Exploring Multiple Sclerosis (MS) and Amyotrophic Lateral Scler osis (ALS) as Neurodegenerative Diseases and their Treatments: A Review Study

Author(s): Omar Deeb*, Maisa Nabulsi

Journal Name: Current Topics in Medicinal Chemistry

Volume 20 , Issue 26 , 2020


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Abstract:

Growing concern about neurodegenerative diseases is becoming a global issue. It is estimated that not only will their prevalence increase but also morbidity and health burden will be concerning. Scientists, researchers and clinicians share the responsibility of raising the awareness and knowledge about the restricting and handicapping health restrains related to these diseases.

Multiple Sclerosis (MS), as one of the prevalent autoimmune diseases, is characterized by abnormal regulation of the immune system that periodically attacks parts of the nervous system; brain and spinal cord. Symptoms and impairments include weakness, numbness, visual problems, tingling pain that are quietly variable among patients.

Amyotrophic Lateral Sclerosis (ALS) is another neurodegenerative disease that is characterized by the degeneration of motor neurons in the brain and spinal cord. Unlike MS, symptoms begin with muscle weakness and progress to affect speech, swallowing and finally breathing. Despite the major differences between MS and ALS, misdiagnosis is still influencing disease prognosis and patient’s quality of life.

Diagnosis depends on obtaining a careful history and neurological examination as well as the use of Magnetic Resonance Imaging (MRI), which are considered challenging and depend on the current disease status in individuals.

Fortunately, a myriad of treatments is available now for MS. Most of the cases are steroid responsive. Disease modifying therapy is amongst the most important set of treatments.

In ALS, few medications that slow down disease progression are present. The aim of this paper is to summarize what has been globally known and practiced about MS and ALS, as they are currently classified as important growing key players among autoimmune diseases. In terms of treatments, it is concluded that special efforts and input should be directed towards repurposing of older drugs and on stem cells trials. As for ALS, it is highlighted that supportive measurements and supplementary treatments remain essentially needed for ALS patients and their families. On the other hand, it is noteworthy to clarify that the patient-doctor communication is relatively a cornerstone in selecting the best treatment for each MS patient.

Keywords: Neurodegeneration, Neuroinflammatory, Disease modifying therapies (DMTs), Multiple sclerosis, Amyotrophic Lateral sclerosis, Blood brain barrier.

[1]
Chen, W.W.; Zhang, X.; Huang, W.J. Role of neuroinflammation in neurodegenerative diseases. (Review) Mol. Med. Rep., 2016, 13(4), 3391-3396.
[http://dx.doi.org/10.3892/mmr.2016.4948 ] [PMID: 26935478]
[2]
McClean, P.L.; Parthsarathy, V.; Faivre, E.; Hölscher, C. The diabetes drug liraglutide prevents degenerative processes in a mouse model of Alzheimer’s disease. J. Neurosci., 2011, 31(17), 6587-6594.
[http://dx.doi.org/10.1523/JNEUROSCI.0529-11.2011 ] [PMID: 21525299]
[3]
Osakwe, O.; Rizvi, S.A.A. Social Aspects of Drug Discovery, Development and Commercialization, 1st ed; Academic press: London, 2016.
[4]
Durães, F.; Pinto, M.; Sousa, E. Old drugs as new treatments for neurodegenerative diseases. Pharmaceuticals (Basel), 2018, 11(2), 1-21.
[http://dx.doi.org/10.3390/ph11020044 ] [PMID: 29751602]
[5]
Luo, C.; Jian, C.; Liao, Y.; Huang, Q.; Wu, Y.; Liu, X.; Zou, D.; Wu, Y. The role of microglia in multiple sclerosis. Neuropsychiatr. Dis. Treat., 2017, 13, 1661-1667.
[http://dx.doi.org/10.2147/NDT.S140634 ] [PMID: 28721047]
[6]
Ponomarev, E.D.; Shriver, L.P.; Maresz, K.; Dittel, B.N. Microglial cell activation and proliferation precedes the onset of CNS autoimmunity. J. Neurosci. Res., 2005, 81(3), 374-389.
[http://dx.doi.org/10.1002/jnr.20488 ] [PMID: 15959904]
[7]
Lassmann, H.; Brück, W.; Lucchinetti, C.F. The immunopathology of multiple sclerosis: an overview. Brain Pathol., 2007, 17(2), 210-218.
[http://dx.doi.org/10.1111/j.1750-3639.2007.00064.x ] [PMID: 17388952]
[8]
Segal, B.M. Enhancing natural killer cells is beneficial in multiple sclerosis - Commentary. Mult. Scler., 2019, 25(4), 513-514.
[http://dx.doi.org/10.1177/1352458518809296 ] [PMID: 30421650]
[9]
Merkelbach, S.; Haensch, C.A.; Hemmer, B.; Koehler, J.; König, N.H.; Ziemssen, T. Multiple sclerosis and the autonomic nervous system. J. Neurol., 2006, 253(1)(Suppl. 1), I21-I25.
[http://dx.doi.org/10.1007/s00415-006-1105-z ] [PMID: 16477481]
[10]
Trapp, B.D.; Nave, K-A. Multiple sclerosis: an immune or neurodegenerative disorder? Annu. Rev. Neurosci., 2008, 31(1), 247-269.
[http://dx.doi.org/10.1146/annurev.neuro.30.051606.094313 ] [PMID: 18558855]
[11]
Hu, C.J.; Octave, J.N. Editorial: Risk factors and outcome predicating biomarker of neurodegenerative diseases. Front. Neurol., 2019, 10, 45.
[http://dx.doi.org/10.3389/fneur.2019.00045 ] [PMID: 30778328]
[12]
Belbasis, L.; Bellou, V.; Evangelou, E.; Ioannidis, J.P.A.; Tzoulaki, I. Environmental risk factors and multiple sclerosis: an umbrella review of systematic reviews and meta-analyses. Lancet Neurol., 2015, 14(3), 263-273.
[http://dx.doi.org/10.1016/S1474-4422(14)70267-4 ] [PMID: 25662901]
[13]
Canto, E.; Oksenberg, J.R. Multiple sclerosis genetics. Mult. Scler., 2018, 24(1), 75-79.
[http://dx.doi.org/10.1177/1352458517737371 ] [PMID: 29307290]
[14]
Gilmour, H.; Ramage-Morin, P.L.; Wong, S.L. Multiple sclerosis: Prevalence and impact. Health Rep., 2018, 29(1), 3-8.
[PMID: 29341025]
[15]
Isobe, N.; Madireddy, L.; Khankhanian, P.; Matsushita, T.; Caillier, S.J.; Moré, J.M.; Gourraud, P.A.; McCauley, J.L.; Beecham, A.H.; Piccio, L.; Herbert, J.; Khan, O.; Cohen, J.; Stone, L.; Santaniello, A.; Cree, B.A.; Onengut-Gumuscu, S.; Rich, S.S.; Hauser, S.L.; Sawcer, S.; Oksenberg, J.R. International Multiple Sclerosis Genetics Consortium. An ImmunoChip study of multiple sclerosis risk in African Americans. Brain, 2015, 138(Pt 6), 1518-1530.
[http://dx.doi.org/10.1093/brain/awv078 ] [PMID: 25818868]
[16]
komori M., Blake A., Greenwood M et al, Cerebrospinal fluid markers reveal intrathecal inflamation in progressive multiple sclerosis. Ann Neurol., 2015, 78(1), 3-20.
[17]
Keegan, B.M.; Noseworthy, J.H. Multiple sclerosis. Annu. Rev. Med., 2002, 53, 285-302.
[http://dx.doi.org/10.1146/annurev.med.53.082901.103909 ] [PMID: 11818475]
[18]
Goldenberg, M.M. Multiple sclerosis review. P&T, 2012, 37(3), 175-184.
[PMID: 22605909]
[19]
Lublin, F.D.; Reingold, S.C.; Cohen, J.A.; Cutter, G.R.; Sørensen, P.S.; Thompson, A.J.; Wolinsky, J.S.; Balcer, L.J.; Banwell, B.; Barkhof, F.; Bebo, B., Jr; Calabresi, P.A.; Clanet, M.; Comi, G.; Fox, R.J.; Freedman, M.S.; Goodman, A.D.; Inglese, M.; Kappos, L.; Kieseier, B.C.; Lincoln, J.A.; Lubetzki, C.; Miller, A.E.; Montalban, X.; O’Connor, P.W.; Petkau, J.; Pozzilli, C.; Rudick, R.A.; Sormani, M.P.; Stüve, O.; Waubant, E.; Polman, C.H. Defining the clinical course of multiple sclerosis: the 2013 revisions. Neurology, 2014, 83(3), 278-286.
[http://dx.doi.org/10.1212/WNL.0000000000000560 ] [PMID: 24871874]
[20]
Lublin, F.D. New multiple sclerosis phenotypic classification. Eur. Neurol., 2014, 72(Suppl. 1), 1-5.
[http://dx.doi.org/10.1159/000367614 ] [PMID: 25278115]
[21]
Hemond, C.C.; Healy, B.C.; Tauhid, S.; Mazzola, M.A.; Quintana, F.J.; Gandhi, R.; Weiner, H.L.; Bakshi, R. MRI phenotypes in MS: Longitudinal changes and miRNA signatures. Neurol. Neuroimmunol. Neuroinflamm., 2019, 6(2) e530
[http://dx.doi.org/10.1212/NXI.0000000000000530 ] [PMID: 30800720]
[22]
Kantarci, O.H. Phases and phenotypes of multiple sclerosis. Continuum (Minneap. Minn.), 2019, 25(3), 636-654.
[http://dx.doi.org/10.1212/CON.0000000000000737 ] [PMID: 31162309]
[23]
Bar-Or, A. The immunology of multiple sclerosis. Semin. Neurol., 2008, 28(1), 29-45.
[http://dx.doi.org/10.1055/s-2007-1019124 ] [PMID: 18256985]
[24]
Tavazzi, E.; Rovaris, M.; La Mantia, L. Drug therapy for multiple sclerosis. CMAJ, 2014, 186(11), 833-840.
[http://dx.doi.org/10.1503/cmaj.130727 ] [PMID: 24756629]
[25]
Higuera, L.; Carlin, C.S.; Anderson, S. Adherence to disease-modifying therapies for multiple sclerosis. J. Manag. Care Spec. Pharm., 2016, 22(12), 1394-1401.
[http://dx.doi.org/10.18553/jmcp.2016.22.12.1394 ] [PMID: 27882830]
[26]
Mathis, A.S. Managed care aspects of managing multiple sclerosis. Am. J. Manag. Care, 2013, 19(2)(Suppl.), S28-S34.
[PMID: 23544718]
[27]
Saguil, A.; Kane, S.; Farnell, E. Multiple sclerosis: a primary care perspective. Am. Fam. Physician, 2014, 90(9), 644-652.
[PMID: 25368924]
[28]
Munsell, M.; Frean, M.; Menzin, J.; Phillips, A.L. An evaluation of adherence in patients with multiple sclerosis newly initiating treatment with a self-injectable or an oral disease-modifying drug. Patient Prefer. Adherence, 2016, 11, 55-62.
[http://dx.doi.org/10.2147/PPA.S118107 ] [PMID: 28115831]
[29]
TaŞKapilioĞLu. Ö. Recent advances in the treatment for multiple sclerosis; current new drugs specific for multiple sclerosis. Noro Psikiyatri Arsivi, 2018, 55(Suppl. 1), S15-S20.
[PMID: 30692849]
[30]
Lattanzi, S.; Cagnetti, C.; Danni, M.; Provinciali, L.; Silvestrini, M. Oral and intravenous steroids for multiple sclerosis relapse: a systematic review and meta-analysis. J. Neurol., 2017, 264(8), 1697-1704.
[http://dx.doi.org/10.1007/s00415-017-8505-0 ] [PMID: 28492970]
[31]
Chataway, J. Oral versus intravenous steroids in multiple sclerosis relapses - a perennial question? Mult. Scler., 2014, 20(6), 643-645.
[http://dx.doi.org/10.1177/1352458514531088 ] [PMID: 24756993]
[32]
Sloka, J.S.; Stefanelli, M. The mechanism of action of methylprednisolone in the treatment of multiple sclerosis. Mult. Scler., 2005, 11(4), 425-432.
[http://dx.doi.org/10.1191/1352458505ms1190oa ] [PMID: 16042225]
[33]
Therapy, D.; Multiple, F.O.R. Drug therapy for multiple myeloma., American Cancer Society, 2020. Available from:. https://www.cancer.org/content/dam/CRC/PDF/Public/8741.00.pdf
[34]
Rae-Grant, A.; Day, G.S.; Marrie, R.A.; Rabinstein, A.; Cree, B.A.C.; Gronseth, G.S.; Haboubi, M.; Halper, J.; Hosey, J.P.; Jones, D.E.; Lisak, R.; Pelletier, D.; Potrebic, S.; Sitcov, C.; Sommers, R.; Stachowiak, J.; Getchius, T.S.D.; Merillat, S.A.; Pringsheim, T. Practice guideline recommendations summary: Disease-modifying therapies for adults with multiple sclerosis: Report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology. Neurology, 2018, 90(17), 777-788.
[http://dx.doi.org/10.1212/WNL.0000000000005347 ] [PMID: 29686116]
[35]
Ontaneda, D.; Rae-Grant, A.D. Management of acute exacerbations in multiple sclerosis. Ann. Indian Acad. Neurol., 2009, 12(4), 264-272.
[http://dx.doi.org/10.4103/0972-2327.58283 ] [PMID: 20182574]
[36]
La Mantia, L.; Milanese, C.; Mascoli, N.; D’Amico, R.; Weinstock-Guttman, B. Cyclophosphamide for multiple sclerosis. Cochrane Database Syst. Rev., 2007, 1 CD002819
[PMID: 17253481]
[37]
Awad, A.; Stüve, O. Cyclophosphamide in multiple sclerosis: scientific rationale, history and novel treatment paradigms. Ther. Adv. Neurol. Disorder., 2009, 2(6), 50-61.
[http://dx.doi.org/10.1177/1756285609344375 ] [PMID: 21180630]
[38]
Robertson, D.; Moreo, N. Disease-modifying therapies in multiple sclerosis: overview and treatment considerations. Fed. Pract., 2016, 33(6), 28-34.
[PMID: 30766181]
[39]
O’Connor, P.W.; Oh, J. Disease-modifying agents in multiple sclerosis. Handb. Clin. Neurol., 2014, 122, 465-501.
[http://dx.doi.org/10.1016/B978-0-444-52001-2.00021-2 ] [PMID: 24507532]
[40]
Dhib-Jalbut, S.; Marks, S. Interferon-beta mechanisms of action in multiple sclerosis. Neurology, 2010, 74(Suppl. 1), S17-S24.
[http://dx.doi.org/10.1212/WNL.0b013e3181c97d99 ] [PMID: 20038758]
[41]
Kilsdonk, I.D.; Jonkman, L.E.; Klaver, R.; van Veluw, S.J.; Zwanenburg, J.J.M.; Kuijer, J.P.A.; Pouwels, P.J.; Twisk, J.W.; Wattjes, M.P.; Luijten, P.R.; Barkhof, F.; Geurts, J.J. Increased cortical grey matter lesion detection in multiple sclerosis with 7 T MRI: a post-mortem verification study. Brain, 2016, 139(Pt 5), 1472-1481.
[http://dx.doi.org/10.1093/brain/aww037 ] [PMID: 26956422]
[42]
La Mantia, L.; Munari, L.M.; Lovati, R. Glatiramer acetate for multiple sclerosis. Cochrane Database Syst. Rev., 2010, 5(5) CD004678
[http://dx.doi.org/10.1002/14651858.CD004678.pub2 ] [PMID: 20464733]
[43]
Freedman, MS.; Patry, D.G.; Grand’Maison, F.; Myles, M.L.; Paty, D.W.; Selchen, D.H.; Canadian, M.S. Working Group. Treatment optimization in multiple sclerosis. Can. J. Neurol. Sci., 2004, 31(2), 157-168.
[http://dx.doi.org/10.1017/S0317167100053804 ] [PMID: 15198439]
[44]
Polman, C.H.; Uitdehaag, B.M.J. Drug treatment of multiple sclerosis. BMJ, 2000, 321(7259), 490-494.
[http://dx.doi.org/10.1136/bmj.321.7259.490 ] [PMID: 10948033]
[45]
Multiple Sclerosis Association of America; 2019. Available from:. https://mymsaa.org/publications/msresearch-update-2019/
[46]
Kappos, L.; Bar-Or, A.; Cree, B.A.C.; Fox, R.J.; Giovannoni, G.; Gold, R.; Vermersch, P.; Arnold, D.L.; Arnould, S.; Scherz, T.; Wolf, C.; Wallström, E.; Dahlke, F. EXPAND Clinical Investigators. Siponimod versus placebo in secondary progressive multiple sclerosis (EXPAND): a double-blind, randomised, phase 3 study. Lancet, 2018, 391(10127), 1263-1273.
[http://dx.doi.org/10.1016/S0140-6736(18)30475-6 ] [PMID: 29576505]
[47]
Giovannoni, G.; Comi, G.; Cook, S.; Rammohan, K.; Rieckmann, P.; Soelberg Sørensen, P.; Vermersch, P.; Chang, P.; Hamlett, A.; Musch, B.; Greenberg, S.J. CLARITY Study Group. A placebo-controlled trial of oral cladribine for relapsing multiple sclerosis. N. Engl. J. Med., 2010, 362(5), 416-426.
[http://dx.doi.org/10.1056/NEJMoa0902533 ] [PMID: 20089960]
[48]
Giovannoni, G. Cladribine to treat relapsing forms of multiple sclerosis. Neurotherapeutics, 2017, 14(4), 874-887.
[http://dx.doi.org/10.1007/s13311-017-0573-4 ] [PMID: 29168160]
[49]
Brandstadter, R.; Katz Sand, I. The use of natalizumab for multiple sclerosis. Neuropsychiatr. Dis. Treat., 2017, 13, 1691-1702.
[http://dx.doi.org/10.2147/NDT.S114636 ] [PMID: 28721050]
[50]
Hauser, S.L.; Bar-Or, A.; Comi, G.; Giovannoni, G.; Hartung, H.P.; Hemmer, B.; Lublin, F.; Montalban, X.; Rammohan, K.W.; Selmaj, K.; Traboulsee, A.; Wolinsky, J.S.; Arnold, D.L.; Klingelschmitt, G.; Masterman, D.; Fontoura, P.; Belachew, S.; Chin, P.; Mairon, N.; Garren, H.; Kappos, L. OPERA I and OPERA II Clinical Investigators. Ocrelizumab versus Interferon Beta-1a in Relapsing Multiple Sclerosis. N. Engl. J. Med., 2017, 376(3), 221-234.
[http://dx.doi.org/10.1056/NEJMoa1601277 ] [PMID: 28002679]
[51]
Mulero, P.; Midaglia, L.; Montalban, X. Ocrelizumab: a new milestone in multiple sclerosis therapy. Ther. Adv. Neurol. Disorder., 2018, 11 1756286418773025
[http://dx.doi.org/10.1177/1756286418773025 ] [PMID: 29774057]
[52]
Prosperini, L.; Pontecorvo, S. Dimethyl fumarate in the management of multiple sclerosis: appropriate patient selection and special considerations. Ther. Clin. Risk Manag., 2016, 12, 339-350.
[http://dx.doi.org/10.2147/TCRM.S85099 ] [PMID: 27042079]
[53]
Río, J.; Porcel, J.; Téllez, N.; Sánchez-Betancourt, A.; Tintoré, M.; Arévalo, M.J.; Nos, C.; Montalban, X. Factors related with treatment adherence to interferon β and glatiramer acetate therapy in multiple sclerosis. Mult. Scler., 2005, 11(3), 306-309.
[http://dx.doi.org/10.1191/1352458505ms1173oa ] [PMID: 15957512]
[54]
Gajofatto, A.; Benedetti, M.D. Treatment strategies for multiple sclerosis: When to start, when to change, when to stop? World J. Clin. Cases, 2015, 3(7), 545-555.
[http://dx.doi.org/10.12998/wjcc.v3.i7.545 ] [PMID: 26244148]
[55]
Hooijmans, C.R.; Hlavica, M.; Schuler, F.A.F.; Good, N.; Good, A.; Baumgartner, L.; Galeno, G.; Schneider, M.P.; Jung, T.; de Vries, R.; Ineichen, B.V. Remyelination promoting therapies in multiple sclerosis animal models: a systematic review and meta-analysis. Sci. Rep., 2019, 9(1), 822-839.
[http://dx.doi.org/10.1038/s41598-018-35734-4 ] [PMID: 30696832]
[56]
Horton, D.K.; Mehta, P.; Antao, V.C. Quantifying a nonnotifiable disease in the United States: the national amyotrophic lateral sclerosis registry model. JAMA, 2014, 312(11), 1097-1098.
[http://dx.doi.org/10.1001/jama.2014.9799 ] [PMID: 25057819]
[57]
Wijesekera, L.C.; Leigh, P.N. Amyotrophic lateral sclerosis. Orphanet J. Rare Dis., 2009, 4(1), 3.
[http://dx.doi.org/10.1186/1750-1172-4-3 ] [PMID: 19192301]
[58]
Nowicka, N.; Juranek, J.; Juranek, J.K.; Wojtkiewicz, J. Risk factors and emerging therapies in amyotrophic lateral sclerosis. Int. J. Mol. Sci., 2019, 20(11), 2616.
[http://dx.doi.org/10.3390/ijms20112616 ] [PMID: 31141951]
[59]
Bonduelle, M. Amyotrophic lateral sclerosis. Rev. Neurol. (Paris), 1982, 138(12), 1027-1039.
[PMID: 6763288]
[60]
Logroscino, G.; Traynor, B.J.; Hardiman, O.; Chiò, A.; Mitchell, D.; Swingler, R.J.; Millul, A.; Benn, E.; Beghi, E. EURALS. Incidence of amyotrophic lateral sclerosis in Europe. J. Neurol. Neurosurg. Psychiatry, 2010, 81(4), 385-390.
[http://dx.doi.org/10.1136/jnnp.2009.183525 ] [PMID: 19710046]
[61]
Rosen, D.R.; Siddique, T.; Patterson, D.; Figlewicz, D.A.; Sapp, P.; Hentati, A.; Donaldson, D.; Goto, J.; O’Regan, J.P.; Deng, H.X. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature, 1993, 362(6415), 59-62.
[http://dx.doi.org/10.1038/362059a0 ] [PMID: 8446170]
[62]
Cacciapuoti, F. Oxidative stress as “mother” of many human diseases at strong clinical impact. J Cardiovasc Med Cardiol., 2016, 3, 1-6.
[63]
Fogarty, M.J. Amyotrophic lateral sclerosis as a synaptopathy. Neural Regen. Res., 2019, 14(2), 189-192.
[http://dx.doi.org/10.4103/1673-5374.244782 ] [PMID: 30530995]
[64]
Tubert-Brohman, I.; Sherman, W.; Repasky, M.; Beuming, T. Improved docking of polypeptides with Glide. J. Chem. Inf. Model., 2013, 53(7), 1689-1699.
[http://dx.doi.org/10.1021/ci400128m ] [PMID: 23800267]
[65]
Ngo, S.T.; Mi, J.D.; Henderson, R.D.; McCombe, P.A.; Steyn, F.J. Exploring targets and therapies for amyotrophic lateral sclerosis: current insights into dietary interventions. Degener. Neurol. Neuromuscul. Dis., 2017, 7, 95-108.
[http://dx.doi.org/10.2147/DNND.S120607 ] [PMID: 30050381]
[66]
Beghi, E.; Chiò, A.; Couratier, P.; Esteban, J.; Hardiman, O.; Logroscino, G.; Millul, A.; Mitchell, D.; Preux, P.M.; Pupillo, E.; Stevic, Z.; Swingler, R.; Traynor, B.J.; Van den Berg, L.H.; Veldink, J.H.; Zoccolella, S. Eurals Consortium. The epidemiology and treatment of ALS: focus on the heterogeneity of the disease and critical appraisal of therapeutic trials. Amyotroph. Lateral Scler., 2011, 12(1), 1-10.
[http://dx.doi.org/10.3109/17482968.2010.502940 ] [PMID: 20698807]
[67]
Orrell, R.W.; Lane, R.J.M.; Ross, M. A systematic review of antioxidant treatment for amyotrophic lateral sclerosis/motor neuron disease. Amyotroph. Lateral Scler., 2008, 9(4), 195-211.
[http://dx.doi.org/10.1080/17482960801900032 ] [PMID: 18608090]
[68]
Dharmadasa, T.; Kiernan, M.C. Riluzole, disease stage and survival in ALS. Lancet Neurol., 2018, 17(5), 385-386.
[http://dx.doi.org/10.1016/S1474-4422(18)30091-7 ] [PMID: 29525493]
[69]
Cruz, M.P. Edaravone (Radicava): A novel neuroprotective agent for the treatment of amyotrophic lateral sclerosis. P&T, 2018, 43(1), 25-28.
[PMID: 29290672]
[70]
Bhandari, R.; Kuhad, A.; Kuhad, A. Edaravone: a new hope for deadly amyotrophic lateral sclerosis. Drugs Today (Barc), 2018, 54(6), 349-360.
[http://dx.doi.org/10.1358/dot.2018.54.6.2828189 ] [PMID: 29998226]
[71]
Faissner, S. Letter to the editor regarding Gholamzad et al., “A comprehensive review on the treatment approaches of multiple sclerosis: currently and in the future. Inflamm. Res., 2020, 69(2), 153.
[http://dx.doi.org/10.1007/s00011-019-01310-3 ] [PMID: 31927617]
[72]
Zarei, S.; Carr, K.; Reiley, L.; Diaz, K.; Guerra, O.; Altamirano, P.F.; Pagani, W.; Lodin, D.; Orozco, G.; Chinea, A. A comprehensive review of amyotrophic lateral sclerosis. Surg. Neurol. Int., 2015, 6(1), 171.
[http://dx.doi.org/10.4103/2152-7806.169561 ] [PMID: 26629397]
[73]
Calabresi, P.A.; Kieseier, B.C.; Arnold, D.L.; Balcer, L.J.; Boyko, A.; Pelletier, J.; Liu, S.; Zhu, Y.; Seddighzadeh, A.; Hung, S.; Deykin, A. ADVANCE Study Investigators. Pegylated interferon β-1a for relapsing-remitting multiple sclerosis (ADVANCE): a randomised, phase 3, double-blind study. Lancet Neurol., 2014, 13(7), 657-665.
[http://dx.doi.org/10.1016/S1474-4422(14)70068-7 ] [PMID: 24794721]
[74]
Cohen, J.A.; Coles, A.J.; Arnold, D.L.; Confavreux, C.; Fox, E.J.; Hartung, H.P.; Havrdova, E.; Selmaj, K.W.; Weiner, H.L.; Fisher, E.; Brinar, V.V.; Giovannoni, G.; Stojanovic, M.; Ertik, B.I.; Lake, S.L.; Margolin, D.H.; Panzara, M.A.; Compston, D.A. CARE-MS I investigators. Alemtuzumab versus interferon beta 1a as first-line treatment for patients with relapsing-remitting multiple sclerosis: a randomised controlled phase 3 trial. Lancet, 2012, 380(9856), 1819-1828.
[http://dx.doi.org/10.1016/S0140-6736(12)61769-3 ] [PMID: 23122652]
[75]
Coles, A.J.; Twyman, C.L.; Arnold, D.L.; Cohen, J.A.; Confavreux, C.; Fox, E.J.; Hartung, H.P.; Havrdova, E.; Selmaj, K.W.; Weiner, H.L.; Miller, T.; Fisher, E.; Sandbrink, R.; Lake, S.L.; Margolin, D.H.; Oyuela, P.; Panzara, M.A.; Compston, D.A. CARE-MS II investigators. Alemtuzumab for patients with relapsing multiple sclerosis after disease-modifying therapy: a randomised controlled phase 3 trial. Lancet, 2012, 380(9856), 1829-1839.
[http://dx.doi.org/10.1016/S0140-6736(12)61768-1 ] [PMID: 23122650]


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VOLUME: 20
ISSUE: 26
Year: 2020
Published on: 24 September, 2020
Page: [2391 - 2403]
Pages: 13
DOI: 10.2174/1568026620666200924114827
Price: $65

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