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Osteoporosis and fractures in multiple sclerosis: pathogenesis, risk factors, treatment options, and prevention


Authors: Zikán Vít 1;  Kvasničková Ivana 1;  Týblová Michaela 2
Authors‘ workplace: III. interní klinika 1. LF UK a VFN v Praze 1;  Neurologická klinika 1. LF UK a VFN v Praze 2
Published in: Clinical Osteology 2018; 23(4): 146-161
Category:

Overview

Patients with neurological diseases are at higher risk of osteoporosis and fragility fractures compared to age-matched controls. This review summarizes the risk factors and pathophysiologic pathways that play a role in development of osteoporosis and fractures in multiple sclerosis (MS) patients. The research in this area has been active over recent years. Osteoporosis related fractures cause increased morbidity and mortality and add to the burden of having MS. There are currently no guidelines how to best prevent and treat osteoporosis in patients with neurological diseases. The work proposes an algorithm for the screening, prevention and treatment of osteoporosis in patients with MS.

Keywords:

Pathogenesis – Multiple sclerosis – osteoporosis – type 2 diabetes mellitus


Sources
  1. Blahová-Dušánková J, Kalinčik T, Doležal T et al. Cost of multiple sclerosis in the Czech Republic: the COMS study. Mult Scler 2012; 18(5): 662–668. Dostupné z DOI: <http://dx.doi.org/10.1177/1352458511424422>.
  2. Compston A, Coles A. Multiple sclerosis. Lancet 2008; 372(9648): 1502–1517. Dostupné z DOI: <http://dx.doi.org/10.1016/S0140–6736(08)61620–7>.
  3. Štěpán JJ, Havrdová E, Týblová M et al. Markers of bone remodeling predict rate of bone loss in multiple sclerosis patients treated with low dose glucocorticoids. Clin Chim Acta 2004; 348(1–2): 147–154. Dostupné z DOI: <http://dx.doi.org/10.1016/j.cccn.2004.05.012>.
  4. Havrdová E. Roztroušená skleróza. 2. ed. Maxdorf: Praha 2009. ISBN 978–80–7345–187–5.
  5. Weinstock-Guttman B, Gallagher E, Baier M et al. Risk of bone loss in men with multiple sclerosis. Mult Scler 2004; 10(2):170–175. Dostupné z DOI: <http://dx.doi.org/10.1191/1352458504ms993oa>.
  6. Bazelier MT, van Staa T, Uitdehaag BM et al. The risk of fracture in patients with multiple sclerosis: the UK general practice research database. J Bone Miner Res 2011; 26(9): 2271–2279. Dostupné z DOI: <http://dx.doi.org/10.1002/jbmr.418.>.
  7. Dobson R, Ramagopalan S, Giovannoni G et al. Risk of fractures in patients with multiple sclerosis: a population-based cohort study. Neurology 2012; 79(18): 1934–1935. Dostupné z DOI: <http://dx.doi.org/10.1212/01.wnl.0000422676.74031.07>.
  8. Gregson CL, Dennison EM, Compston JE et al. Disease-specific perception of fracture risk and incident fracture rates: GLOW cohort study. Osteoporos Int 2014; 25(1): 85–95. Dostupné z DOI: <http://dx.doi.org/10.1007/s00198–013–2438-y>.
  9. Marrie RA, Cutter G, Tyry T et al. A cross-sectional study of bone health in multiple sclerosis. Neurology 2009; 73(17):1394–1398. Dostupné z DOI: <http://dx.doi.org/10.1212/WNL.0b013e3181beece8>.
  10. Bazelier MT, Bentzen J, Vestergaard P et al. The risk of fracture in incident multiple sclerosis patients: The Danish National Health Registers. Mult Scler 2012; 18(11): 1609–1616. Dostupné z DOI: <http://dx.doi.org/10.1177/1352458512442755>.
  11. Dimitri P, Rosen C. The Central Nervous System and Bone Metabolism: An Evolving Story. Calcif Tissue Int 2017; 100(5): 476–485. Dostupné z DOI: <http://dx.doi.org/10.1007/s00223–016–0179–6>.
  12. Elefteriou F, Campbell P, Ma Y. Control of bone remodeling by the peripheral sympathetic nervous system. Calcif Tissue Int 2014; 94(1):140–151. Dostupné z DOI: <http://dx.doi.org/10.1007/s00223–013–9752–4>.
  13. Formica CA, Cosman F, Nieves J et al. Reduced bone mass and fat-free mass in women with multiple sclerosis: effects of ambulatory status and glucocorticoid use. Calcif Tissue Int 1997; 61(2): 129–133.
  14. Gupta S, Ahsan I, Mahfooz N et al. Osteoporosis and multiple sclerosis: risk factors, pathophysiology, and therapeutic interventions. CNS Drugs 2014; 28(8): 731–742. Dostupné z DOI: <http://dx.doi.org/10.1007/s40263–014–0173–3>.
  15. Bloomfield SA. Disuse osteopenia. Curr Osteoporos Rep 2010; 8(2): 91–97. Dostupné z DOI: <http://dx.doi.org/10.1007/s11914–010–0013–4.
  16. Hamrick MW, McNeil PL, Patterson SL. Role of muscle-derived growth factors in bone formation. J Musculoskelet Neuronal Interact 2010; 10(1): 64–70.
  17. Cianferotti L, Brandi ML. Muscle-bone interactions: basic and clinical aspects. Endocrine 2014; 45(2): 165–177. Dostupné z DOI: <http://dx.doi.org/10.1007/s12020–013–0026–8>.
  18. Laurent MR, Dubois V, Claessens F et al. Muscle-bone interactions: From experimental models to the clinic? A critical update. Mol Cell Endocrinol 2016; 432: 14–36. Dostupné z DOI: <http://dx.doi.org/10.1016/j.mce.2015.10.017>.
  19. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983; 33(11): 1444–1452.
  20. Zikán V, Týblová M, Raška I jr et al. Bone mineral density and body composition in men with multiple sclerosis chronically treated with low-dose glucocorticoids. Physiol Res 2012; 61(4): 405–417.
  21. Týblová M, Zikán V, Luchavová M et al. Snížená denzita kostního minerálu u žen s roztroušenou sklerózou: vliv motorického deficitu, úbytku svalové hmoty a léčby glukokortikoidy. Článek: Cesk Slov Neurol 2013; 76(1): 35–44.
  22. Týblová M, Kalinčík T, Zikán V, Havrdová E. Impaired ambulation and steroid therapy impact negatively on bone health in multiple sclerosis. Eur J Neurol 2015; 22(4): 624–632. Dostupné z DOI: <http://dx.doi.org/10.1111/ene.12479>.
  23. Moen SM, Celius EG, Sandvik L et al. Low bone mass in newly diagnosed multiple sclerosis and clinically isolated syndrome. Neurology 2011; 77(2): 151–157. Dostupné z DOI: <http://dx.doi.org/10.1212/WNL.0b013e3182242d34>.
  24. Sioka C, Fotopoulos A, Georgiou A et al. Body composition in ambulatory patients with multiple sclerosis. J Clin Densitom 2011; 14(4): 465–470. Dostupné z DOI: <http://dx.doi.org/10.1016/j.jocd.2011.04.012>.
  25. Wens I, Dalgas U, Vandenabeele F et al. Multiple sclerosis affects skeletal muscle characteristics. PLoS One 2014; 9(9): e108158. Dostupné z DOI: <http://dx.doi.org/10.1371/journal.pone.0108158>.
  26. Nilsagard Y, Lundholm C, Denison E et al. Predicting accidental falls in people with multiple sclerosis – a longitudinal study. Clin Rehabil 2009; 23(3): 259–269. Dostupné z DOI: <http://dx.doi.org/10.1177/0269215508095087>.
  27. Zeigelboim BS, Arruda WO, Mangabeira-Albernaz PL et al. Vestibular findings in relapsing-remitting multiple sclerosis: a study of thirty patients. Int Tinnitus J 2008; 14(2): 139–145.
  28. Ozgen G, Karapolat H, Akkoc Y et al. Is customized vestibular rehabilitation effective in patients with multiple sclerosis? A randomized controlled trial. Eur J Phys Rehabil Med 2016; 52(4):466–478.
  29. Vignaux G, Ndong JD, Perrien DS et al. Inner Ear Vestibular Signals Regulate Bone Remodeling via the Sympathetic Nervous System. J Bone Miner Res 2015; 30(6): 1103–1111. Dostupné z DOI: <http://dx.doi.org/10.1002/jbmr.2426>.
  30. Vignaux G, Besnard S, Ndong J et al. Bone remodeling is regulated by inner ear vestibular signals. J Bone Miner Res 2013; 28(10): 2136–2144. Dostupné z DOI: <http://dx.doi.org/10.1002/jbmr.1940>.
  31. Bigelow RT, Semenov YR, Anson E et al. Impaired Vestibular Function and Low Bone Mineral Density: Data from the Baltimore Longitudinal Study of Aging. J Assoc Res Otolaryngol 2016; 17(5): 433–440. Dostupné z DOI: <http://dx.doi.org/10.1007/s10162–016–0577–5>.
  32. Gironi M, Solaro C, Meazza C et al. Growth hormone and disease severity in early stage of multiple sclerosis. Mult Scler Int 2013; 2013: 836486. Dostupné z DOI: <http://dx.doi.org/10.1155/2013/836486>.
  33. Lanzillo R, Di Somma C, Quarantelli M et al. Insulin-like growth factor (IGF)-I and IGF-binding protein-3 serum levels in relapsing-remitting and secondary progressive multiple sclerosis patients. Eur J Neurol 2011; 18(12): 1402–1406. Dostupné z DOI: <http://dx.doi.org/10.1111/j.1468–1331.2011.03433.x>.
  34. Ysrraelit MC, Gaitan MI, Lopez AS et al. Impaired hypothalamic-pituitary-adrenal axis activity in patients with multiple sclerosis. Neurology 2008; 71(24): 1948–1954. Dostupné z DOI: <http://dx.doi.org/10.1212/01.wnl.0000336918.32695.6b>.
  35. Melief J, de Wit SJ, van Eden CG et al. HPA axis activity in multiple sclerosis correlates with disease severity, lesion type and gene expression in normal-appearing white matter. Acta Neuropathol 2013; 126(2): 237–249. Dostupné z DOI: <http://dx.doi.org/10.1007/s00401–013–1140–7>.
  36. Bove R, Musallam A, Healy BC et al. Low testosterone is associated with disability in men with multiple sclerosis. Mult Scler 2014; 20(12): 1584–1592. Dostupné z DOI: <http://dx.doi.org/10.1177/1352458514527864>.
  37. Vandenput L, Mellström D, Laughlin GA et al. Low Testosterone, but not Estradiol, Is Associated with Incident Falls in Older Men – The International MrOS Study. J Bone Miner Res 2017; 32(6): 1174–1181. Dostupné z DOI: <http://dx.doi.org/10.1002/jbmr.3088>.
  38. Lee KC, Lanyon LE. Mechanical loading influences bone mass through estrogen receptor alpha. Exerc Sport Sci Rev 2004; 32(2): 64–68.
  39. Wei T, Lightman SL. The neuroendocrine axis in patients with multiple sclerosis. Brain 1997; 120(Pt 6): 1067–1076.
  40. Garcia LA, King KK, Ferrini MG et al. 1,25(OH)2vitamin D3 stimulates myogenic differentiation by inhibiting cell proliferation and modulating the expression of promyogenic growth factors and myostatin in C2C12 skeletal muscle cells. Endocrinology 2011; 152(8): 2976–2986. Dostupné z DOI: <http://dx.doi.org/10.1210/en.2011–0159>.
  41. Swanson CM, Srikanth P, Lee CG et al. Osteoporotic Fractures in Men MrOS Study Research Group. Associations of 25-Hydroxyvitamin D and 1,25-Dihydroxyvitamin D With Bone Mineral Density, Bone Mineral Density Change, and Incident Nonvertebral Fracture. J Bone Miner Res 2015; 30(8): 1403–1413. Dostupné z DOI: <http://dx.doi.org/10.1002/jbmr.2487>.
  42. Terzi T, Terzi M, Tander B et al. Changes in bone mineral density and bone metabolism markers in premenopausal women with multiple sclerosis and the relationship to clinical variables. J Clin Neurosci 2010; 17(10): 1260–1264. Dostupné z DOI: <http://dx.doi.org/10.1016/j.jocn.2010.01.044>.
  43. Jin D, Wu S, Zhang YG et al. Lack of vitamin D receptor causes dysbiosis and changes the functions of the murine intestinal microbiome. Clin Ther 2015; 37(5): 996–1009. Dostupné z DOI: <http://dx.doi.org/10.1016/j.clinthera.2015.04.004>.
  44. Manolagas SC. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 2000; 21(2): 115–137. Dostupné z DOI: <http://dx.doi.org/10.1210/edrv.21.2.0395>.
  45. Olsson A, Oturai DB, Sørensen PS et al. Short-term, high-dose glucocorticoid treatment does not contribute to reduced bone mineral density in patients with multiple sclerosis. Mult Scler 2015; 21(12): 1557–1565. Dostupné z DOI: <http://dx.doi.org/10.1177/1352458514566417>.
  46. Dovio A, Perazzolo L, Osella G et al. Immediate fall of bone formation and transient increase of bone resorption in the course of high-dose, short-term glucocorticoid therapy in young patients with multiple sclerosis. J Clin Endocrinol Metab 2004; 89(10): 4923–4928. Dostupné z DOI: <http://dx.doi.org/10.1210/jc.2004–0164>.
  47. Ozgocmen S, Bulut S, Ilhan N et al. Vitamin D deficiency and reduced bone mineral density in multiple sclerosis: effect of ambulatory status and functional capacity. J Bone Miner Metab 2005; 23(4): 309–313. Dostupné z DOI: <http://dx.doi.org/10.1007/s00774–005–0604–9>.
  48. Van Staa TP, Laan RF, Barton IP et al. Bone density threshold and other predictors of vertebral fracture in patients receiving oral glucocorticoid therapy. Arthritis Rheum 2003; 48(11): 3224–3229. Dostupné z DOI: <http://dx.doi.org/10.1002/art.11283>.
  49. Swidsinski A, Dörffel Y, Loening-Baucke V et al. Reduced Mass and Diversity of the Colonic Microbiome in Patients with Multiple Sclerosis and Their Improvement with Ketogenic Diet. Front Microbiol 2017; 8: 1141. Dostupné z DOI: <http://dx.doi.org/10.3389/fmicb.2017.01141>.
  50. Camara-Lemarroy CR, Metz LM, Yong VW. Focus on the gut-brain axis: Multiplesclerosis, the intestinal barrier and the microbiome. World J Gastroenterol 2018; 24(37): 4217–4223. Dostupné z DOI: <http://dx.doi.org/10.3748/wjg.v24.i37.4217>.
  51. Dendrou CA, Fugger L, Friese MA. Immunopathology of multiple sclerosis. Nat Rev Immunol 2015; 15(9): 545–558. Dostupné z DOI: <http://dx.doi.org/10.1038/nri3871>.
  52. Kurban S, Akpinar Z, Mehmetoglu I. Receptor activator of nuclear factor kappa B ligand (RANKL) and osteoprotegerin levels in multiple sclerosis. Mult Scler 2008; 14(3): 431–432. Dostupné z DOI: <http://dx.doi.org/10.1177/1352458507084028>.
  53. Takeda S. Osteoporosis: a neuroskeletal disease? Int J Biochem Cell Biol 2009; 41(3): 455–459. Dostupné z DOI: <http://dx.doi.org/10.1016/j.biocel.2008.08.002>.
  54. Takarada T, Xu C, Ochi H et al. Bone Resorption Is Regulated by Circadian Clock in Osteoblasts. J Bone Miner Res 2017; 32(4): 872–881. Dostupné z DOI: <http://dx.doi.org/10.1002/jbmr.3053>.
  55. Hirai T, Tanaka K, Togari A. beta-adrenergic receptor signaling regulates Ptgs2 by driving circadian gene expression in osteoblasts. J Cell Sci 2014; 127(Pt 17): 3711–3719. Dostupné z DOI: <http://dx.doi.org/10.1242/jcs.148148>.
  56. Fujihara Y, Kondo H, Noguchi T et al. Glucocorticoids mediate circadian timing in peripheral osteoclasts resulting in the circadian expression rhythm of osteoclast-related genes. Bone 2014; 61: 1–9. Dostupné z DOI: <http://dx.doi.org/10.1016/j.bone.2013.12.026>.
  57. Golombek DA, Casiraghi LP, Agostino PV et al. The times they’re a-changing: effects of circadian desynchronization on physiology and disease. J Physiol Paris 2013; 107(4): 310–322. Dostupné z DOI: <http://dx.doi.org/10.1016/j.jphysparis.2013.03.007>.
  58. Videira G, Castro P, Vieira B et al. Autonomic dysfunction in multiple sclerosis is better detected by heart rate variability and is not correlated with central autonomic network damage. J Neurol Sci 2016; 367: 133–137. Dostupné z DOI: <http://dx.doi.org/10.1016/j.jns.2016.05.049>.
  59. Yao Q, Liang H, Huang B et al. Beta-adrenergic signaling affect osteoclastogenesis via osteocytic MLO-Y4 cells' RANKL production. Biochem Biophys Res Commun 2017; 488(4): 634–640. Dostupné z DOI: <http://dx.doi.org/10.1016/j.bbrc.2016.11.011>.
  60. Buenafe AC. Diurnal rhythms are altered in a mouse model of multiple sclerosis. J Neuroimmunol 2012; 243(1–2): 12–17. Dostupné z DOI: <http://dx.doi.org/10.1016/j.jneuroim.2011.12.002>.
  61. Braley TJ, Boudreau EA. Sleep Disorders in Multiple Sclerosis. Curr Neurol Neurosci Rep 2016; 16(5): 50. Dostupné z DOI: <http://dx.doi.org/10.1007/s11910–016–0649–2>.
  62. Tononi G, Massimini M, Riedner BA. Sleepy dialogues between cortex and hippocampus: who talks to whom? Neuron 2006; 52(5):748–749. Dostupné z DOI: <http://dx.doi.org/10.1016/j.neuron.2006.11.014>.
  63. Damasceno A, Moraes AS, Farias A et al. Disruption of melatonin circadian rhythm production is related to multiple sclerosis severity: A preliminary study. J Neurol Sci 2015; 353(1–2): 166–168. Dostupné z DOI: <http://dx.doi.org/10.1016/j.jns.2015.03.040>.
  64. Cardinali DP, Ladizesky MG, Boggio V et al. Melatonin effects on bone: experimental facts and clinical perspectives. J Pineal Res 2003; 34(2): 81–87.
  65. Amstrup AK, Sikjaer T, Heickendorff L et al. Melatonin improves bone mineral density at the femoral neck in postmenopausal women with osteopenia: a randomized controlled trial. J Pineal Res 2015; 59(2): 221–229. Dostupné z DOI: <http://dx.doi.org/10.1111/jpi.12252>.
  66. Hood S, Amir S. The aging clock: circadian rhythms and later life. J Clin Invest 2017; 127(2): 437–446. Dostupné z DOI: <http://dx.doi.org/10.1172/JCI90328>.
  67. Pan W, Kastin AJ. Leptin: a biomarker for sleep disorders? Sleep Med Rev 2014; 18(3): 283–290. Dostupné z DOI: <http://dx.doi.org/10.1016/j.smrv.2013.07.003>.
  68. Motyl KJ, Rosen CJ. The skeleton and the sympathetic nervous system: it's about time! J Clin Endocrinol Metab 2012; 97(11): 3908–3911. Dostupné z DOI: <http://dx.doi.org/10.1210/jc.2012–3205>.
  69. Kondo H, Togari A. Continuous treatment with a low dose beta-agonist reduces bone mass by increasing bone resorption without suppressing bone formation. Calcif Tissue Int 2011; 88(1): 23–32. Dostupné z DOI: <http://dx.doi.org/10.1007/s00223–010–9421–9>.
  70. Guo B, Zhang ZK, Liang C et al. Molecular Communication from Skeletal Muscle to Bone: A Review for Muscle-Derived Myokines Regulating Bone Metabolism. Calcif Tissue Int 2017; 100(2): 184–192. Dostupné z DOI: <http://dx.doi.org/10.1007/s00223–016–0209–4>.
  71. Tosun A, Dogru MT, Aydn G et al. Does autonomic dysfunction exist in postmenopausal osteoporosis? Am J Phys Med Rehabil 2011; 90(12): 1012–1019. Dostupné z DOI: <http://dx.doi.org/10.1097/PHM.0b013e31822dea1a>.
  72. Farr JN, Charkoudian N, Barnes JN et al. Relationship of sympathetic activity to bone micro-structure, turnover, and plasma osteopontin levels in women. J Clin Endocrinol Metab 2012; 97(11): 4219–4227. Dostupné z DOI: <http://dx.doi.org/10.1210/jc.2012–2381>.
  73. Polak PE, Kalinin S, Feinstein DL. Locus coeruleus damage and noradrenaline reductions in multiple sclerosis and experimental autoimmune encephalomyelitis. Brain 2011; 134(Pt 3): 665–677. Dostupné z DOI: <http://dx.doi.org/10.1093/brain/awq362>.
  74. Rajda C, Bencsik K, Füvesi J et al. The norepinephrine level is decreased in the lymphocytes of long-term interferon-beta-treated multiple sclerosis patients. Mult Scler 2006; 12(3): 265–270. Dostupné z DOI: <http://dx.doi.org/10.1191/135248506ms1269oa>.
  75. Boeschoten RE, Braamse AM, Beekman AT et al. Prevalence of depression and anxiety in Multiple Sclerosis: A systematic review and meta-analysis. J Neurol Sci 2017; 372: 331–341. Dostupné z DOI: <http://dx.doi.org/10.1016/j.jns.2016.11.067>.
  76. Cizza G, Primma S, Csako G. Depression as a risk factor for osteoporosis. Trends Endocrinol Metab 2009; 20(8): 367–373. Dostupné z DOI: <http://dx.doi.org/10.1016/j.tem.2009.05.003>.
  77. Iwamoto I, Douchi T, Kosha S et al. Relationships between serum leptin level and regional bone mineral density, bone metabolic markers in healthy women. Acta Obstet Gynecol Scand 2000; 79(12): 1060–1064.
  78. Yirmiya R, Goshen I, Bajayo A et al. Depression induces bone loss through stimulation of the sympathetic nervous system. Proc Natl Acad Sci USA 2006; 103(45): 16876–16881. Dostupné z DOI: <http://dx.doi.org/10.1073/pnas.0604234103>.
  79. Marcum ZA, Perera S, Thorpe JM et al. Health ABC Study. Antidepressant Use and Recurrent Falls in Community-Dwelling Older Adults: Findings from the Health ABC Study. Ann Pharmacother 2016; 50(7): 525–533. Dostupné z DOI: <http://dx.doi.org/10.1177/1060028016644466>.
  80. Wang CY, Fu SH, Wang CL et al. Serotonergic antidepressant use and the risk of fracture: a population-based nested case-control study. Osteoporos Int 2016; 27(1): 57–63. Dostupné z DOI: <http://dx.doi.org//10.1007/s00198–015–3213-z>.
  81. Weinstein RS. Clinical practice. Glucocorticoid-induced bone disease. N Engl J Med 2011; 365(1): 62–70. Dostupné z DOI: <http://dx.doi.org/10.1056/NEJMcp1012926>.
  82. Hearn AP, Silber E. Osteoporosis in multiple sclerosis. Mult Scler 2010; 16(9): 1031–1043. Dostupné z DOI: <http://dx.doi.org/10.1177/1352458510368985>.
  83. Edwards MH, Jameson K, Denison H et al. Clinical risk factors, bone density and fall history in the prediction of incident fracture among men and women. Bone 2013; 52(2): 541–547. Dostupné z DOI: <http://dx.doi.org/10.1016/j.bone.2012.11.006>.
  84. Kanis JA, McCloskey E, Johansson H et al. FRAX (®) with and without bone mineral density. Calcif Tissue Int 2011; 90(1): 1–13. Dostupné z DOI: <http://dx.doi.org/10.1007/s00223–011–9544–7>.
  85. Binks S, Dobson R. Risk Factors, Epidemiology and Treatment Strategies for Metabolic Bone Disease in Patients with Neurological Disease. Curr Osteoporos Rep 2016; 14(5):199–210. Dostupné z DOI: <http://dx.doi.org/10.1007/s11914–016–0320–5>.
  86. Williams P, Frank A, Crawford CM et al. Unrecongised femoral fractures in patients with paraplegia due to multiple sclerosis. Br Med J (Clin Res Ed) 1984; 289(6443): 501.
  87. Raška I Jr, Týblová M, Rašková M et al. Omezená schopnost chůze významně přispívá k úbytku kostní denzity v proximálním femuru u premenopauzálních i postmenopauzálních žen s roztroušenou sklerózou. Osteologický bulletin 2012; 17(4): 128–135.
  88. Dalgas U, Stenager E, Jakobsen J et al. Resistance training improves muscle strength and functional capacity in multiple sclerosis. Neurology 2009; 73(18): 1478–1484. Dostupné z DOI: <http://dx.doi.org/10.1212/WNL.0b013e3181bf98b4>.
  89. Snook EM, Motl RW. Effect of exercise training on walking mobility in multiple sclerosis: a meta-analysis. Neurorehabil Neural Repair 2009; 23(2): 108–116. Dostupné z DOI: <http://dx.doi.org/10.1177/1545968308320641>.
  90. Ryan AS, Ivey FM, Hurlbut DE et al. Regional bone mineral density after resistive training in young and older men and women. Scand J Med Sci Sports 2004; 14(1): 16–23.
  91. Štěpán J. Osteoporóza a metabolická onemocnění skeletu. In: Pavelka K et al (eds). Revmatologie. Maxdorf: Praha 2012: 544–553. ISBN 978–80–7345–295–7.
  92. Krupa-Kozak U, Markiewicz LH, Lamparski G, Juśkiewicz J. Administration of Inulin-Supplemented Gluten-Free Diet Modified Calcium Absorption and Caecal Microbiota in Rats in a Calcium-Dependent Manner. Nutrients 2017; 9(7): pii:E702. Dostupné z DOI: <http://dx.doi.org/10.3390/nu9070702>.
  93. Wicherts IS, van Schoor NM, Boeke AJ et al. Vitamin D status predicts physical performance and its decline in older persons. J Clin Endocrinol Metab 2007; 92(6): 2058–2065. Dostupné z DOI: <http://dx.doi.org/10.1210/jc.2006–1525>.
  94. Bischoff-Ferrari HA, Dawson-Hughes B, Staehelin HB et al. Fall prevention with supplemental and active forms of vitamin D: a metaanalysis of randomised controlled trials. BMJ 2009; 339:b3692. Dostupné z DOI: <http://dx.doi.org/10.1136/bmj.b3692>.
  95. Tanner SB, Harwell SA. More than healthy bones: a review of vitamin D in muscle health. Ther Adv Musculoskelet Dis 2015; 7(4):152–159. Dostupné z DOI: <http://dx.doi.org/10.1177/1759720X15588521>.
  96. Bouillon R, Van Schoor NM, Gielen E et al. Optimal vitamin D status: a critical analysis on the basis of evidence-based medicine. J Clin Endocrinol Metab 2013; 98(8): E1283–1304. Dostupné z DOI: <http://dx.doi.org/10.1210/jc.2013–1195>.
  97. Rizzoli R, Boonen S, Brandi ML et al. Vitamin D supplementation in elderly or postmenopausal women: a 2013 update of the 2008 recommendations from the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO). Curr Med Res Opin 2013; 29(4): 305–313. Dostupné z DOI: <http://dx.doi.org/10.1185/03007995.2013.766162>.
  98. Lieben L, Carmeliet G. The delicate balance between vitamin D, calcium and bone homeostasis: lessons learned from intestinal- and osteocyte-specific VDR null mice. J Steroid Biochem Mol Biol 2013; 136: 102–106. Dostupné z DOI: <http://dx.doi.org/10.1016/j.jsbmb.2012.09.019>.
  99. Glendenning P, Inderjeeth CA. Controversy and consensus regarding vitamin D: Recent methodological changes and the risks and benefits of vitamin D supplementation. Crit Rev Clin Lab Sci 2016; 53(1):13–28. Dostupné z DOI: <http://dx.doi.org/10.3109/10408363.2015.1074157>.
  100. Hadgkiss EJ, Jelinek GA, Weiland TJ et al. The association of diet with quality of life, disability, and relapse rate in an international sample of people with multiple sclerosis. Nutr Neurosci 2015; 18(3):125–136. Dostupné z DOI: <http://dx.doi.org/10.1179/1476830514Y.0000000117>.
  101. Chu F, Shi M, Lang Y et al. Gut Microbiota in Multiple Sclerosis and Experimental Autoimmune Encephalomyelitis: Current Applications and Future Perspectives. Mediators Inflamm 2018; 2018:8168717.
  102. Marietta E, Horwath I, Balakrishnan B et al. Role of the intestinal microbiome in autoimmune diseases and its use in treatments. Cell Immunol 2018; pii: S0008–8749(18)30418–0. Dostupné z DOI: <http://dx.doi.org/10.1016/j.cellimm.2018.10.005>.
  103. Whisner CM, Castillo LF. Prebiotics, Bone and Mineral Metabolism. Calcif Tissue Int 2018; 102(4): 443–479. Dostupné z DOI: <http://dx.doi.org/10.1007/s00223–017–0339–3>.
  104. Biver E, Durosier-Izart C, Merminod F et al. Fermented dairy products consumption is associated with attenuated cortical bone loss independently of total calcium, protein, and energy intakes in healthy postmenopausal women. Osteoporos Int 2018; 29(8): 1771–1782. Dostupné z DOI: <http://dx.doi.org/10.1007/s00198–018–4535–4>.
  105. Seeliger C, Schyschka L, Kronbach Z et al. Signaling pathway STAT1 is strongly activated by IFN-β in the pathogenesis of osteoporosis. Eur J Med Res 2015; 20:1. Dostupné z DOI: <http://dx.doi.org/10.1186/s40001–014–0074–4>.
  106. Miyazaki Y, Niino M, Kanazawa I et al. Fingolimod sDostupné z DOI: uppresses bone resorption in female patients with multiple sclerosis. J Neuroimmunol 2016; 298: 24–31. Dostupné z DOI: <http://dx.doi.org/10.1016/j.jneuroim.2016.06.007>.
  107. Bubbear JS, Gall A, Middleton FR et al. Early treatment with zoledronic acid prevents bone loss at the hip following acute spinal cord injury. Osteoporos Int 2011; 22(1):271–279. Dostupné z DOI: <http://dx.doi.org/10.1007/s00198–010–1221–6>.
  108. Mok CC, Tong KH, To CH et al. Risedronate for prevention of bone mineral density loss in patients receiving high-dose glucocorticoids: a randomized double-blind placebo-controlled trial. Osteoporos Int 2008; 19(3): 357–364. Dostupné z DOI: <http://dx.doi.org/10.1007/s00198–007–0505-y>.
  109. Siu WS, Ko CH, Hung LK et al. Effect of anti-osteoporotic agents on the prevention of bone loss in unloaded bone. Mol Med Rep 2013, 8(4): 1188–1194. Dostupné z DOI: <http://dx.doi.org/10.3892/mmr.2013.1647>.
  110. Dempster D, Zhou HH, Recker RR et al. A longitudinal study of skeletal histomorphometry at 6 and 24 months across four bone envelopes in postmenopausal women with osteoporosis receiving teriparatide or zoledronic acid in the SHOTZ trial. J Bone Miner Res 2016; 31(7):1429–1439. Dostupné z DOI: <http://dx.doi.org/10.1002/jbmr.2804>.
  111. Lamy O, Gonzalez-Rodriguez E, Stoll D et al. Severe rebound-associated vertebral fractures after denosumab discontinuation: nine clinical cases report. J Clin Endocrinol Metab 2017; 102(2): 354–358. Dostupné z DOI: <http://dx.doi.org/10.1210/jc.2016–3170>.
  112. Saag KG, Zanchetta JR, Devogelaer JP et al. Effects of teriparatide versus alendronate for treating glucocorticoid-induced osteoporosis: thirty-six-month results of a randomized, double-blind, controlled trial. Arthritis Rheum 2009; 60(11): 3346–3355. Dostupné z DOI: <http://dx.doi.org/10.1002/art.24879>.
  113. Turner RT, Evans GL, Lotinun S et al. Dose-response effects of intermittent PTH on cancellous bone in hindlimb unloaded rats. J Bone Miner Res 2007; 22(1): 64–71. Dostupné z DOI: <http://dx.doi.org/10.1359/jbmr.061006>.
  114. Michalská D, Zikán V, Týblová M et al. Srovnání léčby teriparatidem a risedronatem v prevenci úbytku kostní hmoty u postmeno-pauzálních žen s roztroušenou sklerózou léčených nízkou dávkou glukokortikoidů. Osteologický Bulletin 2015; 20(1): 3–9.
  115. Cosman F, Crittenden DB, Adachi JD et al. Romosozumab Treatment in Postmenopausal Women with Osteoporosis. N Engl J Med 2016; 375(16): 1532–1543. Dostupné z DOI: <http://dx.doi.org/10.1056/NEJMoa1607948>.
  116. Tian X, Jee WS, Li X et al. Sclerostin antibody increases bone mass by stimulating bone formation and inhibiting bone resorption in a hindlimb-immobilization rat model. Bone 2011; 48(2): 197–201. Dostupné z DOI: <http://dx.doi.org/10.1016/j.bone.2010.09.009>.
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