Glucocorticosteroid-induced osteoporosis in adult primiparous Göttingen miniature pigs: Effects on bone mineral and mineral metabolism

American Journal of Physiology - Endocrinology and Metabolism

Volumn 293, Issue 1, 2007, Pages

  Scholz Ahrens, K E ^a   Delling, G ^b   Stampa, B ^c,f   Helfenstein, A ^d   Hahne, H J ^d   Acil Y ^e   Timm, W ^c   Barkmann, R ^c   Hassenpflug, J ^d   Schrezenmeir, J ^a   Gluer C C ^c  

^a FEDERAL RESEARCH INSTITUTE OF NUTRITION AND FOOD   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c Department of Diagnostic Radiology

^d UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^e UNIVERSITY OF KIEL   (Germany)

^f Synarc Inc   (Germany)

Author keywords

Bone marker; Bone mechanical property; Bone mineral density; Calcium balance; Histomorphometry

Indexed keywords

CALCIFEDIOL; CALCITRIOL; CALCIUM; PARATHYROID HORMONE; PREDNISOLONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOMECHANICS; BONE DEVELOPMENT; BONE MINERAL; BONE STRENGTH; CALCIUM ABSORPTION; CONTROLLED STUDY; CORTICOSTEROID INDUCED OSTEOPOROSIS; CROSS-SECTIONAL STUDY; DOSE RESPONSE; DRUG EFFECT; DRUG TOLERABILITY; FEMALE; HORMONE BLOOD LEVEL; IN VIVO STUDY; LONG TERM CARE; MINERAL METABOLISM; MINIPIG; NONHUMAN; OSTEOBLAST; OUTCOME ASSESSMENT; PRIORITY JOURNAL; STATISTICAL ANALYSIS; TRABECULAR BONE; TREATMENT DURATION;

ANIMALS; BODY WEIGHT; BONE AND BONES; BONE DENSITY; CALCIUM; COMPRESSIVE STRENGTH; DISEASE MODELS, ANIMAL; FEMALE; GLUCOCORTICOIDS; MINERALS; OSTEOPOROSIS; PARITY; PHOSPHORUS; PREGNANCY; SWINE; TIME FACTORS;

EID: 34547105542     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00627.2006     Document Type: Article

References (69)

1. Açil Y, Müller PK. Rapid method for the isolation of the mature collagen cross-links, hydroxylysylpyridinoline and lysylpyridinoline. J Chromatogr A 664: 183-188, 1994.
2. Adachi JD. Corticosteroid-induced osteoporosis. Int J Fertil Womens Med 46: 190-205, 2001.
3. Al-Dossari GA, Kshettry VR, Jessurun J, Bolman III TM. Experimental large-animal model of obliterative bronchiolitis after lung transplantation. Ann Thorac Surg 58: 34-40, 1994.
4. Boass A, Lovdal JA, Toverud SU. Pregnanacy-induced and lactation-induced changes in active intestinal calcium transport in rats. Am J Physiol Gastrointest Liver Physiol 263: G127-G134, 1992.
5. Böhm K, Cordes M, Forster T, Krah K. Gesundheit, Krankheitskosten 2002 (Online). p9. Statistisches Bundesamt Wiesbaden 2004. http://www.destatis.de/presse/deutsch/pk/2004/krankheitskosten_2002i and http://www.destatis.de/print_e.php.
6. Bonadonna S, Burattin A, Nuzzo M, Bugari G, Rosei EA, Valle D, Iori N, Bilezikian JP, Veldhuis JD, Giustina A. Chronic glucocorticoid treatment alters spontaneous pulsatile parathyroid hormone secretory dynamics in human subjects. Eur J Endocrinol 152: 199-205, 2005.
7. Buchman AL. Side effects of corticosteroid therapy. J Clin Gastroenterol 33: 289-294, 2001.
8. Canalis E, Giustina A. Glucocorticoid-induced osteoporosis: summary of a workshop. J Clin Endocrinol Metab 86: 5681-5685, 2001.
9. Chavassieux P, Buffet A, Vergnaud P, Garnero P, Meunier PJ. Short-term effects of corticosteroids on trabecular bone remodeling in old ewes. Bone 20: 451-455, 1997.
10. Claassen H, Cellarius C, Scholz-Ahrens KE, Schrezenmeir J, Glüer CC, Schünke M, Kurz B. Extracellular matrix changes in knee joint cartilage following bone-active drug treatment. Cell Tissue Res 324: 279-289, 2006.
11. Deloffre P, Hans D, Rumelhart C, Mitton D, Tsouderos Y, Meunier PJ. Comparison between bone density and bone strength in glucocorticoid-treated aged ewes. Bone 17: 409S-414S, 1995.
12. Devogelaer JP, Goemaere S, Boonen S, Body JJ, Kaufman JM, Reginster JY, Rozenberg S, Boutsen Y. Evidence-based guidelines for the prevention and treatment of glucocorticoid-induced osteoporosis: a consensus document of the Belgian Bone Club. Osteoporos Int 17: 8-19, 2006.
13. Ebeling PR, Erbas B, Hopper JL, Wark JD, Rubinfeld AR. Bone mineral density and bone turnover in asthmatics treated with long-term inhaled or oral glucocorticoids. J Bone Miner Res 13: 1283-1289, 1998.
14. Gennari C, Gonnelli S, Bruni D, Gennari L, Brandi ML. PTH in the pathogenesis and treatment of glucocorticoid-induced osteoporosis. Front Horm Res 30: 184-197, 2002.
15. Glüer CC, Blake G, Lu Y, Blunt BA, Jergas M, Genant HK. Accurate assessment of precision errors: How to measure the reproducibility of bone densitometry techniques. Osteoporosis Int 5: 262-270, 1995.
16. Glüer CC, Scholz-Ahrens KE, Helfenstein A, Delling G, Timm W, Açil Y, Barkmann R, Hassenpflug J, Stampa B, Hahne Bauss F, Schrezenmeir J. Ibandronate treatment reverses glucocorticoid-induced loss of bone mineral density and strength in minipigs. Bone 40: 645-655, 2007.
17. Gram J, Junker P, Nielsen HK, Bollerslev J. Effects of short-term treatment with prednisolone and 1,25-dihydroxyvitamin D3 on bone and mineral metabolism in normal men. Bone 23: 297-302, 1998.
18. Hahn TJ, Halstead LR, Teitelbaum SL, Hahn BH. Altered mineral metabolism in glucocorticoid-induced osteopenia. Effect of 25-hydroxyvitamin D administration. J Clin Invest 64: 655-665, 1979.
19. Harrison HE, Harrison HC. Transfer of Ca45 across intestinal wall in vitro in relation to action of vitamin D and cortisol. Am J Physiol 199: 265-271, 1960.
20. Heitland W, Bäumler W. Vögel und Säuger-Ein kleines Nachschlagwerk zum Kurs "84 Bestimmungsübungen an Vögeln und Säugern." (Online). http://www.faunistik.net/BSWT/MAMMALIA/ UNGULATA/SUIDAE/SUS/sus.scrofa_01.html [2003].
21. Hodsman AB, Toogood JH, Jennings B, Fraher LJ, Baskerville JC. Differential effects of inhaled budesonide and oral prednisolone on serum osteocalcin. J Clin Endocrinol Metab 72: 530-540, 1991.
22. Holick MF. Stay tuned to PXR: an orphan actor that may not be D-structive only to bone. J Clin Invest 115: 32-34, 2005.
23. Ikeda S, Morishita Y, Tsutsumi H, Ito M, Shiraishi A, Arita S, Akahoshi S, Narusawa K, Nakamura T. Reductions in bone turnover, mineral, and structure associated with mechanical properties of lumbar vertebra and femur in glucocorticoid-treated growing minipigs. Bone 33: 779-787, 2003.
24. Kaiser H, Kley HK. Cortisontherapie. Stuttgart, Germany: Georg Thieme Verlag, 1997.
25. Kalender WA, Klotz E, Süss C. Vertebral bone mineral analysis: an integrated approach. Radiology 164: 419-423, 1987.
26. Kapadia RD, Stroup GB, Badger AM, Koller B, Levin JM, Coatney RW, Dodds RA, Liang X, Lark MW, Gowen M. Applications of micro-CT and MR microscopy to study pre-clinical models of osteoporosis and osteoarthritis. Technol Health Care 6: 361-372, 1998.
27. Karpman RR. Musculoskeletal disease in the United States: who provides the care? Clin Orthop Relat Res 385: 52-56, 2001.
28. King CS, Weir EC, Gundberg CW, Fox J, Insogna KL. Effects of continuous glucocorticoid infusion on bone metabolism in the rat. Calcif Tissue Int 59: 184-191, 1996.
29. Kirwan JR. The effect of glucocorticoids on joint destruction in rheumatoid arthritis. The Arthritis and Rheumatism Council Low-Dose Glucocorticoid Study Group. N Engl J Med 333: 142-146, 1995.
30. Klein RG, Arnaud SB, Gallagher JC, Deluca HF, Riggs BL. Intestinal calcium absorption in exogenous hypercortisonism. Role of 25-hydroxyvitamin D and corticosteroid dose. J Clin Invest 60: 253-259, 1977.
31. Lee GS, Choi KC, Jeung EB. Glucocorticoids differentially regulate expression of duodenal and renal calbindin-D9k through glucocorticoid receptor-mediated pathway in mouse model. Am J Physiol Endocrinol Metab 290: E299-E307, 2006.
32. Lill CA, Fluegel AK, Schneider E. Effect of ovariectomy, malnutrition and glucocorticoid application on bone properties in sheep: a pilot study. Osteoporos Int 13: 480-486, 2002.
33. Linde F, Hvid I, Madsen F. The effect of specimen geometry on the mechanical behaviour of trabecular bone specimens. J Biomech 25: 359-368, 1992.
34. Liss M. Rekonstruktion der Altersstrukturen subadulter Individuen anhand von Lang- und Beckenknochen aus dem mittelalterlichen Gräberfeld von Dresden-Briesnitz (dissertation). Jena, Germany: University of Jena, 1966.
35. Lyles KW, Jackson TW, Nesbitt T, Quarles LD. Salmon calcitonin reduces vertebral bone loss in glucocorticoid-treated beagles. Am J Physiol Endocrinol Metab 264: E938-E942, 1993.
36. Manolagas SC, Weinstein RS. New developments in the pathogenesis and treatment of steroid-induced osteoporosis. J Bone Miner Res 14: 1061-1066, 1999.
37. Meunier PJ. Bone-forming agents. In: Osteoporosis 1996, edited by Papapoulos SE, Lips P, Pols HAP, Johnston CC, and Delmas PD. Amsterdam, The Netherlands: Elsevier, 1996, p. 305-313.
38. Mosekilde L. Assessing bone quality: animal models in preclinical osteoporosis research. Bone 17, Suppl 4: 343S-352S, 1995.
39. Nielsen HK, Thomsen K, Eriksen EF, Charles P, Storm T, Mosekilde L. The effects of high-dose glucocorticoid administration on serum bone gamma carboxyglutamic acid-containing protein, serum alkaline phosphatase and vitamin D metabolites in normal subjects. Bone Miner 4: 105-113, 1988.
40. Nordin RW, Histand MB, Sheahan HJ, Carpenter TR. Effects of corticosteroids on mechanical strength of intervertebral joints and vertebrae in dogs. Clin Orthop Relat Res 259: 268-276, 1990.
41. O'Brien CA, Jia D, Plotkin LI, Bellido T, Powers CC, Stewart SA, Manolagas SC, Weinstein RS. Glucocorticoids act directly on osteoblasts and osteocytes to induce their apoptosis and reduce bone formation and strength. Endocrinology 145: 1835-1841, 2004.
42. Omdahl JL, Morris HA, May BK. Hydroxylase enzymes of the vitamin D pathway: expression, function, and regulation. Annu Rev Nutr 22: 139-166, 2002.
43. Pascussi JM, Robert A, Nguyen M, Walrant-Debray O, Garabedian M, Martin P, Pineau T, Saric J, Navarro F, Maurel P, Vilarem MJ. Possible involvement of pregnane X receptor-enhanced CYP24 expression in drug-induced osteomalacia. J Clin Invest 115: 177-186, 2005.
44. Pascussi JM, Maurel P, Vilarem MJ. Response to Zhou et al. J Clin Invest 116: 2564, 2006.
45. Pearce G, Tabensky DA, Delmas PD, Baker HW, Seeman E. Corticosteroid-induced bone loss in men. J Clin Endocrinol Metab 83: 801-806, 1998.
46. Prior JC, Vigna YM, Wark JD, Eyre DR, Lentle BC, Li DK, Ebeling PR, Atley L. Premenopausal ovariectomy-related bone loss: a randomized, double-blind, one-year trial of conjugated estrogen or medroxyprogesterone acetate. J Bone Miner Res 12: 1851-1863, 1997.
47. Prummel MF, Wiersinga WM, Lips P, Sanders GT, Sauerwein HP. The course of biochemical parameters of bone turnover during treatment with corticosteroids. J Clin Endocrinol Metab 72: 382-386, 1991.
48. Pufe T, Scholz-Ahrens KE, Franke AT, Petersen W, Mentlein R, Varoga D, Tillmann B, Schrezenmeir J, Glüer CC. The role of vascular endothelial growth factor in glucocorticoid-induced bone loss: evaluation in a minipig model. Bone 33: 869-876, 2003.
49. Quarles LD. Prednisone-induced osteopenia in beagles-variable effects mediated by differential suppression of bone-formation. Am J Physiol Endocrinol Metab 263: E136-E141, 1992.
50. Sambrook PN, Hughes DR, Nelson AE, Robinson BG, Mason RS. Osteocyte viability with glucocorticoid treatment: relation to histomorphometry. Ann Rheum Dis 62: 1215-1217, 2003.
51. Scholz-Ahrens KE, Schrezenmeir J. Effects of bioactive substances in milk on mineral and trace element metabolism with special reference to casein phosphopeptides. Br J Nutr 84, Suppl 1: S147-S153, 2000.
52. Scholz-Ahrens KE, Hagemeister H, Unshelm J, Agergaard N, Barth CA. Response of hormones modulating plasma cholesterol to dietary casein or soy protein in minipigs. J Nutr 120: 1387-1392, 1990.
53. Scholz-Ahrens KE, Delling G, Jungblut PW, Kallweit E, Barth CA. Effect of ovariectomy on bone histology and plasma parameters of bone metabolism in nulliparous and multiparous sows. Z Ernährungswiss 35: 13-21, 1996.
54. Scholz-Ahrens KE, Barth CA, Kann P, Lüttges J, Roberts H, Schrezenmeir J. Impact of dietary calcium on the effect of ovariectomy on bone density in minipigs (Abstract). Osteoporosis Int 8, Suppl 3: 101, 1998.
55. Schorlemmer S, Gohl C, Iwabu S, Ignatius A, Claes L, Augat P. Glucocorticoid treatment of ovariectomized sheep affects mineral density, structure, and mechanical properties of cancellous bone. J Bone Miner Res 18: 2010-2015, 2003.
56. Seeman E, Kumar R, Hunder GG, Scott M, Heath 3rd H, Riggs BL. Production, degradation, and circulating levels of 1,25-dihydroxyvitamin D in health and in chronic glucocorticoid excess. J Clin Invest 66: 664-669, 1980.
57. Smith BJ, Phillips PJ, Pannall PR, Cain HJ, Leckie WJ. Effect of orally administered beclomethasone dipropionate on calcium absorption from the gut in normal subjects. Thorax 48: 890-893, 1993.
58. Struijs A, Smals A, de Witte SA, Hackeng WH, Mulder H. Acute effects of etidronate on glucocorticoid-induced bone degradation. Rheumatology (Oxford) 39: 523-529, 2000.
59. Suzuki Y, Ichikawa Y, Saito E, Homma M. Importance of increased urinary calcium excretion in the development of secondary hyperparathyroidism of patients under glucocorticoid therapy. Metabolism 32: 151-156, 1983.
60. Turner CH. Fluoride and the FDA: a curious case. J Bone Miner Res 11: 1369-1371, 1996.
61. Van den Ham EC, Kooman JP, Christiaans MH, Nieman FH, van Hooff JP. Weight changes after renal transplantation: a comparison between patients on 5-mg maintenance steroid therapy and those on steroid-free immunosuppressive therapy. Transpl Int 16: 300-306, 2003.
62. Van der Veen MJ, Bijlsma JW. Effects of different regimes of corticosteroid treatment on calcium and bone metabolism in rheumatoid arthritis. Clin Rheumatol 11: 388-392, 1992.
63. Van Staa TP, Leufkens HG, Cooper C. The epidemiology of corticosteroid-induced osteoporosis: a meta-analysis. Osteoporos Int 13: 777-787, 2002.
64. Verhoeven MC, Boers MJ. Limited bone loss due to corticosteroids; A systematic review of prospective studies in rheumatoid arthritis and other diseases. J Rheumatol 24: 1495-1503, 1997.
65. Weiler HA, Wang Z, Atkonson SA. Dexamethasone treatment impairs calcium regulation and reduces bone mineralization in infant pigs. Am J Clin Nutr 61: 805-811, 1995.
66. Weinstein RS. Glucocorticoid-induced osteoporosis. Rev Endocr Metab Disord 2: 65-73, 2001.
67. Weinstein RS, Jilka RL, Parfitt AM, Manolagas SC. Inhibition of osteoblastogenesis and promotion of apoptosis of osteoblasts and osteocytes by glucocorticoids. Potential mechanisms of their deleterious effects on bone. J Clin Invest 102: 274-282, 1998.
68. Yelin E, Cisternas MG, Pasta DJ, Trupin L, Murphy L, Helmick CG. Medical care expenditures and earnings losses of persons with arthritis and other rheumatic conditions in the United States in 1997: total and incremental estimates. Arthritis Rheum 50: 2317-2326, 2004.
69. Zhou C, Assem M, Tay JC, Watkins PB, Blumberg B, Schuetz EG, Thummel KE. Steroid and xenobiotic receptor and vitamin D receptor crosstalk mediates CYP24 expression and drug-induced osteomalacia. J Clin Invest 116: 1703-1712, 2006.