Multilevel Approach of a 1-Year Program of Dietary and Exercise Interventions on Bone Mineral Content and Density in Metabolic Syndrome--the RESOLVE Randomized Controlled Trial

Daniel Courteix, João Valente-dos-Santos, Béatrice Ferry, Gérard Lac, Bruno Lesourd, Robert Chapier, Geraldine Naughton, Geoffroy Marceau, Manuel João Coelho-e-Silva, Agnès Vinet, Guillaume Walther, Philippe Obert, Frédéric Dutheil, Daniel Courteix, João Valente-dos-Santos, Béatrice Ferry, Gérard Lac, Bruno Lesourd, Robert Chapier, Geraldine Naughton, Geoffroy Marceau, Manuel João Coelho-e-Silva, Agnès Vinet, Guillaume Walther, Philippe Obert, Frédéric Dutheil

Abstract

Background: Weight loss is a public health concern in obesity-related diseases such as metabolic syndrome (MetS). However, restrictive diets might induce bone loss. The nature of exercise and whether exercise with weight loss programs can protect against potential bone mass deficits remains unclear. Moreover, compliance is essential in intervention programs. Thus, we aimed to investigate the effects that modality and exercise compliance have on bone mineral content (BMC) and density (BMD).

Methods: We investigated 90 individuals with MetS who were recruited for the 1-year RESOLVE trial. Community-dwelling seniors with MetS were randomly assigned into three different modalities of exercise (intensive resistance, intensive endurance, moderate mixed) combined with a restrictive diet. They were compared to 44 healthy controls who did not undergo the intervention.

Results: This intensive lifestyle intervention (15-20 hours of training/week + restrictive diet) resulted in weight loss, body composition changes and health improvements. Baseline BMC and BMD for total body, lumbar spine and femoral neck did not differ between MetS groups and between MetS and controls. Despite changes over time, BMC or BMD did not differ between the three modalities of exercise and when compared with the controls. However, independent of exercise modality, compliant participants increased their BMC and BMD compared with their less compliant peers. Decreases in total body lean mass and negative energy balance significantly and independently contributed to decreases in lumbar spine BMC.

Conclusion: After the one year intervention, differences relating to exercise modalities were not evident. However, compliance with an intensive exercise program resulted in a significantly higher bone mass during energy restriction than non-compliance. Exercise is therefore beneficial to bone in the context of a weight loss program.

Trial registration: ClinicalTrials.gov NCT00917917.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Flow chart of participants.
Fig 1. Flow chart of participants.
re: moderate-resistance-moderate-endurance; Re: high-Resistance-moderate-endurance; rE: moderate-resistance-high-Endurance.
Fig 2. Changes (360 days) on total…
Fig 2. Changes (360 days) on total body bone mineral content (BMC) and density (BMD), lumbar spine BMC and BMD and femoral neck BMC and BMD for re, Re and rE groups.
re: moderate-resistance-moderate-endurance; Re: high-Resistance-moderate-endurance; rE: moderate-resistance-high-Endurance. There were no significant differences in BMD and BMC parameters between re, Re and rE participants across the intervention. Participants in the intervention did not have significantly greater or lower bone mass or density development than controls.
Fig 3. Compliance effect (360 days) on…
Fig 3. Compliance effect (360 days) on total body bone mineral content (BMC), lumbar spine BMC and femoral neck BMC for re, Re and rE groups.
re: moderate-resistance-moderate-endurance; Re: high-Resistance-moderate-endurance; rE: moderate-resistance-high-Endurance. * Compliant participants significantly different from non-compliants (p<0.05). ‡ Non-compliant participants significantly different from controls.
Fig 4. Compliance effect (360 days) on…
Fig 4. Compliance effect (360 days) on total body bone mineral density (BMD), lumbar spine BMD and femoral neck BMD for re, Re and rE groups.
re: moderate-resistance-moderate-endurance; Re: high-Resistance-moderate-endurance; rE: moderate-resistance-high-Endurance. *Compliant participants significantly different from non-compliants (p<0.05).

References

    1. Pedersen SD (2013) Metabolic complications of obesity. Best Pract Res Clin Endocrinol Metab 27: 179–193. 10.1016/j.beem.2013.02.004
    1. Shapses SA, Riedt CS (2006) Bone, body weight, and weight reduction: what are the concerns? J Nutr 136: 1453–1456.
    1. Hinton PS, LeCheminant JD, Smith BK, Rector RS, Donnelly JE (2009) Weight loss-induced alterations in serum markers of bone turnover persist during weight maintenance in obese men and women. Journal of the American College of Nutrition 28: 565–573.
    1. Sukumar D, Ambia-Sobhan H, Zurfluh R, Schlussel Y, Stahl TJ, Gordon CL, et al. (2011) Areal and volumetric bone mineral density and geometry at two levels of protein intake during caloric restriction: A randomized, controlled trial. Journal of Bone and Mineral Research 26: 1339–1348. 10.1002/jbmr.318
    1. Redman LM, Rood J, Anton SD, Champagne C, Smith SR, Ravussin E (2008) Calorie restriction and bone health in young, overweight individuals. Archives of Internal Medicine 168: 1859–1866. 10.1001/archinte.168.17.1859
    1. Hamilton KC, Fisher G, Roy JL, Gower BA, Hunter GR (2013) The effects of weight loss on relative bone mineral density in premenopausal women. Obesity (Silver Spring) 21: 441–448. 10.1002/oby.20052
    1. Villareal DT, Chode S, Parimi N, Sinacore DR, Hilton T, Armamento-Villareal R, et al. (2011) Weight loss, exercise, or both and physical function in obese older adults. N Engl J Med 364: 1218–1229. 10.1056/NEJMoa1008234
    1. Villareal DT, Fontana L, Weiss EP, Racette SB, Steger-May K, Schechtman KB, et al. (2006) Bone mineral density response to caloric restriction-induced weight loss or exercise-induced weight loss: a randomized controlled trial. Archives of Internal Medicine 166: 2502–2510.
    1. Shapses SA, Sukumar D, Schneider SH, Schlussel Y, Sherrell RM, Field MP, et al. (2013) Vitamin D supplementation and calcium absorption during caloric restriction: a randomized double-blind trial. American Journal of Clinical Nutrition 97: 637–645. 10.3945/ajcn.112.044909
    1. Shapses SA, Sukumar D (2012) Bone metabolism in obesity and weight loss. Annual Review of Nutrition 32: 287–309. 10.1146/annurev.nutr.012809.104655
    1. Hinton PS, Rector RS, Donnelly JE, Smith BK, Bailey B (2010) Total body bone mineral content and density during weight loss and maintenance on a low- or recommended-dairy weight-maintenance diet in obese men and women. European Journal of Clinical Nutrition 64: 392–399. 10.1038/ejcn.2009.156
    1. Pop LC, Sukumar D, Tomaino K, Schlussel Y, Schneider SH, Gordon CL, et al. (2015) Moderate weight loss in obese and overweight men preserves bone quality. American Journal of Clinical Nutrition 101: 659–667. 10.3945/ajcn.114.088534
    1. Armamento-Villareal R, Sadler C, Napoli N, Shah K, Chode S, Sinacore DR, et al. (2012) Weight loss in obese older adults increases serum sclerostin and impairs hip geometry but both are prevented by exercise training. Journal of Bone and Mineral Research 27: 1215–1221. 10.1002/jbmr.1560
    1. Bielohuby M, Matsuura M, Herbach N, Kienzle E, Slawik M, Hoeflich A, et al. (2010) Short-term exposure to low-carbohydrate, high-fat diets induces low bone mineral density and reduces bone formation in rats. Journal of Bone and Mineral Research 25: 275–284. 10.1359/jbmr.090813
    1. Ricci TA, Heymsfield SB, Pierson RN Jr., Stahl T, Chowdhury HA, Shapses SA (2001) Moderate energy restriction increases bone resorption in obese postmenopausal women. American Journal of Clinical Nutrition 73: 347–352.
    1. Alberti KG, Zimmet P, Shaw J (2005) The metabolic syndrome—a new worldwide definition. Lancet 366: 1059–1062.
    1. Deng Y, Scherer PE (2010) Adipokines as novel biomarkers and regulators of the metabolic syndrome. Annals of the New York Academy of Sciences 1212: E1–E19.
    1. Swanberg M, McGuigan FE, Ivaska KK, Gerdhem P, Akesson K (2012) Polymorphisms in the inflammatory genes CIITA, CLEC16A and IFNG influence BMD, bone loss and fracture in elderly women. PLoS One 7: e47964 10.1371/journal.pone.0047964
    1. Guadalupe-Grau A, Fuentes T, Guerra B, Calbet JA (2009) Exercise and bone mass in adults. Sports Med 39: 439–468. 10.2165/00007256-200939060-00002
    1. Shah K, Armamento-Villareal R, Parimi N, Chode S, Sinacore DR, Hilton TN, et al. (2011) Exercise training in obese older adults prevents increase in bone turnover and attenuates decrease in hip BMD induced by weight loss despite decline in bone-active hormones. J Bone Miner Res.
    1. Pritchard JE, Nowson CA, Wark JD (1996) Bone loss accompanying diet-induced or exercise-induced weight loss: a randomised controlled study. International Journal of Obesity and Related Metabolic Disorders 20: 513–520.
    1. Fappa E, Yannakoulia M, Pitsavos C, Skoumas I, Valourdou S, Stefanadis C (2008) Lifestyle intervention in the management of metabolic syndrome: could we improve adherence issues? Nutrition 24: 286–291. 10.1016/j.nut.2007.11.008
    1. Dutheil F, Lac G, Lesourd B, Chapier R, Walther G, Vinet A, et al. (2013) Different modalities of exercise to reduce visceral fat mass and cardiovascular risk in metabolic syndrome: the RESOLVE randomized trial. International Journal of Cardiology 168: 3634–3642. 10.1016/j.ijcard.2013.05.012
    1. Dutheil F, Walther G, Chapier R, Mnatzaganian G, Lesourd B, Naughton G, et al. (2014) Atherogenic subfractions of lipoproteins in the treatment of metabolic syndrome by physical activity and diet—the RESOLVE Trial. Lipids Health Dis 13: 112 10.1186/1476-511X-13-112
    1. Kamel EG, McNeill G, Han TS, Smith FW, Avenell A, Davidson L, et al. (1999) Measurement of abdominal fat by magnetic resonance imaging, dual-energy X-ray absorptiometry and anthropometry in non-obese men and women. Int J Obes Relat Metab Disord 23: 686–692.
    1. Silcocks P (2012) How many strata in an RCT? A flexible approach. British Journal of Cancer 106: 1259–1261. 10.1038/bjc.2012.84
    1. Dutheil F, Lac G, Courteix D, Dore E, Chapier R, Roszyk L, et al. (2012) Treatment of metabolic syndrome by combination of physical activity and diet needs an optimal protein intake: a randomized controlled trial. Nutr J 11: 72 10.1186/1475-2891-11-72
    1. Baxter-Jones AD, Mirwald RL, McKay HA, Bailey DA (2003) A longitudinal analysis of sex differences in bone mineral accrual in healthy 8-19-year-old boys and girls. Annals of Human Biology 30: 160–175.
    1. Jackowski SA, Baxter-Jones AD, Gruodyte-Raciene R, Kontulainen SA, Erlandson MC (2015) A longitudinal study of bone area, content, density, and strength development at the radius and tibia in children 4–12 years of age exposed to recreational gymnastics. Osteoporosis International.
    1. Slinker BK, Glantz SA (1985) Multiple regression for physiological data analysis: the problem of multicollinearity. American Journal of Physiology 249: R1–12.
    1. Bemben DA, Bemben MG (2011) Dose-response effect of 40 weeks of resistance training on bone mineral density in older adults. Osteoporosis International 22: 179–186. 10.1007/s00198-010-1182-9
    1. Jensen LB, Quaade F, Sorensen OH (1994) Bone loss accompanying voluntary weight loss in obese humans. J Bone Miner Res 9: 459–463.
    1. Compston JE, Laskey MA, Croucher PI, Coxon A, Kreitzman S (1992) Effect of diet-induced weight loss on total body bone mass. Clin Sci (Lond) 82: 429–432.
    1. Hyldstrup L, Andersen T, McNair P, Breum L, Transbol I (1993) Bone metabolism in obesity: changes related to severe overweight and dietary weight reduction. Acta Endocrinol (Copenh) 129: 393–398.
    1. Kemmler W, von Stengel S (2014) Dose-response effect of exercise frequency on bone mineral density in post-menopausal, osteopenic women. Scandinavian Journal of Medicine and Science in Sports 24: 526–534. 10.1111/sms.12024
    1. Santhanakrishnan I, Lakshminarayanan S, Kar SS (2014) Factors affecting compliance to management of diabetes in Urban Health Center of a tertiary care teaching hospital of south India. J Nat Sci Biol Med 5: 365–368. 10.4103/0976-9668.136186
    1. Ishikawa S, Kim Y, Kang M, Morgan DW (2013) Effects of weight-bearing exercise on bone health in girls: a meta-analysis. Sports Medicine 43: 875–892. 10.1007/s40279-013-0060-y
    1. Wolff I, van Croonenborg JJ, Kemper HC, Kostense PJ, Twisk JW (1999) The effect of exercise training programs on bone mass: a meta-analysis of published controlled trials in pre- and postmenopausal women. Osteoporosis International 9: 1–12.
    1. Ben Chihaoui M, Elleuch M, Sahli H, Cheour I, Romdhane RH, Sellami S (2008) [Stress facture: epidemiology, physiopathology and risk factors]. Tunisie Medicale 86: 1031–1035.
    1. Martin TJ, Seeman E (2008) Bone remodelling: its local regulation and the emergence of bone fragility. Best Pract Res Clin Endocrinol Metab 22: 701–722. 10.1016/j.beem.2008.07.006
    1. Dutheil F, Lesourd B, Courteix D, Chapier R, Dore E, Lac G (2010) Blood lipids and adipokines concentrations during a 6-month nutritional and physical activity intervention for metabolic syndrome treatment. Lipids Health Dis 9: 148 10.1186/1476-511X-9-148
    1. Beverly MC, Rider TA, Evans MJ, Smith R (1989) Local bone mineral response to brief exercise that stresses the skeleton. BMJ 299: 233–235.
    1. Labouesse MA, Gertz ER, Piccolo BD, Souza EC, Schuster GU, Witbracht MG, et al. (2014) Associations among endocrine, inflammatory, and bone markers, body composition and weight loss induced bone loss. Bone 64: 138–146. 10.1016/j.bone.2014.03.047
    1. Sarkis KS, Pinheiro Mde M, Szejnfeld VL, Martini LA (2012) High bone density and bone health. Endocrinol Nutr 59: 207–214. 10.1016/j.endonu.2011.10.010
    1. Theodoratou E, Tzoulaki I, Zgaga L, Ioannidis JP (2014) Vitamin D and multiple health outcomes: umbrella review of systematic reviews and meta-analyses of observational studies and randomised trials. BMJ 348: g2035 10.1136/bmj.g2035
    1. Chaplais E, Thivel D, Greene D, Dutheil F, Duche P, Naughton G, et al. (2015) Bone-adiposity cross-talk: implications for pediatric obesity: A narrative review of literature. Journal of Bone and Mineral Metabolism.<

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