Glucocorticoid-associated osteoporosis in chronic inflammatory diseases: Epidemiology, mechanisms, diagnosis, and treatment

Current Osteoporosis Reports

Volumn 12, Issue 3, 2014, Pages 289-299

  Von Scheven, Emily ^a   Corbin, Kathleen Jo ^a   Stefano, Stagi ^b   Cimaz, Rolando ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Bone density; Children; Corticosteroids; Crohn's disease; Glucocorticoids; Juvenile dermatomyositis; Juvenile idiopathic arthritis; Osteoporosis; Pediatric; Rheumatic disease; Systemic lupus erythematosus

Indexed keywords

ALENDRONIC ACID; ALKALINE PHOSPHATASE BONE ISOENZYME; BISPHOSPHONIC ACID DERIVATIVE; CALCIUM; GLUCOCORTICOID; GROWTH HORMONE; INTERLEUKIN 1; INTERLEUKIN 6; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PLACEBO; PREDNISOLONE; PREDNISONE; RECOMBINANT PARATHYROID HORMONE; RISEDRONIC ACID; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA INHIBITOR; VITAMIN D; BONE DENSITY CONSERVATION AGENT; HUMAN GROWTH HORMONE;

ASTHMA; BONE DENSITY; BONE FRAGILITY; BONE MASS; BONE METABOLISM; BONE MINERAL; BONE MINERALIZATION; BONE REMODELING; BONE STRENGTH; BONE TURNOVER; COMPUTER ASSISTED TOMOGRAPHY; CONNECTIVE TISSUE DISEASE; CORTICOSTEROID INDUCED MYOPATHY; CORTICOSTEROID INDUCED OSTEOPOROSIS; CORTICOSTEROID THERAPY; CROHN DISEASE; DOSE RESPONSE; DUAL ENERGY X RAY ABSORPTIOMETRY; FRACTURE; HUMAN; HUMERUS FRACTURE; HYPOPARATHYROIDISM; INFLAMMATORY DISEASE; JUVENILE DERMATOMYOSITIS; JUVENILE RHEUMATOID ARTHRITIS; JUVENILE SYSTEMIC SCLEROSIS; MUSCLE MASS; OSTEOCLASTOGENESIS; OSTEOGENESIS IMPERFECTA; OSTEOPENIA; OSTEOPOROSIS; PHYSICAL ACTIVITY; QUANTITATIVE COMPUTED TOMOGRAPHY; REMISSION; RESPIRATORY TRACT DISEASE; REVIEW; RHEUMATIC DISEASE; RISK ASSESSMENT; SECONDARY OSTEOPOROSIS; SPINE FRACTURE; SPONDYLOARTHROPATHY; SYSTEMIC LUPUS ERYTHEMATOSUS; SYSTEMIC SCLEROSIS; SYSTEMIC VASCULITIS; CHEMICALLY INDUCED; CHILD; CHRONIC DISEASE; FRACTURES, BONE; LUPUS ERYTHEMATOSUS, SYSTEMIC; RHEUMATIC DISEASES;

BONE DENSITY CONSERVATION AGENTS; CALCIUM; CHILD; CHRONIC DISEASE; CROHN DISEASE; FRACTURES, BONE; GLUCOCORTICOIDS; HUMAN GROWTH HORMONE; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; OSTEOPOROSIS; RHEUMATIC DISEASES; VITAMIN D;

EID: 84906311384     PISSN: 15441873     EISSN: 15442241     Source Type: Journal    
DOI: 10.1007/s11914-014-0228-x     Document Type: Review

References (117)

1. Bonjour JP, Chevalley T, Ferrari S, Rizzoli R. The importance and relevance of peak bone mass in the prevalence of osteoporosis. Salud Publica Mex. 2009;51 Suppl 1:S5-17.
2. Peitz J FO, Schoenau E. Quantifying bone disease in pediatric rheumatic patients and its problems. Rheumatol Curr Res. 2012;S2(006). doi:10.4172/2161-1149.S2-006.
3. Uziel Y, Zifman E, Hashkes PJ. Osteoporosis in children: pediatric and pediatric rheumatology perspective: a review. Pediatr Rheumatol Online J. 2009;7:16.
4. Brabnikova MK. Secondary osteoporosis in patients with juvenile idiopathic arthritis. J Osteoporos. 2011;2011:569417.
5. Epstein S, Inzerillo AM, Caminis J, Zaidi M. Disorders associated with acute rapid and severe bone loss. J Bone Min Res. 2003;18(12):2083-94. (Pubitemid 37463302)
6. Hofbauer LC, Gori F, Riggs BL, Lacey DL, Dunstan CR, Spelsberg TC, et al. Stimulation of osteoprotegerin ligand and inhibition of osteoprotegerin production by glucocorticoids in human osteoblastic lineage cells: potential paracrine mechanisms of glucocorticoid-induced osteoporosis. Endocrinology. 1999;140(10):4382-9. (Pubitemid 30666099)
7. Rubin J, Biskobing DM, Jadhav L, Fan D, Nanes MS, Perkins S, et al. Dexamethasone promotes expression of membrane-bound macrophage colony-stimulating factor in murine osteoblast-like cells. Endocrinology. 1998;139(3):1006-12. (Pubitemid 28510117)
8. Jia D, O'Brien CA, Stewart SA, Manolagas SC, Weinstein RS. Glucocorticoids act directly on osteoclasts to increase their life span and reduce bone density. Endocrinology. 2006;147(12):5592-9. (Pubitemid 44833476)
9. Dempster DW, Moonga BS, Stein LS, Horbert WR, Antakly T. Glucocorticoids inhibit bone resorption by isolated rat osteoclasts by enhancing apoptosis. J Endocrinol. 1997;154(3):397-406. (Pubitemid 27375034)
10. Weinstein RS. Clinical practice. Glucocorticoid-induced bone disease. N Engl J Med. 2011;365(1):62-70.
11. Canalis E, Mazziotti G, Giustina A, Bilezikian JP. Glucocorticoidinduced osteoporosis: pathophysiology and therapy. Osteoporos Int. 2007;18(10):1319-28.
12. O'Brien CA, Jia D, Plotkin LI, Bellido T, Powers CC, Stewart SA, et al. Glucocorticoids act directly on osteoblasts and osteocytes to induce their apoptosis and reduce bone formation and strength. Endocrinology. 2004;145(4):1835-41. (Pubitemid 38402392)
13. 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. 1998;102(2):274-82. (Pubitemid 28335186)
14. Tsampalieros A, Gupta P, Denburg MR, Shults J, Zemel BS, Mostoufi-Moab S, et al. Glucocorticoid effects on changes in bone mineral density and cortical structure in childhood nephrotic syndrome. J Bone Min Res. 2013;28(3):480-8.
15. Burnham JM. Inflammatory diseases and bone health in children. Curr Op Rheumatol. 2012;24(5):548-53.
16. Leonard MB. Glucocorticoid-induced osteoporosis in children: impact of the underlying disease. Pediatrics. 2007;119 Suppl 2:S166-74. (Pubitemid 46397939)
17. Hanaoka BY, Peterson CA, Horbinski C, Crofford LJ. Implications of glucocorticoid therapy in idiopathic inflammatory myopathies. Nature Rev Rheumatol. 2012;8(8):448-57.
18. Akki A, Yang H, Gupta A, Chacko VP, Yano T, Leppo MK, et al. Skeletal muscle ATP kinetics are impaired in frail mice. Age (Dordr). 2014;36(1):21-30.
19. Cimaz R. Osteoporosis in childhood rheumatic diseases: prevention and therapy. Best Pract Res Rheumatol. 2002;16(3):397-409.
20. van Staa TP, Leufkens HG, Cooper C. The epidemiology of corticosteroid-induced osteoporosis: a meta-analysis. Osteoporos Int. 2002;13(10):777-87. (Pubitemid 36336722)
21. De Vries F, Bracke M, Leufkens HG, Lammers JW, Cooper C, Van Staa TP. Fracture risk with intermittent high-dose oral glucocorticoid therapy. Arthritis Rheumatism. 2007;56(1):208-14. (Pubitemid 46106193)
22. van Staa TP, Leufkens HG, Abenhaim L, Zhang B, Cooper C. Oral corticosteroids and fracture risk: relationship to daily and cumulative doses. Rheumatology. 2000;39(12):1383-9. (Pubitemid 32045866)
23. Compston J. Management of glucocorticoid-induced osteoporosis. Nature Rev Rheumatol. 2010;6(2):82-8.
24. van Staa TP, Cooper C, Leufkens HG, Bishop N. Children and the risk of fractures caused by oral corticosteroids. J Bone Min Res. 2003;18(5):913-8. (Pubitemid 37294976)
25. •• Takayanagi H. New developments in osteoimmunology. Nature Rev Rheumatol. 2012;8(11):684-9. Osteoimmunology studies the relationship between bone and immune cells. Many recent developments have been achieved, and this reviwew nicely summarizes modern discoveries in the field.
26. Rabinovich CE. Bone mineral status in juvenile rheumatoid arthritis. J Rheumatol Suppl. 2000;58:34-7. (Pubitemid 30340292)
27. McInnes IB, Schett G. Cytokines in the pathogenesis of rheumatoid arthritis. Nat Rev Immunol. 2007;7(6):429-42. (Pubitemid 46834849)
28. Varonos S, Ansell BM, Reeve J. Vertebral collapse in juvenile chronic arthritis: its relationship with glucocorticoid therapy. Calcif Tissue Int. 1987;41(2):75-8.
29. Long AR, Rouster-Stevens KA. The role of exercise therapy in the management of juvenile idiopathic arthritis. Curr Op Rheumatol. 2010;22(2):213-7.
30. Malleson PN, Bennett SM, MacKinnon M, Jespersen DK, Coutts KD, Turner SP, et al. Physical fitness and its relationship to other indices of health status in children with chronic arthritis. J Rheumatol. 1996;23(6):1059-65. (Pubitemid 26196099)
31. Stagi S, Giani T, Simonini G, Falcini F. Thyroid function, autoimmune thyroiditis and coeliac disease in juvenile idiopathic arthritis. Rheumatology. 2005;44(4):517-20. (Pubitemid 41511144)
32. Lurati A, Cimaz R, Gattinara M, Gerloni V, Teruzzi B, Salmaso A, et al. [Skeletal mineralization in a prepubertal female population affected by juvenile idiopathic arthritis]. Reumatismo. 2008;60(3):224-9.
33. Nisar MK, Masood F, Cookson P, Sansome A, Ostor AJ. What do we know about juvenile idiopathic arthritis and vitamin D? A systematic literature review andmeta-analysis of current evidence. Clin Rheumatol. 2013;32(6):729-34.
34. Ringold S, Wallace CA, Rivara FP. Health-related quality of life, physical function, fatigue, and disease activity in children with established polyarticular juvenile idiopathic arthritis. J Rheumatol. 2009;36(6):1330-6.
35. Schoenau E. From mechanostat theory to development of the "Functional Muscle-Bone-Unit". J Musculoskelet Neuronal Interact. 2005;5(3):232-8. (Pubitemid 41684172)
36. Felin EM, Prahalad S, Askew EW, Moyer-Mileur LJ. Musculoskeletal abnormalities of the tibia in juvenile rheumatoid arthritis. Arthritis Rheumatism. 2007;56(3):984-94. (Pubitemid 46399447)
37. Roth J, Palm C, Scheunemann I, Ranke MB, Schweizer R, Dannecker GE. Musculoskeletal abnormalities of the forearm in patients with juvenile idiopathic arthritis relate mainly to bone geometry. Arthritis Rheumatism. 2004;50(4):1277-85. (Pubitemid 38480839)
38. Burnham JM, Shults J, Dubner SE, Sembhi H, Zemel BS, Leonard MB. Bone density, structure, and strength in juvenile idiopathic arthritis: importance of disease severity and muscle deficits. Arthritis Rheumatism. 2008;58(8):2518-27.
39. • Brabnikova Maresova K, Jarosova K, Pavelka K, Stepan JJ. The association between lean mass and bone mineral content in the high disease activity group of adult patients with juvenile idiopathic arthritis. BMC Musculoskelet Disord. 2014;15(1):51. Very recent paper emphasizing the importance of lean mass on bone density.
40. Alsufyani KA, Ortiz-Alvarez O, Cabral DA, Tucker LB, Petty RE, Nadel H, et al. Bone mineral density in children and adolescents with systemic lupus erythematosus, juvenile dermatomyositis, and systemic vasculitis: relationship to disease duration, cumulative corticosteroid dose, calciumintake, and exercise. J Rheumatology. 2005;32(4):729-33. (Pubitemid 40524708)
41. Casella CB, Seguro LP, Takayama L, Medeiros D, Bonfa E, Pereira RM. Juvenile onset systemic lupus erythematosus: a possible role for vitamin D in disease status and bone health. Lupus. 2012;21(12):1335-42.
42. Compeyrot-Lacassagne S, Tyrrell PN, Atenafu E, Doria AS, Stephens D, Gilday D, et al. Prevalence and etiology of low bone mineral density in juvenile systemic lupus erythematosus. Arthritis Rheumatism. 2007;56(6):1966-73. (Pubitemid 47110395)
43. Regio P, Bonfa E, Takayama L, Pereira R. The influence of lean mass in trabecular and cortical bone in juvenile onset systemic lupus erythematosus. Lupus. 2008;17(9):787-92.
44. Stagi S, Cavalli L, Bertini F, Matucci Cerinic M, Luisa Brandi M, Falcini F. Cross-sectional and longitudinal evaluation of bone mass and quality in children and young adults with juvenile onset systemic lupus erythematosus (JSLE): role of bone mass determinants analyzed by DXA, PQCT and QUS. Lupus. 2014;23(1):57-68.
45. Trapani S, Civinini R, Ermini M, Paci E, Falcini F. Osteoporosis in juvenile systemic lupus erythematosus: a longitudinal study on the effect of steroids on bone mineral density. Rheumatol Int. 1998;18(2):45-9. (Pubitemid 28432833)
46. Santiago RA, Silva CA, Caparbo VF, Sallum AM, Pereira RM. Bone mineral apparent density in juvenile dermatomyositis: the role of lean body mass and glucocorticoid use. Scand J Rheumatol. 2008;37(1):40-7.
47. • Rodd C, Lang B, Ramsay T, Alos N, Huber AM, Cabral DA, et al. Incident vertebral fractures among children with rheumatic disorders 12 months after glucocorticoid initiation: a national observational study. Arthritis Care Res. 2012;64(1):122-31. This article reports on a nice study on vertebral fractures, the most feared complication while on glucocorticoids, on a nationwide basis.
48. Rouster-Stevens KA, Langman CB, Price HE, Seshadri R, Shore RM, Abbott K, et al. RANKL: osteoprotegerin ratio and bone mineral density in children with untreated juvenile dermatomyositis. Arthritis Rheumatism. 2007;56(3):977-83. (Pubitemid 46399446)
49. Omori CH, Silva CA, Sallum AM, Rodrigues Pereira RM, Luciade Sa Pinto A, Roschel H, et al. Exercise training in juvenile dermatomyositis. Arthritis Care Res. 2012;64(8):1186-94.
50. La Torre F, Martini G, Russo R, Katsicas MM, Corona F, Calcagno G, et al. A preliminary disease severity score for juvenile systemic sclerosis. Arthritis Rheumatism. 2012;64(12):4143-50.
51. Shinjo SK, Bonfa E, de Falco Caparbo V, Pereira RM. Low bone mass in juvenile onset sclerosis systemic: the possible role for 25-hydroxyvitamin D insufficiency. Rheumatol Int. 2011;31(8): 1075-80.
52. Souza RB, Borges CT, Takayama L, Aldrighi JM, Pereira RM. Systemic sclerosis and bone loss: the role of the disease and body composition. Scand J Rheumatol. 2006;35(5):384-7. (Pubitemid 44601073)
53. Frediani B, Baldi F, Falsetti P, Acciai C, Filippou G, Spreafico A, et al. Clinical determinants of bone mass and bone ultrasonometry in patients with systemic sclerosis. Clin Exp Rheumatol. 2004;22(3):313-8. (Pubitemid 38585234)
54. Sampaio-Barros PD, Costa-Paiva L, Filardi S, Sachetto Z, Samara AM, Marques-Neto JF. Prognostic factors of low bone mineral density in systemic sclerosis. Clin Exp Rheumatol. 2005;23(2):180-4. (Pubitemid 40662997)
55. Sylvester FA, Wyzga N, Hyams JS, Davis PM, Lerer T, Vance K, et al. Natural history of bonemetabolismand bone mineral density in children with inflammatory bowel disease. Inflamm Bowel Dis. 2007;13(1):42-50. (Pubitemid 46080008)
56. Podolsky DK. Inflammatory bowel disease. N Engl J Med. 2002;347(6):417-29. (Pubitemid 34851835)
57. Redlich K, Smolen JS. Inflammatory bone loss: pathogenesis and therapeutic intervention. Nature Rev Drug Discov. 2012;11(3):234-50.
58. Hyams JS, Wyzga N, Kreutzer DL, Justinich CJ, Gronowicz GA. Alterations in bone metabolism in children with inflammatory bowel disease: an in vitro study. J Pediat Gastroenterol Nutrit. 1997;24(3):289-95. (Pubitemid 27199618)
59. Sylvester FA, Wyzga N, Hyams JS, Gronowicz GA. Effect of Crohn's disease on bonemetabolismin vitro: a role for interleukin-6. J Bone Min Res. 2002;17(4):695-702. (Pubitemid 34246645)
60. Varghese S, Wyzga N, Griffiths AM, Sylvester FA. Effects of serum from children with newly diagnosed Crohn disease on primary cultures of rat osteoblasts. J Pediat Gastroenterol Nutrit. 2002;35(5):641-8. (Pubitemid 35417735)
61. Fewtrell MS, British P, Adolescent BG. Bone densitometry in children assessed by dual x ray absorptiometry: uses and pitfalls. Arch Dis Child. 2003;88(9):795-8. (Pubitemid 37094235)
62. Pappa H, Thayu M, Sylvester F, Leonard M, Zemel B, Gordon C. Skeletal health of children and adolescents with inflammatory bowel disease. J Pediat Gastroenterol Nutrit. 2011;53(1):11-25.
63. •• Zemel BS, Kalkwarf HJ, Gilsanz V, Lappe JM, Oberfield S, Shepherd JA, et al. Revised reference curves for bone mineral content and areal bone mineral density according to age and sex for Black and non-Black children: results of the bone mineral density in childhood study. J Clin Endocrinol Metab. 2011;96(10):3160-9. In pediatrics normative values are essential in order to perform studies and interpret data. For bone density this is particularly important, this article details reference curves according to age and sex in different ethnic groups.
64. •• Crabtree NJ, Arabi A, Bachrach LK, Fewtrell M, El-Hajj Fuleihan G, Kecskemethy HH, et al. Dual-energy X-Ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD Pediatric Official Positions. J Clin Densitom. 2014;17(2):225-42. An essential statement paper related to pediatrics from the International Society that deals with densitometric studies.
65. Bishop N, Arundel P, Clark E, Dimitri P, Farr J, Jones G, et al. Fracture prediction and the definition of osteoporosis in children and adolescents: the ISCD2013 Pediatric Official Positions. J Clin Densitom. 2014;17(2):275-80.
66. Zemel BS, Leonard MB, Kelly A, Lappe JM, Gilsanz V, Oberfield S, et al. Height adjustment in assessing dual energy x-ray absorptiometry measurements of bone mass and density in children. J Clin Endocrinol Metab. 2010;95(3):1265-73.
67. Zemel BS. Quantitative computed tomography and computed tomography in children. Curr Osteoporos Rep. 2011;9(4):284-90.
68. Dubner SE, Shults J, Baldassano RN, Zemel BS, Thayu M, Burnham JM, et al. Longitudinal assessment of bone density and structure in an incident cohort of children with Crohn's disease. Gastroenterology. 2009;136(1):123-30.
69. Tsampalieros A, Kalkwarf HJ, Wetzsteon RJ, Shults J, Zemel BS, Foster BJ, et al. Changes in bone structure and the muscle-bone unit in children with chronic kidney disease. Kidney Int. 2013;83(3):495-502.
70. Adams JE, Engelke K, Zemel BS, Ward KA. Quantitative computer tomography in children and adolescents: the 2013 ISCD Pediatric Official Positions. J Clin Densitom. 2014;17(2):258-74.
71. Lien G, Flato B, Haugen M, Vinje O, Sorskaar D, Dale K, et al. Frequency of osteopenia in adolescents with early-onset juvenile idiopathic arthritis: a long-term outcome study of one hundred five patients. Arthritis Rheumatism. 2003;48(8):2214-23. (Pubitemid 36959202)
72. Pepmueller PH, Cassidy JT, Allen SH, Hillman LS. Bone mineralization and bone mineral metabolism in children with juvenile rheumatoid arthritis. Arthritis Rheumatism. 1996;39(5):746-57. (Pubitemid 26140419)
73. Stagi S, Masi L, Capannini S, Cimaz R, Tonini G, Matucci-Cerinic M, et al. Cross-sectional and longitudinal evaluation of bone mass in children and young adults with juvenile idiopathic arthritis: the role of bone mass determinants in a large cohort of patients. J Rheumatol. 2010;37(9):1935-43.
74. Reed AM, Haugen M, Pachman LM, Langman CB. Repair of osteopenia in children with juvenile rheumatoid arthritis. J Pediatr. 1993;122(5 Pt 1):693-6. (Pubitemid 23134951)
75. Burnham JM, Shults J, Weinstein R, Lewis JD, Leonard MB. Childhood onset arthritis is associated with an increased risk of fracture: a population based study using the General Practice Research Database. Ann Rheum Dis. 2006;65(8):1074-9. (Pubitemid 44133272)
76. Valta H, Lahdenne P, Jalanko H, Aalto K, Makitie O. Bone health and growth in glucocorticoid-treated patients with juvenile idiopathic arthritis. J Rheumatol. 2007;34(4):831-6. (Pubitemid 46641393)
77. Nakhla M, Scuccimarri R, Duffy KN, Chedeville G, Campillo S, Duffy CM, et al. Prevalence of vertebral fractures in children with chronic rheumatic diseases at risk for osteopenia. J Pediatr. 2009;154(3):438-43.
78. Huber AM, Gaboury I, Cabral DA, Lang B, Ni A, Stephure D, et al. Prevalent vertebral fractures among children initiating glucocorticoid therapy for the treatment of rheumatic disorders. Arthritis Care Res. 2010;62(4):516-26.
79. Cassidy JT, Hillman LS. Abnormalities in skeletal growth in children with juvenile rheumatoid arthritis. Rheum Dis Clin North Am. 1997;23(3):499-522. (Pubitemid 27397118)
80. Falcini F, Trapani S, Civinini R, Capone A, Ermini M, Bartolozzi G. The primary role of steroids on the osteoporosis in juvenile rheumatoid patients evaluated by dual energy X-ray absorptiometry. J Endocrinol Invest. 1996;19(3):165-9. (Pubitemid 26162609)
81. Lin YT, Wang CT, Gershwin ME, Chiang BL. The pathogenesis of oligoarticular/polyarticular vs systemic juvenile idiopathic arthritis. Autoimmun Rev. 2011;10(8):482-9.
82. Henderson CJ, Specker BL, Sierra RI, Campaigne BN, Lovell DJ. Total-body bone mineral content in non-corticosteroid-treated postpubertal females with juvenile rheumatoid arthritis: frequency of osteopenia and contributing factors. Arthritis Rheumatism. 2000;43(3):531-40. (Pubitemid 30394943)
83. Stewart WA, Acott PD, Salisbury SR, Lang BA. Bone mineral density in juvenile dermatomyositis: assessment using dual x-ray absorptiometry. Arthritis Rheumatism. 2003;48(8):2294-8. (Pubitemid 36959211)
84. Gokhale R, Favus MJ, Karrison T, Sutton MM, Rich B, Kirschner BS. Bone mineral density assessment in children with inflammatory bowel disease. Gastroenterology. 1998;114(5):902-11. (Pubitemid 28217555)
85. Jahnsen J, Falch JA, Aadland E, Mowinckel P. Bone mineral density is reduced in patients with Crohn's disease but not in patients with ulcerative colitis: a population based study. Gut. 1997;40(3):313-9. (Pubitemid 27145642)
86. Boot AM, Bouquet J, Krenning EP, de Muinck Keizer-Schrama SM. Bone mineral density and nutritional status in children with chronic inflammatory bowel disease. Gut. 1998;42(2):188-94. (Pubitemid 28214002)
87. Thayu M, Denson LA, Shults J, Zemel BS, Burnham JM, Baldassano RN, et al. Determinants of changes in linear growth and body composition in incident pediatric Crohn's disease. Gastroenterology. 2010;139(2):430-8.
88. Burnham JM, Shults J, Semeao E, Foster B, Zemel BS, Stallings VA, et al. Whole body BMC in pediatric Crohn disease: independent effects of altered growth, maturation, and body composition. J Bone Min Res. 2004;19(12):1961-8. (Pubitemid 41103410)
89. Cowan FJ, Warner JT, Dunstan FD, Evans WD, Gregory JW, Jenkins HR. Inflammatory bowel disease and predisposition to osteopenia. Arch Dis Child. 1997;76(4):325-9. (Pubitemid 27174542)
90. Bernstein CN, Blanchard JF, Leslie W, Wajda A, Yu BN. The incidence of fracture among patients with inflammatory bowel disease. A population-based cohort study. Ann Intern Med. 2000;133(10):795-9.
91. Semeao EJ, Stallings VA, Peck SN, Piccoli DA. Vertebral compression fractures in pediatric patients with Crohn's disease. Gastroenterology. 1997;112(5):1710-3. (Pubitemid 27181398)
92. Lamb EJ, Wong T, Smith DJ, Simpson DE, Coakley AJ, Moniz C, et al. Metabolic bone disease is present at diagnosis in patients with inflammatory bowel disease. Aliment Pharmacol Ther. 2002;16(11):1895-902. (Pubitemid 35253005)
93. Pigot F, Roux C, Chaussade S, Hardelin D, Pelleter O, Du Puy Montbrun T, et al. Low bone mineral density in patients with inflammatory bowel disease. Dig Dis Sci. 1992;37(9):1396-403.
94. Ward LM, Rauch F, Matzinger MA, Benchimol EI, Boland M, Mack DR. Iliac bone histomorphometry in children with newly diagnosed inflammatory bowel disease. Osteoporos Int. 2010;21(2):331-7.
95. Tuchman S, Thayu M, Shults J, Zemel BS, Burnham JM, Leonard MB. Interpretation of biomarkers of bone metabolism in children: impact of growth velocity and body size in healthy children and chronic disease. J Pediatr. 2008;153(4):484-90.
96. Semeao EJ, Jawad AF, Stouffer NO, Zemel BS, Piccoli DA, Stallings VA. Risk factors for low bonemineral density in children and young adults with Crohn's disease. J Pediatr. 1999;135(5):593-600. (Pubitemid 30180450)
97. de Jong DJ, Corstens FH, Mannaerts L, van Rossum LG, Naber AH. Corticosteroid-induced osteoporosis: does it occur in patients with Crohn's disease? Am J Gastroenterol. 2002;97(8):2011-5.
98. Johnston Jr CC, Miller JZ, Slemenda CW, Reister TK, Hui S, Christian JC, et al. Calciumsupplementation and increases in bone mineral density in children. N Engl J Med. 1992;327(2):82-7.
99. Gunter KB, Almstedt HC, Janz KF. Physical activity in childhood may be the key to optimizing lifespan skeletal health. Exerc Sport Sci Rev. 2012;40(1):13-21.
100. Ubesie AC, Heubi JE, Kocoshis SA, Henderson CJ, Mezoff AG, Rao MB, et al. Vitamin D deficiency and lowbonemineral density in pediatric and young adult intestinal failure. J Pediat Gastroenterol Nutrit. 2013;57(3):372-6.
101. van Bodegraven AA, Bravenboer N, Witte BI, Dijkstra G, van der Woude CJ, Stokkers PC, et al. Treatment of bone loss in osteopenic patients with Crohn's disease: a double-blind, randomised trial of oral risedronate 35 mg once weekly or placebo, concomitant with calcium and vitamin D supplementation. Gut. 2013. doi:10.1136/gutjnl-2013-305523.
102. Karalus J, Chlebna-Sokol D. The clinical efficacy of vitamin D in children with primary low bone mass. Pediatr Endocrinol Diabetes Metab. 2011;17(1):35-40.
103. Soo J, Malik BA, Turner JM, Persad R, Wine E, Siminoski K, et al. Use of exclusive enteral nutrition is just as effective as corticosteroids in newly diagnosed pediatric Crohn's disease. Dig Dis Sci. 2013;58(12):3584-91.
104. Werkstetter KJ, Schatz SB, Alberer M, Filipiak-Pittroff B, Koletzko S. Influence of exclusive enteral nutrition therapy on bone density and geometry in newly diagnosed pediatric Crohn's disease patients. Ann Nutr Metab. 2013;63(1-2):10-6.
105. Cundy T. Recent advances in osteogenesis imperfecta. Calcif Tissue Int. 2012;90(6):439-49.
106. • Bianchi ML, Cimaz R, Bardare M, Zulian F, Lepore L, Boncompagni A, et al. Efficacy and safety of alendronate for the treatment of osteoporosis in diffuse connective tissue diseases in children: a prospective multicenter study. Arthritis Rheumatism. 2000;43(9):1960-6. First prospective study on the use of alendronate in children with arthritis and connective tissue diseases.
107. • Guo Z, Wu R, Gong J, Zhu W, Li Y, Li N, et al. The efficacy and safety of bisphosphonates for osteoporosis or osteopenia in Crohn's disease: a meta-analysis. Dig Dis Sci. 2013;58(4):915-22. A meta-analysis on the studies perfomed on bisphosphonateds in Crohn, concluding that routine use cannot be yet recommended.
108. Bachrach LK, Ward LM. Clinical review 1: bisphosphonate use in childhood osteoporosis. J Clin Endocrinol Metab. 2009;94(2):400-9.
109. Ward L, Tricco AC, Phuong P, Cranney A, Barrowman N, Gaboury I, et al. Bisphosphonate therapy for children and adolescents with secondary osteoporosis. Cochrane Database Syst Rev. 2007;4, CD005324.
110. Thornton J, Ashcroft DM, Mughal MZ, Elliott RA, O'Neill TW, Symmons D. Systemat ic review of effectiveness of bisphosphonates in treatment of low bone mineral density and fragility fractures in juvenile idiopathic arthritis. Arch Dis Child. 2006;91(9):753-61. (Pubitemid 44351176)
111. Barbehenn EK, Lurie P, Wolfe SM. Osteosarcoma risk in rats using PTH 1-34. Trends Endocrinol Metab. 2001;12(9):383.
112. • Linglart A, Rothenbuhler A, Gueorgieva I, Lucchini P, Silve C, Bougneres P. Long-term results of continuous subcutaneous recombinant PTH (1-34) infusion in children with refractory hypoparathyroidism. J Clin Endocrinol Metab. 2011;96(11):3308-12. PTH use is feared inthe pediatric age, this paper shows long-term results even if not in children with inflammatory disorders.
113. Brabnikova Maresova K, Jarosova K, Pavelka K, Stepan JJ. Bone status in adults with early-onset juvenile idiopathic arthritis following 1-year anti-TNFalpha therapy and discontinuation of glucocorticoids. Rheumatol Int. 2013;33(8):2001-7.
114. Simonini G, Giani T, Stagi S, de Martino M, Falcini F. Bone status over 1 year of etanercept treatment in juvenile idiopathic arthritis. Rheumatology. 2005;44(6):777-80. (Pubitemid 41487209)
115. Thayu M, Leonard MB, Hyams JS, Crandall WV, Kugathasan S, Otley AR, et al. Improvement in biomarkers of bone formation during infliximab therapy in pediatric Crohn's disease: results of the REACH study. Clin Gastroenterol Hepatol. 2008;6(12):1378-84.
116. Bechtold S, Beyerlein A, Ripperger P, Roeb J, Dalla Pozza R, Hafner R, et al. Total pubertal growth in patients with juvenile idiopathic arthritis treated with growth hormone: analysis of a single center. Growth Horm IGF Res. 2012;22(5):180-5.
117. Vortia E, Kay M, Wyllie R. The role of growth hormone and insulin-like growth factor-1 in Crohn's disease: implications for therapeutic use of human growth hormone in pediatric patients. Curr Opin Pediatr. 2011;23(5):545-51.