Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature

Oncel, Ibrahim; Solmaz, Ismail

doi:10.55730/1300-0144.5434

Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature

Ibrahim Oncel, (Hacettepe Üniversitesi, Tıp Fakültesi, Çocuk Sağlığı ve Hastalıkları Anabilim Dalı Çocuk Nörolojisi Anabilim Dalı, Ankara, Türkiye)

İsmail SOLMAZ (Hacettepe Üniversitesi, Tıp Fakültesi, Çocuk Sağlığı ve Hastalıkları Bölümü, Çocuk Nörolojisi Anabilim Dalı, Ankara, Türkiye)

Turkish Journal of Medical Sciences

2 1

Yıl: 2022 Cilt: 52 Sayı: 4 Sayfa Aralığı: 1281 - 1287 Metin Dili: İngilizce DOI: 10.55730/1300-0144.5434 İndeks Tarihi: 26-12-2022

Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature

Öz:

Background/aim: Clinically isolated syndrome (CIS) may be the first presentation of pediatric onset multiple sclerosis (POMS). We retrospectively evaluated the clinical and laboratory data of pediatric CIS (pCIS) patients who were diagnosed with POMS upon follow- up for any predictive variables. We also reviewed the literature concerning the management of pCIS. Materials and methods: This single-center study involved patients who had pCIS in childhood that converted to POMS during follow- up between 2011 and 2021. Sixteen patients were included in the study. The data were evaluated retrospectively and analyzed with descriptive statistics. Results: The majority of the pCIS patients were female (F/M: 10/6, 62/38%), and the first pCIS attack was at 13.3 ± 2.6 years old (mean ± SD). Mean follow-up was 3.1 ± 1.4 years; 6 of the patients relapsed within 1 year and 6 within 2 years. The time from the first pCIS attacks of the patients to the diagnosis of POMS was 15.75 ± 11.07 months. The annualized relapse rate (ARR) was 0.9 ± 0.7. The majority (68%) of the patients had a monosymptomatic onset, optic neuritis (ON) being the most common initial presentation (44%). Cerebrospinal fluid (CSF) oligoclonal bands (OCBs) were found in 9/12 (75%) and the immunoglobulin G index (IgG index) was elevated in 5/11 (45%). An autoimmune disorder was reported in the 1st or 2nd degree relatives of 6 patients: four (25%) MS, one ulcerative colitis, and one Hashimoto’s thyroiditis. Our pCIS patients did not receive any disease-modifying treatment (DMT) for their first attack. When the diagnosis changed to POMS, most (68%) were started on interferons. The Expanded Disability Status Scale (EDSS) increased in one patient during follow-up (EDSS: 3) while in the others it was 0 at the last visit. The literature is reviewed in order to compare results for suggestions regarding the management of pCIS. Conclusion: The presence of OCBs in the initial episode, MS in the family, and monosymptomatic onset may increase the possibility of developing POMS. Whether DMTs given at the pCIS stage are effective in preventing relapses and disability needs to be evaluated in longitudinal follow-up of large cohorts.

Anahtar Kelime: Pediatric clinically isolated syndrome multiple sclerosis predictive

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık

1. Fromont A, Binquet C, Sauleau EA, Fournel I, Bellisario A et al. Geographic variations of multiple sclerosis in France. Brain 2010; 133 (7): 1889-1899. https://doi.org/10.1093/brain/ awq134
2. Chitnis T, Glanz B, Jaffin S, Healy B. Demographics of pediatric- onset multiple sclerosis in an MS center population from the Northeastern United States. Multiple Sclerosis Journal 2009; 15 (5): 627-631. https://doi.org/10.1177/1352458508101933
3. Banwell B, Krupp L, Kennedy J, Tellier R, Tenembaum S et al. Clinical features and viral serologies in children with multiple sclerosis: a multinational observational study. The Lancet Neurology 2007; 6 (9): 773-781. https://doi.org/10.1016/s1474- 4422(07)70196-5
4. Renoux C, Vukusic S, Mikaeloff Y, Edan G, Clanet M et al. Natural history of multiple sclerosis with childhood onset. New England Journal of Medicine 2007; 356 (25): 2603-2613. https://doi.org/10.1056/NEJMoa067597
5. Mikaeloff Y, Caridade G, Assi S, Suissa S, Tardieu M. Prognostic factors for early severity in a childhood multiple sclerosis cohort. Pediatrics 2006; 118 (3): 1133-1139. https:// doi.org/10.1542/peds.2006-0655
6. Gorman MP, Healy BC, Polgar-Turcsanyi M, Chitnis T. Increased relapse rate in pediatric-onset compared with adult- onset multiple sclerosis. Archives of Neurology 2009; 66 (1): 54-59. https://doi.org/10.1001/archneurol.2008.505
7. Benson LA, Healy BC, Gorman MP, Baruch NF, Gholipour T et al. Elevated relapse rates in pediatric compared to adult MS persist for at least 6 years. Multiple Sclerosis and Related Disorders 2014; 3 (2): 186-193. https://doi.org/10.1016/j. msard.2013.06.004
8. Yeh EA, Weinstock-Guttman B, Ramanathan M, Ramasamy DP, Willis L et al. Magnetic resonance imaging characteristics of children and adults with paediatric-onset multiple sclerosis. Brain 2009; 132 (12): 3392-3400. https://doi.org/10.1093/ brain/awp278
9. Amato MP, Goretti B, Ghezzi A, Hakiki B, Niccolai C et al. Neuropsychological features in childhood and juvenile multiple sclerosis: five-year follow-up. Neurology 2014; 83 (16): 1432-1438. https://doi.org/10.1212/ wnl.0000000000000885
10. Öztürk Z, Gücüyener K, Soysal Ş, Konuşkan GD, Konuşkan B et al. Cognitive functions in pediatric multiple sclerosis: 2-years follow-up. Neurological Research 2020; 42 (2): 159- 163. https://doi.org/10.1080/01616412.2019.1710417
11. Ghassemi R, Narayanan S, Banwell B, Sled JG, Shroff M et al. Quantitative determination of regional lesion volume and distribution in children and adults with relapsing-remitting multiple sclerosis. PLoS One 2014; 9 (2): 85741. https://doi. org/10.1371/journal.pone.0085741
12. Chitnis T, Krupp L, Yeh A, Rubin J, Kuntz N et al. Pediatric multiple sclerosis. Neurologic clinics 2011; 29 (2): 481-505. https://doi.org/10.1016/j.ncl.2011.01.004.
13. Kopp TI, Blinkenberg M, Chalmer TA, Petersen T, Ravnborg MH et al. Predictors of treatment outcome in patients with paediatric onset multiple sclerosis. Multiple Sclerosis Journal 2020; 26 (8): 964-975. https://doi. org/10.1177/1352458519846100
14. Fisher KS, Cuascut FX, Rivera VM, Hutton GJ. Current Advances in Pediatric Onset Multiple Sclerosis. Biomedicines 2020; 8 (4): 71 https://doi.org/10.3390/biomedicines8040071
15. Rocca MA, Absinta M, Moiola L, Ghezzi A, Colombo B 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. https://doi. org/10.1148/radiol.09090463
16. Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA et al. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Annals of Neurology 2011; 69 (2): 292-302. https://doi.org/10.1002/ana.22366
17. Krupp LB, Tardieu M, Amato MP, Banwell B, Chitnis T et al. International Pediatric Multiple Sclerosis Study Group criteria for pediatric multiple sclerosis and immune-mediated central nervous system demyelinating disorders: revisions to the 2007 definitions. Multiple Sclerosis Journal 2013; 19 (10): 1261- 1267. https://doi.org/10.1177/1352458513484547
18. Miller DH, Chard DT, Ciccarelli O. Clinically isolated syndromes. The Lancet Neurology 2012; 11 (2): 157-169. https://doi.org/10.1016/s1474-4422(11)70274-5
19. Hacohen Y, Brownlee W, Mankad K, Chong WK, Thompson A et al. Improved performance of the 2017 McDonald criteria for diagnosis of multiple sclerosis in children in a real-life cohort. Multiple Sclerosis Journal 2020; 26 (11): 1372-1380. https:// doi.org/10.1177/1352458519863781
20. Grzegorski T, Losy J. What do we currently know about the clinically isolated syndrome suggestive of multiple sclerosis? An update. Reviews in the Neurosciences 2020; 31 (3): 335- 349. https://doi.org/10.1515/revneuro-2019-0084
21. Armoiry X, Kan A, Melendez-Torres GJ, Court R, Sutcliffe P et al. Short- and long-term clinical outcomes of use of beta- interferon or glatiramer acetate for people with clinically isolated syndrome: a systematic review of randomised controlled trials and network meta-analysis. Journal of Neurology 2018; 265 (5): 999-1009. https://doi.org/10.1007/ s00415-018-8752-8
22. Papetti L, Figà Talamanca L, Spalice A, Vigevano F, Centonze D et al. Predictors of Evolution Into Multiple Sclerosis After a First Acute Demyelinating Syndrome in Children and Adolescents. Frontiers in Neurology 2019; 9: 1156. https://doi. org/10.3389/fneur.2018.01156
23. Nourbakhsh B, Cordano C, Asteggiano C, Ruprecht K, Otto C et al. Multiple Sclerosis Is Rare in Epstein-Barr Virus-Seronegative Children with Central Nervous System Inflammatory Demyelination. Annals of Neurology 2021; 89 (6): 1234-1239. https://doi.org/10.1002/ana.26062
24. Kilic H, Mavi D, Yalcinkaya BC, Yildiz EP, Kizilkilic O et al. Evaluation of inflammatory acquired demyelinating syndromes in children: a single-center experience. Acta Neurologica Belgica 2021: 1-7. https://doi.org/10.1007/s13760-021-01703-4
25. Zouari Mallouli S, Ben Nsir S, Bouchaala W, Kamoun Feki F, Charfi Triki C. Acute Demyelinating Syndromes: A report of child neurology department of Sfax University Hospital. Multiple Sclerosis and Relatated Disorders 2021; 56: 103291. https://doi.org/10.1016/j.msard.2021.103291
26. Yılmaz Ü, Anlar B, Gücüyener K. Characteristics of pediatric multiple sclerosis: The Turkish pediatric multiple sclerosis database. European Journal of Paediatric Neurology 2017; 21 (6): 864-872. https://doi.org/10.1016/j.ejpn.2017.06.004
27. Tur C, Montalban X. CSF oligoclonal bands are important in the diagnosis of multiple sclerosis, unreasonably downplayed by the McDonald criteria 2010: No. Multiple Sclerosis Journal 2013; 19 (6): 717-718. https://doi.org/10.1177/1352458513477713
28. Bektaş G, Özkan MU, Yıldız EP, Uzunhan TA, Sencer S et al. Clinically isolated syndrome and multiple sclerosis in children: a single center study. The Turkish Journal of Pediatrics 2020; 62 (2): 244-251. https://doi.org/10.24953/turkjped.2020.02.010
29. Fadda G, Brown RA, Longoni G, Castro DA, O’Mahony J 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. The Lancet Child & Adolescent Health 2018; 2 (3): 191-204. https:// doi.org/10.1016/s2352-4642(18)30026-9
30. Derle E, Kurne AT, Konuşkan B, Karabudak R, Anlar B. Unfavorable outcome of pediatric onset multiple sclerosis: Follow-up in the pediatric and adult neurology departments of one referral center, in Turkey. Multiple Sclerosis and Related Disorders 2016; 9: 1-4. https://doi.org/10.1016/j. msard.2016.06.002
31. Ghezzi A, Pozzilli C, Liguori M, Marrosu MG, Milani N et al. Prospective study of multiple sclerosis with early onset. Multiple Sclerosis Journal 2002; 8 (2): 115-118. https://doi. org/10.1191/1352458502ms786oa
32. Ghezzi A, Deplano V, Faroni J, Grasso MG, Liguori M et al. Multiple sclerosis in childhood: clinical features of 149 cases. Multiple Sclerosis Journal 1997; 3 (1): 43-46. https://doi. org/10.1177/135245859700300105
33. AlTokhis AI, AlAmrani A, Alotaibi A, Podlasek A, Constantinescu CS. Magnetic Resonance Imaging as a Prognostic Disability Marker in Clinically Isolated Syndrome and Multiple Sclerosis: A Systematic Review and Meta- Analysis. Diagnostics 2022; 12 (2): 270. https://doi.org/10.3390/ diagnostics12020270
34. Yik JT, Becquart P, Gill J, Petkau J, Traboulsee A et al. Serum neurofilament light chain correlates with myelin and axonal magnetic resonance imaging markers in multiple sclerosis. Multiple Sclerosis and Related Disorders 2022; 57: 103366. https://doi.org/10.1016/j.msard.2021.103366
35. Kolčava J, Kočica J, Hulová M, Dušek L, Horáková M et al. Conversion of clinically isolated syndrome to multiple sclerosis: a prospective study. Multiple Sclerosis and Related Disorders 2020; 44: 102262. https://doi.org/10.1016/j. msard.2020.102262
36. Al-Namaeh M. Systematic review and meta-analysis of the development of multiple sclerosis in clinically isolated syndrome. European Journal of Ophthalmology 2021; 31 (4): 1643-1655. https://doi.org/10.1177/1120672120983179
37. Kuhle J, Disanto G, Dobson R, Adiutori R, Bianchi L et al. Conversion from clinically isolated syndrome to multiple sclerosis: A large multicentre study. Multiple Sclerosis Journal 2015; 21 (8): 1013-1024. https://doi. org/10.1177/1352458514568827
38. Dalla Costa G, Martinelli V, Sangalli F, Moiola L, Colombo B et al. Prognostic value of serum neurofilaments in patients with clinically isolated syndromes. Neurology 2019; 92 (7): 733-741. https://doi.org/10.1212/wnl.0000000000006902
39. van der Vuurst de Vries RM, Wong YYM, Mescheriakova JY, van Pelt ED, Runia TF et al. High neurofilament levels are associated with clinically definite multiple sclerosis in children and adults with clinically isolated syndrome. Multiple Sclerosis Journal 2019; 25 (7): 958-967. https://doi. org/10.1177/1352458518775303
40. Disanto G, Adiutori R, Dobson R, Martinelli V, Dalla Costa G et al. Serum neurofilament light chain levels are increased in patients with a clinically isolated syndrome. Journal of Neurology, Neurosurgery & Psychiatry 2016; 87 (2): 126-129. https://doi.org/10.1136/jnnp-2014-309690
41. Hou Y, Jia Y, Hou J. Natural Course of Clinically Isolated Syndrome: A Longitudinal Analysis Using a Markov Model. Scientific Reports 2018; 8 (1): 1-7. https://doi.org/10.1038/ s41598-018-29206-y
42. Krysko KM, Graves JS, Rensel M, Weinstock-Guttman B, Rutatangwa A et al. Real-World Effectiveness of Initial Disease- Modifying Therapies in Pediatric Multiple Sclerosis. Annals of Neurology 2020; 88 (1): 42-55. https://doi.org/10.1002/ ana.25737
43. Tintore M, Rovira À, Río J, Otero-Romero S, Arrambide G et al. Defining high, medium and low impact prognostic factors for developing multiple sclerosis. Brain 2015; 138 (7): 1863- 1874. https://doi.org/10.1093/brain/awv105
44. Kappos L, Freedman MS, Polman CH, Edan G, Hartung HP et al. Effect of early versus delayed interferon beta-1b treatment on disability after a first clinical event suggestive of multiple sclerosis: a 3-year follow-up analysis of the BENEFIT study. The Lancet 2007; 370 (9585): 389-397. https://doi.org/10.1016/ s0140-6736(07)61194-5
45. Peche SS, Alshekhlee A, Kelly J, Lenox J, Mar S. A long-term follow-up study using IPMSSG criteria in children with CNS demyelination. Pediatric Neurology 2013; 49 (5): 329-334. https://doi.org/10.1016/j.pediatrneurol.2013.06.023
46. Krupp LB, Banwell B, Tenembaum S. Consensus definitions proposed for pediatric multiple sclerosis and related disorders. Neurology 2007; 68 (16): 7-12. https://doi.org/10.1212/01. wnl.0000259422.44235.a8
47. Dale RC, Pillai SC. Early relapse risk after a first CNS inflammatory demyelination episode: examining international consensus definitions. Developmental Medicine & Child Neurology 2007; 49 (12): 887-893. https://doi.org/10.1111/ j.1469-8749.2007.00887.x
48. Neuteboom RF, Boon M, Catsman Berrevoets CE, Vles JS, Gooskens RH et al. Prognostic factors after a first attack of inflammatory CNS demyelination in children. Neurology 2008; 71 (13): 967-973. https://doi.org/10.1212/01. wnl.0000316193.89691.e1
49. Alper G, Heyman R, Wang L. Multiple sclerosis and acute disseminated encephalomyelitis diagnosed in children after long-term follow-up: comparison of presenting features. Developmental Medicine & Child Neurology 2009; 51 (6): 480- 486. https://doi.org/10.1111/j.1469-8749.2008.03136.x
50. Tantsis EM, Prelog K, Brilot F, Dale RC. Risk of multiple sclerosis after a first demyelinating syndrome in an Australian Paediatric cohort: clinical, radiological features and application of the McDonald 2010 MRI criteria. Multiple Sclerosis Journal 2013; 19 (13): 1749-1759. https://doi. org/10.1177/1352458513484377
51. Chitnis T, Arnold DL, Banwell B, Brück W, Ghezzi A et al. Trial of Fingolimod versus Interferon Beta-1a in Pediatric Multiple Sclerosis. New England Journal of Medicine 2018; 379 (11): 1017-1027. https://doi.org/10.1056/NEJMoa1800149
52. Chitnis T, Banwell B, Kappos L, Arnold DL, Gücüyener K et al. Safety and efficacy of teriflunomide in paediatric multiple sclerosis (TERIKIDS): a multicentre, double-blind, phase 3, randomised, placebo-controlled trial. The Lancet Neurology 2021; 20 (12): 1001-1011. https://doi.org/10.1016/s1474- 4422(21)00364-1
53. Allen CM, Mowry E, Tintore M, Evangelou N. Prognostication and contemporary management of clinically isolated syndrome. Journal of Neurology, Neurosurgery & Psychiatry 2021; 92 (4): 391-397. https://doi.org/10.1136/jnnp-2020-323087
54. Wallach AI, Waltz M, Casper TC, Aaen G, Belman A et al. Cognitive processing speed in pediatric-onset multiple sclerosis: Baseline characteristics of impairment and prediction of decline. Multiple Sclerosis Journal 2020; 26 (14): 1938-1947. https://doi.org/10.1177/1352458519891984
55. McKay KA, Manouchehrinia A, Berrigan L, Fisk JD, Olsson T et al. Long-term Cognitive Outcomes in Patients With Pediatric-Onset vs Adult-Onset Multiple Sclerosis. JAMA Neurology 2019; 76 (9): 1028-1034. https://doi.org/10.1001/ jamaneurol.2019.1546
56. Iaffaldano P, Simone M, Lucisano G, Ghezzi A, Coniglio G et al. Prognostic indicators in pediatric clinically isolated syndrome. Annals of Neurology 2017; 81 (5): 729-739. https:// doi.org/10.1002/ana.24938
57. Miller AE, Wolinsky JS, Kappos L, Comi G, Freedman MS et al. Oral teriflunomide for patients with a first clinical episode suggestive of multiple sclerosis (TOPIC): a randomised, double-blind, placebo-controlled, phase 3 trial. The Lancet Neurology 2014; 13 (10): 977-986. https://doi.org/10.1016/ s1474-4422(14)70191-7
58. Kinkel RP, Dontchev M, Kollman C, Skaramagas TT, O’Connor PW et al. Association between immediate initiation of intramuscular interferon beta-1a at the time of a clinically isolated syndrome and long-term outcomes: a 10-year follow- up of the Controlled High-Risk Avonex Multiple Sclerosis Prevention Study in Ongoing Neurological Surveillance. Archives of Neurology 2012; 69 (2): 183-190. https://doi. org/10.1001/archneurol.2011.1426
59. Heussinger N, Kontopantelis E, Gburek-Augustat J, Jenke A, Vollrath G et al. Oligoclonal bands predict multiple sclerosis in children with optic neuritis. Annals of Neurology 2015; 77 (6): 1076-1082. https://doi.org/10.1002/ana.24409
60. Waubant E, Banwell B, Wassmer E, Sormani MP, Amato MP et al. Clinical trials of disease-modifying agents in pediatric MS: Opportunities, challenges, and recommendations from the IPMSSG. Neurology 2019; 92 (22): 2538-2549. https://doi. org/10.1212/wnl.0000000000007572

APA	Oncel I, Solmaz I (2022). Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature. , 1281 - 1287. 10.55730/1300-0144.5434
Chicago	Oncel Ibrahim,Solmaz Ismail Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature. (2022): 1281 - 1287. 10.55730/1300-0144.5434
MLA	Oncel Ibrahim,Solmaz Ismail Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature. , 2022, ss.1281 - 1287. 10.55730/1300-0144.5434
AMA	Oncel I,Solmaz I Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature. . 2022; 1281 - 1287. 10.55730/1300-0144.5434
Vancouver	Oncel I,Solmaz I Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature. . 2022; 1281 - 1287. 10.55730/1300-0144.5434
IEEE	Oncel I,Solmaz I "Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature." , ss.1281 - 1287, 2022. 10.55730/1300-0144.5434
ISNAD	Oncel, Ibrahim - Solmaz, Ismail. "Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature". (2022), 1281-1287. https://doi.org/10.55730/1300-0144.5434

APA	Oncel I, Solmaz I (2022). Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature. Turkish Journal of Medical Sciences, 52(4), 1281 - 1287. 10.55730/1300-0144.5434
Chicago	Oncel Ibrahim,Solmaz Ismail Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature. Turkish Journal of Medical Sciences 52, no.4 (2022): 1281 - 1287. 10.55730/1300-0144.5434
MLA	Oncel Ibrahim,Solmaz Ismail Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature. Turkish Journal of Medical Sciences, vol.52, no.4, 2022, ss.1281 - 1287. 10.55730/1300-0144.5434
AMA	Oncel I,Solmaz I Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature. Turkish Journal of Medical Sciences. 2022; 52(4): 1281 - 1287. 10.55730/1300-0144.5434
Vancouver	Oncel I,Solmaz I Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature. Turkish Journal of Medical Sciences. 2022; 52(4): 1281 - 1287. 10.55730/1300-0144.5434
IEEE	Oncel I,Solmaz I "Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature." Turkish Journal of Medical Sciences, 52, ss.1281 - 1287, 2022. 10.55730/1300-0144.5434
ISNAD	Oncel, Ibrahim - Solmaz, Ismail. "Evolution of clinically isolated syndrome to pediatric-onset multiple sclerosis and a review of the literature". Turkish Journal of Medical Sciences 52/4 (2022), 1281-1287. https://doi.org/10.55730/1300-0144.5434