Abstract
Summary
Link between obesity and bone health is controversial. It seems that maybe the difference in metabolic status leads to this difference. We studied relation between metabolically healthy/unhealthy components with bone mineral density. Results showed metabolically unhealthy obesity (MUHO) phenotypes have better bone status at hip site than metabolically healthy obesity (MHO). Also, component metabolic can effect on BMD in different sites.
Purpose/Introduction
This cross-sectional study aimed to compare total BMD and L-L4 BMD in MHO and MUHO base on Karelis criteria.
Methods
We enrolled 272 Iranian obese women and men (BMI ≥ 30). According to Karelis criteria, the participants were grouped base to MHO and MUHO. The body composition and BMD were assessed for all cases. Serum HDL-C, LDL-C, total cholesterol, triglyceride (TG), fasting blood glucose, homeostatic model assessment-insulin resistance (HOMA-IR), and hypersensitive C-reactive protein (hs-CRP) levels were quantified by ELISA method.
Results
Our results demonstrate MUHO phenotype have high total BMD more than MHO (P = 0.01, CI = 0.12 to 0.21). Also, the results of logistic regression analysis showed MUHO have strongly associated with total BMD (β = −0.42, CI = − 0.31 to − 0.04, P = 0.009), but did not affected L2-L4 BMD (β = − 0.09, CI = − 0.14 to 0.08, P = 0.578); this represents that there was discordance in MUHO subjects. Our evidence implicated that HOMA-IR, high level serum TG, hs-CRP, and low level serum HDL had mediatory effect on relationship between obesity and high BMD at the hip region in MUHO subjects (P < 0.05).
Conclusion
Present evidence indicates that, could be a novel link between difference in MUH phenotype and MH phenotype with bone status. Also, component metabolic can effect on BMD in different sites.
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Abbreviations
- BMI:
-
Body mass index
- BIA:
-
Bioelectrical impedance analysis
- BMD:
-
Bone mineral density
- BW:
-
Body weight
- DXA:
-
Dual-energy X-ray absorptiometry
- FBS:
-
Fasting blood glucose
- FFM:
-
Fat-free mass
- FM:
-
Fat mass
- HOMA-IR:
-
Homeostatic model assessment-insulin resistance
- HDL:
-
High-density lipoprotein cholesterol
- LDL:
-
Low-density lipoprotein cholesterol
- LRM:
-
Linear regression models
- L2-L4 BMD:
-
Lumbar spine (vertebrae L2-L4) bone mineral density
- hs-CRP:
-
Hypersensitive C-reactive protein
- IL-6:
-
Interleukin-6
- IGF-I:
-
Insulin-like growth factor 1
- MH:
-
Metabolically healthy
- MUH:
-
Metabolically unhealthy
- MHO:
-
Metabolically healthy obesity
- MUHO:
-
Metabolically unhealthy obesity
- TBW:
-
Total body water
- Total-Chol:
-
Total cholesterol
- Total BMD:
-
Hip bone mineral density
- TG:
-
Triglyceride
References
Hwang LC, Bai CH, Sun CA, Chen CJ (2012) Prevalence of metabolically healthy obesity and its impacts on incidences of hypertension, diabetes and the metabolic syndrome in Taiwan. Asia Pac J Clin Nutr 21(2):227–233
Phillips CM, Dillon C, Harrington JM, McCarthy VJ, Kearney PM, Fitzgerald AP et al (2013) Defining metabolically healthy obesity: role of dietary and lifestyle factors. PLoS One 8(10):e76188
Swinburn BA, Sacks G, Hall KD, McPherson K, Finegood DT, Moodie ML et al (2011) The global obesity pandemic: shaped by global drivers and local environments. Lancet 378(9793):804–814
Di Ciaula A, Portincasa P (2017) Diet and contaminants: driving the rise to obesity epidemics? Curr Med Chem
van Vliet-Ostaptchouk JV, Nuotio ML, Slagter SN, Doiron D, Fischer K, Foco L et al (2014) The prevalence of metabolic syndrome and metabolically healthy obesity in Europe: a collaborative analysis of ten large cohort studies. BMC Endocr Disord 14:9
Bell JA, Kivimaki M, Hamer M (2014) Metabolically healthy obesity and risk of incident type 2 diabetes: a meta-analysis of prospective cohort studies. Obes Rev 15(6):504–515
Pischon T, Boeing H, Hoffmann K, Bergmann M, Schulze MB, Overvad K et al (2008) General and abdominal adiposity and risk of death in Europe. N Engl J Med 359(20):2105–2120
Hinnouho GM, Czernichow S, Dugravot A, Batty GD, Kivimaki M, Singh-Manoux A (2013) Metabolically healthy obesity and risk of mortality: does the definition of metabolic health matter? Diabetes Care 36(8):2294–2300
Karelis AD, Brochu M, Rabasa-Lhoret R (2004) Can we identify metabolically healthy but obese individuals (MHO)? Diabetes Metabolism 30(6):569–572
Messier V, Karelis AD, Prud'homme D, Primeau V, Brochu M, Rabasa-Lhoret R (2010) Identifying metabolically healthy but obese individuals in sedentary postmenopausal women. Obesity 18(5):911–917
Marini MA, Succurro E, Frontoni S, Hribal ML, Andreozzi F, Lauro R et al (2007) Metabolically healthy but obese women have an intermediate cardiovascular risk profile between healthy nonobese women and obese insulin-resistant women. Diabetes Care 30(8):2145–2147
Shaharyar S, Roberson LL, Jamal O, Younus A, Blaha MJ, Ali SS et al (2015) Obesity and metabolic phenotypes (metabolically healthy and unhealthy variants) are significantly associated with prevalence of elevated C-reactive protein and hepatic steatosis in a large healthy Brazilian population. J Obes 2015:178526
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 Mineral Res 8(5):567–573
Salamat MR, Salamat AH, Janghorbani M (2016) Association between obesity and bone mineral density by gender and menopausal status. Endocrinol Metab (Seoul) 31(4):547–558
Cummings SR, Nevitt MC, Browner WS, Stone K, Fox KM, Ensrud KE et al (1995) Risk factors for hip fracture in white women. Study of Osteoporotic Fractures Research Group. N Engl J Med 332(12):767–773
Ravn P, Cizza G, Bjarnason NH, Thompson D, Daley M, Wasnich RD et al (1999) Low body mass index is an important risk factor for low bone mass and increased bone loss in early postmenopausal women. Early Postmenopausal Intervention Cohort (EPIC) study group. J Bone Mineral Res 14(9):1622–1627
Janicka A, Wren TA, Sanchez MM, Dorey F, Kim PS, Mittelman SD et al (2007) Fat mass is not beneficial to bone in adolescents and young adults. J Clin Endocrinol Metab 92(1):143–147
Zhao LJ, Liu YJ, Liu PY, Hamilton J, Recker RR, Deng HW (2007) Relationship of obesity with osteoporosis. J Clin Endocrinol Metab 92(5):1640–1646
Mirzaei K, Hossein-Nezhad A, Keshavarz SA, Eshaghi SM, Koohdani F, Saboor-Yaraghi AA et al (2014) Insulin resistance via modification of PGC1alpha function identifying a possible preventive role of vitamin D analogues in chronic inflammatory state of obesity. A double blind clinical trial study. Minerva Med 105(1):63–78
Hinnouho G-M, Czernichow S, Dugravot A, Batty GD, Kivimaki M, Singh-Manoux A (2013) Metabolically healthy obesity and risk of mortality. Diabetes Care 36(8):2294–2300
Hossein-Nezhad A, Nikoo MK, Mirzaei K, Mokhtarei F, Meybodi HA (2010) Comparison of the bone turn-over markers in patients with multiple sclerosis and healthy control subjects. Eur J Inflammation 8(2):67–73
Cui LH, Shin MH, Chung EK, Lee YH, Kweon SS, Park KS et al (2005) Association between bone mineral densities and serum lipid profiles of pre- and post-menopausal rural women in South Korea. Osteoporos Int 16(12):1975–1981
Salamat MR, Salamat AH, Abedi I, Janghorbani M (2013) Relationship between weight, body mass index and bone mineral density in men referred for dual-energy X-Ray absorptiometry scan in Isfahan. Iran J Osteoporosis 2013:205963
Black DM, Steinbuch M, Palermo L, Dargent-Molina P, Lindsay R, Hoseyni MS et al (2001) An assessment tool for predicting fracture risk in postmenopausal women. Osteoporos Int 12(7):519–528
Taes YE, Lapauw B, Vanbillemont G, Bogaert V, De Bacquer D, Zmierczak H et al (2009) Fat mass is negatively associated with cortical bone size in young healthy male siblings. J Clin Endocrinol Metab 94(7):2325–2331
Cao JJ (2011) Effects of obesity on bone metabolism. J Orthop Surg Res 6:30
Thrailkill KM, Lumpkin CK Jr, Bunn RC, Kemp SF, Fowlkes JL (2005) Is insulin an anabolic agent in bone? Dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab 289(5):E735–E745
Shin D, Kim S, Kim KH, Lee K, Park SM (2014) Association between insulin resistance and bone mass in men. J Clin Endocrinol Metab 99(3):988–995
Dennison EM, Syddall HE, Aihie Sayer A, Craighead S, Phillips DI, Cooper C (2004) Type 2 diabetes mellitus is associated with increased axial bone density in men and women from the Hertfordshire Cohort Study: evidence for an indirect effect of insulin resistance? Diabetologia 47(11):1963–1968
Birkeland KI, Hanssen KF, Torjesen PA, Vaaler S (1993) Level of sex hormone-binding globulin is positively correlated with insulin sensitivity in men with type 2 diabetes. J Clin Endocrinol Metab 76(2):275–278
Tritos NA, Klibanski A (2016) Effects of growth hormone on bone. Prog Mol Biol Transl Sci 138:193–211
Canalis E, Lian JB (1988) Effects of bone associated growth factors on DNA, collagen and osteocalcin synthesis in cultured fetal rat calvariae. Bone 9(4):243–246
Thiebaud D, Ng KW, Findlay DM, Harker M, Martin TJ (1990) Insulinlike growth factor 1 regulates mRNA levels of osteonectin and pro-alpha 1(I)-collagen in clonal preosteoblastic calvarial cells. J Bone Mineral Res 5(7):761–767
Edwards CJ, Hart DJ, Spector TD (2000) Oral statins and increased bone-mineral density in postmenopausal women. Lancet 355(9222):2218–2219
Orozco P (2004) Atherogenic lipid profile and elevated lipoprotein (a) are associated with lower bone mineral density in early postmenopausal overweight women. Eur J Epidemiol 19(12):1105–1112
Parhami F, Morrow AD, Balucan J, Leitinger N, Watson AD, Tintut Y et al (1997) Lipid oxidation products have opposite effects on calcifying vascular cell and bone cell differentiation. A possible explanation for the paradox of arterial calcification in osteoporotic patients. Arterioscler Thromb Vasc Biol 17(4):680–687
Parhami F, Garfinkel A, Demer LL (2000) Role of lipids in osteoporosis. Arterioscler Thromb Vasc Biol 20(11):2346–2348
Orozco P (2004) Atherogenic lipid profile and elevated lipoprotein (a) are associated with lower bone mineral density in early postmenopausal overweight women. Eur J Epidemiol 19(12):1105–1112
Ackert-Bicknell CL (2012) HDL cholesterol and bone mineral density: is there a genetic link? Bone 50(2):525–533
Nombela-Arrieta C, Ritz J, Silberstein LE (2011) The elusive nature and function of mesenchymal stem cells. Nat Rev Mol Cell Biol 12(2):126–131
Chin KY, Ima-Nirwana S, Mohamed IN, Ahmad F, Ramli ES, Aminuddin A et al (2014) Serum osteocalcin is significantly related to indices of obesity and lipid profile in Malaysian men. Int J Med Sci 11(2):151–157
Dennison EM, Syddall HE, Aihie Sayer A, Martin HJ, Cooper C (2007) Lipid profile, obesity and bone mineral density: the Hertfordshire Cohort Study. QJM 100(5):297–303
Adami S, Braga V, Zamboni M, Gatti D, Rossini M, Bakri J et al (2004) Relationship between lipids and bone mass in 2 cohorts of healthy women and men. Calcif Tissue Int 74(2):136–142
Woodson G (2000) Dual X-ray absorptiometry T-score concordance and discordance between the hip and spine measurement sites. J Clin Densitom 3(4):319–324
Kohrt WM, Snead DB, Slatopolsky E, Birge SJ Jr (1995) Additive effects of weight-bearing exercise and estrogen on bone mineral density in older women. J Bone Mineral Res 10(9):1303–1311
Park KH, Lim JS, Kim KM, Rhee Y, Lim SK (2016) Z-score discordance and contributing factors in healthy premenopausal women with low bone mineral density: the Korean National Health and Nutrition Examination Survey 2008–9. J Bone Miner Metab 34(6):668–677
Duncan EL, Danoy P, Kemp JP, Leo PJ, McCloskey E, Nicholson GC et al (2011) Genome-wide association study using extreme truncate selection identifies novel genes affecting bone mineral density and fracture risk. PLoS Genet 7(4):e1001372
Erdogan MO, Yildiz H, Artan S, Solak M, Tascioglu F, Dundar U et al (2011) Association of estrogen receptor alpha and collagen type I alpha 1 gene polymorphisms with bone mineral density in postmenopausal women. Osteoporos Int 22(4):1219–1225
Napoli N, Varadharajan A, Rini GB, Del Fiacco R, Yarramaneni J, Mumm S et al (2009) Effects of polymorphisms of the sex hormone-binding globulin (SHBG) gene on free estradiol and bone mineral density. Bone 45(6):1169–1174
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 Mineral Res 21(5):758–764
Funding
This study was supported by Osteoporosis Research Center, Endocrine Diseases and Metabolism Research Institute, Tehran University of Medical Sciences and grants of Tehran University of Medical Sciences (Grants ID: 91-02-27-18041 and 94-02-161-29547).
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All participants provided written and informed consent forms (approved by TUMS Ethics Committee, with the following identification (91-02-27-18041-69439). The study protocol was approved by the local ethical committee of Endocrinology and Metabolism Research Institute of Tehran University of Medical Sciences.
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Mirzababaei, A., Mirzaei, K., Khorrami-nezhad, L. et al. Metabolically healthy/unhealthy components may modify bone mineral density in obese people. Arch Osteoporos 12, 95 (2017). https://doi.org/10.1007/s11657-017-0381-9
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DOI: https://doi.org/10.1007/s11657-017-0381-9