The influence of age on adaptive bone formation and bone resorption

Biomaterials

Volumn 35, Issue 34, 2014, Pages 9290-9301

  Birkhold, Annette I ^a,b   Razi, Hajar ^a,b   Duda, Georg N ^a   Weinkamer, Richard ^c   Checa, Sara ^a   Willie, Bettina M ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b Berlin Brandenburg School for Regenerative Therapies   (Germany)

^c MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

Author keywords

Adaptation; Aging; Bone remodeling; Image analysis; Microstructure

Indexed keywords

AGING OF MATERIALS; IMAGE ANALYSIS; MAMMALS; MICROSTRUCTURE;

ADAPTATION; ADAPTIVE CAPACITY; ADAPTIVE RESPONSE; BONE REMODELING; BONE-FORMING CELLS; MECHANICAL LOADING; MECHANICAL PERFORMANCE; MECHANICAL STIMULATION;

BONE;

ADAPTATION; ADULT; AGED; AGING; ANIMAL EXPERIMENT; ARTICLE; BONE MASS; BONE REMODELING; BONE STRUCTURE; CONTROLLED STUDY; FEMALE; IMAGE ANALYSIS; MECHANICAL LOADING; MECHANICAL STIMULATION; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; MOUSE; MUSCULOSKELETAL SYSTEM PARAMETERS; NONHUMAN; OSSIFICATION; OSTEOLYSIS; PRIORITY JOURNAL; THICKNESS; THREE DIMENSIONAL IMAGING; TIBIA; TRABECULAR BONE; AGE; ANIMAL; BONE DENSITY; BONE DEVELOPMENT; C57BL MOUSE; COMPUTER ASSISTED TOMOGRAPHY; IMAGE PROCESSING; PHYSIOLOGY; RADIOGRAPHY; REPRODUCIBILITY; ANIMAL CELL; ANIMAL TISSUE; GROUPS BY AGE; OSTEOBLAST;

ADAPTATION, PHYSIOLOGICAL; AGE FACTORS; ANIMALS; BONE DENSITY; BONE REMODELING; FEMALE; IMAGE PROCESSING, COMPUTER-ASSISTED; MICE; MICE, INBRED C57BL; OSTEOGENESIS; REPRODUCIBILITY OF RESULTS; TIBIA; TOMOGRAPHY, X-RAY COMPUTED;

ANIMALIA; MAMMALIA; MUS;

EID: 84906781688     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2014.07.051     Document Type: Article

References (50)

1. Frost H.M. Bone dynamics in metabolic bone disease. JBone Jt Surg Am 1966, 48(6):1192-1203.
2. 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(3):443-453.
3. Fuchs R.K., Bauer J.J., Snow C.M. Jumping improves hip and lumbar spine bone mass in prepubescent children: a randomized controlled trial. JBone Min Res 2001, 16(1):148-156.
4. Heinonen A., Kannus P., Sievanen H., Oja P., Pasanen M., Rinne M., et al. Randomised controlled trial of effect of high-impact exercise on selected risk factors for osteoporotic fractures. Lancet 1996, 348(9038):1343-1347.
5. Kato T., Terashima T., Yamashita T., Hatanaka Y., Honda A., Umemura Y. Effect of low-repetition jump training on bone mineral density in young women. JAppl Physiol 2006, 100(3):839-843.
6. Kohrt W.M., Ehsani A.A., Birge S.J. Effects of exercise involving predominantly either joint-reaction or ground-reaction forces on bone mineral density in older women. JBone Min Res 1997, 12(8):1253-1261.
7. Buhl K.M., Jacobs C.R., Turner R.T., Evans G.L., Farrell P.A., Donahue H.J. Aged bone displays an increased responsiveness to low-intensity resistance exercise. JAppl Physiol 2001, 90(4):1359-1364.
8. Leppanen O.V., Sievanen H., Jokihaara J., Pajamaki I., Kannus P., Jarvinen T.L. Pathogenesis of age-related osteoporosis: impaired mechano-responsiveness of bone is not the culprit. PLoS One 2008, 3(7):e2540.
9. Birkhold A.I., Razi H., Duda G.N., Weinkamer R., Checa S., Willie B.M. Mineralizing surface is the main target of mechanical stimulation independent of age: 3D dynamic invivo morphometry. Bone 2014, 66C:15-25.
10. Silbermann M., Bar-Shira-Maymon B., Coleman R., Reznick A., Weisman Y., Steinhagen-Thiessen E., et al. Long-term physical exercise retards trabecular bone loss in lumbar vertebrae of aging female mice. Calcif Tissue Int 1990, 46(2):80-93.
11. Hoshi A., Watanabe H., Chiba M., Inaba Y. Effects of exercise at different ages on bone density and mechanical properties of femoral bone of aged mice. Tohoku J Exp Med 1998, 185(1):15-24.
12. Srinivasan S., Agans S.C., King K.A., Moy N.Y., Poliachik S.L., Gross T.S. Enabling bone formation in the aged skeleton via rest-inserted mechanical loading. Bone 2003, 33(6):946-955.
13. Jarvinen T.L., Pajamaki I., Sievanen H., Vuohelainen T., Tuukkanen J., Jarvinen M., et al. Femoral neck response to exercise and subsequent deconditioning in young and adult rats. JBone Min Res 2003, 18(7):1292-1299.
14. Raab D.M., Smith E.L., Crenshaw T.D., Thomas D.P. Bone mechanical properties after exercise training in young and old rats. JAppl Physiol 1990, 68(1):130-134.
15. Umemura Y., Ishiko T., Tsujimoto H., Miura H., Mokushi N., Suzuki H. Effects of jump training on bone hypertrophy in young and old rats. Int J Sports Med 1995, 16(6):364-367.
16. Brodt M.D., Silva M.J. Aged mice have enhanced endocortical response and normal periosteal response compared with young-adult mice following 1 week of axial tibial compression. JBone Min Res 2010, 25(9):2006-2015.
17. Lynch M.E., Main R.P., Xu Q., Walsh D.J., Schaffler M.B., Wright T.M., et al. Cancellous bone adaptation to tibial compression is not sex dependent in growing mice. JAppl Physiol 2010, 109(3):685-691.
18. De Souza R.L., Matsuura M., Eckstein F., Rawlinson S.C., Lanyon L.E., Pitsillides A.A. Non-invasive axial loading of mouse tibiae increases cortical bone formation and modifies trabecular organization: a new model to study cortical and cancellous compartments in a single loaded element. Bone 2005, 37(6):810-818.
19. Lynch M.E., Main R.P., Xu Q., Schmicker T.L., Schaffler M.B., Wright T.M., et al. Tibial compression is anabolic in the adult mouse skeleton despite reduced responsiveness with aging. Bone 2011, 49(3):439-446.
20. Kesavan C., Mohan S., Oberholtzer S., Wergedal J.E., Baylink D.J. Mechanical loading-induced gene expression and BMD changes are different in two inbred mouse strains. JAppl Physiol 2005, 99(5):1951-1957.
21. Silva M.J., Brodt M.D., Lynch M.A., Stephens A.L., Wood D.J., Civitelli R. Tibial loading increases osteogenic gene expression and cortical bone volume in mature and middle-aged mice. PLoS One 2012, 7(4):e34980.
22. Willie B.M., Birkhold A.I., Razi H., Thiele T., Aido M., Kruck B., et al. Diminished response to invivo mechanical loading in trabecular and not cortical bone in adulthood of female C57Bl/6 mice coincides with a reduction in deformation to load. Bone 2013, 55(2):335-346.
23. Hauge E.M., Mosekilde L., Melsen F. Stereological considerations concerning the measurement of individual osteoid seams and resorption cavities. Bone Mineral 1994, 26(1):89-90.
24. Slyfield C.R., Tkachenko E.V., Wilson D.L., Hernandez C.J. Three-dimensional dynamic bone histomorphometry. JBone Min Res 2012, 27(2):486-495.
25. Waarsing J.H., Day J.S., van der Linden J.C., Ederveen A.G., Spanjers C., De Clerck N., et al. Detecting and tracking local changes in the tibiae of individual rats: a novel method to analyse longitudinal invivo micro-CT data. Bone 2004, 34(1):163-169.
26. Schulte F.A., Lambers F.M., Kuhn G., Muller R. Invivo micro-computed tomography allows direct three-dimensional quantification of both bone formation and bone resorption parameters using time-lapsed imaging. Bone 2011, 48(3):433-442.
27. Lambers F.M., Kuhn G., Schulte F.A., Koch K., Muller R. Longitudinal assessment of invivo bone dynamics in a mouse tail model of postmenopausal osteoporosis. Calcif Tissue Int 2012, 90(2):108-119.
28. Lambers F.M., Schulte F.A., Kuhn G., Webster D.J., Muller R. Mouse tail vertebrae adapt to cyclic mechanical loading by increasing bone formation rate and decreasing bone resorption rate as shown by time-lapsed invivo imaging of dynamic bone morphometry. Bone 2011, 49(6):1340-1350.
29. Fritton J.C., Myers E.R., Wright T.M., van der Meulen M.C. Loading induces site-specific increases in mineral content assessed by microcomputed tomography of the mouse tibia. Bone 2005, 36(6):1030-1038.
30. Clarke K.A., Still J. Gait analysis in the mouse. Physiol Behav 1999, 66(5):723-729.
31. Sugiyama T., Saxon L.K., Zaman G., Moustafa A., Sunters A., Price J.S., et al. Mechanical loading enhances the anabolic effects of intermittent parathyroid hormone (1-34) on trabecular and cortical bone in mice. Bone 2008, 43(2):238-248.
32. Sugiyama T., Meakin L.B., Browne W.J., Galea G.L., Price J.S., Lanyon L.E. Bones' adaptive response to mechanical loading is essentially linear between the low strains associated with disuse and the high strains associated with the lamellar/woven bone transition. JBone Min Res 2012, 27(8):1784-1793.
33. Schulte F.A., Lambers F.M., Mueller T.L., Stauber M., Muller R. Image interpolation allows accurate quantitative bone morphometry in registered micro-computed tomography scans. Comput Methods Biomech Biomed Engin 2014, 17(5):539-548.
34. Meijering E.H.W. Spline interpolation in medical imaging: comparison with other convolution-based approaches. Signal processing X: theories and applications-proceedings of EUSIPCO 2000, M., the European association for signal processing, Tampere 2000, vol. IV:1989-1996.
35. 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. JBone Min Res 2010, 25(7):1468-1486.
36. Dempster D.W., Compston J.E., Drezner M.K., Glorieux F.H., Kanis J.A., Malluche H., et al. Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR histomorphometry nomenclature committee. JBone Min Res 2013, 28(1):2-17.
37. Hochberg Y. Asharper bonferroni procedure for multiple tests of significance. Biometrika 1988, 75(4):800-802.
38. Buie H.R., Moore C.P., Boyd S.K. Postpubertal architectural developmental patterns differ between the L3 vertebra and proximal tibia in three inbred strains of mice. JBone Min Res 2008, 23(12):2048-2059.
39. Glatt V., Canalis E., Stadmeyer L., Bouxsein M.L. Age-related changes in trabecular architecture differ in female and male C57BL/6J mice. JBone Min Res 2007, 22(8):1197-1207.
40. Somerville J.N., Aspden R.M., Armour K.E., Armour K.J., Reid D.M. Growth of C57B1/6 mice and the material and mechanical properties of cortical bone from the tibia. Calcif Tissue Int 2004, 74(5):469-475.
41. Hildebrand T., Ruegsegger P. Anew method for the model-independent assessment of thickness in three-dimensional images. JMicrosc-Oxford 1997, 185:67-75.
42. Fritton J.C., Myers E.R., Wright T.M., van der Meulen M.C. Bone mass is preserved and cancellous architecture altered due to cyclic loading of the mouse tibia after orchidectomy. JBone Min Res 2008, 23(5):663-671.
43. Pflanz D., Berthet E., Birkhold A.I., Thiele T., Li C., Ke H.Z., et al. No additive effects of invivo loading and sclerostin antibody treatment on bone anabolism in elderly mice. JBone Min Res 2012, 27(Suppl.1).
44. Barak M.M., Weiner S., Shahar R. Importance of the integrity of trabecular bone to the relationship between load and deformation of rat femora: an optical metrology study. JMater Chem 2008, 18(32):3855-3864.
45. Meganck J.A., Kozloff K.M., Thornton M.M., Broski S.M., Goldstein S.A. Beam hardening artifacts in micro-computed tomography scanning can be reduced by x-ray beam filtration and the resulting images can be used to accurately measure BMD. Bone 2009, 45(6):1104-1116.
46. Klinck R.J., Campbell G.M., Boyd S.K. Radiation effects on bone architecture in mice and rats resulting from invivo micro-computed tomography scanning. Med Eng Phys 2008, 30(7):888-895.
47. Bonucci E., Ballanti P., Della Rocca C., Milani S., Lo Cascio V., Imbimbo B. Technical variability of bone histomorphometric measurements. Bone Mineral 1990, 11(2):177-186.
48. Erben R.G. Bone-labeling techniques. Handbook of histology methods for bone and cartilage 2002, 99-117. Chapter 5, Humana Press. Y. An, K. Martin (Eds.).
49. Riggs B.L., Khosla S., Melton L.J. Sex steroids and the construction and conservation of the adult skeleton. Endocr Rev 2002, 23(3):279-302.
50. Syed F.A., Modder U.I., Roforth M., Hensen I., Fraser D.G., Peterson J.M., et al. Effects of chronic estrogen treatment on modulating age-related bone loss in female mice. JBone Min Res 2010, 25(11):2438-2446.