Independent Association of Muscular Strength and Carotid Intima-Media Thickness in Children

X. Melo; H. Santa-Clara; D. A. Santos; N. M. Pimenta; C. S. Minderico; B. Fernhall; L. B. Sardinha

doi:10.1055/s-0034-1398678

International Journal of Sports Medicine, Table of Contents

Int J Sports Med 2015; 36(08): 624-630
DOI: 10.1055/s-0034-1398678

Physiology & Biochemistry

Independent Association of Muscular Strength and Carotid Intima-Media Thickness in Children

X. Melo

¹CIPER – Exercise and Health Laboratory, Faculty of Human Kinetics – University of Lisbon, Lisbon, Portugal

,

H. Santa-Clara

²Health and Fitness, Sport Sciences School of Rio Maior – Polytechnic Institute of Santarem, Rio Maior, Portugal

,

D. A. Santos

¹CIPER – Exercise and Health Laboratory, Faculty of Human Kinetics – University of Lisbon, Lisbon, Portugal

,

N. M. Pimenta

²Health and Fitness, Sport Sciences School of Rio Maior – Polytechnic Institute of Santarem, Rio Maior, Portugal

,

C. S. Minderico

¹CIPER – Exercise and Health Laboratory, Faculty of Human Kinetics – University of Lisbon, Lisbon, Portugal

,

B. Fernhall

³Kinesiology, Nutrition, and Rehabilitation, University of Illinois Chicago, Chicago, United States

,

L. B. Sardinha

¹CIPER – Exercise and Health Laboratory, Faculty of Human Kinetics – University of Lisbon, Lisbon, Portugal

› Author Affiliations

Abstract

The aim of this cross-sectional study was to examine the influence of muscular strength on carotid intima-media thickness (cIMT) in children, controlling for the effect of cardiorespiratory fitness (CRF) and central adiposity and to examine if differences among muscular strength tertiles translate to physiological differences. We assessed cIMT of the common carotid artery in 366 children between 11–12 years of age (191 girls). Measures included cIMT assessed with high-resolution ultrasonography, a maximal handgrip strength test, body fat mass and lean mass from DXA and CRF determined using a maximal cycle ergometer test. Association between muscular strength and cIMT adjusted for CRF and central adiposity, as measured by trunk fat, was tested with multiple linear regression analysis. Differences in risk factors among muscular strength groups were tested with ANOVA. The Muscular Strength Index (MSI) was inversely associated with cIMT independently of CRF and central adiposity (p<0.05). The low MSI group had the highest values of cIMT, waist circumference and systolic blood pressure and the lowest CRF (p<0.05). There was an inverse and independent association between muscular strength and cIMT. Low muscular strength was associated with higher levels of cardiovascular disease risk factors in children.

Key words

handgrip - cardiorespiratory fitness - central adiposity - intima-media thickness

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References

References
1 Adegboye AR, Anderssen SA, Froberg K, Sardinha LB, Heitmann BL, Steene-Johannessen J, Kolle E, Andersen LB. Recommended aerobic fitness level for metabolic health in children and adolescents: a study of diagnostic accuracy. Br J Sports Med 2011; 45: 722-728
2 Artero EG, España-Romero V, Ortega FB, Jiménez-Pavón D, Ruiz JR, Vicente-Rodríguez G, Bueno M, Marcos A, Gómez-Martínez S, Urzanqui A, González-Gross M, Moreno LA, Gutiérrez A, Castillo MJ. Health-related fitness in adolescents: underweight, and not only overweight, as an influencing factor. The AVENA study. Scand J Med Sci Sports 2010; 20: 418-427
3 Artero EG, Ruiz JR, Ortega FB, España-Romero V, Vicente-Rodríguez G, Molnar D, Gottrand F, González-Gross M, Breidenassel C, Moreno LA, Gutiérrez A, Group LA, Group HS. Muscular and cardiorespiratory fitness are independently associated with metabolic risk in adolescents: the HELENA study. Pediatr Diabetes 2011; 12: 704-712
4 Begum N, Song Y, Rienzie J, Ragolia L. Vascular smooth muscle cell growth and insulin regulation of mitogen-activated protein kinase in hypertension. Am J Physiol 1998; 275: C42-C49
5 Behm DG, Faigenbaum AD, Falk B, Klentrou P. Canadian Society for Exercise Physiology position paper: resistance training in children and adolescents. Appl Physiol Nutr Metab 2008; 33: 547-561
6 Blair SN, Kampert JB, Kohl 3rd HW, Barlow CE, Macera CA, Paffenbarger Jr RS, Gibbons LW. Influences of cardiorespiratory fitness and other precursors on cardiovascular disease and all-cause mortality in men and women. JAMA 1996; 276: 205-210
7 Cole TJ, Lobstein T. Extended international (IOTF) body mass index cut-offs for thinness, overweight and obesity. Pediatr Obes 2012; 7: 284-294
8 Fernhall B, Agiovlasitis S. Arterial function in youth: window into cardiovascular risk. J Appl Physiol 2008; 105: 325-333
9 Gale CR, Martyn CN, Cooper C, Sayer AA. Grip strength, body composition, and mortality. Int J Epidemiol 2007; 36: 228-235
10 Grøntved A, Ried-Larsen M, Ekelund U, Froberg K, Brage S, Andersen LB. Independent and combined association of muscle strength and cardiorespiratory fitness in youth with insulin resistance and β-cell function in young adulthood: the European Youth Heart Study. Diabetes Care 2013; 36: 2575-2581
11 Grøntved A, Ried-Larsen M, Møller NC, Kristensen PL, Froberg K, Brage S, Andersen LB. Muscle strength in youth and cardiovascular risk in young adulthood (the European Youth Heart Study). Br J Sports Med 2013; Epub ahead of print
12 Hansen HS, Froberg K, Nielsen JR, Hyldebrandt N. A new approach to assessing maximal aerobic power in children: the Odense School Child Study. Eur J Appl Physiol 1989; 58: 618-624
13 Harriss DJ, Atkinson G. Ethical standards in sport and exercise science research: 2014 update•. Int J Sports Med 2013; 34: 1025-1028
14 Heymsfield SB, Smith R, Aulet M, Bensen B, Lichtman S, Wang J, Pierson RN. Appendicular skeletal muscle mass: measurement by dual-photon absorptiometry. Am J Clin Nutr 1990; 52: 214-218
15 Hoeks AP, Willekes C, Boutouyrie P, Brands PJ, Willigers JM, Reneman RS. Automated detection of local artery wall thickness based on M-line signal processing. Ultrasound Med Biol 1997; 23: 1017-1023
16 Ishizu T, Ishimitsu T, Yanagi H, Seo Y, Obara K, Moriyama N, Watanabe S, Yamaguchi I. Effect of age on carotid arterial intima-media thickness in childhood. Heart Vessels 2004; 19: 189-195
17 Jourdan C, Wuhl E, Litwin M, Fahr K, Trelewicz J, Jobs K, Schenk JP, Grenda R, Mehls O, Troger J, Schaefer F. Normative values for intima-media thickness and distensibility of large arteries in healthy adolescents. J Hypertens 2005; 23: 1707-1715
18 Katzmarzyk PT, Craig CL. Musculoskeletal fitness and risk of mortality. Med Sci Sports Exerc 2002; 34: 740-744
19 Klasson-Heggebø L, Andersen LB, Wennlöf AH, Sardinha LB, Harro M, Froberg K, Anderssen SA. Graded associations between cardiorespiratory fitness, fatness, and blood pressure in children and adolescents. Br J Sports Med 2006; 40: 25-29 discussion 25–29
20 Koeijvoets KC, Rodenburg J, Hutten BA, Wiegman A, Kastelein JJ, Sijbrands EJ. Low-density lipoprotein receptor genotype and response to pravastatin in children with familial hypercholesterolemia: substudy of an intima-media thickness trial. Circulation 2005; 112: 3168-3173
21 Lamotte C, Iliescu C, Libersa C, Gottrand F. Increased intima-media thickness of the carotid artery in childhood: a systematic review of observational studies. Eur J Pediatr 2010;
22 Lee S, Bacha F, Hannon T, Kuk JL, Boesch C, Arslanian S. Effects of aerobic versus resistance exercise without caloric restriction on abdominal fat, intrahepatic lipid, and insulin sensitivity in obese adolescent boys: a randomized, controlled trial. Diabetes 2012; 61: 2787-2795
23 Lloyd-Jones DM, Hong Y, Labarthe D, Mozaffarian D, Appel LJ, Van Horn L, Greenlund K, Daniels S, Nichol G, Tomaselli GF, Arnett DK, Fonarow GC, Ho PM, Lauer MS, Masoudi FA, Robertson RM, Roger V, Schwamm LH, Sorlie P, Yancy CW, Rosamond WD. Committee AHASPTF, Statistics. Defining and setting national goals for cardiovascular health promotion and disease reduction: the American Heart Association’s strategic Impact Goal through 2020 and beyond. Circulation 2010; 121: 586-613
24 Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M. Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation 2007; 115: 459-467
25 Lynch NA, Metter EJ, Lindle RS, Fozard JL, Tobin JD, Roy TA, Fleg JL, Hurley BF. Muscle quality. I. Age-associated differences between arm and leg muscle groups. J Appl Physiol 1999; 86: 188-194
26 Meinders JM, Kornet L, Hoeks AP. Assessment of spatial inhomogeneities in intima media thickness along an arterial segment using its dynamic behavior. Am J Physiol 2003; 285: H384-H391
27 Melo X, Santa-Clara H, Pimenta NM, Carrolo M, Martins SS, Minderico CS, Fernhall B, Sardinha LB. Body composition phenotypes and carotid intima-media thickness in 11–13-year-old children. Eur J Pediatr 2013;
28 Melo X, Santa-Clara H, Pimenta NM, Martins SS, Minderico CS, Fernhall B, Sardinha LB. Intima-media thickness in 11–13 years-old children: variation attributed to sedentary behavior, physical activity, cardiorespiratory fitness and waist circumference. J Phys Act Health 2014;
29 Meyer AA, Kundt G, Lenschow U, Schuff-Werner P, Kienast W. Improvement of early vascular changes and cardiovascular risk factors in obese children after a six-month exercise program. J Am Coll Cardiol 2006; 48: 1865-1870
30 Mirwald RL, Baxter-Jones AD, Bailey DA, Beunen GP. An assessment of maturity from anthropometric measurements. Med Sci Sports Exerc 2002; 34: 689-694
31 Nagai M, Kamide K, Rakugi H, Takiuchi S, Imai M, Kida I, Matsukawa N, Higaki J, Ogihara T. Role of endothelin-1 induced by insulin in the regulation of vascular cell growth. Am J Hypertens 2003; 16: 223-228
32 Ortega FB, Artero EG, Ruiz JR, España-Romero V, Jiménez-Pavón D, Vicente-Rodriguez G, Moreno LA, Manios Y, Béghin L, Ottevaere C, Ciarapica D, Sarri K, Dietrich S, Blair SN, Kersting M, Molnar D, González-Gross M, Gutiérrez A, Sjöström M, Castillo MJ, study H. Physical fitness levels among European adolescents: the HELENA study. Br J Sports Med 2011; 45: 20-29
33 Ortega FB, Silventoinen K, Tynelius P, Rasmussen F. Muscular strength in male adolescents and premature death: cohort study of one million participants. BMJ 2012; 345: e7279
34 Pahkala K, Hietalampi H, Laitinen TT, Viikari JS, Rönnemaa T, Niinikoski H, Lagström H, Talvia S, Jula A, Heinonen OJ, Juonala M, Simell O, Raitakari OT. Ideal cardiovascular health in adolescence: effect of lifestyle intervention and association with vascular intima-media thickness and elasticity (the Special Turku Coronary Risk Factor Intervention Project for Children [STRIP] study). Circulation 2013; 127: 2088-2096
35 Pahkala K, Hietalampi H, Laitinen TT, Viikari JS, Rönnemaa T, Niinikoski H, Lagström H, Talvia S, Jula A, Heinonen OJ, Juonala M, Simell O, Raitakari OT. Ideal Cardiovascular Health in Adolescence: Effect of Lifestyle Intervention and Association with Vascular Intima-Media Thickness and Elasticity (the STRIP Study). Circulation 2013;
36 Sandvik L, Erikssen J, Thaulow E, Erikssen G, Mundal R, Rodahl K. Physical fitness as a predictor of mortality among healthy, middle-aged Norwegian men. N Engl J Med 1993; 328: 533-537
37 Santos DA, Dawson JA, Matias CN, Rocha PM, Minderico CS, Allison DB, Sardinha LB, Silva AM. Reference values for body composition and anthropometric measurements in athletes. PLoS One 2014; 9: e97846
38 Sardinha LB, Santos R, Vale S, ESilva MJ, Raimundo AM, Moreira H, Baptista F, Mota J. Waist circumference percentiles for Portuguese children and adolescents aged 10 to 18 years. Eur J Pediatr 2012; 171: 499-505
39 Sass C, Herbeth B, Chapet O, Siest G, Visvikis S, Zannad F. Intima-media thickness and diameter of carotid and femoral arteries in children, adolescents and adults from the Stanislas cohort: effect of age, sex, anthropometry and blood pressure. J Hypertens 1998; 16: 1593-1602
40 Stabouli S, Kotsis V, Karagianni C, Zakopoulos N, Konstantopoulos A. Blood pressure and carotid artery intima-media thickness in children and adolescents: the role of obesity. Hellenic J Cardiol 2012; 53: 41-47
41 Stary HC. Evolution and progression of atherosclerotic lesions in coronary arteries of children and young adults. Arteriosclerosis 1989; 9: I19-I32
42 Steene-Johannessen J, Anderssen SA, Kolle E, Andersen LB. Low muscle fitness is associated with metabolic risk in youth. Med Sci Sports Exerc 2009; 41: 1361-1367
43 Urbina EM, Williams RV, Alpert BS, Collins RT, Daniels SR, Hayman L, Jacobson M, Mahoney L, Mietus-Snyder M, Rocchini A, Steinberger J, McCrindle B. Noninvasive assessment of subclinical atherosclerosis in children and adolescents: recommendations for standard assessment for clinical research: a scientific statement from the American Heart Association. Hypertension 2009; 54: 919-950
44 Van Der Heijden GJ, Wang ZJ, Chu Z, Toffolo G, Manesso E, Sauer PJ, Sunehag AL. Strength exercise improves muscle mass and hepatic insulin sensitivity in obese youth. Med Sci Sports Exerc 2010; 42: 1973-1980
45 Wiegman A, de Groot E, Hutten BA, Rodenburg J, Gort J, Bakker HD, Sijbrands EJ, Kastelein JJ. Arterial intima-media thickness in children heterozygous for familial hypercholesterolaemia. Lancet 2004; 363: 369-370
46 Woo KS, Chook P, Yu CW, Sung RY, Qiao M, Leung SS, Lam CW, Metreweli C, Celermajer DS. Effects of diet and exercise on obesity-related vascular dysfunction in children. Circulation 2004; 109: 1981-1986
47 Yang Q, Cogswell ME, Flanders WD, Hong Y, Zhang Z, Loustalot F, Gillespie C, Merritt R, Hu FB. Trends in cardiovascular health metrics and associations with all-cause and CVD mortality among US adults. JAMA 2012; 307: 1273-1283