Effects of weight loss on bone turnover, inflammatory cytokines, and adipokines in Chinese overweight and obese adults

D Yu, W Chen, J Zhang, L Wei, J Qin, M Lei, H Tang, Y Wang, S Xue, J Dong, Y Chen, L Xie, H Di, D Yu, W Chen, J Zhang, L Wei, J Qin, M Lei, H Tang, Y Wang, S Xue, J Dong, Y Chen, L Xie, H Di

Abstract

Purpose: Plenty of studies have examined the long term effect of weight loss on bone mineral density. This study aimed to explore the effects of 10% weight loss on early changes in bone metabolism as well as the possible influencing factors.

Methods: Overweight and obese outpatients (BMI > 24.0 kg/m2) were recruited from the nutrition clinic and followed a calorie-restricted, high-protein, low-carbohydrate diet program. Dietary intake, body composition, serum procollagen type I N-propeptide (PINP), β-Crosslaps, PTH, 25(OH) VitD, a series of inflammatory cytokines and adipokines were measured for the participants before starting to lose weight and after 10% weight loss (NCT04207879).

Results: A total of 75 participants were enrolled and 37 participants achieved a weight loss of at least 10%. It was found that PINP decreased (p = 0.000) and the β-Crosslaps increased (p = 0.035) in female participants. Decreases in PTH (p = 0.001), serum IL-2 (p = 0.013), leptin (p = 0.001) and increases in 25(OH) VitD (p = 0.001), serum ghrelin (p = 0.033) were found in 37 participants after 10% of their weight had been lost. Change in PINP was detected to be significantly associated with change in lean body mass (r = 0.418, p = 0.012) and change in serum ghrelin(r = - 0.374, p = 0.023).

Conclusions: Bone formation was suppressed and bone absorption was increased in female subjects after a 10% weight loss. Bone turnover was found to be associated with lean body mass and affected by the circulating ghrelin level.

Keywords: Adipokines; Bone turnover; Inflammatory cytokines; Obesity; Weight loss.

Conflict of interest statement

All authors declare that they have no conflicts of interest.

© 2022. The Author(s).

Figures

Fig. 1
Fig. 1
Flowchart for the study
Fig. 2
Fig. 2
Velocity of body weight reduction over the course of the weight loss diet program
Fig. 3
Fig. 3
Macronutrient distribution at baseline, the 5% weight-loss visit, and 10% weight-loss visit

References

    1. Peeters A, Barendregt JJ, Willekens F, Mackenbach JP, Al Mamun A, Bonneux L. Obesity in adulthood and its consequences for life expectancy: a life-table analysis. Ann Intern Med. 2003;138:24–32. doi: 10.7326/0003-4819-138-1-200301070-00008.
    1. Williamson DF, Pamuk E, Thun M, Flanders D, Byers T, Heath C. Prospective study of intentional weight loss and mortality in never-smoking overweight US white women aged 40–64 years. Am J Epidemiol. 1995;141:1128–1141. doi: 10.1093/oxfordjournals.aje.a117386.
    1. Srivastava AK, Vliet EL, Lewiecki EM, Maricic M, Abdelmalek A, Gluck O, Baylink DJ. Clinical use of serum and urine bone markers in the management of osteoporosis. Curr Med Res Opin. 2005;21:1015–1026. doi: 10.1185/030079905X49635.
    1. Romero Barco CM, Manrique Arija S, Rodríguez Pérez M. Biochemical markers in osteoporosis: usefulness in clinical practice. Reumatol Clínica. 2012;8:149–152. doi: 10.1016/j.reuma.2011.05.010.
    1. Camacho PM, Petak SM, Binkley N, Clarke BL, Harris ST, Hurley DL, Kleerekoper M, Lewiecki EM, Miller PD, Narula HS, Pessah-Pollack R, Tangpricha V, Wimalawansa SJ, Watts NB. American association of Clinical Endocrinologists and American College of endocrinology clinical practice guidelines for the diagnosis and treatment of postmenopausal osteoporosis—2016—executive summary. Endocr Pract. 2016;22:1111–1118. doi: 10.4158/EP161435.ESGL.
    1. Cosman F, de Beur SJ, LeBoff MS, Lewiecki EM, Tanner B, Randall S, Lindsay R, National Osteoporosis F. Clinician’s guide to prevention and treatment of osteoporosis. Osteoporos Int. 2014;25:2359–2381. doi: 10.1007/s00198-014-2794-2.
    1. Vasikaran S, Eastell R, Bruyere O, Foldes AJ, Garnero P, Griesmacher A, McClung M, Morris HA, Silverman S, Trenti T, Wahl DA, Cooper C, Kanis JA, IOF-IFCC Bone Marker Standards Working Group Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int. 2011;22:391–420. doi: 10.1007/s00198-010-1501-1.
    1. Hwang JS, Chan DC, Chen JF, Cheng TT, Wu CH, Soong YK, Tsai KS, Yang RS. Clinical practice guidelines for the prevention and treatment of osteoporosis in Taiwan: summary. J Bone Miner Metab. 2014;32:10–16. doi: 10.1007/s00774-013-0495-0.
    1. Vasikaran S, Cooper C, Eastell R, Griesmacher A, Morris HA, Trenti T, Kanis JA. International osteoporosis foundation and international federation of clinical chemistry and laboratory medicine position on bone marker standards in osteoporosis. Clin Chem Lab Med. 2011;49:1271–1274. doi: 10.1515/CCLM.2011.602.
    1. Shapses SA, Sukumar D. Bone metabolism in obesity and weight loss. Annu Rev Nutr. 2012;32:287–309. doi: 10.1146/annurev.nutr.012809.104655.
    1. Uusi-Rasi K, Rauhio A, Kannus P, Pasanen M, Kukkonen-Harjula K, Fogelholm M, Sievänen H. Three-month weight reduction does not compromise bone strength in obese premenopausal women. Bone. 2010;46:1286–1293. doi: 10.1016/j.bone.2009.10.013.
    1. Rector RS, Loethen J, Ruebel M, Thomas TR, Hinton PS. Serum markers of bone turnover are increased by modest weight loss with or without weight-bearing exercise in overweight premenopausal women. Appl Physiol Nutr Metab. 2009;34:933–941. doi: 10.1139/H09-098.
    1. Uusi-Rasi K, Sievanen H, Kannus P, Pasanen M, Kukkonen-Harjula K, Fogelholm M. Influence of weight reduction on muscle performance and bone mass, structure and metabolism in obese premenopausal women. Musculoskelet Neuronal Interact. 2009;9:72–80.
    1. Ricci TA, Heymsfield SB, Pierson RN, Jr, Stahl T, Chowdhury HA, Shapses SA. Moderate energy restriction increases bone resorption in obese postmenopausal women. Am J ClinNutr. 2001;73:347–352. doi: 10.1093/ajcn/73.2.347.
    1. Zibellini J, Seimon RV, Lee CM, Gibson AA, Hsu MS, Shapses SA, Nguyen TV, Sainsbury A. Does diet-induced weight loss lead to bone loss in overweight or obese adults? A systematic review and meta-analysis of clinical trials. J Bone Miner Res. 2015;30:2168–2178. doi: 10.1002/jbmr.2564.
    1. Southmayd EA, Williams NI, Mallinson RJ, Souza MJD. Energy deficiency suppresses bone turnover in exercising women with menstrual disturbances. J Clin Endocrinol Metab. 2019;104(8):3131–3145. doi: 10.1210/jc.2019-00089.
    1. Cashman KD. Diet, nutrition, and bone health. J Nutr. 2007;137(11, Suppl):2507–2512. doi: 10.1093/jn/137.11.2507S.
    1. Lee AM, Sawyer RK, Moore AJ, Morris HA, O'Loughlin PD, Anderson PH. Adequate dietary vitamin D and calcium are both required to reduce bone turnover and increased bone mineral volume. J Steroid Biochem Mol Biol. 2014;144A:159–162. doi: 10.1016/j.jsbmb.2013.11.009.
    1. Razny U, Goralska J, Calder PC, Gruca A, Childs CE, Kapusta M, Slowinska-Solnica K, Dembinska-Kiec A, Solnica B, Malczewska-Malec M. The effect of caloric restriction with and without n-3 PUFA supplementation on bone turnover markers in blood of subjects with abdominal obesity: a randomized placebo-controlled trial. Nutrients. 2021;13:3096. doi: 10.3390/nu13093096.
    1. Hinton PS, LeCheminant JD, Smith BK, Rector RS, Donnelly JE. Weight loss-induced alterations in serum markers of bone turnover persist during weight maintenance in obese men and women. J Am Coll Nutr. 2009;28:565–573. doi: 10.1080/07315724.2009.10719788.
    1. Josse AR, Atkinson SA, Tarnopolsky MA, Phillips SM. Diets higher in dairy foods and dietary protein support bone health during diet- and exercise-induced weight loss in overweight and obese premenopausal women. J Clin Endocr Metab. 2012;97:251–260. doi: 10.1210/jc.2011-2165.
    1. Olmos JM, Vázquez LA, Amado JA, Hernández JL, González Macías J. Mineral metabolism in obese patients following vertical banded gastroplasty. Obes Surg. 2008;18:197–203. doi: 10.1007/s11695-007-9307-8.
    1. Das UN. Is obesity an inflammatory condition? Nutrition. 2001;17:953–966. doi: 10.1016/s0899-9007(01)00672-4.
    1. Engström G, Hedblad B, Stavenow L, Lind P, Janzon L, Lindgärde F. Inflammation-sensitive plasma proteins are associated with future weight gain. Diabetes. 2003;52:2097–2101. doi: 10.2337/diabetes.52.8.2097.
    1. Moschen AR, Molnar C, Geiger S, Graziadei I, Ebenbichler CF, Weiss H, Kaser S, Kaser A, Tilg H. Anti-inflammatory effects of excessive weight loss: potent suppression of adipose interleukin 6 and tumour necrosis factor alpha expression. Gut. 2010;59:1259–1264. doi: 10.1136/gut.2010.214577.
    1. Ho TP, Zhao X, Courville AB, Linderman JD, Smith S, Sebring N, Della Valle DM, Fitzpatrick B, Simchowitz L, Celi FS. Effects of a 12-month moderate weight loss intervention on insulin sensitivity and inflammation status in nondiabetic overweight and obese subjects. Horm Metab Res. 2015;47:289–296. doi: 10.1055/s-0034-1382011.
    1. Tajik N, Keshavarz SA, Masoudkabir F, Djalali M, Sadrzadeh-Yeganeh HH, Eshraghian MR, Chamary M, Ahmadivand Z, Yazdani T, Javanbakht MH. Effect of diet-induced weight loss on inflammatory cytokines in obese women. J Endocrinol Investig. 2013;36:211–215. doi: 10.3275/8465.
    1. Christiansen T, Paulsen SK, Bruun JM, Pedersen SB, Richelsen B. Exercise training versus diet-induced weight-loss on metabolic risk factors and inflammatory markers in obese subjects: a 12-week randomized intervention study. Am J Physiol Endocrinol Metab. 2010;298:E824–E831. doi: 10.1152/ajpendo.00574.2009.
    1. Bougoulia M, Triantos A, Koliakos G. Effect of weight loss with or without orlistat treatment on adipocytokines, inflammation, and oxidative markers in obese women. Hormones. 2006;5:259–269. doi: 10.14310/horm.2002.11190.
    1. Keogh JB, Brinkworth GD, Clifton PM. Effects of weight loss on a low-carbohydrate diet on flow-mediated dilatation, adhesion molecules and adiponectin. Brit J Nutr. 2007;98:852–859. doi: 10.1017/S0007114507747815.
    1. Liu G, Qi M, Hutchinson MR, Yang G, Goldys EM. Recent advances in cytokine detection by immunosensing. Biosens bioelectron. 2016;79:810–821. doi: 10.1016/j.bios.2016.01.020.
    1. Juanola-Falgarona M, Salas-Salvadó J, Ibarrola-Jurado N, Rabassa-Soler A, Díaz-López A, Guasch-Ferré M, Hernández-Alonso P, Balanza R, Bulló M. Effect of the glycemic index of the diet on weight loss, modulation of satiety, inflammation, and other metabolic risk factors: a randomized controlled trial. Am J Clin Nutr. 2014;100:27–35. doi: 10.3945/ajcn.113.081216.
    1. O’Dea JP, Wieland RG, Hallberg MC, Llerena LA, Zorn EM, Genuth SM. Effect of dietery weight loss on sex steroid binding sex steroids, and gonadotropins in obese postmenopausal women. J Lab Clin Med. 1979;93:1004–1008.
    1. Eriksen EF, Colvard DS, Berg NJ, Graham ML, Mann KG, Spelsberg TC, Riggs BL. Evidence of estrogen receptors in normal human osteoblast-like cells. Science. 1988;241:84–86. doi: 10.1126/science.3388021.
    1. Heino TJ, Hentunen TA, Väänänen HK. Osteocytes inhibit osteoclastic bone resorption through transforming growth factor-beta: enhancement by estrogen. J Cell Biochem. 2022;85:185–197. doi: 10.1002/jcb.10109.
    1. Erlandson KM, Kitch D, Tierney C, Sax PE, Daar ES, Tebas P, Melbourne K, Ha B, Jahed NC, McComsey GA. Weight and lean body mass change with antiretroviral initiation and impact on bone mineral density. AIDS. 2013;27:2069–2079. doi: 10.1097/QAD.0b013e328361d25d.
    1. Schöffl I, Kemmler W, Kladny B, Vonstengel S, Kalender WA, Engelke K. In healthy elderly postmenopausal women variations in BMD and BMC at various skeletal sites are associated with differences in weight and lean body mass rather than by variations in habitual physical activity, strength or VO2max. J Musculoskelet Neuronal Interact. 2008;8:363–374.
    1. Sato T, Ida T, Nakamura Y, Shiimura Y, Kangawa K, Kojima M. Physiological roles of ghrelin on obesity. Obes Res Clin Pract. 2014;8:e405–e413. doi: 10.1016/j.orcp.2013.10.002.
    1. Cui H, López M, Rahmouni K. The cellular and molecular bases of leptin and ghrelin resistance in obesity. Nat Rev Endocrinol. 2017;13:338–351. doi: 10.1038/nrendo.2016.222.

Source: PubMed

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