Trabecular reorganization in consecutive iliac crest biopsies when switching from bisphosphonate to strontium ranelate treatment

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Jobke, Björn ^a,b   Burghardt, Andrew J ^a   Muche, Burkhard ^c   Hahn, Michael ^d   Semler, Jutta ^c   Amling, Michael ^d   Majumdar, Sharmila ^a   Busse, Björn ^d,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HELIOS KLINIKUM BERLIN BUCH   (Germany)

^c Immanuel Hospital Berlin Wannsee   (Germany)

^d UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE BONE ISOENZYME; BIOLOGICAL MARKER; BISPHOSPHONIC ACID DERIVATIVE; CARBOXY TERMINAL TELOPEPTIDE; STRONTIUM RANELATE; BONE DENSITY CONSERVATION AGENT; ORGANOMETALLIC COMPOUND; THIOPHENE DERIVATIVE;

AGED; ARTICLE; BONE CHARACTERISTICS AND FUNCTIONS; BONE DENSITY; BONE MARROW BIOPSY; BONE MINERALIZATION; BONE STRUCTURE; BONE TURNOVER; BONE VOLUME; CANCELLOUS BONE; CASE REPORT; CONNECTIVITY DENSITY; CONTROLLED STUDY; DRUG MECHANISM; DRUG SUBSTITUTION; DRUG WITHDRAWAL; DUAL ENERGY X RAY ABSORPTIOMETRY; FEMALE; FEMUR NECK; HISTOLOGY; HUMAN; HUMAN TISSUE; ILIAC CREST; LONG TERM CARE; MICRO-COMPUTED TOMOGRAPHY; OSSIFICATION; OSTEOCLAST; OSTEOID; OSTEOLYSIS; OSTEOMETRY; OSTEOPOROSIS; TRABECULAR BONE; TRABECULAR NUMBER; TRABECULAR THICKNESS; X RAY MICROANALYSIS; BIOPSY; BONE; DRUG EFFECT; ILIAC BONE; METABOLISM; PATHOLOGY; PHOTON ABSORPTIOMETRY; POSTMENOPAUSE OSTEOPOROSIS; SPINE FRACTURE; TIME; TREATMENT OUTCOME;

ABSORPTIOMETRY, PHOTON; AGED; BIOPSY; BONE AND BONES; BONE DENSITY; BONE DENSITY CONSERVATION AGENTS; DIPHOSPHONATES; FEMALE; HUMANS; ILIUM; ORGANOMETALLIC COMPOUNDS; OSTEOPOROSIS, POSTMENOPAUSAL; SPINAL FRACTURES; THIOPHENES; TIME FACTORS; TREATMENT OUTCOME; X-RAY MICROTOMOGRAPHY;

EID: 80051683284     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0023638     Document Type: Article

References (73)

1. Torgerson DJ, Bell-Syer SE, (2001) Hormone replacement therapy and prevention of nonvertebral fractures: a meta-analysis of randomized trials. JAMA 285: 2891-2897.
2. Bilezikian JP, (2009) Efficacy of bisphosphonates in reducing fracture risk in postmenopausal osteoporosis. Am J Med 122: S14-21.
3. Ensrud KE, Stock JL, Barrett-Connor E, Grady D, Mosca L, et al. (2008) Effects of raloxifene on fracture risk in postmenopausal women: the Raloxifene Use for the Heart Trial. J Bone Miner Res 23: 112-120.
4. Rachner TD, Khosla S, Hofbauer LC, (2011) Osteoporosis: now and the future. Lancet 377: 1276-1287.
5. Neer RM, Arnaud CD, Zanchetta JR, Prince R, Gaich GA, et al. (2001) Effect of parathyroid hormone (1-34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N Engl J Med 344: 1434-1441.
6. Jobke B, Muche B, Burghardt A, Semler J, Link T, et al. (2011) Teriparatide in Bisphosphonate-Resistant Osteoporosis: Microarchitectural Changes and Clinical Results After 6 and 18 months. Calcified Tissue International pp. 1-10.
7. Meunier PJ, Roux C, Ortolani S, Diaz-Curiel M, Compston J, et al. (2009) Effects of long-term strontium ranelate treatment on vertebral fracture risk in postmenopausal women with osteoporosis. Osteoporos Int 20: 1663-1673.
8. Meunier PJ, Roux C, Seeman E, Ortolani S, Badurski JE, et al. (2004) The effects of strontium ranelate on the risk of vertebral fracture in women with postmenopausal osteoporosis. N Engl J Med 350: 459-468.
9. Reginster JY, Felsenberg D, Boonen S, Diez-Perez A, Rizzoli R, et al. (2008) Effects of long-term strontium ranelate treatment on the risk of nonvertebral and vertebral fractures in postmenopausal osteoporosis: Results of a five-year, randomized, placebo-controlled trial. Arthritis Rheum 58: 1687-1695.
10. Reginster JY, Seeman E, De Vernejoul MC, Adami S, Compston J, et al. (2005) Strontium ranelate reduces the risk of nonvertebral fractures in postmenopausal women with osteoporosis: Treatment of Peripheral Osteoporosis (TROPOS) study. J Clin Endocrinol Metab 90: 2816-2822.
11. Busse B, Jobke B, Hahn M, Priemel M, Niecke M, et al. (2010) Effects of strontium ranelate administration on bisphosphonate-altered hydroxyapatite: Matrix incorporation of strontium is accompanied by changes in mineralization and microstructure. Acta Biomater 6: 4513-4521.
12. Blake GM, Fogelman I, (2007) Effect of bone strontium on BMD measurements. J Clin Densitom 10: 34-38.
13. Liao J, Blake GM, McGregor AH, Patel R, (2010) The effect of bone strontium on BMD is different for different manufacturers' DXA Systems. Bone 47: 882-887.
14. Nielsen SP, Slosman D, Sorensen OH, Basse-Cathalinat B, De Cassin P, et al. (1999) Influence of strontium on bone mineral density and bone mineral content measurements by dual X-ray absorptiometry. J Clin Densitom 2: 371-379.
15. Boivin G, Farlay D, Khebbab MT, Jaurand X, Delmas PD, et al. (2010) In osteoporotic women treated with strontium ranelate, strontium is located in bone formed during treatment with a maintained degree of mineralization. Osteoporos Int 21: 667-677.
16. Li C, Paris O, Siegel S, Roschger P, Paschalis EP, et al. (2010) Strontium is incorporated into mineral crystals only in newly formed bone during strontium ranelate treatment. J Bone Miner Res 25: 968-975.
17. Middleton ET, Steel SA, Aye M, Doherty SM, (2010) The effect of prior bisphosphonate therapy on the subsequent BMD and bone turnover response to strontium ranelate. J Bone Miner Res 25: 455-462.
18. Marx RE, Cillo JE Jr, Ulloa JJ, (2007) Oral bisphosphonate-induced osteonecrosis: risk factors, prediction of risk using serum CTX testing, prevention, and treatment. J Oral Maxillofac Surg 65: 2397-2410.
19. Gomez B Jr, Ardakani S, Ju J, Jenkins D, Cerelli MJ, et al. (1995) Monoclonal antibody assay for measuring bone-specific alkaline phosphatase activity in serum. Clin Chem 41: 1560-1566.
20. DVO (2011) Guideline 2009 for Prevention, Diagnosis and Therapy of Osteoporosis in Adults Osteologie 20: 55-74.
21. Frost HM, (1983) The regional acceleratory phenomenon: a review. Henry Ford Hosp Med J 31: 3-9.
22. Burghardt AJ, Kazakia GJ, Laib A, Majumdar S, (2008) Quantitative assessment of bone tissue mineralization with polychromatic micro-computed tomography. Calcif Tissue Int 83: 129-138.
23. Burghardt AJ, Kazakia GJ, Majumdar S, (2007) A local adaptive threshold strategy for high resolution peripheral quantitative computed tomography of trabecular bone. Ann Biomed Eng 35: 1678-1686.
24. Patel V, Issever AS, Burghardt A, Laib A, Ries M, et al. (2003) MicroCT evaluation of normal and osteoarthritic bone structure in human knee specimens. J Orthop Res 21: 6-13.
25. Odgaard A, Gundersen HJ, (1993) Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 14: 173-182.
26. Doube M, Klosowski MM, Arganda-Carreras I, Cordelières FP, Dougherty RP, et al. (2010) BoneJ: Free and extensible bone image analysis in ImageJ. Bone 47: 1076-1079.
27. Hildebrand T, Rüegsegger P, (1997) Quantification of Bone Microarchitecture with the Structure Model Index. Computer Methods in Biomechanics and Biomedical Engineering 1: 15-23.
28. Hahn M, Vogel M, Pompesius-Kempa M, Delling G, (1992) Trabecular bone pattern factor-a new parameter for simple quantification of bone microarchitecture. Bone 13: 327-330.
29. Thomsen JS, Laib A, Koller B, Prohaska S, Mosekilde L, et al. (2005) Stereological measures of trabecular bone structure: comparison of 3D micro computed tomography with 2D histological sections in human proximal tibial bone biopsies. J Microsc 218: 171-179.
30. Mulder L, Koolstra JH, Van Eijden TM, (2004) Accuracy of microCT in the quantitative determination of the degree and distribution of mineralization in developing bone. Acta Radiol 45: 769-777.
31. Parfitt AM, (1988) Bone histomorphometry: proposed system for standardization of nomenclature, symbols, and units. Calcif Tissue Int 42: 284-286.
32. Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, et al. (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 2: 595-610.
33. Iki M, Akiba T, Matsumoto T, Nishino H, Kagamimori S, et al. (2004) Reference database of biochemical markers of bone turnover for the Japanese female population. Japanese Population-based Osteoporosis (JPOS) Study. Osteoporos Int 15: 981-991.
34. Zikan V, Stepan JJ, (2009) Marked reduction of bone turnover by alendronate attenuates the acute response of bone resorption marker to endogenous parathyroid hormone. Bone 44: 634-638.
35. Sebba AI, Bonnick SL, Kagan R, Thompson DE, Skalky CS, et al. (2004) Response to therapy with once-weekly alendronate 70 mg compared to once-weekly risedronate 35 mg in the treatment of postmenopausal osteoporosis. Current Medical Research and Opinion 20: 2031-2041.
36. Schafer A, Vittinghoff E, Ramachandran R, Mahmoudi N, Bauer D, (2010) Laboratory reproducibility of biochemical markers of bone turnover in clinical practice. Osteoporosis International 21: 439-445.
37. Garnero P, Darte C, Delmas PD, (1999) A model to monitor the efficacy of alendronate treatment in women with osteoporosis using a biochemical marker of bone turnover. Bone 24: 603-609.
38. Garnero P, Borel O, Delmas PD, (2001) Evaluation of a Fully Automated Serum Assay for C-Terminal Cross-Linking Telopeptide of Type I Collagen in Osteoporosis. Clin Chem 47: 694-702.
39. Watts NB, Jenkins DK, Visor JM, Casal DC, Geusens P, (2001) Comparison of Bone and Total Alkaline Phosphatase and Bone Mineral Density in Postmenopausal Osteoporotic Women Treated with Alendronate. Osteoporosis International 12: 279-288.
40. Dos Reis LM, Batalha JR, Muñoz DR, Borelli A, Correa PHS, et al. (2007) Brazilian normal static bone histomorphometry: effects of age, sex, and race. Journal of Bone and Mineral Metabolism 25: 400-406.
41. Vedi S, Compston JE, Webb A, Tighe JR, (1982) Histomorphometric analysis of bone biopsies from the iliac crest of normal British subjects. Metabolic Bone Disease and Related Research 4: 231-236.
42. Schnitzler CM, Pettifor JM, Mesquita JM, Bird MDT, Schnaid E, et al. (1990) Histomorphometry of iliac crest bone in 346 normal black and white South African adults. Bone and Mineral 10: 183-199.
43. Chavassieux PM, Arlot ME, Reda C, Wei L, Yates AJ, et al. (1997) Histomorphometric assessment of the long-term effects of alendronate on bone quality and remodeling in patients with osteoporosis. The Journal of clinical investigation 100: 1475-1480.
44. Eriksen EF, Melsen F, Sod E, Barton I, Chines A, (2002) Effects of long-term risedronate on bone quality and bone turnover in women with postmenopausal osteoporosis. Bone 31: 620-625.
45. Jobke B, (2006) Bisphosphonat-Therapie bei Osteoporosepatienten: Veränderung der dreidimensionalen Spongiosastruktur und Entwicklung des endostalen Umbaus [Dissertation]: University Medical Center Hamburg-Eppendorf.
46. Hahn M, Vogel M, Delling G, (1991) Undecalcified preparation of bone tissue: report of technical experience and development of new methods. Virchows Arch A Pathol Anat Histopathol 418: 1-7.
47. Bromage TG, Goldman HM, McFarlin SC, Warshaw J, Boyde A, et al. (2003) Circularly polarized light standards for investigations of collagen fiber orientation in bone. Anat Rec B New Anat 274: 157-168.
48. Busse B, Hahn M, Soltau M, Zustin J, Puschel K, et al. (2009) Increased calcium content and inhomogeneity of mineralization render bone toughness in osteoporosis: mineralization, morphology and biomechanics of human single trabeculae. Bone 45: 1034-1043.
49. Roschger P, Fratzl P, Eschberger J, Klaushofer K, (1998) Validation of quantitative backscattered electron imaging for the measurement of mineral density distribution in human bone biopsies. Bone 23: 319-326.
50. Roschger P, Paschalis EP, Fratzl P, Klaushofer K, (2008) Bone mineralization density distribution in health and disease. Bone 42: 456-466.
51. Skedros JG, Bloebaum RD, Bachus KN, Boyce TM, Constantz B, (1993) Influence of mineral content and composition on graylevels in backscattered electron images of bone. J Biomed Mater Res 27: 57-64.
52. Bjeoumikhov A, Arkadiev V, Eggert F, Hodoroaba VD, Langhoff N, et al. (2005) A new microfocus x-ray source, iMOXS, for highly sensitive XRF analysis in scanning electron microscopes. X-Ray Spectrometry 34: 493-497.
53. Seitz S, Schnabel C, Busse B, Schmidt HU, Beil FT, et al. (2010) High bone turnover and accumulation of osteoid in patients with neurofibromatosis 1. Osteoporos Int 21: 119-127.
54. Glorieux FH, Travers R, Taylor A, Bowen JR, Rauch F, et al. (2000) Normative data for iliac bone histomorphometry in growing children. Bone 26: 103-109.
55. Won YY, Chung YS, Park YK, Yoo VY, (2003) Correlations between microcomputed tomography and bone histomorphometry in Korean young females. Yonsei Med J 44: 811-815.
56. Stauber M, Muller R, (2006) Volumetric spatial decomposition of trabecular bone into rods and plates-a new method for local bone morphometry. Bone 38: 475-484.
57. Busse B, Hahn M, Schinke T, Puschel K, Duda GN, et al. (2010) Reorganization of the femoral cortex due to age-, sex-, and endoprosthetic-related effects emphasized by osteonal dimensions and remodeling. J Biomed Mater Res A 92: 1440-1451.
58. Eriksen EF, Eghbali-Fatourechi GZ, Khosla S, (2007) Remodeling and vascular spaces in bone. J Bone Miner Res 22: 1-6.
59. Doube M, Kłosowski MM, Wiktorowicz-Conroy AM, Hutchinson JR, Shefelbine SJ, (2011) Trabecular bone scales allometrically in mammals and birds. Proceedings of the Royal Society B: Biological Sciences.
60. Busse B, Djonic D, Milovanovic P, Hahn M, Puschel K, et al. (2010) Decrease in the osteocyte lacunar density accompanied by hypermineralized lacunar occlusion reveals failure and delay of remodeling in aged human bone. Aging Cell 9: 1065-1075.
61. Kufahl RH, Saha S, (1990) A theoretical model for stress-generated fluid flow in the canaliculi-lacunae network in bone tissue. J Biomech 23: 171-180.
62. Ding M, Hvid I, (2000) Quantification of age-related changes in the structure model type and trabecular thickness of human tibial cancellous bone. Bone 26: 291-295.
63. Laib A, Kumer JL, Majumdar S, Lane NE, (2001) The Temporal Changes of Trabecular Architecture in Ovariectomized Rats Assessed by MicroCT. Osteoporosis International 12: 936-941.
64. Liu XS, Sajda P, Saha PK, Wehrli FW, Guo XE, (2006) Quantification of the Roles of Trabecular Microarchitecture and Trabecular Type in Determining the Elastic Modulus of Human Trabecular Bone. Journal of Bone and Mineral Research 21: 1608-1617.
65. Ma YL, Zeng Q, Donley DW, Ste-Marie LG, Gallagher JC, et al. (2006) Teriparatide increases bone formation in modeling and remodeling osteons and enhances IGF-II immunoreactivity in postmenopausal women with osteoporosis. J Bone Miner Res 21: 855-864.
66. Jee WS, Tian XY, Setterberg RB, (2007) Cancellous bone minimodeling-based formation: a Frost, Takahashi legacy. J Musculoskelet Neuronal Interact 7: 232-239.
67. Amling M, Grote HJ, Vogel M, Hahn M, Delling G, (1994) Three-dimensional analysis of the spine in autopsy cases with renal osteodystrophy. Kidney Int 46: 733-743.
68. Woods CG, Bishop MC, Nicholson GD, (1972) Bone histological changes occurring after haemodialysis treatment for chronic renal failure. J Pathol 107: 137-143.
69. Sato K, Byers PD, (1981) Quantitative study of tunneling and hook resorption in metabolic bone disease. Calcif Tissue Int 33: 459-466.
70. Blake GM, Fogelman I, (2005) Long-term effect of strontium ranelate treatment on BMD. J Bone Miner Res 20: 1901-1904.
71. Amling M, Herden S, Pösl M, Hahn M, Ritzel H, et al. (1996) Heterogeneity of the skeleton: Comparison of the trabecular microarchitecture of the spine, the iliac crest, the femur, and the calcaneus. Journal of Bone and Mineral Research 11: 36-45.
72. Hauge EM, Mosekilde L, Melsen F, Frydenberg M, (2001) How many patients are needed? Variation and design considerations in bone histomorphometry. Bone 28: 556-562.
73. Lips P, (2001) Vitamin D Deficiency and Secondary Hyperparathyroidism in the Elderly: Consequences for Bone Loss and Fractures and Therapeutic Implications. Endocrine Reviews 22: 477-501.