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A systematic review of cerebral hemodynamic responses to neural activation following stroke

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Abstract

The aim of this study was to systematically review CBF studies, assess their methodological quality, and identify trends in the association between task-related brain activation patterns and CBF changes in ischemic stroke (IS) patients. We searched the MEDLINE, EMBASE, CINAHL, and Web of Sciences databases for studies of functional recovery with quantification of CBF responses to brain activation paradigms after IS. Titles, abstracts and full text of articles were scrutinised according to pre-defined selection criteria. Two independent reviewers (AS, VH) undertook the methodological quality screening and data extraction of the included studies. Sixteen of the 1,521 identified studies were relevant. Studies showed weaknesses in key methodological criteria (e.g. population size, discussion of limitations), and only seven studies compared responses with a control population. Overall, there was no agreement between CBF responses in either the affected or unaffected hemisphere and prediction of post-IS recovery. Some studies have shown a higher CBF increase in the unaffected hemisphere when the affected hemisphere was stimulated compared to the healthy control responses. However, CBF responses in the affected hemisphere were inconsistent. Many post-IS CBF studies are of poor methodological quality, and do not demonstrate a consistent response post-IS or a relationship with recovery. Further longitudinal studies assessing the natural history of CBF responses to brain paradigms following IS should be undertaken to determine prognostic significance, and to inform future therapeutic strategies.

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References

  1. Aries MJH, Elting JW, De Keyser J, Kremer BPH, Vroomen PCAJ (2010) Cerebral autoregulation in stroke. Stroke 41:2697–2704

    Article  PubMed  Google Scholar 

  2. Attwell D, Iadecola C (2002) The neural basis of functional brain imaging signals. Trends Neurosci 25:621–625

    Article  PubMed  CAS  Google Scholar 

  3. Bor-Seng-Shu E, Kita WS, Figueiredo EG, Paiva WS, Fonoff ET, Teixeira MJ, Panerai RB (2012) Cerebral hemodynamics: concepts of clinical importance. Arq Neuro-Psiquiatr 70:352–356

    Article  Google Scholar 

  4. Bragoni M, Caltagirone C, Troisi E, Matteis M, Vernieri F, Silvestrini M (2000) Correlation of cerebral hemodynamic changes during mental activity and recovery after stroke. Neurology 55:35–40

    Article  PubMed  CAS  Google Scholar 

  5. Brouns R, De Deyn PP (2009) The complexity of neurobiological processes in acute ischemic stroke. Clin Neurol Neurosurg 111:483–495

    Article  PubMed  CAS  Google Scholar 

  6. Bundo M, Inao S, Nakamura A, Kato T, Ito K, Tadokoro M, Kabeya R, Sugimoto T, Kajita Y, Yoshida J (2002) Changes of neural activity correlate with the severity of cortical ischemia in patients with unilateral major cerebral artery occlusion. Stroke 33:61–66

    Article  PubMed  Google Scholar 

  7. Caramia MD, Palmieri MG, Giacomini P, Iani C, Dally L, Silvestrini M (2000) Ipsilateral activation of the unaffected motor cortex in patients with hemiparetic stroke. Clin Neurophysiol 111:1990–1996

    Article  PubMed  CAS  Google Scholar 

  8. Carey LM, Abbott DF, Egan GF, Bernhardt J, Donnan GA (2005) Motor impairment and recovery in the upper limb after stroke—behavioral and neuroanatomical correlates. Stroke 36:625–629

    Article  PubMed  Google Scholar 

  9. Carey LM, Abbott DF, Egan GF, O’Keefe GJ, Jackson GD, Bernhardt J, Donnan GA (2006) Evolution of brain activation with good and poor motor recovery after stroke. Neurorehabil Neural Repair 20:24–41

    Article  PubMed  Google Scholar 

  10. Cuadrado ML, Egido JA, Gonzalez-Gutierrez JL, Varela-de-Seijas E (1999) Bihemispheric contribution to motor recovery after stroke: a longitudinal study with transcranial Doppler ultrasonography. Cerebrovasc Dis 9:337–344

    Article  PubMed  CAS  Google Scholar 

  11. Dennis A, Bosnell R, Dawes H, Howells K, Cockburn J, Kischka U, Matthews P, Johansen-Berg H (2011) Cognitive context determines dorsal premotor cortical activity during hand movement in patients after stroke. Stroke 42:1056–1061

    Article  PubMed  Google Scholar 

  12. Dettmers C, Stephan KM, Lemon RN, Frackowiak RSJ (1997) Reorganization of the executive motor system after stroke. Cerebrovasc Dis 7:187–200

    Article  Google Scholar 

  13. Gerloff C, Richard J, Hadley J, Schulman AE, Honda M, Hallett M (1998) Functional coupling and regional activation of human cortical motor areas during simple, internally paced and externally paced finger movements. Brain 121:1513–1531

    Article  PubMed  Google Scholar 

  14. Girouard H, Iadecola C (2006) Neurovascular coupling in the normal brain and in hypertension, stroke and Alzheimer disease. J Appl Physiol 100:328–335

    Article  PubMed  CAS  Google Scholar 

  15. Honda M, Nagamine T, Fukuyama H, Yonekura Y, Kimura J, Shibasaki H (1997) Movement-related cortical potentials and regional cerebral blood flow change in patients with stroke after motor recovery. J Neurol Sci 146:117–126

    Article  PubMed  CAS  Google Scholar 

  16. Iadecola C (1998) Cerebral circulatory dysregulation in ischemia. In: Ginsberg MD, Bogousslavsky J (eds) Cerebrovascular Disease, vol 1. Blackwell, Cambridge, MA, pp 319–332

  17. Jueptner M, Weiller C (1995) Review: does measurement of regional cerebral blood flow reflect synaptic activity? Implications for PET and fMRI. Neuroimage 2:148–156

    Article  PubMed  CAS  Google Scholar 

  18. Kernagis DN, Laskowitz DT (2012) Evolving role of biomarkers in acute cerebrovascular disease. Ann Neurol 71:289–303

    Article  PubMed  CAS  Google Scholar 

  19. Kessler J, Thiel A, Karbe H, Heiss WD (2000) Piracetam improves activated blood flow and facilitates rehabilitation of poststroke aphasic patients. Stroke 31:2112–2116

    Article  PubMed  CAS  Google Scholar 

  20. Kleiser R, Wittsack HJ, Butefisch CM, Jorgens S, Seitz RJ (2005) Functional activation within the PI-DWI mismatch region in recovery from ischemic stroke: preliminary observations. NeuroImage 24:515–523

    Article  PubMed  CAS  Google Scholar 

  21. Koehler RC, Roman RJ, Harder DR (2009) Astrocytes and the regulation of cerebral blood flow. Trends Neurosci 32:160–169

    Article  PubMed  CAS  Google Scholar 

  22. Lin WH, Hao Q, Rosengarten B, Leung WH, Wong KS (2011) Impaired neurovascular coupling in ischaemic stroke patients with large or small vessel disease. Eur J Neurol 18:731–736

    Article  PubMed  CAS  Google Scholar 

  23. Lindegaard K, Lundar T, Wiberg J, Sjoberg D, Aaslid R, Nornes H (1987) Variations in middle cerebral artery blood flow investigated with noninvasive transcranial blood velocity measurements. Stroke 18:1025–1030

    Article  PubMed  CAS  Google Scholar 

  24. Marshall RS (2004) The functional relevance of cerebral hemodynamics: why blood flow matters to the injured and recovering brain. Cur Opin Neurol 17:705–709

    Article  Google Scholar 

  25. Marshall RS, Perera GM, Lazar RM, Krakauer JW, Constantine RC, DeLaPaz RL (2000) Evolution of cortical activation during recovery from corticospinal tract infarction. Stroke 31:656–661

    Article  PubMed  CAS  Google Scholar 

  26. Marshall RS, Zarahn E, Alon L, Minzer B, Lazar RM, Krakauer JW (2009) Early imaging correlates of subsequent motor recovery after stroke. Ann Neurol 65:596–602

    Article  PubMed  Google Scholar 

  27. Matteis M, Vernieri F, Troisi E, Pasqualetti P, Tibuzzi F, Caltagirone C, Silvestrini M (2003) Early cerebral hemodynamic changes during passive movements and motor recovery after stroke. J Neurol 250:810–817

    Article  PubMed  Google Scholar 

  28. Moody M, Panerai RB, Eames PJ, Potter JF (2005) Cerebral and systemic hemodynamic changes during cognitive and motor activation paradigms. Am J Physiol-Regul Integr Comp Physiol 288:R1581–R1588

    Article  PubMed  CAS  Google Scholar 

  29. Nelles G, Jentzen W, Bockisch A, Diener HC (2011) Neural substrates of good and poor recovery after hemiplegic stroke: a serial pet study. J Neurol 258:2168–2175

    Article  PubMed  CAS  Google Scholar 

  30. Nelles G, Spiekermann G, Jueptner M, Leonhardt G, Muller S, Gerhard H, Diener HC (1999) Reorganization of sensory and motor systems in hemiplegic stroke patients—a positron emission tomography study. Stroke 30:1510–1516

    Article  PubMed  CAS  Google Scholar 

  31. Poulin MJ, Liang PJ, Robbins PA (1996) Dynamics of the cerebral blood flow response to step changes in end-tidal PCO2 and PO2 in humans. J Appl Physiol 81:1084–1095

    PubMed  CAS  Google Scholar 

  32. Rehme AK, Fink GR, von Cramon DY, Grefkes C (2011) The role of the Contralesional motor cortex for motor recovery in the early days after stroke assessed with longitudinal fMRI. Cereb Cortex 21:756–768

    Article  PubMed  Google Scholar 

  33. Remy P, Zilbovicius M, Cesaro P, Amarenco P, Degos JD, Samson Y (1999) Primary somatosensory cortex activation is not altered in patients with ventroposterior thalamic lesions—a PET study. Stroke 30:2651–2658

    Article  PubMed  CAS  Google Scholar 

  34. Roy CS, Sherrington CS (1890) On the regulation of the blood-supply of the brain. J Physiol 11:85–158

    PubMed  CAS  Google Scholar 

  35. Salinet ASM, Panerai RB, Robinson TG (2012) Effects of active, passive and motor imagery paradigms on cerebral and peripheral hemodynamics in older volunteers: a functional TCD study. Ultrasound Med Biol 38:997–1003

    Article  PubMed  Google Scholar 

  36. Salinet ASM, Robinson TG, Panerai RB (2012) Reproducibility of cerebral and peripheral haemodynamic responses to active, passive and motor imagery paradigms in older healthy volunteers: a fTCD study. J Neurosci Methods 206:143–150

    Article  PubMed  Google Scholar 

  37. Seitz RJ, Hoflich P, Binkofski F, Tellmann L, Herzog H, Freund HJ (1998) Role of the premotor cortex in recovery from middle cerebral artery infarction. Arch Neurol 55:1081–1088

    Article  PubMed  CAS  Google Scholar 

  38. Silvestrini M, Caltagirone C, Cupini LM, Matteis M, Troisi E, Bernardi G (1993) Activation of healthy hemisphere in poststroke recovery—a transcranial Doppler study. Stroke 24:1673–1677

    Article  PubMed  CAS  Google Scholar 

  39. Silvestrini M, Cupini LM, Placidi F, Diomedi M, Bernardi G (1998) Bilateral hemispheric activation in the early recovery of motor function after stroke. Stroke 29:1305–1310

    Article  PubMed  CAS  Google Scholar 

  40. Silvestrini M, Troisi E, Matteis M, Cupini LM, Caltagirone C (1995) Involvement of the healthy hemisphere in recovery from aphasia and motor deficit in patients with cortical ischemic infarction: a transcranial Doppler study. Neurology 45:1815–1820

    Article  PubMed  CAS  Google Scholar 

  41. Silvestrini M, Troisi E, Matteis M, Razzano C, Caltagirone C (1998) Correlations of flow velocity changes during mental activity and recovery from aphasia in ischemic stroke. Neurology 50:191–195

    Article  PubMed  CAS  Google Scholar 

  42. Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. JAMA 283:2008–2012

    Article  PubMed  CAS  Google Scholar 

  43. Thiel A, Aleksic B, Klein JC, Rudolf J, Heiss WD (2007) Changes in proprioceptive systems activity during recovery from post-stroke hemiparesis. J Rehabil Med 39:520–525

    Article  PubMed  Google Scholar 

  44. Tiecks FP, Lam AM, Aaslid R, Newell DW (1995) Comparison of static and dynamic cerebral autoregulation measurements. Stroke 26:1014–1019

    Article  PubMed  CAS  Google Scholar 

  45. Treger I, Luzki L, Gil M, Ring H (2007) Transcranial Doppler monitoring during language tasks in stroke patients with aphasia. Disabil Rehabil 29:1177–1183

    Article  PubMed  CAS  Google Scholar 

  46. Weber R, Ramos-Cabrer P, Justicia C, Wiedermann D, Strecker C, Sprenger C, Hoehn M (2008) Early prediction of functional recovery after experimental stroke: functional magnetic resonance imaging, electrophysiology, and behavioural testing in rats. J Neurosci 28:1022–1029

    Article  PubMed  CAS  Google Scholar 

  47. Weder B, Knorr U, Herzog H, Nebeling B, Kleinschmidt A, Huang Y, Steinmetz H, Freund HJ, Seitz RJ (1994) Tactile exploration of shape after subcortical ischaemic infarction studied with PET. Brain 117:593–605

    Article  PubMed  Google Scholar 

  48. Weder B, Seitz RJ (1994) Deficient cerebral activation pattern in stroke recovery. NeuroReport 5:457–460

    Article  PubMed  CAS  Google Scholar 

  49. Weiller C, Chollet F, Friston KJ, Wise RJS, Frackowiak RSJ (1992) Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann Neurol 31:463–472

    Article  PubMed  CAS  Google Scholar 

  50. Weiller C, Ramsay SC, Wise RJ, Friston KJ, Frackowiak RS (1993) Individual patterns of functional reorganization in the human cerebral cortex after capsular infarction. Ann Neurol 33:181–189

    Article  PubMed  CAS  Google Scholar 

  51. Wittenberg GF, Bastian AJ, Dromerick AW, Thach WT, Powers WJ (2000) Mirror movements complicate interpretation of cerebral activation changes during recovery from subcortical infarction. Neurorehabil Neural Repair 14:213–221

    PubMed  CAS  Google Scholar 

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Acknowledgments

Angela Salinet is funded by the Brazilian Ministry of Education (Grant Number 0411-10-8).

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Correspondence to Angela S. M. Salinet.

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Salinet, A.S.M., Haunton, V.J., Panerai, R.B. et al. A systematic review of cerebral hemodynamic responses to neural activation following stroke. J Neurol 260, 2715–2721 (2013). https://doi.org/10.1007/s00415-013-6836-z

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  • DOI: https://doi.org/10.1007/s00415-013-6836-z

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