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Published in: Journal of Neuroinflammation 1/2011

Open Access 01-12-2011 | Research

Serum lipid profiles are associated with disability and MRI outcomes in multiple sclerosis

Authors: Bianca Weinstock-Guttman, Robert Zivadinov, Naeem Mahfooz, Ellen Carl, Allison Drake, Jaclyn Schneider, Barbara Teter, Sara Hussein, Bijal Mehta, Marc Weiskopf, Jacqueline Durfee, Niels Bergsland, Murali Ramanathan

Published in: Journal of Neuroinflammation | Issue 1/2011

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Abstract

Background

The breakdown of the blood-brain-barrier vascular endothelium is critical for entry of immune cells into the MS brain. Vascular co-morbidities are associated with increased risk of progression. Dyslipidemia, elevated LDL and reduced HDL may increase progression by activating inflammatory processes at the vascular endothelium.

Objective

To assess the associations of serum lipid profile variables (triglycerides, high and low density lipoproteins (HDL, LDL) and total cholesterol) with disability and MRI measures in multiple sclerosis (MS).

Methods

This study included 492 MS patients (age: 47.1 ± 10.8 years; disease duration: 12.8 ± 10.1 years) with baseline and follow-up Expanded Disability Status Score (EDSS) assessments after a mean period of 2.2 ± 1.0 years. The associations of baseline lipid profile variables with disability changes were assessed. Quantitative MRI findings at baseline were available for 210 patients.

Results

EDSS worsening was associated with higher baseline LDL (p = 0.006) and total cholesterol (p = 0.001, 0.008) levels, with trends for higher triglyceride (p = 0.025); HDL was not associated. A similar pattern was found for MSSS worsening. Higher HDL levels (p < 0.001) were associated with lower contrast-enhancing lesion volume. Higher total cholesterol was associated with a trend for lower brain parenchymal fraction (p = 0.033).

Conclusions

Serum lipid profile has modest effects on disease progression in MS. Worsening disability is associated with higher levels of LDL, total cholesterol and triglycerides. Higher HDL is associated with lower levels of acute inflammatory activity.
Appendix
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Literature
1.
go back to reference Frohman EM, Racke MK, Raine CS: Multiple sclerosis--the plaque and its pathogenesis. N Engl J Med. 2006, 354: 942-955. 10.1056/NEJMra052130.CrossRefPubMed Frohman EM, Racke MK, Raine CS: Multiple sclerosis--the plaque and its pathogenesis. N Engl J Med. 2006, 354: 942-955. 10.1056/NEJMra052130.CrossRefPubMed
2.
go back to reference Lucchinetti CF, Bruck W, Lassmann H: Evidence for pathogenic heterogeneity in multiple sclerosis. Ann Neurol. 2004, 56: 308-10.1002/ana.20182.CrossRefPubMed Lucchinetti CF, Bruck W, Lassmann H: Evidence for pathogenic heterogeneity in multiple sclerosis. Ann Neurol. 2004, 56: 308-10.1002/ana.20182.CrossRefPubMed
3.
go back to reference Gotthardt M, Trommsdorff M, Nevitt MF, Shelton J, Richardson JA, Stockinger W, Nimpf J, Herz J: Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J Biol Chem. 2000, 275: 25616-25624. 10.1074/jbc.M000955200.CrossRefPubMed Gotthardt M, Trommsdorff M, Nevitt MF, Shelton J, Richardson JA, Stockinger W, Nimpf J, Herz J: Interactions of the low density lipoprotein receptor gene family with cytosolic adaptor and scaffold proteins suggest diverse biological functions in cellular communication and signal transduction. J Biol Chem. 2000, 275: 25616-25624. 10.1074/jbc.M000955200.CrossRefPubMed
4.
go back to reference Stockinger W, Brandes C, Fasching D, Hermann M, Gotthardt M, Herz J, Schneider WJ, Nimpf J: The reelin receptor ApoER2 recruits JNK-interacting proteins-1 and -2. J Biol Chem. 2000, 275: 25625-25632. 10.1074/jbc.M004119200.CrossRefPubMed Stockinger W, Brandes C, Fasching D, Hermann M, Gotthardt M, Herz J, Schneider WJ, Nimpf J: The reelin receptor ApoER2 recruits JNK-interacting proteins-1 and -2. J Biol Chem. 2000, 275: 25625-25632. 10.1074/jbc.M004119200.CrossRefPubMed
5.
go back to reference Roheim PS, Carey M, Forte T, Vega GL: Apolipoproteins in human cerebrospinal fluid. Proc Natl Acad Sci USA. 1979, 76: 4646-4649. 10.1073/pnas.76.9.4646.PubMedCentralCrossRefPubMed Roheim PS, Carey M, Forte T, Vega GL: Apolipoproteins in human cerebrospinal fluid. Proc Natl Acad Sci USA. 1979, 76: 4646-4649. 10.1073/pnas.76.9.4646.PubMedCentralCrossRefPubMed
6.
go back to reference Borghini I, Barja F, Pometta D, James RW: Characterization of subpopulations of lipoprotein particles isolated from human cerebrospinal fluid. Biochim Biophys Acta. 1995, 1255: 192-200.CrossRefPubMed Borghini I, Barja F, Pometta D, James RW: Characterization of subpopulations of lipoprotein particles isolated from human cerebrospinal fluid. Biochim Biophys Acta. 1995, 1255: 192-200.CrossRefPubMed
7.
go back to reference Mockel B, Zinke H, Flach R, Weiss B, Weiler-Guttler H, Gassen HG: Expression of apolipoprotein A-I in porcine brain endothelium in vitro. J Neurochem. 1994, 62: 788-798.CrossRefPubMed Mockel B, Zinke H, Flach R, Weiss B, Weiler-Guttler H, Gassen HG: Expression of apolipoprotein A-I in porcine brain endothelium in vitro. J Neurochem. 1994, 62: 788-798.CrossRefPubMed
8.
go back to reference Assmann G, Gotto AM: HDL cholesterol and protective factors in atherosclerosis. Circulation. 2004, 109: III8-14.CrossRefPubMed Assmann G, Gotto AM: HDL cholesterol and protective factors in atherosclerosis. Circulation. 2004, 109: III8-14.CrossRefPubMed
9.
go back to reference Burger D, Dayer JM: High-density lipoprotein-associated apolipoprotein A-I: the missing link between infection and chronic inflammation?. Autoimmun Rev. 2002, 1: 111-117. 10.1016/S1568-9972(01)00018-0.CrossRefPubMed Burger D, Dayer JM: High-density lipoprotein-associated apolipoprotein A-I: the missing link between infection and chronic inflammation?. Autoimmun Rev. 2002, 1: 111-117. 10.1016/S1568-9972(01)00018-0.CrossRefPubMed
10.
go back to reference Scanu A, Molnarfi N, Brandt KJ, Gruaz L, Dayer JM, Burger D: Stimulated T cells generate microparticles, which mimic cellular contact activation of human monocytes: differential regulation of pro- and anti-inflammatory cytokine production by high-density lipoproteins. J Leukoc Biol. 2008, 83: 921-927. 10.1189/jlb.0807551.CrossRefPubMed Scanu A, Molnarfi N, Brandt KJ, Gruaz L, Dayer JM, Burger D: Stimulated T cells generate microparticles, which mimic cellular contact activation of human monocytes: differential regulation of pro- and anti-inflammatory cytokine production by high-density lipoproteins. J Leukoc Biol. 2008, 83: 921-927. 10.1189/jlb.0807551.CrossRefPubMed
11.
go back to reference Ferretti G, Bacchetti T, Principi F, Di Ludovico F, Viti B, Angeleri VA, Danni M, Provinciali L: Increased levels of lipid hydroperoxides in plasma of patients with multiple sclerosis: a relationship with paraoxonase activity. Mult Scler. 2005, 11: 677-682. 10.1191/1352458505ms1240oa.CrossRefPubMed Ferretti G, Bacchetti T, Principi F, Di Ludovico F, Viti B, Angeleri VA, Danni M, Provinciali L: Increased levels of lipid hydroperoxides in plasma of patients with multiple sclerosis: a relationship with paraoxonase activity. Mult Scler. 2005, 11: 677-682. 10.1191/1352458505ms1240oa.CrossRefPubMed
12.
go back to reference Jamroz-Wisniewska A, Beltowski J, Stelmasiak Z, Bartosik-Psujek H: Paraoxonase 1 activity in different types of multiple sclerosis. Mult Scler. 2009, 15: 399-402. 10.1177/1352458508098371.CrossRefPubMed Jamroz-Wisniewska A, Beltowski J, Stelmasiak Z, Bartosik-Psujek H: Paraoxonase 1 activity in different types of multiple sclerosis. Mult Scler. 2009, 15: 399-402. 10.1177/1352458508098371.CrossRefPubMed
13.
go back to reference Cybulsky MI, Gimbrone MA: Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis. Science. 1991, 251: 788-791. 10.1126/science.1990440.CrossRefPubMed Cybulsky MI, Gimbrone MA: Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis. Science. 1991, 251: 788-791. 10.1126/science.1990440.CrossRefPubMed
14.
go back to reference Sitia S, Tomasoni L, Atzeni F, Ambrosio G, Cordiano C, Catapano A, Tramontana S, Perticone F, Naccarato P, Camici P, et al: From endothelial dysfunction to atherosclerosis. Autoimmun Rev. 2010, 9: 830-834. 10.1016/j.autrev.2010.07.016.CrossRefPubMed Sitia S, Tomasoni L, Atzeni F, Ambrosio G, Cordiano C, Catapano A, Tramontana S, Perticone F, Naccarato P, Camici P, et al: From endothelial dysfunction to atherosclerosis. Autoimmun Rev. 2010, 9: 830-834. 10.1016/j.autrev.2010.07.016.CrossRefPubMed
15.
go back to reference Stokes KY, Calahan L, Hamric CM, Russell JM, Granger DN: CD40/CD40L contributes to hypercholesterolemia-induced microvascular inflammation. Am J Physiol Heart Circ Physiol. 2009, 296: H689-697. 10.1152/ajpheart.00962.2008.PubMedCentralCrossRefPubMed Stokes KY, Calahan L, Hamric CM, Russell JM, Granger DN: CD40/CD40L contributes to hypercholesterolemia-induced microvascular inflammation. Am J Physiol Heart Circ Physiol. 2009, 296: H689-697. 10.1152/ajpheart.00962.2008.PubMedCentralCrossRefPubMed
16.
go back to reference Esteve E, Ricart W, Fernandez-Real JM: Dyslipidemia and inflammation: an evolutionary conserved mechanism. Clin Nutr. 2005, 24: 16-31. 10.1016/j.clnu.2004.08.004.CrossRefPubMed Esteve E, Ricart W, Fernandez-Real JM: Dyslipidemia and inflammation: an evolutionary conserved mechanism. Clin Nutr. 2005, 24: 16-31. 10.1016/j.clnu.2004.08.004.CrossRefPubMed
17.
go back to reference Torres A, Askari AD, Malemud CJ: Cardiovascular disease complications in systemic lupus erythematosus. Biomark Med. 2009, 3: 239-252. 10.2217/bmm.09.14.CrossRefPubMed Torres A, Askari AD, Malemud CJ: Cardiovascular disease complications in systemic lupus erythematosus. Biomark Med. 2009, 3: 239-252. 10.2217/bmm.09.14.CrossRefPubMed
18.
go back to reference Boyer JF, Gourraud PA, Cantagrel A, Davignon JL, Constantin A: Traditional cardiovascular risk factors in rheumatoid arthritis: A meta-analysis. Joint Bone Spine. 2010 Boyer JF, Gourraud PA, Cantagrel A, Davignon JL, Constantin A: Traditional cardiovascular risk factors in rheumatoid arthritis: A meta-analysis. Joint Bone Spine. 2010
19.
go back to reference von Eckardstein A, Sibler RA: Possible contributions of lipoproteins and cholesterol to the pathogenesis of diabetes mellitus type 2. Curr Opin Lipidol. 2010 von Eckardstein A, Sibler RA: Possible contributions of lipoproteins and cholesterol to the pathogenesis of diabetes mellitus type 2. Curr Opin Lipidol. 2010
20.
go back to reference Li Y, Wang H, Hu X, Peng F, Yang Y: Serum lipoprotein levels in patients with neuromyelitis optica elevated but had little correlation with clinical presentations. Clin Neurol Neurosurg. 2010, 112: 478-481. 10.1016/j.clineuro.2010.03.017.CrossRefPubMed Li Y, Wang H, Hu X, Peng F, Yang Y: Serum lipoprotein levels in patients with neuromyelitis optica elevated but had little correlation with clinical presentations. Clin Neurol Neurosurg. 2010, 112: 478-481. 10.1016/j.clineuro.2010.03.017.CrossRefPubMed
21.
go back to reference Giubilei F, Antonini G, Di Legge S, Sormani MP, Pantano P, Antonini R, Sepe-Monti M, Caramia F, Pozzilli C: Blood cholesterol and MRI activity in first clinical episode suggestive of multiple sclerosis. Acta Neurol Scand. 2002, 106: 109-112.CrossRefPubMed Giubilei F, Antonini G, Di Legge S, Sormani MP, Pantano P, Antonini R, Sepe-Monti M, Caramia F, Pozzilli C: Blood cholesterol and MRI activity in first clinical episode suggestive of multiple sclerosis. Acta Neurol Scand. 2002, 106: 109-112.CrossRefPubMed
22.
go back to reference Marrie RA, Rudick R, Horwitz R, Cutter G, Tyry T, Campagnolo D, Vollmer T: Vascular comorbidity is associated with more rapid disability progression in multiple sclerosis. Neurology. 2010, 74: 1041-1047. 10.1212/WNL.0b013e3181d6b125.PubMedCentralCrossRefPubMed Marrie RA, Rudick R, Horwitz R, Cutter G, Tyry T, Campagnolo D, Vollmer T: Vascular comorbidity is associated with more rapid disability progression in multiple sclerosis. Neurology. 2010, 74: 1041-1047. 10.1212/WNL.0b013e3181d6b125.PubMedCentralCrossRefPubMed
23.
go back to reference McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, Lublin FD, McFarland HF, Paty DW, Polman CH, Reingold SC, et al: Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol. 2001, 50: 121-127. 10.1002/ana.1032.CrossRefPubMed McDonald WI, Compston A, Edan G, Goodkin D, Hartung HP, Lublin FD, McFarland HF, Paty DW, Polman CH, Reingold SC, et al: Recommended diagnostic criteria for multiple sclerosis: guidelines from the International Panel on the diagnosis of multiple sclerosis. Ann Neurol. 2001, 50: 121-127. 10.1002/ana.1032.CrossRefPubMed
24.
go back to reference Zivadinov R, Reder AT, Filippi M, Minagar A, Stuve O, Lassmann H, Racke MK, Dwyer MG, Frohman EM, Khan O: Mechanisms of action of disease-modifying agents and brain volume changes in multiple sclerosis. Neurology. 2008, 71: 136-144. 10.1212/01.wnl.0000316810.01120.05.CrossRefPubMed Zivadinov R, Reder AT, Filippi M, Minagar A, Stuve O, Lassmann H, Racke MK, Dwyer MG, Frohman EM, Khan O: Mechanisms of action of disease-modifying agents and brain volume changes in multiple sclerosis. Neurology. 2008, 71: 136-144. 10.1212/01.wnl.0000316810.01120.05.CrossRefPubMed
25.
go back to reference Zivadinov R, Weinstock-Guttman B, Zorzon M, Uxa L, Serafin M, Bosco A, Bratina A, Maggiore C, Grop A, Tommasi MA, et al: Gene-environment interactions between HLA B7/A2, EBV antibodies are associated with MRI injury in multiple sclerosis. J Neuroimmunol. 2009, 209: 123-130. 10.1016/j.jneuroim.2009.01.023.CrossRefPubMed Zivadinov R, Weinstock-Guttman B, Zorzon M, Uxa L, Serafin M, Bosco A, Bratina A, Maggiore C, Grop A, Tommasi MA, et al: Gene-environment interactions between HLA B7/A2, EBV antibodies are associated with MRI injury in multiple sclerosis. J Neuroimmunol. 2009, 209: 123-130. 10.1016/j.jneuroim.2009.01.023.CrossRefPubMed
26.
go back to reference Zivadinov R, Weinstock-Guttman B, Hashmi K, Abdelrahman N, Stosic M, Dwyer M, Hussein S, Durfee J, Ramanathan M: Smoking is associated with increased lesion volumes and brain atrophy in multiple sclerosis. Neurology. 2009, 73: 504-510. 10.1212/WNL.0b013e3181b2a706.PubMedCentralCrossRefPubMed Zivadinov R, Weinstock-Guttman B, Hashmi K, Abdelrahman N, Stosic M, Dwyer M, Hussein S, Durfee J, Ramanathan M: Smoking is associated with increased lesion volumes and brain atrophy in multiple sclerosis. Neurology. 2009, 73: 504-510. 10.1212/WNL.0b013e3181b2a706.PubMedCentralCrossRefPubMed
27.
go back to reference Jorgensen B, Tsao M: Dispersion models and longitudinal data analysis. Stat Med. 1999, 18: 2257-2270. 10.1002/(SICI)1097-0258(19990915/30)18:17/18<2257::AID-SIM253>3.0.CO;2-M.CrossRefPubMed Jorgensen B, Tsao M: Dispersion models and longitudinal data analysis. Stat Med. 1999, 18: 2257-2270. 10.1002/(SICI)1097-0258(19990915/30)18:17/18<2257::AID-SIM253>3.0.CO;2-M.CrossRefPubMed
28.
go back to reference Alexander JS, Harris MK, Wells SR, Mills G, Chalamidas K, Ganta VC, McGee J, Jennings MH, Gonzalez-Toledo E, Minagar A: Alterations in serum MMP-8, MMP-9, IL-12p40 and IL-23 in multiple sclerosis patients treated with interferon-beta1b. Mult Scler. 2010, 16: 801-809. 10.1177/1352458510370791.CrossRefPubMed Alexander JS, Harris MK, Wells SR, Mills G, Chalamidas K, Ganta VC, McGee J, Jennings MH, Gonzalez-Toledo E, Minagar A: Alterations in serum MMP-8, MMP-9, IL-12p40 and IL-23 in multiple sclerosis patients treated with interferon-beta1b. Mult Scler. 2010, 16: 801-809. 10.1177/1352458510370791.CrossRefPubMed
29.
go back to reference Minagar A, Jy W, Jimenez JJ, Alexander JS: Multiple sclerosis as a vascular disease. Neurol Res. 2006, 28: 230-235. 10.1179/016164106X98080.CrossRefPubMed Minagar A, Jy W, Jimenez JJ, Alexander JS: Multiple sclerosis as a vascular disease. Neurol Res. 2006, 28: 230-235. 10.1179/016164106X98080.CrossRefPubMed
30.
go back to reference Inglese M, Park SJ, Johnson G, Babb JS, Miles L, Jaggi H, Herbert J, Grossman RI: Deep gray matter perfusion in multiple sclerosis: dynamic susceptibility contrast perfusion magnetic resonance imaging at 3 T. Arch Neurol. 2007, 64: 196-202. 10.1001/archneur.64.2.196.CrossRefPubMed Inglese M, Park SJ, Johnson G, Babb JS, Miles L, Jaggi H, Herbert J, Grossman RI: Deep gray matter perfusion in multiple sclerosis: dynamic susceptibility contrast perfusion magnetic resonance imaging at 3 T. Arch Neurol. 2007, 64: 196-202. 10.1001/archneur.64.2.196.CrossRefPubMed
31.
go back to reference De Keyser J, Steen C, Mostert JP, Koch MW: Hypoperfusion of the cerebral white matter in multiple sclerosis: possible mechanisms and pathophysiological significance. J Cereb Blood Flow Metab. 2008, 28: 1645-1651. 10.1038/jcbfm.2008.72.CrossRefPubMed De Keyser J, Steen C, Mostert JP, Koch MW: Hypoperfusion of the cerebral white matter in multiple sclerosis: possible mechanisms and pathophysiological significance. J Cereb Blood Flow Metab. 2008, 28: 1645-1651. 10.1038/jcbfm.2008.72.CrossRefPubMed
32.
go back to reference Swank RL, Dugan BB: Effect of low saturated fat diet in early and late cases of multiple sclerosis. Lancet. 1990, 336: 37-39. 10.1016/0140-6736(90)91533-G.CrossRefPubMed Swank RL, Dugan BB: Effect of low saturated fat diet in early and late cases of multiple sclerosis. Lancet. 1990, 336: 37-39. 10.1016/0140-6736(90)91533-G.CrossRefPubMed
33.
go back to reference Zhang SM, Willett WC, Hernan MA, Olek MJ, Ascherio A: Dietary fat in relation to risk of multiple sclerosis among two large cohorts of women. Am J Epidemiol. 2000, 152: 1056-1064. 10.1093/aje/152.11.1056.CrossRefPubMed Zhang SM, Willett WC, Hernan MA, Olek MJ, Ascherio A: Dietary fat in relation to risk of multiple sclerosis among two large cohorts of women. Am J Epidemiol. 2000, 152: 1056-1064. 10.1093/aje/152.11.1056.CrossRefPubMed
34.
go back to reference Willey JZ, Elkind MS: 3-Hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors in the treatment of central nervous system diseases. Arch Neurol. 2010, 67: 1062-1067. 10.1001/archneurol.2010.199.PubMedCentralPubMed Willey JZ, Elkind MS: 3-Hydroxy-3-methylglutaryl-coenzyme A reductase inhibitors in the treatment of central nervous system diseases. Arch Neurol. 2010, 67: 1062-1067. 10.1001/archneurol.2010.199.PubMedCentralPubMed
35.
go back to reference Youssef S, Stuve O, Patarroyo JC, Ruiz PJ, Radosevich JL, Hur EM, Bravo M, Mitchell DJ, Sobel RA, Steinman L, Zamvil SS: The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature. 2002, 420: 78-84. 10.1038/nature01158.CrossRefPubMed Youssef S, Stuve O, Patarroyo JC, Ruiz PJ, Radosevich JL, Hur EM, Bravo M, Mitchell DJ, Sobel RA, Steinman L, Zamvil SS: The HMG-CoA reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature. 2002, 420: 78-84. 10.1038/nature01158.CrossRefPubMed
36.
go back to reference Maier O, De Jonge J, Nomden A, Hoekstra D, Baron W: Lovastatin induces the formation of abnormal myelin-like membrane sheets in primary oligodendrocytes. Glia. 2009, 57: 402-413. 10.1002/glia.20769.CrossRefPubMed Maier O, De Jonge J, Nomden A, Hoekstra D, Baron W: Lovastatin induces the formation of abnormal myelin-like membrane sheets in primary oligodendrocytes. Glia. 2009, 57: 402-413. 10.1002/glia.20769.CrossRefPubMed
37.
go back to reference Klopfleisch S, Merkler D, Schmitz M, Kloppner S, Schedensack M, Jeserich G, Althaus HH, Bruck W: Negative impact of statins on oligodendrocytes and myelin formation in vitro and in vivo. J Neurosci. 2008, 28: 13609-13614. 10.1523/JNEUROSCI.2765-08.2008.CrossRefPubMed Klopfleisch S, Merkler D, Schmitz M, Kloppner S, Schedensack M, Jeserich G, Althaus HH, Bruck W: Negative impact of statins on oligodendrocytes and myelin formation in vitro and in vivo. J Neurosci. 2008, 28: 13609-13614. 10.1523/JNEUROSCI.2765-08.2008.CrossRefPubMed
38.
go back to reference Sellner J, Weber MS, Vollmar P, Mattle HP, Hemmer B, Stuve O: The Combination of Interferon-Beta and HMG-CoA Reductase Inhibition in Multiple Sclerosis: Enthusiasm Lost too Soon?. CNS Neurosci Ther. 2010 Sellner J, Weber MS, Vollmar P, Mattle HP, Hemmer B, Stuve O: The Combination of Interferon-Beta and HMG-CoA Reductase Inhibition in Multiple Sclerosis: Enthusiasm Lost too Soon?. CNS Neurosci Ther. 2010
39.
go back to reference Vollmer T, Key L, Durkalski V, Tyor W, Corboy J, Markovic-Plese S, Preiningerova J, Rizzo M, Singh I: Oral simvastatin treatment in relapsing-remitting multiple sclerosis. Lancet. 2004, 363: 1607-1608. 10.1016/S0140-6736(04)16205-3.CrossRefPubMed Vollmer T, Key L, Durkalski V, Tyor W, Corboy J, Markovic-Plese S, Preiningerova J, Rizzo M, Singh I: Oral simvastatin treatment in relapsing-remitting multiple sclerosis. Lancet. 2004, 363: 1607-1608. 10.1016/S0140-6736(04)16205-3.CrossRefPubMed
40.
go back to reference Rudick RA, Pace A, Rani MR, Hyde R, Panzara M, Appachi S, Shrock J, Maurer SL, Calabresi PA, Confavreux C, et al: Effect of statins on clinical and molecular responses to intramuscular interferon beta-1a. Neurology. 2009, 72: 1989-1993. 10.1212/WNL.0b013e3181a92b96.PubMedCentralCrossRefPubMed Rudick RA, Pace A, Rani MR, Hyde R, Panzara M, Appachi S, Shrock J, Maurer SL, Calabresi PA, Confavreux C, et al: Effect of statins on clinical and molecular responses to intramuscular interferon beta-1a. Neurology. 2009, 72: 1989-1993. 10.1212/WNL.0b013e3181a92b96.PubMedCentralCrossRefPubMed
41.
go back to reference Waubant E, Pelletier D, Mass M, Cohen J, Kita M, Cross A, Bar-Or A, Vollmer T, Racke MK, Stüve O, et al: Atorvastatin therapy in patients with Clinically Isolated Syndrome (CIS): the STAyCIS study. 134th Annual Meeting, American Neurological Assocation; Baltimore, MD. 2010 Waubant E, Pelletier D, Mass M, Cohen J, Kita M, Cross A, Bar-Or A, Vollmer T, Racke MK, Stüve O, et al: Atorvastatin therapy in patients with Clinically Isolated Syndrome (CIS): the STAyCIS study. 134th Annual Meeting, American Neurological Assocation; Baltimore, MD. 2010
42.
go back to reference Markovic-Plese S, Jewells V, Speer D: Combining beta interferon and atorvastatin may increase disease activity in multiple sclerosis. Neurology. 2009, 72: 1965-1966. 10.1212/01.wnl.0000349667.27301.c8. 1965; author replyCrossRefPubMed Markovic-Plese S, Jewells V, Speer D: Combining beta interferon and atorvastatin may increase disease activity in multiple sclerosis. Neurology. 2009, 72: 1965-1966. 10.1212/01.wnl.0000349667.27301.c8. 1965; author replyCrossRefPubMed
43.
go back to reference Sorensen PS, Lycke J, Eralinna JP, Edland A, Wu X, Frederiksen JL, Oturai A, Malmestrom C, Stenager E, Sellebjerg F, Sondergaard HB: Simvastatin as add-on therapy to interferon beta-1a for relapsing-remitting multiple sclerosis (SIMCOMBIN study): a placebo-controlled randomised phase 4 trial. Lancet Neurol. 2011, 10: 691-701. 10.1016/S1474-4422(11)70144-2.CrossRefPubMed Sorensen PS, Lycke J, Eralinna JP, Edland A, Wu X, Frederiksen JL, Oturai A, Malmestrom C, Stenager E, Sellebjerg F, Sondergaard HB: Simvastatin as add-on therapy to interferon beta-1a for relapsing-remitting multiple sclerosis (SIMCOMBIN study): a placebo-controlled randomised phase 4 trial. Lancet Neurol. 2011, 10: 691-701. 10.1016/S1474-4422(11)70144-2.CrossRefPubMed
Metadata
Title
Serum lipid profiles are associated with disability and MRI outcomes in multiple sclerosis
Authors
Bianca Weinstock-Guttman
Robert Zivadinov
Naeem Mahfooz
Ellen Carl
Allison Drake
Jaclyn Schneider
Barbara Teter
Sara Hussein
Bijal Mehta
Marc Weiskopf
Jacqueline Durfee
Niels Bergsland
Murali Ramanathan
Publication date
01-12-2011
Publisher
BioMed Central
Published in
Journal of Neuroinflammation / Issue 1/2011
Electronic ISSN: 1742-2094
DOI
https://doi.org/10.1186/1742-2094-8-127

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