Abstract
Background
Increasing evidence highlights the role of muscular strength as a protective factor for cardiometabolic health in adolescents. However, it is not known the relationship between liver enzyme concentrations, liver disease risk factors, and muscular strength among young populations. The aim of this study was to determine the association between muscle strength and liver enzymes and chronic liver disease risk among US adolescents.
Methods
Data from the NHANES cross-sectional study (2011–2014) was used. A total of 1270 adolescents were included in the final analysis (12–17 years old). Absolute handgrip strength (kg) was normalized according to body composition parameters by body weight [NHSw], whole-body fat [NHSf], and trunk fat [NHSt]).
Results
In boys, handgrip strength was inversely associated with higher values of aspartate aminotransferase (AST) and gamma glutamyl transpeptidase (GGT) for all estimations of muscle strength (NHSw, NHSf, and NHSt) (p < 0.050). Likewise, boys with high and intermediate NHSw, NHSf, and NHSt presented lower AST and GGT than their counterparts with low handgrip strength (p < 0.050).
Conclusions
Our findings highlight the importance of muscular strength during adolescence since they could help in developing better liver enzyme profiles among adolescent population.
Impact
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Our research suggests that US adolescents with low handgrip strength have higher values of liver enzymes as well as a higher prevalence of chronic liver disease.
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These findings are clinically meaningful and highlight the importance of muscular strength during adolescence since they could help in developing better liver enzyme profiles among young populations.
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References
Sattar, N., Forrest, E. & Preiss, D. Non-alcoholic fatty liver disease. BMJ 349, g4596 (2014).
Labayen, I. et al. Liver enzymes and clustering cardiometabolic risk factors in European adolescents: the HELENA study: liver enzymes and metabolic risk. Pediatr. Obes. 10, 361–370 (2015).
Balkau, B., Lange, C., Vol, S., Fumeron, F. & Bonnet, F. Nine-year incident diabetes is predicted by fatty liver indices: the French D.E.S.I.R. study. BMC Gastroenterol. 10, 56 (2010).
Hanley, A. J. G. et al. Liver markers and development of the metabolic syndrome: The Insulin Resistance Atherosclerosis Study. Diabetes 54, 3140–3147 (2005).
Sorbi, D., Boynton, J. & Lindor, K. D. The ratio of aspartate aminotransferase to alanine aminotransferase: potential value in differentiating nonalcoholic steatohepatitis from alcoholic liver disease. Am. J. Gastroenterol. 94, 1018–1022 (1999).
García-Hermoso, A., Ramírez-Campillo, R. & Izquierdo, M. Is muscular fitness associated with future health benefits in children and adolescents? A systematic review and meta-analysis of longitudinal studies. Sports Med. 49, 1079–1094 (2019).
García-Hermoso, A., Ramírez-Velez, R., García-Alonso, Y., Alonso-Martinez, A. & Izquierdo, M. Association of cardiorespiratory fitness levels during youth with health risk later in life. A systematic review and meta-analysis. JAMA Pediatr. 174, 1–9 (2020).
Ramírez-Vélez, R. et al. Grip strength moderates the association between anthropometric and body composition indicators and liver fat in youth with an excess of adiposity. J. Clin. Med. 7, 347 (2018).
Lee, K. Moderation effect of handgrip strength on the associations of obesity and metabolic syndrome with fatty liver in adolescents. J. Clin. Densitom. 23, 278–285 (2020).
Medrano, M. et al. Associations of physical activity and fitness with hepatic steatosis, liver enzymes, and insulin resistance in children with overweight/obesity. Pediatr. Diabetes 21, 565–574 (2020).
Pandey, S. Association of nonalcoholic fatty liver disease with relative skeletal muscle mass: a public health perspective. Hepatology 68, 1657–1657 (2018).
Kim, G. et al. Relationship between relative skeletal muscle mass and nonalcoholic fatty liver disease: a 7‐year longitudinal study. Hepatology 68, 1755–1768 (2018).
Fan, R., Wang, J. & Du, J. Association between body mass index and fatty liver risk: a dose-response analysis. Sci. Rep. 8, 15273 (2018).
Kelishadi, R. et al. Association of alanine aminotransferase concentration with cardiometabolic risk factors in children and adolescents: the CASPIAN-V cross-sectional study. Sao Paulo Med. J. 136, 511–519 (2018).
Kuczmarski, R. J., Ogden, C. L. & Guo, S. S. 2000 CDC growth charts for the United States: methods and development. Vital and health statistics. Series 11, Data from the national health survey. https://www.cdc.gov/nchs/data/series/sr_11/sr11_246.pdf (2002).
Schwimmer, J. B. et al. SAFETY Study: alanine aminotransferase cutoff values are set too high for reliable detection of pediatric chronic liver disease. Gastroenterology 138, 1357–1364.e2 (2010).
Centers of Disease Control and Prevention. National Health and Nutrition Examination Survey (NHANES): muscle strength procedures manual. https://wwwn.cdc.gov/nchs/data/nhanes/2011-2012/manuals/Muscle_Strength_Proc_Manual.pdf (2011).
Ruiz, J. R. et al. Field-based fitness assessment in young people: the ALPHA health-related fitness test battery for children and adolescents. Br. J. Sports Med. 45, 518–524 (2011).
Fraser, A., Longnecker, M. P. & Lawlor, D. A. Prevalence of elevated alanine aminotransferase among US adolescents and associated factors: NHANES 1999–2004. Gastroenterology 133, 1814–1820 (2007).
Kim, J. W. et al. Prevalence and risk factors of elevated alanine aminotransferase among Korean adolescents: 2001–2014. BMC Public Health 18, 617 (2018).
Chen, S. C.-C. et al. Gender difference of alanine aminotransferase elevation may be associated with higher hemoglobin levels among male adolescents. PLoS ONE 5, e13269 (2010).
Baker, C. J. et al. Effect of exercise on hepatic steatosis: are benefits seen without dietary intervention? A systematic review and meta‐analysis. J. Diabetes 13, 63–77 (2021).
González-Ruiz, K., Ramírez-Vélez, R., Correa-Bautista, J. E., Peterson, M. D. & García-Hermoso, A. The effects of exercise on abdominal fat and liver enzymes in pediatric obesity: a systematic review and meta-analysis. Child Obes. 13, 272–282 (2017).
Hao, L., Wang, Z., Wang, Y., Wang, J. & Zeng, Z. Association between cardiorespiratory fitness, relative grip strength with non-alcoholic fatty liver disease. Med. Sci. Monit. Int. Med. J. Exp. Clin. Res. 26, e923015 (2020).
Stricker, P. R., Faigenbaum, A. D. & McCambridge, T. M. Resistance training for children and adolescents. Pediatrics 145, e20201011 (2020).
Barbat-Artigas, S., Rolland, Y., Zamboni, M. & Aubertin-Leheudre, M. How to assess functional status: a new muscle quality index. J. Nutr. Health Aging 16, 67–77 (2012).
Stefan, N. & Häring, H.-U. The role of hepatokines in metabolism. Nat. Rev. Endocrinol. 9, 144–152 (2013).
Mizgier, M. L., Casas, M., Contreras-Ferrat, A., Llanos, P. & Galgani, J. E. Potential role of skeletal muscle glucose metabolism on the regulation of insulin secretion: organ crosstalk and insulin secretion. Obes. Rev. 15, 587–597 (2014).
Poggiogalle, E., Donini, L. M., Lenzi, A., Chiesa, C. & Pacifico, L. Non-alcoholic fatty liver disease connections with fat-free tissues: a focus on bone and skeletal muscle. World J. Gastroenterol. 23, 1747 (2017).
Laurson, K. R., Saint-Maurice, P. F., Welk, G. J. & Eisenmann, J. C. Reference curves for field tests of musculoskeletal fitness in U.S. children and adolescents: The 2012 NHANES National Youth Fitness Survey. J. Strength Cond. Res. 31, 2075–2082 (2017).
Acknowledgements
A.G.-H. is a Miguel Servet Fellow (Instituto de Salud Carlos III-FSE – CP18/0150). R.R.-V. is funded in part by a Postdoctoral Fellowship Resolution ID 420/2019 of the Universidad Pública de Navarra. This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
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Conceptualization, J.F.L.-G. and A.G.-H.; methodology, J.F.L.-G., and A.G.-H.; software, J.F.L.-G. and A.G.-H.; validation, J.F.L.-G and A.G.-H.; formal analysis, A.G.-H.; data curation, J.F.L.-G. and A.G.-H.; writing—original draft preparation, J.F.L.-G., A.G.-H., J.A.-J., and R.R.-V.; writing—review and editing, R.R.-V., and M.I.; visualization, A.G.-H. and R.R.-V.; supervision, A.G.-H. and M.I.; all authors have read and agreed to the published version of the manuscript.
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López-Gil, J.F., Ramírez-Vélez, R., Alarcón-Jiménez, J. et al. Low handgrip strength is associated with higher liver enzyme concentrations in US adolescents. Pediatr Res 91, 984–990 (2022). https://doi.org/10.1038/s41390-021-01530-6
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DOI: https://doi.org/10.1038/s41390-021-01530-6
