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Published in: CNS Drugs 8/2014

01-08-2014 | Review Article

Osteoporosis and Multiple Sclerosis: Risk Factors, Pathophysiology, and Therapeutic Interventions

Authors: Sahil Gupta, Irfan Ahsan, Naeem Mahfooz, Noureldin Abdelhamid, Murali Ramanathan, Bianca Weinstock-Guttman

Published in: CNS Drugs | Issue 8/2014

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Abstract

Multiple sclerosis (MS) is a chronic inflammatory-demyelinating disease of the nervous system. There has been mounting evidence showing that MS is associated with increased risk of osteoporosis and fractures. The development of osteoporosis in MS patients can be related to the cumulative effects of various factors. This review summarizes the common risk factors and physiologic pathways that play a role in development of osteoporosis in MS patients. Physical inactivity and reduced mechanical load on the bones (offsetting gravity) is likely the major contributing factor for osteoporosis in MS. Additional possible factors leading to reduced bone mass are low vitamin D levels, and use of medications such as glucocorticoids and anticonvulsants. The role of the inflammatory processes related to the underlying disease is considered in the context of the complex bone metabolism. The known effect of different MS disease-modifying therapies on bone health is limited. An algorithm for diagnosis and management of osteoporosis in MS is proposed.
Literature
2.
go back to reference Sa MJ. Physiopathology of symptoms and signs in multiple sclerosis. Arq Neuropsiquiatr. 2012;70(9):733–40.PubMedCrossRef Sa MJ. Physiopathology of symptoms and signs in multiple sclerosis. Arq Neuropsiquiatr. 2012;70(9):733–40.PubMedCrossRef
3.
go back to reference Weinstock-Guttman B, et al. Risk of bone loss in men with multiple sclerosis. Mult Scler. 2004;10(2):170–5.PubMedCrossRef Weinstock-Guttman B, et al. Risk of bone loss in men with multiple sclerosis. Mult Scler. 2004;10(2):170–5.PubMedCrossRef
5.
go back to reference Zorzon M, et al. Long-term effects of intravenous high dose methylprednisolone pulses on bone mineral density in patients with multiple sclerosis. Eur J Neurol. 2005;12(7):550–6.PubMedCrossRef Zorzon M, et al. Long-term effects of intravenous high dose methylprednisolone pulses on bone mineral density in patients with multiple sclerosis. Eur J Neurol. 2005;12(7):550–6.PubMedCrossRef
7.
go back to reference Sioka C, Kyritsis AP, Fotopoulos A. Multiple sclerosis, osteoporosis, and vitamin D. J Neurol Sci. 2009;287(1–2):1–6.PubMedCrossRef Sioka C, Kyritsis AP, Fotopoulos A. Multiple sclerosis, osteoporosis, and vitamin D. J Neurol Sci. 2009;287(1–2):1–6.PubMedCrossRef
8.
9.
go back to reference Josyula S, et al. The nervous system’s potential role in multiple sclerosis associated bone loss. J Neurol Sci. 2012;319(1–2):8–14.PubMedCrossRef Josyula S, et al. The nervous system’s potential role in multiple sclerosis associated bone loss. J Neurol Sci. 2012;319(1–2):8–14.PubMedCrossRef
10.
11.
go back to reference Levis S, Theodore G. Summary of AHRQ’s comparative effectiveness review of treatment to prevent fractures in men and women with low bone density or osteoporosis: update of the 2007 report. J Manag Care Pharm. 2012;18(4 Suppl B):S1–15 (discussion S13).PubMed Levis S, Theodore G. Summary of AHRQ’s comparative effectiveness review of treatment to prevent fractures in men and women with low bone density or osteoporosis: update of the 2007 report. J Manag Care Pharm. 2012;18(4 Suppl B):S1–15 (discussion S13).PubMed
12.
go back to reference Cosman F, et al. Fracture history and bone loss in patients with MS. Neurology. 1998;51(4):1161–5.PubMedCrossRef Cosman F, et al. Fracture history and bone loss in patients with MS. Neurology. 1998;51(4):1161–5.PubMedCrossRef
13.
go back to reference Nieves J, et al. High prevalence of vitamin D deficiency and reduced bone mass in multiple sclerosis. Neurology. 1994;44(9):1687–92.PubMedCrossRef Nieves J, et al. High prevalence of vitamin D deficiency and reduced bone mass in multiple sclerosis. Neurology. 1994;44(9):1687–92.PubMedCrossRef
14.
go back to reference Ozgocmen S, 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):309–13.PubMedCrossRef Ozgocmen S, 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):309–13.PubMedCrossRef
15.
go back to reference Achiron A, et al. Bone strength in multiple sclerosis: cortical midtibial speed-of-sound assessment. Mult Scler. 2004;10(5):488–93.PubMedCrossRef Achiron A, et al. Bone strength in multiple sclerosis: cortical midtibial speed-of-sound assessment. Mult Scler. 2004;10(5):488–93.PubMedCrossRef
16.
go back to reference Moen SM, et al. Low bone mass in newly diagnosed multiple sclerosis and clinically isolated syndrome. Neurology. 2011;77(2):151–7.PubMedCrossRef Moen SM, et al. Low bone mass in newly diagnosed multiple sclerosis and clinically isolated syndrome. Neurology. 2011;77(2):151–7.PubMedCrossRef
17.
18.
19.
go back to reference Luis Neyro J, Jesus Cancelo M, Palacios S. Inhibition of RANK-L in the pathophysiology of osteoporosis. Clinical evidences of its use. Ginecol Obstet Mex. 2013;81(3):146–57.PubMed Luis Neyro J, Jesus Cancelo M, Palacios S. Inhibition of RANK-L in the pathophysiology of osteoporosis. Clinical evidences of its use. Ginecol Obstet Mex. 2013;81(3):146–57.PubMed
20.
go back to reference Negishi-Koga T, et al. Suppression of bone formation by osteoclastic expression of semaphorin 4D. Nat Med. 2011;17(11):1473–80.PubMedCrossRef Negishi-Koga T, et al. Suppression of bone formation by osteoclastic expression of semaphorin 4D. Nat Med. 2011;17(11):1473–80.PubMedCrossRef
22.
go back to reference Manolagas SC, Jilka RL. Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med. 1995;332(5):305–11.PubMedCrossRef Manolagas SC, Jilka RL. Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med. 1995;332(5):305–11.PubMedCrossRef
23.
24.
go back to reference Altintas A, et al. The role of osteopontin: a shared pathway in the pathogenesis of multiple sclerosis and osteoporosis? J Neurol Sci. 2009;276(1–2):41–4.PubMedCrossRef Altintas A, et al. The role of osteopontin: a shared pathway in the pathogenesis of multiple sclerosis and osteoporosis? J Neurol Sci. 2009;276(1–2):41–4.PubMedCrossRef
25.
go back to reference Vogt MH, et al. Increased osteopontin plasma levels in multiple sclerosis patients correlate with bone-specific markers. Mult Scler. 2010;16(4):443–9.PubMedCrossRef Vogt MH, et al. Increased osteopontin plasma levels in multiple sclerosis patients correlate with bone-specific markers. Mult Scler. 2010;16(4):443–9.PubMedCrossRef
26.
go back to reference Slavov GS, et al. Vitamin D immunomodulatory potential in multiple sclerosis. Folia Med (Plovdiv). 2013;55(2):5–9. Slavov GS, et al. Vitamin D immunomodulatory potential in multiple sclerosis. Folia Med (Plovdiv). 2013;55(2):5–9.
27.
go back to reference Munger KL, et al. Vitamin D intake and incidence of multiple sclerosis. Neurology. 2004;62(1):60–5.PubMedCrossRef Munger KL, et al. Vitamin D intake and incidence of multiple sclerosis. Neurology. 2004;62(1):60–5.PubMedCrossRef
28.
go back to reference George PM, et al. Pharmacology and therapeutic potential of interferons. Pharmacol Ther. 2012;135(1):44–53.PubMedCrossRef George PM, et al. Pharmacology and therapeutic potential of interferons. Pharmacol Ther. 2012;135(1):44–53.PubMedCrossRef
29.
go back to reference Abraham AK, et al. Mechanisms of interferon-beta effects on bone homeostasis. Biochem Pharmacol. 2009;77(12):1757–62.PubMedCrossRef Abraham AK, et al. Mechanisms of interferon-beta effects on bone homeostasis. Biochem Pharmacol. 2009;77(12):1757–62.PubMedCrossRef
30.
go back to reference Moen SM, et al. Bone turnover and metabolism in patients with early multiple sclerosis and prevalent bone mass deficit: a population-based case-control study. PLoS One. 2012;7(9):e45703.PubMedCentralPubMedCrossRef Moen SM, et al. Bone turnover and metabolism in patients with early multiple sclerosis and prevalent bone mass deficit: a population-based case-control study. PLoS One. 2012;7(9):e45703.PubMedCentralPubMedCrossRef
31.
go back to reference Thomas T, et al. Leptin acts on human marrow stromal cells to enhance differentiation to osteoblasts and to inhibit differentiation to adipocytes. Endocrinology. 1999;140(4):1630–8.PubMed Thomas T, et al. Leptin acts on human marrow stromal cells to enhance differentiation to osteoblasts and to inhibit differentiation to adipocytes. Endocrinology. 1999;140(4):1630–8.PubMed
32.
go back to reference Gordeladze JO, et al. Leptin stimulates human osteoblastic cell proliferation, de novo collagen synthesis, and mineralization: impact on differentiation markers, apoptosis, and osteoclastic signaling. J Cell Biochem. 2002;85(4):825–36.PubMedCrossRef Gordeladze JO, et al. Leptin stimulates human osteoblastic cell proliferation, de novo collagen synthesis, and mineralization: impact on differentiation markers, apoptosis, and osteoclastic signaling. J Cell Biochem. 2002;85(4):825–36.PubMedCrossRef
33.
go back to reference Ducy P, et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell. 2000;100(2):197–207.PubMedCrossRef Ducy P, et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell. 2000;100(2):197–207.PubMedCrossRef
35.
go back to reference Ruhl CE, et al. Body mass index and serum leptin concentration independently estimate percentage body fat in older adults. Am J Clin Nutr. 2007;85(4):1121–6.PubMed Ruhl CE, et al. Body mass index and serum leptin concentration independently estimate percentage body fat in older adults. Am J Clin Nutr. 2007;85(4):1121–6.PubMed
36.
go back to reference Friedman JM. The function of leptin in nutrition, weight, and physiology. Nutr Rev. 2002;60(10 Pt 2):S1–14 (discussion S68–84, 85–7).PubMedCrossRef Friedman JM. The function of leptin in nutrition, weight, and physiology. Nutr Rev. 2002;60(10 Pt 2):S1–14 (discussion S68–84, 85–7).PubMedCrossRef
37.
go back to reference Glauber HS, et al. Body weight versus body fat distribution, adiposity, and frame size as predictors of bone density. J Clin Endocrinol Metab. 1995;80(4):1118–23.PubMed Glauber HS, et al. Body weight versus body fat distribution, adiposity, and frame size as predictors of bone density. J Clin Endocrinol Metab. 1995;80(4):1118–23.PubMed
38.
go back to reference Wardlaw GM. Putting body weight and osteoporosis into perspective. Am J Clin Nutr. 1996;63(3 Suppl):433S–6S.PubMed Wardlaw GM. Putting body weight and osteoporosis into perspective. Am J Clin Nutr. 1996;63(3 Suppl):433S–6S.PubMed
39.
go back to reference Carlton ED, Demas GE, French SS. Leptin, a neuroendocrine mediator of immune responses, inflammation, and sickness behaviors. Horm Behav. 2012;62(3):272–9.PubMedCrossRef Carlton ED, Demas GE, French SS. Leptin, a neuroendocrine mediator of immune responses, inflammation, and sickness behaviors. Horm Behav. 2012;62(3):272–9.PubMedCrossRef
40.
go back to reference Yadav VK, et al. A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure. Cell. 2009;138(5):976–89.PubMedCentralPubMedCrossRef Yadav VK, et al. A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure. Cell. 2009;138(5):976–89.PubMedCentralPubMedCrossRef
41.
42.
go back to reference De Rosa V, et al. Leptin neutralization interferes with pathogenic T cell autoreactivity in autoimmune encephalomyelitis. J Clin Invest. 2006;116(2):447–55.PubMedCentralPubMedCrossRef De Rosa V, et al. Leptin neutralization interferes with pathogenic T cell autoreactivity in autoimmune encephalomyelitis. J Clin Invest. 2006;116(2):447–55.PubMedCentralPubMedCrossRef
43.
go back to reference Matarese G, et al. Requirement for leptin in the induction and progression of autoimmune encephalomyelitis. J Immunol. 2001;166(10):5909–16.PubMedCrossRef Matarese G, et al. Requirement for leptin in the induction and progression of autoimmune encephalomyelitis. J Immunol. 2001;166(10):5909–16.PubMedCrossRef
44.
go back to reference Budhiraja S, Chugh A. Neuromedin U: physiology, pharmacology and therapeutic potential. Fund Clin Pharmacol. 2009;23(2):149–57.CrossRef Budhiraja S, Chugh A. Neuromedin U: physiology, pharmacology and therapeutic potential. Fund Clin Pharmacol. 2009;23(2):149–57.CrossRef
45.
46.
go back to reference Shi YC, Baldock PA. Central and peripheral mechanisms of the NPY system in the regulation of bone and adipose tissue. Bone. 2012;50(2):430–6.PubMedCrossRef Shi YC, Baldock PA. Central and peripheral mechanisms of the NPY system in the regulation of bone and adipose tissue. Bone. 2012;50(2):430–6.PubMedCrossRef
47.
go back to reference Khor EC, Baldock P. The NPY system and its neural and neuroendocrine regulation of bone. Curr Osteoporos Rep. 2012;10(2):160–8.PubMedCrossRef Khor EC, Baldock P. The NPY system and its neural and neuroendocrine regulation of bone. Curr Osteoporos Rep. 2012;10(2):160–8.PubMedCrossRef
48.
go back to reference Inose H, et al. Efficacy of serotonin inhibition in mouse models of bone loss. J Bone Miner Res. 2011;26(9):2002–11.PubMedCrossRef Inose H, et al. Efficacy of serotonin inhibition in mouse models of bone loss. J Bone Miner Res. 2011;26(9):2002–11.PubMedCrossRef
49.
go back to reference Karsenty G, Yadav VK. Regulation of bone mass by serotonin: molecular biology and therapeutic implications. Annu Rev Med. 2011;62:323–31.PubMedCrossRef Karsenty G, Yadav VK. Regulation of bone mass by serotonin: molecular biology and therapeutic implications. Annu Rev Med. 2011;62:323–31.PubMedCrossRef
50.
go back to reference Yuan XQ, et al. Fluoxetine promotes remission in acute experimental autoimmune encephalomyelitis in rats. Neuroimmunomodulation. 2012;19(4):201–8.PubMedCrossRef Yuan XQ, et al. Fluoxetine promotes remission in acute experimental autoimmune encephalomyelitis in rats. Neuroimmunomodulation. 2012;19(4):201–8.PubMedCrossRef
51.
go back to reference Elefteriou F, et al. Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature. 2005;434(7032):514–20.PubMedCrossRef Elefteriou F, et al. Leptin regulation of bone resorption by the sympathetic nervous system and CART. Nature. 2005;434(7032):514–20.PubMedCrossRef
52.
go back to reference Shi Y, et al. Signaling through the M(3) muscarinic receptor favors bone mass accrual by decreasing sympathetic activity. Cell Metab. 2010;11(3):231–8.PubMedCentralPubMedCrossRef Shi Y, et al. Signaling through the M(3) muscarinic receptor favors bone mass accrual by decreasing sympathetic activity. Cell Metab. 2010;11(3):231–8.PubMedCentralPubMedCrossRef
53.
go back to reference Smith CJ, Fischer TH. Particulate and vapor phase constituents of cigarette mainstream smoke and risk of myocardial infarction. Atherosclerosis. 2001;158(2):257–67.PubMedCrossRef Smith CJ, Fischer TH. Particulate and vapor phase constituents of cigarette mainstream smoke and risk of myocardial infarction. Atherosclerosis. 2001;158(2):257–67.PubMedCrossRef
54.
go back to reference Didilescu AC, et al. The role of smoking in changing essential parameters in body homeostasis. Pneumologia. 2009;58(2):89–94.PubMed Didilescu AC, et al. The role of smoking in changing essential parameters in body homeostasis. Pneumologia. 2009;58(2):89–94.PubMed
55.
go back to reference Emre M, de Decker C. Effects of cigarette smoking on motor functions in patients with multiple sclerosis. Arch Neurol. 1992;49(12):1243–7.PubMedCrossRef Emre M, de Decker C. Effects of cigarette smoking on motor functions in patients with multiple sclerosis. Arch Neurol. 1992;49(12):1243–7.PubMedCrossRef
56.
57.
go back to reference Manouchehrinia A, et al. Tobacco smoking and disability progression in multiple sclerosis: United Kingdom cohort study. Brain. 2013;136(Pt 7):2298–304.PubMedCentralPubMedCrossRef Manouchehrinia A, et al. Tobacco smoking and disability progression in multiple sclerosis: United Kingdom cohort study. Brain. 2013;136(Pt 7):2298–304.PubMedCentralPubMedCrossRef
58.
go back to reference Hernan MA, Olek MJ, Ascherio A. Cigarette smoking and incidence of multiple sclerosis. Am J Epidemiol. 2001;154(1):69–74.PubMedCrossRef Hernan MA, Olek MJ, Ascherio A. Cigarette smoking and incidence of multiple sclerosis. Am J Epidemiol. 2001;154(1):69–74.PubMedCrossRef
59.
go back to reference Brot C, Jorgensen NR, Sorensen OH. The influence of smoking on vitamin D status and calcium metabolism. Eur J Clin Nutr. 1999;53(12):920–6.PubMedCrossRef Brot C, Jorgensen NR, Sorensen OH. The influence of smoking on vitamin D status and calcium metabolism. Eur J Clin Nutr. 1999;53(12):920–6.PubMedCrossRef
60.
go back to reference Fini M, et al. Role of obesity, alcohol and smoking on bone health. Front Biosci (Elite Ed). 2012;4:2686–706.CrossRef Fini M, et al. Role of obesity, alcohol and smoking on bone health. Front Biosci (Elite Ed). 2012;4:2686–706.CrossRef
61.
go back to reference Borer KT. Physical activity in the prevention and amelioration of osteoporosis in women: interaction of mechanical, hormonal and dietary factors. Sports Med. 2005;35(9):779–830.PubMedCrossRef Borer KT. Physical activity in the prevention and amelioration of osteoporosis in women: interaction of mechanical, hormonal and dietary factors. Sports Med. 2005;35(9):779–830.PubMedCrossRef
62.
go back to reference Mojtahedi MC, et al. Bone health in ambulatory individuals with multiple sclerosis: impact of physical activity, glucocorticoid use, and body composition. J Rehabil Res Dev. 2008;45(6):851–61.PubMedCrossRef Mojtahedi MC, et al. Bone health in ambulatory individuals with multiple sclerosis: impact of physical activity, glucocorticoid use, and body composition. J Rehabil Res Dev. 2008;45(6):851–61.PubMedCrossRef
63.
go back to reference Steffensen LH, Mellgren SI, Kampman MT. Predictors and prevalence of low bone mineral density in fully ambulatory persons with multiple sclerosis. J Neurol. 2010;257(3):410–8.PubMedCrossRef Steffensen LH, Mellgren SI, Kampman MT. Predictors and prevalence of low bone mineral density in fully ambulatory persons with multiple sclerosis. J Neurol. 2010;257(3):410–8.PubMedCrossRef
64.
go back to reference De Nijs RN. Glucocorticoid-induced osteoporosis: a review on pathophysiology and treatment options. Minerva Med. 2008;99(1):23–43.PubMed De Nijs RN. Glucocorticoid-induced osteoporosis: a review on pathophysiology and treatment options. Minerva Med. 2008;99(1):23–43.PubMed
65.
go back to reference Dovio A, 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):4923–8.PubMedCrossRef Dovio A, 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):4923–8.PubMedCrossRef
66.
go back to reference Tuzun S, et al. Bone status in multiple sclerosis: beyond corticosteroids. Mult Scler. 2003;9(6):600–4.PubMedCrossRef Tuzun S, et al. Bone status in multiple sclerosis: beyond corticosteroids. Mult Scler. 2003;9(6):600–4.PubMedCrossRef
67.
go back to reference Schwid SR, et al. Sporadic corticosteroid pulses and osteoporosis in multiple sclerosis. Arch Neurol. 1996;53(8):753–7.PubMedCrossRef Schwid SR, et al. Sporadic corticosteroid pulses and osteoporosis in multiple sclerosis. Arch Neurol. 1996;53(8):753–7.PubMedCrossRef
68.
go back to reference Olafsson E, Benedikz J, Hauser WA. Risk of epilepsy in patients with multiple sclerosis: a population-based study in Iceland. Epilepsia. 1999;40(6):745–7.PubMedCrossRef Olafsson E, Benedikz J, Hauser WA. Risk of epilepsy in patients with multiple sclerosis: a population-based study in Iceland. Epilepsia. 1999;40(6):745–7.PubMedCrossRef
70.
go back to reference Petty SJ, et al. Effect of antiepileptic medication on bone mineral measures. Neurology. 2005;65(9):1358–65.PubMedCrossRef Petty SJ, et al. Effect of antiepileptic medication on bone mineral measures. Neurology. 2005;65(9):1358–65.PubMedCrossRef
71.
go back to reference Lee RH, Lyles KW, Colon-Emeric C. A review of the effect of anticonvulsant medications on bone mineral density and fracture risk. Am J Geriatr Pharmacother. 2010;8(1):34–46.PubMedCentralPubMedCrossRef Lee RH, Lyles KW, Colon-Emeric C. A review of the effect of anticonvulsant medications on bone mineral density and fracture risk. Am J Geriatr Pharmacother. 2010;8(1):34–46.PubMedCentralPubMedCrossRef
73.
go back to reference Solaro C, Trabucco E, Messmer Uccelli M. Pain and multiple sclerosis: pathophysiology and treatment. Curr Neurol Neurosci Rep. 2013;13(1):320.PubMedCrossRef Solaro C, Trabucco E, Messmer Uccelli M. Pain and multiple sclerosis: pathophysiology and treatment. Curr Neurol Neurosci Rep. 2013;13(1):320.PubMedCrossRef
74.
75.
go back to reference Elhassan AM, et al. Methionine-enkephalin in bone and joint tissues. J Bone Miner Res. 1998;13(1):88–95.PubMedCrossRef Elhassan AM, et al. Methionine-enkephalin in bone and joint tissues. J Bone Miner Res. 1998;13(1):88–95.PubMedCrossRef
76.
go back to reference Loskutova N, et al. Bone density and brain atrophy in early Alzheimer’s disease. J Alzheimers Dis. 2009;18(4):777–85.PubMedCentralPubMed Loskutova N, et al. Bone density and brain atrophy in early Alzheimer’s disease. J Alzheimers Dis. 2009;18(4):777–85.PubMedCentralPubMed
77.
go back to reference Batista S, et al. Cognitive impairment is associated with reduced bone mass in multiple sclerosis. Mult Scler. 2012;18(10):1459–65.PubMedCrossRef Batista S, et al. Cognitive impairment is associated with reduced bone mass in multiple sclerosis. Mult Scler. 2012;18(10):1459–65.PubMedCrossRef
78.
go back to reference Shuhaibar M, et al. Favorable effect of immunomodulator therapy on bone mineral density in multiple sclerosis. Ir J Med Sci. 2009;178(1):43–5.PubMedCrossRef Shuhaibar M, et al. Favorable effect of immunomodulator therapy on bone mineral density in multiple sclerosis. Ir J Med Sci. 2009;178(1):43–5.PubMedCrossRef
79.
go back to reference Weinstock-Guttman B, et al. Interferon-beta modulates bone-associated cytokines and osteoclast precursor activity in multiple sclerosis patients. Mult Scler. 2006;12(5):541–50.PubMedCrossRef Weinstock-Guttman B, et al. Interferon-beta modulates bone-associated cytokines and osteoclast precursor activity in multiple sclerosis patients. Mult Scler. 2006;12(5):541–50.PubMedCrossRef
82.
go back to reference Sato C, et al. Sphingosine 1-phosphate receptor activation enhances BMP-2-induced osteoblast differentiation. Biochem Biophys Res Commun. 2012;423(1):200–5.PubMedCrossRef Sato C, et al. Sphingosine 1-phosphate receptor activation enhances BMP-2-induced osteoblast differentiation. Biochem Biophys Res Commun. 2012;423(1):200–5.PubMedCrossRef
83.
86.
go back to reference Dennison EM, et al. Effect of co-morbidities on fracture risk: findings from the global longitudinal study of osteoporosis in women (GLOW). Bone. 2012;50(6):1288–93.PubMedCrossRef Dennison EM, et al. Effect of co-morbidities on fracture risk: findings from the global longitudinal study of osteoporosis in women (GLOW). Bone. 2012;50(6):1288–93.PubMedCrossRef
87.
88.
go back to reference Sundstrom P, Salzer J. Vitamin D and multiple sclerosis: timing of sampling, treatment and prevention. Biomark Med. 2013;7(2):193–5.PubMedCrossRef Sundstrom P, Salzer J. Vitamin D and multiple sclerosis: timing of sampling, treatment and prevention. Biomark Med. 2013;7(2):193–5.PubMedCrossRef
89.
90.
91.
go back to reference Ascherio A, et al. Vitamin D as an early predictor of multiple sclerosis activity and progression. JAMA Neurol. 2014;71(3):306–14.PubMedCrossRef Ascherio A, et al. Vitamin D as an early predictor of multiple sclerosis activity and progression. JAMA Neurol. 2014;71(3):306–14.PubMedCrossRef
92.
go back to reference Kmietowicz Z. NICE publishes osteoporosis guidance after more than six years of consultation. BMJ. 2008;337:a2397.PubMedCrossRef Kmietowicz Z. NICE publishes osteoporosis guidance after more than six years of consultation. BMJ. 2008;337:a2397.PubMedCrossRef
94.
go back to reference McClung MR, Grauer A, Boonen S, et al. Romosozumab in postmenopausal women with low bone mineral density. N Engl J Med. 2014; 370(5):412-20 McClung MR, Grauer A, Boonen S, et al. Romosozumab in postmenopausal women with low bone mineral density. N Engl J Med. 2014; 370(5):412-20
95.
go back to reference Cummings SR, et al. Lasofoxifene in postmenopausal women with osteoporosis. N Engl J Med. 2010;362(8):686–96.PubMedCrossRef Cummings SR, et al. Lasofoxifene in postmenopausal women with osteoporosis. N Engl J Med. 2010;362(8):686–96.PubMedCrossRef
96.
go back to reference Trojano M, et al. The transition from relapsing-remitting MS to irreversible disability: clinical evaluation. Neurol Sci. 2003;24(Suppl 5):S268–70.PubMedCrossRef Trojano M, et al. The transition from relapsing-remitting MS to irreversible disability: clinical evaluation. Neurol Sci. 2003;24(Suppl 5):S268–70.PubMedCrossRef
97.
go back to reference Lenart BA, Lorich DG, Lane JM. Atypical fractures of the femoral diaphysis in postmenopausal women taking alendronate. N Engl J Med. 2008;358(12):1304–6.PubMedCrossRef Lenart BA, Lorich DG, Lane JM. Atypical fractures of the femoral diaphysis in postmenopausal women taking alendronate. N Engl J Med. 2008;358(12):1304–6.PubMedCrossRef
98.
go back to reference Black DM, et al. Bisphosphonates and fractures of the subtrochanteric or diaphyseal femur. N Engl J Med. 2010;362(19):1761–71.PubMedCrossRef Black DM, et al. Bisphosphonates and fractures of the subtrochanteric or diaphyseal femur. N Engl J Med. 2010;362(19):1761–71.PubMedCrossRef
99.
go back to reference Odvina CV, et al. Unusual mid-shaft fractures during long-term bisphosphonate therapy. Clin Endocrinol. 2010;72(2):161–8.CrossRef Odvina CV, et al. Unusual mid-shaft fractures during long-term bisphosphonate therapy. Clin Endocrinol. 2010;72(2):161–8.CrossRef
100.
go back to reference Shane E, et al. Atypical subtrochanteric and diaphyseal femoral fractures: second report of a task force of the American society for bone and mineral research. J Bone Miner Res. 2014;29(1):1–23.PubMedCrossRef Shane E, et al. Atypical subtrochanteric and diaphyseal femoral fractures: second report of a task force of the American society for bone and mineral research. J Bone Miner Res. 2014;29(1):1–23.PubMedCrossRef
101.
go back to reference Formica CA, 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):129–33.PubMedCrossRef Formica CA, 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):129–33.PubMedCrossRef
Metadata
Title
Osteoporosis and Multiple Sclerosis: Risk Factors, Pathophysiology, and Therapeutic Interventions
Authors
Sahil Gupta
Irfan Ahsan
Naeem Mahfooz
Noureldin Abdelhamid
Murali Ramanathan
Bianca Weinstock-Guttman
Publication date
01-08-2014
Publisher
Springer International Publishing
Published in
CNS Drugs / Issue 8/2014
Print ISSN: 1172-7047
Electronic ISSN: 1179-1934
DOI
https://doi.org/10.1007/s40263-014-0173-3

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