Deficits in Trabecular Bone Microarchitecture in Young Women with Type 1 Diabetes Mellitus

Journal of Bone and Mineral Research

Volumn 30, Issue 8, 2015, Pages 1386-1393

  Abdalrahaman, Naiemh ^a   McComb, Christie ^b,c   Foster, John E ^b,c   McLean, John ^b,d   Lindsay, Robert S ^c,e   McClure, John ^c   McMillan, Martin ^a   Drummond, Russell ^e   Gordon, Derek ^e   McKay, Gerard A ^e   Shaikh, M Guftar ^a   Perry, Colin G ^e   Ahmed, S Faisal ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b NHS GREATER GLASGOW AND CLYDE   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d SOUTHERN GENERAL HOSPITAL   (United Kingdom)

^e STOBHILL HOSPITAL   (United Kingdom)

Author keywords

ADIPOSITY; BONE HEALTH; BONE MARROW; GLYCEMIA; MRI

Indexed keywords

BIOCHEMICAL MARKER; SEX HORMONE;

ABDOMINAL FAT; ADULT; ARTICLE; BONE MARROW; BONE MASS; BONE METABOLISM; CONTROLLED STUDY; FEMALE; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; INTRAABDOMINAL FAT; NUCLEAR MAGNETIC RESONANCE IMAGING; OBESITY; RETINOPATHY; TRABECULAR BONE; YOUNG ADULT; ADOLESCENT; CLINICAL TRIAL; DIABETES MELLITUS; FRACTURE; METABOLISM; MULTICENTER STUDY; PATHOLOGY; PATHOPHYSIOLOGY; SPINE; TIBIA;

ADIPOSITY; ADOLESCENT; ADULT; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 1; FEMALE; FRACTURES, BONE; HUMANS; SPINE; TIBIA;

EID: 84930469618     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2465     Document Type: Article

References (50)

1. Forsén L, Meyer HE, Midthjell K, Edna TH., Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trøndelag Health Survey. Diabetologia. 1999; 42: 920-5.
2. Nicodemus KK, Folsom AR., Iowa Women's Health Study. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care. 2001; 24: 1192-7.
3. Hothersall EJ, Livingstone SJ, Looker HC, et al., Contemporary risk of hip fracture in type 1 and type 2 diabetes: a National Registry study from Scotland. J Bone Miner Res. 2014; 29: 1054-60.
4. Chamberlain G, Fox J, Ashton B, Middleton J., Concise review: mesenchymal stem cells: their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells. 2007; 25: 2739-49.
5. Wagegg M, Gaber T, Lohanatha FL, et al., Hypoxia promotes osteogenesis but suppresses adipogenesis of human mesenchymal stromal cells in a hypoxia-inducible factor-1 dependent manner. PLoS One. 2012; 7: e46483.
6. Dunger DB, Regan F, Acerini CL., Childhood and adolescent diabetes. Endocr Dev. 2005; 9: 107-20.
7. Giustina A, Mazziotti G, Canalis E., Growth hormone, insulin-like growth factors, and the skeleton. Endocr Rev. 2008; 29: 535-59.
8. Bredella MA, Torriani M, Ghomi RH, et al., Vertebral bone marrow fat is positively associated with visceral fat and inversely associated with IGF-1 in obese women. Obesity (Silver Spring). 2011; 19: 49-53.
9. Martin LM, McCabe LR., Type I diabetic bone phenotype is location but not gender dependent. Histochem Cell Biol. 2007; 128: 125-33.
10. Zemel B., Bone mineral accretion its relationship to growth, sexual maturation and body composition during childhood and adolescence. World Rev Nutr Diet. 2013; 106: 39-45.
11. Vestergaard P., Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes-a meta-analysis. Osteoporos Int. 2007; 18: 427-44.
12. Genant HK, Engelke K, Fuerst T, et al., Noninvasive assessment of bone mineral and structure: state of the art. J Bone Miner Res. 1996; 11: 707-30.
13. Issever AS, Link TM, Newitt D, Munoz T, Majumdar S., Interrelationships between 3-T-MRI-derived cortical and trabecular bone structure parameters and quantitative-computed-tomography-derived bone mineral density. Magn Reson Imaging. 2010; 28: 1299-305.
14. Shen W, Chen J, Punyanitya M, Shapses S, Heshka S, Heymsfield SB., MRI-measured bone marrow adipose tissue is inversely related to DXA measured bone mineral in Caucasian women. Osteoporos Int. 2007; 18: 641-7.
15. Fazeli PK, Horowitz MC, MacDougald OA, et al., Marrow fat and bone-new perspectives. J Clin Endocrinol Metab. 2013; 98: 935-45.
16. McComb C, Harpur A, Yacoubian C, et al., MRI-based abnormalities in young adults at risk of adverse bone health due to childhood-onset metabolic and endocrine conditions. Clin Endocrinol (Oxf). 2013; 80: 811-7.
17. Vanhamme L, van den Boogaart A, Van Huffel S., Improved method for accurate and efficient quantification of MRS data with use of prior knowledge. J Magn Reson. 1997; 129: 35-43.
18. Naressi A, Couturier C, Devos JM, et al., Java-based graphical user interface for the MRUI quantitation package. Magn Reson Mater Phys. 2001; 12: 141-52.
19. Schellinger D, Lin CS, Lim J, Hatipoglu HG, Pezzullo JC, Singer AJ., Bone marrow fat and bone mineral density on proton MR spectroscopy and dual-energy x-ray absorptiometry: their ratio as a new indicator of bone weakening. Am J Roentgen. 2004; 183: 1761-5.
20. Benjamin Y, Hochberg Y., Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statist Soc Ser B. 1995; 57: 289-300.
21. Svoren BM, Volkening LK, Wood JR, Laffel LM., Significant vitamin D deficiency in youth with type 1 diabetes mellitus. J Pediatr. 2009; 154: 132-4.
22. Al-Daghri NM, Al-Attas OS, Alokail MS, et al., Lower vitamin D status is more common among Saudi adults with diabetes mellitus type 1 than in non-diabetics. BMC Public Health. 2014; 14: 153.
23. Donaldson LJ, Reckless IP, Scholes S, Mindell JS, Shelton NJ., The epidemiology of fractures in England. J Epidemiol Community Health. 2008; 62: 174-180.
24. Slade JM, Coe LM, Meyer RA, McCabe LR., Human bone marrow adiposity is linked with serum lipid levels not T1-diabetes. J Diabetes Complications. 2012; 26: 1-9.
25. Wędrychowicz A, Stec M, Sztefko K, Starzyk JB., Associations between bone, fat tissue and metabolic control in children and adolescents with type 1 diabetes mellitus. Exp Clin Endocrinol Diabetes. 2014; 122: 491-5.
26. Baroncelli GI, Bertelloni S, Ceccarelli C, Cupelli D, Saggese G., Dynamics of bone turnover in children with GH deficiency treated with GH until final height. Eur J Endocrinol. 2000; 142: 549-56.
27. Qvist P, Christgau S, Pedersen BJ, Schlemmer A, Christiansen C., Circadian variation in the serum concentration of C-terminal telopeptide of type I collagen (serumCTx): effects of gender, age, menopausal status, posture, daylight, serum cortisol, and fasting. Bone. 2002; 31: 57-61.
28. Gevers EF, Loveridge N, Robinson IC., Bone marrow adipocytes: a neglected target tissue for growth hormone. Endocrinology. 2002; 143: 4065-73.
29. Guler H-P, Zapf J, Schmid C, Froesch ER., Insulin-like growth factors-I and -II in healthy man: estimation of half-lives and production rates. Acta Endocrinol. 1989; 121: 753-8.
30. Baxter RC, Martin JL, Beniac VA., High molecular weight insulin-like growth factor binding protein complex: purification and properties of the acid-labile subunit from human serum. J Biol Chem. 1989; 264: 11843-8.
31. Amiel SA, Sherwin RS, Hintz RL, Gertner JM, Press CM, Tamborlane WV., Effect of diabetes and its control on insulin-like growth factors in the young subject with type-1 diabetes. Diabetes. 1984; 33: 1175-9.
32. Bereket A, Wilson TA, Blethen SL, et al., Regulation of the acid-labile subunit of the insulin-like growth factor ternary complex in patients with insulin-dependent diabetes mellitus and severe burns. Clin Endocrinol. 1996; 44: 525-32.
33. Dai J, Baxter RC., Regulation in vivo of the acid-labile subunit of the rat serum insulin-like growth factor-binding protein complex. Endocrinology. 1994; 135: 2335-41.
34. Brismar K, Fernqvist-Forbes E, Wahren J, Hall K., Effect of insulin on the hepatic production of insulin-like growth factor-binding protein-1 (IGFBP-1), IGFBP-3 and IGF-I in insulin-dependent diabetes. J Clin Endocrinol Metab. 1994; 79: 872-8.
35. Santos JM, Mohammad G, Zhong Q, Kowluru RA., Diabetic retinopathy, superoxide damage and antioxidants. Curr Pharm Biotechnol. 2011; 12: 352-61.
36. Goettsch C, Babelova A, Trummer O, et al., NADPH oxidase 4 limits bone mass by promoting osteoclastogenesis. J Clin Invest. 2013; 123: 4731-8.
37. Almeida M, O'Brien CA., Basic biology of skeletal aging: role of stress response pathways. J Gerontol A Biol Sci Med Sci. 2013; 68: 1197-208.
38. Miller KK, Biller BM, Lipman JG, Bradwin G, Rifai N, Klibanski A., Truncal adiposity, relative growth hormone deficiency, and cardiovascular risk. J Clin Endocrinol Metab. 2005; 90: 768-74.
39. Menagh PJ, Turner RT, Jump DB, et al., Growth hormone regulates the balance between bone formation and bone marrow adiposity. J Bone Miner Res. 2010; 25: 757-68.
40. Kawai M, de Paula FJ, Rosen CJ., New insights into osteoporosis: the bone-fat connection. J Intern Med. 2012; 272: 317-29.
41. Botolin S, McCabe LR., Bone loss and increased bone adiposity in spontaneous and pharmacologically induced diabetic mice. Endocrinology. 2007; 148: 198-205.
42. Bredella MA, Torriani M, Ghomi RH, et al., Vertebral bone marrow fat is positively associated with visceral fat and inversely associated with IGF-1 in obese women. Obesity. 2011; 19: 49-53.
43. Fazeli PK, Bredella MA, Freedman L, et al., Marrow fat and preadipocyte factor-1 levels decrease with recovery in women with anorexia nervosa. J Bone Miner Res. 2012; 27: 1864-71.
44. Li X, Kuo D, Schafer AL, et al., Quantification of vertebral bone marrow fat content using 3 Tesla MR spectroscopy: reproducibility, vertebral variation, and applications in osteoporosis. J Magn Reson Imaging. 2011; 33: 974-9.
45. Rosen CJ, Bouxsein ML., Mechanisms of disease: is osteoporosis the obesity of bone ? Nat Clin Pract Rheumatol. 2006; 2: 35-43.
46. Justesen J, Stenderup K, Ebbesen EN, Mosekilde L, Steiniche T, Kassem M., Adipocyte tissue volume in bone marrow is increased with aging and in patients with osteoporosis. Biogerontology. 2001; 2: 165-71.
47. Dhaliwal R, Cibula D, Ghosh C, Weinstock RS, Moses AM., Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int. 2014; 25: 1969-73.
48. Govan L, Maietti E, Torsney B, et al., The effect of deprivation and HbA1c on admission to hospital for diabetic ketoacidosis in type 1 diabetes. Diabetologia. 2012; 55: 2356-60.
49. Neumann T, Lodes S, Kästner B, et al., High serum pentosidine but not esRAGE is associated with prevalent fractures in type 1 diabetes independent of bone mineral density and glycaemic control. Osteoporos Int. 2014; 25: 1527-33.
50. Patsch JM, Li X, Baum T, et al., Bone marrow fat composition as a novel imaging biomarker in postmenopausal women with prevalent fragility fractures. J Bone Miner Res. 2013; 28: 1721-8.