Perinatal and childhood stroke: definitions, epidemiology, classifications, risk factors, etiologies, diagnostic approach, and clinical and neurodevelopmental outcomes
Main Article Content
Abstract
Introduction: Strokes in children are more frequent in neonates, and are associated with clinical and neurodevelopmental consequences, resulting in impact for the whole family. Objective: To present an updated synthesis of knowledge about strokes in pediatrics, expand the information of studies published in the last five years and encourage more research in this area of knowledge in Brazil. Data sources: Pubmed, LILACS and MEDLINE databases. Data
synthesis: Strokes are classified as perinatal and childhood types. The perinatal strokes occur between 20 weeks of fetal life and 28 days of postnatal life, are divided into symptomatic acute perinatal stroke with presentation in the first 28 days of postnatal life, which is subdivided into neonatal arterial ischemic stroke, neonatal cerebral sinovenous thrombosis and neonatal hemorrhagic stroke; and
presumed perinatal strokes with presentation after the first 28 days of postnatal life, which is subdivided into arterial presumed perinatal ischemic stroke, periventricular venous infarction and presumed perinatal hemorrhagic stroke. Childhood strokes occur and present after 28 days of postnatal life up to 18 years, being subclassified in arterial ischemic stroke, cerebral sinovenous thrombosis and hemorrhagic stroke. Conclusions: In the last 5 years studies have brought new information. A new classification for the perinatal strokes and changes in diagnostic investigation. Expansion in the myriad of etiologies for ischemic childhood strokes and in their diagnostic investigations, with a new international classification for the arterial ischemic stroke. New specific scales are available for
measuring outcomes and quality of life.
Downloads
Article Details
This work is licensed under a Creative Commons Attribution 4.0 International License.
References
1. Ferriero DM, Fullerton HJ, Bernard TJ, Billinghurst L, Daniels SR, DeBaun MR, deVeber G, Ichord RN, Jordan LC, Massicotte P, Meldau J, Roach ES, Smith ER. American Heart Association Stroke Council and Council on Cardiovascular and Stroke Nursing. Management of Stroke in Neonates and Children. A Scientific Statement From the American Heart Association/American Stroke Association. Stroke 2019 Mar;50(3):e51-e96. doi: 10.1161/STR.0000000000000183.
2. McKinney SM, Magruder JT, Abramo TJ. An Update on Pediatric Stroke Protocol. Pediatr Emerg Care. 2018 Nov;34(11):810-815. doi: 10.1097/PEC.0000000000001653.
3. Bernson-Leung ME, Rivkin MJ. Stroke in Neonates and Children. Pediatr Rev. 2016 Nov;37(11):463-477. doi: 10.1542/pir.2016-0002. PMID: 27803143.
4. O'Keeffe F, Stark D, Murphy O, Ganesan V, King J, Murphy T. Psychosocial outcome and quality of life following childhood stroke: A systematic review. Dev Neurorehabil. 2017 Oct;20(7):428-442. doi: 10.1080/17518423.2017.1282052. Epub 2017 Feb 16. PMID: 28632465.
5. Jacomb I, Porter M, Brunsdon R, Mandalis A, Parry L. Cognitive outcomes of pediatric stroke. Child Neuropsychol. 2018 Apr;24(3):287-303. doi: 10.1080/09297049.2016.1265102. Epub 2016 Dec 14. PMID: 27960625.
6. Fuentes A, Westmacott R, Deotto A, deVeber G, Desrocher M. Working memory outcomes following unilateral arterial ischemic stroke in childhood. Child Neuropsychol. 2017 Oct;23(7):803-821. doi: 10.1080/09297049.2016.1205008. Epub 2016 Jul 18. PMID: 27424626.
7. Williams TS, Roberts SD, Coppens AM, Crosbie J, Dlamini N, Westmacott R. Secondary attention-deficit/hyperactivity disorder following perinatal and childhood stroke: impact on cognitive and academic outcomes. Child Neuropsychol. 2018 Aug;24(6):763-783. doi: 10.1080/09297049.2017.1333091. Epub 2017 May 30. PMID: 28554265.
8. Rivkin MJ. Epilepsy as the 'echo' of acute stroke in children. Dev Med Child Neurol. 2017 Jan;59(1):6. doi: 10.1111/dmcn.13231. Epub 2016 Aug 13. PMID: 27519161.
9. Dunbar M, Kirton A. Perinatal stroke. Semin Pediatr Neurol. 2019 Dec;32:100767. doi: 10.1016/j.spen.2019.08.003.
10. Gacio S, Muñoz Giacomelli F, Klein F. Presumed perinatal ischemic stroke: A review. Arch Argent Pediatr. 2015 Oct;113(5):449-55. English, Spanish. doi: 10.5546/aap.2015.449. PMID: 26294151.
11. Ilves P, Laugesaar R, Loorits D, Kolk A, Tomberg T, Lõo S, Talvik I, Kahre T, Talvik T. Presumed Perinatal Stroke: Risk Factors, Clinical and Radiological Findings. J Child Neurol. 2016 Apr;31(5):621-8. Doi: 10.1177/0883073815609149.
12. Dunbar M, Kirton A. Perinatal stroke. Semin Pediatr Neurol. 2019 Dec;32:100767. doi: 10.1016/j.spen.2019.08.003.
13. Fluss J, Dinomais M, Chabrier S. Perinatal stroke syndromes: Similarities and diversities in aetiology, outcome and management. Eur J Paediatr Neurol. 2019 May;23(3):368-383. doi: 10.1016/j.ejpn.2019.02.013.
14. Lehman LL, Beaute J, Kapur K, Danehy AR, Bernson-Leung ME, Malkin H, Rivkin MJ, Trenor CC 3rd. Workup for Perinatal Stroke Does Not Predict Recurrence. Stroke. 2017 Aug;48(8):2078-2083. doi: 10.1161/STROKEAHA.117.017356. Epub 2017 Jul 13. PMID: 28706112.
15. Lehman LL, Khoury JC, Taylor JM, Yeramaneni S, Sucharew H, Alwell K, Moomaw CJ, Peariso K, Flaherty M, Khatri P, Broderick JP, Kissela BM, Kleindorfer DO. Pediatric stroke rates over 17 years: report from a population-based study. J Child Neurol. 2018;33:463-467. doi: 10.1177/0883073818767039.
16. Lee S, Mirsky DM, Beslow LA, Amlie-Lefond C, Danehy AR, Lehman L, Stence NV, Vossough A, Wintermark M, Rivkin MJ; International Paediatric Stroke Study Neuroimaging Consortium and the Paediatric Stroke Neuroimaging Consortium. Pathways for Neuroimaging of Neonatal Stroke. Pediatr Neurol. 2017 Apr;69:37-48. doi: 10.1016/j.pediatrneurol.2016.12.008. Epub 2017 Jan 26. PMID: 28262550.
17. deVeber GA, Kirton A, Booth FA, Yager JY, Wirrell EC, Wood E, Shevell M, Surmava AM, McCusker P, Massicotte MP, MacGregor D, MacDonald EA, Meaney B, Levin S, Lemieux BG, Jardine L, Humphreys P, David M, Chan AK, Buckley DJ, Bjornson BH. Epidemiology and outcomes of arterial ischemic stroke in children: the Canadian Pediatric Ischemic Stroke Registry. Pediatr Neurol. 2017;69:58-70. doi: 10.1016/j.pediatrneurol.2017.01.016.
18. Olivé G, Agut T, Echeverría-Palacio CM, Arca G, García-Alix A. Usefulness of Cranial Ultrasound for Detecting Neonatal Middle Cerebral Artery Stroke. Ultrasound Med Biol. 2019 Mar;45(3):885-890. doi: 10.1016/j.ultrasmedbio.2018.11.004. Epub 2019 Jan 11. PMID: 30642660.
19. Fluss J, Garcia-Tarodo S, Granier M, Villega F, Ferey S, Husson B, Kossorotoff M, Muehlethaler V, Lebon S, Chabrier S. Perinatal arterial ischemic stroke related to carotid artery occlusion. Eur J Paediatr Neurol. 2016 Jul;20(4):639-48. doi: 10.1016/j.ejpn.2016.03.003. Epub 2016 Mar 16. PMID: 27025300.
20. Guiraut C, Cauchon N, Lepage M, Sébire G. Perinatal Arterial Ischemic Stroke Is Associated to Materno-Fetal Immune Activation and Intracranial Arteritis. Int J Mol Sci. 2016 Nov 25;17(12):1980. doi: 10.3390/ijms17121980. PMID: 27898024; PMCID: PMC5187780.
21. Giraud A, Guiraut C, Chevin M, Chabrier S, Sébire G. Role of Perinatal Inflammation in Neonatal Arterial Ischemic Stroke. Front Neurol. 2017 Nov 16;8:612. doi: 10.3389/fneur.2017.00612. PMID: 29201015; PMCID: PMC5696351.
22. Curtis C, Mineyko A, Massicotte P, Leaker M, Jiang XY, Floer A, Kirton A. Thrombophilia risk is not increased in children after perinatal stroke. Blood. 2017 May 18;129(20):2793-2800. doi: 10.1182/blood-2016-11-750893. Epub 2017 Mar 3. Erratum in: Blood. 2017 Jul 20;130(3):382. PMID: 28258054.
23. Martinez-Biarge M, Cheong JL, Diez-Sebastian J, Mercuri E, Dubowitz LM, Cowan FM. Risk Factors for Neonatal Arterial Ischemic Stroke: The Importance of the Intrapartum Period. J Pediatr. 2016 Jun;173:62-68.e1. doi: 10.1016/j.jpeds.2016.02.064. Epub 2016 Apr 3. PMID: 27049002.
24. Li C, Miao JK, Xu Y, Hua YY, Ma Q, Zhou LL, Liu HJ, Chen QX. Prenatal, perinatal and neonatal risk factors for perinatal arterial ischaemic stroke: a systematic review and meta-analysis. Eur J Neurol. 2017 Aug;24(8):1006-1015. doi: 10.1111/ene.13337. Epub 2017 Jun 24. PMID: 28646492.
25. Adami RR, Grundy ME, Poretti A, Felling RJ, Lemmon M, Graham EM. Distinguishing Arterial Ischemic Stroke From Hypoxic-Ischemic Encephalopathy in the Neonate at Birth. Obstet Gynecol. 2016 Oct;128(4):704-12. doi: 10.1097/AOG.0000000000001631. PMID: 27607878; PMCID: PMC5895085.
26. Siddiq I, Armstrong D, Surmava AM, Dlamini N, MacGregor D, Moharir M, Askalan R. Utility of Neurovascular Imaging in Acute Neonatal Arterial Ischemic Stroke. J Pediatr. 2017 Sep;188:110-114. doi: 10.1016/j.jpeds.2017.05.046. Epub 2017 Jun 15. PMID: 28624098.
27. Chalia M, Dempsey LA, Cooper RJ, Lee CW, Gibson AP, Hebden JC, Austin T. Diffuse optical tomography for the detection of perinatal stroke at the cot side: a pilot study. Pediatr Res. 2019 Jun;85(7):1001-1007. doi: 10.1038/s41390-018-0263-x. Epub 2019 Feb 13. PMID: 30759451; PMCID: PMC6760550.
28. Goeggel Simonetti B, Rafay MF, Chung M, Lo WD, Beslow LA, Billinghurst LL, Fox CK, Pagnamenta A, Steinlin M, Mackay MT; IPSS Study Group. Comparative study of posterior and anterior circulation stroke in childhood: Results from the International Pediatric Stroke Study. Neurology. 2020 Jan 28;94(4):e337-e344. doi: 10.1212/WNL.0000000000008837. Epub 2019 Dec 19. PMID: 31857436.
29. Ecury-Goossen GM, van der Haer M, Smit LS, Feijen-Roon M, Lequin M, de Jonge RC, Govaert P, Dudink J. Neurodevelopmental outcome after neonatal perforator stroke. Dev Med Child Neurol. 2016 Jan;58(1):49-56. doi: 10.1111/dmcn.12857. Epub 2015 Jul 26. PMID: 26212612.
30. Benninger KL, Ruess L, Slaughter LA, Maitre NL, Rusin JA. Neonatal Vein of Labbé Infarction Size is Associated With Long-Term Language Outcomes. Pediatr Neurol. 2017 Jul;72:70-75.e1. doi: 10.1016/j.pediatrneurol.2017.03.015. Epub 2017 Apr 1. PMID: 28495146; PMCID: PMC5480620.
31. Merlini L, Hanquinet S, Fluss J. Thalamic Hemorrhagic Stroke in the Term Newborn: A Specific Neonatal Syndrome With Non-uniform Outcome. J Child Neurol. 2017 Jul;32(8):746-753. doi: 10.1177/0883073817703503. Epub 2017 Apr 21. PMID: 28429607.
32. Cole L, Dewey D, Letourneau N, Kaplan BJ, Chaput K, Gallagher C, Hodge J, Floer A, Kirton A. Clinical Characteristics, Risk Factors, and Outcomes Associated With Neonatal Hemorrhagic Stroke: A Population-Based Case-Control Study. JAMA Pediatr. 2017 Mar 1;171(3):230-238. doi: 10.1001/jamapediatrics.2016.4151. Erratum in: JAMA Pediatr. 2017 Jun 1;171(6):602. PMID: 28114647.
33. Gerstl L, Badura K, Heinen F, Weinberger R, Peraud A, Dorn F, Bonfert MV, Berweck S, O'Callaghan FJ. Childhood haemorrhagic stroke: a 7-year single-centre experience. Arch Dis Child. 2019 Dec;104(12):1198-1202. doi: 10.1136/archdischild-2018-316749. Epub 2019 Jun 20. PMID: 31221624.
34. Bernard TJ, Beslow LA, Manco-Johnson MJ, Armstrong-Wells J, Boada R, Weitzenkamp D, Hollatz A, Poisson S, Amlie-Lefond C, Lo W, deVeber G, Goldenberg NA, Dowling MM, Roach ES, Fullerton HJ, Benseler SM, Jordan LC, Kirton A, Ichord RN. Inter-rater reliability of the CASCADE criteria: challenges in classifying arteriopathies. Stroke. 2016;47:2443-2449. doi: 10.1161/STROKEAHA.116.013544.
35. Böhmer M, Niederstadt T, Heindel W, Wildgruber M, Sträter R, Hanning U, Kemmling A, Sporns PB. Impact of Childhood Arterial Ischemic Stroke Standardized Classification and Diagnostic Evaluation Classification on Further Course of Arteriopathy and Recurrence of Childhood Stroke. Stroke. 2018 Dec 7:STROKEAHA118023060. doi: 10.1161/STROKEAHA.118.023060. Epub ahead of print. PMID: 30580701.
36. Aborkhees G, Mitchell LG. Predicting risk for recurrence of arterial ischemic stroke in children: thrombophilia as another piece of the puzzle. Haematologica. 2019 Aug;104(8):1513-1514. doi: 10.3324/haematol.2019.222695. PMID: 31366465; PMCID: PMC6669139.
37. Uohara MY, Beslow LA, Billinghurst L, Jones BM, Kessler SK, Licht DJ, Ichord RN. Incidence of recurrence in posterior circulation childhood arterial ischemic stroke. JAMA Neurol. 2017;74:316-323. doi: 10.1001/jamaneurol.2016.5166.
38. Fullerton HJ, deVeber GA, Hills NK, Dowling MM, Fox CK, Mackay MT, Kirton A, Yager JY, Bernard TJ, Hod EA, Wintermark M, Elkind MS; VIPS Investigators. Inflammatory biomarkers in childhood arterial ischemic stroke: correlates of stroke cause and recurrence. Stroke. 2016;47:2221-2228. doi: 10.1161/STROKEAHA.116.013719.
39. Rodrigues DO, Ribeiro LC, Sudário LC, Teixeira MT, Martins ML, Pittella AM, Junior IO. Genetic determinants and stroke in children with sickle cell disease. J Pediatr (Rio J). 2016 Nov-Dec;92(6):602-608. doi: 10.1016/j.jped.2016.01.010. Epub 2016 Jun 5. PMID: 27268459.
40. Felling RJ, Sun LR, Maxwell EC, Goldenberg N, Bernard T. Pediatric arterial ischemic stroke: epidemiology, risk factors, and management. Blood Cells Mol Dis. 2017;67:23-33. doi: 10.1016/j.bcmd. 2017.03.003.
41. Chabrier S, Sébire G, Fluss J. Transient Cerebral Arteriopathy, Postvaricella Arteriopathy, and Focal Cerebral Arteriopathy or the Unique Susceptibility of the M1 Segment in Children With Stroke. Stroke. 2016 Oct;47(10):2439-41. doi: 10.1161/STROKEAHA.116.014606. Epub 2016 Sep 15. PMID: 27633022.
42. Steinlin M. Neuroinflammation in Ischemic Pediatric Stroke. Semin Pediatr Neurol. 2017 Aug;24(3):201-206. doi: 10.1016/j.spen.2017.08.006. Epub 2017 Sep 20. PMID: 29103427.
43. Garzon MC, Epstein LG, Heyer GL, Frommelt PC, Orbach DB, Baylis AL, Blei F, Burrows PE, Chamlin SL, Chun RH, Hess CP, Joachim S, Johnson K, Kim W, Liang MG, Maheshwari M, McCoy GN, Metry DW, Monrad PA, Pope E, Powell J, Shwayder TA, Siegel DH, Tollefson MM, Vadivelu S, Lew SM, Frieden IJ, Drolet BA. PHACE syndrome: consensus-derived diagnosis and care recommendations. J Pediatr. 2016;178:24-33.e2. doi: 10.1016/j.jpeds.2016.07.054.
44. Ko A, Lee SJ, Lee YM. Focal cerebellar infarction as an initial sign of mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes. J Inherit Metab Dis. 2019 May;42(3):575-576. doi: 10.1002/jimd.12020. Epub 2019 Jan 28. PMID: 30693531.
45. Paramasivam A, Venkatapathi C, Sandeep G, Meena AK, Uppin MS, Mohapatra S, Pitceathly RDS, Thangaraj K. Homozygous R627W mutations in POLG cause mitochondrial DNA depletion leading to encephalopathy, seizures and stroke-like episodes. Mitochondrion. 2019 Sep;48:78-83. doi: 10.1016/j.mito.2019.08.003. Epub 2019 Aug 16. PMID: 31425757.
46. McCrea N, Saunders D, Bagkeris E, Chitre M, Ganesan V. Diagnosis of vertebral artery dissection in childhood posterior circulation arterial ischaemic stroke. Dev Med Child Neurol. 2016 Jan;58(1):63-9. doi: 10.1111/dmcn.12945. Epub 2015 Oct 26. PMID: 26502795.
47. Carey S, Wrogemann J, Booth FA, Rafay MF. Epidemiology, Clinical Presentation, and Prognosis of Posterior Circulation Ischemic Stroke in Children. Pediatr Neurol. 2017 Sep;74:41-50. doi: 10.1016/j.pediatrneurol.2017.05.007. Epub 2017 May 19. PMID: 28676245.
48. Ritchey Z, Hollatz AL, Weitzenkamp D, Fenton LZ, Maxwell EC, Bernard TJ, Stence NV. Pediatric cortical vein thrombosis: frequency and association with venous infarction. Stroke. 2016;47:866-868. doi: 10.1161/STROKEAHA.115.011291.
49. Ichord RN, Benedict SL, Chan AK, Kirkham FJ, Nowak-Göttl U; International Paediatric Stroke Study Group. Paediatric cerebral sinovenous thrombosis: findings of the International Paediatric Stroke Study. Arch Dis Child. 2015;100:174-179. doi: 10.1136/archdischild-2014-306382.
50. Suppiej A, Gentilomo C, Saracco P, Sartori S, Agostini M, Bagna R, Bassi B, Giordano P, Grassi M, Guzzetta A, Lasagni D, Luciani M, Molinari AC, Palmieri A, Putti MC, Ramenghi LA, Rota LL, Sperlì D, Laverda AM, Simioni P; Stroke Working Group of the Italian Registry of Pediatric Thrombosis. Paediatric arterial ischaemic stroke and cerebral sinovenous thrombosis: first report from the Italian Registry of Pediatric Thrombosis (R.I.T.I., Registro Italiano Trombosi Infantili). Thromb Haemost. 2015;113:1270-1277. doi: 10.1160/TH14-05-0431.
51. Zanoletti E, Cazzador D, Faccioli C, Sari M, Bovo R, Martini A. Intracranial venous sinus thrombosis as a complication of otitis media in children: critical review of diagnosis and management. Int J Pediatr Otorhinolaryngol. 2015;79:2398-2403. doi: 10.1016/j.ijporl.2015.10.059.
52. Ghanem KM, Dhayni RM, Al-Aridi C, Tarek N, Tamim H, Chan AKC, Saab R, Abboud MR, El-Solh H, Muwakkit SA. Cerebral sinus venous thrombosis during childhood acute lymphoblastic leukemia therapy: risk factors and management [published online October 18, 2017]. Pediatr Blood Cancer. doi: 10.1002/pbc.26694.
53. Petrov D, Uohara MY, Ichord R, Ali Z, Jastrzab L, Lang SS, Billinghurst L. Pediatric cerebral sinovenous thrombosis following cranial surgery. Childs Nerv Syst. 2017;33:491-497. doi: 10.1007/s00381-016-3329-2.
54. Sarikaya H, Steinlin M. Cerebellar stroke in adults and children. Handb Clin Neurol. 2018;155:301-312. doi: 10.1016/B978-0-444-64189-2.00020-2. PMID: 29891068.
55. Mackay MT, Churilov L, Donnan GA, Babl FE, Monagle P. Performance of bedside stroke recognition tools in discriminating childhood stroke from mimics. Neurology. 2016;86:2154-2161. doi: 10.1212/WNL.0000000000002736.
56. Greenham M, Gordon A, Anderson V, Mackay MT. Outcome in Childhood Stroke. Stroke. 2016 Apr;47(4):1159-64. doi: 10.1161/STROKEAHA.115.011622. Epub 2016 Mar 8. PMID: 26956257.
57. Crawford LB, Golomb MR. Childhood Stroke and Vision: A Review of the Literature. Pediatr Neurol. 2018 Apr;81:6-13. doi: 10.1016/j.pediatrneurol.2017.11.007. Epub 2017 Nov 20. PMID: 29526346.
58. Slim M, Fox CK, Friefeld S, Dlamini N, Westmacott R, Moharir M, MacGregor D, deVeber G; SIPS Investigators. Validation of the pediatric stroke outcome measure for classifying overall neurological deficit. Pediatr Res. 2020 Aug;88(2):234-242. doi: 10.1038/s41390-020-0842-5. Epub 2020 Mar 16. PMID: 32179868.
59. Ghotra SK, Johnson JA, Qiu W, Newton AS, Rasmussen C, Yager JY. Health-related quality of life and its determinants in paediatric arterial ischaemic stroke survivors. Arch Dis Child. 2018 Oct;103(10):930-936. doi: 10.1136/archdischild-2017-313334. Epub 2018 Mar 8. PMID: 29519944.
60. Fiume A, Deveber G, Jang SH, Fuller C, Viner S, Friefeld S. Development and validation of the Pediatric Stroke Quality of Life Measure. Dev Med Child Neurol. 2018 Jun;60(6):587-595. doi: 10.1111/dmcn.13684. Epub 2018 Feb 16. PMID: 29451699.