Abstract
Purpose
Recent evidence has demonstrated an obesity-induced, skeletal muscle-specific reduction in contractile performance. The extent and magnitude of these changes in relation to total dose of high-fat diet consumption remains unclear. This study aimed to examine the dose–response relationship between a high-fat diet and isolated skeletal muscle contractility.
Methods
120 female CD1 mice were randomly assigned to either control group or groups receiving 2, 4, 8 or 12 weeks of a high-calorie diet (N = 24). At 20 weeks, soleus, EDL or diaphragm muscle was isolated (n = 8 in each case) and isometric force, work loop power output and fatigue resistance were measured.
Results
When analysed with respect to feeding duration, there was no effect of diet on the measured parameters prior to 8 weeks of feeding. Compared to controls, 8-week feeding caused a reduction in normalised power of the soleus, and 8- and 12-week feeding caused reduced normalised isometric force, power and fatigue resistance of the EDL. Diaphragm from the 12-week group produced lower normalised power, whereas 8- and 12-week groups produced significantly lower normalised isometric force. Correlation statistics indicated that body fat accumulation and decline in contractility will be specific to the individual and independent of the feeding duration.
Conclusion
The data indicate that a high-fat diet causes a decline in muscle quality with specific contractile parameters being affected in each muscle. We also uniquely demonstrate that the amount of fat gain, irrespective of feeding duration, may be the main factor in reducing contractile performance.
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Abbreviations
- ANOVA:
-
Analysis of variance
- CF:
-
Cycle frequency
- EDL:
-
Extensor digitorum longus
- HFD:
-
High-fat diet
- PO:
-
Power output
- WL:
-
Work loop
References
Abdelmoula A, Martin V, Bouchant A et al (2012) Knee extension strength in obese and nonobese male adolescents. Appl Physiol Nutr Metab 37:269–275
Akhmedov D, Berdeaux R (2013) The effects of obesity on skeletal muscle regeneration. Front Physiol 4:371. https://doi.org/10.3389/fphys.2013.00371
Altringham JD, Young IS (1991) Power output and the frequency of oscillatory work in mammalian diaphragm muscle: the effects of animal size. J Exp Biol 157:381–389
Anderson SR, Gilge DA, Steiber AL, Previs SF (2008) Diet-induced obesity alters protein synthesis: tissue-specific effects in fasted versus fed mice. Metab Clin Exp 57:347–354
Aucouturier J, Lazaar N, Dore E, Meyer M, Ratel S, Duche P (2007) Cycling peak power in obese and lean 6-to 8-year-old girls and boys. Appl Physiol Nutr Metab 32:367–371
Barclay C (1996) Mechanical efficiency and fatigue of fast and slow muscles of the mouse. J Physiol 497:781–794
Barclay C (2005) Modelling diffusive O2 supply to isolated preparations of mammalian skeletal and cardiac muscle. J Muscle Res Cell Motil 26:225–235
Blimkie CJ, Ebbesen B, MacDougall D, Bar-Or O, Sale D (1989) Voluntary and electrically evoked strength characteristics of obese and nonobese preadolescent boys. Human biol 61:515–532
Bott KN, Gittings W, Fajardo VA et al (2017) Musculoskeletal structure and function in response to the combined effect of an obesogenic diet and age in male C57BL/6J mice. Mol Nutr Food Res
Brotto MA, Biesiadecki BJ, Brotto LS, Nosek TM, Jin JP (2006) Coupled expression of troponin T and troponin I isoforms in single skeletal muscle fibers correlates with contractility. Am J Physiol Cell Physiol 290:C567–C576. doi:00422.2005
Bruton JD, Katz A, Lännergren J, Abbate F, Westerblad H (2002) Regulation of myoplasmic Ca 2 in genetically obese (ob/ob) mouse single skeletal muscle fibres. Pflügers Arch Euro J Physiol 444:692–699
Capodaglio P, Vismara L, Menegoni F, Baccalaro G, Galli M, Grugni G (2009) Strength characterization of knee flexor and extensor muscles in Prader–Willi and obese patients. BMC Musculoskelet Disord 10:47
Ciapaite J, Van Den Berg SA, Houten SM, Nicolay K, van Dijk KW, Jeneson JA (2015) Fiber-type-specific sensitivities and phenotypic adaptations to dietary fat overload differentially impact fast-versus slow-twitch muscle contractile function in C57BL/6J mice. J Nutr Biochem 26:155–164
de Wilde J, Mohren R, van den Berg S et al (2008) Short-term high fat-feeding results in morphological and metabolic adaptations in the skeletal muscle of C57BL/6J mice. Physiol Genomics 32:360–369. doi:00219.2007
Denies MS, Johnson J, Maliphol AB et al (2014) Diet-induced obesity alters skeletal muscle fiber types of male but not female mice. Physiol Rep 2:e00204. https://doi.org/10.1002/phy2.204
Eshima H, Tamura Y, Kakehi S et al (2017) Long-term, but not short-term high-fat diet induces fiber composition changes and impaired contractile force in mouse fast-twitch skeletal muscle. Physiol Rep 5:e13250. https://doi.org/10.14814/phy2.13250
Goodpaster BH, He J, Watkins S, Kelley DE (2001) Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab 86:5755–5761
Hulens M, Vansant G, Lysens R, Claessens A, Muls E, Brumagne S (2001) Study of differences in peripheral muscle strength of lean versus obese women: an allometric approach. Int J Obes 25:676
James RS, Altringham JD, Goldspink DF (1995) The mechanical properties of fast and slow skeletal muscles of the mouse in relation to their locomotory function. J Exp Biol 198:491–502
James RS, Young IS, Cox VM, Goldspink DF, Altringham JD (1996) Isometric and isotonic muscle properties as determinants of work loop power output. Pflügers Archiv Euro J Physiol 432:767–774
James RS, Kohlsdorf T, Cox VM, Navas CA (2005) 70 µM caffeine treatment enhances in vitro force and power output during cyclic activities in mouse extensor digitorum longus muscle. Eur J Appl Physiol 95:74–82
Josephson RK (1985) Mechanical power output from striated muscle during cyclic contraction. J Exp Biol 114:493–512
Josephson RK (1993) Contraction dynamics and power output of skeletal muscle. Annu Rev Physiol 55:527–546
Kemp J, Blazev R, Stephenson DG, Stephenson G (2009) Morphological and biochemical alterations of skeletal muscles from the genetically obese (ob/ob) mouse. Int J Obes 33:831
Kopelman P (2007) Health risks associated with overweight and obesity. Obesity Rev 8:13–17
Mendez J, Keys A (1960) Density and composition of mammalian muscle. Metabolism 9:184–188
Machann J, Bachmann OP, Brechtel K et al (2003) Lipid content in the musculature of the lower leg assessed by fat selective MRI: intra-and interindividual differences and correlation with anthropometric and metabolic data. J Magn Reson Imaging 17:350–357
Maffiuletti NA, Jubeau M, Munzinger U et al (2007) Differences in quadriceps muscle strength and fatigue between lean and obese subjects. Eur J Appl Physiol 101:51–59
Maffiuletti NA, Ratel S, Sartorio A, Martin V (2013) The impact of obesity on in vivo human skeletal muscle function. Curr Obesity Rep 2:251–260
Matsakas A, Prosdocimo DA, Mitchell R et al (2015) Investigating mechanisms underpinning the detrimental impact of a high-fat diet in the developing and adult hypermuscular myostatin null mouse. Skeletal muscle 5:38
Miyatake N, Fujii M, Nishikawa H et al (2000) Clinical evaluation of muscle strength in 20–79-years-old obese Japanese. Diabetes Res Clin Pract 48:15–21
Paolillo FR, Milan JC, Bueno Pde G et al (2012) Effects of excess body mass on strength and fatigability of quadriceps in postmenopausal women. Menopause 19:556–561. https://doi.org/10.1097/gme.0b013e3182364e80
Pette D, Staron RS (1997) Mammalian skeletal muscle fiber type transitions. Int Rev Cytol 170:143–223
Rogers P, Webb GP (1980) Estimation of body fat in normal and obese mice. Br J Nutr 43(1):83–86
Rolland Y, Lauwers-Cances V, Pahor M, Fillaux J, Grandjean H, Vellas B (2004) Muscle strength in obese elderly women: effect of recreational physical activity in a cross-sectional study. Am J Clin Nutr 79:552–557
Seebacher F, Tallis J, McShea K, James R (2017) Obesity-induced decreases in muscle performance are not reversed by weight loss. Int J Obes
Shortreed KE, Krause MP, Huang JH et al (2009) Muscle-specific adaptations, impaired oxidative capacity and maintenance of contractile function characterize diet-induced obese mouse skeletal muscle. PloS one 4:e7293
Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ (2009) Autophagy regulates lipid metabolism. Nature 458(7242):1131
Szymura J, Gradek J, Maciejczyk M, Wiȩcek M, Cempla J (2011) The anaerobic capacity in obese children. Gastroenterol Polska 18:147–153
Tallis J, James RS, Cox VM, Duncan MJ (2012) The effect of physiological concentrations of caffeine on the power output of maximally and submaximally stimulated mouse EDL (fast) and soleus (slow) muscle. J Appl Physiol (1985) 112:64–71. https://doi.org/10.1152/japplphysiol.00801.2011
Tallis J, James RS, Little AG, Cox VM, Duncan MJ, Seebacher F (2014) Early effects of ageing on the mechanical performance of isolated locomotory (EDL) and respiratory (diaphragm) skeletal muscle using the work-loop technique. Am J Physiol Regul Integr Comp Physiol 307:R670–R684. https://doi.org/10.1152/ajpregu.00115.2014
Tallis J, Higgins MF, Seebacher F, Cox VM, Duncan MJ, James RS (2017a) The effects of 8 weeks voluntary wheel running on the contractile performance of isolated locomotory (soleus) and respiratory (diaphragm) skeletal muscle during early ageing. J Exp Biol 220:3733–3741. https://doi.org/10.1242/jeb.166603
Tallis J, Hill C, James RS, Cox VM, Seebacher F (2017b) The effect of obesity on the contractile performance of isolated mouse soleus, EDL, and diaphragm muscles. J Appl Physiol (1985) 122:170–181. https://doi.org/10.1152/japplphysiol.00836.2016
Tallis J, James RS, Seebacher F (2018) The effects of obesity on skeletal muscle contractile function. J Exp Biol 221(13):jeb163840. https://doi.org/10.1242/jeb.163840
Tanner CJ, Barakat HA, Dohm GL et al (2002) Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 282:E1191–E1196. https://doi.org/10.1152/ajpendo.00416.2001
Thomas MM, Trajcevski KE, Coleman SK et al (2014) Early oxidative shifts in mouse skeletal muscle morphology with high-fat diet consumption do not lead to functional improvements. Physiolo Rep 2:e12149
Tomlinson D, Erskine R, Morse C, Winwood K, Onambélé-Pearson G (2016) The impact of obesity on skeletal muscle strength and structure through adolescence to old age. Biogerontology 17:467–483
Trajcevski KE, O’Neill HM, Wang DC et al (2013) Enhanced lipid oxidation and maintenance of muscle insulin sensitivity despite glucose intolerance in a diet-induced obesity mouse model. PLoS One 8:e71747
Tuttle LJ, Sinacore DR, Mueller MJ (2012) Intermuscular adipose tissue is muscle specific and associated with poor functional performance. J Aging Res 2012
Ward DS, Trost SG, Felton G et al (1997) Physical activity and physical fitness in African-American girls with and without obesity. Obesity 5:572–577
Warmington S, Tolan R, McBennett S (2000) Functional and histological characteristics of skeletal muscle and the effects of leptin in the genetically obese (ob/ob) mouse. Int J Obes 24:1040
Wronska A, Kmiec Z (2012) Structural and biochemical characteristics of various white adipose tissue depots. Acta Physiol 205(2):194–208
Yoshida Y, Marcus RL, Lastayo PC (2012) Intramuscular adipose tissue and central activation in older adults. Muscle Nerve 46:813–816
Zurlo F, Larson K, Bogardus C, Ravussin E (1990) Skeletal muscle metabolism is a major determinant of resting energy expenditure. J Clin Invest 86:1423–1427. https://doi.org/10.1172/JCI114857 [doi]
World health organisation (WHO) (2017) Available at http://www.who.int/en/news-room/factsheets/detail/obesity-and-overweight. Visited on 05 Dec 2017
World obesity federation (WOF) (2017) Available at https://www.worldobesity.org/data/child-obesity/. Visited on 05 Dec 2017
D’Souza DM, Trajcevski KE, Al-Sajee D et al (2015) Diet-induced obesity impairs muscle satellite cell activation and muscle repair through alterations in hepatocyte growth factor signaling. Physiol Rep. https://doi.org/10.14814/phy2.12506
Acknowledgements
We wish to acknowledge Mark Bodycote and Bethan Grist for technical assistance.
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JH, CH performed experiments; JH, JT analysed data; JH, JT, and RSJ interpreted results of experiments; JH prepared figures; JH and JT drafted manuscript; All edited and revised the manuscript; All approved the final version of manuscript.
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Communicated by Phillip D Chilibeck.
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Hurst, J., James, R.S., Cox, V.M. et al. Investigating a dose–response relationship between high-fat diet consumption and the contractile performance of isolated mouse soleus, EDL and diaphragm muscles. Eur J Appl Physiol 119, 213–226 (2019). https://doi.org/10.1007/s00421-018-4017-6
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DOI: https://doi.org/10.1007/s00421-018-4017-6