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Published in: BMC Musculoskeletal Disorders 1/2014

Open Access 01-12-2014 | Research article

Intramuscular fat in ambulant young adults with bilateral spastic cerebral palsy

Authors: Jonathan J Noble, Geoffrey D Charles-Edwards, Stephen F Keevil, Andrew P Lewis, Martin Gough, Adam P Shortland

Published in: BMC Musculoskeletal Disorders | Issue 1/2014

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Abstract

Background

It is known that individuals with bilateral spastic cerebral palsy (BSCP) have small and weak muscles. However, no studies to date have investigated intramuscular fat infiltration in this group. The objective of this study is to determine whether adults with BSCP have greater adiposity in and around their skeletal muscles than their typically developing (TD) peers as this may have significant functional and cardio-metabolic implications for this patient group.

Methods

10 young adults with BSCP (7 male, mean age 22.5 years, Gross Motor Function Classification System (GMFCS) levels I-III), and 10 TD young adults (6 male, mean age 22.8 years) took part in this study. 11 cm sections of the left leg of all subjects were imaged using multi-echo gradient echo chemical shift imaging (mDixon). Percentage intermuscular fat (IMAT), intramuscular fat (IntraMF) and a subcutaneous fat to muscle volume ratio (SF/M) were calculated.

Results

IntraMF was higher with BSCP for all muscles (p = 0.001-0.013) and was significantly different between GMFCS levels (p < 0.001), with GMFCS level III having the highest IntraMF content. IMAT was also higher with BSCP p < 0.001). No significant difference was observed in SF/M between groups.

Conclusion

Young adults with BSCP have increased intermuscular and intramuscular fat compared to their TD peers. The relationship between these findings and potential cardio-metabolic and functional sequelae are yet to be investigated.
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Literature
1.
go back to reference Lieber RL, Friden J: Functional and clinical significance of skeletal muscle architecture. Muscle Nerve. 2000, 23 (11): 1647-1666.PubMedCrossRef Lieber RL, Friden J: Functional and clinical significance of skeletal muscle architecture. Muscle Nerve. 2000, 23 (11): 1647-1666.PubMedCrossRef
2.
go back to reference Fry NR, Gough M, McNee AE, Shortland AP: Changes in the volume and length of the medial gastrocnemius after surgical recession in children with spastic diplegic cerebral palsy. J Pediatr Orthop. 2007, 27 (7): 769-774.PubMedCrossRef Fry NR, Gough M, McNee AE, Shortland AP: Changes in the volume and length of the medial gastrocnemius after surgical recession in children with spastic diplegic cerebral palsy. J Pediatr Orthop. 2007, 27 (7): 769-774.PubMedCrossRef
3.
go back to reference Oberhofer K, Stott NS, Mithraratne K, Anderson IA: Subject-specific modelling of lower limb muscles in children with cerebral palsy. Clin Biomech (Bristol, Avon). 2010, 25 (1)): 88-94.CrossRef Oberhofer K, Stott NS, Mithraratne K, Anderson IA: Subject-specific modelling of lower limb muscles in children with cerebral palsy. Clin Biomech (Bristol, Avon). 2010, 25 (1)): 88-94.CrossRef
4.
go back to reference Noble JJ, Fry NR, Lewis AP, Keevil SF, Gough M, Shortland AP: Lower limb muscle volumes in bilateral spastic cerebral palsy. Brain Dev. 2013, 36 (4): 294-300.PubMedCrossRef Noble JJ, Fry NR, Lewis AP, Keevil SF, Gough M, Shortland AP: Lower limb muscle volumes in bilateral spastic cerebral palsy. Brain Dev. 2013, 36 (4): 294-300.PubMedCrossRef
5.
go back to reference Booth CM, Cortina-Borja MJ, Theologis TN: Collagen accumulation in muscles of children with cerebral palsy and correlation with severity of spasticity. Dev Med Child Neurol. 2001, 43 (5): 314-320.PubMedCrossRef Booth CM, Cortina-Borja MJ, Theologis TN: Collagen accumulation in muscles of children with cerebral palsy and correlation with severity of spasticity. Dev Med Child Neurol. 2001, 43 (5): 314-320.PubMedCrossRef
6.
go back to reference Lieber RL, Runesson E, Einarsson F, Friden J: Inferior mechanical properties of spastic muscle bundles due to hypertrophic but compromised extracellular matrix material. Muscle Nerve. 2003, 28 (4): 464-471.PubMedCrossRef Lieber RL, Runesson E, Einarsson F, Friden J: Inferior mechanical properties of spastic muscle bundles due to hypertrophic but compromised extracellular matrix material. Muscle Nerve. 2003, 28 (4): 464-471.PubMedCrossRef
7.
go back to reference Manini TM, Clark BC, Nalls MA, Goodpaster BH, Ploutz-Snyder LL, Harris TB: Reduced physical activity increases intermuscular adipose tissue in healthy young adults. Am J Clin Nutr. 2007, 85 (2): 377-384.PubMed Manini TM, Clark BC, Nalls MA, Goodpaster BH, Ploutz-Snyder LL, Harris TB: Reduced physical activity increases intermuscular adipose tissue in healthy young adults. Am J Clin Nutr. 2007, 85 (2): 377-384.PubMed
8.
go back to reference Tuttle LJ, Sinacore DR, Cade WT, Mueller MJ: Lower physical activity is associated with higher intermuscular adipose tissue in people with type 2 diabetes and peripheral neuropathy. Phys Ther. 2011, 91 (6): 923-930.PubMedPubMedCentralCrossRef Tuttle LJ, Sinacore DR, Cade WT, Mueller MJ: Lower physical activity is associated with higher intermuscular adipose tissue in people with type 2 diabetes and peripheral neuropathy. Phys Ther. 2011, 91 (6): 923-930.PubMedPubMedCentralCrossRef
9.
go back to reference Leskinen T, Sipila S, Alen M, Cheng S, Pietilainen KH, Usenius JP, Suominen H, Kovanen V, Kainulainen H, Kaprio J, Kujala UM: Leisure-time physical activity and high-risk fat: a longitudinal population-based twin study. Int J Obes (Lond). 2009, 33 (11): 1211-1218.CrossRef Leskinen T, Sipila S, Alen M, Cheng S, Pietilainen KH, Usenius JP, Suominen H, Kovanen V, Kainulainen H, Kaprio J, Kujala UM: Leisure-time physical activity and high-risk fat: a longitudinal population-based twin study. Int J Obes (Lond). 2009, 33 (11): 1211-1218.CrossRef
10.
go back to reference Goodpaster BH, Chomentowski P, Ward BK, Rossi A, Glynn NW, Delmonico MJ, Kritchevsky SB, Pahor M, Newman AB: Effects of physical activity on strength and skeletal muscle fat infiltration in older adults: a randomized controlled trial. J Appl Physiol. 2008, 105 (5): 1498-1503.PubMedPubMedCentralCrossRef Goodpaster BH, Chomentowski P, Ward BK, Rossi A, Glynn NW, Delmonico MJ, Kritchevsky SB, Pahor M, Newman AB: Effects of physical activity on strength and skeletal muscle fat infiltration in older adults: a randomized controlled trial. J Appl Physiol. 2008, 105 (5): 1498-1503.PubMedPubMedCentralCrossRef
11.
go back to reference Gaskin CJ, Morris T: Physical activity, health-related quality of life, and psychosocial functioning of adults with cerebral palsy. J Phys Act Health. 2008, 5 (1): 146-157.PubMed Gaskin CJ, Morris T: Physical activity, health-related quality of life, and psychosocial functioning of adults with cerebral palsy. J Phys Act Health. 2008, 5 (1): 146-157.PubMed
12.
go back to reference van Eck M, Dallmeijer AJ, Beckerman H, van den Hoven PA, Voorman JM, Becher JG: Physical activity level and related factors in adolescents with cerebral palsy. Pediatr Exerc Sci. 2008, 20 (1): 95-106.PubMed van Eck M, Dallmeijer AJ, Beckerman H, van den Hoven PA, Voorman JM, Becher JG: Physical activity level and related factors in adolescents with cerebral palsy. Pediatr Exerc Sci. 2008, 20 (1): 95-106.PubMed
13.
go back to reference Hardin BJ, Campbell KS, Smith JD, Arbogast S, Smith J, Moylan JS, Reid MB: TNF-alpha acts via TNFR1 and muscle-derived oxidants to depress myofibrillar force in murine skeletal muscle. J Appl Physiol. 2008, 104 (3): 694-699.PubMedCrossRef Hardin BJ, Campbell KS, Smith JD, Arbogast S, Smith J, Moylan JS, Reid MB: TNF-alpha acts via TNFR1 and muscle-derived oxidants to depress myofibrillar force in murine skeletal muscle. J Appl Physiol. 2008, 104 (3): 694-699.PubMedCrossRef
14.
go back to reference Peterson MD, Gordon PM, Hurvitz EA: Chronic disease risk among adults with cerebral palsy: the role of premature sarcopoenia, obesity and sedentary behaviour. Obes Rev. 2012, 14 (2): 171-182.PubMedCrossRef Peterson MD, Gordon PM, Hurvitz EA: Chronic disease risk among adults with cerebral palsy: the role of premature sarcopoenia, obesity and sedentary behaviour. Obes Rev. 2012, 14 (2): 171-182.PubMedCrossRef
15.
go back to reference Elder CP, Apple DF, Bickel CS, Meyer RA, Dudley GA: Intramuscular fat and glucose tolerance after spinal cord injury–a cross-sectional study. Spinal Cord. 2004, 42 (12): 711-716.PubMedCrossRef Elder CP, Apple DF, Bickel CS, Meyer RA, Dudley GA: Intramuscular fat and glucose tolerance after spinal cord injury–a cross-sectional study. Spinal Cord. 2004, 42 (12): 711-716.PubMedCrossRef
16.
go back to reference Kovanlikaya A, Mittelman SD, Ward A, Geffner ME, Dorey F, Gilsanz V: Obesity and fat quantification in lean tissues using three-point Dixon MR imaging. Pediatr Radiol. 2005, 35 (6): 601-607.PubMedCrossRef Kovanlikaya A, Mittelman SD, Ward A, Geffner ME, Dorey F, Gilsanz V: Obesity and fat quantification in lean tissues using three-point Dixon MR imaging. Pediatr Radiol. 2005, 35 (6): 601-607.PubMedCrossRef
17.
go back to reference Strauss D, Cable W, Shavelle R: Causes of excess mortality in cerebral palsy. Dev Med Child Neurol. 1999, 41 (9): 580-585.PubMedCrossRef Strauss D, Cable W, Shavelle R: Causes of excess mortality in cerebral palsy. Dev Med Child Neurol. 1999, 41 (9): 580-585.PubMedCrossRef
18.
go back to reference Johnson DL, Miller F, Subramanian P, Modlesky CM: Adipose tissue infiltration of skeletal muscle in children with cerebral palsy. J Pediatr. 2009, 154 (5): 715-720.PubMedCrossRef Johnson DL, Miller F, Subramanian P, Modlesky CM: Adipose tissue infiltration of skeletal muscle in children with cerebral palsy. J Pediatr. 2009, 154 (5): 715-720.PubMedCrossRef
19.
go back to reference Bandini LG, Schoeller DA, Fukagawa NK, Wykes LJ, Dietz WH: Body composition and energy expenditure in adolescents with cerebral palsy or myelodysplasia. Pediatr Res. 1991, 29 (1): 70-77.PubMedCrossRef Bandini LG, Schoeller DA, Fukagawa NK, Wykes LJ, Dietz WH: Body composition and energy expenditure in adolescents with cerebral palsy or myelodysplasia. Pediatr Res. 1991, 29 (1): 70-77.PubMedCrossRef
20.
go back to reference Bauman WA: The potential metabolic consequences of cerebral palsy: inferences from the general population and persons with spinal cord injury. Dev Med Child Neurol. 2009, 51 (Suppl 4): 64-78.PubMedCrossRef Bauman WA: The potential metabolic consequences of cerebral palsy: inferences from the general population and persons with spinal cord injury. Dev Med Child Neurol. 2009, 51 (Suppl 4): 64-78.PubMedCrossRef
23.
go back to reference Karampinos DC, Baum T, Nardo L, Alizai H, Yu H, Carballido-Gamio J, Yap SP, Shimakawa A, Link TM, Majumdar S: Characterization of the regional distribution of skeletal muscle adipose tissue in type 2 diabetes using chemical shift-based water/fat separation. J Magn Reson Imaging. 2012, 35 (4): 899-907.PubMedCrossRef Karampinos DC, Baum T, Nardo L, Alizai H, Yu H, Carballido-Gamio J, Yap SP, Shimakawa A, Link TM, Majumdar S: Characterization of the regional distribution of skeletal muscle adipose tissue in type 2 diabetes using chemical shift-based water/fat separation. J Magn Reson Imaging. 2012, 35 (4): 899-907.PubMedCrossRef
24.
go back to reference Wren TA, Bluml S, Tseng-Ong L, Gilsanz V: Three-point technique of fat quantification of muscle tissue as a marker of disease progression in Duchenne muscular dystrophy: preliminary study. AJR Am J Roentgenol. 2008, 190 (1): W8-W12.PubMedCrossRef Wren TA, Bluml S, Tseng-Ong L, Gilsanz V: Three-point technique of fat quantification of muscle tissue as a marker of disease progression in Duchenne muscular dystrophy: preliminary study. AJR Am J Roentgenol. 2008, 190 (1): W8-W12.PubMedCrossRef
25.
26.
go back to reference Elder GC, Kirk J, Stewart G, Cook K, Weir D, Marshall A, Leahey L: Contributing factors to muscle weakness in children with cerebral palsy. Dev Med Child Neurol. 2003, 45 (8): 542-550.PubMedCrossRef Elder GC, Kirk J, Stewart G, Cook K, Weir D, Marshall A, Leahey L: Contributing factors to muscle weakness in children with cerebral palsy. Dev Med Child Neurol. 2003, 45 (8): 542-550.PubMedCrossRef
27.
go back to reference Barber L, Hastings-Ison T, Baker R, Barrett R, Lichtwark G: Medial gastrocnemius muscle volume and fascicle length in children aged 2 to 5 years with cerebral palsy. Dev Med Child Neurol. 2011, 53 (6): 543-548.PubMedCrossRef Barber L, Hastings-Ison T, Baker R, Barrett R, Lichtwark G: Medial gastrocnemius muscle volume and fascicle length in children aged 2 to 5 years with cerebral palsy. Dev Med Child Neurol. 2011, 53 (6): 543-548.PubMedCrossRef
28.
go back to reference Barrett RS, Lichtwark GA: Gross muscle morphology and structure in spastic cerebral palsy: a systematic review. Dev Med Child Neurol. 2010, 52 (9): 794-804.PubMedCrossRef Barrett RS, Lichtwark GA: Gross muscle morphology and structure in spastic cerebral palsy: a systematic review. Dev Med Child Neurol. 2010, 52 (9): 794-804.PubMedCrossRef
29.
go back to reference Malaiya R, McNee AE, Fry NR, Eve LC, Gough M, Shortland AP: The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy. J Electromyogr Kinesiol. 2007, 17 (6): 657-663.PubMedCrossRef Malaiya R, McNee AE, Fry NR, Eve LC, Gough M, Shortland AP: The morphology of the medial gastrocnemius in typically developing children and children with spastic hemiplegic cerebral palsy. J Electromyogr Kinesiol. 2007, 17 (6): 657-663.PubMedCrossRef
30.
go back to reference Shortland A: Muscle deficits in cerebral palsy and early loss of mobility: can we learn something from our elders?. Dev Med Child Neurol. 2009, 51 (Suppl 4): 59-63.PubMedCrossRef Shortland A: Muscle deficits in cerebral palsy and early loss of mobility: can we learn something from our elders?. Dev Med Child Neurol. 2009, 51 (Suppl 4): 59-63.PubMedCrossRef
31.
go back to reference Poon DM, Hui-Chan CW: Hyperactive stretch reflexes, co-contraction, and muscle weakness in children with cerebral palsy. Dev Med Child Neurol. 2009, 51 (2): 128-135.PubMedCrossRef Poon DM, Hui-Chan CW: Hyperactive stretch reflexes, co-contraction, and muscle weakness in children with cerebral palsy. Dev Med Child Neurol. 2009, 51 (2): 128-135.PubMedCrossRef
32.
go back to reference Wiley ME, Damiano DL: Lower-extremity strength profiles in spastic cerebral palsy. Dev Med Child Neurol. 1998, 40 (2): 100-107.PubMedCrossRef Wiley ME, Damiano DL: Lower-extremity strength profiles in spastic cerebral palsy. Dev Med Child Neurol. 1998, 40 (2): 100-107.PubMedCrossRef
33.
go back to reference Stackhouse SK, Stevens JE, Lee SC, Pearce KM, Snyder-Mackler L, Binder-Macleod SA: Maximum voluntary activation in nonfatigued and fatigued muscle of young and elderly individuals. Phys Ther. 2001, 81 (5): 1102-1109.PubMed Stackhouse SK, Stevens JE, Lee SC, Pearce KM, Snyder-Mackler L, Binder-Macleod SA: Maximum voluntary activation in nonfatigued and fatigued muscle of young and elderly individuals. Phys Ther. 2001, 81 (5): 1102-1109.PubMed
34.
go back to reference Stackhouse SK, Binder-Macleod SA, Lee SC: Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve. 2005, 31 (5): 594-601.PubMedPubMedCentralCrossRef Stackhouse SK, Binder-Macleod SA, Lee SC: Voluntary muscle activation, contractile properties, and fatigability in children with and without cerebral palsy. Muscle Nerve. 2005, 31 (5): 594-601.PubMedPubMedCentralCrossRef
35.
go back to reference Kewalramani G, Bilan PJ, Klip A: Muscle insulin resistance: assault by lipids, cytokines and local macrophages. Curr Opin Clin Nutr Metab Care. 2010, 13 (4): 382-390.PubMedCrossRef Kewalramani G, Bilan PJ, Klip A: Muscle insulin resistance: assault by lipids, cytokines and local macrophages. Curr Opin Clin Nutr Metab Care. 2010, 13 (4): 382-390.PubMedCrossRef
36.
go back to reference Lara-Castro C, Garvey WT: Intracellular lipid accumulation in liver and muscle and the insulin resistance syndrome. Endocrinol Metab Clin North Am. 2008, 37 (4): 841-856.PubMedPubMedCentralCrossRef Lara-Castro C, Garvey WT: Intracellular lipid accumulation in liver and muscle and the insulin resistance syndrome. Endocrinol Metab Clin North Am. 2008, 37 (4): 841-856.PubMedPubMedCentralCrossRef
37.
go back to reference Schick F, Eismann B, Jung WI, Bongers H, Bunse M, Lutz O: Comparison of localized proton NMR signals of skeletal muscle and fat tissue in vivo: two lipid compartments in muscle tissue. Magn Reson Med. 1993, 29 (2): 158-167.PubMedCrossRef Schick F, Eismann B, Jung WI, Bongers H, Bunse M, Lutz O: Comparison of localized proton NMR signals of skeletal muscle and fat tissue in vivo: two lipid compartments in muscle tissue. Magn Reson Med. 1993, 29 (2): 158-167.PubMedCrossRef
38.
go back to reference Brechtel K, Dahl DB, Machann J, Bachmann OP, Wenzel I, Maier T, Claussen CD, Haring HU, Jacob S, Schick F: Fast elevation of the intramyocellular lipid content in the presence of circulating free fatty acids and hyperinsulinemia: a dynamic 1H-MRS study. Magn Reson Med. 2001, 45 (2): 179-183.PubMedCrossRef Brechtel K, Dahl DB, Machann J, Bachmann OP, Wenzel I, Maier T, Claussen CD, Haring HU, Jacob S, Schick F: Fast elevation of the intramyocellular lipid content in the presence of circulating free fatty acids and hyperinsulinemia: a dynamic 1H-MRS study. Magn Reson Med. 2001, 45 (2): 179-183.PubMedCrossRef
39.
go back to reference Krssak M, Falk Petersen K, Dresner A, DiPietro L, Vogel SM, Rothman DL, Roden M, Shulman GI: Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia. 1999, 42 (1): 113-116.PubMedCrossRef Krssak M, Falk Petersen K, Dresner A, DiPietro L, Vogel SM, Rothman DL, Roden M, Shulman GI: Intramyocellular lipid concentrations are correlated with insulin sensitivity in humans: a 1H NMR spectroscopy study. Diabetologia. 1999, 42 (1): 113-116.PubMedCrossRef
40.
go back to reference Petersen KF, Hendler R, Price T, Perseghin G, Rothman DL, Held N, Amatruda JM, Shulman GI: 13C/31P NMR studies on the mechanism of insulin resistance in obesity. Diabetes. 1998, 47 (3): 381-386.PubMedCrossRef Petersen KF, Hendler R, Price T, Perseghin G, Rothman DL, Held N, Amatruda JM, Shulman GI: 13C/31P NMR studies on the mechanism of insulin resistance in obesity. Diabetes. 1998, 47 (3): 381-386.PubMedCrossRef
41.
go back to reference Misra A, Sinha S, Kumar M, Jagannathan NR, Pandey RM: Proton magnetic resonance spectroscopy study of soleus muscle in non-obese healthy and Type 2 diabetic Asian Northern Indian males: high intramyocellular lipid content correlates with excess body fat and abdominal obesity. Diabet Med. 2003, 20 (5): 361-367.PubMedCrossRef Misra A, Sinha S, Kumar M, Jagannathan NR, Pandey RM: Proton magnetic resonance spectroscopy study of soleus muscle in non-obese healthy and Type 2 diabetic Asian Northern Indian males: high intramyocellular lipid content correlates with excess body fat and abdominal obesity. Diabet Med. 2003, 20 (5): 361-367.PubMedCrossRef
42.
go back to reference Jacob S, Machann J, Rett K, Brechtel K, Volk A, Renn W, Maerker E, Matthaei S, Schick F, Claussen CD, Haring HU: Association of increased intramyocellular lipid content with insulin resistance in lean nondiabetic offspring of type 2 diabetic subjects. Diabetes. 1999, 48 (5): 1113-1119.PubMedCrossRef Jacob S, Machann J, Rett K, Brechtel K, Volk A, Renn W, Maerker E, Matthaei S, Schick F, Claussen CD, Haring HU: Association of increased intramyocellular lipid content with insulin resistance in lean nondiabetic offspring of type 2 diabetic subjects. Diabetes. 1999, 48 (5): 1113-1119.PubMedCrossRef
43.
go back to reference Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, Jenkins AB, Storlien LH: Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes. 1997, 46 (6): 983-988.PubMedCrossRef Pan DA, Lillioja S, Kriketos AD, Milner MR, Baur LA, Bogardus C, Jenkins AB, Storlien LH: Skeletal muscle triglyceride levels are inversely related to insulin action. Diabetes. 1997, 46 (6): 983-988.PubMedCrossRef
44.
go back to reference Stump CS, Henriksen EJ, Wei Y, Sowers JR: The metabolic syndrome: role of skeletal muscle metabolism. Ann Med. 2006, 38 (6): 389-402.PubMedCrossRef Stump CS, Henriksen EJ, Wei Y, Sowers JR: The metabolic syndrome: role of skeletal muscle metabolism. Ann Med. 2006, 38 (6): 389-402.PubMedCrossRef
45.
go back to reference Ryan AS, Dobrovolny CL, Smith GV, Silver KH, Macko RF: Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil. 2002, 83 (12): 1703-1707.PubMedCrossRef Ryan AS, Dobrovolny CL, Smith GV, Silver KH, Macko RF: Hemiparetic muscle atrophy and increased intramuscular fat in stroke patients. Arch Phys Med Rehabil. 2002, 83 (12): 1703-1707.PubMedCrossRef
46.
go back to reference Yoshida Y, Marcus RL, Lastayo PC: Intramuscular adipose tissue and central activation in older adults. Muscle Nerve. 2012, 46 (5): 813-816.PubMedCrossRef Yoshida Y, Marcus RL, Lastayo PC: Intramuscular adipose tissue and central activation in older adults. Muscle Nerve. 2012, 46 (5): 813-816.PubMedCrossRef
47.
go back to reference Visser M, Kritchevsky SB, Goodpaster BH, Newman AB, Nevitt M, Stamm E, Harris TB: Leg muscle mass and composition in relation to lower extremity performance in men and women aged 70 to 79: the health, aging and body composition study. J Am Geriatr Soc. 2002, 50 (5): 897-904.PubMedCrossRef Visser M, Kritchevsky SB, Goodpaster BH, Newman AB, Nevitt M, Stamm E, Harris TB: Leg muscle mass and composition in relation to lower extremity performance in men and women aged 70 to 79: the health, aging and body composition study. J Am Geriatr Soc. 2002, 50 (5): 897-904.PubMedCrossRef
48.
go back to reference Marcus RL, Addison O, Dibble LE, Foreman KB, Morrell G, Lastayo P: Intramuscular adipose tissue, sarcopenia, and mobility function in older individuals. J Aging Res. 2012, 2012: 629637-PubMedPubMedCentralCrossRef Marcus RL, Addison O, Dibble LE, Foreman KB, Morrell G, Lastayo P: Intramuscular adipose tissue, sarcopenia, and mobility function in older individuals. J Aging Res. 2012, 2012: 629637-PubMedPubMedCentralCrossRef
49.
go back to reference Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, DiPietro L, Cline GW, Shulman GI: Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science. 2003, 300 (5622): 1140-1142.PubMedPubMedCentralCrossRef Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, DiPietro L, Cline GW, Shulman GI: Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science. 2003, 300 (5622): 1140-1142.PubMedPubMedCentralCrossRef
50.
go back to reference Faulkner JA, Larkin LM, Claflin DR, Brooks SV: Age-related changes in the structure and function of skeletal muscles. Clin Exp Pharmacol Physiol. 2007, 34 (11): 1091-1096.PubMedCrossRef Faulkner JA, Larkin LM, Claflin DR, Brooks SV: Age-related changes in the structure and function of skeletal muscles. Clin Exp Pharmacol Physiol. 2007, 34 (11): 1091-1096.PubMedCrossRef
51.
go back to reference Alnaqeeb MA, Al Zaid NS, Goldspink G: Connective tissue changes and physical properties of developing and ageing skeletal muscle. J Anat. 1984, 139 (Pt 4): 677-689.PubMedPubMedCentral Alnaqeeb MA, Al Zaid NS, Goldspink G: Connective tissue changes and physical properties of developing and ageing skeletal muscle. J Anat. 1984, 139 (Pt 4): 677-689.PubMedPubMedCentral
52.
go back to reference Yokoo T, Bydder M, Hamilton G, Middleton MS, Gamst AC, Wolfson T, Hassanein T, Patton HM, Lavine JE, Schwimmer JB, Sirlin CB: Nonalcoholic fatty liver disease: diagnostic and fat-grading accuracy of low-flip-angle multiecho gradient-recalled-echo MR imaging at 1.5 T. Radiology. 2009, 251 (1): 67-76.PubMedPubMedCentralCrossRef Yokoo T, Bydder M, Hamilton G, Middleton MS, Gamst AC, Wolfson T, Hassanein T, Patton HM, Lavine JE, Schwimmer JB, Sirlin CB: Nonalcoholic fatty liver disease: diagnostic and fat-grading accuracy of low-flip-angle multiecho gradient-recalled-echo MR imaging at 1.5 T. Radiology. 2009, 251 (1): 67-76.PubMedPubMedCentralCrossRef
53.
go back to reference Gerber C, Fuchs B, Hodler J: The results of repair of massive tears of the rotator cuff. J Bone Joint Surg Am. 2000, 82 (4): 505-515.PubMed Gerber C, Fuchs B, Hodler J: The results of repair of massive tears of the rotator cuff. J Bone Joint Surg Am. 2000, 82 (4): 505-515.PubMed
54.
go back to reference Liu W, Liu Y, Lai X, Kuang S: Intramuscular adipose is derived from a non-Pax3 lineage and required for efficient regeneration of skeletal muscles. Dev Biol. 2012, 361 (1): 27-38.PubMedCrossRef Liu W, Liu Y, Lai X, Kuang S: Intramuscular adipose is derived from a non-Pax3 lineage and required for efficient regeneration of skeletal muscles. Dev Biol. 2012, 361 (1): 27-38.PubMedCrossRef
55.
go back to reference Contreras-Shannon V, Ochoa O, Reyes-Reyna SM, Sun D, Michalek JE, Kuziel WA, McManus LM, Shireman PK: Fat accumulation with altered inflammation and regeneration in skeletal muscle of CCR2-/- mice following ischemic injury. Am J Physiol Cell Physiol. 2007, 292 (2): C953-C967.PubMedCrossRef Contreras-Shannon V, Ochoa O, Reyes-Reyna SM, Sun D, Michalek JE, Kuziel WA, McManus LM, Shireman PK: Fat accumulation with altered inflammation and regeneration in skeletal muscle of CCR2-/- mice following ischemic injury. Am J Physiol Cell Physiol. 2007, 292 (2): C953-C967.PubMedCrossRef
56.
go back to reference Gumucio JP, Davis ME, Bradley JR, Stafford PL, Schiffman CJ, Lynch EB, Claflin DR, Bedi A, Mendias CL: Rotator cuff tear reduces muscle fiber specific force production and induces macrophage accumulation and autophagy. J Orthop Res. 2012, 30 (12): 1963-1970.PubMedPubMedCentralCrossRef Gumucio JP, Davis ME, Bradley JR, Stafford PL, Schiffman CJ, Lynch EB, Claflin DR, Bedi A, Mendias CL: Rotator cuff tear reduces muscle fiber specific force production and induces macrophage accumulation and autophagy. J Orthop Res. 2012, 30 (12): 1963-1970.PubMedPubMedCentralCrossRef
Metadata
Title
Intramuscular fat in ambulant young adults with bilateral spastic cerebral palsy
Authors
Jonathan J Noble
Geoffrey D Charles-Edwards
Stephen F Keevil
Andrew P Lewis
Martin Gough
Adam P Shortland
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2014
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/1471-2474-15-236

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