Reduced serum concentrations of carboxylated and undercarboxylated osteocalcin are associated with risk of developing type 2 diabetes mellitus in a high cardiovascular risk population: A nested case-control study

Journal of Clinical Endocrinology and Metabolism

Volumn 98, Issue 11, 2013, Pages 4524-4531

  Díaz López, Andrés ^a,b   Bulló, Mònica ^a,b   Juanola Falgarona, Marti ^a,b   Martínez González, Miguel A ^b,d   Estruch, Ramón ^b,e   Covas, Maria Isabel ^b,f   Arós, Fernando ^c,g   Salas Salvadó, Jordi ^a,b  

^a INSTITUT D INVESTIGACIÓ SANITÀRIA PERE VIRGILI IISPV   (Spain)

^b Instituto de Salud Carlos III   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

^d UNIVERSITY OF NAVARRA   (Spain)

^e HOSPITAL CLÍNIC   (Spain)

^f INST MUNIC D INVESTIGACIO MEDICA   (Spain)

^g HOSPITAL TXAGORRITXU   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLATED OSTEOCALCIN; INSULIN; OLIVE OIL; OSTEOCALCIN; UNCARBOXYLATED OSTEOCALCIN; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CASE CONTROL STUDY; CONTROLLED STUDY; DIABETOGENESIS; FAMILY HISTORY; FEMALE; FOLLOW UP; HIGH RISK POPULATION; HOMEOSTASIS; HUMAN; INSULIN RESISTANCE; LIFESTYLE; LOW FAT DIET; MAJOR CLINICAL STUDY; MALE; MEDITERRANEAN DIET; MULTICENTER STUDY (TOPIC); NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK FACTOR;

AGED; AGING; CARDIOVASCULAR DISEASES; CASE-CONTROL STUDIES; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; INCIDENCE; MALE; MEDITERRANEAN REGION; MIDDLE AGED; OSTEOCALCIN; PROSPECTIVE STUDIES; RISK FACTORS;

EID: 84887488911     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2013-2472     Document Type: Article

References (32)

1. Narayan KM, Gregg EW, Fagot-Campagna A, EngelgauMM,Vinicor F. Diabetes - a common, growing, serious, costly, and potentially preventable public health problem. Diabetes Res Clin Pract 2000;50(suppl 2):S77-S84.
2. Whiting DR, Guariguata L, Weil C, Shaw J. IDF diabetes atlas: global estimates of the prevalence of diabetes for 2011 and 2030. Diabetes Res Clin Pract. 2011;94: 311-321.
3. Tabák AG, Jokela M, Akbaraly TN, Brunner EJ, Kivimäki M, Witte DR. Trajectories of glycaemia, insulin sensitivity, and insulin secretion before diagnosis of type 2 diabetes: an analysis from the Whitehall II study. Lancet. 2009;373: 2215-2221.
4. Clemens TL, Karsenty G. The osteoblast: an insulin target cell controlling glucose homeostasis. J Bone Miner Res. 2011;26: 677-680.
5. Villafán-Bernal JR, Sánchez-Enríquez S, Muñoz-Valle JF. Molecular modulation of osteocalcin and its relevance in diabetes (review). Int J Mol Med. 2011;28: 283-293.
6. Lee NK, Sowa H, Hinoi E, et al. Endocrine regulation of energy metabolism by the skeleton. Cell. 2007;130: 456-469.
7. Ferron M, Hinoi E, Karsenty G, Ducy P. Osteocalcin differentially regulates β cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci USA. 2008;105: 5266-5270.
8. Ferron M, McKeeMD,Levine RL, Ducy P, Karsenty G. Intermittent injections of osteocalcin improve glucose metabolism and prevent type 2 diabetes in mice. Bone. 2012;50: 568-575.
9. Kindblom JM, Ohlsson C, Ljunggren O, et al. Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. J Bone Miner Res. 2009;24: 785-791.
10. Saleem U, Mosley TH Jr, Kullo IJ. Serum osteocalcin is associated with measures of insulin resistance, adipokine levels, and the presence of metabolic syndrome. Arterioscler Thromb Vasc Biol. 2010; 30: 1474-1478.
11. Kanazawa I, Yamaguchi T, Tada Y, et al. Serum osteocalcin level is positively associated with insulin sensitivity and secretion in patients with type 2 diabetes. Bone. 2011;48: 720-725.
12. Kanazawa I, Yamaguchi T, Yamauchi M, et al. Serum undercarboxylated osteocalcin was inversely associated with plasma glucose level and fat mass in type 2 diabetes mellitus. Osteoporos Int. 2011; 22: 187-194.
13. Sarkar PD, Choudhury AB. Relationship of serum osteocalcin levels with blood glucose, insulin resistance and lipid profile in central Indian men with type 2 diabetes. Arch Physiol Biochem. 2012;118: 260-264.
14. Iki M, Tamaki J, Fujita Y, Kouda K, et al. Serum undercarboxylated osteocalcin levels are inversely associated with glycemic status and insulin resistance in an elderly Japanese male population: Fujiwarakyo Osteoporosis Risk in Men (FORMEN) study. Osteoporos Int. 2012;23: 761-770.
15. Zhou M, Ma X, Li H, et al. Serum osteocalcin concentrations in relation to glucose and lipid metabolism in chinese individuals. Eur J Endocrinol. 2009;161: 723-729.
16. Hwang YC, Jeong IK, Ahn KJ, Chung HY. Circulating osteocalcin level is associated with improved glucose tolerance, insulin secretion and sensitivity independent of the plasma adiponectin level. Osteoporos Int. 2012;23: 1337-1342.
17. OosterwerffMM,van SchoorNM,Lips P, EekhoffEM.Osteocalcin as a predictor of the metabolic syndrome in older persons: a population- based study. Clin Endocrinol (Oxf). 2013;78: 242-247.
18. Bulló M, Moreno-Navarrete JM, Fernández-Real JM, et al. Total and undercarboxylated osteocalcin predict changes in insulin sensitivity andβ cell function in elderly men at high cardiovascular risk. Am J Clin Nutr. 2012;95: 249-255.
19. Shea MK, Gundberg CM, Meigs JB, et al. γ-Carboxylation of osteocalcin and insulin resistance in older men and women. Am J Clin Nutr. 2009;90: 1230-1235.
20. Ngarmukos C, Chailurkit LO, Chanprasertyothin S, Hengprasith B, Sritara P, Ongphiphadhanakul B. A reduced serum level of total osteocalcin in men predicts the development of diabetes in a longterm follow-up cohort. Clin Endocrinol (Oxf). 2012;77: 42-46.
21. Hwang YC, Jee JH, Jeong IK, Ahn KJ, Chung HY, Lee MK. Circulating osteocalcin level is not associated with incident type 2 diabetes in middle-aged male subjects: mean 8.4-year retrospective follow-up study. Diabetes Care. 2012;35: 1919-1924.
22. Martínez-González MÁ, Corella D, Salas-Salvadó J, et al. for the PREDIMED Study Investigators Cohort profile: design and methods of the PREDIMED study. Int J Epidemiol. 2012;41: 377-385.
23. Estruch R, Ros E, Salas-Salvadó J, et al. Primary prevention of cardiovascular disease with a Mediterranean diet.NEngl J Med. 2013; 368: 1279-1290.
24. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2013;36(suppl 1):S67-S74.
25. Fernández-Ballart JD, Piñol JL, Zazpe I, et al. Relative validity of a semi-quantitative food-frequency questionnaire in an elderly Mediterranean population of Spain. Br J Nutr. 2010;103: 1808-1816.
26. Schröder H, Fitó M, Estruch R, et al. A short screener is valid for assessing Mediterranean diet adherence among older Spanish men and women. J Nutr. 2011;141: 1140-1145.
27. Elosua R, Marrugat J, Molina L, Pons S, Pujol E. Validation of the Minnesota leisure time physical activity questionnaire in Spanish men. TheMARATHOMinvestigators. Am J Epidemiol. 1994;139: 1197-1209.
28. Hwang YC, Jeong IK, Ahn KJ, Chung HY. The uncarboxylated form of osteocalcin is associated with improved glucose tolerance and enhancedβ-cell function in middle-aged male subjects. Diabetes Metab Res Rev. 2009;25: 768-772.
29. Yoshida M, Jacques PF, Meigs JB, et al. Effect of vitamin K supplementation on insulin resistance in older men and women. Diabetes Care. 2008;31: 2092-2096.
30. Binkley NC, Krueger DC, Engelke JA, Foley AL, Suttie JW. Vitamin K supplementation reduces serum concentrations of under-γ-carboxylated osteocalcin in healthy young and elderly adults.AmJ Clin Nutr. 2000;72: 1523-1528.
31. Lubin JH, Gail MH. Biased selection of controls for case-control analyses of cohort studies. Biometrics. 1984;40: 63-75.
32. Wacholder S. Bias in full cohort and nested case-control studies? Epidemiology. 2009;20: 339-340.