Low fatness, reduced fat intake and adequate plasmatic concentrations of LDL-cholesterol are associated with high bone mineral density in women: a cross-sectional study with control group

Lipids in Health and Disease

Marcelo M Pinheiro³  Vera L Szejnfeld⁴  Lígia A Martini¹  Karin S Sarkis² 

[1] Nutrition Department, School of Public Health, Sao Paulo University, Av. Dr. Arnaldo, 715, São Paulo - SP, Brazil CEP-01246-904;Nutrition Department, School of Public Health, Sao Paulo University, Av. Dr. Arnaldo, 715, São Paulo-SP, Brazil CEP-01246-904;Rheumatology Division, Universidade Federal de São Paulo/Escola Paulista de Medicina (Unifesp/EPM), Rua Pedro de Toledo, 650-2° Andar-Vila Clementino, CEP 04039-002 São Paulo-SP, Brazil, Disciplina de Reumatologia;Rheumatology Division, Universidade Federal de São Paulo/Escola Paulista de Medicina (Unifesp/EPM), Av Dr Altino Arantes, 669, apto 105, Vila Clementino, São Paulo-SP, Brazil CEP 04042-033

关键词: Women;    Mineral metabolism;    Diet;    Lipid metabolism;    Body composition;    Bone mineral density;   

Others  :  1160337
DOI  :  10.1186/1476-511X-11-37

 received in 2011-12-27, accepted in 2012-03-12,  发布年份 2012

【 摘 要 】

Background

Several parameters are associated with high bone mineral density (BMD), such as overweight, black background, intense physical activity (PA), greater calcium intake and some medications. The objectives are to evaluate the prevalence and the main aspects associated with high BMD in healthy women.

Methods

After reviewing the database of approximately 21,500 BMD scans performed in the metropolitan area of São Paulo, Brazil, from June 2005 to October 2010, high BMD (over 1400 g/cm² at lumbar spine and/or above 1200 g/cm² at femoral neck) was found in 421 exams. Exclusion criteria were age below 30 or above 60 years, black ethnicity, pregnant or obese women, disease and/or medications known to interfere with bone metabolism. A total of 40 women with high BMD were included and matched with 40 healthy women with normal BMD, paired to weight, age, skin color and menopausal status. Medical history, food intake and PA were assessed through validated questionnaires. Body composition was evaluated through a GE-Lunar DPX MD + bone densitometer. Radiography of the thoracic and lumbar spine was carried out to exclude degenerative alterations or fractures. Biochemical parameters included both lipid and hormonal profiles, along with mineral and bone metabolism. Statistical analysis included parametric and nonparametric tests and linear regression models. P < 0.05 was considered significant.

Results

The mean age was 50.9 (8.3) years. There was no significant difference between groups in relation to PA, smoking, intake of calcium and vitamin D, as well as laboratory tests, except serum C-telopeptide of type I collagen (s-CTX), which was lower in the high BMD group (p = 0.04). In the final model of multivariate regression, a lower fat intake and body fatness as well a better profile of LDL-cholesterol predicted almost 35% of high BMD in women. (adjusted R2 = 0.347; p < 0.001). In addition, greater amounts of lean mass and higher IGF-1 serum concentrations played a protective role, regardless age and weight.

Conclusion

Our results demonstrate the potential deleterious effect of lipid metabolism-related components, including fat intake and body fatness and worse lipid profile, on bone mass and metabolism in healthy women.

【 授权许可】

   
2012 Sarkis et al; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Pesonem J, Sirola J, Tuppurainen M, Jurvelin J, Alhava E, Honkaken R, Kröguer H: High bone mineral density among perimenopausal women. Osteoporosis Int 2005, 16:1899-1906.
• [2]World Health Organization (WHO): Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. World Health Organ Tech Rep Ser 1994, 84:31-129.
• [3]Orwoll ES, Bevan L, Phipps KR: Determinants of bone mineral density in older men. Osteoporos Int 2000, 11:815-821.
• [4]Bell NH: Bone and mineral metabolism in African Americans. Trends Endocrinol Metab 1997, 8:240-245.
• [5]Van Wesenbeeck L, Cleiren E, Gram J, Beals RK, Bénichou O, Scopelliti D, Key L, Renton T, Bartels C, Gong Y, Warman ML, De Vernejoul MC, Bollerslev J, Van Hul W: Six novel missense mutations in the LDL receptor-related protein 5 (LRP5) gene in different conditions with an increased bone density. Am J Hum Genet 2003, 72:763-771.
• [6]Lord SR, Ward JA, Williams P, Zivanovic E: The effects of a community exercise program on fracture risk factors in older women. Osteoporos Int 1996, 6:61-367.
• [7]Heaney RP, Recker RR, Stegman MR, Moy AJ: Calcium absorption in women: relationships to calcium intake, estrogen status, and age. J Bone Miner Res 1989, 4:469-475.
• [8]Qin X, Wang S, Yu M, Zhang L, Li X, Zuo Z, Zhang X, Wang L: Child Skeletal Fluorosis from Indoor Burning of Coal in Southwestern China. J Environ Public Health 2009, 200(9):969764.
• [9]Pasco JA, Kotowicz MA, Henry MJ, Sanders KM, Nicholson GC, Geelong Osteoporosis Study: Statin use, bone mineral density, and fracture risk: Geelong Osteoporosis Study. Arch Intern Med 2002, 162:537-540.
• [10]Kamel HK: Low-dose thiazide and bone density. Ann Intern Med 2002, 136:252-253.
• [11]Cauley JA, Lucas FL, Kuller LH, Vogt MT, Browner WS, Cummings SR: Bone mineral density and risk of breast cancer in older women: the study of osteoporotic fractures. Study of Osteoporotic Fractures Research Group. JAMA 1996, 276:1404-1408.
• [12]Whyte MP, Mills BG, Reinue WR, Podgomik MN, Roodman GD, Gannon FH, Eddy MC, McAlister WH: Espnasile skeletal hyperphosphatasia: a new familial metabolic bone disease. J Bone Miner Res 2000, 15:2330-344.
• [13]Trutschnigg B, Chong C, Habermayerova L, Karelis AD, Komorowski J: Female boxers have high bone mineral density despide low fat mass, high energy expenditure, and high inidence of oligomenorrhea. Appl Physiol Nutr Metab 2008, 33:863-869.
• [14]Food and Nutrition Board, Institute of Medicine: Dietary Reference Intakes for Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids (Macronutrients). Washington DC: National Academy Press; 2005.
• [15]Food and Nutrition Board, Institute of Medicine: Dietary Reference Intakes for calcium, phosphorus, magnesium, vitamin D and fluoride. Washington DC: National Academy Press; 1997.
• [16]Food and Nutrition Board, Institute of Medicine: Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium, and Carotenoids. Washington DC: National Academy Press; 2000.
• [17]International Society for Clinical Densitometry Official Positions [http://http\www.iscd.org\Updated 2007] webcite Accessed March 2011
• [18]Simonelli C, Adler RA, Blake GM, Caudill JP, Khan A, Leib E, Maricic M, Prior JC, Eis SR, Rosen C, Kendler DL: Dual-energy x-ray absorptiometry technical issues: the 2007 ISCD Official Positions. J Clin Densitom 2008, 11:109-122.
• [19]Morgan SL, Peace F, Lopez-Ben R, Fineberg N: Distribution of Z-scores in a University cohort with an emphasis on "high" bone mineral density. J Clin Densitom 2010, 13:385-391.
• [20]Hill PA, Reynolds JJ, Meikle MC: Osteoblasts mediate insulin-like growth factor-I and -II stimulation of osteoclast formation and function. Endocrinology 1995, 136:124-131.
• [21]Barrett-Connor E, Goodman-Gruen D: Gender differences in insulinlike growth factor and bone mineral density association in old age: the Rancho Bernardo Study. J Bone Miner Res 1998, 13:1343-1349.
• [22]Boonen S, Lesaffre E, Dequeker J, Aerssens J, Nijs J, Pelemans W, Bouillon R: Relationship between baseline insulin-like growth factor-I (IGF-I) and femoral bone density in women aged over 70 years: potential implications for the prevention of age-related bone loss. J Am Geriatr Soc 1996, 44:1301-1306.
• [23]Janssen JA, Burger H, Stolk RP, Grobbee DE, de Jong FH, Lamberts SW, Pols HA: Gender-specific relationship between serum free and totalIGF-1 and bone mineral density in elderly men and women. Eur J Endocrinol 1998, 138:627-632.
• [24]Cohen A, Dempster DW, Recker RR, Stein EM, Lappe JM, Zhou H, Wirth AJ, van Lenthe GH, Kohler T, Zwahlen A, Müller R, Rosen CJ, Cremers S, Nickolas TL, McMahon DJ, Rogers H, Staron RB, LeMaster J, Shane E: Abnormal Bone Microarchitecture and Evidence of Osteoblast Dysfunction in Premenopausal Women with Idiopathic Osteoporosis. J Clin Endocrinol Metab 2011, 96:3095-3101.
• [25]Clemens TL, Karsenty G: The osteoblast: an insulin target cell controlling glucose homeostasis. J Bone Miner Res 2011, 26:677-680.
• [26]Juzwiak CR, Amancio OM, Vitalle MS, Szejnfeld VL, Pinheiro MM: Effect of calcium intake, tennis playing, and body composition on bone-mineral density of Brazilian male adolescents. Int J Sport Nutr Exerc Metab 2008, 18:524-538.
• [27]Penteado VS, Castro CH, Pinheiro Mde M, Santana M, Bertolino S, de Mello MT, Szejnfeld VL: Diet, body composition, and bone mass in well-trained cyclists. J Clin Densitom 2010, 13:43-50.
• [28]Genaro PS, Pereira GA, Pinheiro MM, Szejnfeld VL, Martini LA: Influence of body composition on bone mass in postmenopausal osteoporotic women. Arch Gerontol Geriatr 2010, 51:295-298.
• [29]Pedreira PG, Pinheiro MM, Szejnfeld VL: Bone mineral density and body composition in postmenopausal women with psoriasis and psoriatic arthritis. Arthritis Res Ther 2011, 13:R16. BioMed Central Full Text
• [30]Ilich-Ernst J, Brownbill RA, Ludemann MA, Fu R: Critical factors for bone health in women across age span: how important is muscle mass? Medscape Womens Health 2002, 7:2.
• [31]Bonewald LF: The amazing osteocyte. J Bone Miner Res 2011, 26:229-38.
• [32]Perrien DS, Achenbach SJ, Bledsoe SE, Walser B, Suva LJ, Khosla S, Gaddy D: Bone turnover across the menopause transition: correlations with inhibins and follicle-stimulating hormone. J Clin Endocrinol Metab 2006, 91:1669-1670.
• [33]Xu ZR, Wang AH, Wu XP, Zhang H, Sheng ZF, Wu XY, Xie H, Luo XH, Liao EY: Relationship of age-related concentrations of serum FSH and LH with bone mineral density, prevalence of osteoporosis in native Chinese women. Clin Chim Acta 2009, 400:8-13.
• [34]Reid IR, Plank LD, Evans MC: Fat mass is an important determinant of whole body bone density in premenopausal women but not in men. J Clin Endocrinol Metab 1992, 75:779-782.
• [35]Hsu Y, Venners S, Terwedow H, Feng Y, Niu T, Li Z, Laird N, Brain JD, Cummings SR, Bouxsein ML, Rosen CJ, Xu X: 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 2006, 83:146-154.
• [36]Lu TW, Taylor SJ, O'Connor JJ, Walker PS: Influence of muscle activity on the forces in the femur: an in vivo study. J Biomech 1997, 30:101-1106.
• [37]Jeon YK, Lee JG, Kim SS, Kim BH, Kim SJ, Kim YK, Kim IJ: Association between bone mineral density and metabolic syndrome in pre- and postmenopausal women. Endocr J 2011, 58:87-93.
• [38]Karsenty G: Convergence between bone and energy homeostases: leptin regulation of bone mass. Cell Metab 2006, 4:341-348.
• [39]Graham LS, Parhami F, Tintut Y, Kitchen CM, Demer LL, Effros RB: Oxidized lipids enhance RANKL production by T lymphocytes: implications for lipid-induced bone loss. Clin Immunol 2009, 133:265-75.
• [40]Graham LS, Tintut Y, Parhami F, Kitchen CM, Ivanov Y, Tetradis S, Effros RB: Bone density and hyperlipidemia: the T-lymphocyte connection. J Bone Miner Res 2010, 25:2460-2469.
• [41]Parhami F, Mody N, Gharavi N, Ballard AJ, Tintut Y, Demer LL: Role of the cholesterol biosynthetic pathway in osteoblastic differentiation of marrow stromal cells. J Bone Miner Res 2002, 17:1997-2003.
• [42]Tarakida A, Iino K, Abe K, Taniguchi R, Higuchi T, Mizunuma H, Nakaji S: Hypercholesterolemia accelerates bone loss in postmenopausal women. Climacteric 2011, 14:105-111.
• [43]Majima T, Shimatsu A, Kamatsu Y, Satoh N, Fukao A, Ninomya K, Marsumura T, Atao K: Increased bone turnover in patients with hypercholesterolemia. Endocr J 2008, 55:143-5190.
• [44]Orozco P: Atherogenic lipid profile and elevated lipoprotein (a) are associated with lower bone mineral density in early postmenopausal overweight women. Eur J Epidemiol 2004, 19:1105-1112.
• [45]Yue J, Zhang X, Dong B, Yang M: Statins and bone health in postmenopausal women: a systematic review of randomized controlled trials. Menopause 2010, 17:1071-1079.
• [46]Macdonald HM, New SA, Golden MHN, Campbell MK, Reid DM: Nutritional associations with bone loss during the menopausal transition: evidence of a beneficial effect of calcium, alcohol, and fruit and vegetable nutrients and of a detrimental effect of fatty acids. Am J Clin Nutr 2004, 79:155-165.
• [47]Parhami F: Possible role of oxidized lipids in osteoporosis: hyperlipidemia be a risk factor? Prostaglandins Leukot Essent Fatty Acids 2003, 68:373-378.
• [48]Ackert-Bicknell CL, Demissie S, Marín de Evsikova C, Hsu YH, DeMambro VE, Karasik D, Cupples LA, Ordovas JM, Tucker KL, Cho K, Canalis E, Paigen B, Churchill GA, Forejt J, Beamer WG, Ferrari S, Bouxsein ML, Kiel DP, Rosen CJ: PPARG by dietary fat interaction influences bone mass in mice and humans. J Bone Miner Res 2008, 23:1398-1408.
• [49]Windelinckx A, De Mars G, Beunen G, Aerssens J, Delecluse C, Lefevre J, Thomis MA: Polymorphisms in the vitamin D receptor gene are associated with muscle strength in men and women. Osteoporos Int 2007, 18:1235-1242.
• [50]Promislow JH, Goodman-Gruen D, Slymen DJ, Barrett-Connor E: Protein consumption and bone mineral density in the elderly: the Rancho Bernardo Study. Am J Epidemiol 2002, 155:636-644.
• [51]Sellmeyer DE, Stone KL, Sebastian A, Cummings SR: A high ratio of dietary animal to vegetable protein increases the rate of bone loss and the risk of fracture in postmenopausal women. Study of Osteoporotic Fractures Research Group. Am J Clin Nutr 2001, 73:118-122.
• [52]Fenton TR, Lyon AW, Eliasziw M, Tough SC, Hanley DA: Metaanalysis of the effect of the acid-ash hypothesis of osteoporosis on calcium balance. J Bone Miner Res 2009, 24:1835-1840.
• [53]Hunt JR, Johnson LK, Fariba Roughead ZK: Dietary protein and calcium interact to influence calcium retention: a controlled feeding study. Am J Clin Nutr 2009, 89:1357-1365.
• [54]Dawson DA, Grant BF, Li TK: Quantifying the risks associated with exceeding recommended drinking limits. Alcohol Clin Exp Res 2005, 29:902-908.
• [55]Butler L, Santoro N: The reproductive endocrinology of the menopausal transition. Steroids 2011, 76:627-635.
• [56]Pereira GA, Genaro PS, Sarkis KS, Peters BSE, Santos LC, Martins TA, Martini LA: Validação do questionário de freqüência alimentar para mulheres com osteoporose. Nutrire 2005, 30:85.
• [57]Willett W, Stampfer M: Implications of total energy intake for epidemiological analyses. In Nutrition epidemiology. 2nd edition. Edited by Willett W. New York: Oxford University Press; 1998:514.
• [58]Baeck JA, Jurema J, Frijters JE: A short questionnaire for the measurement of habitual activity in epidemiological studies. Am J Clin Nutri 1982, 36:936-942.
• [59]Brandão CMA, Camargos BM, Zerbini CA, Plapler PG, Mendonça LM, Albergaria BH, Pinheiro MM, Prado M, Eis SR: Posições Oficiais 2008 da Sociedade Brasileira de Densitometria Clínica (SBDens). Arq Bras Endocrinol Metabol 2009, 53:107-112.
• [60]Baumgartner RN, Stauber PM, Koehler KM, Romero L, Garry PJ: Associations of fat and muscle masses with bone mineral in elderly men and women. Am J Clin Nutr 1996, 63:365-372.
• [61]Dawson-Hughes B, Heaney RP, Holick MF, Lips P, Meunier PJ, Vieth R: Estimates of optimal vitamin status. Osteoporosis Int 2005, 16:713-716.