Anti-inflammatory nutritional intervention in patients with relapsing-remitting and primary-progressive multiple sclerosis: A pilot study

Experimental Biology and Medicine

Volumn 241, Issue 6, 2016, Pages 620-635

  Riccio, Paolo ^a   Rossano, Rocco ^a   Larocca, Marilena ^a   Trotta, Vincenzo ^a   Mennella, Ilario ^b   Vitaglione, Paola ^b   Ettorre, Michele ^c   Graverini, Antonio ^d   De Santis, Alessandro ^d   Di Monte, Elisabetta ^e   Coniglio, Maria Gabriella ^e  

^a UNIVERSITY OF BASILICATA   (Italy)

^b UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^c Center for Applied Nutrition   (Italy)

^d OTI Officine Terapie Innovative Srl   (Italy)

^e Hospital ASL 4 Madonna Delle Grazie   (Italy)

Author keywords

complementary and alternative medicine; diet; gelatinases; inflammation; interferon ; Multiple sclerosis; quality of life; vitamin D

Indexed keywords

ARACHIDONIC ACID; BETA1A INTERFERON; CALCIFEDIOL; COLECALCIFEROL; CREATININE; DOCOSAHEXAENOIC ACID; FIBRINOGEN; FISH OIL; GELATINASE; GLATIRAMER; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; ICOSAPENTAENOIC ACID; INTERFERON BETA SERINE; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MULTIVITAMIN; RESVERATROL; THIOCTIC ACID; TRIACYLGLYCEROL; VITAMIN D; ANTIINFLAMMATORY AGENT; BIOLOGICAL MARKER; FATTY ACID;

ADULT; ANTHROPOMETRIC PARAMETERS; ARTICLE; BIOCHEMICAL ANALYSIS; CONTROLLED STUDY; DIET RESTRICTION; DIET SUPPLEMENTATION; DIETARY INTAKE; EXPANDED DISABILITY STATUS SCALE; FATIGUE SEVERITY SCALE; FATTY ACID ANALYSIS; FEMALE; FOLLOW UP; GAS CHROMATOGRAPHY; HAMILTON DEPRESSION RATING SCALE; HUMAN; INFLAMMATION; MAJOR CLINICAL STUDY; MALE; MULTIPLE SCLEROSIS; NUTRITIONAL STATUS; QUESTIONNAIRE; RANDOMIZED CONTROLLED TRIAL; SHORT FORM 36; ZYMOGRAPHY; ANTHROPOMETRY; BLOOD; CHEMISTRY; DIET; MIDDLE AGED; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; NEUROLOGIC EXAMINATION; PATHOLOGY; PILOT STUDY; PROCEDURES; RECURRENT DISEASE; SERUM; TREATMENT OUTCOME; YOUNG ADULT;

ADULT; ANTHROPOMETRY; ANTI-INFLAMMATORY AGENTS; BIOMARKERS; DIET; FATTY ACIDS; FEMALE; GELATINASES; HUMANS; MALE; MIDDLE AGED; MULTIPLE SCLEROSIS, CHRONIC PROGRESSIVE; NEUROLOGIC EXAMINATION; PILOT PROJECTS; RECURRENCE; SERUM; SURVEYS AND QUESTIONNAIRES; TREATMENT OUTCOME; VITAMIN D; YOUNG ADULT;

EID: 84960342471     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370215618462     Document Type: Article

References (81)

1. C.S.ConstantinescuB.Gran. Multiple sclerosis: autoimmune associations in multiple sclerosis. Nat Rev Neurol2010; 6: 591–2.
2. E.Miller. Multiple sclerosis. Adv Exp Med Biol2012; 724: 222–38. Review.
3. H.Lassmann. Multiple sclerosis: Lessons from molecular neuropathology. Exp Neurol2014; 262: 2–7.
4. M.NaegeleR.Martin. The good and the bad of neuroinflammation in multiple sclerosis. Handb Clin Neurol2014; 122: 59–87.
5. A.Ben-NunN.KaushanskyN.KawakamiG.KrishnamoorthyK.BererR.LiblauR.HohlfeldH.Wekerle. From classic to spontaneous and humanized models of multiple sclerosis: impact on understanding pathogenesis and drug development. J Autoimmun2014; 54: 33–50.
6. F.H.JacquesF.D.Lublin. Defining the clinical course of multiple sclerosis: the 2013 revisions. Neurology2015; 84: 963–963.
7. R.DuttaB.D.Trapp. Relapsing and progressive forms of multiple sclerosis: insights from pathology. Curr Opin Neurol2014; 27: 271–8.
8. A.J.ThompsonC.H.PolmanD.H.MillerW.I.McDonaldB.BrochetM.FilippiD.H.MillerC.H.PolmanV.L.StevensonW.I.McDonald. Primary progressive multiple sclerosis. Brain1997; 120: 1085–96.
9. G.FilippiniC.Del GiovaneL.VacchiR.D’AmicoC.Di PietrantonjD.BeecherG.Salanti. Immunomodulators and immunosuppressants for multiple sclerosis: a network meta-analysis. Cochrane Db Syst Rev2013; 6. CD008933. Review.
10. V.LoleitV.BiberacherB.Hemmer. Current and future therapies targeting the immune system in multiple sclerosis. Curr Pharm Biotechnol2014; 15: 276–96.
11. C.BridelP.H.Lalive. Update on multiple sclerosis treatments. Swiss Med Wkly2014; 144: 14012–14012.
12. A.AscherioK.L.MungerJ.D.Lünemann. The initiation and prevention of multiple sclerosis. Nat Rev Neurol2012; 8: 602–12. Review.
13. A.VenkatesanR.T.Johnson. Infections and multiple sclerosis. Handb Clin Neurol2014; 122: 151–71. Review.
14. L.BelbasisV.BellouE.EvangelouJ.P.IoannidisI.Tzoulaki. Environmental risk factors and multiple sclerosis: an umbrella review of systematic reviews and meta-analyses. Lancet Neurol2015; 14: 263–73.
15. S.G.ZanellaP.Roberti di Sarsina. Personalization of multiple sclerosis treatments: using the chelation therapy approach. Explore2013; 9: 244–8.
16. T.LatronicoM.T.BranàE.MerraA.FasanoG.Di BariE.CasalinoG.M.Liuzzi. Impact of manganese neurotoxicity on MMP-9 production and superoxide dismutase activity in rat primary astrocytes. Effect of resveratrol and therapeutical implications for the treatment of CNS diseases. Toxicol Sci2013; 135: 218–28.
17. N.JafariQ.R.Hintzen. The association between cigarette smoking and multiple sclerosis. J Neurol Sci2011; 311: 78–85. Review.
18. K.L.Munger. Childhood obesity is a risk factor for multiple sclerosis. Mult Scler2013; 19: 1800–1800.
19. P.Riccio. The molecular basis of nutritional intervention in multiple sclerosis: a narrative review. Complement Ther Med2011; 19: 228–37.
20. P.RiccioR.Rossano. Nutrition facts in multiple sclerosis. ASN Neuro2015; 7. 1759091414568185. Review.
21. A.AscherioK.L.MungerR.WhiteK.KöchertK.C.SimonC.H.PolmanM.S.FreedmanH.P.HartungD.H.MillerX.MontalbánG.EdanF.BarkhofD.PleimesE.W.RadüR.SandbrinkL.KapposC.Pohl. Vitamin D as an early predictor of multiple sclerosis activity and progression. JAMA Neurol2014; 71: 306–14.
22. M.FarinottiL.VacchiS.SimiC.Di PietrantonjL.BraitG.Filippini. Dietary interventions for multiple sclerosis. Cochrane Db Syst Rev2012; 12. CD004192. Review.
23. R.L.SwankJ.V.Goodwin. Review of MS patient survival on a Swank low saturated fat diet. Nutrition2003; 19: 161–2.
24. I.NordvikK.M.MyhrH.NylandK.S.Bjerve. Effect of dietary advice and n-3 supplementation in newly diagnosed MS patients. Acta Neurol Scan2000; 102: 143–9.
25. B.Weinstock-GuttmanM.BaierY.ParkJ.FeichterP.Lee-KwenE.GallagherJ.VenkatramanK.MeksawanS.DeinehertD.PendergastA.B.AwadM.RamanathanF.MunschauerR.Rudick. Low fat dietary intervention with omega-3 fatty acid supplementation in multiple sclerosis patients. Prostaglandins Leukot Essent Fatty Acids2005; 73: 397–404.
26. L.1.ShintoG.MarracciS.Baldauf-WagnerA.StrehlowV.YadavL.StuberD.Bourdette. Omega-3 fatty acid supplementation decreases matrix metalloproteinase-9 production in relapsing-remitting multiple sclerosis. Prostaglandins Leukot Essent Fatty Acids2009; 80: 131–6.
27. V.1.Ramirez-RamirezM.A.Macias-IslasG.G.OrtizF.Pacheco-MoisesE.D.Torres-SanchezT.E.Sorto-GomezJ.A.Cruz-RamosG.Orozco-AviñaA.J.Celis de la Rosa. Efficacy of fish oil on serum of TNF α, IL-1 β, and IL-6 oxidative stress markers in multiple sclerosis treated with interferon beta-1b. Oxid Med Cell Longev2013; 2013: ID709493–ID709493.
28. V.1.YadavG.H.MarracciM.Y.MunarG.CheralaL.E.StuberL.AlvarezL.ShintoD.R.KoopD.N.Bourdette. Pharmacokinetic study of lipoic acid in multiple sclerosis: comparing mice and human pharmacokinetic parameters. Mult Scler2010; 16: 387–97.
29. G.SchmitzJ.Ecker. The opposing effects of n-3 and n-6 fatty acids. Progr Lipid Res2008; 47: 147–55.
30. P.C.Calder. n-3 polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr2006; 83: 1505S–1519S.
31. A.A.FarooquiL.A.HorrocksT.Farooqui. Modulation of inflammation in brain: a matter of fat. J Neurochem2007; 101: 577–99.
32. G.M.LiuzziT.LatronicoA.FasanoG.CarloneP.Riccio. Interferon-beta inhibits the expression of metalloproteinases in rat glial cell cultures: implications for multiple sclerosis pathogenesis and treatment. Mult Scler2004; 10: 290–7.
33. G.M.LiuzziT.LatronicoR.RossanoS.ViggianiA.FasanoP.Riccio. Inhibitory effect of polyunsaturated fatty acids on MMP-9 release from microglial cells-implications for complementary multiple sclerosis treatment. Neurochem Res2007; 32: 2184–93.
34. L.R.MehtaR.H.DworkinS.R.Schwid. Polyunsaturated fatty acids and their potential therapeutic role in multiple sclerosis. Nat Clin Pract Neurol2009; 5: 82–92.
35. A.ColucciaP.BorracciG.RennaA.GiustinoT.LatronicoP.RiccioM.R.Carratù. Developmental omega-3 supplementation improves motor skills in juvenile-adult rats”. Int J Dev Neurosci2009; 27: 599–605.
36. Xu ZZ, Zhang L, Liu T, Park JY, Berta T, Yang R, Serhan CN, Ji RR. Resolvins RvE1 and RvD1 attenuate inflammatory pain via central and peripheral actions. Nat Med 201;16:592–7
37. S.HongY.Lu. Omega-3 fatty acid-derived resolvins and protectins in inflammation resolution and leukocyte functions: targeting novel lipid mediator pathways in mitigation of acute kidney injury. Front Immunol2013; 4: 13–13.
38. C.N.SerhanJ.DalliR.A.ColasJ.W.WinklerN.Chiang. Protectins and maresins: New pro-resolving families of mediators in acute inflammation and resolution bioactive metabolome. Biochim Biophys Acta2015; 1851: 397–413. Review.
39. S.SalinthoneV.YadavR.V.SchillaceD.N.BourdetteD.W.Carr. Lipoic acid attenuates inflammation via cAMP and protein kinase A signaling. PLoS One2010; 5: e13058–e13058.
40. S.DasD.K.Das. Anti-inflammatory responses of resveratrol. Inflamm Allergy Drug Targets2007; 6: 168–73.
41. G.ChengX.ZhangD.GaoX.JiangW.Dong. Resveratrol inhibits MMP-9 expression by up-regulating PPAR alpha expression in an oxygen glucose deprivation-exposed neuron model. Neurosci Lett2009; 451: 105–8.
42. M.T.Cantorna. Vitamin D, multiple sclerosis and inflammatory bowel disease. Arch Biochem Biophys2012; 523: 103–6.
43. M.MarziniakS.Meuth. Current perspectives on interferon Beta-1b for the treatment of multiple sclerosis. Adv Ther2014; 31: 915–31.
44. L.H.KasperA.T.Reder. Immunomodulatory activity of interferon-beta. Ann Clin Trans Neurol2014; 1: 622–31. Review.
45. F.MarangoniC.ColomboC.Galli. A method for the direct evaluation of the fatty acid status in a drop of blood from a fingertip in humans: applicability to nutritional and epidemiological studies. Anal Biochem2004; 326: 267–72.
46. R.RossanoM.LaroccaL.RivielloM.G.ConiglioJ.VandoorenG.M.Liuzzi. Heterogeneity of serum gelatinases MMP-2 and MMP-9 isoforms and charge variants. J Cell Mol Med2014; 18: 242–52.
47. T.BelliniA.TrentiniM.C.ManfrinatoC.TamborinoC.A.VoltaV.Di FoggiaE.FainardiF.DallocchioM.Castellazzi. Matrix metalloproteinase-9 activity detected in body fluids is the result of two different enzyme forms. J Biochem2012; 151: 493–9.
48. N.StewartS.SimpsonJrI.van der MeiA.L.PonsonbyL.BlizzardT.DwyerF.PittasD.EylesP.KoB.V.Taylor. Interferon-β and serum 25-hydroxyvitamin D interact to modulate relapse risk in MS. Neurology2012; 79: 254–60.
49. K.YinD.K.Agrawal. Vitamin D and inflammatory diseases. J Inflamm Res2014; 7: 69–87.
50. A.E.HandelG.K.SandveG.DisantoA.J.Berlanga-TaylorG.GalloneH.HanwellF.DrabløsG.GiovannoniG.C.EbersS.V.Ramagopalan. Vitamin D receptor ChIP-seq in primary CD4+ cells: relationship to serum 25-hydroxyvitamin D levels and autoimmune disease. BMC Med2013; 11: 163–163.
51. M.F.Holick. Vitamin D deficiency. N Engl J Med2007; 357: 266–81. Review.
52. M.K.ThomasD.M.Lloyd-JonesR.I.ThadhaniA.C.ShawD.J.DeraskaB.T.KitchE.C.VamvakasI.M.DickR.L.PrinceJ.S.Finkelstein. Hypovitaminosis D in medical inpatients. N Engl J Med1998; 338: 777–83.
53. A.K.HedströmT.OlssonL.Alfredsson. High body mass index before age 20 is associated with increased risk for multiple sclerosis in both men and women. Mult Scler2012; 18: 1334–6.
54. J.B.ChengM.A.LevineN.H.BellD.J.MangelsdorfD.W.Russell. Genetic evidence that the human CYP2R1 enzyme is a key vitamin D 25-hydroxylase. Proc Natl Acad Sci U S A2004; 101: 7711–5.
55. A.DidriksenG.GrimnesM.S.HutchinsonM.KjærgaardJ.SvartbergR.M.JoakimsenR.Jorde. The serum 25-hydroxyvitamin D response to vitamin D supplementation is related to genetic factors, BMI, and baseline levels. Eur J Endocrinol2013; 169: 559–67.
56. Ramasamy A, Trabzuni D, Forabosco P, Smith C, Walker R, Dillman A, Sveinbjornsdottir S; North American Brain Expression Consortium (NABEC), UK Brain Expression Consortium (UKBEC), Hardy J, Weale ME, Ryten M. Genetic evidence for a pathogenic role for the vitamin D3 metabolizing enzyme CYP24A1 in multiple sclerosis. Mult Scler Relat Disord 2014;3:211–9
57. I.Schuster. Cytochromes P450 are essential players in the vitamin D signaling system. Biochim Biophys Acta2011; 1814: 186–99. Review.
58. G.ChielliniS.RapposelliJ.ZhuI.MassarelliM.SaracenoA.M.BianucciL.A.PlumM.Clagett-DameH.F.DeLuca. Synthesis and biological activities of vitamin D-like inhibitors of CYP24 hydroxylase. Steroids2012; 77: 212–23.
59. J.P.KósaP.HorváthJ.WölflingD.KovacsB.BallaP.MatyusE.HorváthG.SpeerI.TakácsZ.NagyH.HorváthP.Lakatos. CYP24A1 inhibition facilitates the anti-tumor effect of vitamin D3 on colorectal cancer cells. World J Gastroenterol2013; 19: 2621–8.
60. M.F.Holick. Vitamin D and brain health: the need for vitamin D supplementation and sensible sun exposure. J Int Med2015; 277: 90–3.
61. N.M.Al-DaghriF.R.GueriniO.S.Al-AttasM.S.AlokailK.M.AlkharfyH.M.DrazC.AgliardiA.S.CostaI.SaulleA.K.MohammedM.BiasinM.Clerici. Vitamin D receptor gene polymorphisms are associated with obesity and inflammosome activity. PLoS One2014; 9: e102141–e102141.
62. A.E.GrzegorzewskaE.JodłowskaA.MostowskaA.SowińskaP.P.Jagodziński. Single nucleotide polymorphisms of vitamin D binding protein, vitamin D receptor and retinoid X receptor alpha genes and response to hepatitis B vaccination in renal replacement therapy patients. Expert Rev Vaccines2014; 13: 1395–1403.
63. A.O.RinaldiI.SanseverinoC.PurificatoA.CorteseR.MechelliS.FrancisciM.SalvettiE.MillefioriniS.GessaniM.C.Gauzzi. Increased circulating levels of vitamin D binding protein in MS patients. Toxins2015; 7: 129–37.
64. B.S.AnL.E.Tavera-MendozaV.DimitrovX.WangM.R.CalderonH.J.WangJ.H.White. Stimulation of Sirt1-regulated FoxO protein function by the ligand-bound vitamin D receptor. Mol Cell Biol2010; 30: 4890–900.
65. 2 oxidant injury through the Mek/Erk-Sirt1 axis activation. J Cardiovasc Transl Res2013; 6: 221–31.
66. D.GolanB.HalhalL.Glass-MarmorE.Staun-RamO.RozenbergI.LaviS.DishonM.BarakS.Ish-ShalomA.Miller. Vitamin D supplementation for patients with multiple sclerosis treated with interferon-beta: a randomized controlled trial assessing the effect on flu-like symptoms and immunomodulatory properties. BMC Neurol2013; 13: 60–60.
67. M.T.CantornaK.McDanielS.BoraJ.ChenJ.James. Vitamin D, immune regulation, the microbiota, and inflammatory bowel disease. Exp Biol Med2014; 239: 1524–30. Review.
68. J.SmoldersJ.DamoiseauxP.MenheereR.Hupperts. Vitamin D as an immune modulator in multiple sclerosis, a review. J Neuroimmunol2008; 194: 7–17.
69. C.Pierrot-Deseilligny. Clinical implications of a possible role of vitamin D in multiple sclerosis. J Neurol2009; 256: 1468–79.
70. B.V.Taylor. Sunshine and multiple sclerosis. J Neurol Neurosurg Psychiatry2013; 84: 1066–1066.
71. R.BouillonG.CarmelietL.LiebenE.van EttenA.VerstuyfH.F.LudererL.LiebenC.MathieuM.Demay. Vitamin D and energy homeostasis: of mice and men. Nat Rev Endocrinol2014; 10: 79–87. Review.
72. J.DörrA.DöringF.Paul. Can we prevent or treat multiple sclerosis by individualized vitamin D supply?EPMA J2013; 4: 4–4.
73. S.Shab-BidarS.BoursP.P.GeusensA.G.KesselsJ.P.van den Bergh. Serum 25(OH)D response to vitamin D3 supplementation: a meta-regression analysis. Nutrition2014; 30: 975–85. Review.
74. A.TrentiniM.C.ManfrinatoM.CastellazziC.TamborinoG.RoversiC.A.VoltaE.3.BaldiM.R.4.TolaE.1.GranieriF.1.DallocchioT.1.BelliniE.5.Fainardi. Emilia-Romagna network for Multiple Sclerosis (ERMES) study group. TIMP-1 resistant matrix metalloproteinase-9 is the predominant serum active isoform associated with MRI activity in patients with multiple sclerosis. Mult Scler J2015; 21: 1121–30.
75. D.EnkoL.FridrichE.RezankaR.StolbaJ.ErnstI.WendlerD.FabianS.HauptlorenzG.Halwachs-Baumann. 25-Hydroxy-vitamin D status: limitations in comparison and clinical interpretation of serum-levels across different assay methods. Clin Lab2014; 60: 1541–50.
76. O.1.FernandezR.MartinA.RoviraS.LlufriuA.Vidal-JordanaV.E.Fernandez-SanchezJ.C.Alvarez-CermenoG.IzquierdoR.Arroyo-GonzalezA.Rodriguez-AntiguedadB.Casanova-EstruchX.Montalban. Biomarkers in multiple sclerosis: an update for 2014. Rev Neurol2014; 58: 553–70.
77. V.M.G.YadavE.KimR.SpainM.CameronS.OversJ.McDougallD.Bourdette. Effects of a low fat plant based diet in multiple sclerosis (MS): results of a 1 year long randomized controlled study (P6.152). Neurology2014; 82(10 suppl): 6.152–6.152.
78. B.BishtW.G.DarlingE.T.ShivapourS.K.LutgendorfL.G.SnetselaarC.A.ChenardT.L.Wahls. Multimodal intervention improves fatigue and quality of life in subjects with progressive multiple sclerosis: a pilot study. Degen Neurol Neuromuscular Dis2015; 5: 19–35.
79. B.BishtW.G.DarlingR.E.GrossmannE.T.ShivapourS.K.LutgendorfL.G.SnetselaarM.J.HallM.B.ZimmermanT.L.Wahls. A multimodal intervention for patients with secondary progressive multiple sclerosis: feasibility and effect on fatigue. J Altern Complem Med2014; 20: 347–355.
80. O.TorkildsenS.WergelandS.BakkeA.G.BeiskeK.S.BjerveH.HovdalR.MidgardF.LilleåsT.PedersenB.BjørnaråF.DaleneG.KlevelandJ.SchepelI.C.OlsenK.M.Myhr. Omega-3 Fatty Acid Treatment in Multiple Sclerosis (OFAMS study): a randomised, double-blind, placebo-controlled trial. Archiv Neurol2012; 69: 1044–51.
81. M.C.PantzarisG.N.LoukaidesE.E.NtzaniI.S.Patrikios. A novel oral nutraceutical formula of omega-3 and omega-6 fatty acids with vitamins (PLP10) in relapsing remitting multiple sclerosis: a randomised, double-blind, placebo-controlled proof-of-concept clinical trial. BMJ Open2013; 3: e002170–e002170.