Bone mineralization is elevated and less heterogeneous in adults with type 2 diabetes and osteoarthritis compared to controls with osteoarthritis alone

Bone

Volumn 54, Issue 1, 2013, Pages 76-82

  Pritchard, J M ^a   Papaioannou, A ^a   Tomowich, C ^a   Giangregorio, L M ^b   Atkinson, S A ^a   Beattie, K A ^a   Adachi, J D ^a   DeBeer, J ^a   Winemaker, M ^a   Avram, V ^a   Schwarcz, H P ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Bone mineralization density distribution (BMDD); Bone quality; Osteoporosis; Quantitative backscattered electron imaging; Type 2 diabetes

Indexed keywords

CALCIUM;

ADULT; AGED; ARTICLE; BONE DENSITY; BONE MINERALIZATION; CALCIUM BONE LEVEL; CAUCASIAN; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; OSTEOARTHRITIS; TRABECULAR BONE;

ADULT; AGED; BONE DENSITY; CALCIFICATION, PHYSIOLOGIC; CALCIUM; CASE-CONTROL STUDIES; DIABETES MELLITUS, TYPE 2; FEMALE; FEMUR NECK; HUMANS; MALE; OSTEOARTHRITIS; REFERENCE STANDARDS;

EID: 84874375764     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.01.032     Document Type: Article

References (78)

1. 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(4):427-444.
2. Janghorbani M., Van Dam R.M., Willett W.C., Hu F.B. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol 2007, 166(5):495-505.
3. Ma L., Oei L., Jiang L., Estrada K., Chen H., Wang Z., et al. Association between bone mineral density and type 2 diabetes mellitus: a meta-analysis of observational studies. Eur J Epidemiol 2012, 27(5):319-332.
4. Kanis J.A., Oden A., Johnell O., Johansson H., De Laet C., Brown J., et al. The use of clinical risk factors enhances the performance of BMD in the prediction of hip and osteoporotic fractures in men and women. Osteoporos Int 2007, 18(8):1033-1046.
5. Fraser L.A., Langsetmo L., Berger C., Ioannidis G., Goltzman D., Adachi J.D., et al. Fracture prediction and calibration of a Canadian FRAX tool: a population-based report from CaMos. Osteoporos Int 2011, 22(3):829-837.
6. Giangregorio L.M., Leslie W.D., Lix L.M., Johansson H., Oden A., McCloskey E., et al. FRAX underestimates fracture risk in patients with diabetes. J Bone Miner Res 2012, 27(2):301-308.
7. Faulkner R.A., McCulloch R.G., Fyke S.L., De Coteau W.E., McKay H.A., Bailey D.A., et al. Comparison of areal and estimated volumetric bone mineral density values between older men and women. Osteoporos Int 1995, 5(4):271-275.
8. Guglielmi G., Floriani I., Torri V., Li J., van Kuijk C., Genant H.K., et al. Effect of spinal degenerative changes on volumetric bone mineral density of the central skeleton as measured by quantitative computed tomography. Acta Radiol 2005, 46(3):269-275.
9. Binkley N., Krueger D., Vallarta-Ast N. An overlying fat panniculus affects femur bone mass measurement. J Clin Densitom 2003, 6(3):199-204.
10. Boivin G., Meunier P.J. Methodological considerations in measurement of bone mineral content. Osteoporos Int 2003, 14(Suppl. 5):S22-S27. [discussion S27-8].
11. Roschger P., Paschalis E.P., Fratzl P., Klaushofer K. Bone mineralization density distribution in health and disease. Bone 2008, 42(3):456-466.
12. Roschger P., Dempster D.W., Zhou H., Paschalis E.P., Silverberg S.J., Shane E., et al. New observations on bone quality in mild primary hyperparathyroidism as determined by quantitative backscattered electron imaging. J Bone Miner Res 2007, 22(5):717-723.
13. Misof B.M., Roschger P., Cosman F., Kurland E.S., Tesch W., Messmer P., et al. Effects of intermittent parathyroid hormone administration on bone mineralization density in iliac crest biopsies from patients with osteoporosis: a paired study before and after treatment. J Clin Endocrinol Metab 2003, 88(3):1150-1156.
14. Reyes-Garcia R., Rozas-Moreno P., Lopez-Gallardo G., Garcia-Martin A., Varsavsky M., Aviles-Perez M.D., et al. Serum levels of bone resorption markers are decreased in patients with type 2 diabetes. Acta Diabetol Nov 1 2011, [Epub ahead of print].
15. Gerdhem P., Isaksson A., Akesson K., Obrant K.J. Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 2005, 16(12):1506-1512.
16. Akin O., Gol K., Akturk M., Erkaya S. Evaluation of bone turnover in postmenopausal patients with type 2 diabetes mellitus using biochemical markers and bone mineral density measurements. Gynecol Endocrinol 2003, 17(1):19-29.
17. Inaba M., Nishizawa Y., Mita K., Kumeda Y., Emoto M., Kawagishi T., et al. Poor glycemic control impairs the response of biochemical parameters of bone formation and resorption to exogenous 1,25-dihydroxyvitamin D3 in patients with type 2 diabetes. Osteoporos Int 1999, 9(6):525-531.
18. Isaia G.C., Ardissone P., Di Stefano M., Ferrari D., Martina V., Porta M., et al. Bone metabolism in type 2 diabetes mellitus. Acta Diabetol 1999, 36(1-2):35-38.
19. Bouillon R. Diabetic bone disease. Low turnover osteoporosis related to decreased IGF-I production. Verh K Acad Geneeskd Belg 1992, 54(4):365-391. [discussion 391-2].
20. Boyde A., Jones S.J. Back-scattered electron imaging of skeletal tissues. Metab Bone Dis Relat Res 1983-1984, 5(3):145-150.
21. Boyde A., Reid S.A. A new method of scanning electron microscopy for imaging biological tissues. Nature 1983, 302(5908):522-523.
22. Reid S.A., Boyde A. Changes in the mineral density distribution in human bone with age: image analysis using backscattered electrons in the SEM. J Bone Miner Res 1987, 2(1):13-22.
23. Ball M.D., McCartney D.G. The measurement of atomic number and composition in an SEM using backscattered detectors. J Microsc 1981, 124(1):57-68.
24. Skedros J.G., Bloebaum R.D., Bachus K.N., Boyce T.M. The meaning of graylevels in backscattered electron images of bone. J Biomed Mater Res 1993, 27(1):47-56.
25. Skedros J.G., Bloebaum R.D., Bachus K.N., Boyce T.M., Constantz B. Influence of mineral content and composition on graylevels in backscattered electron images of bone. J Biomed Mater Res 1993, 27(1):57-64.
26. Roschger P., Plenk H., Klaushofer K., Eschberger J. A new scanning electron microscopy approach to the quantification of bone mineral distribution: backscattered electron image grey-levels correlated to calcium K alpha-line intensities. Scanning Microsc 1995, 9(1):75-86. [discussion 86-8].
27. Vajda E.G., Bloebaum R.D., Skedros J.G. Validation of energy dispersive x-ray spectrometry as a method to standardize backscattered electron images of bone. Cells Mater 1996, 6:79-92.
28. Roschger P., Fratzl P., Eschberger J., Klaushofer K. Validation of quantitative backscattered electron imaging for the measurement of mineral density distribution in human bone biopsies. Bone 1998, 23(4):319-326.
29. Misof B.M., Bodingbauer M., Roschger P., Wekerle T., Pakrah B., Haas M., et al. Short-term effects of high-dose zoledronic acid treatment on bone mineralization density distribution after orthotopic liver transplantation. Calcif Tissue Int 2008, 83(3):167-175.
30. Hofstaetter J.G., Hofstaetter S.G., Nawrot-Wawrzyniak K., Hiertz H., Grohs J.G., Trieb K., et al. Mineralization pattern of vertebral bone material following fragility fracture of the spine. J Orthop Res 2012, 30(7):1089-1094.
31. Hofstaetter J.G., Roetzer K.M., Krepler P., Nawrot-Wawrzyniak K., Schwarzbraun T., Klaushofer K., et al. Altered bone matrix mineralization in a patient with Rett syndrome. Bone 2010, 47(3):701-705.
32. Hofstaetter J.G., Roschger P., Klaushofer K., Kim H.K. Increased matrix mineralization in the immature femoral head following ischemic osteonecrosis. Bone 2010, 46(2):379-385.
33. Canadian Diabetes Association Clinical Practice Guidelines Committee Canadian Diabetes Association 2008 clinical practice guidelines for the prevention and management of diabetes in Canada. Can J Diabetes 2008, 32:S1-S201.
34. Roschger P., Gupta H.S., Berzlanovich A., Ittner G., Dempster D.W., Fratzl P., et al. Constant mineralization density distribution in cancellous human bone. Bone 2003, 32(3):316-323.
35. Zhang W., Moskowitz R.W., Nuki G., Abramson S., Altman R.D., Arden N., et al. OARSI recommendations for the management of hip and knee osteoarthritis, Part II: OARSI evidence-based, expert consensus guidelines. Osteoarthritis Cartilage 2008, 16(2):137-162.
36. Cockcroft D.W., Gault M.H. Prediction of creatinine clearance from serum creatinine. Nephron 1976, 16(1):31-41.
37. Kanis J.A., Oden A., Johnell O., Jonsson B., de Laet C., Dawson A. The burden of osteoporotic fractures: a method for setting intervention thresholds. Osteoporos Int 2001, 12(5):417-427.
38. Charlson M.E., Pompei P., Ales K.L., MacKenzie C.R. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 1987, 40(5):373-383.
39. Washburn R.A., Smith K.W., Jette A.M., Janney C.A. The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol 1993, 46(2):153-162.
40. Boyde A. Scanning electron microscopy of bone. Methods Mol Biol 2012, 816:365-400.
41. Hayat M.A. Fixation for electron microscopy 1981, Academic Press, New York, NY.
42. Vajda E.G., Humphrey S., Skedros J.G., Bloebaum R.D. Influence of topography and specimen preparation on backscattered electron images of bone. Scanning 1999, 21(6):379-387.
43. Otsu N.A. A threshold selection method from gray-level histograms. IEEE Trans Syst Man Cybern 1979, 9:62-66.
44. Frost H.M. Tetracycline-based histological analysis of bone remodeling. Calcif Tissue Res 1969, 3(3):211-237.
45. Parfitt A.M. Skeletal heterogeneity and the purpose of bone remodeling: implications for understanding osteoporosis. Fundamentals of osteoporosis 2009, Academic Press, New York, NY. 3rd ed. R. Marcus, D. Feldman, D. Nelson, C.J. Rosen (Eds.).
46. Burr D.B. Remodeling and the repair of fatigue damage. Calcif Tissue Int 1993, 53(Suppl. 1):S75-S80. [discussion S80-1].
47. Burr D.B., Martin R.B. Calculating the probability that microcracks initiate resorption spaces. J Biomech 1993, 26(4-5):613-616.
48. Boyce T.M., Bloebaum R.D., Bachus K.N., Skedros J.G. Reproducible methods for calibrating the backscattered electron signal for quantitative assessment of mineral content in bone. Scanning Microsc 1990, 4:591-600. [discussion 600-3].
49. Bloebaum R.D., Skedros J.G., Vajda E.G., Bachus K.N., Constantz B.R. Determining mineral content variations in bone using backscattered electron imaging. Bone 1997, 20(5):485-490.
50. Elliot J.C. Calcium phosphate biominerals. Geochemical, geobiological and materials importance 2002, 427-453. Mineralogical Society of America, Washington, DC. M.J. Kohn, J.F. Rakovan, J.M. Hughes (Eds.).
51. Smirnov N.V. Table for estimating the goodness of fit of empirical distributions. Ann Math Stat 1948, 19(2):279-281.
52. Currey J.D. Effects of differences in mineralization on the mechanical properties of bone. Philos Trans R Soc Lond B Biol Sci 1984, 304(1121):509-518.
53. McCormack J., Stover S.M., Gibeling J.C., Fyhrie D.P. Effects of mineral content on the fracture properties of equine cortical bone in double-notched beams. Bone 2012, 50(6):1275-1280.
54. Busse B., Hahn M., Soltau M., Zustin J., Puschel K., Duda G.N., et al. Increased calcium content and inhomogeneity of mineralization render bone toughness in osteoporosis: mineralization, morphology and biomechanics of human single trabeculae. Bone 2009, 45(6):1034-1043.
55. Currey J.D. Changes in the impact energy absorption of bone with age. J Biomech 1979, 12(6):459-469.
56. Currey J.D., Brear K., Zioupos P. The effects of ageing and changes in mineral content in degrading the toughness of human femora. J Biomech 1996, 29:257-260.
57. Vajda E.G., Bloebaum R.D. Age-related hypermineralization in the female proximal human femur. Anat Rec 1999, 255(2):202-211.
58. Boyce T.M., Bloebaum R.D. Cortical aging differences and fracture implications for the human femoral neck. Bone 1993, 14(5):769-778.
59. Ascenzi A., Bonucci E., Ostrowski K., Sliwowski A., Dziedzic-Goclawska A., Stachowicz W., et al. Initial studies on the crystallinity of the mineral fraction and ash content of isolated human and bovine osteons differing in the their degree of calcification. Calcif Tissue Res 1977, 23(1):7-11.
60. Paschalis E., DiCarlo E., Betts F., Sherman P., Mendelsohn R., Boskey A.L. FTIR microspectroscopic analysis of human osteonal bone. Calcif Tissue Int 1996, 59(6):480-487.
61. Dyer D.G., Blackledge J.A., Katz B.M., Hull C.J., Adkisson H.D., Thorpe S.R., et al. The Maillard reaction in vivo. Z Ernahrungswiss 1991, 30(1):29-45.
62. Boehm B.O., Schilling S., Rosinger S., Lang G.E., Lang G.K., Kientsch-Engel R., et al. Elevated serum levels of N(epsilon)-carboxymethyl-lysine, an advanced glycation end product, are associated with proliferative diabetic retinopathy and macular oedema. Diabetologia 2004, 47(8):1376-1379.
63. Schwartz A.V., Garnero P., Hillier T.A., Sellmeyer D.E., Strotmeyer E.S., Feingold K.R., et al. Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metab 2009, 94(7):2380-2386.
64. Ehrlich H., Hanke T., Simon P., Born R., Fischer C., Frolov A., et al. Carboxymethylation of the fibrillar collagen with respect to the formation of hydroxyapatite. J Biomed Mater Res B Appl Biomater 2010, 92B:542-551.
65. Ruffoni D., Fratzl P., Roschger P., Klaushofer K., Weinkamer R. The bone mineralization density distribution as a fingerprint of the mineralization process. Bone 2007, 40(5):1308-1319.
66. Misof B.M., Paschalis E.P., Blouin S., Fratzl-Zelman N., Klaushofer K., Roschger P. Effects of 1year of daily teriparatide treatment on iliacal bone mineralization density distribution (BMDD) in postmenopausal osteoporotic women previously treated with alendronate or risedronate. J Bone Miner Res 2010, 25(11):2297-2303.
67. Roschger P., Rinnerthaler S., Yates J., Rodan G.A., Fratzl P., Klaushofer K. Alendronate increases degree and uniformity of mineralization in cancellous bone and decreases the porosity in cortical bone of osteoporotic women. Bone 2001, 29(2):185-191.
68. Zoehrer R., Roschger P., Paschalis E.P., Hofstaetter J.G., Durchschlag E., Fratzl P., et al. Effects of 3- and 5-year treatment with risedronate on bone mineralization density distribution in triple biopsies of the iliac crest in postmenopausal women. J Bone Miner Res 2006, 21(7):1106-1112.
69. Recker R., Masarachai P., Santora A., Howard T., Chavassieux P., Arlot M., et al. Trabecular bone microarchitecture after alendronate treatment of osteoporotic women. Curr Med Res Opin 2005, 21(2):185-194.
70. Follet H., Viguet-Carrin S., Burt-Pichat B., Depalle B., Bala Y., Gineyts E., et al. Effects of preexisting microdamage, collagen cross-links, degree of mineralization, age, and architecture on compressive mechanical properties of elderly human vertebral trabecular bone. J Orthop Res 2011, 29(4):481-488.
71. Burr D. Microdamage and bone strength. Osteoporos Int 2003, 14(Suppl. 5):S67-S72.
72. Hamann C., Goettsch C., Mettelsiefen J., Henkenjohann V., Rauner M., Hempel U., et al. Delayed bone regeneration and low bone mass in a rat model of insulin-resistant type 2 diabetes mellitus is due to impaired osteoblast function. Am J Physiol Endocrinol Metab 2011, 301(6):E1220-E1228.
73. Carpentier V.T., Wong J., Yeap Y., Gan C., Sutton-Smith P., Badiei A., et al. Increased proportion of hypermineralized osteocyte lacunae in osteoporotic and osteoarthritic human trabecular bone: implications for bone remodeling. Bone 2012, 50:688-694.
74. Boyde A., Jones S.J., Aerssens J., Dequeker J. Mineral density quantitation of the human cortical iliac crest by backscattered electron image analysis: variations with age, sex, and degree of osteoarthritis. Bone 1995, 16:619-627.
75. Cornish J., Callon K.E., Reid I.R. Insulin increases histomorphometric indices of bone formation In vivo. Calcif Tissue Int 1996, 59(6):492-495.
76. Saito M., Fujii K., Mori Y., Marumo K. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int 2006, 17:1514-1523.
77. Pritchard J.M., Giangregorio L.M., Atkinson S.A., Beattie K.A., Inglis D., Ioannidis G., et al. Association of larger holes in the trabecular bone at the distal radius in postmenopausal women with type 2 diabetes mellitus compared to controls. Arthritis Care Res 2012, 64:83-91.
78. Keegan T.H., Schwartz A.V., Bauer D.C., Sellmeyer D.E., Kelsey J.L. Effect of alendronate on bone mineral density and biochemical markers of bone turnover in type 2 diabetic women: the fracture intervention trial. Diabetes Care 2004, 27(7):1547-1553.