The impact of underlying disease on fracture risk and bone mineral density in children with rheumatic disorders: A review of current literature

Seminars in Arthritis and Rheumatism

Volumn 46, Issue 1, 2016, Pages 49-63

  Huber, Adam M ^a   Ward, Leanne M ^b  

^a IWK HEALTH CENTRE   (Canada)

^b CHILDREN S HOSPITAL OF EASTERN ONTARIO   (Canada)

Author keywords

Bone fragility; Bone mineral density; Juvenile arthritis; Juvenile dermatomyositis; Juvenile idiopathic arthritis; Juvenile rheumatic disease; Juvenile systemic lupus erythematosus; Non vertebral fractures; Vertebral fractures

Indexed keywords

CORTICOSTEROID; GLUCOCORTICOID;

BONE DENSITY; CHILD; DISEASE ASSOCIATION; DISEASE DURATION; FRACTURE RISK; HIGH RISK PATIENT; HUMAN; JUVENILE DERMATOMYOSITIS; JUVENILE RHEUMATOID ARTHRITIS; MUSCULOSKELETAL DISEASE ASSESSMENT; ONSET AGE; PRIORITY JOURNAL; REVIEW; RHEUMATIC DISEASE; RISK; RISK ASSESSMENT; RISK REDUCTION; SPINE FRACTURE; SYSTEMIC LUPUS ERYTHEMATOSUS; COMPLICATION; DRUG EFFECTS; FRACTURES, BONE; PATHOPHYSIOLOGY; PHYSIOLOGY; RHEUMATIC DISEASES;

BONE DENSITY; CHILD; FRACTURES, BONE; GLUCOCORTICOIDS; HUMANS; RHEUMATIC DISEASES;

EID: 84961784551     PISSN: 00490172     EISSN: 1532866X     Source Type: Journal    
DOI: 10.1016/j.semarthrit.2016.02.003     Document Type: Review

References (111)

1. [1] Gannotti, M.E., Nahorniak, M., Gorton, G.E. 3rd, Sciascia, K., Sueltenfuss, M., Synder, M., et al. Can exercise influence low bone mineral density in children with juvenile rheumatoid arthritis?. Pediatr Phys Ther 19 (2007), 128–139.
2. [2] McLean, R.R., Proinflammatory cytokines and osteoporosis. Curr Osteoporos Rep 7 (2009), 134–139.
3. [3] Weitzmann, M.N., The role of inflammatory cytokines, the RANKL/OPG axis, and the immunoskeletal interface in physiological bone turnover and osteoporosis. Scientifica, 2013, 2013, 125705.
4. [4] Amarasekara, D.S., Yu, J., Rho, J., Bone loss triggered by the cytokine network in inflammatory autoimmune diseases. J Immunol Res, 2015, 2015, 832127.
5. [5] Ward, L.M., Osteoporosis due to glucocorticoid use in children with chronic illness. Horm Res 64 (2005), 209–221.
6. [6] Bianchi, M.L., Osteoporosis in children and adolescents. Bone 41 (2007), 486–495.
7. [7] Rauch, F., Plotkin, H., DiMeglio, L., Engelbert, R.H., Henderson, R.C., Munns, C., et al. Fracture prediction and the definition of osteoporosis in children and adolescents: the ISCD 2007 Pediatric Official Positions. J Clin Densitom 11:1 (2008), 22–28.
8. [8] 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 ISCD 2013 Pediatric Official Positions. J Clin Densitom 17 (2014), 275–280.
9. [9] Huber, A.M., Gaboury, I., Cabral, D.A., 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 62 (2010), 516–526.
10. [10] Rodd, C., Lang, B.A., Ramsay, T., Alos, N., Huber, A.M., Cabral, D.A., et al. Incident vertebral fractures among children with rheumatic disorders 12 months post-glucocorticoid initiation: a national observational study. Arthritis Care Res 64 (2012), 122–131.
11. [11] LeBlanc, C.M., Ma, J., Taljaard, M., Roth, J., Scuccimarri, R., Miettunen, P., et al. Incident vertebral fractures and risk factors in the first three years following glucocorticoid initiation among pediatric patients with rheumatic disorders. J Bone Miner Res 30 (2015), 1667–1675.
12. [12] Ma, J., Siminoski, K., Alos, N., Halton, J., Lentle, B., Matzinger, M.A., et al. The Choice of normative pediatric reference database changes spine bone mineral density Z-scores but not the relationship of bone mineral density with prevalent vertebral fractures. J Clin Endocrinol Metab 100 (2015), 1018–1027.
13. [13] Dubner, S.E., Shults, J., Leonard, M.B., Zemel, B.S., Sembhi, H., Burnham, J.M., Assessment of spine bone mineral density in juvenile idiopathic arthritis: impact of scan projection. J Clin Densitom 11 (2008), 302–308.
14. [14] Gaspari, S., Marcovecchio, M.L., Breda, L., Chiarelli, F., Growth in juvenile idiopathic arthritis: the role of inflammation. Clin Exp Rheumatol 29 (2011), 104–110.
15. [15] van der Sluis, I., de Ridder, M., Boot, A., Krenning, E., de Muinck Keizer-Schrama, S.M., Reference data for bone density and body composition measured with dual energy X-ray absoptiometry in white children and young adults. Arch Dis Child 87 (2002), 341–347.
16. [16] Zemel, B.S., Leonard, M.B., Kelly, A., Lappe, J.M., 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 95 (2010), 1265–1273.
17. [17] Crabtree, N.J., Hogler, W., Cooper, M.S., Shaw, N.J., Diagnostic evaluation of bone densitometric size adjustment techniques in children with and without low trauma fractures. Osteoporosis Int 24 (2013), 2015–2024.
18. [18] Rousseau-Nepton, I., Lang, B., Rodd, C., Long-term bone health in glucocorticoid-treated children with rheumatic diseases. Curr Rheumatol Rep, 15, 2013, 315.
19. [19] Elsasser, U., Wilkins, B., Hesp, R., Thurnham, D.I., Reeve, J., Ansell, B.M., Bone rarefaction and crush fractures in juvenile chronic arthritis. Arch Dis Child 57 (1982), 377–380.
20. [20] Nakhla, M., Scuccimarri, R., Duffy, K.N., Chedeville, G., Campillo, S., Duffy, C.M., et al. Prevalence of vertebral fractures in children with chronic rheumatic diseases at risk for osteopenia. J Pediatr 154 (2009), 438–443.
21. [21] Reeve, J., Loftus, J., Hesp, R., Ansell, B.M., Wright, D.J., Woo, P.M., Biochemical prediction of changes in spinal bone mass in juvenile chronic (or rheumatoid) arthritis treated with glucocorticoids. J Rheumatol 20 (1993), 1189–1195.
22. [22] Markula-Patjas, K.P., Valta, H.L., Kerttula, L.I., Soini, I.H., Honkanen, V.E., Toiviainen-Salo, S.M., et al. Prevalence of vertebral compression fractures and associated factors in children and adolescents with severe juvenile idiopathic arthritis. J Rheumatol 39 (2012), 365–373.
23. [23] Bechtold, S., Ripperger, P., Dalla Pozza, R., Schmidt, H., Hafner, R., Schwarz, H.P., Musculoskeletal and functional muscle–bone analysis in children with rheumatic disease using peripheral quantitative computed tomography. Osteoporos Int 16 (2005), 757–763.
24. [24] Valta, H., Lahdenne, P., Jalanko, H., Aalto, K., Makitie, O., Bone health and growth in glucocorticoid-treated patients with juvenile idiopathic arthritis. J Rheumatol 34 (2007), 831–836.
25. [25] Baroncelli, G.I., Federico, G., Bertelloni, S., Sodini, F., De Terlizzi, F., Cadossi, R., et al. Assessment of bone quality by quantitative ultrasound of proximal phalanges of the hand and fracture rate in children and adolescents with bone and mineral disorders. Pediatr Res 54 (2003), 125–136.
26. [26] Burnham, J.M., Shults, J., Weinstein, R., Lewis, J.D., Leonard, M.B., Childhood onset arthritis is associated with an increased risk of fracture: a population based study using the General Practice Research Database. Ann Rheum Dis 65 (2006), 1074–1079.
27. [27] Lien, G., Selvaag, A.M., Flato, B., Haugen, M., Vinje, O., Sorskaar, D., et al. A two-year prospective controlled study of bone mass and bone turnover in children with early juvenile idiopathic arthritis. Arthritis Rheum 52 (2005), 833–840.
28. [28] Varonos, S., Ansell, B., Reeve, J., Vertebral collapse in juvenile chronic arthritis: its relationship with glucocorticoid therapy. Calcif Tissue Int 41 (1987), 75–78.
29. [29] Stewart, W.A., Acott, P.D., Salisbury, S.R., Lang, B.A., Bone mineral density in juvenile dermatomyositis: assessment using dual X-ray absorptiometry. Arthritis Rheum 48 (2003), 2294–2298.
30. [30] 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 17 (2008), 787–792.
31. [31] Bianchi, M.L., Bardare, M., Caraceni, M.P., Cohen, E., Falvella, S., Borzani, M., et al. Bone metabolism in juvenile rheumatoid arthritis. Bone Miner 9 (1990), 153–162.
32. [32] 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 19 (1996), 165–169.
33. [33] Henderson, C.J., Cawkwell, G.D., Specker, B.L., Sierra, R.I., Wilmott, R.W., Campaigne, B.N., et al. Predictors of total body bone mineral density in non-corticosteroid-treated prepubertal children with juvenile rheumatoid arthritis. Arthritis Rheum 40 (1997), 1967–1975.
34. [34] Hillman, L., Cassidy, J.T., Johnson, L., Lee, D., Allen, S.H., Vitamin D metabolism and bone mineralization in children with juvenile rheumatoid arthritis. J Pediatr 124 (1994), 910–916.
35. [35] Hopp, R., Degan, J., Gallagher, J.C., Cassidy, J.T., Estimation of bone mineral density in children with juvenile rheumatoid arthritis. J Rheumatol 18 (1991), 1235–1239.
36. [36] Kotaniemi, A., Growth retardation and bone loss as determinants of axial osteopenia in juvenile chronic arthritis. Scand J Rheumatol 26 (1997), 14–18.
37. [37] Kotaniemi, A., Savolainen, A., Kautiainen, H., Kroger, H., Estimation of central osteopenia in children with chronic polyarthritis treated with glucocorticoids. Pediatrics 91 (1993), 1127–1130.
38. [38] Kotaniemi, A., Savolainen, A., Kroger, H., Kautiainen, H., Isomaki, H., Development of bone mineral density at the lumbar spine and femoral neck in juvenile chronic arthritis—a prospective one year followup study. J Rheumatol 25 (1998), 2450–2455.
39. [39] Pereira, R.M., Corrente, J.E., Chahade, W.H., Yoshinari, N.H., Evaluation by dual X-ray absorptiometry (DXA) of bone mineral density in children with juvenile chronic arthritis. Clin Exp Rheumatol 16 (1998), 495–501.
40. [40] Bianchi, M.L., Cimaz, R., Galbiati, E., Corona, F., Cherubini, R., Bardare, M., Bone mass change during methotrexate treatment in patients with juvenile rheumatoid arthritis. Osteoporos Int 10 (1999), 20–25.
41. [41] Brik, R., Keidar, Z., Schapira, D., Israel, O., Bone mineral density and turnover in children with systemic juvenile chronic arthritis. J Rheumatol 25 (1998), 990–992.
42. [42] Celiker, R., Bal, S., Bakkaloglu, A., Ozaydin, E., Coskun, T., Cetin, A., et al. Factors playing a role in the development of decreased bone mineral density in juvenile chronic arthritis. Rheumatology Int 23 (2003), 127–129.
43. [43] Cetin, A., Celiker, R., Dincer, F., Ariyurek, M., Bone mineral density in children with juvenile chronic arthritis. Clin Rheumatol 17 (1998), 551–553.
44. [44] Haugen, M., Lien, G., Flato, B., Kvammen, J., Vinje, O., Sorskaar, D., et al. Young adults with juvenile arthritis in remission attain normal peak bone mass at the lumbar spine and forearm. Arthritis Rheum 43 (2000), 1504–1510.
45. [45] Henderson, C.J., Specker, B.L., Sierra, R.I., Campaigne, B.N., Lovell, D.J., Total-body bone mineral content in non-corticosteroid-treated postpubertal females with juvenile rheumatoid arthritis: frequency of osteopenia and contributing factors. Arthritis Rheum 43 (2000), 531–540.
46. [46] Kotaniemi, A., Savolainen, A., Kröger, H., Kautiainen, H., Isomäki, H., Weight-bearing physical activity, calcium intake, systemic glucocorticoids, chronic inflammation, and body constitution as determinants of lumbar and femoral bone mineral in juvenile chronic arthritis. Scand J Rheumatol 28 (1999), 19–26.
47. [47] Touati, G., Ruiz, J.C., Porquet, D., Kindermans, C., Prieur, A.M., Czernichow, P., Effects on bone metabolism of one year recombinant human growth hormone administration to children with juvenile chronic arthritis undergoing chronic steroid therapy. J Rheumatol 27 (2000), 1287–1293.
48. [48] Zak, M., Hassager, C., Lovell, D.J., Nielsen, S., Henderson, C.J., Pedersen, F.K., Assessment of bone mineral density in adults with a history of juvenile chronic arthritis: a cross-sectional long-term followup study. Arthritis Rheum 42 (1999), 790–798.
49. [49] Burnham, J., Shults, J., Dubner, S., Sembhi, H., Zemel, B., Leonard, M., Bone density, structure, and strength in juvenile idiopathic arthritis: importance of disease severity and muscle deficits. Arthritis Rheum 58 (2008), 2518–2527.
50. [50] Dey, S., Jahan, A., Yadav, T.P., Bhagwani, D.K., Sachdev, N., Measurement of bone mineral density by dual energy X-ray absorptiometry in juvenile idiopathic arthritis. Indian J Pediatr 81 (2014), 126–132.
51. [51] Felin, E.M., Prahalad, S., Askew, E.W., Moyer-Mileur, L.J., Musculoskeletal abnormalities of the tibia in juvenile rheumatoid arthritis. Arthritis Rheum 56 (2007), 984–994.
52. [52] Gorska, A., Urban, M., Bartnicka, M., Zelazowska-Rutkowska, B., Wysocka, J., Bone mineral metabolism in children with juvenile idiopathic arthritis—preliminary report. Ortop Traumatol Rehabil 10 (2008), 54–62.
53. [53] Hamalainen, H., Arkela-Kautiainen, M., Kautiainen, H., Haapasaari, J., Leirisalo-Repo, M., Bone mineral content in young adults with active or inactive juvenile idiopathic arthritis and in controls. Scand J Rheumatol 39 (2010), 219–222.
54. [54] Kandil, M.E., Mourad, A., El Hamshary, A., Hussein, G., Ahmed, A., Mawgoud, S.A., Evaluation of bone mineral density and bone turnover markers in Egyptian children with juvenile rheumatoid arthritis. Arch Med Sci 5 (2009), 434–442.
55. [55] Simonini, G., Giani, T., Stagi, S., de Martino, M., Falcini, F., Bone status over 1 year of etanercept treatment in juvenile idiopathic arthritis. Rheumatology (Oxford) 44 (2005), 777–780.
56. [56] Stagi, S., Cavalli, L., Signorini, C., Bertini, F., Cerinic, M.M., Brandi, M.L., et al. Bone mass and quality in patients with juvenile idiopathic arthritis: longitudinal evaluation of bone mass determinants using dual energy X-ray absorptiometry, peripheral quantitative computed tomography, and quantitative ultrasonography. Arthritis Res Ther, 16, 2014, R83.
57. [57] 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 37 (2010), 1935–1943.
58. [58] van Summeren, M.J., Vermeer, C., Engelbert, R.H., Schurgers, L.J., Takken, T., Fischer, K., et al. Extremes in vitamin K status of bone are related to bone ultrasound properties in children with juvenile idiopathic arthritis. Clin Exp Rheumatol 26 (2008), 484–491.
59. [59] Falcini, F., Bindi, G., Ermini, M., Galluzzi, F., Poggi, G., Rossi, S., et al. Comparison of quantitative calcaneal ultrasound and dual energy X-ray absorptiometry in the evaluation of osteoporotic risk in children with chronic rheumatic diseases. Calcif Tissue Int 67 (2000), 19–23.
60. [60] Falcini, F., Bindi, G., Simonini, G., Stagi, S., Galluzzi, F., Masi, L., et al. Bone status evaluation with calcaneal ultrasound in children with chronic rheumatic diseases. A one year followup study. J Rheumatol 30 (2003), 179–184.
61. [61] Fantini, F., Beltrametti, P., Gallazzi, M., Gattinara, M., Gerloni, V., Murelli, M., et al. Evaluation by dual-photon absorptiometry of bone mineral loss in rheumatic children on long-term treatment with corticosteroids. Clin Exp Rheumatol 9 Suppl. 6 (1991), 21–28.
62. [62] Kashef, S., Saki, F., Karamizadeh, Z., Kashef, M., Bone mineral density in children with systemic lupus erythematosus and juvenile rheumatoid arthritis. Ann Saudi Med 27 (2007), 427–431.
63. [63] Bechtold, S., Ripperger, P., Bonfig, W., Schmidt, H., Bitterling, H., Hafner, R., et al. Bone mass development and bone metabolism in juvenile idiopathic arthritis: treatment with growth hormone for 4 years. J Rheumatol 31 (2004), 1407–1412.
64. [64] Roth, J., Palm, C., Scheunemann, I., Ranke, M.B., Schweizer, R., Dannecker, G.E., Musculoskeletal abnormalities of the forearm in patients with juvenile idiopathic arthritis relate mainly to bone geometry. Arthritis Rheum 50 (2004), 1277–1285.
65. [65] Roth, J., Linge, M., Tzaribachev, N., Schweizer, R., Kuemmerle-Deschner, J., Musculoskeletal abnormalities in juvenile idiopathic arthritis—a 4-year longitudinal study. Rheumatology (Oxford) 46 (2007), 1180–1184.
66. [66] Bechtold, S., Ripperger, P., Dalla Pozza, R., Roth, J., Hafner, R., Michels, H., et al. Dynamics of body composition and bone in patients with juvenile idiopathic arthritis treated with growth hormone. J Clin Endocrinol Metab 95 (2010), 178–185.
67. [67] Mul, D., van Suijlekom-Smit, L.W., ten Cate, R., Bekkering, W.P., de Muinck Keizer-Schrama, S.M., Bone mineral density and body composition and influencing factors in children with rheumatic diseases treated with corticosteroids. J Pediatr Endocrinol Metab 15 (2002), 187–192.
68. [68] Simon, D., Lucidarme, N., Prieur, A.M., Ruiz, J.C., Czernichow, P., Effects on growth and body composition of growth hormone treatment in children with juvenile idiopathic arthritis requiring steroid therapy. J Rheumatol 30 (2003), 2492–2499.
69. [69] Polito, C., Strano, C.G., Rea, L., Alessio, M., Iammarrone, C.S., Todisco, N., et al. Reduced bone mineral content and normal serum osteocalcin in non-steroid-treated patients with juvenile rheumatoid arthritis. Ann Rheum Dis 54 (1995), 193–196.
70. [70] Head, A.J., Myers, L.K., Watsky, M.A., Greenwell, M.W., Barrow, K.D., Michelson, J.A., et al. Bone mineral density and turnover in non-corticosteroid treated African American children with juvenile rheumatoid arthritis. J Rheumatol 33 (2006), 1001–1003.
71. [71] Castro, T., Terreri, M., Szejnfled, V., Castro, C., Fisberg, M., Gabay, M., et al. Bone mineral density in juvenile systemic lupus erythematosus. Braz J Med Biol Res 35 (2002), 1159–1163.
72. [72] Compeyrot-Lacassagne, S., Tyrrell, P., Atenafu, E., Doria, A., Stephens, D., Gilday, D., et al. Prevalence and etiology of low bone mineral density in juvenile systemic lupus erythematosus. Arthritis Rheum 56 (2007), 1966–1973.
73. [73] Lilleby, V., Lien, G., Frey Froslie, K., Haugen, M., Flato, B., Forre, O., Frequency of osteopenia in children and young adults with childhood-onset systemic lupus erythematosus. Arthritis Rheum 52 (2005), 2051–2059.
74. [74] 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 18 (1998), 45–49.
75. [75] Baker-LePain, J.C., Nakamura, M.C., Shepherd, J., von Scheven, E., Assessment of bone remodelling in childhood-onset systemic lupus erythematosus. Rheumatology (Oxford) 50 (2011), 611–619.
76. [76] Casella, C.B., Seguro, L.P., Takayama, L., Medeiros, D., Bonfa, E., Pereira, R.M., Juvenile onset systemic lupus erythematosus: a possible role for vitamin D in disease status and bone health. Lupus 21 (2012), 1335–1342.
77. [77] Lim, S.H.L., Benseler, S.M., Tyrrell, P.N., Harvey, E., Herbert, D., Charron, M., et al. Predicting longitudinal trajectory of bone mineral density in paediatric systemic lupus erythematosus patients. Ann Rheum Dis 71 (2012), 1686–1691.
78. [78] Lim, S.H.L., Benseler, S.M., Tyrrell, P.N., Charron, M., Harvey, E., Hebert, D., et al. Low bone mineral density is present in newly diagnosed paediatric systemic lupus erythematosus patients. Ann Rheum Dis 70 (2011), 1991–1994.
79. [79] Mok, C.C., Wong, S.N., Ma, K.M., Childhood-onset disease carries a higher risk of low bone mineral density in an adult population of systemic lupus erythematosus. Rheumatology (Oxford) 51 (2012), 468–475.
80. [80] So, M., Mok, C.C., Ma, K.M., Kwok, A., Leung, P., Wong, S., Frequency of low bone mineral density and its associated factors in patients with juvenile systemic lupus erythematosus. HK J Paediatr 16 (2011), 77–84.
81. [81] 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 23 (2014), 57–68.
82. [82] Alsufyani, K.A., Ortiz-Alvarez, O., Cabral, D.A., Tucker, L.B., Petty, R.E., 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, calcium intake, and exercise. J Rheumatol 32 (2005), 729–733.
83. [83] Grote, F.K., Van Suijlekom-Smit, L.W., Mul, D., Hop, W.C., Ten Cate, R., Oostdijk, W., et al. Growth hormone treatment in children with rheumatic disease, corticosteroid induced growth retardation, and osteopenia. Arch Dis Child 91 (2006), 56–60.
84. [84] Hartman, C., Shamir, R., Eshach-Adiv, O., Iosilevsky, G., Brik, R., Assessment of osteoporosis by quantitative ultrasound versus dual energy X-ray absorptiometry in children with chronic rheumatic diseases. J Rheumatol 31 (2004), 981–985.
85. [85] Perez, M.D., Abrams, S.A., Loddeke, L., Shypailo, R., Ellis, K.J., Effects of rheumatic disease and corticosteroid treatment on calcium metabolism and bone density in children assessed one year after diagnosis, using stable isotopes and dual energy X-ray absorptiometry. J Rheumatol 27:Suppl. 58 (2000), 38–43.
86. [86] Rudge, S., Hailwood, S., Horne, A., Lucas, J., Wu, F., Cundy, T., Effects of once-weekly oral alendronate on bone in children on glucocorticoid treatment. Rheumatology (Oxford) 44 (2005), 813–818.
87. [87] von Scheven, E., Gordon, C.M., Wypij, D., Wertz, M., Gallagher, K.T., Bachrach, L., Variable deficits of bone mineral despite chronic glucocorticoid therapy in pediatric patients with inflammatory diseases: a Glaser Pediatric Research Network study. J Pediatr Endocrinol Metab 19 (2006), 821–830.
88. [88] Cohran, V.C., Griffiths, M., Heubi, J.E., Bone mineral density in children exposed to chronic glucocorticoid therapy. Clin Pediatr 47 (2008), 469–475.
89. [89] Castro, T.C., Terreri, M.T., Szejnfeld, V.L., Len, C., Fonseca, A.S., Hilário, M.O., Bone mineral density of Brazilian girls with juvenile dermatomyositis. Braz J Med Biol Res 38 (2005), 309–313.
90. [90] Ellis, K.J., Shypailo, R.J., Hardin, D.S., Perez, M.D., Motil, K.J., Wong, W.W., et al. Z score prediction model for assessment of bone mineral content in pediatric diseases. J Bone Miner Res 16 (2001), 1658–1664.
91. [91] Santiago, R., Silva, C., Caparbo, V., Sallum, A., Pereira, R., Bone mineral apparent density in juvenile dermatomyositis: the role of lean body mass and glucocorticoid use. Scand J Rheumatol 37 (2008), 40–47.
92. [92] Rouster-Stevens, K., Langman, C., Price, H., Seshadri, R., Shore, R., Abbott, K., et al. RANKL:Osteoprotegerin ratio and bone mineral density in children with untreated dermatomyositis. Arthritis Rheum 56 (2007), 977–983.
93. [93] French, A.R., Mason, T., Nelson, A.M., Crowson, C.S., O׳Fallon, W.M., Khosla, S., et al. Osteopenia in adults with a history of juvenile rheumatoid arthritis. A population based study. J Rheumatol 29 (2002), 1065–1070.
94. [94] Havelka, S., Vavrincova, P., Stepan, J., Metabolic bone status in young women with juvenile chronic arthritis. J Rheumatol Suppl 20:Suppl. 37 (1993), 14–16.
95. [95] Thornton, J., Pye, S.R., O׳Neill, T.W., Rawlings, D., Francis, R.M., Symmons, D.P., et al. Bone health in adult men and women with a history of juvenile idiopathic arthritis. J Rheumatol 38 (2011), 1689–1693.
96. [96] Reed, A.M., Haugen, M., Pachman, L.M., Langman, C.B., Repair of osteopenia in children with juvenile rheumatoid arthritis. J Pediatr 122:5 Pt 1 (1993), 693–696.
97. [97] Makitie, O., Doria, A.S., Henriques, F., Cole, W.G., Compeyrot, S., Silverman, E., et al. Radiographic vertebral morphology: a diagnostic tool in pediatric osteoporosis. J Pediatr 146 (2005), 395–401.
98. [98] Genant, H.K., Engelke, K., Fuerst, T., Gluer, C.C., Grampp, S., Harris, S.T., et al. Noninvasive assessment of bone mineral and structure: state of the art. J Bone Miner Res 11 (1996), 707–730.
99. [99] Bianchi, M.L., Leonard, M.B., Bechtold, S., Hogler, W., Mughal, M.Z., Schonau, E., et al. Bone health in children and adolescents with chronic diseases that may affect the skeleton: the 2013 ISCD Pediatric Official Positions. J Clin Densitom 17 (2014), 281–294.
100. [100] Crabtree, N.J., Arabi, A., Bachrach, L.K., Fewtrell, M., El-Hajj Fuleihan, G., Kecskemethy, H.H., et al. Dual-energy X-ray absorptiometry interpretation and reporting in children and adolescents: the revised 2013 ISCD Pediatric Official Positions. J Clin Densitom 17 (2014), 225–242.
101. [101] Jensen, K.K., Tougaard, L., A simple X-ray method for monitoring progress of osteoporosis. Lancet 2 (1981), 19–20.
102. [102] Reed, A., Haugen, M., Pachman, L.M., Langman, C.B., 25-Hydroxyvitamin D therapy in children with active juvenile rheumatoid arthritis: short-term effects on serum osteocalcin levels and bone mineral density. J Pediatr 119 (1991), 657–660.
103. [103] Bayer, M., Stepan, J., Nemcova, D., Kutilek, S., Hoza, J., Juvenile chronic arthritis—bone mineral density in relation to corticosteroid therapy. Acta Univ Carol Med (Praha) 40 (1994), 33–35.
104. [104] Pepmueller, P.H., Cassidy, J.T., Allen, S.H., Hillman, L.S., Bone mineralization and bone mineral metabolism in children with juvenile rheumatoid arthritis. Arthritis Rheum 39 (1996), 746–757.
105. [105] Njeh, C.F., Shaw, N., Gardner-Medwin, J.M., Boivin, C.M., Southwood, T.R., Use of quantitative ultrasound to assess bone status in children with juvenile idiopathic arthritis: a pilot study. J Clin Densitom 3 (2000), 251–260.
106. [106] 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 Rheum 48 (2003), 2214–2223.
107. [107] Kutilek, S., Bayer, M., Dolezalova, P., Nemcova, D., Quantitative ultrasonometry of the calcaneus in children with juvenile idiopathic arthritis. Rheumatology (Oxford) 45 (2006), 1273–1275.
108. [108] Okumus, O., Erguven, M., Deveci, M., Yilmaz, O., Okumus, M., Growth and bone mineralization in patients with juvenile idiopathic arthritis. Indian J Pediatr 75 (2008), 239–243.
109. [109] Billiau, A.D., Loop, M., Le, P.Q., Berthet, F., Philippet, P., Kasran, A., et al. Etanercept improves linear growth and bone mass acquisition in MTX-resistant polyarticular-course juvenile idiopathic arthritis. Rheumatology (Oxford) 49 (2010), 1550–1558.
110. [110] Sandstedt, E., Fasth, A., Fors, H., Beckung, E., Bone health in children and adolescents with juvenile idiopathic arthritis and the influence of short-term physical exercise. Pediatr Phys Ther 24 (2012), 155–161 discussion 162.
111. [111] Brabnikova Maresova, K., Jarosova, K., Pavelka, K., Stepan, J.J., Bone status in adults with early-onset juvenile idiopathic arthritis following 1-year anti-TNFalpha therapy and discontinuation of glucocorticoids. Rheumatol Int 33 (2013), 2001–2007.