Suppressed bone turnover in obesity: A link to energy metabolism? a case-control study

Journal of Clinical Endocrinology and Metabolism

Volumn 99, Issue 6, 2014, Pages 2155-2163

  Viljakainen, Heli ^a   Ivaska, Kaisa K ^d   Paldánius, Päivi ^a,e   Lipsanen Nyman, Marita ^a   Saukkonen, Tero ^a,f   Pietiläinen, Kirsi H ^b   Andersson, Sture ^a   Laitinen, Kalevi ^c   Mäkitie, Outi ^a,g,h  

^a UNIVERSITY OF HELSINKI AND HELSINKI UNIVERSITY HOSPITAL   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^d UNIVERSITY OF TURKU   (Finland)

^e NOVARTIS PHARMA AG   (Switzerland)

^f NOVO NORDISK A S   (Denmark)

^g FOLKHÄLSAN RESEARCH CENTER   (Finland)

^h KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE TARTRATE RESISTANT ISOENZYME; ALKALINE PHOSPHATASE; COLLAGEN; CROSS LINKED TELOPEPTIDE OF TYPE 1 COLLAGEN; GLUCOSE; INSULIN; N TERMINAL PROPEPTIDE OF TYPE 1 COLLAGEN; UNCLASSIFIED DRUG;

ADULT; AGE; ARTICLE; BODY MASS; BONE TURNOVER; CASE CONTROL STUDY; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; ENERGY METABOLISM; FEMALE; GENDER; GLUCOSE METABOLISM; HUMAN; MAJOR CLINICAL STUDY; MALE; OBESITY; ONSET AGE; ORAL GLUCOSE TOLERANCE TEST; PRIORITY JOURNAL;

ADOLESCENT; ADULT; BIOLOGICAL MARKERS; BONE AND BONES; BONE REMODELING; CASE-CONTROL STUDIES; ENERGY METABOLISM; FEMALE; GLUCOSE TOLERANCE TEST; HUMANS; MALE; OBESITY; OSTEOCALCIN; YOUNG ADULT;

EID: 84902352371     PISSN: 0021972X     EISSN: 19457197     Source Type: Journal    
DOI: 10.1210/jc.2013-3097     Document Type: Article

References (55)

1. Fukumoto S, Martin TJ. Bone as an endocrine organ. Trends Endocrinol Metab. 2009;20(5):230-236.
2. Lieben L, Callewaert F, Bouillon R. Bone and metabolism: a complex crosstalk. Horm Res. 2009;71(suppl 1):134-138.
3. Wei J, Ducy P. Co-dependence of bone and energy metabolisms. Arch Biochem Biophys. 2010;503(1):35-40.
4. Lee NK Sowa H Hinoi E et al Endocrine regulation of energy metabolism by the skeleton Cell. 2007 130 3 456-469.
5. Ivaska KK, Gerdhem P, Vaananen HK, Akesson K, Obra nt KJ. Bone turnover markers and prediction of fracture: a prospective follow-up study of 1040 elderly women for a mean of 9 years. J Bone Miner Res. 2010;25(2):393-403.
6. Lenora J, Ivaska KK, Obra nt KJ, Gerdhem P. Prediction of bone loss using biochemical markers of bone turnover. Osteoporos Int. 2007; 18(9):1297-1305.
7. Ferron M, Hinoi E, Karsenty G, Ducy P. Osteocalcin di fferentially regulates beta cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci USA. 2008;105(13):5266-5270.
8. Hinoi E, Gao N, Jung DY, et al. The sympathetic tone mediates leptin's inhibition of insulin secretion by modulating osteocalcin bioactivity. J Cell Biol. 2008;183(7):1235-1242.
9. 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(2):568-575.
10. Fulzele K, Riddle RC, DiGirolamo DJ, et al. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell. 2010;142(2):309-319.
11. Ferron M, Wei J, Yoshizawa T, Del Fattore A, et al. Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell. 2010;142(2):296-308.
12. Booth SL, Centi A, Smith SR , Gundberg C. The role of osteocalcin in human glucose metabolism: marker or mediator? Nat Rev Endocrinol. 2013;9(1):43-55.
13. Gundberg CM, Lian JB, Booth SL. Vitamin K-dependent carboxylation of osteocalcin: friend or foe? Adv Nutr. 2012;3(2):149-157.
14. Kindblom JM, Ohlsson C, Ljunggren O, et al. Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish m en. J Bone Miner Res. 2009;24(5):785-791.
15. Pittas AG, Harris SS, Eliades M, Stark P, Dawson-Hughes B. Association between serum osteocalcin and markers of metabolic phenotype. J Clin Endocrinol Metab. 2009;94(3):827-832.
16. Paldanius PM, Ivaska KK, Hovi P, et al. Total and carboxylated osteocalcin associate with insulin levels in young adults born with normal or very lo w birth weight. PLoS One. 2013;8(5):e63036.
17. Lucey AJ, Paschos GK, Thorsdottir I, Martinez JA, Cashman KD, Kiely M. Young overweight and obese women with lower circulating osteocalcin concentrations exhibit higher insulin resistance and concentrations of C-reactive protein. Nutr Res. 2013;33(1):67-75.
18. 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(4):1337-1342.
19. Lu C, Ivaska KK, Alen M, et al. Serum osteocalcin is not associated with glucose but is inversely associated with leptin across generations of nondiabetic women. J Clin Endocrinol Metab. 2012;97(11): 4106-4114.
20. Shea MK, Gundberg CM , Meigs JB, et al.-Carboxylation of osteocalcin and insulin resistance in older men and women. Am J Clin Nutr. 2009;90(5):1230-1235.
21. Schwartz AV, Schafer AL, Grey A, et al. Eff ects of antiresorptive therapies on glucose metabolism: results from the FIT, HORIZONPFT, and FREEDOM trials. J Bone Miner Res. 2013;28(6):1348-1354.
22. Rosen CJ, Bouxsein ML. Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol. 2006;2(1):35-43.
23. Idelevich A, Sato K, Baron R. What are the effects of leptin on bone and where are they exerted? J Bone Miner Res. 2013;28(1):18-21.
24. Janghorbani M, Van Dam RM, Willett WC, Hu FB. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007;166(5):495-505.
25. Hamann C, Kirschner S, Gunther KP, Hofbauer LC. Bone, sweet bone-osteoporotic fractures in diabetes mellitus. Nat Rev Endocrinol. 2012;8(5):297-305.
26. Dimitri P Bishop N Walsh JS Eastell R Obesity is a risk factor for fracture in children but is protective against fracture in adults: a paradox Bone. 2012 50 2 457-466.
27. Sinha R, Fisch G, Teague B, et al. Prevalence of impaired glucose tolerance among children and adolescents with marked obesity. N Engl J Med. 2002;346(11):802-810.
28. Molgaard C, Thomsen BL, Michaelsen KF. Whole body bone mineral accretion in healthy children and adolescents. Arch Dis Child. 1999;81(1):10-15.
29. World Health Organization, Department of Noncommunicable Disease Surveillance. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus. Geneva: World Health Organization; 1999.
30. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412-419.
31. Kakonen SM, Hellman J, Karp M, et al. Development and evaluation of three immunofluorometric assays that measure different forms of osteocalcin in serum. Clin Chem. 2000;46(3):332-337.
32. Paldanius PM, Ivaska KK, Hovi P, et al. The effect of oral glucose tolerance test on serum osteocalcin and bone turnover markers in young adults. Calcif Tissue Int. 2012;90(2):90-95.
33. Alatalo SL, Ivaska KK, Waguespack SG, Econs MJ, Vaananen HK, Halleen JM. Osteoclast-derived serum tartrate-resistant acid phosphatase 5b in Albers-Schonberg disease (type II autosomal dominant osteopetrosis). Clin Chem. 2004;50(5):883-890.
34. Rissanen JP, Suominen MI, Peng Z, Halleen JM. Secreted tartrateresistant acid phosphatase 5b is a marke r of osteoclast number in human osteoclast cultures and the rat ovariectomy model. Calcif Tissue Int. 2008;82(2):108-115.
35. Eastell R, Robins SP, Colwell T, Assiri AM, Riggs BL, Russell RG. Evaluation of bone turnover in type I osteoporosis using biochemical markers specific for both bone formation and bone resorption. Osteoporos Int. 1993;3(5):255-260.
36. Hind K, Oldroyd B, Truscott JG. In vivo precision of the GE lunar iDXA densitometer for the measurement of total-body, lumbar spine, and femoral bone mineral density in adults. J Clin Densitom. 2010;13(4):4 13-417.
37. McAuley KA, Williams SM, Mann JI, et al. Diagnosing insulin resistance in the general population. Diabetes Care. 2001;24(3):460-464.
38. Bini V, Igli B aroncelli G, Papi F, Celi F, Saggese G, Falorni A. Relationships of serum leptin levels with biochemical markers of bone turnover and with growth factors in normal weight and overweight children. Horm Res. 2004;61(4 ):170-175.
39. Cohen A, Dempster DW, Recker RR, et al. Abdominal fat is associated with lower bone formation and inferior bone quality in healthy premenopausal women: a transiliac bone biopsy study. J Clin Endocrinol Metab. 2013;98(6):2562-2572.
40. Abseyi N, Siklar Z, Berberoglu M, Hacihamdioglu B, Savas Erdeve S, Ocal G. Relationships between osteocalcin, glucose metabolism, and adiponectin in obese children: is there crosstalk between bone tissue and glucose metabolism? J Clin Res Pediatr Endocrinol. 2012; 4(4):182-188.
41. Dimitri P, Wales JK, Bishop N. Adipokines, bone-derived facto rs and bone turnover in obese children: evidence for altered fat-bone signalling resulting in reduced bone mass. Bone. 2011;48(2):189-196.
42. Grethen E, Hill KM, Jones R, et al. Serum leptin, p arathyroid hormone, 1,25-dihydroxyvitamin D, fibroblast growth factor 23, bone alkaline phosphatase, and sclerostin relationships in obesity. J Clin Endocrinol Metab. 2012;97(5):1655-1662.
43. Cosman F, Ruff ing J, Zion M, et al. Determinants of stress fracture risk in United States military academy cadets. Bone. 2013;55(2): 359-366.
44. Clowes JA, Allen HC, Prentis DM, Eastell R, Blumso hn A. Octreotide abolishes the acute decrease in bone turnover in response to oral glucose. J Clin Endocrinol Metab. 2003;88(10):4867-4873.
45. Thrailkill KM, Lumpkin CK Jr, Bunn RC, Kemp SF , Fowlkes JL. Is insulin an anabolic agent in bone? dissecting the diabetic bone for clues. Am J Physiol Endocrinol Metab. 2005;289(5):E735-E745.
46. Hoang QQ, Sicheri F, Howard AJ, Yang DS. Bone recognition mechanism of porcine osteocalcin from crystal structure. Nature. 2003;425(6961):977-980.
47. Clemens TL Karsenty G The osteoblast: an insulin target cell controlling glucose homeostasis J Bone Miner Res. 2011 26 4 677-680.
48. Sinha N, Shieh A, Stein EM, et al. IncreasedPTHand 1.25(OH)(2)D levels associated with increased markers of bone turnover followi ng bariatric surgery. Obesity (Silver Spring). 2011;19(12):2388-2393.
49. Legiran S, Brandi ML. Bone mass regulation of leptin and postmenopausal osteoporosis with obesity. Clin Cases Miner Bone Metab. 2012;9(3):145-149.
50. Goulding A, Cannan R, Williams SM, Gold EJ, Taylor RW, Lewis-Barned NJ. Bone mineral density in girls with forearm fractures. J Bone Miner Res. 1998;13(1):143-148.
51. Valerio G, Galle F, Mancusi C, et al. Prevalence of overweight in children with bone fractures: a case control study. BMC Pediatr. 2012;12:166.
52. Kessler J, Koebnick C, Smith N, Adams A. Childhood obesity is associated with increased risk of most lower extremity fractures. Clin Orthop Relat Res. 471(4):1199-1207.
53. Henriksen DB, Alexandersen P, Byrjalsen I, et al. Reduction of nocturnal rise in bone resorption by subcutaneous GLP-2. Bone. 2004; 34(1):140-147.
54. Henriksen DB, Alexandersen P, Hartmann B, et al. Disassociation of bone resorption and formation by GLP-2: a 14-day study in healthy postmenopausal women. Bone. 2007;40( 3):723-729.
55. Henriksen DB, Alexandersen P, Hartmann B, et al. Four-month treatment with GLP-2 significantly increases hip BMD: a randomized, placebo-controlled, dose-ranging study in postmenopausal women with low BMD. Bone. 2009;45(5):833-842.