A 2 year physical activity and dietary intervention attenuates the increase in insulin resistance in a general population of children: the PANIC study

Timo A Lakka, Niina Lintu, Juuso Väistö, Anna Viitasalo, Taisa Sallinen, Eero A Haapala, Tuomo T Tompuri, Sonja Soininen, Panu Karjalainen, Theresia M Schnurr, Santtu Mikkonen, Mustafa Atalay, Tuomas O Kilpeläinen, Tomi Laitinen, David E Laaksonen, Kai Savonen, Soren Brage, Ursula Schwab, Jarmo Jääskeläinen, Virpi Lindi, Aino-Maija Eloranta, Timo A Lakka, Niina Lintu, Juuso Väistö, Anna Viitasalo, Taisa Sallinen, Eero A Haapala, Tuomo T Tompuri, Sonja Soininen, Panu Karjalainen, Theresia M Schnurr, Santtu Mikkonen, Mustafa Atalay, Tuomas O Kilpeläinen, Tomi Laitinen, David E Laaksonen, Kai Savonen, Soren Brage, Ursula Schwab, Jarmo Jääskeläinen, Virpi Lindi, Aino-Maija Eloranta

Abstract

Aims/hypothesis: We studied for the first time the long-term effects of a combined physical activity and dietary intervention on insulin resistance and fasting plasma glucose in a general population of predominantly normal-weight children.

Methods: We carried out a 2 year non-randomised controlled trial in a population sample of 504 children aged 6-9 years at baseline. The children were allocated to a combined physical activity and dietary intervention group (306 children at baseline, 261 children at 2-year follow-up) or a control group (198 children, 177 children) without blinding. We measured fasting insulin and fasting glucose, calculated HOMA-IR, assessed physical activity and sedentary time by combined heart rate and body movement monitoring, assessed dietary factors by a 4 day food record, used the Finnish Children Healthy Eating Index (FCHEI) as a measure of overall diet quality, and measured body fat percentage (BF%) and lean body mass by dual-energy x-ray absorptiometry. The intervention effects on insulin, glucose and HOMA-IR were analysed using the intention-to-treat principle and linear mixed-effects models after adjustment for sex, age at baseline, and pubertal status at baseline and 2 year follow-up. The measures of physical activity, sedentary time, diet and body composition at baseline and 2 year follow-up were entered one-by-one as covariates into the models to study whether changes in these variables might partly explain the observed intervention effects.

Results: Compared with the control group, fasting insulin increased 4.65 pmol/l less (absolute change +8.96 vs +13.61 pmol/l) and HOMA-IR increased 0.18 units less (+0.31 vs +0.49 units) over 2 years in the combined physical activity and dietary intervention group. The intervention effects on fasting insulin (regression coefficient β for intervention effect -0.33 [95% CI -0.62, -0.04], p = 0.026) and HOMA-IR (β for intervention effect -0.084 [95% CI -0.156, -0.012], p = 0.023) were statistically significant after adjustment for sex, age at baseline, and pubertal status at baseline and 2 year follow-up. The intervention had no effect on fasting glucose, BF% or lean body mass. Changes in total physical activity energy expenditure, light physical activity, moderate-to-vigorous physical activity, total sedentary time, the reported consumption of high-fat (≥60%) vegetable oil-based spreads, and FCHEI, but not a change in BF% or lean body mass, partly explained the intervention effects on fasting insulin and HOMA-IR.

Conclusions/interpretation: The combined physical activity and dietary intervention attenuated the increase in insulin resistance over 2 years in a general population of predominantly normal-weight children. This beneficial effect was partly mediated by changes in physical activity, sedentary time and diet but not changes in body composition.

Trial registration: ClinicalTrials.gov NCT01803776 Graphical abstract.

Keywords: Body fat; Children; Diet; Glucose; HOMA-IR; Insulin; Intervention; Lean body mass; Physical activity; Sedentary time.

Figures

https://www.ncbi.nlm.nih.gov/pmc/articles/instance/7527318/bin/125_2020_5250_Figa_HTML.jpg
Graphical abstract
Fig. 1
Fig. 1
Flowchart of the PANIC study

References

    1. Chen L, Magliano DJ, Zimmet PZ. The worldwide epidemiology of type 2 diabetes mellitus - present and future perspectives. Nat Rev Endocrinol. 2011;8(4):228–236. doi: 10.1038/nrendo.2011.183.
    1. Fazeli Farsani S, van der Aa MP, van der Vorst MMJ, et al. Global trends in the incidence and prevalence of type 2 diabetes in children and adolescents: a systematic review and evaluation of methodological approaches. Diabetologia. 2013;56(7):1471–1488. doi: 10.1007/s00125-013-2915-z.
    1. Paulweber B, Valensi P, Lindström J, et al. A European evidence-based guideline for the prevention of type 2 diabetes. Horm Metab Res. 2010;42(Suppl 1):S3–S36. doi: 10.1055/s-0029-1240928.
    1. Laakso M. Is insulin resistance a feature of or a primary risk factor for cardiovascular disease? Curr Diab Rep. 2015;15(12):105. doi: 10.1007/s11892-015-0684-4.
    1. Moran A, Jacobs DR, Jr, Steinberger J, et al. Insulin resistance during puberty: results from clamp studies in 357 children. Diabetes. 1999;48(10):2039–2044. doi: 10.2337/diabetes.48.10.2039.
    1. Jeffery AN, Metcalf BS, Hosking J, et al. Age before stage: insulin resistance rises before the onset of puberty: a 9-year longitudinal study (EarlyBird 26) Diabetes Care. 2012;35(3):536–541. doi: 10.2337/dc11-1281.
    1. Ferguson MA, Gutin B, Le NA, et al. Effects of exercise training and its cessation on components of the insulin resistance syndrome in obese children. Int J Obes Relat Metab Disord. 1999;23(8):889–895. doi: 10.1038/sj.ijo.0800968.
    1. Carrel AL, Clark RR, Peterson SE, et al. Improvement of fitness, body composition, and insulin sensitivity in overweight children in a school-based exercise program: a randomized, controlled study. Arch Pediatr Adolesc Med. 2005;159(10):963–968. doi: 10.1001/archpedi.159.10.963.
    1. Bell LM, Watts K, Siafarikas A, et al. Exercise alone reduces insulin resistance in obese children independently of changes in body composition. J Clin Endocrinol Metab. 2007;92(11):4230–4235. doi: 10.1210/jc.2007-0779.
    1. Davis CL, Pollock NK, Waller JL, et al. Exercise dose and diabetes risk in overweight and obese children: a randomized controlled trial. JAMA. 2012;308(11):1103–1112. doi: 10.1001/2012.jama.10762.
    1. Lee S, Bacha F, Hannon T, et al. 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(11):2787–2795. doi: 10.2337/db12-0214.
    1. Mendelson M, Michallet AS, Monneret D, et al. Impact of exercise training without caloric restriction on inflammation, insulin resistance and visceral fat mass in obese adolescents. Pediatr Obes. 2015;10(4):311–319. doi: 10.1111/ijpo.255.
    1. Ho M, Garnett SP, Baur LA, et al. Impact of dietary and exercise interventions on weight change and metabolic outcomes in obese children and adolescents: a systematic review and meta-analysis of randomized trials. JAMA Pediatr. 2013;167(8):759–768. doi: 10.1001/jamapediatrics.2013.1453.
    1. Savoye M, Shaw M, Dziura J, et al. Effects of a weight management program on body composition and metabolic parameters in overweight children: a randomized controlled trial. JAMA. 2007;297(24):2697–2704. doi: 10.1001/jama.297.24.2697.
    1. Shaw M, Savoye M, Cali A, et al. Effect of a successful intensive lifestyle program on insulin sensitivity and glucose tolerance in obese youth. Diabetes Care. 2009;32(1):45–47. doi: 10.2337/dc08-0808.
    1. Davis JN, Kelly LA, Lane CJ, et al. Randomized control trial to improve adiposity and insulin resistance in overweight Latino adolescents. Obesity (Silver Spring) 2009;17(8):1542–1548. doi: 10.1038/oby.2009.19.
    1. Savoye M, Caprio S, Dziura J, et al. Reversal of early abnormalities in glucose metabolism in obese youth: results of an intensive lifestyle randomized controlled trial. Diabetes Care. 2014;37(2):317–324. doi: 10.2337/dc13-1571.
    1. Harder-Lauridsen NM, Birk NM, Ried-Larsen M, et al. A randomized controlled trial on a multicomponent intervention for overweight school-aged children – Copenhagen, Denmark. BMC Pediatr. 2014;14(1):273. doi: 10.1186/1471-2431-14-273.
    1. Marson EC, Delevatti RS, Prado AK, et al. Effects of aerobic, resistance, and combined exercise training on insulin resistance markers in overweight or obese children and adolescents: a systematic review and meta-analysis. Prev Med. 2016;93:211–218. doi: 10.1016/j.ypmed.2016.10.020.
    1. Kaitosaari T, Rönnemaa T, Viikari J, et al. Low-saturated fat dietary counseling starting in infancy improves insulin sensitivity in 9-year-old healthy children: the Special Turku Coronary Risk Factor Intervention Project for Children (STRIP) study. Diabetes Care. 2006;29(4):781–785. doi: 10.2337/diacare.29.04.06.dc05-1523.
    1. Li X-H, Lin S, Guo H, et al. Effectiveness of a school-based physical activity intervention on obesity in school children: a nonrandomized controlled trial. BMC Public Health. 2014;14(1):1282. doi: 10.1186/1471-2458-14-1282.
    1. Viitasalo A, Eloranta AM, Lintu N, et al. The effects of a 2-year individualized and family-based lifestyle intervention on physical activity, sedentary behavior and diet in children. Prev Med. 2016;87:81–88. doi: 10.1016/j.ypmed.2016.02.027.
    1. Venäläinen TM, Viitasalo AM, Schwab US, et al. Effect of a 2-y dietary and physical activity intervention on plasma fatty acid composition and estimated desaturase and elongase activities in children: the Physical Activity and Nutrition in Children Study. Am J Clin Nutr. 2016;104(4):964–972. doi: 10.3945/ajcn.116.136580.
    1. Matthews DR, Hosker JP, Rudenski AS, et al. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–419. doi: 10.1007/BF00280883.
    1. Väistö J, Haapala EA, Viitasalo A, et al. Longitudinal associations of physical activity and sedentary time with cardiometabolic risk factors in children. Scand J Med Sci Sports. 2019;29(1):113–123. doi: 10.1111/sms.13315.
    1. Brage S, Brage N, Franks PW, et al. Reliability and validity of the combined heart rate and movement sensor Actiheart. Eur J Clin Nutr. 2005;59(4):561–570. doi: 10.1038/sj.ejcn.1602118.
    1. Brage S, Brage N, Franks PW, et al. Branched equation modeling of simultaneous accelerometry and heart rate monitoring improves estimate of directly measured physical activity energy expenditure. J Appl Physiol. 2004;96(1):343–351. doi: 10.1152/japplphysiol.00703.2003.
    1. Strath SJ, Brage S, Ekelund U. Integration of physiological and accelerometer data to improve physical activity assessment. Med Sci Sports Exerc. 2005;37(Supplement):S563–S571. doi: 10.1249/01.mss.0000185650.68232.3f.
    1. Brage S, Westgate K, Franks PW, et al. Estimation of free-living energy expenditure by heart rate and movement sensing: a doubly-labelled water study. PLoS One. 2015;10(9):1–19. doi: 10.1371/journal.pone.0137206.
    1. Eloranta A-M, Schwab U, Venäläinen T, et al. Dietary quality indices in relation to cardiometabolic risk among Finnish children aged 6–8 years – the PANIC study. Nutr Metab Cardiovasc Dis. 2016;26(9):833–841. doi: 10.1016/j.numecd.2016.05.005.
    1. Kyttälä P, Erkkola M, Lehtinen-Jacks S, et al. Finnish Children Healthy Eating Index (FCHEI) and its associations with family and child characteristics in pre-school children. Public Health Nutr. 2014;17(11):2519–2527. doi: 10.1017/S1368980013002772.
    1. Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969;44(235):291–303. doi: 10.1136/adc.44.235.291.
    1. Marshall WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970;45(239):13–23. doi: 10.1136/adc.45.239.13.
    1. Caprio S, Bronson M, Sherwin RS, et al. Co-existence of severe insulin resistance and hyperinsulinaemia in pre-adolescent obese children. Diabetologia. 1996;39(12):1489–1497. doi: 10.1007/s001250050603.
    1. Arslanian S, Suprasongsin C. Insulin sensitivity, lipids, and body composition in childhood: is ‘syndrome X’ present? J Clin Endocrinol Metab. 1996;81(3):1058–1062. doi: 10.1210/jcem.81.3.8772576.
    1. Stumvoll M. Control of glycaemia: from molecules to men. Minkowski Lecture 2003. Diabetologia. 2004;47(5):770–781. doi: 10.1007/s00125-004-1400-0.
    1. Wojtaszewski JFP, Richter EA. Effect of acute exercise and training on insulin action and sensitivity: focus on molecular mechanisms in muscle. Essays Biochem. 2006;42:31–46. doi: 10.1042/bse0420031.
    1. Holloszy JO. Exercise-induced increase in muscle insulin sensitivity. J Appl Physiol. 2005;99(1):338–343. doi: 10.1152/japplphysiol.00123.2005.
    1. Lillioja S, Young AA, Culter CL, et al. Skeletal muscle capillary density and fiber type are possible determinants of in vivo insulin resistance in man. J Clin Invest. 1987;80(2):415–424. doi: 10.1172/JCI113088.
    1. Hawley JA, Hargreaves M, Zierath JR. Signalling mechanisms in skeletal muscle: role in substrate selection and muscle adaptation. Essays Biochem. 2006;42:1–12. doi: 10.1042/bse0420001.
    1. Turcotte LP, Richter EA, Kiens B. Increased plasma FFA uptake and oxidation during prolonged exercise in trained vs. untrained humans. Am J Phys. 1992;262:E791–E799.
    1. Bruce CR, Thrush AB, Mertz VA, et al. Endurance training in obese humans improves glucose tolerance and mitochondrial fatty acid oxidation and alters muscle lipid content. Am J Physiol Endocrinol Metab. 2006;291(1):E99–E107. doi: 10.1152/ajpendo.00587.2005.
    1. Petersen AM, Pedersen BK. The anti-inflammatory effect of exercise. J Appl Physiol. 2005;98(4):1154–1162. doi: 10.1152/japplphysiol.00164.2004.
    1. Salminen A, Vihko V. Endurance training reduces the susceptibility of mouse skeletal muscle to lipid peroxidation in vitro. Acta Physiol Scand. 1983;117(1):109–113. doi: 10.1111/j.1748-1716.1983.tb07184.x.
    1. Corcoran MP, Lamon-Fava S, Fielding RA. Skeletal muscle lipid deposition and insulin resistance: effect of dietary fatty acids and exercise. Am J Clin Nutr. 2007;85(3):662–677. doi: 10.1093/ajcn/85.3.662.
    1. Sergi D, Naumovski N, Heilbronn LK, et al. Mitochondrial (dys)function and insulin resistance: from pathophysiological molecular mechanisms to the impact of diet. Front Physiol. 2019;10:532. doi: 10.3389/fphys.2019.00532.
    1. Metcalf BS, Hosking J, Henley WE, et al. Physical activity attenuates the mid-adolescent peak in insulin resistance but by late adolescence the effect is lost: a longitudinal study with annual measures from 9-16 years (EarlyBird 66) Diabetologia. 2015;58(12):2699–2708. doi: 10.1007/s00125-015-3714-5.
    1. Oranta O, Pahkala K, Ruottinen S, et al. Infancy-onset dietary counseling of low-saturated-fat diet improves insulin sensitivity in healthy adolescents 15-20 years of age: the Special Turku Coronary Risk Factor Intervention Project (STRIP) study. Diabetes Care. 2013;36(10):2952–2959. doi: 10.2337/dc13-0361.
    1. Saari A, Sankilampi U, Hannila ML, et al. New Finnish growth references for children and adolescents aged 0 to 20 years: length/height-for-age, weight-for-length/height, and body mass index-for-age. Ann Med. 2011;43(3):235–248. doi: 10.3109/07853890.2010.515603.
    1. Showell NN, Fawole O, Segal J, et al. A systematic review of home-based childhood obesity prevention studies. Pediatrics. 2013;132(1):E193–E200. doi: 10.1542/peds.2013-0786.

Source: PubMed

Спонсоры и соавторы

Заболевания

Медикаментозные вмешательства

Подписаться