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Research Article| Volume 367, P143-147, August 15, 2016

Dissociation among hemodynamic measures in asymptomatic high grade carotid artery stenosis

      Highlights

      • Cerebral hemodynamics can be measured in several ways in unilateral high-grade carotid stenosis.
      • Each measure showed significant asymmetry, but there was low correlation among them.
      • Low correlation among hemodynamic measures suggests unique physiological contributions.
      • Choice of hemodynamic measurement techniques depends on the outcome of interest.

      Abstract

      Background

      Cerebral blood flow (CBF) regulation is a critical element in cerebrovascular pathophysiology, particularly in large vessel disease, but the best method to use for hemodynamic assessment is not clear. We examined 4 different blood-flow related measures in patients with unilateral high-grade carotid artery disease, assessing asymmetry between the occluded vs non-occluded side, and the correlations among the measures.

      Methods

      Thirty-three patients (age 50–93, 19 M) with unilateral 80–100% ICA occlusion but no stroke underwent: 1) mean flow velocity (MFV) in both middle cerebral arteries by transcranial Doppler (TCD), 2) quantitative resting CBF using pseudo-continuous arterial spin labeling (pCASL) MRI, 3) vasomotor reactivity (VMR) in response to 5% CO2 inhalation, and 4) dynamic cerebral autoregulation (DCA) assessing the counter-regulation of blood flow to spontaneous changes in blood pressure using TCD monitoring and finger photoplethysmography. Paired t-tests and Pearson correlations assessed side-to-side differences within each measure, and correlations between measures.

      Results

      CBF (p = 0.001), MFV (p < 0.001), VMR (p = 0.008), and DCA (p = 0.047) all showed significantly lower values on the occluded side. The 4 measures were independent of each other on correlation analysis, even when controlling for age and anterior circle of Willis collateral (all partial correlations <0.233 and p-values >0.468).

      Conclusions

      These 4 measures showed high sensitivity to the occluded carotid artery, but their dissociation suggests that any given measure only partially characterizes the hemodynamic state. Additional research is needed to explore the multifaceted biology of cerebral blood flow regulation.

      Keywords

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      References

        • Derdeyn C.P.
        • Grubb Jr., R.L.
        • Powers W.J.
        Cerebral hemodynamic impairment: methods of measurement and association with stroke risk.
        Neurology. 1999 Jul 22; 53 (PubMed PMID: 10430410): 251-259
        • Hartmann A.
        • Mast H.
        • Thompson J.L.
        • Sia R.M.
        • Mohr J.P.
        Transcranial Doppler waveform blunting in severe extracranial carotid artery stenosis.
        Cerebrovasc. Dis. 2000 Jan-Feb; 10 (PubMed PMID: 10629344): 33-38
        • Bos M.J.
        • Koudstaal P.J.
        • Hofman A.
        • Witteman J.C.
        • Breteler M.M.
        Transcranial Doppler hemodynamic parameters and risk of stroke: the Rotterdam study.
        Stroke. 2007 Sep; 38 (PubMed PMID: 17673712): 2453-2458
        • Bokkers R.P.
        • Bremmer J.P.
        • van Berckel B.N.
        • Lammertsma A.A.
        • Hendrikse J.
        • Pluim J.P.
        • et al.
        Arterial spin labeling perfusion MRI at multiple delay times: a correlative study with H(2)(15)O positron emission tomography in patients with symptomatic carotid artery occlusion.
        J. Cereb. Blood Flow Metab. 2010 Jan; 30 (PubMed PMID: 19809464. Pubmed Central PMCID: 2949108): 222-229
        • Vernieri F.
        • Pasqualetti P.
        • Passarelli F.
        • Rossini P.M.
        • Silvestrini M.
        Outcome of carotid artery occlusion is predicted by cerebrovascular reactivity.
        Stroke. 1999 Mar; 30 (PubMed PMID: 10066857): 593-598
        • Marshall R.S.
        • Lazar R.M.
        • Young W.L.
        • Solomon R.A.
        • Joshi S.
        • Duong D.H.
        • et al.
        Clinical utility of quantitative cerebral blood flow measurements during internal carotid artery test occlusions.
        Neurosurgery. 2002 May; 50 (discussion -5. PubMed PMID: 11950402): 996-1004
        • Reinhard M.
        • Schwarzer G.
        • Briel M.
        • Altamura C.
        • Palazzo P.
        • King A.
        • et al.
        Cerebrovascular reactivity predicts stroke in high-grade carotid artery disease.
        Neurology. 2014 Oct 14; 83 (PubMed PMID: 25217057. Pubmed Central PMCID: 4206163): 1424-1431
        • Diehl R.R.
        • Linden D.
        • Lucke D.
        • Berlit P.
        Phase relationship between cerebral blood flow velocity and blood pressure. A clinical test of autoregulation.
        Stroke. 1995 Oct; 26 (PubMed PMID: 7570728): 1801-1804
        • Zhang R.
        • Zuckerman J.H.
        • Giller C.A.
        • Levine B.D.
        Transfer function analysis of dynamic cerebral autoregulation in humans.
        Am. J. Phys. 1998 Jan; 274 (PubMed PMID: 9458872): H233-H241
        • Reinhard M.
        • Hetzel A.
        • Lauk M.
        • Lucking C.H.
        Dynamic cerebral autoregulation testing as a diagnostic tool in patients with carotid artery stenosis.
        Neurol. Res. 2001 Jan; 23 (PubMed PMID: 11210431. Epub 2001/02/24. eng): 55-63
        • Panerai R.B.
        Cerebral autoregulation: from models to clinical applications.
        Cardiovascular engineering. 2008 Mar; 8 (PubMed PMID: 18041584): 42-59
        • Verghese J.
        • Lipton R.B.
        • Hall C.B.
        • Kuslansky G.
        • Katz M.J.
        Low blood pressure and the risk of dementia in very old individuals.
        Neurology. 2003 Dec 23; 61 (PubMed PMID: 14694027): 1667-1672
        • Birns J.
        • Markus H.
        • Kalra L.
        Blood pressure reduction for vascular risk: is there a price to be paid?.
        Stroke. 2005 Jun; 36 (PubMed PMID: 15860749): 1308-1313
        • Hadjiev D.I.
        • Mineva P.P.
        Antihypertensive treatment with cerebral hemodynamics monitoring by ultrasonography in elderly hypertensives without a history of stroke may prevent or slow down cognitive decline. A pending issue.
        Med. Hypotheses. 2011 Mar; 76 (PubMed PMID: 21134723): 434-437
        • Balestrini S.
        • Perozzi C.
        • Altamura C.
        • Vernieri F.
        • Luzzi S.
        • Bartolini M.
        • et al.
        Severe carotid stenosis and impaired cerebral hemodynamics can influence cognitive deterioration.
        Neurology. 2013 Jun 4; 80 (PubMed PMID: 23624562): 2145-2150
        • Asllani I.
        • Borogovac A.
        • Brown T.R.
        Regression algorithm correcting for partial volume effects in arterial spin labeling MRI.
        Magn. Reson. Med. 2008 Dec; 60 (PubMed PMID: 18828149): 1362-1371
        • Dai W.
        • Garcia D.
        • de Bazelaire C.
        • Alsop D.C.
        Continuous flow-driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields.
        Magn. Reson. Med. 2008 Dec; 60 (PubMed PMID: 19025913. Pubmed Central PMCID: 2750002): 1488-1497
        • Borogovac A.
        • Habeck C.
        • Small S.A.
        • Asllani I.
        Mapping brain function using a 30-day interval between baseline and activation: a novel arterial spin labeling fMRI approach.
        J. Cereb. Blood Flow Metab. 2010 Oct; 30 (PubMed PMID: 20648039. Pubmed Central PMCID: 3023398. Epub 2010/07/22. eng): 1721-1733
        • Petersen N.H.
        • Ortega-Gutierrez S.
        • Reccius A.
        • Masurkar A.
        • Huang A.
        • Marshall R.S.
        Comparison of Non-invasive and Invasive Arterial Blood Pressure Measurement for Assessment of Dynamic Cerebral Autoregulation.
        Neurocrit Care, 2013 Nov 14 (PubMed PMID: 24233812)
        • Bokkers R.P.
        • van Osch M.J.
        • van der Worp H.B.
        • de Borst G.J.
        • Mali W.P.
        • Hendrikse J.
        Symptomatic carotid artery stenosis: impairment of cerebral autoregulation measured at the brain tissue level with arterial spin-labeling MR imaging.
        Radiology. 2010 Jul; 256 (PubMed PMID: 20574097): 201-208
        • Powers W.J.
        • Zazulia A.R.
        The use of positron emission tomography in cerebrovascular disease.
        Neuroimaging Clin. N. Am. 2003 Nov; 13 (PubMed PMID: 15024958): 741-758
        • Teng M.M.
        • Cheng H.C.
        • Kao Y.H.
        • Hsu L.C.
        • Yeh T.C.
        • Hung C.S.
        • et al.
        MR perfusion studies of brain for patients with unilateral carotid stenosis or occlusion: evaluation of maps of “time to peak” and “percentage of baseline at peak”.
        J. Comput. Assist. Tomogr. 2001 Jan-Feb; 25 (PubMed PMID: 11176306): 121-125
        • Kluytmans M.
        • van der Grond J.
        • van Everdingen K.J.
        • Klijn C.J.
        • Kappelle L.J.
        • Viergever M.A.
        Cerebral hemodynamics in relation to patterns of collateral flow.
        Stroke. 1999 Jul; 30 (PubMed PMID: 10390319): 1432-1439
        • Tzeng Y.C.
        • Ainslie P.N.
        • Cooke W.H.
        • Peebles K.C.
        • Willie C.K.
        • MacRae B.A.
        • et al.
        Assessment of cerebral autoregulation: the quandary of quantification.
        Am. J. Physiol. Heart Circ. Physiol. 2012 Sep 15; 303 (PubMed PMID: 22821992): H658-H671
        • Petersen N.H.
        • Ortega-Gutierrez S.
        • Reccius A.
        • Masurkar A.
        • Huang A.
        • Marshall R.S.
        Dynamic cerebral autoregulation is transiently impaired for one week after large-vessel acute ischemic stroke.
        Cerebrovasc. Dis. 2015; 39 (PubMed PMID: 25661277): 144-150
        • Dawson S.L.
        • Blake M.J.
        • Panerai R.B.
        • Potter J.F.
        Dynamic but not static cerebral autoregulation is impaired in acute ischaemic stroke.
        Cerebrovasc. Dis. 2000 Mar-Apr; 10 (PubMed PMID: 10686451): 126-132
        • Eames P.J.
        • Blake M.J.
        • Dawson S.L.
        • Panerai R.B.
        • Potter J.F.
        Dynamic cerebral autoregulation and beat to beat blood pressure control are impaired in acute ischaemic stroke.
        J. Neurol. Neurosurg. Psychiatry. 2002 Apr; 72 (PubMed PMID: 11909905): 467-472
        • Guo Z.N.
        • Xing Y.
        • Wang S.
        • Ma H.
        • Liu J.
        • Yang Y.
        Characteristics of dynamic cerebral autoregulation in cerebral small vessel disease: diffuse and sustained.
        Scientific reports. 2015; 5 (PubMed PMID: 26469343): 15269
        • Gommer E.D.
        • Staals J.
        • van Oostenbrugge R.J.
        • Lodder J.
        • Mess W.H.
        • Reulen J.P.
        Dynamic cerebral autoregulation and cerebrovascular reactivity: a comparative study in lacunar infarct patients.
        Physiol. Meas. 2008 Nov; 29 (PubMed PMID: 18843165): 1293-1303
        • Giannopoulos S.
        • Boden-Albala B.
        • Choi J.H.
        • Carrera E.
        • Doyle M.
        • Perez T.
        • et al.
        Metabolic syndrome and cerebral vasomotor reactivity.
        Eur. J. Neurol. 2010 Dec; 17 (PubMed PMID: 20500212. Epub 2010/05/27. eng): 1457-1462
        • Huq R.
        • Philbey C.E.
        • Mistri A.K.
        • Panerai R.B.
        • Robinson T.G.
        Dynamic cerebral autoregulation assessed by respiratory manoeuvres in non-insulin-treated type 2 diabetes mellitus.
        Diabet. Med. 2012 May; 29 (PubMed PMID: 22004530): 609-613
        • Reinhard M.
        • Roth M.
        • Muller T.
        • Czosnyka M.
        • Timmer J.
        • Hetzel A.
        Cerebral autoregulation in carotid artery occlusive disease assessed from spontaneous blood pressure fluctuations by the correlation coefficient index.
        Stroke. 2003 Sep; 34 (PubMed PMID: 12920261. Epub 2003/08/16. eng): 2138-2144
        • Roc A.C.
        • Wang J.
        • Ances B.M.
        • Liebeskind D.S.
        • Kasner S.E.
        • Detre J.A.
        Altered hemodynamics and regional cerebral blood flow in patients with hemodynamically significant stenoses.
        Stroke. 2006 Feb; 37 (PubMed PMID: 16373653): 382-387
        • Klijn C.J.
        • Kappelle L.J.
        • van Huffelen A.C.
        • Visser G.H.
        • Algra A.
        • Tulleken C.A.
        • et al.
        Recurrent ischemia in symptomatic carotid occlusion: prognostic value of hemodynamic factors.
        Neurology. 2000 Dec 26; 55 (PubMed PMID: 11134377): 1806-1812
        • Yujie Q.
        • Borogovac A.
        • Laine A.
        • Hirsch J.
        • Asllani I.
        Tissue specific arterial spin labeling fMRI: a superior method for imaging cerebral blood flow in aging and disease.
        Conf. Proc. IEEE Eng. Med. Biol. Soc. 2014; 2014 (PubMed PMID: 25571530): 6687-6690
        • Yoshiura T.
        • Hiwatashi A.
        • Yamashita K.
        • Ohyagi Y.
        • Monji A.
        • Takayama Y.
        • et al.
        Simultaneous measurement of arterial transit time, arterial blood volume, and cerebral blood flow using arterial spin-labeling in patients with Alzheimer disease.
        AJNR Am. J. Neuroradiol. 2009 Aug; 30 (PubMed PMID: 19342545): 1388-1393
        • Bokkers R.P.
        • van der Worp H.B.
        • Mali W.P.
        • Hendrikse J.
        Noninvasive MR imaging of cerebral perfusion in patients with a carotid artery stenosis.
        Neurology. 2009 Sep 15; 73 (PubMed PMID: 19752454): 869-875
        • Leoni R.F.
        • Paiva F.F.
        • Kang B.T.
        • Henning E.C.
        • Nascimento G.C.
        • Tannus A.
        • et al.
        Arterial spin labeling measurements of cerebral perfusion territories in experimental ischemic stroke.
        Translational stroke research. 2012 Mar; 3 (PubMed PMID: 24323754): 44-55
        • Avirame K.
        • Lesemann A.
        • List J.
        • Witte A.V.
        • Schreiber S.J.
        • Floel A.
        Cerebral autoregulation and brain networks in occlusive processes of the internal carotid artery.
        J. Cereb. Blood Flow Metab. 2015 Feb; 35 (PubMed PMID: 25388676. Pubmed Central PMCID: 4426740): 240-247
        • Hess D.C.
        • Hoda M.N.
        • Khan M.B.
        Humoral mediators of remote ischemic conditioning: important role of eNOS/NO/nitrite.
        Acta Neurochir. Suppl. 2016; 121 (PubMed PMID: 26463921): 45-48
        • Franklin T.R.
        • Wang Z.
        • Sciortino N.
        • Harper D.
        • Li Y.
        • Hakun J.
        • et al.
        Modulation of resting brain cerebral blood flow by the GABA B agonist, baclofen: a longitudinal perfusion fMRI study.
        Drug and alcohol dependence. 2011 Sep 1; 117 (PubMed PMID: 21333466. Pubmed Central PMCID: 3348615): 176-183
        • Jing Z.
        • Shi C.
        • Zhu L.
        • Xiang Y.
        • Chen P.
        • Xiong Z.
        • et al.
        Chronic cerebral hypoperfusion induces vascular plasticity and hemodynamics but also neuronal degeneration and cognitive impairment.
        J. Cereb. Blood Flow Metab. 2015 Aug; 35 (PubMed PMID: 25853908. Pubmed Central PMCID: 4528009): 1249-1259
        • Wirth M.
        • Pichet Binette A.
        • Brunecker P.
        • Kobe T.
        • Witte A.V.
        • Floel A.
        Divergent regional patterns of cerebral hypoperfusion and gray matter atrophy in mild cognitive impairment patients.
        J. Cereb. Blood Flow Metab. 2016 Apr 1; (PubMed PMID: 27037094)
        • Olsen T.S.
        • Larsen B.
        • Herning M.
        • Skriver E.B.
        • Lassen N.A.
        Blood flow and vascular reactivity in collaterally perfused brain tissue. Evidence of an ischemic penumbra in patients with acute stroke.
        Stroke. 1983 May-Jun; 14 (PubMed PMID: 6658900): 332-341
        • Kawamura Y.
        • Meyer J.S.
        • Hiromoto H.
        • Aoyagi M.
        • Hashi K.
        Neurogenic control of cerebral blood flow in the baboon. Effects of alpha adrenergic blockade with phenoxybenzamine on cerebral autoregulation and vasomotor reactivity to changes in PaCO2.
        Stroke. 1974 Nov-Dec; 5 (PubMed PMID: 4432254): 747-758
        • Panerai R.B.
        • Deverson S.T.
        • Mahony P.
        • Hayes P.
        • Evans D.H.
        Effects of CO2 on dynamic cerebral autoregulation measurement.
        Physiol. Meas. 1999 Aug; 20 (PubMed PMID: 10475580): 265-275
        • Carrera E.
        • Lee L.K.
        • Giannopoulos S.
        • Marshall R.S.
        Cerebrovascular reactivity and cerebral autoregulation in normal subjects.
        J. Neurol. Sci. 2009 Oct 15; 285 (PubMed PMID: 19608202. Epub 2009/07/18. eng): 191-194