Age-related changes in the fracture resistance of male Fischer F344 rat bone

Bone

Volumn 83, Issue , 2016, Pages 220-232

  Uppuganti, Sasidhar ^a,b   Granke, Mathilde ^a,b   Makowski, Alexander J ^a,b,c   Does, Mark D ^c,d   Nyman, Jeffry S ^a,b,c  

^a DEPARTMENT OF VETERANS AFFAIRS   (United States)

^b VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

Advanced glycation end products; Bound water; Fracture toughness; Porosity; Raman spectroscopy

Indexed keywords

COLLAGEN;

AGE; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE CHARACTERISTICS AND FUNCTIONS; BONE STRENGTH; BONE STRUCTURE; BONE TOUGHNESS; CORTICAL BONE; CROSS LINKING; DISEASE RESISTANCE; FEMUR DIAPHYSIS; FISCHER F344 RAT; FRACTURE; MALE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POROSITY; RAMAN SPECTROMETRY; RAT; RAT STRAIN; TIBIA; TRABECULAR BONE; VERTEBRA BODY; ANIMAL; BIOMECHANICS; BODY WEIGHT; BONE; DIAGNOSTIC IMAGING; FEMUR; FINITE ELEMENT ANALYSIS; FISCHER 344 RAT; LUMBAR VERTEBRA; MICRO-COMPUTED TOMOGRAPHY; PATHOLOGY; PATHOPHYSIOLOGY; RADIUS;

AGING; ANIMALS; BIOMECHANICAL PHENOMENA; BODY WEIGHT; BONE AND BONES; FEMUR; FINITE ELEMENT ANALYSIS; FRACTURES, BONE; LUMBAR VERTEBRAE; MALE; POROSITY; RADIUS; RATS, INBRED F344; SPECTRUM ANALYSIS, RAMAN; X-RAY MICROTOMOGRAPHY;

EID: 84949239071     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2015.11.009     Document Type: Article

References (61)

1. Melton L.J. The prevalence of osteoporosis: gender and racial comparison. Calcif. Tissue Int. 2001, 69:179-181.
2. Mikyas Y., Agodoa I., Yurgin N. A systematic review of osteoporosis medication adherence and osteoporosis-related fracture costs in men. Appl. Health Econ. Health Policy 2014, 12:267-277.
3. Melton L.J., Crowson C.S., O'Fallon W.M. Fracture incidence in Olmsted County, Minnesota: comparison of urban with rural rates and changes in urban rates over time. Osteoporos. Int. 1999, 9:29-37.
4. Haentjens P., Magaziner J., Colon-Emeric C.S., Vanderschueren D., Milisen K., Velkeniers B., Boonen S. Meta-analysis: excess mortality after hip fracture among older women and men. Ann. Intern. Med. 2010, 152:380-390.
5. Johnell O., Kanis J.A., Oden A., Johansson H., De Laet C., Delmas P., Eisman J.A., Fujiwara S., Kroger H., Mellstrom D., Meunier P.J., Melton L.J., O'Neill T., Pols H., Reeve J., Silman A., Tenenhouse A. Predictive value of BMD for hip and other fractures. J. Bone Miner. Res. 2005, 20:1185-1194.
6. Zimmermann E.A. On the Multiscale Origins of Fracture Resistance in Human Bone and Its Biological Degradation 2012.
7. Ekstrom W., Samuelsson B., Ponzer S., Cederholm T., Thorngren K.G., Hedstrom M. Sex effects on short-term complications after hip fracture: a prospective cohort study. Clin. Interv. Aging 2015, 10:1259-1266.
8. Pande I., Scott D.L., O'Neill T.W., Pritchard C., Woolf A.D., Davis M.J. Quality of life, morbidity, and mortality after low trauma hip fracture in men. Ann. Rheum. Dis. 2006, 65:87-92.
9. Burstein A.H., Reilly D.T., Martens M. Aging of bone tissue: mechanical properties. J. Bone Joint Surg. Am. 1976, 58:82-86.
10. McCalden R.W., McGeough J.A., Barker M.B., Court-Brown C.M. Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure. J. Bone Joint Surg. Am. 1993, 75:1193-1205.
11. Zioupos P., Currey J.D., Hamer A.J. The role of collagen in the declining mechanical properties of aging human cortical bone. J. Biomed. Mater. Res. 1999, 45:108-116.
12. Wang X., Shen X., Li X., Agrawal C.M. Age-related changes in the collagen network and toughness of bone. Bone 2002, 31:1-7.
13. Zioupos P., Currey J.D. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone 1998, 22:57-66.
14. Bloomfield S.A., Hogan H.A., Delp M.D. Decreases in bone blood flow and bone material properties in aging Fischer-344 rats. Clin. Orthop. Relat. Res. 2002, 248-57.
15. Kalu D.N., Hardin R.R., Cockerham R., Yu B.P., Norling B.K., Egan J.W. Lifelong food restriction prevents senile osteopenia and hyperparathyroidism in F344 rats. Mech. Ageing Dev. 1984, 26:103-112.
16. Kiebzak G.M., Smith R., Gundberg C.C., Howe J.C., Sacktor B. Bone status of senescent male rats: chemical, morphometric, and mechanical analysis. J. Bone Miner. Res. 1988, 3:37-45.
17. Wang L., Banu J., McMahan C.A., Kalu D.N. Male rodent model of age-related bone loss in men. Bone 2001, 29:141-148.
18. Perrien D.S., Akel N.S., Dupont-Versteegden E.E., Skinner R.A., Siegel E.R., Suva L.J., Gaddy D. Aging alters the skeletal response to disuse in the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292:R988-R996.
19. Pietschmann P., Skalicky M., Kneissel M., Rauner M., Hofbauer G., Stupphann D., Viidik A. Bone structure and metabolism in a rodent model of male senile osteoporosis. Exp. Gerontol. 2007, 42:1099-1108.
20. Duque G., Rivas D., Li W., Li A., Henderson J.E., Ferland G., Gaudreau P. Age-related bone loss in the LOU/c rat model of healthy ageing. Exp. Gerontol. 2009, 44:183-189.
21. Raab D.M., Smith E.L., Crenshaw T.D., Thomas D.P. Bone mechanical properties after exercise training in young and old rats. J. Appl. Physiol. (1985) 1990, (68):130-134.
22. Pinkerton K.E., Barry B.E., O'Neil J.J., Raub J.A., Pratt P.C., Crapo J.D. Morphologic changes in the lung during the lifespan of Fischer 344 rats. Am. J. Anat. 1982, 164:155-174.
23. Tomasek J.J., Meyers S.W., Basinger J.B., Green D.T., Shew R.L. Diabetic and age-related enhancement of collagen-linked fluorescence in cortical bones of rats. Life Sci. 1994, 55:855-861.
24. Akkus O., Adar F., Schaffler M.B. Age-related changes in physicochemical properties of mineral crystals are related to impaired mechanical function of cortical bone. Bone 2004, 34:443-453.
25. Diez-Perez A., Guerri R., Nogues X., Caceres E., Pena M.J., Mellibovsky L., Randall C., Bridges D., Weaver J.C., Proctor A., Brimer D., Koester K.J., Ritchie R.O., Hansma P.K. Microindentation for in vivo measurement of bone tissue mechanical properties in humans. J. Bone Miner. Res. 2010, 25:1877-1885.
26. Manhard M.K., Horch R.A., Gochberg D.F., Nyman J.S., Does M.D. In vivo quantitative MR imaging of bound and pore water in cortical bone. Radiology 2015, (in press).
27. Baron R., Tross R., Vignery A. Evidence of sequential remodeling in rat trabecular bone: morphology, dynamic histomorphometry, and changes during skeletal maturation. Anat. Rec. 1984, 208:137-145.
28. Zhou H., Chernecky R., Davies J.E. Deposition of cement at reversal lines in rat femoral bone. J. Bone Miner. Res. 1994, 9:367-374.
29. Duranova H., Martiniakova M., Omelka R., Grosskopf B., Bobonova I., Toman R. Changes in compact bone microstructure of rats subchronically exposed to cadmium. Acta Vet. Scand. 2014, 56:64.
30. Perilli E., Bala Y., Zebaze R., Reynolds K.J., Seeman E. Regional heterogeneity in the configuration of the intracortical canals of the femoral shaft. Calcif. Tissue Int. 2015, 97:327-335.
31. Ritchie R.O., Koester K.J., Ionova S., Yao W., Lane N.E., Ager J.W. Measurement of the toughness of bone: a tutorial with special reference to small animal studies. Bone 2008, 43:798-812.
32. Bouxsein M.L., Boyd S.K., Christiansen B.A., Guldberg R.E., Jepsen K.J., Muller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J. Bone Miner. Res. 2010, 25:1468-1486.
33. Makowski A.J., Uppuganti S., Wadeer S.A., Whitehead J.M., Rowland B.J., Granke M., Mahadevan-Jansen A., Yang X., Nyman J.S. The loss of activating transcription factor 4 (ATF4) reduces bone toughness and fracture toughness. Bone 2014, 62:1-9.
34. Nyman J.S., Uppuganti S., Makowski A.J., Rowland B.J., Merkel A.R., Sterling J.A., Bredbenner T.L., Perrien D.S. Predicting mouse vertebra strength with micro-computed tomography-derived finite element analysis. BonKey Reports 2015, 4. (In press).
35. Easley S.K., Jekir M.G., Burghardt A.J., Li M., Keaveny T.M. Contribution of the intra-specimen variations in tissue mineralization to PTH- and raloxifene-induced changes in stiffness of rat vertebrae. Bone 2010, 46:1162-1169.
36. Turner C.H., Burr D.B. Basic biomechanical measurements of bone: a tutorial. Bone 1993, 14:595-608.
37. ASTM E399-12. Standard Test Method for Linear-Elastic Plane-Strain Fracture Toughness KIc of Metallic Materials 2013, American Society for Testing and Materials International.
38. Gallant M.A., Brown D.M., Organ J.M., Allen M.R., Burr D.B. Reference-point indentation correlates with bone toughness assessed using whole-bone traditional mechanical testing. Bone 2013, 53:301-305.
39. Granke M., Coulmier A., Uppuganti S., Gaddy J.A., Does M.D., Nyman J.S. Insights into reference point indentation involving human cortical bone: sensitivity to tissue anisotropy and mechanical behavior. J. Mech. Behav. Biomed. Mater. 2014, 37:174-185.
40. Rosner B. Percentage points for a generalized ESD many-outlier procedure. Technometrics 1983, 25:165-172.
41. Nyman J.S., Makowski A.J., Patil C.A., Masui T.P., O'Quinn E.C., Bi X., Guelcher S.A., Nicollela D.P., Mahadevan-Jansen A. Measuring differences in compositional properties of bone tissue by confocal Raman spectroscopy. Calcif. Tissue Int. 2011, 89:111-122.
42. 1H NMR signal in human cortical bone for magnetic resonance imaging. Magn. Reson. Med. 2010, 64:680-687.
43. Horch R.A., Wilkens K., Gochberg D.F., Does M.D. RF coil considerations for short-T2 MRI. Magn. Reson. Med. 2010, 64:1652-1657.
44. Bank R.A., Beekman B., Verzijl N., de Roos J.A., Sakkee A.N., TeKoppele J.M. Sensitive fluorimetric quantitation of pyridinium and pentosidine crosslinks in biological samples in a single high-performance liquid chromatographic run. J. Chromatogr. B Biomed. Sci. Appl. 1997, 703:37-44.
45. Granke M., Makowski A.J., Uppuganti S., Does M.D., Nyman J.S. Identifying novel clinical surrogates to assess human bone fracture toughness. J. Bone Miner. Res. 2015, (in press).
46. Nyman J.S., Roy A., Tyler J.H., Acuna R.L., Gayle H.J., Wang X. Age-related factors affecting the postyield energy dissipation of human cortical bone. J. Orthop. Res. 2007, 25:646-655.
47. Buckley A., Hill K.E., Davison J.S. Methods in Enzymology: Immunochemical Techniques: Part M: Chemotaxis and Inflammation 1988, Academic Press.
48. Jepsen K.J., Andarawis-Puri N. The amount of periosteal apposition required to maintain bone strength during aging depends on adult bone morphology and tissue-modulus degradation rate. J. Bone Miner. Res. 2012, 27:1916-1926.
49. Sato M., Vahle J., Schmidt A., Westmore M., Smith S., Rowley E., Ma L.Y. Abnormal bone architecture and biomechanical properties with near-lifetime treatment of rats with PTH. Endocrinology 2002, 143:3230-3242.
50. Dalle Carbonare L., Giannini S. Bone microarchitecture as an important determinant of bone strength. J. Endocrinol. Investig. 2004, 27:99-105.
51. Johnell O., Oden A., Caulin F., Kanis J.A. Acute and long-term increase in fracture risk after hospitalization for vertebral fracture. Osteoporos. Int. 2001, 12:207-214.
52. Rockoff S.D., Sweet E., Bleustein J. The relative contribution of trabecular and cortical bone to the strength of human lumbar vertebrae. Calcif. Tissue Res. 1969, 3:163-175.
53. Christiansen B.A., Kopperdahl D.L., Kiel D.P., Keaveny T.M., Bouxsein M.L. Mechanical contributions of the cortical and trabecular compartments contribute to differences in age-related changes in vertebral body strength in men and women assessed by QCT-based finite element analysis. J. Bone Miner. Res. 2011, 26:974-983.
54. Ke H.Z., Qi H., Chidsey-Frink K.L., Crawford D.T., Thompson D.D. Lasofoxifene (CP-336,156) protects against the age-related changes in bone mass, bone strength, and total serum cholesterol in intact aged male rats. J. Bone Miner. Res. 2001, 16:765-773.
55. Westerbeek Z.W., Hepple R.T., Zernicke R.F. Effects of aging and caloric restriction on bone structure and mechanical properties. J. Gerontol. A Biol. Sci. Med. Sci. 2008, 63:1131-1136.
56. Zimmermann E.A., Schaible E., Bale H., Barth H.D., Tang S.Y., Reichert P., Busse B., Alliston T., Ager J.W., Ritchie R.O. Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales. PNAS 2011, 108:14416-14421.
57. Granke M., Does M.D., Nyman J.S. The role of water compartments in the material properties of cortical bone. Calcif. Tissue Int. 2015, (in press).
58. Akkus O., Polyakova-Akkus A., Adar F., Schaffler M.B. Aging of microstructural compartments in human compact bone. J. Bone Miner. Res. 2003, 18:1012-1019.
59. Yerramshetty J.S., Lind C., Akkus O. The compositional and physicochemical homogeneity of male femoral cortex increases after the sixth decade. Bone 2006, 39:1236-1243.
60. Allen M.R., Newman C.L., Smith E., Brown D.M., Organ J.M. Variability of in vivo reference point indentation in skeletally mature inbred rats. J. Biomech. 2014, 47:2504-2507.
61. Jenkins T., Coutts L.V., Dunlop D.G., Oreffo R.O., Cooper C., Harvey N.C., Thurner P.J., OStEO group Variability in reference point microindentation and recommendations for testing cortical bone: maximum load, sample orientation, mode of use, sample preparation and measurement spacing. J. Mech. Behav. Biomed. Mater. 2015, 42:311-324.