Abstract
Summary
Indicators of total and abdominal obesity were negatively associated with femoral neck strength indices. There are age-, sex-, and fat distribution-specific differences in the magnitude of these associations. These suggested that indicators of obesity with different magnitude according to age, sex, and fat distribution associated with poor bone health.
Introduction
Fat regulates bone metabolism, but the associations of total and abdominal obesity with bone health are inconsistent. We investigated the association between indicators of obesity and composite indices of femoral neck (FN) strength reflecting the risk of hip fracture.
Methods
This population-based cross-sectional study examined data from the Korea National Health and Nutrition Examination Surveys. Participants were divided into groups according to age (25–49/≥50 years) and sex. We examined total fat mass (TFM) and percentage fat mass (pFM) as indicators of total obesity and truncal fat mass (TrFM) as an indicator of abdominal obesity. We calculated the composite indices of FN strength and anthropometric clinical indicators of abdominal obesity.
Results
TFM, pFM, and TrFM were negatively associated with the composite indices, irrespective of age and sex (P < 0.001–0.005). Most anthropometric clinical indicators of abdominal obesity showed negative associations with the composite indices regardless of age and sex (P < 0.001–0.048), except for women aged 25–49 years. In men, magnitudes of the negative contributions of TFM to the composite indices were significantly stronger at age 25–49 years than at age ≥50 years. Magnitudes of negative associations of TFM with the composite indices were greater in men than in women. TrFM had a more detrimental effect than TFM on FN strength in men aged 25–49 years and in women of both ages.
Conclusion
Indicators of total and abdominal obesity negatively associated with FN strength, and magnitudes of their effects on bone health differed according to age, sex, and fat distribution.
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Abbreviations
- BMD:
-
Bone mineral density
- FN:
-
Femoral neck
- FNW:
-
Femoral neck width
- HAL:
-
Hip axis length
- FM:
-
Fat mass
- TFM:
-
Total fat mass
- pFM:
-
Percentage fat mass
- TrFM:
-
Truncal fat mass
- KNHANES:
-
Korea National Health and Nutrition Examination Surveys
- eGFR:
-
Estimated glomerular filtration rate
- WC:
-
Waist circumference
- BMI:
-
Body mass index
- TG:
-
Triglyceride
- HDL-C:
-
High-density lipoprotein cholesterol
- 25(OH)D:
-
25-Hydroxyvitamin D
- DXA:
-
Dual-energy X-ray absorptiometry
- HSA:
-
Hip structure analysis
- VAI:
-
Visceral adiposity index
- C index:
-
Conicity index
- WHtR:
-
Waist-to-height ratio
- SI:
-
Strength index
- VIF:
-
Variance inflation factor
References
Reginster JY, Burlet N (2006) Osteoporosis: a still increasing prevalence. Bone 38:S4–S9. doi:10.1016/j.bone.2005.11.024
Park C, Ha YC, Jang S, Jang S, Yoon HK, Lee YK (2011) The incidence and residual lifetime risk of osteoporosis-related fractures in Korea. J Bone Miner Metab 29:744–751. doi:10.1007/s00774-011-0279-3
Johnell O, Kanis J (2005) Epidemiology of osteoporotic fractures. Osteoporos Int 16(Suppl 2):S3–S7. doi:10.1007/s00198-004-1702-6
Mayhew PM, Thomas CD, Clement JG, Loveridge N, Beck TJ, Bonfield W, Burgoyne CJ, Reeve J (2005) Relation between age, femoral neck cortical stability, and hip fracture risk. Lancet 366:129–135. doi:10.1016/s0140-6736(05)66870-5
Wainwright SA, Marshall LM, Ensrud KE, Cauley JA, Black DM, Hillier TA, Hochberg MC, Vogt MT, Orwoll ES (2005) Hip fracture in women without osteoporosis. J Clin Endocrinol Metab 90:2787–2793. doi:10.1210/jc.2004-1568
Sanders KM, Nicholson GC, Watts JJ, Pasco JA, Henry MJ, Kotowicz MA, Seeman E (2006) Half the burden of fragility fractures in the community occur in women without osteoporosis. When is fracture prevention cost-effective? Bone 38:694–700. doi:10.1016/j.bone.2005.06.004
Karlamangla AS, Barrett-Connor E, Young J, Greendale GA (2004) Hip fracture risk assessment using composite indices of femoral neck strength: the Rancho Bernardo study. Osteoporos Int 15:62–70. doi:10.1007/s00198-003-1513-1
Ishii S, Greendale GA, Cauley JA, Crandall CJ, Huang MH, Danielson ME, Karlamangla AS (2012) Fracture risk assessment without race/ethnicity information. J Clin Endocrinol Metab 97:3593–3602. doi:10.1210/jc.2012-1997
Yu N, Liu YJ, Pei Y et al (2010) Evaluation of compressive strength index of the femoral neck in Caucasians and Chinese. Calcif Tissue Int 87:324–332. doi:10.1007/s00223-010-9406-8
Ishii S, Cauley JA, Crandall CJ, Srikanthan P, Greendale GA, Huang MH, Danielson ME, Karlamangla AS (2012) Diabetes and femoral neck strength: findings from the Hip Strength Across the Menopausal Transition Study. J Clin Endocrinol Metab 97:190–197. doi:10.1210/jc.2011-1883
Faje A, Klibanski A (2012) Body composition and skeletal health: too heavy? too thin? Curr Osteoporos Rep 10:208–216. doi:10.1007/s11914-012-0106-3
Gonnelli S, Caffarelli C, Nuti R (2014) Obesity and fracture risk. Clin Cases Miner Bone Metab 11:9–14
Ahn SH, Lee SH, Kim H, Kim BJ, Koh JM (2014) Different relationships between body compositions and bone mineral density according to gender and age in Korean populations (KNHANES 2008-2010). J Clin Endocrinol Metab 99:3811–3820. doi:10.1210/jc.2014-1564
Klahr S (1989) The modification of diet in renal disease study. N Engl J Med 320:864–866. doi:10.1056/nejm198903303201310
Kelly TL, Wilson KE, Heymsfield SB (2009) Dual energy X-ray absorptiometry body composition reference values from NHANES. PLoS One 4:e7038. doi:10.1371/journal.pone.0007038
Lee EY, Kim D, Kim KM, Kim KJ, Choi HS, Rhee Y, Lim SK (2012) Age-related bone mineral density patterns in Koreans (KNHANES IV). J Clin Endocrinol Metab 97:3310–3318. doi:10.1210/jc.2012-1488
Myong JP, Kim HR, Choi SE, Koo JW (2013) Dose-related effect of urinary cotinine levels on bone mineral density among Korean females. Osteoporos Int 24:1339–1346. doi:10.1007/s00198-012-2107-6
Beck TJ, Looker AC, Ruff CB, Sievanen H, Wahner HW (2000) Structural trends in the aging femoral neck and proximal shaft: analysis of the Third National Health and Nutrition Examination Survey dual-energy X-ray absorptiometry data. J Bone Miner Res 15:2297–2304. doi:10.1359/jbmr.2000.15.12.2297
Amato MC, Giordano C, Galia M, Criscimanna A, Vitabile S, Midiri M, Galluzzo A (2010) Visceral adiposity index: a reliable indicator of visceral fat function associated with cardiometabolic risk. Diabetes Care 33:920–922. doi:10.2337/dc09-1825
Zhang X, Shu XO, Li H, Yang G, Xiang YB, Cai Q, Ji BT, Gao YT, Zheng W (2013) Visceral adiposity and risk of coronary heart disease in relatively lean Chinese adults. Int J Cardiol 168:2141–2145. doi:10.1016/j.ijcard.2013.01.275
Valdez R (1991) A simple model-based index of abdominal adiposity. J Clin Epidemiol 44:955–956
Weaver B, Wuensch KL (2013) SPSS and SAS programs for comparing Pearson correlations and OLS regression coefficients. Behav Res Methods 45:880–895. doi:10.3758/s13428-012-0289-7
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. doi:10.1210/jcem.75.3.1517366
Hsu YH, Venners SA, Terwedow HA et al (2006) Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women. Am J Clin Nutr 83:146–154
Shao HD, Li GW, Liu Y, Qiu YY, Yao JH, Tang GY (2015) Contributions of fat mass and fat distribution to hip bone strength in healthy postmenopausal Chinese women. J Bone Miner Metab 33:507–515. doi:10.1007/s00774-014-0613-7
Parhami F, Jackson SM, Tintut Y, Le V, Balucan JP, Territo M, Demer LL (1999) Atherogenic diet and minimally oxidized low density lipoprotein inhibit osteogenic and promote adipogenic differentiation of marrow stromal cells. J Bone Miner Res 14:2067–2078. doi:10.1359/jbmr.1999.14.12.2067
Takeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, Parker KL, Armstrong D, Ducy P, Karsenty G (2002) Leptin regulates bone formation via the sympathetic nervous system. Cell 111:305–317
Okorodudu DO, Jumean MF, Montori VM, Romero-Corral A, Somers VK, Erwin PJ, Lopez-Jimenez F (2010) Diagnostic performance of body mass index to identify obesity as defined by body adiposity: a systematic review and meta-analysis. Int J Obes 34:791–799. doi:10.1038/ijo.2010.5
Amato MC, Giordano C (2014) Visceral adiposity index: an indicator of adipose tissue dysfunction. Int J Endocrinol 2014:730827. doi:10.1155/2014/730827
Roriz AK, Passos LC, de Oliveira CC, Eickemberg M, Moreira Pde A, Sampaio LR (2014) Evaluation of the accuracy of anthropometric clinical indicators of visceral fat in adults and elderly. PLoS One 9:e103499. doi:10.1371/journal.pone.0103499
Sogaard AJ, Holvik K, Omsland TK, Tell GS, Dahl C, Schei B, Falch JA, Eisman JA, Meyer HE (2015) Abdominal obesity increases the risk of hip fracture: a population-based study of 43,000 women and men aged 60-79 years followed for 8 years. Cohort of Norway J Intern Med 277:306–317. doi:10.1111/joim.12230
Nguyen ND, Pongchaiyakul C, Center JR, Eisman JA, Nguyen TV (2005) Abdominal fat and hip fracture risk in the elderly: the Dubbo Osteoporosis Epidemiology Study. BMC Musculoskelet Disord 6:11. doi:10.1186/1471-2474-6-11
Folsom AR, Kushi LH, Anderson KE, Mink PJ, Olson JE, Hong CP, Sellers TA, Lazovich D, Prineas RJ (2000) Associations of general and abdominal obesity with multiple health outcomes in older women: the Iowa Women’s Health Study. Arch Intern Med 160:2117–2128
Calle EE, Thun MJ, Petrelli JM, Rodriguez C, Heath CW Jr (1999) Body-mass index and mortality in a prospective cohort of U.S. adults. N Engl J Med 341:1097–1105. doi:10.1056/nejm199910073411501
Zamboni M, Armellini F, Sheiban I, De Marchi M, Todesco T, Bergamo-Andreis IA, Cominacini L, Bosello O (1992) Relation of body fat distribution in men and degree of coronary narrowings in coronary artery disease. Am J Cardiol 70:1135–1138
Bjorntorp P (1988) Abdominal obesity and the development of noninsulin-dependent diabetes mellitus. Diabetes Metab Rev 4:615–622
Acknowledgements
This study was supported by a grant (2014-1215) from the Asan Institute for Life Sciences, Seoul, Republic of Korea, and by a grant from the Korean Health Technology R&D Project, Ministry of Health & Welfare, Republic of Korea (project no.: HI14C2258).
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Kim, H., Lee, S.H., Kim, B.J. et al. Association between obesity and femoral neck strength according to age, sex, and fat distribution. Osteoporos Int 28, 2137–2146 (2017). https://doi.org/10.1007/s00198-017-4015-2
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DOI: https://doi.org/10.1007/s00198-017-4015-2