Skip to main content
SpringerLink
Log in

Relative Cerebral Blood Transit Time Decline and Neurological Improvement in Patients After Internal Carotid Artery Stenting

  • Chapter
  • First Online:
Advances in Biomedicine

Part of the book series: Advances in Experimental Medicine and Biology ((CLEXBI,volume 1176))

Abstract

In this study we hypothesized that the alleviation of neurological symptoms long after internal carotid artery (ICA) stenting may be related to sustained improvement of cerebral perfusion. Thirty-four subjects (F/M; 15/19) with >70% stenosis of a single internal carotid artery and neurological symptoms, who underwent a carotid artery stenting procedure, were studied. Brain computed tomography perfusion (CTP) imaging was performed before and 3 years after ICA stenting. The following relative variables were compared: cerebral blood flow (rCBF), cerebral blood volume (rCBV), mean transit time (rMTT), time to peak (rTTP), and permeability surface area product (rPS). A survey also was conducted to compare the patients’ clinical symptoms. Overall, we found that a trend toward rMTT decline was the only persisting change after ICA stenting. We then stratified the patients into the subgroups of <2%, 2–5%, and > 5% rMTT decline and found that those with a rMTT decline >2% reported a prominent reduction in subjective clinical symptoms such as headache, dizziness, tinnitus, blurred vision, transient blindness, a sense of gravity of the head, and pain in the eyeballs. We conclude that a shortened mean rMTT, likely reflecting improved cerebral microcirculation, underlies the improvement of neurological symptoms in patients with ICA stenosis.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Arba F, Mair G, Carpenter T, Sakka E, Sandercock PAG, Lindley RI, Inzitari D, Wardlaw JM, IST–3 Trial Collaborators (2017) Cerebral white matter hypoperfusion increases with small–vessel disease burden. Data from the Third International Stroke Trial. J Stroke Cerebrovasc Dis 26:1506–1513

    Article  Google Scholar 

  • Aribisala BS, Morris Z, Eadie E, Thomas A, Gow A, Valdés Hernández MC, Royle NA, Bastin ME, Starr J, Deary IJ, Wardlaw JM (2014) Blood pressure, internal carotid artery flow parameters, and age–related white matter hyperintensities. Hypertension 63:1011–1018

    Article  CAS  Google Scholar 

  • Bakker FC, Klijn CJ, Jennekens–Schinkel A, Kappelle LJ (2000) Cognitive disorders in patients with occlusive disease of the carotid artery: a systematic review of the literature. J Neurol 247:669–676

    Article  CAS  Google Scholar 

  • Cao W, Yassi N, Sharma G, Yan B, Desmond PM, Davis SM, Campbell BC (2016) Diagnosing acute lacunar infarction using CT perfusion. J Clin Neurosci 29:70–72

    Article  CAS  Google Scholar 

  • Chida K, Ogasawara K, Aso K, Suga Y, Kobayashi M, Yoshida K, Terasaki K, Tsushina E, Ogawa A (2010) Postcarotid endarterectomy improvement in cognition is associated with resolution of crossed cerebellar hypoperfusion and increase in 123I–iomazenil uptake in the cerebral cortex: a SPECT study. Cerebrovasc Dis 29(4):343–351

    Article  Google Scholar 

  • Ding L, Hong Y, Peng B (2017) Association between large artery atherosclerosis and cerebral microbleeds: a systematic review and meta–analysis. Stroke Vasc Neurol 2:7–14

    Article  Google Scholar 

  • Duan Y, Li G, Yang Y, Li J, Huang H, Wang H, Xu F, Chen W (2012) Changes in cerebral hemodynamics after carotid stenting of symptomatic carotid artery. Eur J Radiol 81:744–748

    Article  Google Scholar 

  • Duncombe J, Kitamura A, Hase Y, Ihara M, Kalaria RN, Horsburgh K (2017) Chronic cerebral hypoperfusion: a key mechanism leading to vascular cognitive impairment and dementia. Closing the translational gap between rodent models and human vascular cognitive impairment and dementia. Clin Sci 131:2451–2468

    Article  CAS  Google Scholar 

  • Esteban JM, Cervera V (2004) Perfusion CT and angio CT in the assessment of acute stroke. Neuroradiology 46:705–715

    Article  CAS  Google Scholar 

  • Fadrná T, Mikšová Z, Herzig R, Langová K, Ličman L, Školoudík D (2018) Factors influencing quality of life in patients followed in the neurosonology laboratory for carotid stenosis. Health Qual Life Outcomes 16(1):79

    Article  Google Scholar 

  • Fiorella D, Heiserman J, Prenger E, Partovi S (2004) Assessment of the reproducibility of postprocessing dynamic CT perfusion data. AJNR Am J Neuroradiol 25:97–107

    PubMed  Google Scholar 

  • Frydrychowski AF, Winklewski PJ, Szarmach A, Halena G, Bandurski T (2013) Near–infrared transillumination back scattering sounding––new method to assess brain microcirculation in patients with chronic carotid artery stenosis. PLoS One 8:e61936

    Article  CAS  Google Scholar 

  • Goessens BM, Visseren FL, Kappelle LJ, Algra A, van der Graaf Y (2007) Asymptomatic carotid artery stenosis and the risk of new vascular events in patients with manifest arterial disease: the SMART Study. Stroke 38:1470–1475

    Article  Google Scholar 

  • Grunwald IQ, Supprian T, Politi M, Struffert T, Falkai P, Krick C, Backens M, Reith W (2006) Cognitive changes after carotid artery stenting. Neuroradiology 48:319–323

    Article  CAS  Google Scholar 

  • Huang H, Chen K, Guo T, Zhang Y, Qu W, Zhou Z, Liu G, Chen L (2012) Treatment with carotid angioplasty stent placement for post-stroke depression compared to antidepressants. Neurosciences (Riyadh) 17(1):53–56

    Google Scholar 

  • Jain R, Ellika SK, Scarpace L, Schultz LR, Rock JP, Gutierrez J, Patel SC, Ewing J, Mikkelsen T (2008) Quantitative estimation of permeability surface–area product in astroglial brain tumors using perfusion CT and correlation with histopathologic grade. Am J Neuroradiol 29:694–700

    Article  CAS  Google Scholar 

  • Kaiser D, Weise G, Möller K, Scheibe J, Pösel C, Baasch S, Gawlitza M, Lobsien D, Diederich K, Minnerup J, Kranz A, Boltze J, Wagner DC (2014) Spontaneous white matter damage, cognitive decline and neuroinflammation in middle–aged hypertensive rats: an animal model of early–stage cerebral small vessel disease. Acta Neuropathol Commun 2:169

    Article  Google Scholar 

  • Kamalian S, Kamalian S, Maas MB, Goldmacher GV, Payabvash S, Akbar A, Schaefer PW, Furie KL, Gonzalez RG, Lev MH (2011) CT cerebral blood flow maps optimally correlate with admission diffusion–weighted imaging in acute stroke but thresholds vary by postprocessing platform. Stroke 42:1923–1928

    Article  Google Scholar 

  • Kim HA, Miller AA, Drummond GR, Thrift AG, Arumugam TV, Phan TG, Srikanth VK, Sobey CG (2012) Vascular cognitive impairment and Alzheimer’s disease: role of cerebral hypoperfusion and oxidative stress. Naunyn Schmiedeberg’s Arch Pharmacol 385:953–959

    Article  CAS  Google Scholar 

  • Koenig M, Kraus M, Theek C, Klotz E, Gehlen W, Heuser L (2001) Quantitative assessment of the ischemic brain by means of perfusion–related parameters derived from perfusion CT. Stroke 32:431–437

    Article  CAS  Google Scholar 

  • Kudo K, Sasaki M, Yamada K, Momoshima S, Utsunomiya H, Shirato H, Ogasawara K (2010) Differences in CT perfusion maps generated by different commercial software: quantitative analysis by using identical source data of acute stroke patients. Radiology 254:200–209

    Article  Google Scholar 

  • Lin K, Kazmi KS, Law M, Babb J, Peccerelli N, Pramanik BK (2007) Measuring elevated microvascular permeability and predicting hemorrhagic transformation in acute ischemic stroke using first–pass dynamic perfusion CT imaging. AJNR Am J Neuroradiol 28:1292–1298

    Article  CAS  Google Scholar 

  • Lovett JK, Rothwell PM (2002) Suicide in a patient with symptomatic carotid occlusion. J R Soc Med 95:93–94

    Article  CAS  Google Scholar 

  • Mathiesen EB, Waterloo K, Joakimsen O, Bakke SJ, Jacobsen EA, Bønaa KH (2004) Reduced neuropsychological test performance in asymptomatic carotid stenosis: The Tromso Study. Neurology 62:695–701

    Article  CAS  Google Scholar 

  • Mencl S, Garz C, Niklass S, Braun H, Göb E, Homola G, Heinze HJ, Reymann KG, Kleinschnitz C, Schreiber S (2013) Early microvascular dysfunction in cerebral small vessel disease is not detectable on 3.0 Tesla magnetic resonance imaging: a longitudinal study in spontaneously hypertensive stroke–prone rats. Exp Transl Stroke Med 5:8

    Article  Google Scholar 

  • Merckel LG, Van der Heijden J, Jongen LM, van Es HW, Prokop M, Waaijer A (2012) Effect of stenting on cerebral CT perfusion in symptomatic and asymptomatic patients with carotid artery stenosis. AJNR Am J Neuroradiol 33:280–285

    Article  CAS  Google Scholar 

  • NASCET – North American Symptomatic Carotid Endarterectomy Trial Collaborators (1991) Beneficial effect of carotid endarterectomy in symptomatic patients with high–grade carotid stenosis. N Engl J Med 325:445–453

    Article  Google Scholar 

  • Nicolaides AN, Kakkos SK, Griffin M (2005) Severity of asymptomatic carotid stenosis and risk of ipsilateral hemispheric ischaemic events: results from the ACSRS study. Eur J Vasc Endovasc Surg 30:275–284

    Article  CAS  Google Scholar 

  • Niesen WD, Rosenkranz M, Eckert B, Meissner M, Weiller C, Sliwka U (2004) Hemodynamic changes of the cerebral circulation after stent–protected carotid angioplasty. Am J Neuroradiol 25:1162–1167

    PubMed  Google Scholar 

  • Picchetto L, Spalletta G, Casolla B, Cacciari C, Cavallari M, Fantozzi C, Ciuffoli A, Rasura M, Imperiale F, Sette G, Caltagirone C, Taurino M, Orzi F (2013) Cognitive performance following carotid endarterectomy or stenting in asymptomatic patients with severe ICA stenosis. Cardiovasc Psychiatry Neurol 2013:342571

    Article  Google Scholar 

  • Popovic IM, Lovrencic–Huzjan A, Simundic AM, Popovic A, Seric V, Demarin V (2011) Cognitive performance in asymptomatic patients with advanced carotid disease. Cogn Behav Neurol 24:145–151

    Article  Google Scholar 

  • Pucite E, Krievina I, Miglane E, Erts R, Krievins D (2017) Influence of severe carotid stenosis on cognition, depressive symptoms and quality of life. Clin Pract Epidemiol Ment Health 13:168–180

    Article  Google Scholar 

  • Rao R, Jackson S, Howard R (2001) Depression in older people with mild stroke, carotid stenosis and peripheral vascular disease: a comparison with healthy controls. Int J Geriatr Psychiatry 16:175–183

    Article  CAS  Google Scholar 

  • Ricotta JJ, Aburahma A, Ascher E (2011) Updated society for vascular surgery guidelines for management of extracranial carotid disease. J Vasc Surg 54:e1–e31

    Article  Google Scholar 

  • Romero JR, Beiser A, Seshadri S, Benjamin EJ, Polak JF, Vasan RS, Au R, DeCarli C, Wolf PA (2009) Carotid artery atherosclerosis, MRI indices of brain ischemia, aging, and cognitive impairment: the Framingham study. Stroke 40:1590–1596

    Article  Google Scholar 

  • Rouhl RP, Damoiseaux JG, Lodder J, Theunissen RO, Knottnerus IL, Staals J, Henskens LH, Kroon AA, de Leeuw PW, Tervaert JW, van Oostenbrugge RJ (2012) Vascular inflammation in cerebral small vessel disease. Neurobiol Aging 33:1800–1806

    Article  CAS  Google Scholar 

  • Samson RH, Showalter DP, Yunis JP, Dorsay DA, Kulman HI, Silverman SR (1999) Hemodynamically significant early recurrent carotid stenosis: an often self–limiting and self–reversing condition. J Vasc Surg 30:446–452

    Article  CAS  Google Scholar 

  • Schreiber S, Bueche CZ, Garz C, Kropf S, Angenstein F, Goldschmidt J, Neumann J, Heinze HJ, Goertler M, Reymann KG, Braun H (2012) The pathologic cascade of cerebrovascular lesions in SHRSP: is erythrocyte accumulation an early phase? J Cereb Blood Flow Metab 32:278–290

    Article  CAS  Google Scholar 

  • Schreiber S, Bueche CZ, Garz C, Braun H (2013) Blood brain barrier breakdown as the starting point of cerebral small vessel disease? New insights from a rat model. Exp Transl Stroke Med 5:4

    Article  Google Scholar 

  • Shan L, Shan J, Saxena A, Robinson D (2015) Quality of life and functional status after carotid revascularisation: a systematic review and meta–analysis. Eur J Vasc Endovasc Surg 49:634–645

    Article  CAS  Google Scholar 

  • Singer J, Trollor JN, Baune BT, Sachdev PS, Smith E (2014) Arterial stiffness, the brain and cognition: a systematic review. Ageing Res Rev 15:16–27

    Article  Google Scholar 

  • St Lawrence KS, Lee TY (1998a) An adiabatic approximation to the tissue homogeneity model for water exchange in the brain: I. Theoretical derivation. J Cereb Blood Flow Metab 18:1365–1377

    Article  CAS  Google Scholar 

  • St Lawrence KS, Lee TY (1998b) An adiabatic approximation to the tissue homogeneity model for water exchange in the brain: II. Experimental validation. J Cereb Blood Flow Metab 18:1378–1385

    Article  CAS  Google Scholar 

  • Szarmach A, Halena G, Kaszubowski M, Piskunowicz M, Szurowska E, Frydrychowski AF, Winklewski PJ (2016) Perfusion computed tomography: 4 cm versus 8 cm coverage size in subjects with chronic carotid artery stenosis. Br J Radiol 89:20150949

    Article  Google Scholar 

  • Szarmach A, Halena G, Kaszubowski M, Piskunowicz M, Studniarek M, Lass P, Szurowska E, Winklewski PJ (2017) Carotid artery stenting and blood–brain barrier permeability in subjects with chronic carotid artery stenosis. Int J Mol Sci 18:E1008

    Article  Google Scholar 

  • Sztriha LK, Nemeth D, Sefcsik T, Vecsei L (2009) Carotid stenosis and the cognitive function. J Neurol Sci 283:36–40

    Article  Google Scholar 

  • Topakian R, Barrick T, Howe F, Markus H (2010) Blood–brain barrier permeability is increased in normal–appearing white matter in patients with lacunar stroke and leucoaraiosis. J Neurol Neurosurg Psychiatry 81:192–197

    Article  CAS  Google Scholar 

  • Trojanowska A, Drop A, Jargiello T, Wojczal J, Szczerbo–Trojanowska M (2006) Changes in cerebral hemodynamics after carotid stenting: evaluation with CT perfusion studies. J Neuroradiol 33:169–174

    Article  CAS  Google Scholar 

  • van Sloten TT, Protogerou AD, Henry RM, Schram MT, Launer LJ, Stehouwer CD (2015) Association between arterial stiffness, cerebral small vessel disease and cognitive impairment: a systematic review and meta–analysis. Neurosci Biobehav Rev 53:121–130

    Article  Google Scholar 

  • Wang T, Mei B, Zhang J (2016) Atherosclerotic carotid stenosis and cognitive function. Clin Neurol Neurosurg 146:64–70

    Article  Google Scholar 

  • Wang T, Sun D, Liu Y, Mei B, Li H, Zhang S, Zhang J (2017) The impact of carotid artery stenting on cerebral perfusion, functional connectivity, and cognition in severe asymptomatic carotid stenosis patients. Front Neurol 8:403

    Article  Google Scholar 

  • Wardlaw JM, Allerhand M, Eadie E, Thomas A, Corley J, Pattie A, Taylor A, Shenkin SD, Cox S, Gow A, Starr JM, Deary IJ (2017) Carotid disease at age 73 and cognitive change from age 70 to 76 years: a longitudinal cohort study. J Cereb Blood Flow Metab 37:3042–3052

    Article  Google Scholar 

  • Wilkinson ID, Griffiths PD, Hoggard N, Cleveland TJ, Gaines PA, Macdonald S, McKevitt F, Venables GS (2003) Short–term changes in cerebral microhemodynamics after carotid stenting. AJNR Am J Neuroradiol 24:1501–1507

    PubMed  Google Scholar 

  • Winklewski PJ, Kaszubowski M, Halena G, Sabisz A, Chwojnicki K, Piskunowicz M, Kurhaluk N, Szurowska E, Szarmach A (2019) Computed tomography indicators of cerebral microperfusion improve long term after carotid stenting in symptomatic patients. Acta Biochim Pol https://doi.org/10.18388/abp.2017

    Google Scholar 

  • Yamashita T, Ogasawara K, Kuroda H, Suzuki T, Chida K, Kobayashi M, Yoshida K, Kubo Y, Ogawa A (2012) Combination of preoperative cerebral blood flow and 123I–iomazenil SPECT imaging predicts postoperative cognitive improvement in patients undergoing uncomplicated endarterectomy for unilateral carotid stenosis. Clin Nucl Med 37(2):128–133

    Article  Google Scholar 

  • Zhang J, Wang J, Geng D, Li Y, Song D, Gu Y (2013) Whole–brain CT perfusion and CT angiography assessment of Moyamoya disease before and after surgical revascularization: preliminary study with 256–slice CT. PLoS One 8:e57595

    Article  CAS  Google Scholar 

  • Zussman BM, Boghosian G, Gorniak RJ, Olszewski ME, Read KM, Siddiqui KM, Flanders AE (2011) The relative effect of vendor variability in CT perfusion results: a method comparison study. AJR Am J Roentgenol 197:468–473

    Article  Google Scholar 

Download references

Acknowledgments

The study was funded by the statutory budgets of the medical universities of Gdansk and Warsaw. Dr. Pawel J. Winklewski was supported by the Polish National Science Center grant 2017/01/X/NZ5/00909.

Conflicts of Interest

The authors declare no conflicts of interest in relation to this article.

Ethical Approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The experimental protocol of the study was approved by the Ethics Committee of the Medical University in Gdansk, Poland.

Informed Consent

Written informed consent was obtained from all individual participants included in the study.

Author information

Authors and Affiliations

  1. Second Department of Radiology, Faculty of Health Sciences, Medical University of Gdansk, Gdansk, Poland

    Arkadiusz Szarmach, Piotr Łyźniak, Edyta Szurowska & Paweł J. Winklewski

  2. Department of Human Physiology, Faculty of Health Sciences, Medical University of Gdansk, Gdansk, Poland

    Marta A. Małkiewicz & Paweł J. Winklewski

  3. Department of Psychiatry, Faculty of Medicine, Medical University of Gdansk, Gdansk, Poland

    Marta A. Małkiewicz

  4. Department of Quality of Life Research, Faculty of Health Sciences, Medical University of Gdansk, Gdansk, Poland

    Agata Zdun-Ryżewska

  5. Department of Cardiovascular Surgery, Faculty of Medicine, Medical University of Gdansk, Gdansk, Poland

    Grzegorz Halena

  6. Department of Immunopathology of Infectious and Parasitic Diseases, Warsaw Medical University, Warsaw, Poland

    Marek Radkowski

  7. Department of Neurosurgery, Faculty of Medicine, Medical University of Gdansk, Gdansk, Poland

    Jarosław Dzierżanowski

  8. Department of Neurology, Faculty of Medicine, Medical University of Gdansk, Gdansk, Poland

    Kamil Chwojnicki

  9. Faculty of Electrical Engineering, Gdynia Maritime University, Gdynia, Poland

    Adam Muc

  10. Department of Diagnostics Imaging, Ceynowa Hospital, Wejherowo, Poland

    Tomasz Damaszko

  11. First Department of Radiology, Faculty of Medicine, Medical University of Gdansk, Gdansk, Poland

    Maciej Piskunowicz

  12. Department of Laboratory Diagnostics and Clinical Immunology of Developmental Age, Warsaw Medical University, Warsaw, Poland

    Urszula Demkow

  13. Department of Clinical Anatomy and Physiology, Faculty of Health Sciences, Pomeranian University of Slupsk, Slupsk, Poland

    Paweł J. Winklewski

Authors
  1. Arkadiusz Szarmach
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marta A. Małkiewicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Agata Zdun-Ryżewska
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Grzegorz Halena
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Marek Radkowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jarosław Dzierżanowski
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kamil Chwojnicki
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Adam Muc
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Tomasz Damaszko
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Piotr Łyźniak
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Maciej Piskunowicz
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Edyta Szurowska
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Urszula Demkow
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Paweł J. Winklewski
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Urszula Demkow .

Editor information

Editors and Affiliations

  1. Opole Medical School, Opole, Poland

    Mieczyslaw Pokorski

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Szarmach, A. et al. (2019). Relative Cerebral Blood Transit Time Decline and Neurological Improvement in Patients After Internal Carotid Artery Stenting. In: Pokorski, M. (eds) Advances in Biomedicine. Advances in Experimental Medicine and Biology(), vol 1176. Springer, Cham. https://doi.org/10.1007/5584_2019_378

Download citation

Publish with us

Policies and ethics

Search

Navigation