Skip to main content
Top
Published in: Osteoporosis International 2/2012

01-02-2012 | Original Article

Serum undercarboxylated osteocalcin levels are inversely associated with glycemic status and insulin resistance in an elderly Japanese male population: Fujiwara-kyo Osteoporosis Risk in Men (FORMEN) Study

Authors: M. Iki, J. Tamaki, Y. Fujita, K. Kouda, A. Yura, E. Kadowaki, Y. Sato, J. S. Moon, K. Tomioka, N. Okamoto, N. Kurumatani

Published in: Osteoporosis International | Issue 2/2012

Login to get access

Abstract

Summary

Recent animal studies have demonstrated that undercarboxylated osteocalcin upregulates insulin secretion via osteoblast-insulin signaling. However, it remains unclear whether such a pathway exists in humans. This study showed that serum undercarboxylated osteocalcin levels were inversely associated with fasting plasma glucose, hemoglobin A1c, and homeostasis model assessment of insulin resistance (HOMA-IR) levels in community-dwelling elderly Japanese men.

Introduction

Undercarboxylated osteocalcin (ucOC) was reported to increase insulin secretion and improve glucose tolerance via osteoblast-insulin signaling in animal-based studies. Whether this pathway also exists in humans is unknown. We aimed to clarify whether serum ucOC levels are associated with glycemic status and insulin resistance in the general Japanese population.

Methods

We included 2,174 Japanese men (≥65 years) who were able to walk without aid from others and lived at home in four cities of Nara Prefecture. We excluded participants with a history of diseases or medications that affect bone metabolism, other than type 2 diabetes mellitus (T2DM). Fasting plasma glucose, glycated hemoglobin A1c, and HOMA-IR levels were determined as outcome measures.

Results

Of the 1,597 participants included in the analysis, both intact OC (iOC) and ucOC levels showed significant inverse correlations with all outcome measures, even after adjusting for potential confounders. Mean values of outcome measures showed a significant decreasing trend with higher quintiles of iOC or ucOC after adjusting for confounders. This trend remained significant for ucOC quintiles after further adjustment for iOC levels, but was not significant for iOC quintiles after adjusting for ucOC levels. These results were attenuated, but still apparent, after excluding participants receiving drug therapy for T2DM.

Conclusions

Levels of ucOC, but not iOC, were inversely associated with glycemic index and insulin resistance in a population of Japanese men. These findings will need to be confirmed with longitudinal studies.
Literature
1.
go back to reference Delmas PD, Eastell R, Garnero P, Seibel MJ, Stepan J, Committee of Scientific Advisors of the International Osteoporosis Foundation (2000) The use of biochemical markers of bone turnover in osteoporosis. Osteoporos Int 11(Suppl 6):S2–17PubMedCrossRef Delmas PD, Eastell R, Garnero P, Seibel MJ, Stepan J, Committee of Scientific Advisors of the International Osteoporosis Foundation (2000) The use of biochemical markers of bone turnover in osteoporosis. Osteoporos Int 11(Suppl 6):S2–17PubMedCrossRef
2.
go back to reference Christiansen C, Riis BJ, Rodbro P (1990) Screening procedure for women at risk of developing postmenopausal osteoporosis. Osteoporos Int 1:35–40PubMedCrossRef Christiansen C, Riis BJ, Rodbro P (1990) Screening procedure for women at risk of developing postmenopausal osteoporosis. Osteoporos Int 1:35–40PubMedCrossRef
3.
go back to reference Iki M, Morita A, Ikeda Y, Sato Y, Akiba T, Matsumoto T, Nishino H, Kagamimori S, Kagawa Y, Yoneshima H, JPOS Study Group (2006) Biochemical markers of bone turnover predict bone loss in perimenopausal women but not in postmenopausal women—the Japanese Population-based Osteoporosis (JPOS) Cohort Study. Osteoporos Int 17:1086–1095PubMedCrossRef Iki M, Morita A, Ikeda Y, Sato Y, Akiba T, Matsumoto T, Nishino H, Kagamimori S, Kagawa Y, Yoneshima H, JPOS Study Group (2006) Biochemical markers of bone turnover predict bone loss in perimenopausal women but not in postmenopausal women—the Japanese Population-based Osteoporosis (JPOS) Cohort Study. Osteoporos Int 17:1086–1095PubMedCrossRef
4.
go back to reference Garnero P, Sornay-Rendu E, Duboeuf F, Delmas PD (1999) Markers of bone turnover predict postmenopausal forearm bone loss over 4 years: the OFELY study. J Bone Miner Res 14:1614–1621PubMedCrossRef Garnero P, Sornay-Rendu E, Duboeuf F, Delmas PD (1999) Markers of bone turnover predict postmenopausal forearm bone loss over 4 years: the OFELY study. J Bone Miner Res 14:1614–1621PubMedCrossRef
5.
go back to reference Luukinen H, Käkönen SM, Pettersson K, Koski K, Laippala P, Lövgren T, Kivelä SL, Väänänen HK (2000) Strong prediction of fractures among older adults by the ratio of carboxylated to total serum osteocalcin. J Bone Miner Res 15:2473–2478PubMedCrossRef Luukinen H, Käkönen SM, Pettersson K, Koski K, Laippala P, Lövgren T, Kivelä SL, Väänänen HK (2000) Strong prediction of fractures among older adults by the ratio of carboxylated to total serum osteocalcin. J Bone Miner Res 15:2473–2478PubMedCrossRef
6.
go back to reference Sarkar S, Reginster JY, Crans GG, Diez-Perez A, Pinette KV, Delmas PD (2004) Relationship between changes in biochemical markers of bone turnover and BMD to predict vertebral fracture risk. J Bone Miner Res 19:394–401PubMedCrossRef Sarkar S, Reginster JY, Crans GG, Diez-Perez A, Pinette KV, Delmas PD (2004) Relationship between changes in biochemical markers of bone turnover and BMD to predict vertebral fracture risk. J Bone Miner Res 19:394–401PubMedCrossRef
7.
go back to reference Inukai T, Fujiwara Y, Tayama K, Aso Y, Takemura Y (1997) Alterations in serum levels of 1 alpha 25(OH)2 D3 and osteocalcin in patients with early diabetic nephropathy. Diab Res Clin Pract 38:53–59CrossRef Inukai T, Fujiwara Y, Tayama K, Aso Y, Takemura Y (1997) Alterations in serum levels of 1 alpha 25(OH)2 D3 and osteocalcin in patients with early diabetic nephropathy. Diab Res Clin Pract 38:53–59CrossRef
8.
go back to reference Akin O, Göl K, Aktürk M, Erkaya S (2003) Evaluation of bone turnover in postmenopausal patients with type 2 diabetes mellitus using biochemical markers and bone mineral density measurements. Gynecol Endocrinol 17:19–29PubMed Akin O, Göl K, Aktürk M, Erkaya S (2003) Evaluation of bone turnover in postmenopausal patients with type 2 diabetes mellitus using biochemical markers and bone mineral density measurements. Gynecol Endocrinol 17:19–29PubMed
9.
go back to reference Dobnig H, Piswanger-Sölkner JC, Roth M, Obermayer-Pietsch B, Tiran A, Strele A, Maier E, Maritschnegg P, Sieberer C, Fahrleitner-Pammer A (2006) Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91:3355–3363PubMedCrossRef Dobnig H, Piswanger-Sölkner JC, Roth M, Obermayer-Pietsch B, Tiran A, Strele A, Maier E, Maritschnegg P, Sieberer C, Fahrleitner-Pammer A (2006) Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91:3355–3363PubMedCrossRef
10.
go back to reference Im JA, Yu BP, Jeon JY, Kim SH (2008) Relationship between osteocalcin and glucose metabolism in postmenopausal women. Clin Chim Acta 396:66–69PubMedCrossRef Im JA, Yu BP, Jeon JY, Kim SH (2008) Relationship between osteocalcin and glucose metabolism in postmenopausal women. Clin Chim Acta 396:66–69PubMedCrossRef
11.
go back to reference Zhou M, Ma X, Li H, Pan X, Tang J, Gao Y, Hou X, Lu H, Bao Y, Jia W (2009) Serum osteocalcin concentrations in relation to glucose and lipid metabolism in Chinese individuals. Eur J Endocrinol 161:723–729PubMedCrossRef Zhou M, Ma X, Li H, Pan X, Tang J, Gao Y, Hou X, Lu H, Bao Y, Jia W (2009) Serum osteocalcin concentrations in relation to glucose and lipid metabolism in Chinese individuals. Eur J Endocrinol 161:723–729PubMedCrossRef
12.
go back to reference Okazaki R, Totsuka Y, Hamano K, Ajima M, Miura M, Hirota Y, Hata K, Fukumoto S, Matsumoto T (1997) Metabolic improvement of poorly controlled noninsulin-dependent diabetes mellitus decreases bone turnover. J Clin Endocrinol Metab 82:2915–2920PubMedCrossRef Okazaki R, Totsuka Y, Hamano K, Ajima M, Miura M, Hirota Y, Hata K, Fukumoto S, Matsumoto T (1997) Metabolic improvement of poorly controlled noninsulin-dependent diabetes mellitus decreases bone turnover. J Clin Endocrinol Metab 82:2915–2920PubMedCrossRef
13.
go back to reference Kanazawa I, Yamaguchi T, Yamauchi M, Yamamoto M, Kurioka S, Yano S, Sugimoto T (2009) Adiponectin is associated with changes in bone markers during glycemic control in type 2 diabetes mellitus. J Clin Endocrinol Metab 94:3031–3037PubMedCrossRef Kanazawa I, Yamaguchi T, Yamauchi M, Yamamoto M, Kurioka S, Yano S, Sugimoto T (2009) Adiponectin is associated with changes in bone markers during glycemic control in type 2 diabetes mellitus. J Clin Endocrinol Metab 94:3031–3037PubMedCrossRef
14.
go back to reference Rosato MT, Schneider SH, Shapses SA (1998) Bone turnover and insulin-like growth factor I levels increase after improved glycemic control in noninsulin-dependent diabetes mellitus. Calcif Tissue Int 63:107–111PubMedCrossRef Rosato MT, Schneider SH, Shapses SA (1998) Bone turnover and insulin-like growth factor I levels increase after improved glycemic control in noninsulin-dependent diabetes mellitus. Calcif Tissue Int 63:107–111PubMedCrossRef
15.
go back to reference Sayinalp S, Gedik O, Koray Z (1995) Increasing serum osteocalcin after glycemic control in diabetic men. Calcif Tissue Int 57:422–425PubMedCrossRef Sayinalp S, Gedik O, Koray Z (1995) Increasing serum osteocalcin after glycemic control in diabetic men. Calcif Tissue Int 57:422–425PubMedCrossRef
16.
go back to reference Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G (2007) Endocrine regulation of energy metabolism by the skeleton. Cell 130:456–469PubMedCrossRef Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G (2007) Endocrine regulation of energy metabolism by the skeleton. Cell 130:456–469PubMedCrossRef
17.
go back to reference Ferron M, Hinoi E, Karsenty G, Ducy P (2008) Osteocalcin differentially regulates beta cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci USA 105:5266–5270PubMedCrossRef Ferron M, Hinoi E, Karsenty G, Ducy P (2008) Osteocalcin differentially regulates beta cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci USA 105:5266–5270PubMedCrossRef
18.
go back to reference Kanazawa I, Yamaguchi T, Yamamoto M, Yamauchi M, Kurioka S, Yano S, Sugimoto T (2009) Serum osteocalcin level is associated with glucose metabolism and atherosclerosis parameters in type 2 diabetes mellitus. J Clin Endocrinol Metab 94:45–49PubMedCrossRef Kanazawa I, Yamaguchi T, Yamamoto M, Yamauchi M, Kurioka S, Yano S, Sugimoto T (2009) Serum osteocalcin level is associated with glucose metabolism and atherosclerosis parameters in type 2 diabetes mellitus. J Clin Endocrinol Metab 94:45–49PubMedCrossRef
19.
go back to reference Pittas AG, Harris SS, Eliades M, Stark P, Dawson-Hughes B (2009) Association between serum osteocalcin and markers of metabolic phenotype. J Clin Endocrinol Metab 94:827–832PubMedCrossRef Pittas AG, Harris SS, Eliades M, Stark P, Dawson-Hughes B (2009) Association between serum osteocalcin and markers of metabolic phenotype. J Clin Endocrinol Metab 94:827–832PubMedCrossRef
20.
go back to reference Kindblom JM, Ohlsson C, Ljunggren O, Karlsson MK, Tivesten A, Smith U, Mellström D (2009) Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. J Bone Miner Res 24:785–791PubMedCrossRef Kindblom JM, Ohlsson C, Ljunggren O, Karlsson MK, Tivesten A, Smith U, Mellström D (2009) Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. J Bone Miner Res 24:785–791PubMedCrossRef
21.
go back to reference Yeap BB, Chubb SA, Flicker L, McCaul KA, Ebeling PR, Beilby JP, Norman PE (2010) Reduced serum total osteocalcin is associated with metabolic syndrome in older men via waist circumference, hyperglycemia, and triglyceride levels. Eur J Endocrinol 163:265–272PubMedCrossRef Yeap BB, Chubb SA, Flicker L, McCaul KA, Ebeling PR, Beilby JP, Norman PE (2010) Reduced serum total osteocalcin is associated with metabolic syndrome in older men via waist circumference, hyperglycemia, and triglyceride levels. Eur J Endocrinol 163:265–272PubMedCrossRef
22.
go back to reference Shea MK, Gundberg CM, Meigs JB, Dallal GE, Saltzman E, Yoshida M, Jacques PF, Booth SL (2009) γ-carboxylation of osteocalcin and insulin resistance in older men and women. Am J Clin Nutr 90:1230–1235PubMedCrossRef Shea MK, Gundberg CM, Meigs JB, Dallal GE, Saltzman E, Yoshida M, Jacques PF, Booth SL (2009) γ-carboxylation of osteocalcin and insulin resistance in older men and women. Am J Clin Nutr 90:1230–1235PubMedCrossRef
23.
go back to reference Hwang YC, Jeong IK, Ahn KJ, Chung HY (2009) The uncarboxylated form of osteocalcin is associated with improved glucose tolerance and enhanced beta-cell function in middle-aged male subjects. Diab Metab Res Rev 25:768–772CrossRef Hwang YC, Jeong IK, Ahn KJ, Chung HY (2009) The uncarboxylated form of osteocalcin is associated with improved glucose tolerance and enhanced beta-cell function in middle-aged male subjects. Diab Metab Res Rev 25:768–772CrossRef
24.
go back to reference Kanazawa I, Yamaguchi T, Yamauchi M, Yamamoto M, Kurioka S, Yano S, Sugimoto T (2010) Serum undercarboxylated osteocalcin was inversely associated with plasma glucose level and fat mass in type 2 diabetes mellitus. Osteoporos Int. doi:10.1007/s00198-101-1184-7 Kanazawa I, Yamaguchi T, Yamauchi M, Yamamoto M, Kurioka S, Yano S, Sugimoto T (2010) Serum undercarboxylated osteocalcin was inversely associated with plasma glucose level and fat mass in type 2 diabetes mellitus. Osteoporos Int. doi:10.​1007/​s00198-101-1184-7
25.
go back to reference Iki M, Fujita Y, Tamaki J, Kouda K, Yura A, Kadowaki E, Sato Y, Moon JS, Okamoto N, Kurumatani N, Study Group for Functioning Capacity and Quality of Life in Elderly Japanese (Fujiwara-kyo Study Group) (2009) Design and baseline characteristics of a prospective cohort study for determinants of osteoporotic fracture in community-dwelling elderly Japanese men: the Fujiwara-kyo osteoporosis risk in men (FORMEN) study. BMC Musculoskelet Disord 10:165PubMedCrossRef Iki M, Fujita Y, Tamaki J, Kouda K, Yura A, Kadowaki E, Sato Y, Moon JS, Okamoto N, Kurumatani N, Study Group for Functioning Capacity and Quality of Life in Elderly Japanese (Fujiwara-kyo Study Group) (2009) Design and baseline characteristics of a prospective cohort study for determinants of osteoporotic fracture in community-dwelling elderly Japanese men: the Fujiwara-kyo osteoporosis risk in men (FORMEN) study. BMC Musculoskelet Disord 10:165PubMedCrossRef
26.
go back to reference Ikeda Y, Iki M, Morita A, Kajita E, Kagamimori S, Kagawa Y, Yoneshima H (2006) Intake of fermented soybeans, natto, is associated with reduced bone loss in postmenopausal women: Japanese Population-Based Osteoporosis (JPOS) Study. J Nutr 136:1323–1328PubMed Ikeda Y, Iki M, Morita A, Kajita E, Kagamimori S, Kagawa Y, Yoneshima H (2006) Intake of fermented soybeans, natto, is associated with reduced bone loss in postmenopausal women: Japanese Population-Based Osteoporosis (JPOS) Study. J Nutr 136:1323–1328PubMed
27.
go back to reference Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE, Pratt M, Ekelund U, Yngve A, Sallis JF, Oja P (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35:1381–1395PubMedCrossRef Craig CL, Marshall AL, Sjostrom M, Bauman AE, Booth ML, Ainsworth BE, Pratt M, Ekelund U, Yngve A, Sallis JF, Oja P (2003) International physical activity questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35:1381–1395PubMedCrossRef
28.
go back to reference American Diabetes Association (2010) Diagnosis and classification of diabetes mellitus. Diab Care 33(Suppl 1):S62–S69CrossRef American Diabetes Association (2010) Diagnosis and classification of diabetes mellitus. Diab Care 33(Suppl 1):S62–S69CrossRef
29.
go back to reference Seino Y, Nanjo K, Tajima N, Kadowaki T, Kasiwaki A, Araki E, Ito C, Inagaki N, Iwamoto Y, Kasuga M, Hanafusa T, Naneda K, Ueki K, Japan Diabetes Society Committee for the Classification and Diagnostic Criteria of Diabetes Mellitus (2010) Committee Report. J Jpn Diabetes Soc 53:450–465, in Japanese Seino Y, Nanjo K, Tajima N, Kadowaki T, Kasiwaki A, Araki E, Ito C, Inagaki N, Iwamoto Y, Kasuga M, Hanafusa T, Naneda K, Ueki K, Japan Diabetes Society Committee for the Classification and Diagnostic Criteria of Diabetes Mellitus (2010) Committee Report. J Jpn Diabetes Soc 53:450–465, in Japanese
30.
go back to reference Kashiwagi A, Kadowaki T, Haneda K, Nawata H, Ito H, Tominaga M, Oikawa S, Noda M, Kawamura T, Sanke T, Namba M, Hasiramoto M, Sasahara T, Nishio Y, Takei I, Umemoto M, Kuwa K, Murakami M, Oguri T, Committee for Standardization of Diabetes-related Laboratory Measurements (2009) The Japanese deal to world-wide standardization of the hemoglobin A1c measurement. J Jpn Diabetes Soc 52:811–818, in Japanese Kashiwagi A, Kadowaki T, Haneda K, Nawata H, Ito H, Tominaga M, Oikawa S, Noda M, Kawamura T, Sanke T, Namba M, Hasiramoto M, Sasahara T, Nishio Y, Takei I, Umemoto M, Kuwa K, Murakami M, Oguri T, Committee for Standardization of Diabetes-related Laboratory Measurements (2009) The Japanese deal to world-wide standardization of the hemoglobin A1c measurement. J Jpn Diabetes Soc 52:811–818, in Japanese
31.
go back to reference Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419PubMedCrossRef Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419PubMedCrossRef
32.
go back to reference Kawaguchi H, Matsumoto T, Kurokawa T, Orimo H, Mizunashi K, Takuwa Y, Niimi H, Shiraki M, Ohara T, Shishiba Y, Tsuchiya Y, Takahshi H, Takatsuki K, Seino Y, Morii H, Fujita T, Okamoto S, Ogata E (1990) Serum levels of BGP determined by two-site immunoradiometric assay (IRMA) using monoclonal antibodies. Clin Endocrinol 38:1291–1296 (in Japanese) Kawaguchi H, Matsumoto T, Kurokawa T, Orimo H, Mizunashi K, Takuwa Y, Niimi H, Shiraki M, Ohara T, Shishiba Y, Tsuchiya Y, Takahshi H, Takatsuki K, Seino Y, Morii H, Fujita T, Okamoto S, Ogata E (1990) Serum levels of BGP determined by two-site immunoradiometric assay (IRMA) using monoclonal antibodies. Clin Endocrinol 38:1291–1296 (in Japanese)
33.
go back to reference Nishimura J, Arai N, Tohmatsu J (2007) Measurement of serum undercarboxylated osteocalcin by electrochemiluminescence immunoassay with the “Picolumi ucOC” kit. Igaku to Yakugaku 57:523–535 (in Japanese) Nishimura J, Arai N, Tohmatsu J (2007) Measurement of serum undercarboxylated osteocalcin by electrochemiluminescence immunoassay with the “Picolumi ucOC” kit. Igaku to Yakugaku 57:523–535 (in Japanese)
34.
go back to reference Ishizawa Y, Inaba M, Ishii K, Yamashita H, Miki T, Goto H, Yamada S, Chaki O, Kurasawa K, Mochiduki Y (2005) Evaluation of newly developed kit for measurement of bone-specific tartrate-resistant acid phosphatase in blood. Igaku to Yakugaku 54:709–717 (in Japanese) Ishizawa Y, Inaba M, Ishii K, Yamashita H, Miki T, Goto H, Yamada S, Chaki O, Kurasawa K, Mochiduki Y (2005) Evaluation of newly developed kit for measurement of bone-specific tartrate-resistant acid phosphatase in blood. Igaku to Yakugaku 54:709–717 (in Japanese)
35.
go back to reference Fulzele K, Riddle RC, Digirolamo DJ, Cao X, Wan C, Chen D, Faugere MC, Aja S, Hussain MA, Brüning JC, Clemens TL (2010) Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell 142:309–319PubMedCrossRef Fulzele K, Riddle RC, Digirolamo DJ, Cao X, Wan C, Chen D, Faugere MC, Aja S, Hussain MA, Brüning JC, Clemens TL (2010) Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell 142:309–319PubMedCrossRef
37.
go back to reference Yoshida M, Jacques PF, Meigs JB, Saltzman E, Shea MK, Gundberg C, Dawson-Hughes B, Dallal G, Booth SL (2008) Effect of vitamin K supplementation on insulin resistance in older men and women. Diab Care 31:2092–2096CrossRef Yoshida M, Jacques PF, Meigs JB, Saltzman E, Shea MK, Gundberg C, Dawson-Hughes B, Dallal G, Booth SL (2008) Effect of vitamin K supplementation on insulin resistance in older men and women. Diab Care 31:2092–2096CrossRef
38.
go back to reference Yoshida M, Booth SL, Meigs JB, Saltzman E, Jacques PF (2008) Phylloquinone intake, insulin sensitivity, and glycemic status in men and women. Am J Clin Nutr 88:210–215PubMed Yoshida M, Booth SL, Meigs JB, Saltzman E, Jacques PF (2008) Phylloquinone intake, insulin sensitivity, and glycemic status in men and women. Am J Clin Nutr 88:210–215PubMed
39.
go back to reference Bouillon R, Bex M, Van Herck E, Laureys J, Dooms L, Lesaffre E, Ravussin E (1995) Influence of age, sex, and insulin on osteoblast function: osteoblast dysfunction in diabetes mellitus. J Clin Endocrinol Metab 80:1194–1202PubMedCrossRef Bouillon R, Bex M, Van Herck E, Laureys J, Dooms L, Lesaffre E, Ravussin E (1995) Influence of age, sex, and insulin on osteoblast function: osteoblast dysfunction in diabetes mellitus. J Clin Endocrinol Metab 80:1194–1202PubMedCrossRef
40.
go back to reference Lumachi F, Camozzi V, Tombolan V, Luisetto G (2009) Bone mineral density, osteocalcin, and bone-specific alkaline phosphatase in patients with insulin-dependent diabetes mellitus. Ann NY Acad Sci 1173(Suppl 1):E64–67PubMedCrossRef Lumachi F, Camozzi V, Tombolan V, Luisetto G (2009) Bone mineral density, osteocalcin, and bone-specific alkaline phosphatase in patients with insulin-dependent diabetes mellitus. Ann NY Acad Sci 1173(Suppl 1):E64–67PubMedCrossRef
41.
go back to reference Danielson KK, Elliott ME, LeCaire T, Binkley N, Palta M (2010) Poor glycemic control is associated with low BMD detected in premenopausal women with type 1 diabetes. Osteoporos Int 20:923–933CrossRef Danielson KK, Elliott ME, LeCaire T, Binkley N, Palta M (2010) Poor glycemic control is associated with low BMD detected in premenopausal women with type 1 diabetes. Osteoporos Int 20:923–933CrossRef
42.
go back to reference Maggio AB, Ferrari S, Kraenzlin M, Marchand LM, Schwitzgebel V, Beghetti M, Rizzoli R, Farpour-Lambert NJ (2010) Decreased bone turnover in children and adolescents with well controlled type 1 diabetes. J Pediatr Endocrinol Metab 23:697–707PubMedCrossRef Maggio AB, Ferrari S, Kraenzlin M, Marchand LM, Schwitzgebel V, Beghetti M, Rizzoli R, Farpour-Lambert NJ (2010) Decreased bone turnover in children and adolescents with well controlled type 1 diabetes. J Pediatr Endocrinol Metab 23:697–707PubMedCrossRef
43.
go back to reference Botolin S, McCabe LR (2006) Chronic hyperglycemia modulates osteoblast gene expression through osmotic and non-osmotic pathways. J Cell Biochem 99:411–424PubMedCrossRef Botolin S, McCabe LR (2006) Chronic hyperglycemia modulates osteoblast gene expression through osmotic and non-osmotic pathways. J Cell Biochem 99:411–424PubMedCrossRef
44.
go back to reference Balint E, Szabo P, Marshall CF, Sprague SM (2001) Glucose-induced inhibition of in vitro bone mineralization. Bone 28:21–28PubMedCrossRef Balint E, Szabo P, Marshall CF, Sprague SM (2001) Glucose-induced inhibition of in vitro bone mineralization. Bone 28:21–28PubMedCrossRef
45.
go back to reference Gundberg CM, Nieman SD, Abrams S, Rosen H (1998) Vitamin K status and bone health: an analysis of methods for determination of undercarboxylated osteocalcin. J Clin Endocrinol Metab 83:3258–3266PubMedCrossRef Gundberg CM, Nieman SD, Abrams S, Rosen H (1998) Vitamin K status and bone health: an analysis of methods for determination of undercarboxylated osteocalcin. J Clin Endocrinol Metab 83:3258–3266PubMedCrossRef
46.
Metadata
Title
Serum undercarboxylated osteocalcin levels are inversely associated with glycemic status and insulin resistance in an elderly Japanese male population: Fujiwara-kyo Osteoporosis Risk in Men (FORMEN) Study
Authors
M. Iki
J. Tamaki
Y. Fujita
K. Kouda
A. Yura
E. Kadowaki
Y. Sato
J. S. Moon
K. Tomioka
N. Okamoto
N. Kurumatani
Publication date
01-02-2012
Publisher
Springer-Verlag
Published in
Osteoporosis International / Issue 2/2012
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-011-1600-7

Other articles of this Issue 2/2012

Osteoporosis International 2/2012 Go to the issue