Benign course in multiple sclerosis: a review

Since the 1950s, it has been recognized that a subgroup of multiple sclerosis (MS) patients exists that shows little or no progression in the severity of the disease over time. This group is referred to as ‘benign’ MS. Although a substantial amount of research in MS indicates a multifactorial background in disease severity, to date it is still difficult to predict whether the course will be benign at onset and it is difficult to find factors that influence the course of the disease over time. Maintaining or restoring neural conduction inside a central nervous system lesion seems to be the essence of staying ‘benign’.

[1]  S. Reingold,et al.  Defining the clinical course of multiple sclerosis , 1996, Neurology.

[2]  E. Norrby,et al.  Genetic basis of multiple sclerosis: HLA antigens, disease progression, and oligoclonal IgG in CSF , 1979, Acta neurologica Scandinavica.

[3]  A. Thompson,et al.  Patterns of disease activity in multiple sclerosis: clinical and magnetic resonance imaging study. , 1990, BMJ.

[4]  A. Prange,et al.  Course and prognosis of chronic progressive multiple sclerosis: Results of an epidemiological study , 1988, Acta neurologica Scandinavica.

[5]  W. Mcdonald,et al.  The longstanding MS lesion. A quantitative MRI and electron microscopic study. , 1991, Brain : a journal of neurology.

[6]  C. Marsden,et al.  Differentiation of multiple system atrophy from idiopathic Parkinson's disease using proton magnetic resonance spectroscopy , 1995, Annals of neurology.

[7]  G. Vega,et al.  Apolipoproteins in human cerebrospinal fluid. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[8]  S. Poser,et al.  Age at onset, initial symptomatology and the course of multiple sclerosis , 1982, Acta neurologica Scandinavica.

[9]  H. Carton,et al.  Clinical parameters and intrathecal IgG synthesis as prognostic features in multiple sclerosis. Part I , 2004, Journal of Neurology.

[10]  S H Snyder,et al.  A novel neuronal messenger molecule in brain: The free radical, nitric oxide , 1992, Annals of neurology.

[11]  D. Middleton,et al.  A study of the HLA-DR region in clinical subgroups of multiple sclerosis and its influence on prognosis , 1999, Journal of the Neurological Sciences.

[12]  P. Klivényi,et al.  The Prevalence of Multiple Sclerosis, Distribution of Clinical Forms of the Disease and Functional Status of Patients in Csongrád County, Hungary , 2001, European Neurology.

[13]  Anders Odén,et al.  Prediction of outcome in multiple sclerosis based on multivariate models , 1994, Journal of Neurology.

[14]  A. Ghezzi,et al.  The benign form of multiple sclerosis , 1984 .

[15]  M. Amato,et al.  A prospective study on the prognosis of multiple sclerosis , 2000, Neurological Sciences.

[16]  Massimo Filippi,et al.  A spinal cord MRI study of benign and secondary progressive multiple sclerosis , 2004, Journal of Neurology.

[17]  Sandro Sorbi,et al.  Benign multiple sclerosis , 2006, Journal of Neurology.

[18]  J. Kurtzke,et al.  Survival in multiple sclerosis. , 1989, Journal of clinical epidemiology.

[19]  R. Muller Course and prognosis of disseminated sclerosis in relation to age of onset. , 1951, A.M.A. archives of neurology and psychiatry.

[20]  A. Thompson,et al.  A clinical and laboratory study of benign multiple sclerosis. , 1986, The Quarterly journal of medicine.

[21]  P. Christiansen,et al.  Early Time Course of JV-Acetylaspartate , Creatine and Phosphocreatine , and Compounds Containing Choline in the Brain After Acute Stroke , 2005 .

[22]  S. Croul,et al.  Oxidative damage to mitochondrial DNA and activity of mitochondrial enzymes in chronic active lesions of multiple sclerosis , 2000, Journal of the Neurological Sciences.

[23]  N. Wilczak,et al.  Beta 2-adrenoceptor involvement in inflammatory demyelination and axonal degeneration in multiple sclerosis. , 2004, Trends in pharmacological sciences.

[24]  L. Steinman A few autoreactive cells in an autoimmune infiltrate control a vast population of nonspecific cells: a tale of smart bombs and the infantry. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[25]  F. Muntoni,et al.  Multiple sclerosis in Sardinia is associated and in linkage disequilibrium with HLA-DR3 and -DR4 alleles. , 1997, American journal of human genetics.

[26]  B. Weinshenker,et al.  Identifying disease modifying genes in multiple sclerosis , 2002, Journal of Neuroimmunology.

[27]  R. Forbes,et al.  An epidemiologic study of multiple sclerosis in Northern Ireland. , 1999, Neurology.

[28]  P. Pocklington,et al.  Course of multiple sclerosis. First results of a prospective study carried out of 102 MS patients from 1976-1980. , 1982, Acta neurologica Scandinavica.

[29]  O. Kantarci,et al.  Survival and predictors of disability in Turkish MS patients , 1998, Neurology.

[30]  J. Baskerville,et al.  The natural history of multiple sclerosis: a geographically based study. 5. The clinical features and natural history of primary progressive multiple sclerosis. , 1999, Brain : a journal of neurology.

[31]  A. Thompson,et al.  Serial gadolinium‐enhanced MRI in relapsing/remitting multiple sclerosis of varying disease duration , 1992, Neurology.

[32]  K. Spitzer,et al.  Prognostic relevance of initial clinical and paraclinical parameters for the course of multiple sclerosis , 1988, Journal of Neuroimmunology.

[33]  Kenneth J. Smith,et al.  Electrically active axons degenerate when exposed to nitric oxide , 2001, Annals of neurology.

[34]  Y. Lapierre,et al.  Clinical Sub-Groups of Multiple Sclerosis in Relation to HLA: DR Alleles as Possible Markers of Disease Progression , 1985, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[35]  A. Goris,et al.  High-resolution analysis of IL-6 minisatellite polymorphism in Sardinian multiple sclerosis: effect on course and onset of disease , 2000, Genes and Immunity.

[36]  C. Pozzilli,et al.  Prospective study of multiple sclerosis with early onset , 2002, Multiple sclerosis.

[37]  T. Riise,et al.  Prognostic factors for life expectancy in multiple sclerosis analysed by Cox-models. , 1988, Journal of clinical epidemiology.

[38]  William H. Oldendorf,et al.  N-Acetyl-L-Aspartic acid: A literature review of a compound prominent in 1H-NMR spectroscopic studies of brain , 1989, Neuroscience & Biobehavioral Reviews.

[39]  A. Hirano,et al.  Asymptomatic Demyelinated Plaque , 1974 .

[40]  R. Herndon,et al.  Multiple sclerosis. The spectrum of severity. , 1983, Archives of neurology.

[41]  K. Lauer,et al.  Prognostic criteria in an epidemiological group of patients with multiple sclerosis: an exploratory study , 1992, Journal of Neurology.

[42]  K. Lauer,et al.  Epidemiological investigations into multiple sclerosis in Southern Hesse. V. Course and prognosis , 1987, Acta neurologica Scandinavica.

[43]  P. Livrea,et al.  Course and prognosis in early-onset MS , 2002, Neurology.

[44]  J. Haines,et al.  HLA-DR2 dose effect on susceptibility to multiple sclerosis and influence on disease course. , 2003, American journal of human genetics.

[45]  G. Serio,et al.  Multivariate analysis of predictive factors of multiple sclerosis course with a validated method to assess clinical events. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[46]  T. Olsen,et al.  Early Time Course of N‐Acetylaspartate, Creatine and Phosphocreatine, and Compounds Containing Choline in the Brain After Acute Stroke: A Proton Magnetic Resonance Spectroscopy Study , 1992, Stroke.

[47]  D. Mcalpine The benign form of multiple sclerosis. A study based on 241 cases seen within three years of onset and followed up until the tenth year or more of the disease. , 1961, Brain : a journal of neurology.

[48]  K. Lauer,et al.  Early prognostic factors for disability in multiple sclerosis, a European multicenter study , 1992, Acta neurologica Scandinavica.

[49]  W. I. McDonald,et al.  Heterogeneity of blood‐brain barrier changes in multiple sclerosis , 1990, Neurology.

[50]  O. Andersen,et al.  Prognostic factors in a multiple sclerosis incidence cohort with twenty-five years of follow-up. , 1993, Brain : a journal of neurology.

[51]  K. Smith,et al.  Nitric oxide donors reversibly block axonal conduction: demyelinated axons are especially susceptible. , 1997, Brain : a journal of neurology.

[52]  V. Clark,et al.  Onset symptoms as predictors of mortality and disability in multiple sclerosis , 1984, Acta neurologica Scandinavica.

[53]  V. Clark,et al.  Factors associated with a malignant or benign course of multiple sclerosis. , 1982, JAMA.

[54]  G. Barker,et al.  Correlation of magnetization transfer ration with clinical disability in multiple sclerosis , 1994, Annals of neurology.

[55]  T Locatelli,et al.  Brain magnetic resonance imaging and multimodal evoked potentials in benign and secondary progressive multiple sclerosis. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[56]  David E. Anderson,et al.  Molecular pathogenesis of multiple sclerosis , 1999, Journal of Neuroimmunology.

[57]  T. L. Bennett,et al.  In Search of a Conceptualization of Multiple Sclerosis: A Historical Perspective , 2003, Neuropsychology Review.

[58]  K. Gharagozli,et al.  Multiple sclerosis: report on 200 cases from Iran , 2003, Multiple sclerosis.

[59]  R. P. Mackay,et al.  Forms of benign multiple sclerosis. Report of two "clinically silent" cases discovered at autopsy. , 1967, Archives of neurology.

[60]  E. Waubant,et al.  Multiple sclerosis that is progressive from the time of onset: clinical characteristics and progression of disability. , 1999, Archives of neurology.

[61]  V Cosi,et al.  Multiple sclerosis: disability and mortality in a cohort of clinically diagnosed patients. , 1989, Neuroepidemiology.

[62]  T. Pekmezović,et al.  Survival of Multiple Sclerosis Patients in the Belgrade Population , 2002, Neuroepidemiology.

[63]  P. Cabre,et al.  MS and neuromyelitis optica in Martinique (French West Indies) , 2001, Neurology.

[64]  M. Mendez,et al.  Malignant monophasic multiple sclerosis or “Marburg's disease" , 1988, Neurology.

[65]  J. Birley,et al.  A CLINICAL AND EXPERIMENTAL CONTRIBUTION TO THE PATHOGENESIS OF DISSEMINATED SCLEROSIS , 1921 .

[66]  J. G. Phadke Clinical aspects of multiple sclerosis in north-east Scotland with particular reference to its course and prognosis. , 1990, Brain : a journal of neurology.

[67]  G V McDonnell,et al.  Benign multiple sclerosis? Clinical course, long term follow up, and assessment of prognostic factors , 1999, Journal of neurology, neurosurgery, and psychiatry.

[68]  M. Hutchinson Disability due to multiple sclerosis: a community-based study on an Irish county. , 1986, Irish medical journal.

[69]  J. G. Phadke Survival pattern and cause of death in patients with multiple sclerosis: results from an epidemiological survey in north east Scotland. , 1987, Journal of neurology, neurosurgery, and psychiatry.

[70]  G. Aimard,et al.  Course and prognosis of multiple sclerosis assessed by the computerized data processing of 349 patients. , 1980, Brain : a journal of neurology.

[71]  K. Lauer,et al.  Prognostic indicators in multiple sclerosis , 1986, Acta neurologica Scandinavica.

[72]  D. Goodin Survey of multiple sclerosis in Northern California , 1999 .

[73]  N. Maurits,et al.  Early prediction of a benign course of multiple sclerosis on clinical grounds: a systematic review , 2001, Multiple sclerosis.

[74]  J. Baskerville,et al.  The natural history of multiple sclerosis: a geographically based study. 3. Multivariate analysis of predictive factors and models of outcome. , 1991, Brain : a journal of neurology.

[75]  Wolfgang Brück,et al.  Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time. , 2002, Brain : a journal of neurology.

[76]  C. Buttinelli,et al.  Evolution and severity markers in 233 MS patients. , 1987, Rivista di neurologia.

[77]  M. Hakama,et al.  Survival of multiple sclerosis in Finland between 1964 and 1993 , 2002, Multiple sclerosis.

[78]  Pierre Marie's Lectures on Diseases of the Spinal Cord , 1895, Glasgow Medical Journal.

[79]  W. Firnhaber,et al.  PROGNOSTIC CRITERIA IN MULTIPLE SCLEROSIS , 1965, Annals of the New York Academy of Sciences.

[80]  C. Wolfson,et al.  A Markov model of the natural history of multiple sclerosis. , 1985, Neuroepidemiology.

[81]  D. Mcalpine The Benign form of Multiple Sclerosis: Results of a Long-term Study , 1964, British medical journal.

[82]  M. Alter,et al.  CLINICAL FACTORS ASSOCIATED WITH INCREASED DISABILITY IN MULTIPLE SCLEROSIS , 1970, Acta neurologica Scandinavica.

[83]  A Benazzouz,et al.  Lysolecithin-induced demyelination in primates: preliminary in vivo study with MR and magnetization transfer. , 1995, AJNR. American journal of neuroradiology.

[84]  W. Brück,et al.  Acute axonal injury in multiple sclerosis. Correlation with demyelination and inflammation. , 2000, Brain : a journal of neurology.

[85]  John Noseworthy,et al.  Clinical implications of benign multiple sclerosis: A 20‐year population‐based follow‐up study , 2004, Annals of neurology.

[86]  Alireza Minagar,et al.  Blood-brain barrier disruption in multiple sclerosis , 2003, Multiple sclerosis.

[87]  P. Adeleine,et al.  Early clinical predictors and progression of irreversible disability in multiple sclerosis: an amnesic process. , 2003, Brain : a journal of neurology.

[88]  T. Riise,et al.  Prognostic factors for survival in multiple sclerosis: a longitudinal, population based study in Møre and Romsdal, Norway. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[89]  B. Bramwell Clinical Studies. XII.—The Prognosis in Disseminated Sclerosis; Duration in Two Hundred Cases of Disseminated Sclerosis , 1917, Edinburgh Medical Journal.

[90]  P. Rudge The value of natural history studies of multiple sclerosis. , 1999, Brain : a journal of neurology.

[91]  A. Svejgaard,et al.  HL-A antigens and multiple sclerosis. , 1972, Lancet.

[92]  P. Gallo,et al.  The HLA-DR13 haplotype is associated with “benign” multiple sclerosis in northeast Italy , 2001, Neurology.

[93]  E. A. Velde,et al.  Presenting signs and symptoms in multiple sclerosis , 1986, Acta neurologica Scandinavica.

[94]  D. Turnbull,et al.  Mitochondrial dysfunction plays a key role in progressive axonal loss in Multiple Sclerosis. , 2005, Medical hypotheses.

[95]  R. Fossdal,et al.  The natural history of untreated multiple sclerosis in Iceland. A total population-based 50 year prospective study , 2002, Clinical Neurology and Neurosurgery.

[96]  T. Pekmezović,et al.  Prognostic factors for survival in multiple sclerosis , 1999, Multiple sclerosis.

[97]  Gianfranco Siracusa,et al.  A prospective study on the natural history of multiple sclerosis: clues to the conduct and interpretation of clinical trials , 1999, Journal of the Neurological Sciences.

[98]  A. D. Roses,et al.  Association of apolipoprotein E allele €4 with late-onset familial and sporadic Alzheimer’s disease , 2006 .

[99]  J. Valk,et al.  1H and 31P magnetic resonance spectroscopy of the brain in degenerative cerebral disorders , 1992, Annals of neurology.

[100]  T. Richards Proton MR spectroscopy in multiple sclerosis: value in establishing diagnosis, monitoring progression, and evaluating therapy. , 1991, AJR. American journal of roentgenology.

[101]  P. Pocklington,et al.  Course of multiple sclerosis , 1982 .

[102]  G. Barker,et al.  1H magnetic resonance spectroscopy of chronic cerebral white matter lesions and normal appearing white matter in multiple sclerosis , 1997, Journal of neurology, neurosurgery, and psychiatry.

[103]  G. Beebe,et al.  Studies on the natural history of multiple sclerosis--8. Early prognostic features of the later course of the illness. , 1977, Journal of chronic diseases.

[104]  M. Guérin,et al.  Neurodegenerative disorders: the role of peroxynitrite , 1999, Brain Research Reviews.

[105]  D. Li,et al.  Benign versus chronic progressive multiple sclerosis: Magnetic resonance imaging features , 1989, Annals of neurology.

[106]  J. Kurtzke Rating neurologic impairment in multiple sclerosis , 1983, Neurology.

[107]  N. Evangelou,et al.  Association of the APOE ε4 allele with disease activity in multiple sclerosis , 1999, Journal of neurology, neurosurgery, and psychiatry.

[108]  D. Paty,et al.  A population-based study of multiple sclerosis in twins. , 1986, The New England journal of medicine.

[109]  R. Mahley,et al.  Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. , 1988, Science.

[110]  R. Weiner,et al.  Effects of ECT on diabetes mellitus , 1984, Acta psychiatrica Scandinavica.

[111]  Carlo Berzuini,et al.  Predicting secondary progression in relapsing–remitting multiple sclerosis: a Bayesian analysis , 2001, Journal of the Neurological Sciences.

[112]  D. Shepherd Clinical features of multiple sclerosis in north‐east Scotland , 1979, Acta neurologica Scandinavica.

[113]  M. Horsfield,et al.  Benign and secondary progressive multiple sclerosis: a preliminary quantitative MRI study , 1994, Journal of Neurology.