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Review

Pediatric multiple sclerosis: developments in timely diagnosis and prognostication

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Pages 393-403 | Received 23 Feb 2022, Accepted 07 Apr 2022, Published online: 13 Apr 2022

References

  • Fadda G, Armangue T, Hacohen Y, et al. Paediatric multiple sclerosis and antibody-associated demyelination: clinical, imaging, and biological considerations for diagnosis and care. Lancet Neurol. 2021;20(2):136–149.
  • Renoux C, Vukusic S, Mikaeloff Y, et al., Natural history of multiple sclerosis with childhood onset. N Engl J Med. 2007;356(25):2603–2613.
  • Mikaeloff Y, Adamsbaum C, Husson B, et al. MRI prognostic factors for relapse after acute CNS inflammatory demyelination in childhood. Brain. 2004;127(Pt 9):1942–1947.
  • Chabas D, Castillo-Trivino T, Mowry EM, et al. Vanishing MS T2-bright lesions before puberty: a distinct MRI phenotype? Neurology. 2008;71(14):1090–1093.
  • Abdel-Mannan O, Cortese R, Wassmer E, et al. Primary progressive multiple sclerosis presenting under the age of 18 years: fact or fiction? Mult Scler. 2021;27(2):309–314.
  • McKay KA, Hillert J, Manouchehrinia A. Long-term disability progression of pediatric-onset multiple sclerosis. Neurology. 2019;92(24):e2764–e2773.
  • Waubant E, Chabas D, Okuda DT, et al. Difference in disease burden and activity in pediatric patients on brain magnetic resonance imaging at time of multiple sclerosis onset vs adults. Arch Neurol. 2009;66(8):967–971.
  • Belman AL, Krupp LB, Olsen CS, et al. Characteristics of children and adolescents with multiple sclerosis. Pediatrics. 2016;138(1). https://doi.org/10.1542/peds.2016-0120.
  • Chitnis T, Glanz B, Jaffin S, et al. Demographics of pediatric-onset multiple sclerosis in an MS center population from the Northeastern United States. Mult Scler. 2009;15(5):627–631.
  • McKay KA, Manouchehrinia A, Berrigan L, et al. Long-term cognitive outcomes in patients with pediatric-onset vs adult-onset multiple sclerosis. JAMA Neurol. 2019;76(9):1028–1034.
  • Amato MP, Krupp LB, Charvet LE, et al. Pediatric multiple sclerosis: cognition and mood. Neurology. 2016;87(9 Suppl 2):S82–87.
  • Krysko KM, Graves JS, Rensel M, et al. Real-world effectiveness of initial disease-modifying therapies in pediatric multiple sclerosis. Ann Neurol. 2020;88(1):42–55.
  • Baroncini D, Simone M, Iaffaldano P, et al. Risk of persistent disability in patients with pediatric-onset multiple sclerosis. JAMA Neurol. 2021;78(6):726–735.
  • Bar-Or A, Hintzen RQ, Dale RC, et al. Immunopathophysiology of pediatric CNS inflammatory demyelinating diseases. Neurology. 2016;87(9 Suppl 2):S12–19.
  • Chitnis T, Aaen G, Belman A, et al. Improved relapse recovery in paediatric compared to adult multiple sclerosis. Brain. 2020;143(9):2733–2741.
  • Filippi M, Bruck W, Chard D, et al. Association between pathological and MRI findings in multiple sclerosis. Lancet Neurol. 2019;18(2):198–210.
  • Goldschmidt T, Antel J, Konig FB, et al. Remyelination capacity of the MS brain decreases with disease chronicity. Neurology. 2009;72(22):1914–1921.
  • Albert M, Antel J, Bruck W, et al. Extensive cortical remyelination in patients with chronic multiple sclerosis. Brain Pathol. 2007;17(2):129–138.
  • Pfeifenbring S, Bunyan RF, Metz I, et al. Extensive acute axonal damage in pediatric multiple sclerosis lesions. Ann Neurol. 2015;77(4):655–667.
  • Yeh EA, Weinstock-Guttman B, Ramanathan M, et al. Magnetic resonance imaging characteristics of children and adults with paediatric-onset multiple sclerosis. Brain. 2009;132(Pt 12):3392–3400.
  • Ghassemi R, Antel SB, Narayanan S, et al. Lesion distribution in children with clinically isolated syndromes. Ann Neurol. 2008;63(3):401–405.
  • Verhey LH, Signori A, Arnold DL, et al. Clinical and MRI activity as determinants of sample size for pediatric multiple sclerosis trials. Neurology. 2013;81(14):1215–1221.
  • Ghassemi R, Narayanan S, Banwell B, et al. Quantitative determination of regional lesion volume and distribution in children and adults with relapsing-remitting multiple sclerosis. PLoS One. 2014;9(2):e85741.
  • Paus T. Mapping brain maturation and cognitive development during adolescence. Trends Cogn Sci. 2005;9(2):60–68.
  • De Meo E, Filippi M, Trojano M, et al., Comparing natural history of early and late onset pediatric multiple sclerosis. Ann Neurol. 2022;91(4):483–495.
  • Longoni G, Brown RA, MomayyezSiahkal P, et al. White matter changes in paediatric multiple sclerosis and monophasic demyelinating disorders. Brain. 2017;140(5):1300–1315.
  • Vishwas MS, Healy BC, Pienaar R, et al. Diffusion tensor analysis of pediatric multiple sclerosis and clinically isolated syndromes. AJNR Am J Neuroradiol. 2013;34(2):417–423.
  • Margoni M, Villani U, Finos L, et al. Neurite orientation dispersion and density imaging discloses early changes in the normal-appearing white matter in paediatric multiple sclerosis. J Neurol Neurosurg Psychiatry. 2022;93(3):332–334.
  • Akbar N, Giorgio A, Till C, et al. Alterations in functional and structural connectivity in pediatric-onset multiple sclerosis. PLoS One. 2016;11(1):e0145906.
  • Rocca MA, Sonkin M, Copetti M, et al. Diffusion tensor magnetic resonance imaging in very early onset pediatric multiple sclerosis. Mult Scler. 2016;22(5):620–627.
  • Lebel C, Walker L, Leemans A, et al. Microstructural maturation of the human brain from childhood to adulthood. Neuroimage. 2008;40(3):1044–1055.
  • Rocca MA, De Meo E, Amato MP, et al. Cognitive impairment in paediatric multiple sclerosis patients is not related to cortical lesions. Mult Scler. 2015;21(7):956–959.
  • Absinta M, Rocca MA, Moiola L, et al. Cortical lesions in children with multiple sclerosis. Neurology. 2011;76(10):910–913.
  • Calabrese M, Seppi D, Romualdi C, et al. Gray matter pathology in MS: a 3-year longitudinal study in a pediatric population. AJNR Am J Neuroradiol. 2012;33(8):1507–1511.
  • Fadda G, Brown RA, Magliozzi R, et al., A surface-in gradient of thalamic damage evolves in pediatric multiple sclerosis. Ann Neurol. 2019;85(3):340–351.
  • De Meo E, Meani A, Moiola L, et al., Dynamic gray matter volume changes in pediatric multiple sclerosis: a 3.5 year MRI study. Neurology. 2019;92(15):e1709–e1723.
  • De Meo E, Storelli L, Moiola L, et al. In vivo gradients of thalamic damage in paediatric multiple sclerosis: a window into pathology. Brain. 2021;144(1):186–197.
  • Bonacchi R, Meani A, Pagani E, et al., Association of age at onset with gray matter volume and white matter microstructural abnormalities in people with multiple sclerosis. Neurology. 2021;97(20):e2007–e2019.
  • Weier K, Till C, Fonov V, et al. Contribution of the cerebellum to cognitive performance in children and adolescents with multiple sclerosis. Mult Scler. 2016;22(5):599–607.
  • Aubert-Broche B, Fonov V, Narayanan S, et al. Onset of multiple sclerosis before adulthood leads to failure of age-expected brain growth. Neurology. 2014;83(23):2140–2146.
  • Tomassini V, Matthews PM, Thompson AJ, et al. Neuroplasticity and functional recovery in multiple sclerosis. Nat Rev Neurol. 2012;8(11):635–646.
  • Gruchot J, Weyers V, Gottle P, et al. The molecular basis for remyelination failure in multiple sclerosis. Cells. 2019;8(8):825.
  • Ghassemi R, Brown R, Banwell B, et al. Canadian pediatric demyelinating disease study g. quantitative measurement of tissue damage and recovery within new T2w lesions in pediatric- and adult-onset multiple sclerosis. Mult Scler. 2015;21(6):718–725.
  • Brown RA, Narayanan S, Banwell B, et al. Magnetization transfer ratio recovery in new lesions decreases during adolescence in pediatric-onset multiple sclerosis patients. Neuroimage Clin. 2014;6:237–242.
  • Kolb B, Gibb R. Brain plasticity and behaviour in the developing brain. J Can Acad Child Adolesc Psychiatry. 2011;20(4):265–276.
  • Barlow-Krelina E, Turner GR, Akbar N, et al. Enhanced recruitment during executive control processing in cognitively preserved patients with pediatric-onset MS. J Int Neuropsychol Soc. 2019;25(4):432–442.
  • Rocca MA, Valsasina P, Absinta M, et al. Intranetwork and internetwork functional connectivity abnormalities in pediatric multiple sclerosis. Hum Brain Mapp. 2014;35(8):4180–4192.
  • De Meo E, Moiola L, Ghezzi A, et al. MRI substrates of sustained attention system and cognitive impairment in pediatric MS patients. Neurology. 2017;89(12):1265–1273.
  • Rocca MA, Absinta M, Ghezzi A, et al. Is a preserved functional reserve a mechanism limiting clinical impairment in pediatric MS patients? Hum Brain Mapp. 2009;30(9):2844–2851.
  • Rocca MA, Absinta M, Moiola L, et al. Functional and structural connectivity of the motor network in pediatric and adult-onset relapsing-remitting multiple sclerosis. Radiology. 2010;254(2):541–550.
  • Thompson AJ, Banwell BL, Barkhof F, et al. Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol. 2018;17(2):162–173.
  • Hacohen Y, Brownlee W, Mankad K, et al. Improved performance of the 2017 McDonald criteria for diagnosis of multiple sclerosis in children in a real-life cohort. Mult Scler. 2020;26(11):1372–1380.
  • Wong YYM, de Mol CL, van der Vuurst de Vries RM, et al. Real-world validation of the 2017 McDonald criteria for pediatric MS. Neurol Neuroimmunol Neuroinflamm. 2019;6(2):e528.
  • Fadda G, Brown RA, Longoni G, et al., MRI and laboratory features and the performance of international criteria in the diagnosis of multiple sclerosis in children and adolescents: a prospective cohort study. Lancet Child Adolesc Health. 2018;2(3):191–204.
  • Rostasy K, Mader S, Schanda K, et al. Anti-myelin oligodendrocyte glycoprotein antibodies in pediatric patients with optic neuritis. Arch Neurol. 2012;69(6):752–756.
  • Hacohen Y, Absoud M, Deiva K, et al. Myelin oligodendrocyte glycoprotein antibodies are associated with a non-MS course in children. Neurol Neuroimmunol Neuroinflamm. 2015;2(2):e81.
  • Hacohen Y, Mankad K, Chong WK, et al. Diagnostic algorithm for relapsing acquired demyelinating syndromes in children. Neurology. 2017;89(3):269–278.
  • Verhey LH, Branson HM, Shroff MM, et al. MRI parameters for prediction of multiple sclerosis diagnosis in children with acute CNS demyelination: a prospective national cohort study. Lancet Neurol. 2011;10(12):1065–1073.
  • Mikaeloff Y, Suissa S, Vallee L, et al. First episode of acute CNS inflammatory demyelination in childhood: prognostic factors for multiple sclerosis and disability. J Pediatr. 2004;144(2):246–252. hazard ratio [HR]=0.23 [95% confidence interval, CI=0.10-0.56]; and 0.59 [95% CI=0.33-1.07]), whereas age at onset ≥ 10 years and the presence of an optic nerve lesion on MRI at onset increased the risk of a second clinical attack (HR=1.67 [95% CI=1.04-2.67] and 2.59 [95% CI=1.27-5.29], respectively.
  • Iaffaldano P, Simone M, Lucisano G, et al. Prognostic indicators in pediatric clinically isolated syndrome. Ann Neurol. 2017;81(5):729–739. [95% CI=1.06-1.55]; and HR=1.42 [95% CI=1.10-1.84]), whereas exposure to disease modifying therapies was protective (HR=0.75 [95% CI=0.60-0.95]). The presence of oligoclonal bands was not predictive of time to a second attack.
  • Heussinger N, Kontopantelis E, Gburek-Augustat J, et al. Oligoclonal bands predict multiple sclerosis in children with optic neuritis. Ann Neurol. 2015;77(6):1076–1082.
  • van der Vuurst de Vries RM, Wong YYM, Mescheriakova JY, et al. High neurofilament levels are associated with clinically definite multiple sclerosis in children and adults with clinically isolated syndrome. Mult Scler. 2019;25(7):958–967.
  • van der Vuurst de Vries RM, van Pelt ED, Mescheriakova JY, et al. Disease course after clinically isolated syndrome in children versus adults: a prospective cohort study. Eur J Neurol. 2017;24(2):315–321.
  • Boiko A, Vorobeychik G, Paty D, et al., University of British Columbia MSCN. Early onset multiple sclerosis: a longitudinal study. Neurology. 2002;59(7):1006–1010.
  • De Meo E, Bonacchi R, Moiola L, et al., Early predictors of 9-year disability in pediatric multiple sclerosis. Ann Neurol. 2021;89(5):1011–1022.
  • Pinhas-Hamiel O, Sarova-Pinhas I, Achiron A. Multiple sclerosis in childhood and adolescence: clinical features and management. Paediatr Drugs. 2001;3(5):329–336.
  • Neuteboom RF, Boon M, Catsman Berrevoets CE, et al. Prognostic factors after a first attack of inflammatory CNS demyelination in children. Neurology. 2008;71(13):967–973.
  • Mikaeloff Y, Caridade G, Assi S, et al. Prognostic factors for early severity in a childhood multiple sclerosis cohort. Pediatrics. 2006;118(3):1133–1139.
  • Akhtar S, Alroughani R, Ahmed SF, et al. Prognostic indicators of secondary progression in a paediatric-onset multiple sclerosis cohort in Kuwait. Mult Scler. 2016;22(8):1086–1093.
  • Pascual-Leone A, Amedi A, Fregni F, et al. The plastic human brain cortex. Annu Rev Neurosci. 2005;28(1):377–401.
  • Zatorre RJ, Fields RD, Johansen-Berg H. Plasticity in gray and white: neuroimaging changes in brain structure during learning. Nat Neurosci. 2012;15(4):528–536.
  • Margoni M, Rinaldi F, Perini P, et al. Therapy of pediatric-onset multiple sclerosis: state of the art, challenges, and opportunities. Front Neurol. 2021;12:676095.
  • Zipoli V, Goretti B, Hakiki B, et al. Cognitive impairment predicts conversion to multiple sclerosis in clinically isolated syndromes. Mult Scler. 2010;16(1):62–67.
  • Carotenuto A, Moccia M, Costabile T, et al. Associations between cognitive impairment at onset and disability accrual in young people with multiple sclerosis. Sci Rep. 2019;9(1):18074.
  • Wattjes MP, Ciccarelli O, Reich DS, et al. MAGNIMS-CMSC-NAIMS consensus recommendations on the use of MRI in patients with multiple sclerosis. Lancet Neurol. 2021;20(8):653–670.

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