Abstract
Summary
The researchers sought to test the possible link between resting metabolic rate and bone mineral density through four adipokines. Participants with lower resting metabolic rate (RMR) per kilogram demonstrated higher total bone mineral density (BMD), total T-score, and total Z-score. Omentin-1 had a mediatory effect on the relationship between RMR/kg of body weight and bone parameters.
Introduction
The previous results of studies regarding the links between obesity and bone health are controversial. For this reason, the researchers sought to test the possible link between RMR and BMD through the following four adipokines: vaspin, retinol binding protein 4, angiopoietin-like 6 (ANGPL6), and omentin-1.
Methods
We enrolled 312 obese Iranian women (30 ≤ body mass index <40) in this cross-sectional study. In order to examine the association of serum adipokine levels with RMR and BMD, the participants were grouped based on RMR per body weight. Body composition, dietary intake, bone mineral density, and resting metabolic rate were assessed in all participants. Serum adipokine levels were quantified by the enzyme-linked immunosorbent assay (ELISA) method.
Results
Low levels of RMR/kg were strongly associated with higher weight, body mass index, fat mass, and visceral fat levels. In fact, participants with an RMR/kg of body weight <20 kcal/24 h/kg were more obese (p < 0.05). Another noteworthy finding was that participants with lower RMR/kg demonstrated higher total BMD, total T-score, and total Z-score. Our results showed that omentin-1 had a mediatory effect on the relationship between RMR per kilogram of body weight and bone parameters (p < 0.05). Nevertheless, other adipokines such as vaspin, retinol-binding protein 4 (RBP4), and ANGPL6 did not affect the relationship between RMR and BMD (p > 0.05).
Conclusions
The inhibitory effect of omentin-1 on TNF-alpha seems to be able to reduce the amount of circulating leptin as adipokine, affecting energy expenditure and improving bone loss induced by estrogen deficiency and controlled effect of RMR on BMD.
Similar content being viewed by others
Abbreviations
- BH:
-
Body height
- BMI:
-
Body mass index
- BIA:
-
Bioelectrical impedance analysis
- BMD:
-
Bone mineral density
- BW:
-
Body weight
- RMR:
-
Resting metabolic rate
- DXA:
-
Dual-energy X-ray absorptiometry
- EDTA:
-
Ethylenediaminetetraacetic acid
- EMRI:
-
Endocrinology and Metabolism Research Institute
- FBS:
-
Fasting blood glucose
- FFM:
-
Fat-free mass
- FM:
-
Fat mass
- LRMs:
-
Linear regression models
- hs-CRP:
-
Hypersensitive C-reactive protein
- IL6:
-
Interleukin-6
- IL4:
-
Interleukin-4
- IL10:
-
Interleukin-10
- PTH:
-
Parathyroid hormone
- TBW:
-
Total body water
- TNF-α:
-
Tumor necrosis factor alpha
- 3DR:
-
Three-day dietary recall
- COX:
-
Cyclooxygenase
- ANGPTL6:
-
Angiopoietin-related growth factor 6
- RBP4:
-
Retinol-binding protein 4
References
Groneberg DA, Franke K, Klingelhofer D, Schwarzer M, Ohlendorf D (2015) Density equalizing mapping of obesity: analysis of a global epidemic. Zeitschrift fur Gastroenterologie 53:553–561
Compston J (2015) Obesity and fractures in postmenopausal women. Curr Opin Rheumatol 27:414–419
Gower BA, Casazza K (2013) Divergent effects of obesity on bone health. Journal of clinical densitometry: the official journal of the International Society for Clinical Densitometry 16:450–454
Migliaccio S, Greco EA, Wannenes F, Donini LM, Lenzi A (2014) Adipose, bone and muscle tissues as new endocrine organs: role of reciprocal regulation for osteoporosis and obesity development. Hormone molecular biology and clinical investigation 17:39–51
Varga I, Miko M, Oravcova L, Backayova T, Koller J, Danisovic L (2015) Ultra-structural morphology of long-term cultivated white adipose tissue-derived stem cells. Cell Tissue Bank 16:639–647
Xu L, Kitade H, Ni Y, Ota T (2015) Roles of chemokines and chemokine receptors in obesity-associated insulin resistance and nonalcoholic fatty liver disease. Biomolecules 5:1563–1579
Mirzaei K, Hossein-Nezhad A, Keshavarz SA, Koohdani F, Saboor-Yaraghi AA, Hosseini S, Eshraghian MR, Djalali M (2013) Crosstalk between circulating peroxisome proliferator-activated receptor gamma, adipokines and metabolic syndrome in obese subjects. Diabetol Metab Syndr 5:1758–5996
Antonopoulos AS, Antoniades C, Tousoulis D (2015) Unravelling the “adipokine paradox”: when the classic proatherogenic adipokine leptin is deemed the beneficial one. Int J Cardiol 197:125–127
Pobeha P, Ukropec J, Skyba P et al (2011) Relationship between osteoporosis and adipose tissue leptin and osteoprotegerin in patients with chronic obstructive pulmonary disease. Bone 48:1008–1014
Dimitriadis GK, Kyrou I, Randeva HS (2016) Polycystic ovary syndrome as a proinflammatory state: the role of adipokines. Curr Pharm Des 22:5535–5546
Liao L, Chen Y, Wang W (2016) The current progress in understanding the molecular functions and mechanisms of visfatin in osteoarthritis. J Bone Miner Metab 34:485–490
Olarescu NC, Bollerslev J (2016) The impact of adipose tissue on insulin resistance in acromegaly. Trends Endocrinol Metab 27:226–237
Karrasch T, Schaeffler A (2016) Adipokines and the role of visceral adipose tissue in inflammatory bowel disease. Ann Gastroenterol 29:424–438
Cervellati C, Bonaccorsi G, Bergamini CM, Fila E, Greco P, Valacchi G, Massari L, Gonelli A, Tisato V (2016) Association between circulatory levels of adipokines and bone mineral density in postmenopausal women. Menopause 23:984–992
Do R, Bailey SD, Desbiens K, Belisle A, Montpetit A, Bouchard C, Pérusse L, Vohl M-C, Engert JC (2008) Genetic variants of FTO influence adiposity, insulin sensitivity, leptin levels, and resting metabolic rate in the Quebec family study. Diabetes 57:1147–1150
Loos RJ, Ruchat S, Rankinen T, Tremblay A, Perusse L, Bouchard C (2007) Adiponectin and adiponectin receptor gene variants in relation to resting metabolic rate, respiratory quotient, and adiposity-related phenotypes in the Quebec family study. Am J Clin Nutr 85:26–34
Moradi S, Mirzaei K, Abdurahman AA, Keshavarz SA, Hossein-Nezhad A (2016) Mediatory effect of circulating vaspin on resting metabolic rate in obese individuals. Eur J Nutr 55:1297–1305
Ansar H, Mirzaei K, Malek A, Najmafshar A, Hossein-nezhad A (2015) Possible resting metabolic rate modification by the circulating RBP4 in obese subjects. Diabetes & metabolic syndrome 9:19–23
Tan CO, Battaglino RA, Doherty AL, Gupta R, Lazzari AA, Garshick E, Zafonte R, Morse LR (2014) Adiponectin is associated with bone strength and fracture history in paralyzed men with spinal cord injury. Osteoporosis international: a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA 25:2599–2607
Peng X-D, Xie H, Zhao Q, Wu X-P, Sun Z-Q, Liao E-Y (2008) Relationships between serum adiponectin, leptin, resistin, visfatin levels and bone mineral density, and bone biochemical markers in Chinese men. Clin Chim Acta 387:31–35
Sucunza N, Barahona MJ, Resmini E, Fernandez-Real J-M, Ricart W, Farrerons J, Rodríguez Espinosa J, Marin A-M, Puig T, Webb SM (2009) A link between bone mineral density and serum adiponectin and visfatin levels in acromegaly. The Journal of Clinical Endocrinology & Metabolism 94:3889–3896
Iacobellis G, Iorio M, Napoli N, Cotesta D, Zinnamosca L, Marinelli C, Petramala L, Minisola S, D’Erasmo E, Letizia C (2011) Relation of adiponectin, visfatin and bone mineral density in patients with metabolic syndrome. J Endocrinol Investig 34:e12–e15
He J, Li JC, Xie H, Xu ZH, Sun YW, Shan Q (2015) Serum chemerin levels in relation to osteoporosis and bone mineral density: a case-control study. Dis Markers 2015:786708
Shi L, Mao C, Wang X et al (2016) Association of chemerin levels and bone mineral density in Chinese obese postmenopausal women. Medicine 95:e4583
Weiss LA, Barrett-Connor E, von Muhlen D, Clark P (2006) Leptin predicts BMD and bone resorption in older women but not older men: the rancho Bernardo study. J Bone Miner Res Off J Am Soc Bone Miner Res 21:758–764
Assadi M, Salimipour H, Akbarzadeh S, Nemati R, Jafari SM, Bargahi A, Samani Z, Seyedabadi M, Sanjdideh Z, Nabipour I (2011) Correlation of circulating omentin-1 with bone mineral density in multiple sclerosis: the crosstalk between bone and adipose tissue. PLoS One 6:e24240
Högström M, Nordström A, Nordström P (2008) Retinol, retinol-binding protein 4, abdominal fat mass, peak bone mineral density, and markers of bone metabolism in men: the Northern Osteoporosis and Obesity (NO2) Study. Eur J Endocrinol 158:765–770
Colaianni G, Brunetti G, Faienza MF, Colucci S, Grano M (2014) Osteoporosis and obesity: role of Wnt pathway in human and murine models. World journal of orthopedics 5:242–246
Ma Y, Olendzki BC, Pagoto SL, Hurley TG, Magner RP, Ockene IS, Schneider KL, Merriam PA, Hebert JR (2009) Number of 24-hour diet recalls needed to estimate energy intake. Ann Epidemiol 19:553–559
Mirzaei K, Hossein-Nezhad A, Chamari M, Shahbazi S (2011) Evidence of a role of ANGPTL6 in resting metabolic rate and its potential application in treatment of obesity. Minerva Endocrinol 36:13–21
Baron RM, Kenny DA (1986) The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol 51:1173–1182
Astrup A, Gøtzsche PC, van de Werken K, Ranneries C, Toubro S, Raben A, Buemann B (1999) Meta-analysis of resting metabolic rate in formerly obese subjects. Am J Clin Nutr 69:1117–1122
Miller WM, Spring TJ, Zalesin KC, Kaeding KR, Nori Janosz KE, McCullough PA, Franklin BA (2012) Lower than predicted resting metabolic rate is associated with severely impaired cardiorespiratory fitness in obese individuals. Obesity (Silver Spring) 20:505–511
Astrup A, Buemann B, Toubro S, Ranneries C, Raben A (1996) Low resting metabolic rate in subjects predisposed to obesity: a role for thyroid status. Am J Clin Nutr 63:879–883
Johannsen DL, Welk GJ, Sharp RL, Flakoll PJ (2008) Differences in daily energy expenditure in lean and obese women: the role of posture allocation. Obesity (Silver Spring) 16:34–39
Fernandez-Sanchez A, Madrigal-Santillan E, Bautista M, Esquivel-Soto J, Morales-Gonzalez A, Esquivel-Chirino C, Durante-Montiel I, Sanchez-Rivera G, Valadez-Vega C, Morales-Gonzalez JA (2011) Inflammation, oxidative stress, and obesity. Int J Mol Sci 12:3117–3132
Yudkin JS, Stehouwer CD, Emeis JJ, Coppack SW (1999) C-reactive protein in healthy subjects: associations with obesity, insulin resistance, and endothelial dysfunction: a potential role for cytokines originating from adipose tissue? Arterioscler Thromb Vasc Biol 19:972–978
Lagathu C, Bastard J-P, Auclair M, Maachi M, Capeau J, Caron M (2003) Chronic interleukin-6 (IL-6) treatment increased IL-6 secretion and induced insulin resistance in adipocyte: prevention by rosiglitazone. Biochem Biophys Res Commun 311:372–379
Yang RZ, Lee MJ, Hu H, Pray J, Wu HB, Hansen BC, Shuldiner AR, Fried SK, McLenithan JC, Gong DW (2006) Identification of omentin as a novel depot-specific adipokine in human adipose tissue: possible role in modulating insulin action. Am J Phys Endocrinol Metab 290:E1253–E1261
Rabe K, Lehrke M, Parhofer KG, Broedl UC (2008) Adipokines and insulin resistance. Mol Med 14:741–751
Glauber HS, Vollmer WM, Nevitt MC, Ensrud KE, Orwoll ES (1995) Body weight versus body fat distribution, adiposity, and frame size as predictors of bone density. J Clin Endocrinol Metab 80:1118–1123
Khosla S, Atkinson EJ, Riggs BL, Melton LJ (1996) Relationship between body composition and bone mass in women. J Bone Miner Res 11:857–863
Ricci TA, Heymsfield SB, Pierson RN Jr, Stahl T, Chowdhury HA, Shapses SA (2001) Moderate energy restriction increases bone resorption in obese postmenopausal women. Am J Clin Nutr 73:347–352
Reid IR (2002) Relationships among body mass, its components, and bone. Bone 31:547–555
Barrett-Connor E, Kritz-Silverstein D (1996) Does hyperinsulinemia preserve bone? Diabetes Care 19:1388–1392
Xie H, Xie P-L, Wu X-P, Chen S-M, Zhou H-D, Yuan L-Q, Sheng Z-F, Tang S-Y, Luo X-H, Liao E-Y (2011) Omentin-1 attenuates arterial calcification and bone loss in osteoprotegerin-deficient mice by inhibition of RANKL expression. Cardiovasc Res 92:296–306
Xie H, Xie P-L, Luo X-H, Wu X-P, Zhou H-D, Tang S-Y, Liao E-Y (2012) Omentin-1 exerts bone-sparing effect in ovariectomized mice. Osteoporos Int 23:1425–1436
Nielson CM, Srikanth P, Orwoll ES (2012) Obesity and fracture in men and women: an epidemiologic perspective. J Bone Miner Res 27:1–10
Clevenger HC, Stevenson JL, Cooper JA (2015) Metabolic responses to dietary fatty acids in obese women. Physiol Behav 139:73–79
Lovejoy JC, Smith SR, Champagne CM, Most MM, Lefevre M, DeLany JP, Denkins YM, Rood JC, Veldhuis J, Bray GA (2002) Effects of diets enriched in saturated (palmitic), monounsaturated (oleic), or trans (elaidic) fatty acids on insulin sensitivity and substrate oxidation in healthy adults. Diabetes Care 25:1283–1288
van Marken Lichtenbelt WD, Mensink RP, Westerterp KR (1997) The effect of fat composition of the diet on energy metabolism. Zeitschrift fur Ernahrungswissenschaft 36:303–305
Jones PJH, Jew S, AbuMweis S (2008) The effect of dietary oleic, linoleic, and linolenic acids on fat oxidation and energy expenditure in healthy men. Metabolism 57:1198–1203
Astrup A, Grunwald GK, Melanson EL, Saris WH, Hill JO (2000) The role of low-fat diets in body weight control: a meta-analysis of ad libitum dietary intervention studies. International journal of obesity and related metabolic disorders: journal of the International Association for the Study of Obesity 24:1545–1552
Yamawaki H, Kuramoto J, Kameshima S, Usui T, Okada M, Hara Y (2011) Omentin, a novel adipocytokine inhibits TNF-induced vascular inflammation in human endothelial cells. Biochem Biophys Res Commun 408:339–343
Zhong X, Li X, Liu F, Tan H, Shang D (2012) Omentin inhibits TNF-α-induced expression of adhesion molecules in endothelial cells via ERK/NF-κB pathway. Biochem Biophys Res Commun 425:401–406
Rizzo MR, Mari D, Barbieri M, Ragno E, Grella R, Provenzano R, Villa I, Esposito K, Giugliano D, Paolisso G (2005) Resting metabolic rate and respiratory quotient in human longevity. J Clin Endocrinol Metab 90:409–413
Luhrmann PM, Edelmann-Schafer B, Neuhauser-Berthold M (2010) Changes in resting metabolic rate in an elderly German population: cross-sectional and longitudinal data. J Nutr Health Aging 14:232–236
Poehlman ET, Goran MI, Gardner AW, Ades PA, Arciero PJ, Katzman-Rooks SM, Montgomery SM, Toth MJ, Sutherland PT (1993) Determinants of decline in resting metabolic rate in aging females. Am J Phys 264:E450–E455
Acknowledgements
The authors thank the directors of the Osteoporosis Research Center (ORC), the Endocrine Diseases and Metabolism Research Institute, Tehran University of Medical Sciences, for allowing them to conduct the comparative cross-sectional study for the purpose of evaluating BMD and RMR association. This study was supported by an ORC grant and research grants from Tehran University of Medical Sciences (Grant IDs 91-02-27-18041 and 94-01-161-28473).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The study was approved by the local ethics committee of Tehran University of Medical Sciences (Ethics Committee number 91-02-27-18041-69439).
Conflict of interest
None.
Rights and permissions
About this article
Cite this article
Moradi, S., Mirzaei, K., Abdurahman, A.A. et al. Adipokines may mediate the relationship between resting metabolic rates and bone mineral densities in obese women. Osteoporos Int 28, 1619–1629 (2017). https://doi.org/10.1007/s00198-017-3914-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-017-3914-6