Development of cerebral microbleeds in patients with cerebral hyperperfusion following carotid endarterectomy and its relation to postoperative cognitive decline

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  • 1 Department of Neurosurgery and
  • 2 Cyclotron Research Center, Iwate Medical University School of Medicine, Morioka, Japan
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OBJECTIVE

A primary cause of cognitive decline after carotid endarterectomy (CEA) is cerebral injury due to cerebral hyperperfusion. However, the mechanisms of how cerebral hyperperfusion induces cerebral cortex and white matter injury are not known. The presence of cerebral microbleeds (CMBs) on susceptibility-weighted imaging (SWI) is independently associated with a decline in global cognitive function. The purpose of this prospective observational study was to determine whether cerebral hyperperfusion following CEA leads to the development of CMBs and if postoperative cognitive decline is related to these developed CMBs.

METHODS

During the 27-month study period, patients who underwent CEA for ipsilateral internal carotid artery stenosis (≥ 70%) also underwent SWI and neuropsychological testing before and 2 months after surgery, as well as quantitative brain perfusion SPECT prior to and immediately after surgery.

RESULTS

According to quantitative brain perfusion SPECT and SWI before and after surgery, 12 (16%) and 7 (9%) of 75 patients exhibited postoperative cerebral hyperperfusion and increased CMBs in the cerebral hemisphere ipsilateral to surgery, respectively. Cerebral hyperperfusion was associated with an increase in CMBs after surgery (logistic regression analysis, 95% CI 5.08–31.25, p < 0.0001). According to neuropsychological assessments before and after surgery, 10 patients (13%) showed postoperative cognitive decline. Increased CMBs were associated with cognitive decline after surgery (logistic regression analysis, 95% CI 6.80–66.67, p < 0.0001). Among the patients with cerebral hyperperfusion after surgery, the incidence of postoperative cognitive decline was higher in those with increased CMBs (100%) than in those without (20%; p = 0.0101).

CONCLUSIONS

Cerebral hyperperfusion following CEA leads to the development of CMBs, and postoperative cognitive decline is related to these developed CMBs.

ABBREVIATIONS CBF = cerebral blood flow; CEA = carotid endarterectomy; CMB = cerebral microbleed; ICA = internal carotid artery; MQ = memory quotient; PIQ = performance IQ; RCFT = Rey-Osterrieth Complex Figure Test; ROI = region of interest; SWI = susceptibility-weighted imaging; VIQ = verbal IQ; WAIS-R = Wechsler Adult Intelligence Scale–Revised; WMS = Wechsler Memory Scale.

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Contributor Notes

Correspondence Kuniaki Ogasawara: Iwate Medical University, Morioka, Japan. kuogasa@iwate-med.ac.jp.

INCLUDE WHEN CITING Published online January 1, 2021; DOI: 10.3171/2020.7.JNS202353.

Disclosures Dr. Ogasawara receives consigned research funds from Nihon Medi-Physics Co., Ltd.

  • 1

    Piepgras DG, Morgan MK, Sundt TM Jr, Intracerebral hemorrhage after carotid endarterectomy. J Neurosurg. 1988;68(4):532536.

  • 2

    Sundt TM Jr, Sharbrough FW, Piepgras DG, Correlation of cerebral blood flow and electroencephalographic changes during carotid endarterectomy: with results of surgery and hemodynamics of cerebral ischemia. Mayo Clin Proc. 1981;56(9):533543.

    • Search Google Scholar
    • Export Citation
  • 3

    Oshida S, Ogasawara K, Saura H, Does preoperative measurement of cerebral blood flow with acetazolamide challenge in addition to preoperative measurement of cerebral blood flow at the resting state increase the predictive accuracy of development of cerebral hyperperfusion after carotid endarterectomy? Results from 500 cases with brain perfusion single-photon emission computed tomography study. Neurol Med Chir (Tokyo). 2015;55(2):141148.

    • Search Google Scholar
    • Export Citation
  • 4

    Bernstein M, Fleming JF, Deck JH. Cerebral hyperperfusion after carotid endarterectomy: a cause of cerebral hemorrhage. Neurosurgery. 1984;15(1):5056.

    • Search Google Scholar
    • Export Citation
  • 5

    Ogasawara K, Sakai N, Kuroiwa T, Intracranial hemorrhage associated with cerebral hyperperfusion syndrome following carotid endarterectomy and carotid artery stenting: retrospective review of 4494 patients. J Neurosurg. 2007;107(6):11301136.

    • Search Google Scholar
    • Export Citation
  • 6

    Yoshida K, Ogasawara K, Saura H, Post-carotid endarterectomy changes in cerebral glucose metabolism on 18F-fluorodeoxyglucose positron emission tomography associated with postoperative improvement or impairment in cognitive function. J Neurosurg. 2015;123(6):15461554.

    • Search Google Scholar
    • Export Citation
  • 7

    Chida K, Ogasawara K, Suga Y, Postoperative cortical neural loss associated with cerebral hyperperfusion and cognitive impairment after carotid endarterectomy: 123I-iomazenil SPECT study. Stroke. 2009;40(2):448453.

    • Search Google Scholar
    • Export Citation
  • 8

    Nanba T, Ogasawara K, Nishimoto H, Postoperative cerebral white matter damage associated with cerebral hyperperfusion and cognitive impairment after carotid endarterectomy: a diffusion tensor magnetic resonance imaging study. Cerebrovasc Dis. 2012;34(5-6):358367.

    • Search Google Scholar
    • Export Citation
  • 9

    Gustavsson AM, Stomrud E, Abul-Kasim K, Cerebral microbleeds and white matter hyperintensities in cognitively healthy elderly: a cross-sectional cohort study evaluating the effect of arterial stiffness. Cerebrovasc Dis Extra. 2015;5(2):4151.

    • Search Google Scholar
    • Export Citation
  • 10

    Mackey J, Wing JJ, Norato G, High rate of microbleed formation following primary intracerebral hemorrhage. Int J Stroke. 2015;10(8):11871191.

    • Search Google Scholar
    • Export Citation
  • 11

    Wilson D, Charidimou A, Ambler G, Recurrent stroke risk and cerebral microbleed burden in ischemic stroke and TIA: a meta-analysis. Neurology. 2016;87(14):15011510.

    • Search Google Scholar
    • Export Citation
  • 12

    Werring DJ, Frazer DW, Coward LJ, Cognitive dysfunction in patients with cerebral microbleeds on T2*-weighted gradient-echo MRI. Brain. 2004;127(Pt 10):22652275.

    • Search Google Scholar
    • Export Citation
  • 13

    Fazekas F, Kleinert R, Roob G, Histopathologic analysis of foci of signal loss on gradient-echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: evidence of microangiopathy-related microbleeds. AJNR Am J Neuroradiol. 1999;20(4):637642.

    • Search Google Scholar
    • Export Citation
  • 14

    Akoudad S, Wolters FJ, Viswanathan A, Association of cerebral microbleeds with cognitive decline and dementia. JAMA Neurol. 2016;73(8):934943.

    • Search Google Scholar
    • Export Citation
  • 15

    Yamashiro K, Tanaka R, Okuma Y, Cerebral microbleeds are associated with worse cognitive function in the nondemented elderly with small vessel disease. Cerebrovasc Dis Extra. 2014;4(3):212220.

    • Search Google Scholar
    • Export Citation
  • 16

    Kakumoto K, Matsumoto S, Nakahara I, Rapid formation of cerebral microbleeds after carotid artery stenting. Cerebrovasc Dis Extra. 2012;2(1):916.

    • Search Google Scholar
    • Export Citation
  • 17

    Gregoire SM, Chaudhary UJ, Brown MM, The Microbleed Anatomical Rating Scale (MARS): reliability of a tool to map brain microbleeds. Neurology. 2009;73(21):17591766.

    • Search Google Scholar
    • Export Citation
  • 18

    Banerjee G, Kim HJ, Fox Z, MRI-visible perivascular space location is associated with Alzheimer’s disease independently of amyloid burden. Brain. 2017;140(4):11071116.

    • Search Google Scholar
    • Export Citation
  • 19

    Ogasawara K, Ito H, Sasoh M, Quantitative measurement of regional cerebrovascular reactivity to acetazolamide using 123I-N-isopropyl-p-iodoamphetamine autoradiography with SPECT: validation study using H2 15O with PET. J Nucl Med. 2003;44(4):520525.

    • Search Google Scholar
    • Export Citation
  • 20

    Ashburner J. SPM: a history. Neuroimage. 2012;62(2):791800.

  • 21

    Takeuchi R, Matsuda H, Yoshioka K, Yonekura Y. Cerebral blood flow SPET in transient global amnesia with automated ROI analysis by 3DSRT. Eur J Nucl Med Mol Imaging. 2004;31(4):578589.

    • Search Google Scholar
    • Export Citation
  • 22

    Shinagawa F, Kobayashi S, Fujita K. Japanese Wechsler Adult Intelligence Scale–Revised. Nihon Bunka Kagakusha; 1990.

  • 23

    Koyama M. Japanese Wechsler Memory Scale. In: Koyama M, ed. Clinical Psychology of Brain Damage. Gakuen Sha; 1985:4854.

  • 24

    Lezak MD. Neuropsychological Assessment. 3rd ed. Oxford University Press; 1995.

  • 25

    Yoshida K, Ogasawara K, Kobayashi M, Improvement and impairment in cognitive function after carotid endarterectomy: comparison of objective and subjective assessments. Neurol Med Chir (Tokyo). 2012;52(3):154160.

    • Search Google Scholar
    • Export Citation
  • 26

    Rutgers DR, Blankensteijn JD, van der Grond J. Preoperative MRA flow quantification in CEA patients: flow differences between patients who develop cerebral ischemia and patients who do not develop cerebral ischemia during cross-clamping of the carotid artery. Stroke. 2000;31(12):30213028.

    • Search Google Scholar
    • Export Citation
  • 27

    Jolink WMT, Lindenholz A, van Etten ES, Contrast leakage distant from the hematoma in patients with spontaneous ICH: a 7 T MRI study. J Cereb Blood Flow Metab. 2020;40(5):10021011.

    • Search Google Scholar
    • Export Citation
  • 28

    Mansour A, Rashad S, Niizuma K, A novel model of cerebral hyperperfusion with blood-brain barrier breakdown, white matter injury, and cognitive dysfunction. J Neurosurg. 2020;133(5):14601472.

    • Search Google Scholar
    • Export Citation
  • 29

    De Rango P, Caso V, Leys D, The role of carotid artery stenting and carotid endarterectomy in cognitive performance: a systematic review. Stroke. 2008;39(11):31163127.

    • Search Google Scholar
    • Export Citation
  • 30

    Lunn S, Crawley F, Harrison MJ, Impact of carotid endarterectomy upon cognitive functioning. A systematic review of the literature. Cerebrovasc Dis. 1999;9(2):7481.

    • Search Google Scholar
    • Export Citation
  • 31

    Hirooka R, Ogasawara K, Sasaki M, Magnetic resonance imaging in patients with cerebral hyperperfusion and cognitive impairment after carotid endarterectomy. J Neurosurg. 2008;108(6):11781183.

    • Search Google Scholar
    • Export Citation
  • 32

    Tanaka A, Ueno Y, Nakayama Y, Small chronic hemorrhages and ischemic lesions in association with spontaneous intracerebral hematomas. Stroke. 1999;30(8):16371642.

    • Search Google Scholar
    • Export Citation
  • 33

    Akoudad S, de Groot M, Koudstaal PJ, Cerebral microbleeds are related to loss of white matter structural integrity. Neurology. 2013;81(22):19301937.

    • Search Google Scholar
    • Export Citation
  • 34

    Zimmermann A, Knappich C, Tsantilas P, Different perioperative antiplatelet therapies for patients treated with carotid endarterectomy in routine practice. J Vasc Surg. 2018;68(6):17531763.

    • Search Google Scholar
    • Export Citation
  • 35

    Ogasawara K, Inoue T, Kobayashi M, Pretreatment with the free radical scavenger edaravone prevents cerebral hyperperfusion after carotid endarterectomy. Neurosurgery. 2004;55(5):10601067.

    • Search Google Scholar
    • Export Citation
  • 36

    Kudo K, Liu T, Murakami T, Oxygen extraction fraction measurement using quantitative susceptibility mapping: comparison with positron emission tomography. J Cereb Blood Flow Metab. 2016;36(8):14241433.

    • Search Google Scholar
    • Export Citation

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