Cerebral blood flow imbalance is associated with motor outcome after pediatric arterial ischemic stroke
Autoři:
Rebekka Leistner aff001; Regula Everts aff001; Andrea Federspiel aff003; Salome Kornfeld aff001; Nedelina Slavova aff004; Leonie Steiner aff001; Roland Wiest aff004; Maja Steinlin aff001; Sebastian Grunt aff001
Působiště autorů:
Division of Neuropediatrics, Development and Rehabilitation, University Children’s Hospital, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
aff001; Department of Diabetes, Endocrinology, Clinical Nutrition and Metabolism, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
aff002; Psychiatric Neuroimaging Unit, Translational Research Center, University Hospital of Psychiatry, University of Bern, Bern, Switzerland
aff003; Department of Diagnostic and Interventional Neuroradiology, Inselspital, Bern University Hospital, University of Bern, Bern, Switzerland
aff004
Vyšlo v časopise:
PLoS ONE 14(10)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0223584
Souhrn
Cerebral hemodynamics after arterial ischemic stroke (AIS) in children are largely unknown. This study aims to explore long-term cerebral perfusion balance of vital tissue and its relation to motor outcome after childhood AIS. Patients diagnosed with childhood AIS (≤16 years at diagnosis, time since stroke ≥2 years) and typically developing peers were examined. Hemiparesis was classified according to the Pediatric Stroke Outcome Measure. Manual ability was assessed using the ABILHAND-Kids questionnaire. Cerebral blood flow was measured by arterial spin labeling and analyzed in the following brain regions: the hemispheres, the territory of the anterior cerebral artery (ACA), the middle cerebral artery (MCA), and in subregions of the MCA territory (MCA anterior, middle, posterior). To assess cerebral perfusion balance, laterality indices were calculated using cerebral blood flow in the ipsi- and contralesional hemisphere. Laterality indices were compared between stroke patients with and without hemiparesis, and peers. Twenty participants diagnosed with AIS were included (12 boys, 8 girls; mean age 14.46±4.96 years; time since stroke 8.08±3.62 years); 9 (45%) were diagnosed with hemiparesis. Additionally, 47 typically developing peers (21 boys, 26 girls; mean age 14.24±5.42 years) were studied. Laterality indices were higher in stroke patients and oriented to the contralesional hemisphere in all brain regions except the ACA territory and MCA posterior subregion. This was significantly different from peers, who showed balanced laterality indices. There was a significant correlation between laterality indices and manual ability, except in the ACA territory. AIS is associated with long-term alterations of cerebral blood flow in vital tissue, even in patients without hemiparesis. The degree of imbalance of cerebral perfusion in children after AIS is associated with manual ability.
Klíčová slova:
stroke – Pediatrics – Ischemic stroke – Magnetic resonance imaging – Cerebral arteries – Blood flow – Cerebral blood flow assay – Balance and falls
Zdroje
1. Fullerton HJ, Wu YW, Zhao S J S. Risk of stroke in children: ethnic and gender disparities. Neurology. 2003;61:189–94. doi: 10.1212/01.wnl.0000078894.79866.95 12874397
2. Giroud M, Lemesle M, Gouyon JB, Nivelon JL, Milan C, Dumas R. Cerebrovascular disease in children under 16 years of age in the city of Dijon, France: A study of incidence and clinical features from 1985 to 1993. J Clin Epidemiol. 1995;48(11):1343–8. doi: 10.1016/0895-4356(95)00039-9 7490597
3. Steinlin M, Pfister I, Pavlovic J, Everts R, Boltshauser E, Mori AC, et al. The first three years of the Swiss Neuropaediatric Stroke Registry (SNPSR): A population-based study of incidence, symptoms and risk factors. Neuropediatrics. 2005;36(2):90–7. doi: 10.1055/s-2005-837658 15822021
4. Nelson KB, Lynch JK. Stroke in newborn infants. Lancet Neurol. 2004;3(3):150–8. doi: 10.1016/S1474-4422(04)00679-9 14980530
5. Lynch JK. Epidemiology and classification of perinatal stroke. Semin Fetal Neonatal Med [Internet]. 2009;14(5):245–9. Available from: http://dx.doi.org/10.1016/j.siny.2009.07.001 19664976
6. Grunt S, Mazenauer L, Buerki SE, Boltshauser E, Mori AC, Datta AN, et al. Incidence and Outcomes of Symptomatic Neonatal Arterial Ischemic Stroke. Pediatrics [Internet]. 2015;135(5):e1220–8. Available from: http://pediatrics.aappublications.org/cgi/doi/10.1542/peds.2014-1520 25896840
7. Greenham M, Gordon A, Anderson V, MacKay MT. Outcome in childhood stroke. Stroke. 2016;47(4):1159–64. doi: 10.1161/STROKEAHA.115.011622 26956257
8. Kornfeld S, Studer M, Winkelbeiner S, Regényi M, Boltshauser E, Steinlin M. Quality of life after paediatric ischaemic stroke. Dev Med Child Neurol. 2016;59(1):45–51. doi: 10.1111/dmcn.13295 27767202
9. Cooper AN, Anderson V, Hearps S, Greenham M, Ditchfield M, Coleman L, et al. Trajectories of Motor Recovery in the First Year After Pediatric Arterial Ischemic Stroke. Pediatrics [Internet]. 2017;140(2):e20163870. Available from: http://pediatrics.aappublications.org/lookup/doi/10.1542/peds.2016-3870 28710246
10. Kornfeld S, Yuan R, Biswal BB, Grunt S, Kamal S, Delgado Rodríguez JA, et al. Resting-state connectivity and executive functions after pediatric arterial ischemic stroke. NeuroImage Clin [Internet]. 2018;17(July 2017):359–67. Available from: http://dx.doi.org/10.1016/j.nicl.2017.10.016
11. Chen J, Licht DJ, Smith SE, Agner SC. Arterial spin labeling perfusion MRI in pediatric arterial ischemic stroke: initial experiences. J Magn [Internet]. 2009;29(2):282–290. Available from: http://onlinelibrary.wiley.com/doi/10.1002/jmri.21641/full
12. Wiest R, Abela E, Missimer J, Schroth G, Hess CW, Sturzenegger M, et al. Interhemispheric cerebral blood flow balance during recovery of motor hand function after ischemic stroke-A longitudinal MRI study using arterial spin labeling perfusion. PLoS One. 2014;9(9).
13. Brumm KP, Perthen JE, Liu TT, Haist F, Ayalon L, Love T. An Arterial Spin Labeling Investigation of Cerebral Blood Flow Deficits in Chronic Stroke Survivors. Neuroimage 2010 July 1; 51(3) 995–1005 2011;51(3):995–1005. doi: 10.1016/j.neuroimage.2010.03.008 20211268
14. Love T, Swinney D, Wong E, Buxton R. Perfusion imaging and stroke: A more sensitive measure of the brain bases of cognitive deficits. Aphasiology. 2002;16(9):873–83. doi: 10.1080/02687030244000356 30906100
15. Richardson JD, Baker JM, Morgan PS, Rorden C, Bonilha L, Fridriksson J. Cerebral perfusion in chronic stroke: Implications for lesion-symptom mapping and functional MRI. Behav Neurol. 2011;24(2):117–22. doi: 10.3233/BEN-2011-0283 21606572
16. Kornfeld S, Rodríguez JAD, Everts R, Kaelin-Lang A, Wiest R, Weisstanner C, et al. Cortical reorganisation of cerebral networks after childhood stroke: Impact on outcome. BMC Neurol [Internet]. 2015;15(1):1–7. Available from: http://dx.doi.org/10.1186/s12883-015-0309-1
17. Bernard TJ, Manco-Johnson MJ, Lo W, MacKay MT, Ganesan V, Deveber G, et al. Towards a consensus-based classification of childhood arterial ischemic stroke. Stroke. 2012;43(2):371–7. doi: 10.1161/STROKEAHA.111.624585 22156694
18. Kitchen L, Westmacott R, Friefeld S, MacGregor D, Curtis R, Allen A, et al. The pediatric stroke outcome measure: A validation and reliability study. Stroke. 2012;43(6):1602–8. doi: 10.1161/STROKEAHA.111.639583 22474056
19. Salmaso D, Longoni AM. Problems in the Assessment of Hand Preference. Cortex [Internet]. 1985;21(4):533–49. Available from: www.sciencedirect.com/science/article/pii/S0010945258800039?via%3Dihub4092483
20. Arnould C, Penta M, Renders A, Thonnard J. A measure of manual ability in children with cerebral palsy. Neurology. 2004;63(5375):1045–52.
21. Wu WC, Fernández-Seara M, Detre JA, Wehrli FW, Wang J. A theoretical and experimental investigation of the tagging efficiency of pseudocontinuous arterial spin labeling. Magn Reson Med. 2007;58(5):1020–7. doi: 10.1002/mrm.21403 17969096
22. Dai W, Garcia D, De Bazelaire C, Alsop DC. Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields. Magn Reson Med. 2008;60(6):1488–97. doi: 10.1002/mrm.21790 19025913
23. Alsop DC, Detre JA, Golay X, Matthias G, Hendrikse J, Hernandez-garcia L, et al. Recommended Implementation of Arterial Spin-Labeled Perfusion MRI for Clinical Applications : A Consensus of the ISMRM Perfusion Study Group and the European Consortium for ASL in Dementia. 2015;116(October 2013):102–16.
24. Neuroimaging W. SPM—Statistical Parametric Mapping [Internet]. Fil.ion.ucl.ac.uk. [cited 24 February 2019]. http://www.fil.ion.ucl.ac.uk/spm/
25. Wang J, Licht DJ, Jahng G-H, Liu C-S, Rubin JT, Haselgrove J, et al. Pediatric perfusion imaging using pulsed arterial spin labeling. J Magn Reson Imaging [Internet]. 2003;18(4):404–13. Available from: http://doi.wiley.com/10.1002/jmri.10372 14508776
26. Buxton RB. Quantifying CBF with arterial spin labeling. J Magn Reson Imaging. 2005;22(6):723–6. doi: 10.1002/jmri.20462 16261574
27. Federspiel A, Müller TJ, Horn H, Kiefer C, Strik WK. Comparison of spatial and temporal pattern for fMRI obtained with BOLD and arterial spin labeling. J Neural Transm. 2006;113(10):1403–15. doi: 10.1007/s00702-006-0434-5 16604307
28. Jann K, Kottlow M, Dierks T, Boesch C, Koenig T. Topographic electrophysiological signatures of fMRI resting state networks. PLoS One. 2010;5(9):1–10.
29. SPSS Statistics for Macintosh, Version 23.0. Armonk, NY: IBM; 2015.
30. Biagi L, Abbruzzese A, Bianchi MC, Alsop DC, Del Guerra A, Tosetti M. Age dependence of cerebral perfusion assessed by magnetic resonance continuous arterial spin labeling. J Magn Reson Imaging. 2007;25(4):696–702. doi: 10.1002/jmri.20839 17279531
31. Satterthwaite TD, Shinohara RT, Wolf DH, Hopson RD, Elliott MA, Vandekar SN, et al. Impact of puberty on the evolution of cerebral perfusion during adolescence. Proc Natl Acad Sci [Internet]. 2014;111(23):8643–8. Available from: http://www.pnas.org/cgi/doi/10.1073/pnas.1400178111 24912164
32. Taki Y, Hashizume H, Sassa Y, Takeuchi H, Wu K, Asano M, et al. Correlation between gray matter density-adjusted brain perfusion and age using brain MR images of 202 healthy children. Hum Brain Mapp. 2011;32(11):1973–85. doi: 10.1002/hbm.21163 21259384
33. Moses P, Dinino M, Hernandez L, Liu TT. Developmental changes in resting and functional cerebral blood flow and their relationship to the BOLD response. Hum Brain Mapp. 2014;35(7):3188–98. doi: 10.1002/hbm.22394 24142547
34. Chugani HT. Biological basis of emotions: brain systems and brain development. Pediatrics. 1998;102(5 Suppl E):1225–9. 9794959
35. Wang J, Licht DJ. Pediatric perfusion MR imaging using arterial spin labeling. Neuroimaging Clin N Am. 2006;16(1):149–67. doi: 10.1016/j.nic.2005.10.002 16543090
36. Taki Y, Hashizume H, Sassa Y, Takeuchi H, Wu K, Asano M, et al. Gender differences in partial-volume corrected brain perfusion using brain MRI in healthy children. Neuroimage [Internet]. 2011;58(3):709–15. Available from: http://dx.doi.org/10.1016/j.neuroimage.2011.07.020 21782958
37. Parkes LM, Rashid W, Chard DT, Tofts PS. Normal Cerebral Perfusion Measurements Using Arterial Spin Labeling: Reproducibility, Stability, and Age and Gender Effects. Magn Reson Med. 2004;51(4):736–43. doi: 10.1002/mrm.20023 15065246
Článok vyšiel v časopise
PLOS One
2019 Číslo 10
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Eliquis (apixaban) nově hrazen ze zdravotního pojištění
Najčítanejšie v tomto čísle
- Correction: Low dose naltrexone: Effects on medication in rheumatoid and seropositive arthritis. A nationwide register-based controlled quasi-experimental before-after study
- Combining CDK4/6 inhibitors ribociclib and palbociclib with cytotoxic agents does not enhance cytotoxicity
- Risk factors associated with IgA vasculitis with nephritis (Henoch–Schönlein purpura nephritis) progressing to unfavorable outcomes: A meta-analysis
- Prevalence of pectus excavatum (PE), pectus carinatum (PC), tracheal hypoplasia, thoracic spine deformities and lateral heart displacement in thoracic radiographs of screw-tailed brachycephalic dogs