Changes in intracortical microporosities induced by pharmaceutical treatment of osteoporosis as detected by high resolution micro-CT

Bone

Volumn 50, Issue 3, 2012, Pages 596-604

  Tommasini, Steven M ^a   Trinward, Andrea ^a   Acerbo, Alvin S ^a,b   de Carlo, Francesco ^c   Miller, Lisa M ^b   Judex, Stefan ^a  

^a St Francis Hospital The Heart Center   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

^c ARGONNE NATIONAL LABORATORY   (United States)

Author keywords

Alendronate; Cortical bone porosity; Osteocyte lacunae; OVX; PTH; Synchrotron micro CT

Indexed keywords

ALENDRONIC ACID; BISPHOSPHONIC ACID DERIVATIVE; PARATHYROID HORMONE[1-34];

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MASS; BONE TURNOVER; CONTROLLED STUDY; CORTICAL BONE; DRUG EFFICACY; DRUG SAFETY; FEMALE; HIGH RESOLUTION COMPUTER TOMOGRAPHY; MORPHOLOGY; NONHUMAN; OSTEOCYTE; OSTEOLYSIS; OSTEOPOROSIS; OVARIECTOMY; POROSITY; RAT; SIGNAL NOISE RATIO; SYNCHROTRON; TREATMENT RESPONSE;

ALENDRONATE; ANIMALS; BONE AND BONES; BONE DENSITY; BONE DENSITY CONSERVATION AGENTS; FEMALE; OSTEOPOROSIS; OVARIECTOMY; PARATHYROID HORMONE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84856971580     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2011.12.012     Document Type: Article

References (65)

1. Agarwal S., Gupta P., Agarwal P.K., Agarwal G., Bansal A. Risk of atypical femoral fracture with long-term use of alendronate (bisphosphonates): a systemic review of literature. Acta Orthop Belg 2010, 76(5):567-571.
2. Mosekilde L., Thomsen J.S., Mackey M.S., Phipps R.J. Treatment with risedronate or alendronate prevents hind-limb immobilization-induced loss of bone density and strength in adult female rats. Bone 2000, 27(5):639-645.
3. Hodsman A.B., Hanley D.A., Ettinger M.P., Bolognese M.A., Fox J., Metcalfe A.J., Lindsay R. Efficacy and safety of human parathyroid hormone-(1-84) in increasing bone mineral density in postmenopausal osteoporosis. J Clin Endocrinol Metab 2003, 88(11):5212-5220.
4. Judex S., Boyd S., Qin Y.X., Turner S., Ye K., Muller R., Rubin C. Adaptations of trabecular bone to low magnitude vibrations result in more uniform stress and strain under load. Ann Biomed Eng 2003, 31(1):12-20.
5. Ciarelli M.J., Goldstein S.A., Kuhn J.L., Cody D.D., Brown M.B. Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography. J Orthop Res 1991, 9(5):674-682.
6. Jepsen K.J., Akkus O.J., Majeska R.J., Nadeau J.H. Hierarchical relationship between bone traits and mechanical properties in inbred mice. Mamm Genome 2003, 14(2):97-104.
7. Kogianni G., Noble B.S. The biology of osteocytes. Curr Osteoporos Rep 2007, 5(2):81-86.
8. Bonewald L.F. Osteocytes as dynamic multifunctional cells. Ann N Y Acad Sci 2007, 1116:281-290.
9. Bonewald L.F. Osteocyte messages from a bony tomb. Cell Metab 2007, 5(6):410-411.
10. Bonewald L.F. Mechanosensation and transduction in osteocytes. Bonekey Osteovision 2006, 3(10):7-15.
11. Seeman E. Osteocytes-martyrs for integrity of bone strength. Osteoporos Int 2006, 17(10):1443-1448.
12. Skerry T.M. The response of bone to mechanical loading and disuse: fundamental principles and influences on osteoblast/osteocyte homeostasis. Arch Biochem Biophys 2008, 473(2):117-123.
13. Qing H., Bonewald L.F. Osteocyte remodeling of the perilacunar and pericanalicular matrix. Int J Oral Sci 2009, 1(2):59-65.
14. Rubin C., Judex S., Hadjiargyrou M. Skeletal adaptation to mechanical stimuli in the absence of formation or resorption of bone. J Musculoskelet Neuronal Interact 2002, 2(3):264-267.
15. Li X., Ominsky M.S., Niu Q.T., Sun N., Daugherty B., D'Agostin D., Kurahara C., Gao Y., Cao J., Gong J., Asuncion F., Barrero M., Warmington K., Dwyer D., Stolina M., Morony S., Sarosi I., Kostenuik P.J., Lacey D.L., Simonet W.S., Ke H.Z., Paszty C. Targeted deletion of the sclerostin gene in mice results in increased bone formation and bone strength. J Bone Miner Res 2008, 23(6):860-869.
16. Li X., Ominsky M.S., Warmington K.S., Morony S., Gong J., Cao J., Gao Y., Shalhoub V., Tipton B., Haldankar R., Chen Q., Winters A., Boone T., Geng Z., Niu Q.T., Ke H.Z., Kostenuik P.J., Simonet W.S., Lacey D.L., Paszty C. Sclerostin antibody treatment increases bone formation, bone mass, and bone strength in a rat model of postmenopausal osteoporosis. J Bone Miner Res 2009, 24(4):578-588.
17. Teti A., Zallone A. Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone 2009, 44(1):11-16.
18. Lane N.E., Yao W., Balooch M., Nalla R.K., Balooch G., Habelitz S., Kinney J.H., Bonewald L.F. Glucocorticoid-treated mice have localized changes in trabecular bone material properties and osteocyte lacunar size that are not observed in placebo-treated or estrogen-deficient mice. J Bone Miner Res 2006, 21(3):466-476.
19. Cullinane D.M. The role of osteocytes in bone regulation: mineral homeostasis versus mechanoreception. J Musculoskelet Neuronal Interact 2002, 2(3):242-244.
20. Parfitt A.M. The cellular basis of bone turnover and bone loss: a rebuttal of the osteocytic resorption-bone flow theory. Clin Orthop Relat Res 1977, 127:236-247.
21. Schneider P., Meier M., Wepf R., Muller R. Towards quantitative 3D imaging of the osteocyte lacuno-canalicular network. Bone 2010, 47(5):848-858.
22. Hannah K.M., Thomas C.D., Clement J.G., De Carlo F., Peele A.G. Bimodal distribution of osteocyte lacunar size in the human femoral cortex as revealed by micro-CT. Bone 2010, 47(5):866-871.
23. Ito M. Assessment of bone quality using micro-computed tomography (micro-CT) and synchrotron micro-CT. J Bone Miner Metab 2005, 23(Suppl):115-121.
24. Jiang Y., Zhao J., White D.L., Genant H.K. Micro CT and Micro MR imaging of 3D architecture of animal skeleton. J Musculoskelet Neuronal Interact 2000, 1(1):45-51.
25. Schneider P., Stauber M., Voide R., Stampanoni M., Donahue L.R., Muller R. Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro- and nano-CT. J Bone Miner Res 2007, 22(10):1557-1570.
26. Lombardi A. Treatment of Paget's disease of bone with alendronate. Bone 1999, 24(5 Suppl):59S-61S.
27. Rosen C.J. What's new with PTH in osteoporosis: where are we and where are we headed?. Trends Endocrinol Metab 2004, 15(5):229-233.
28. Neer R.M., Arnaud C.D., Zanchetta J.R., Prince R., Gaich G.A., Reginster J.Y., Hodsman A.B., Eriksen E.F., Ish-Shalom S., Genant H.K., Wang O., Mitlak B.H. Effect of parathyroid hormone (1-34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N Engl J Med 2001, 344(19):1434-1441.
29. Hodsman A.B., Kisiel M., Adachi J.D., Fraher L.J., Watson P.H. Histomorphometric evidence for increased bone turnover without change in cortical thickness or porosity after 2 years of cyclical hPTH(1-34) therapy in women with severe osteoporosis. Bone 2000, 27(2):311-318.
30. Riggs B.L., Hodgson S.F., O'Fallon W.M., Chao E.Y., Wahner H.W., Muhs J.M., Cedel S.L., Melton L.J. Effect of fluoride treatment on the fracture rate in postmenopausal women with osteoporosis. N Engl J Med 1990, 322(12):802-809.
31. Iida-Klein A., Zhou H., Lu S.S., Levine L.R., Ducayen-Knowles M., Dempster D.W., Nieves J., Lindsay R. Anabolic action of parathyroid hormone is skeletal site specific at the tissue and cellular levels in mice. J Bone Miner Res 2002, 17(5):808-816.
32. Fox J., Miller M.A., Newman M.K., Metcalfe A.F., Turner C.H., Recker R.R., Smith S.Y. Daily treatment of aged ovariectomized rats with human parathyroid hormone (1-84) for 12 months reverses bone loss and enhances trabecular and cortical bone strength. Calcif Tissue Int 2006, 79(4):262-272.
33. Yao W., Hadi T., Jiang Y., Lotz J., Wronski T.J., Lane N.E. Basic fibroblast growth factor improves trabecular bone connectivity and bone strength in the lumbar vertebral body of osteopenic rats. Osteoporos Int 2005, 16(12):1939-1947.
34. Sama A.A., Khan S.N., Myers E.R., Huang R.C., Cammisa F.P., Sandhu H.S., Lane J.M. High-dose alendronate uncouples osteoclast and osteoblast function: a study in a rat spine pseudarthrosis model. Clin Orthop Relat Res 2004, 425:135-142.
35. Peter C., Rodan G.A. Preclinical safety profile of alendronate. Int J Clin Pract Suppl 1999, 101:3-8.
36. Helvering L.M., Liu R., Kulkarni N.H., Wei T., Chen P., Huang S., Lawrence F., Halladay D.L., Miles R.R., Ambrose E.M., Sato M., Ma Y.L., Frolik C.A., Dow E.R., Bryant H.U., Onyia J.E. Expression profiling of rat femur revealed suppression of bone formation genes by treatment with alendronate and estrogen but not raloxifene. Mol Pharmacol 2005, 68(5):1225-1238.
37. Egermann M., Goldhahn J., Schneider E. Animal models for fracture treatment in osteoporosis. Osteoporos Int 2005, 16(S2):S129-S138.
38. Jiang Y., Zhao J., Genant H.K., Dequeker J., Geusens P. Long-term changes in bone mineral and biomechanical properties of vertebrae and femur in aging, dietary calcium restricted, and/or estrogen-deprived/-replaced rats. J Bone Miner Res 1997, 12(5):820-831.
39. Andersson N., Surve V.V., Lehto-Axtelius D., Andersson K., Ryberg B., Ohlsson C., Hakanson R. Pharmacological treatment of osteopenia induced by gastrectomy or ovariectomy in young female rats. Acta Orthop Scand 2004, 75(2):201-209.
40. Akhter M.P., Kimmel D.B., Recker R.R. Effect of parathyroid hormone (hPTH[1-84]) treatment on bone mass and strength in ovariectomized rats. J Clin Densitom 2001, 4(1):13-23.
41. Cheng Z., Yao W., Zimmermann E.A., Busse C., Ritchie R.O., Lane N.E. Prolonged treatments with antiresorptive agents and PTH have different effects on bone strength and the degree of mineralization in old estrogen-deficient osteoporotic rats. J Bone Miner Res 2009, 24(2):209-220.
42. Lane N.E., Haupt D., Kimmel D.B., Modin G., Kinney J.H. Early estrogen replacement therapy reverses the rapid loss of trabecular bone volume and prevents further deterioration of connectivity in the rat. J Bone Miner Res 1999, 14(2):206-214.
43. Jiang Y., Zhao J., Genant H.K., Dequeker J., Geusens P. Bone mineral density and biomechanical properties of spine and femur of ovariectomized rats treated with naproxen. Bone 1998, 22(5):509-514.
44. Andersson N., Surve V.V., Lehto-Axtelius D., Ohlsson C., Hakanson R., Andersson K., Ryberg B. Drug-induced prevention of gastrectomy- and ovariectomy-induced osteopaenia in the young female rat. J Endocrinol 2002, 175(3):695-703.
45. Ito M., Nishida A., Koga A., Ikeda S., Shiraishi A., Uetani M., Hayashi K., Nakamura T. Contribution of trabecular and cortical components to the mechanical properties of bone and their regulating parameters. Bone 2002, 31(3):351-358.
46. 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.
47. Jepsen K.J., Pennington D.E., Lee Y.L., Warman M., Nadeau J. Bone brittleness varies with genetic background in A/J and C57BL/6J inbred mice. J Bone Miner Res 2001, 16(10):1854-1862.
48. Tommasini S.M., Nasser P., Hu B., Jepsen K.J. Biological co-adaptation of morphological and composition traits contributes to mechanical functionality and skeletal fragility. J Bone Miner Res 2008, 23(2):236-246.
49. Donnelly E. Methods for assessing bone quality: a review. Clin Orthop Relat Res 2011, 469(8):2128-2138.
50. Lublinsky S., Ozcivici E., Judex S. An automated algorithm to detect the trabecular-cortical bone interface in micro-computed tomographic images. Calcif Tissue Int 2007, 81(4):285-293.
51. Otsu N. A threshold selection method from gray-level histograms. IEEE T Syst Man Cyb 1979, 9(1):62.
52. Alcobendas M., Baud C.A., Castanet J. Structural changes of the periosteocytic area in Vipera aspis (L.) (Ophidia, Viperidae) bone tissue in various physiological conditions. Calcif Tissue Int 1991, 49(1):53-57.
53. Nakano Y., Toyosawa S., Takano Y. Eccentric localization of osteocytes expressing enzymatic activities, protein, and mRNA signals for type 5 tartrate-resistant acid phosphatase (TRAP). J Histochem Cytochem 2004, 52(11):1475-1482.
54. Baylink D.J., Wergedal J.E. Bone formation by osteocytes. Am J Physiol 1971, 221(3):669-678.
55. Herman B.C., Cardoso L., Majeska R.J., Jepsen K.J., Schaffler M.B. Activation of bone remodeling after fatigue: differential response to linear microcracks and diffuse damage. Bone 2010, 47(4):766-772.
56. Cardoso L., Herman B.C., Verborgt O., Laudier D., Majeska R.J., Schaffler M.B. Osteocyte apoptosis controls activation of intracortical resorption in response to bone fatigue. J Bone Miner Res 2009, 24(4):597-605.
57. Fritton S.P., Weinbaum S. Fluid and solute transport in bone: flow-induced mechanotransduction. Annu Rev Fluid Mech 2009, 41:347-374.
58. Nicolella D.P., Feng J.Q., Moravits D.E., Bonivitch A.R., Wang Y., Dusecich V., Yao W., Lane N., Bonewald L.F. Effects of nanomechanical bone tissue properties on bone tissue strain: implications for osteocyte mechanotransduction. J Musculoskelet Neuronal Interact 2008, 8(4):330-331.
59. Nicolella D.P., Moravits D.E., Gale A.M., Bonewald L.F., Lankford J. Osteocyte lacunae tissue strain in cortical bone. J Biomech 2006, 39(9):1735-1743.
60. Andrews J.C., Almeida E., van der Meulen M.C., Alwood J.S., Lee C., Liu Y., Chen J., Meirer F., Feser M., Gelb J., Rudati J., Tkachuk A., Yun W., Pianetta P. Nanoscale X-ray microscopic imaging of mammalian mineralized tissue. Microsc Microanal 2010, 16(3):327-336.
61. Sissons H.A., Kelman G.J., Marotti G. Mechanisms of bone resorption in calcium-deficient rats. Calcif Tissue Int 1984, 36(6):711-721.
62. Boyde A. Scanning electron microscope studies of bone. The biochemistry and physiology of bone 1972, 259-310. Academic Press, New York and London. G.H. Bourne (Ed.).
63. Borah B., Dufresne T., Nurre J., Phipps R., Chmielewski P., Wagner L., Lundy M., Bouxsein M., Zebaze R., Seeman E. Risedronate reduces intracortical porosity in women with osteoporosis. J Bone Miner Res 2010, 25(1):41-47.
64. Donnelly E., Chen D.X., Boskey A.L., Baker S.P., van der Meulen M.C. Contribution of mineral to bone structural behavior and tissue mechanical properties. Calcif Tissue Int 2010, 87(5):450-460.
65. 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(8):1193-1205.