Association of body mass index and waist circumference with osteocalcin and C-terminal telopeptide in Iranian elderly: results from a cross-sectional study

Springer Science and Business Media LLC - Tập 37 - Trang 179-184 - 2018
Hamed Kord-Varkaneh1, Hadith Tangestani1, Sara Mansouri1, Abbas Rahimi-Foroushani2, Sakineh Shab-Bidar1
1Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran University of Medical Sciences (TUMS), Tehran, Iran
2Department of Occupational Health Engineering, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

Tóm tắt

There is no agreement on the role of obesity as a protection or unfavorable factor on bone. In the present study, the association of body mass index (BMI) and waist circumference (WC) with osteocalcin, C-terminal telopeptide of type 1 collagen (CTX-I), highly sensitive C-reactive protein (hs-CRP), parathormon (PTH) and 25-hydroxyvitamin D (25(OH)D) in elderly people was investigated. This cross-sectional study was conducted on 178 elderly residents in Tehran, with a mean age of 67.04 (60–83). Serum osteocalcin, hs-CRP, 25(OH) D, PTH and urine CTX-I were measured for all participants. Waist circumference, weight and height were measured and BMI was calculated. Linear regression and Pearson correlation were performed to evaluate the relation of BMI and waist circumference with other variables. A significant inverse association was found between BMI with osteocalcin (β = − 0.171, p = 0.027) after control for covariates. In addition, there were a significant relation of BMI and WC with hs-CRP (β = 0.246, p = 0.002 and β = 0.219, p = 0.006, respectively) and PTH (β = 0.1169, p = 0.040 and β = 0.200, p = 0.018), respectively. The present study did not show a significant relation of BMI and WC with urine CTX-I even after adjustment for potential confounders (β = − 0.143, p = 0.065 and β = − 0.104, p = 0.183, respectively). The present study has concluded that obesity is an undesirable factor for bone metabolism by reducing serum osteocalcin and by increasing hs-CRP and PTH which contribute to bone resorption.

Tài liệu tham khảo

Torres MJ, Feart C, Samieri C, Dorigny B, Luiking Y, Berr C, Barberger-Gateau P, Letenneur L (2015) Poor nutritional status is associated with a higher risk of falling and fracture in elderly people living at home in France: the Three-City cohort study. Osteoporos Int 26:2157–2164 Luo J, Yang Z, Ma Y, Yue Z, Lin H, Qu G, Huang J, Dai W, Li C, Zheng C (2016) LGR4 is a receptor for RANKL and negatively regulates osteoclast differentiation and bone resorption. Nat Med 22:539–546 Wang J, Liu R, Wang F, Hong J, Li X, Chen M, Ke Y, Zhang X, Ma Q, Wang R (2013) Ablation of LGR4 promotes energy expenditure by driving white-to-brown fat switch. Nat Cell Biol 15:1455 Felson DT, Zhang Y, Hannan MT, Anderson JJ (1993) Effects of weight and body mass index on bone mineral density in men and women: the Framingham study. J Bone Miner Res 8:567–573 Compston J (2015) Obesity and fractures in postmenopausal women. Curr Opin Rheumatol 27:414–419 Laslett LL, Just Nee Foley SJ, Quinn SJ, Winzenberg TM, Jones G (2012) Excess body fat is associated with higher risk of vertebral deformities in older women but not in men: a cross-sectional study. Osteoporos Int 23:67–74 Armstrong ME, Cairns BJ, Banks E, Green J, Reeves GK, Beral V (2012) Different effects of age, adiposity and physical activity on the risk of ankle, wrist and hip fractures in postmenopausal women. Bone 50:1394–1400 Compston JE, Watts NB, Chapurlat R, Cooper C, Boonen S, Greenspan S, Pfeilschifter J, Silverman S, Diez-Perez A, Lindsay R, Saag KG, Netelenbos JC, Gehlbach S, Hooven FH, Flahive J, Adachi JD, Rossini M, Lacroix AZ, Roux C, Sambrook PN, Siris ES (2011) Obesity is not protective against fracture in postmenopausal women: GLOW. Am J Med 124:1043–1050 Reid IR, Plank LD, Evans MC (1992) Fat mass is an important determinant of whole body bone density in premenopausal women but not in men. J Clin Endocrinol Metab 75:779–782 Bhupathiraju SN, Dawson-Hughes B, Hannan MT, Lichtenstein AH, Tucker KL (2011) Centrally located body fat is associated with lower bone mineral density in older Puerto Rican adults. Am J Clin Nutr 94:1063–1070 Zhao LJ, Liu YJ, Liu PY, Hamilton J, Recker RR, Deng HW (2007) Relationship of obesity with osteoporosis. J Clin Endocrinol Metab 92:1640–1646 Filip R, Raszewski G (2009) Bone mineral density and bone turnover in relation to serum leptin, alpha-ketoglutarate and sex steroids in overweight and obese postmenopausal women. Clin Endocrinol (Oxf) 70:214–220 Douchi T, Yamamoto S, Oki T, Maruta K, Kuwahata R, Yamasaki H, Nagata Y (2000) Difference in the effect of adiposity on bone density between pre- and postmenopausal women. Maturitas 34:261–266 Reid IR (2002) Relationships among body mass, its components, and bone. Bone 31:547–555 Sen B, Xie Z, Case N, Ma M, Rubin C, Rubin J (2008) Mechanical strain inhibits adipogenesis in mesenchymal stem cells by stimulating a durable beta-catenin signal. Endocrinology 149:6065–6075 David V, Martin A, Lafage-Proust MH, Malaval L, Peyroche S, Jones DB, Vico L, Guignandon A (2007) Mechanical loading down-regulates peroxisome proliferator-activated receptor gamma in bone marrow stromal cells and favors osteoblastogenesis at the expense of adipogenesis. Endocrinology 148:2553–2562 Gregoire FM, Smas CM, Sul HS (1998) Understanding adipocyte differentiation. Physiol Rev 78:783–809 Rosen CJ, Bouxsein ML (2006) Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol 2:35–43 Meunier P, Aaron J, Edouard C, Vignon G (1971) Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res 80:147–154 Kang AR, Oh YR, Kim HY, Park MJ, Joo BS, Choi WJ, Lee JY, Jung MH, Ji YI, Choi JS (2012) Up-regulation of inhibitors of DNA binding/differentiation gene during alendronate-induced osteoblast differentiation. Arch Gynecol Obstet 285:1331–1338 Hauschka PV, Lian JB, Cole D, Gundberg CM (1989) Osteocalcin and matrix Gla protein: vitamin K-dependent proteins in bone. Physiol Rev 69:990–1047 Kunutsor SK, Apekey TA, Laukkanen JA (2015) Association of serum total osteocalcin with type 2 diabetes and intermediate metabolic phenotypes: systematic review and meta-analysis of observational evidence. Eur J Epidemiol 30:599–614 Liu C, Wo J, Zhao Q, Wang Y, Wang B, Zhao W (2015) Association between serum total osteocalcin level and type 2 diabetes mellitus: a systematic review and meta-analysis. Horm Metab Res 47:813–819 Liu DM, Guo XZ, Tong HJ, Tao B, Sun LH, Zhao HY, Ning G, Liu JM (2015) Association between osteocalcin and glucose metabolism: a meta-analysis. Osteoporos Int 26:2823–2833 Kindblom JM, Ohlsson C, Ljunggren Ö, Karlsson MK, Tivesten Å, Smith U, Mellström D (2010) Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. J Bone Miner Res 25:2803 Zoch ML, Clemens TL, Riddle RC (2016) New insights into the biology of osteocalcin. Bone 82:42–49 Chubb SP (2012) Measurement of C-terminal telopeptide of type I collagen (CTX) in serum. Clin Biochem 45:928–935 Movahed A, Larijani B, Nabipour I, Kalantarhormozi M, Asadipooya K, Vahdat K, Akbarzadeh S, Farrokhnia M, Assadi M, Amirinejad R (2012) Reduced serum osteocalcin concentrations are associated with type 2 diabetes mellitus and the metabolic syndrome components in postmenopausal women: the crosstalk between bone and energy metabolism. J Bone Miner Metab 30:683–691 McCloskey E, Hannon R, Lakner G, Clack G, Miyamoto A, Eastell R (2007) Interaction between body mass index and bone turnover during aromatase inhibition: evidence from the letrozole (L), exemestane (E), and anastrozole (A) pharmacodynamics (LEAP) trial. J Clin Oncol 25:560 dos Santos Magalhães KB, Magalhães MM, Diniz ET, Lucena CS, Griz L, Bandeira F (2013) Metabolic syndrome and central fat distribution are related to lower serum osteocalcin concentrations. Ann Nutr Metab 62:183–188 Liu T-T, Liu D-M, Xuan Y, Zhao L, Sun L-H, Zhao D-D, Wang X-F, He Y, Guo X-Z, Du R (2017) The association between the baseline bone resorption marker CTX and incident dysglycemia after 4 years. Bone Res 5:17020 Holecki M, Zahorska-Markiewicz B, Chudek J, Wiecek A (2010) Changes in bone mineral density and bone turnover markers in obese women after short-term weight loss therapy during a 5-year follow-up. Pol Arch Med Wewn 120:248–254 Weiler HA, Lowe J, Krahn J, Leslie WD (2013) Osteocalcin and vitamin D status are inversely associated with homeostatic model assessment of insulin resistance in Canadian Aboriginal and white women: the First Nations Bone Health Study. J Nutr Biochem 24:412–418 Kindblom JM, Ohlsson C, Ljunggren Ö, Karlsson MK, Tivesten Å, Smith U, Mellström D (2009) Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. J Bone Miner Res 24:785–791 Chen L-L, Li Q, Yang Z, Ye Z, Huang Y, He M, Wen J, Wang X-C, Lu B, Hu J (2013) Osteocalcin, glucose metabolism, lipid profile and chronic low-grade inflammation in middle-aged and elderly Chinese. Diabet Med 30:309–317 El-Eshmawy M, Abdel Aal I (2015) Relationships between preptin and osteocalcin in obese, overweight, and normal weight adults. Appl Physiol Nutr Metab 40:218–222 Bao Y, Ma X, Yang R, Wang F, Hao Y, Dou J, He H, Jia W (2013) Inverse relationship between serum osteocalcin levels and visceral fat area in Chinese men. J Clin Endocrinol Metab 98:345–351 Foresta C, Strapazzon G, De Toni L, Gianesello L, Calcagno A, Pilon C, Plebani M, Vettor R (2010) Evidence for osteocalcin production by adipose tissue and its role in human metabolism. J Clin Endocrinol Metab 95:3502–3506 Saleem U, Mosley TH, Kullo IJ (2010) Serum osteocalcin is associated with measures of insulin resistance, adipokine levels, and the presence of metabolic syndrome. Arterioscler Thromb Vasc Biol 30:1474–1478 Yeap BB, Chubb SP, Flicker L, McCaul KA, Ebeling PR, Beilby JP, Norman PE (2010) Reduced serum total osteocalcin is associated with metabolic syndrome in older men via waist circumference, hyperglycemia, and triglyceride levels. Eur J Endocrinol 163:265–272 Kord-Varkaneh H, Djafarian K, Khorshidi M, Shab-Bidar S (2017) Association between serum osteocalcin and body mass index: a systematic review and meta-analysis. Endocrine 58:24–32 Hurlimann J, Thorbecke G, Hochwald G (1966) The liver as the site of C-reactive protein formation. J Exp Med 123:365–378 Yudkin JS, Kumari M, Humphries SE, Mohamed-Ali V (2000) Inflammation, obesity, stress and coronary heart disease: is interleukin-6 the link? Atherosclerosis 148:209–214 Calabró P, Willerson JT, Yeh ET (2003) Inflammatory cytokines stimulated C-reactive protein production by human coronary artery smooth muscle cells. Circulation 108:1930–1932 Park HS, Park JY, Yu R (2005) Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-α and IL-6. Diabetes Res Clin Pract 69:29–35 Visser M, Bouter LM, McQuillan GM, Wener MH, Harris TB (1999) Elevated C-reactive protein levels in overweight and obese adults. JAMA 282:2131–2135 Choi J, Joseph L, Pilote L (2013) Obesity and C-reactive protein in various populations: a systematic review and meta-analysis. Obes Rev 14:232–244 Brooks GC, Blaha MJ, Blumenthal RS (2010) Relation of C-reactive protein to abdominal adiposity. Am J Cardiol 106:56–61 Mathieu P, Lemieux I, Després JP (2010) Obesity, inflammation, and cardiovascular risk. Clin Pharmacol Ther 87:407–416 Rittayamai N, Chuaychoo B, Sriwijitkamol A (2012) Prevalence of osteoporosis and osteopenia in Thai COPD patients. J Med Assoc Thail 95:1021 Eriksson AL, Movérare-Skrtic S, Ljunggren Ö, Karlsson M, Mellström D, Ohlsson C (2014) Highsensitivity CRP is an independent risk factor for all fractures and vertebral fractures in elderly men: the MrOS Sweden study. J Bone Miner Res 29:418–423 Habener JF, Rosenblatt M, Potts JT Jr (1984) Parathyroid hormone: biochemical aspects of biosynthesis, secretion, action, and metabolism. Physiol Rev 64:985–1053 Bolland MJ, Grey AB, Gamble GD, Reid IR (2005) Association between primary hyperparathyroidism and increased body weight: a meta-analysis. J Clin Endocrinol Metab 90:1525–1530 Russell J, Lettieri D, Sherwood LM (1986) Suppression by 1, 25 (OH) 2D3 of transcription of the pre-proparathyroid hormone gene. Endocrinology 119:2864–2866 Tanaka R, Tsushima T, Murakami H, Shizume K, Obara T (1994) Insulin-like growth factor I receptors and insulin-like growth factor-binding proteins in human parathyroid tumors. World J Surg 18:635–641 Sadler GP, Jones DL, Woodhead JS, Horgan K, Wheeler MH (1996) Effect of growth factors on growth of bovine parathyroid cells in serum-free medium. World J Surg 20:822–829 Greenberg C, Kukreja S, Bowser E, Hargis G, Henderson W, Williams G (1987) Parathyroid hormone secretion: effect of estradiol and progesterone. Metabolism 36:151–154 Adam MA, Untch BR, Danko ME, Stinnett S, Dixit D, Koh J, Marks JR, Olson JA Jr (2010) Severe obesity is associated with symptomatic presentation, higher parathyroid hormone levels, and increased gland weight in primary hyperparathyroidism. J Clin Endocrinol Metab 95:4917–4924 Caffarelli C, Alessi C, Nuti R, Gonnelli S (2014) Divergent effects of obesity on fragility fractures. Clin Interv Aging 9:1629 Tran H, Grange JS, Adams-Huet B, Nwariaku FE, Rabaglia JL, Woodruff SL, Holt SA, Maalouf NM (2014) The impact of obesity on the presentation of primary hyperparathyroidism. J Clin Endocrinol Metab 99:2359–2364