Evaluating bone quality in patients with chronic kidney disease

Nature Reviews Nephrology

Volumn 9, Issue 11, 2013, Pages 671-680

  Malluche, Hartmut H ^a   Porter, Daniel S ^b   Pienkowski, David ^b  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL MARKER; COLLAGEN;

BACKSCATTER ELECTRON IMAGING; BIOMECHANICS; BONE BIOPSY; BONE DENSITY; BONE MINERALIZATION; BONE STRUCTURE; BONE TURNOVER; CHRONIC KIDNEY DISEASE; COMPUTER ASSISTED TOMOGRAPHY; CROSS LINKING; CRYSTAL STRUCTURE; DUAL ENERGY X RAY ABSORPTIOMETRY; ECHOGRAPHY; ELECTRON MICROSCOPY; ENERGY DISPERSIVE X RAY SPECTROSCOPY; FRACTURE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; ILIAC CREST; IMAGING; INFRARED SPECTROSCOPY; MECHANICAL STRESS; MICRO-COMPUTED TOMOGRAPHY; MICROFRACTURE; MORPHOMETRICS; NANOANALYSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAMAN SPECTROMETRY; RENAL OSTEODYSTROPHY; REVIEW; ROENTGEN SPECTROSCOPY; SCANNING ELECTRON MICROSCOPY; STRESS STRAIN RELATIONSHIP; THREE DIMENSIONAL IMAGING; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

BONE AND BONES; BONE DISEASES, METABOLIC; HUMANS; RENAL INSUFFICIENCY, CHRONIC;

EID: 84890788918     PISSN: 17595061     EISSN: 1759507X     Source Type: Journal    
DOI: 10.1038/nrneph.2013.198     Document Type: Review

References (76)

1. Bouxsein, M. L. Bone quality: Where do we go from here? Osteoporos. Int. 14 (Suppl. 5), S118-S127 (2003).
2. Felsenberg, D. & Boonen, S. The bone quality framework: Determinants of bone strength and their interrelationships, and implications for osteoporosis management. Clin. Ther. 27, 1-11 (2005).
3. Chesnut, C. H. 3rd & Rosen, C. J. Reconsidering the effects of antiresorptive therapies in reducing osteoporotic fracture. J. Bone Miner. Res. 16, 2163-2172 (2001).
4. Watts, N. B. Bone quality: Getting closer to a definition. J. Bone Miner. Res. 17, 1148-1150 (2002).
5. Malluche, H. H. et al. Bone histology in incipient and advanced renal failure. Kidney Int. 9, 355-362 (1976).
6. Malluche, H. H., Werner, E. & Ritz, E. Intestinal absorption of calcium and whole-body calcium retention in incipient and advanced renal failure. Min. Elec. Metab. 4, 263-270 (1978).
7. Moe, S. M. et al. KDIGO clinical practice guideline for the diagnosis, evaluation, prevention, and treatment of chronic kidney disease-mineral and bone disorder (CKD-MBD). Kidney Int. 76, S1-S130 (2009).
8. Hruska, K. A. & Teitelbaum, S. L. Renal osteodystrophy. N. Engl. J. Med. 333, 166-174 (1995).
9. Malluche, H & Faugere, M. Atlas of Mineralized Bone Histology (Karger, 1986).
10. Sherrard, D. J. et al. The spectrum of bone disease in end-stage renal failure - an evolving disorder. Kidney Int. 43, 436-442 (1993).
11. Wesseling-Perry, K. et al. Early skeletal and biochemical alterations in pediatric chronic kidney disease. Clin. J. Am. Soc. Nephrol. 7, 146-152 (2012).
12. Malluche, H. H., Mawad, H. W. & Monier-Faugere, M. C. Renal osteodystrophy in the first decade of the new millennium: Analysis of 630 bone biopsies in black and white patients. J. Bone Miner. Res. 26, 1368-1376 (2011).
13. Malluche, H. H. & Monier-Faugere, M. C. Renal osteodystrophy: What's in a name? Presentation of a clinically useful new model to interpret bone histologic findings. Clin. Nephrol. 65, 235-242 (2006).
14. Ensrud, K. E. et al. Renal function and risk of hip and vertebral fractures in older women. Arch. Intern. Med. 167, 133-139 (2007).
15. Alem, A. M. et al. Increased risk of hip fracture among patients with end-stage renal disease. Kidney Int. 58, 396-399 (2000).
16. Stone, K. L. et al. BMD at multiple sites and risk of fracture of multiple types: Long-term results from the Study of Osteoporotic Fractures. J. Bone Miner. Res. 18, 1947-1954 (2003).
17. Schuit, S. C. et al. Fracture incidence and association with bone mineral density in elderly men and women: The Rotterdam Study. Bone 34, 195-202 (2004).
18. Wainwright, S., Biggs, W., Currey, J & Gosline, J. Mechanical Design in Organisms (Halsted Press, 1976).
19. Pienkowski, D. et al. Calcitonin alters bone quality in beagle dogs. J. Bone Miner. Res. 12, 1936-1943 (1997).
20. Sabin, M. A., Blake, G. M., MacLaughlin-Black, S. M. & Fogelman, I. The accuracy of volumetric bone density measurements in dual X ray absorptiometry. Calcif. Tissue Int. 56, 210-214 (1995).
21. Yenchek, R. H. et al. Bone mineral density and fracture risk in older individuals with CKD. Clin. J. Am. Soc. Nephrol. 7, 1130-1136 (2012).
22. Adragao, T. et al. Low bone volume - a risk factor for coronary calcifications in hemodialysis patients. Clin. J. Am. Soc. Nephrol. 4, 450-455 (2009).
23. Marshall, D., Johnell, O. & Wedel, H. Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ 312, 1254-1259 (1996).
24. Malluche, H. H., Porter, D. S., Monier-Faugere, M. C., Mawad, H. & Pienkowski, D. Differences in bone quality in low-and high-turnover renal osteodystrophy. J. Am. Soc. Nephrol. 23, 525-532 (2012).
25. Gourion-Arsiquaud, S., West, P. A. & Boskey, A. L. Fourier transform-infrared microspectroscopy and microscopic imaging. Methods Mol. Biol. 455, 293-303 (2008).
26. Paschalis, E. P., Betts, F., DiCarlo, E., Mendelsohn, R. & Boskey, A. L. FTIR microspectroscopic analysis of human iliac crest biopsies from untreated osteoporotic bone. Calcif. Tissue Int. 61, 487-492 (1997).
27. Paschalis, E. P. et al. FTIR microspectroscopic analysis of human osteonal bone. Calcif. Tissue Int. 59, 480-487 (1996).
28. Paschalis, E. P. et al. Spectroscopic characterization of collagen cross-links in bone. J. Bone Miner. Res. 16, 1821-1828(2001).
29. Goodyear, S. R. & Aspden, R. M. Raman microscopy of bone. Methods Mol. Biol. 816, 527-534 (2012).
30. 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 20, 485-490 (1997).
31. Mitome, J. et al. Nonenzymatic cross-linking pentosidine increase in bone collagen and are associated with disorders of bone mineralization in dialysis patients. Calcif. Tissue Int. 88, 521-529 (2011).
32. Pothuaud, L. et al. Fractal dimension of trabecular bone projection texture is related to three-dimensional microarchitecture. J. Bone Miner. Res. 15, 691-699 (2000).
33. Nickolas, T. L. et al. Bone mass and microarchitecture in CKD patients with fracture. J. Am. Soc. Nephrol. 21, 1371-1380 (2010).
34. Macneil, J. A. & Boyd, S. K. Bone strength at the distal radius can be estimated from high-resolution peripheral quantitative computed tomography and the finite element method. Bone 42, 1203-1213 (2008).
35. Dall'Ara, E., Pahr, D., Varga, P., Kainberger, F. & Zysset, P. QCT-based finite element models predict human vertebral strength in vitro significantly better than simulated DEXA. Osteoporos. Int. 23, 563-572 (2012).
36. Chappard, C., Marchadier, A. & Benhamou, L. Interindividual and intraspecimen variability of 3 D bone microarchitectural parameters in iliac crest biopsies imaged by conventional micro-computed tomography. J. Bone Miner. Metab. 26, 506-513 (2008).
37. D'Elia, G., Caracchini, G., Cavalli, L. & Innocenti, P. Bone fragility and imaging techniques. Clin. Cases Miner. Bone Metab. 6, 234-246 (2009).
38. Nemec, S. F. et al. High-resolution magnetic resonance imaging and conventional magnetic resonance imaging on a standard field-strength magnetic resonance system compared to arthroscopy in patients with suspected meniscal tears. Acad. Radiol. 15, 928-933 (2008).
39. Link, T. M. et al. High-resolution MRI vs multislice spiral CT: Which technique depicts the trabecular bone structure best? Eur. Radiol. 13, 663-671 (2003).
40. Bhagat, Y. A. et al. Performance of muMRI-based virtual bone biopsy for structural and mechanical analysis at the distal tibia at 7T field strength. J. Magn. Reson. Imaging 33, 372-381 (2011).
41. Wu, Y. et al. Bone mineral imaged in vivo by 31P solid state MRI of human wrists. J. Magn. Reson. Imaging 34, 623-633 (2011).
42. Robson, M. D., Gatehouse, P. D., Bydder, G. M. & Neubauer, S. Human imaging of phosphorus in cortical and trabecular bone in vivo. Magn. Reson. Med. 51, 888-892 (2004).
43. Techawiboonwong, A., Song, H. K., Leonard, M. B. & Wehrli, F. W. Cortical bone water: In vivo quantification with ultrashort echo-time MR imaging. Radiology 248, 824-833 (2008).
44. K/DOQI clinical practice guidelines for chronic kidney disease: Evaluation, classification, and stratification. Am. J. Kidney Dis. 39, S1-S266 (2002).
45. Carvalho, A. B. et al. Vertebral bone density by quantitative computed tomography mirrors bone structure histomorphometric parameters in hemodialysis patients. J. Bone Miner. Metab. http://dx.doi.org/10.1007/s00774-013-0442-0.
46. Tamminen, I. S. et al. Reproducibility and agreement of micro-CT and histomorphometry in human trabecular bone with different metabolic status. J. Bone Miner. Metab. 29, 442-448 (2011).
47. Cohen, A. et al. Assessment of trabecular and cortical architecture and mechanical competence of bone by high-resolution peripheral computed tomography: Comparison with transiliac bone biopsy. Osteoporos. Int. 21, 263-273 (2010).
48. Hong, S. I., Hong, S. K. & Kohn, D. H. Nanostructural analysis of trabecular bone. J. Mater. Sci. Mater. Med. 20, 1419-1426 (2009).
49. Dong, X. N., Almer, J. D. & Wang, X. Post-yield nanomechanics of human cortical bone in compression using synchrotron X ray scattering techniques. J. Biomech. 44, 676-682 (2011).
50. Giri, B., Almer, J. D., Dong, X. N. & Wang, X. In situ mechanical behavior of mineral crystals in human cortical bone under compressive load using synchrotron X ray scattering techniques. J. Mech. Behav. Biomed. Mater. 14, 101-112 (2012).
51. Almer, J. D. & Stock, S. R. Internal strains and stresses measured in cortical bone via high-energy X ray diffraction. J. Struct. Biol. 152, 14-27 (2005).
52. Boyce, T. M., Fyhrie, D. P., Glotkowski, M. C., Radin, E. L. & Schaffler, M. B. Damage type and strain mode associations in human compact bone bending fatigue. J. Orthop. Res. 16, 322-329 (1998).
53. Burr, D. B. & Hooser, M. Alterations to the en bloc basic fuchsin staining protocol for the demonstration of microdamage produced in vivo. Bone 17, 431-433 (1995).
54. Karim, L. & Vashishth, D. Role of trabecular microarchitecture in the formation, accumulation, and morphology of microdamage in human cancellous bone. J. Orthop. Res. 29, 1739-1744 (2011).
55. Wang, L., Shao, J., Ye, T., Deng, L. & Qiu, S. Three-dimensional morphology of microdamage in peri-screw bone: A scanning electron microscopy of methylmethacrylate cast replica. Microsc. Microanal. 18, 1106-1111 (2012).
56. Schaffler, M. B., Pitchford, W. C., Choi, K. & Riddle, J. M. Examination of compact bone microdamage using back-scattered electron microscopy. Bone 15, 483-488 (1994).
57. Larrue, A., Rattner, A., Laroche, N., Vico, L. & Peyrin, F. Feasibility of micro-crack detection in human trabecular bone images from 3D synchrotron microtomography. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2007, 3918-3921 (2007).
58. Diez-Perez, A. et al. Microindentation for in vivo measurement of bone tissue mechanical properties in humans. J. Bone Miner. Res. 25, 1877-1885 (2010).
59. Oliver, W. C. & Pharr, G. M. An improved technique for determining hardness and elastic modulus using load displacement sensing indentation experiments. J. Mater. Res. 7, 1564-1583 (1992).
60. Roy, M. E., Rho, J. Y., Tsui, T. Y., Evans, N. D. & Pharr, G. M. Mechanical and morphological variation of the human lumbar vertebral cortical and trabecular bone. J. Biomed. Mater. Res. 44, 191-197 (1999).
61. Isaksson, H. et al. Infrared spectroscopy indicates altered bone turnover and remodeling activity in renal osteodystrophy. J. Bone Miner. Res. 25, 1360-1366 (2010).
62. Paschalis, E. P. et al. Bone fragility and collagen cross-links. J. Bone Miner. Res. 19, 2000-2004 (2004).
63. Malluche, H., Porter, D. S., Faugere, M. & Pienkowski, D. Low-energy fractures without low BMD t scores of osteoporosis: A possible bone matrix disorder. J. Bone Joint Surg. Am. (in press).
64. Trombetti, A. et al. Alterations of bone microstructure and strength in end-stage renal failure. Osteoporos. Int. 24, 1721-1732 (2012).
65. Negri, A. L. et al. Evaluation of bone microarchitecture by high-resolution peripheral quantitative computed tomography (HR-pQCT) in hemodialysis patients. Osteoporos. Int. 23, 2543-2550 (2012).
66. Bacchetta, J. et al. Early impairment of trabecular microarchitecture assessed with HR pQCT in patients with stage II-IV chronic kidney disease. J. Bone Miner. Res. 25, 849-857 (2010).
67. Bell, G. H., Dunbar, O., Beck, J. S. & Gibb, A. Variations in strength of vertebrae with age and their relation to osteoporosis. Calcif. Tissue Res. 1, 75-86 (1967).
68. Arici, M. et al. Bone mineral density in haemodialysis patients: A comparative study of dual-energy X ray absorptiometry and quantitative ultrasound. Nephrol. Dial. Transplant. 15, 1847-1851 (2000).
69. Foldes, A. J., Arnon, E. & Popovtzer, M. M. Reduced speed of sound in tibial bone of haemodialysed patients: Association with serum PTH level. Nephrol. Dial. Transplant. 11, 1318-1321 (1996).
70. Grabe, D. W., Chan, M. & Eisele, G. Open-label pilot study comparing quantitative ultrasound and dual-energy X ray absorptiometry to assess corticosteroid-induced osteoporosis in patients with chronic kidney disease. Clin. Ther. 28, 255-263 (2006).
71. Wehrli, F. W., Leonard, M. B., Saha, P. K. & Gomberg, B. R. Quantitative high-resolution magnetic resonance imaging reveals structural implications of renal osteodystrophy on trabecular and cortical bone. J. Magn. Reson. Imaging 20, 83-89 (2004).
72. Zioupos, P. & Currey, J. D. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone 22, 57-66 (1998).
73. Norman, T. L. & Wang, Z. Microdamage of human cortical bone: Incidence and morphology in long bones. Bone 20, 375-379 (1997).
74. Nickolas, T. L. et al. Discriminants of prevalent fractures in chronic kidney disease. J. Am. Soc. Nephrol. 22, 1560-1572 (2011).
75. Cejka, D. et al. Bone microarchitecture in hemodialysis patients assessed by HR pQCT. Clin. J. Am. Soc. Nephrol. 6, 2264-2271 (2011).
76. Jamal, S., Cheung, A. M., West, S. & Lok, C. Bone mineral density by DXA and HR pQCT can discriminate fracture status in men and women with stages 3 to 5 chronic kidney disease. Osteoporos. Int. 23, 2805-2813 (2012).