal muscle glucose metabolism with positron emission tomography. IUBMB Life 2001; 52: pp. 279-284.

  • 3. Selberg O., Muller M.J., van den Hoff J., et. al.: Use of positron emission tomography for the assessment of skeletal muscle glucose metabolism. Nutrition 2002; 18: pp. 323-328.

  • 4. Masud M., Fujimoto T., Watanuki S., et. al.: Application of positron emission tomography in physical medicine. Mymensingh Med J 2010; 19: pp. 110-115.

  • 5. Wehrli N.E., Bural G., Houseni M., et. al.: Determination of age-related changes in structure and function of skin, adipose tissue, and skeletal muscle with computed tomography, magnetic resonance imaging, and positron emission tomography. Semin Nucl Med 2007; 37: pp. 195-205.

  • 6. Leung K.: [(18)F]Fluoro-2-deoxy-2-D-glucose. 2004 Oct 1 [updated 2005 Jan 12]. Molecular Imaging and Contrast Agent Database (MICAD) [Internet].2004-2013.National Center for Biotechnology Information (US)Bethesda (MD) Available from http://www.ncbi.nlm.nih.gov/books/NBK23335/ 20641537

  • 7. Pencek R.R., Bertoldo A., Price J., et. al.: Dose-responsive insulin regulation of glucose transport in human skeletal muscle. Am J Physiol Endocrinol Metab 2006; 290: pp. E1124-E1130.

  • 8. Oi N., Iwaya T., Itoh M., et. al.: FDG-PET imaging of lower extremity muscular activity during level walking. J Orthop Sci 2003; 8: pp. 55-61.

  • 9. Hardin D.S., Azzarelli B., Edwards J., et. al.: Mechanisms of enhanced insulin sensitivity in endurance-trained athletes: effects on blood flow and differential expression of GLUT 4 in skeletal muscles. J Clin Endocrinol Metab 1995; 80: pp. 2437-2446.

  • 10. Hardin D.S., Dominguez J.H., Garvey W.T.: Muscle group-specific regulation of GLUT 4 glucose transporters in control, diabetic, and insulin-treated diabetic rats. Metabolism 1993; 42: pp. 1310-1315.

  • 11. Henriksen E.J., Bourey R.E., Rodnick K.J., et. al.: Glucose transporter protein content and glucose transport capacity in rat skeletal muscles. Am J Physiol 1990; 259: pp. E593-E598.

  • 12. Fujimoto T., Kemppainen J., Kalliokoski K.K., et. al.: Skeletal muscle glucose uptake response to exercise in trained and untrained men. Med Sci Sports Exerc 2003; 35: pp. 777-783.

  • 13. Kemppainen J., Fujimoto T., Kalliokoski K.K., et. al.: Myocardial and skeletal muscle glucose uptake during exercise in humans. J Physiol 2002; 542: pp. 403-412.

  • 14. Pappas G.P., Olcott E.W., Drace J.E.: Imaging of skeletal muscle function using (18)FDG PET: force production, activation, and metabolism. J Appl Physiol 2001; 90: pp. 329-337.

  • 15. Masud M.M., Fujimoto T., Miyake M., et. al.: Redistribution of whole-body energy metabolism by exercise: a positron emission tomography study. Ann Nucl Med 2009; 23: pp. 81-88.

  • 16. Torigian D.A.G.-M.J., Liu X., Shofer F.S., et. al.: A study of the feasibility of FDG-PET/CT to systematically detect and quantify differential metabolic effects of chronic tobacco use in organs of the whole body—a prospective pilot study. Acad Radiol 2016;

  • 17. Johnson M.A., Polgar J., Weightman D., et. al.: Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neurol Sci 1973; 18: pp. 111-129.

  • 18. Stuart C.A., McCurry M.P., Marino A., et. al.: Slow-twitch fiber proportion in skeletal muscle correlates with insulin responsiveness. J Clin Endocrinol Metab 2013; 98: pp. 2027-2036.

  • 19. Taylor E.B., An D., Kramer H.F., et. al.: Discovery of TBC1D1 as an insulin-, AICAR-, and contraction-stimulated signaling nexus in mouse skeletal muscle. J Biol Chem 2008; 283: pp. 9787-9796.

  • 20. Gaster M., Poulsen P., Handberg A., et. al.: Direct evidence of fiber type-dependent GLUT-4 expression in human skeletal muscle. Am J Physiol Endocrinol Metab 2000; 278: pp. E910-E916.

  • 21. Gaster M., Staehr P., Beck-Nielsen H., et. al.: GLUT4 is reduced in slow muscle fibers of type 2 diabetic patients: is insulin resistance in type 2 diabetes a slow, type 1 fiber disease?. Diabetes 2001; 50: pp. 1324-1329.

  • 22. Bonen A., Tan M.H., Watson-Wright W.M.: Insulin binding and glucose uptake differences in rodent skeletal muscles. Diabetes 1981; 30: pp. 702-704.

  • 23. Webster B.A., Vigna S.R., Paquette T.: Acute exercise, epinephrine, and diabetes enhance insulin binding to skeletal muscle. Am J Physiol 1986; 250: pp. E186-E197.

  • 24. Gondoh Y., Tashiro M., Itoh M., et. al.: Evaluation of individual skeletal muscle activity by glucose uptake during pedaling exercise at different workloads using positron emission tomography. J Appl Physiol 2009; 107: pp. 599-604.

  • 25. Tashiro M., Fujimoto T., Itoh M., et. al.: 18F-FDG PET imaging of muscle activity in runners. J Nucl Med 1999; 40: pp. 70-76.

  • 26. Shimada H., Kimura Y., Lord S.R., et. al.: Comparison of regional lower limb glucose metabolism in older adults during walking. Scand J Med Sci Sports 2009; 19: pp. 389-397.

  • 27. Shimada H., Kimura Y., Suzuki T., et. al.: The use of positron emission tomography and [18F]fluorodeoxyglucose for functional imaging of muscular activity during exercise with a stride assistance system. IEEE Trans Neural Syst Rehabil Eng 2007; 15: pp. 442-448.

  • 28. Shimada H., Suzuki T., Kimura Y., et. al.: Effects of an automated stride assistance system on walking parameters and muscular glucose metabolism in elderly adults. Br J Sports Med 2008; 42: pp. 922-929.

  • 29. Virtanen K.A., Lonnroth P., Parkkola R., et. al.: Glucose uptake and perfusion in subcutaneous and visceral adipose tissue during insulin stimulation in nonobese and obese humans. J Clin Endocrinol Metab 2002; 87: pp. 3902-3910.

  • 30. Christen T., Sheikine Y., Rocha V.Z., et. al.: Increased glucose uptake in visceral versus subcutaneous adipose tissue revealed by PET imaging. JACC Cardiovasc Imag 2010; 3: pp. 843-851.

  • 31. Im H.J., Paeng J.C., Cheon G.J., et. al.: Feasibility of simultaneous 18F-FDG PET/MRI for the quantitative volumetric and metabolic measurements of abdominal fat tissues using fat segmentation. Nucl Med Commun 2016; 37: pp. 616-622.

  • 32. Ibrahim M.M.: Subcutaneous and visceral adipose tissue: structural and functional differences. Obes Rev 2010; 11: pp. 11-18.

  • 33. Wu J., Bostrom P., Sparks L.M., et. al.: Beige adipocytes are a distinct type of thermogenic fat cell in mouse and human. Cell 2012; 150: pp. 366-376.

  • 34. Oliveira A.L., Azevedo D.C., Bredella M.A., et. al.: Visceral and subcutaneous adipose tissue FDG uptake by PET/CT in metabolically healthy obese subjects. Obesity (Silver Spring) 2015; 23: pp. 286-289.

  • 35. Gheysens O., Postnov A., Deroose C.M., et. al.: Quantification, variability, and reproducibility of basal skeletal muscle glucose uptake in healthy humans using 18F-FDG PET/CT. J Nucl Med 2015; 56: pp. 1520-1526.

  • 36. Simoneau J.A., Kelley D.E.: Altered glycolytic and oxidative capacities of skeletal muscle contribute to insulin resistance in NIDDM. J Appl Physiol 1997; 83: pp. 166-171.

  • 37. Goldsmith R., Joanisse D.R., Gallagher D., et. al.: Effects of experimental weight perturbation on skeletal muscle work efficiency, fuel utilization, and biochemistry in human subjects. Am J Physiol Regul Integr Comp Physiol 2010; 298: pp. R79-R88.

  • 38. Baldwin K.M., Joanisse D.R., Haddad F., et. al.: Effects of weight loss and leptin on skeletal muscle in human subjects. Am J Physiol Regul Integr Comp Physiol 2011; 301: pp. R1259-R1266.

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