Skip to main content
NCBI home page
Journal of Neurology, Neurosurgery, and Psychiatry logoLink to Journal of Neurology, Neurosurgery, and Psychiatry
. 2001 Mar;70(3):333–339. doi: 10.1136/jnnp.70.3.333

Clinical features associated with internal carotid artery occlusion do not correlate with MRA cerebropetal flow measurements

K J van Everdingen 1, L Kappelle 1, C Klijn 1, W Mali 1, J van der Grond 1
PMCID: PMC1737247  PMID: 11181854

Abstract

OBJECTIVES—The aetiology of clinical symptoms in patients with severe internal carotid artery (ICA) lesions may be thromboembolic or haemodynamic. The purpose was to assess whether changes in cerebropetal blood flow caused by an ICA occlusion have an effect on clinical symptoms and cerebral metabolism.
METHODS—Forty three patients with an ICA occlusion who had hemispheric ischaemia (transient ischaemic attack or stroke), retinal ischaemia, or without symptoms, and 34 patients without significant ICA lesions with either hemispheric ischaemia or no symptoms were studied. Magnetic resonance angiography (MRA) was used to investigate total cerebropetal flow (flow in the ICAs plus basilar artery) and the flow in the middle cerebral arteries. Cerebral metabolic changes in the flow territory of the middle cerebral artery were determined with proton MR spectroscopy.
RESULTS—Low total cerebropetal flow (r=−0.15, p<0.05) and low middle cerebral artery flow (r=−0.31, p<0.001) were found in patients with an ICA occlusion, but did not correlate with the clinical syndrome. By contrast, patients with prior symptoms of hemispheric ischaemia had decreased cerebral N-acetylaspartate/choline ratios (r=−0.35, p<0.001). However, the presence of an ICA occlusion (and subsequent low flow) did not correlate with low N-acetylaspartate/choline ratios.
CONCLUSION—Neurological deficit caused by (transient) hemispheric ischaemia is associated with low N-acetylaspartate/choline ratios, whereas prior clinical features are not associated with low cerebropetal blood flow, as measured with MR angiography. As a result, differences in cerebropetal flow cannot explain why patients with similar carotid artery disease experience different neurological features.



Full Text

The Full Text of this article is available as a PDF (137.6 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bakker C. J., Hartkamp M. J., Mali W. P. Measuring blood flow by nontriggered 2D phase-contrast MR angiography. Magn Reson Imaging. 1996;14(6):609–614. doi: 10.1016/0730-725x(96)00092-6. [DOI] [PubMed] [Google Scholar]
  2. Bakker C. J., Hoogeveen R. M., Viergever M. A. Construction of a protocol for measuring blood flow by two-dimensional phase-contrast MRA. J Magn Reson Imaging. 1999 Jan;9(1):119–127. doi: 10.1002/(sici)1522-2586(199901)9:1<119::aid-jmri16>3.0.co;2-f. [DOI] [PubMed] [Google Scholar]
  3. Bakker C. J., Kouwenhoven M., Hartkamp M. J., Hoogeveen R. M., Mali W. P. Accuracy and precision of time-averaged flow as measured by nontriggered 2D phase-contrast MR angiography, a phantom evaluation. Magn Reson Imaging. 1995;13(7):959–965. doi: 10.1016/0730-725x(95)02005-e. [DOI] [PubMed] [Google Scholar]
  4. Barnett H. J., Peerless S. J., Kaufmann J. C. "Stump" on internal carotid artery--a source for further cerebral embolic ischemia. Stroke. 1978 Sep-Oct;9(5):448–456. doi: 10.1161/01.str.9.5.448. [DOI] [PubMed] [Google Scholar]
  5. Baumgartner R. W., Mattle H. P., Schroth G. Transcranial colour-coded duplex sonography of cerebral arteriovenous malformations. Neuroradiology. 1996 Nov;38(8):734–737. doi: 10.1007/s002340050338. [DOI] [PubMed] [Google Scholar]
  6. Bladin C. F., Chambers B. R. Frequency and pathogenesis of hemodynamic stroke. Stroke. 1994 Nov;25(11):2179–2182. doi: 10.1161/01.str.25.11.2179. [DOI] [PubMed] [Google Scholar]
  7. Blankensteijn J. D., van der Grond J., Mali W. P., Eikelboom B. C. Flow volume changes in the major cerebral arteries before and after carotid endarterectomy: an MR angiography study. Eur J Vasc Endovasc Surg. 1997 Dec;14(6):446–450. doi: 10.1016/s1078-5884(97)80122-0. [DOI] [PubMed] [Google Scholar]
  8. Bogousslavsky J., Regli F. Borderzone infarctions distal to internal carotid artery occlusion: prognostic implications. Ann Neurol. 1986 Sep;20(3):346–350. doi: 10.1002/ana.410200312. [DOI] [PubMed] [Google Scholar]
  9. Bogousslavsky J., Regli F. Unilateral watershed cerebral infarcts. Neurology. 1986 Mar;36(3):373–377. doi: 10.1212/wnl.36.3.373. [DOI] [PubMed] [Google Scholar]
  10. Bottomley P. A. Spatial localization in NMR spectroscopy in vivo. Ann N Y Acad Sci. 1987;508:333–348. doi: 10.1111/j.1749-6632.1987.tb32915.x. [DOI] [PubMed] [Google Scholar]
  11. Buijs P. C., Krabbe-Hartkamp M. J., Bakker C. J., de Lange E. E., Ramos L. M., Breteler M. M., Mali W. P. Effect of age on cerebral blood flow: measurement with ungated two-dimensional phase-contrast MR angiography in 250 adults. Radiology. 1998 Dec;209(3):667–674. doi: 10.1148/radiology.209.3.9844657. [DOI] [PubMed] [Google Scholar]
  12. Davis W. L., Turski P. A., Gorbatenko K. G., Weber D. Correlation of cine MR velocity measurements in the internal carotid artery with collateral flow in the circle of Willis: preliminary study. J Magn Reson Imaging. 1993 Jul-Aug;3(4):603–609. doi: 10.1002/jmri.1880030409. [DOI] [PubMed] [Google Scholar]
  13. Derdeyn C. P., Videen T. O., Fritsch S. M., Carpenter D. A., Grubb R. L., Jr, Powers W. J. Compensatory mechanisms for chronic cerebral hypoperfusion in patients with carotid occlusion. Stroke. 1999 May;30(5):1019–1024. doi: 10.1161/01.str.30.5.1019. [DOI] [PubMed] [Google Scholar]
  14. Derdeyn C. P., Yundt K. D., Videen T. O., Carpenter D. A., Grubb R. L., Jr, Powers W. J. Increased oxygen extraction fraction is associated with prior ischemic events in patients with carotid occlusion. Stroke. 1998 Apr;29(4):754–758. doi: 10.1161/01.str.29.4.754. [DOI] [PubMed] [Google Scholar]
  15. Elgersma O. E., van Leersum M., Buijs P. C., van Leeuwen M. S., van de Schouw Y. T., Eikelboom B. C., van der Graaf Y. Changes over time in optimal duplex threshold for the identification of patients eligible for carotid endarterectomy. Stroke. 1998 Nov;29(11):2352–2356. doi: 10.1161/01.str.29.11.2352. [DOI] [PubMed] [Google Scholar]
  16. Evans A. J., Iwai F., Grist T. A., Sostman H. D., Hedlund L. W., Spritzer C. E., Negro-Vilar R., Beam C. A., Pelc N. J. Magnetic resonance imaging of blood flow with a phase subtraction technique. In vitro and in vivo validation. Invest Radiol. 1993 Feb;28(2):109–115. doi: 10.1097/00004424-199302000-00004. [DOI] [PubMed] [Google Scholar]
  17. Felber S. R., Aichner F. T., Sauter R., Gerstenbrand F. Combined magnetic resonance imaging and proton magnetic resonance spectroscopy of patients with acute stroke. Stroke. 1992 Aug;23(8):1106–1110. doi: 10.1161/01.str.23.8.1106. [DOI] [PubMed] [Google Scholar]
  18. Finklestein S., Kleinman G. M., Cuneo R., Baringer J. R. Delayed stroke following carotid occlusion. Neurology. 1980 Jan;30(1):84–88. doi: 10.1212/wnl.30.1.84. [DOI] [PubMed] [Google Scholar]
  19. Fürst G., Steinmetz H., Fischer H., Skutta B., Sitzer M., Aulich A., Kahn T., Mödder U. Selective MR angiography and intracranial collateral blood flow. J Comput Assist Tomogr. 1993 Mar-Apr;17(2):178–183. doi: 10.1097/00004728-199303000-00004. [DOI] [PubMed] [Google Scholar]
  20. Georgiadis D., Grosset D. G., Lees K. R. Transhemispheric passage of microemboli in patients with unilateral internal carotid artery occlusion. Stroke. 1993 Nov;24(11):1664–1666. doi: 10.1161/01.str.24.11.1664. [DOI] [PubMed] [Google Scholar]
  21. Gibbs J. M., Wise R. J., Leenders K. L., Jones T. Evaluation of cerebral perfusion reserve in patients with carotid-artery occlusion. Lancet. 1984 Feb 11;1(8372):310–314. doi: 10.1016/s0140-6736(84)90361-1. [DOI] [PubMed] [Google Scholar]
  22. Gideon P., Sperling B., Arlien-Søborg P., Olsen T. S., Henriksen O. Long-term follow-up of cerebral infarction patients with proton magnetic resonance spectroscopy. Stroke. 1994 May;25(5):967–973. doi: 10.1161/01.str.25.5.967. [DOI] [PubMed] [Google Scholar]
  23. Graham G. D., Kalvach P., Blamire A. M., Brass L. M., Fayad P. B., Prichard J. W. Clinical correlates of proton magnetic resonance spectroscopy findings after acute cerebral infarction. Stroke. 1995 Feb;26(2):225–229. doi: 10.1161/01.str.26.2.225. [DOI] [PubMed] [Google Scholar]
  24. Harrison M. J., Marshall J. The variable clinical and CT findings after carotid occlusion: the role of collateral blood supply. J Neurol Neurosurg Psychiatry. 1988 Feb;51(2):269–272. doi: 10.1136/jnnp.51.2.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hedera P., Bujdáková J., Traubner P. Effect of collateral flow patterns on outcome of carotid occlusion. Eur Neurol. 1995;35(4):212–216. doi: 10.1159/000117130. [DOI] [PubMed] [Google Scholar]
  26. Klijn C. J., Kappelle L. J., Tulleken C. A., van Gijn J. Symptomatic carotid artery occlusion. A reappraisal of hemodynamic factors. Stroke. 1997 Oct;28(10):2084–2093. doi: 10.1161/01.str.28.10.2084. [DOI] [PubMed] [Google Scholar]
  27. Kuzniecky R., Hetherington H., Pan J., Hugg J., Palmer C., Gilliam F., Faught E., Morawetz R. Proton spectroscopic imaging at 4.1 tesla in patients with malformations of cortical development and epilepsy. Neurology. 1997 Apr;48(4):1018–1024. doi: 10.1212/wnl.48.4.1018. [DOI] [PubMed] [Google Scholar]
  28. Leblanc R., Yamamoto Y. L., Tyler J. L., Hakim A. Hemodynamic and metabolic effects of extracranial carotid disease. Can J Neurol Sci. 1989 Feb;16(1):51–57. doi: 10.1017/s031716710002850x. [DOI] [PubMed] [Google Scholar]
  29. Levine R. L., Turski P. A., Holmes K. A., Grist T. M. Comparison of magnetic resonance volume flow rates, angiography, and carotid Dopplers. Preliminary results. Stroke. 1994 Feb;25(2):413–417. doi: 10.1161/01.str.25.2.413. [DOI] [PubMed] [Google Scholar]
  30. Mathews V. P., Barker P. B., Blackband S. J., Chatham J. C., Bryan R. N. Cerebral metabolites in patients with acute and subacute strokes: concentrations determined by quantitative proton MR spectroscopy. AJR Am J Roentgenol. 1995 Sep;165(3):633–638. doi: 10.2214/ajr.165.3.7645484. [DOI] [PubMed] [Google Scholar]
  31. Miller B. L. A review of chemical issues in 1H NMR spectroscopy: N-acetyl-L-aspartate, creatine and choline. NMR Biomed. 1991 Apr;4(2):47–52. doi: 10.1002/nbm.1940040203. [DOI] [PubMed] [Google Scholar]
  32. Miralles M., Dolz J. L., Cotillas J., Aldoma J., Santiso M. A., Giménez A., Capdevila A., Cairols M. A. The role of the circle of Willis in carotid occlusion: assessment with phase contrast MR angiography and transcranial duplex. Eur J Vasc Endovasc Surg. 1995 Nov;10(4):424–430. doi: 10.1016/s1078-5884(05)80164-9. [DOI] [PubMed] [Google Scholar]
  33. Moody D. M., Bell M. A., Challa V. R. Features of the cerebral vascular pattern that predict vulnerability to perfusion or oxygenation deficiency: an anatomic study. AJNR Am J Neuroradiol. 1990 May;11(3):431–439. [PMC free article] [PubMed] [Google Scholar]
  34. Mull M., Schwarz M., Thron A. Cerebral hemispheric low-flow infarcts in arterial occlusive disease. Lesion patterns and angiomorphological conditions. Stroke. 1997 Jan;28(1):118–123. doi: 10.1161/01.str.28.1.118. [DOI] [PubMed] [Google Scholar]
  35. Müller M., Hermes M., Brückmann H., Schimrigk K. Transcranial Doppler ultrasound in the evaluation of collateral blood flow in patients with internal carotid artery occlusion: correlation with cerebral angiography. AJNR Am J Neuroradiol. 1995 Jan;16(1):195–202. [PMC free article] [PubMed] [Google Scholar]
  36. Norris J. W., Krajewski A., Bornstein N. M. The clinical role of the cerebral collateral circulation in carotid occlusion. J Vasc Surg. 1990 Aug;12(2):113–118. doi: 10.1067/mva.1990.21479. [DOI] [PubMed] [Google Scholar]
  37. Pelc L. R., Pelc N. J., Rayhill S. C., Castro L. J., Glover G. H., Herfkens R. J., Miller D. C., Jeffrey R. B. Arterial and venous blood flow: noninvasive quantitation with MR imaging. Radiology. 1992 Dec;185(3):809–812. doi: 10.1148/radiology.185.3.1438767. [DOI] [PubMed] [Google Scholar]
  38. Powers W. J. Cerebral hemodynamics in ischemic cerebrovascular disease. Ann Neurol. 1991 Mar;29(3):231–240. doi: 10.1002/ana.410290302. [DOI] [PubMed] [Google Scholar]
  39. Powers W. J., Press G. A., Grubb R. L., Jr, Gado M., Raichle M. E. The effect of hemodynamically significant carotid artery disease on the hemodynamic status of the cerebral circulation. Ann Intern Med. 1987 Jan;106(1):27–34. doi: 10.7326/0003-4819-106-1-27. [DOI] [PubMed] [Google Scholar]
  40. Schomer D. F., Marks M. P., Steinberg G. K., Johnstone I. M., Boothroyd D. B., Ross M. R., Pelc N. J., Enzmann D. R. The anatomy of the posterior communicating artery as a risk factor for ischemic cerebral infarction. N Engl J Med. 1994 Jun 2;330(22):1565–1570. doi: 10.1056/NEJM199406023302204. [DOI] [PubMed] [Google Scholar]
  41. Scremin O. U., Jenden D. J. Focal ischemia enhances choline output and decreases acetylcholine output from rat cerebral cortex. Stroke. 1989 Jan;20(1):92–95. doi: 10.1161/01.str.20.1.92. [DOI] [PubMed] [Google Scholar]
  42. Spritzer C. E., Pelc N. J., Lee J. N., Evans A. J., Sostman H. D., Riederer S. J. Rapid MR imaging of blood flow with a phase-sensitive, limited-flip-angle, gradient recalled pulse sequence: preliminary experience. Radiology. 1990 Jul;176(1):255–262. doi: 10.1148/radiology.176.1.2353099. [DOI] [PubMed] [Google Scholar]
  43. Stevens H., Jansen H. M., De Reuck J., Lemmerling M., Strijckmans K., Goethals P., Lemahieu I., De Jong B. M., Willemsen A. T., Korf J. 55Co-PET in stroke: relation to bloodflow, oxygen metabolism and gadolinium-MRI. Acta Neurol Belg. 1997 Sep;97(3):172–177. [PubMed] [Google Scholar]
  44. TALLAN H. H. Studies on the distribution of N-acetyl-L-aspartic acid in brain. J Biol Chem. 1957 Jan;224(1):41–45. [PubMed] [Google Scholar]
  45. Tang C., Blatter D. D., Parker D. L. Accuracy of phase-contrast flow measurements in the presence of partial-volume effects. J Magn Reson Imaging. 1993 Mar-Apr;3(2):377–385. doi: 10.1002/jmri.1880030213. [DOI] [PubMed] [Google Scholar]
  46. Tarnawski M., Padayachee S., West D. J., Graves M. J., Ayton V. T., Taylor M. G., Smith M. A. The measurement of time-averaged flow by magnetic resonance imaging using continuous acquisition in the carotid arteries and its comparison with Doppler ultrasound. Clin Phys Physiol Meas. 1990 Feb;11(1):27–36. doi: 10.1088/0143-0815/11/1/002. [DOI] [PubMed] [Google Scholar]
  47. Urenjak J., Williams S. R., Gadian D. G., Noble M. Proton nuclear magnetic resonance spectroscopy unambiguously identifies different neural cell types. J Neurosci. 1993 Mar;13(3):981–989. doi: 10.1523/JNEUROSCI.13-03-00981.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Vanninen R. L., Manninen H. I., Partanen P. L., Vainio P. A., Soimakallio S. Carotid artery stenosis: clinical efficacy of MR phase-contrast flow quantification as an adjunct to MR angiography. Radiology. 1995 Feb;194(2):459–467. doi: 10.1148/radiology.194.2.7824727. [DOI] [PubMed] [Google Scholar]
  49. Vanninen R., Koivisto K., Tulla H., Manninen H., Partanen K. Hemodynamic effects of carotid endarterectomy by magnetic resonance flow quantification. Stroke. 1995 Jan;26(1):84–89. doi: 10.1161/01.str.26.1.84. [DOI] [PubMed] [Google Scholar]
  50. Widder B., Kleiser B., Krapf H. Course of cerebrovascular reactivity in patients with carotid artery occlusions. Stroke. 1994 Oct;25(10):1963–1967. doi: 10.1161/01.str.25.10.1963. [DOI] [PubMed] [Google Scholar]
  51. Yamauchi H., Fukuyama H., Kimura J., Konishi J., Kameyama M. Hemodynamics in internal carotid artery occlusion examined by positron emission tomography. Stroke. 1990 Oct;21(10):1400–1406. doi: 10.1161/01.str.21.10.1400. [DOI] [PubMed] [Google Scholar]
  52. van Everdingen K. J., Klijn C. J., Kappelle L. J., Mali W. P., van der Grond J. MRA flow quantification in patients with a symptomatic internal carotid artery occlusion. The Dutch EC-IC Bypass Study Group. Stroke. 1997 Aug;28(8):1595–1600. doi: 10.1161/01.str.28.8.1595. [DOI] [PubMed] [Google Scholar]
  53. van Everdingen K. J., Visser G. H., Klijn C. J., Kappelle L. J., van der Grond J. Role of collateral flow on cerebral hemodynamics in patients with unilateral internal carotid artery occlusion. Ann Neurol. 1998 Aug;44(2):167–176. doi: 10.1002/ana.410440206. [DOI] [PubMed] [Google Scholar]
  54. van Everdingen K. J., van der Grond J., Kappelle L. J. Overestimation of a stenosis in the internal carotid artery by duplex sonography caused by an increase in volume flow. J Vasc Surg. 1998 Mar;27(3):479–485. doi: 10.1016/s0741-5214(98)99999-2. [DOI] [PubMed] [Google Scholar]
  55. van der Grond J., Eikelboom B. C., Mali W. P. Flow-related anaerobic metabolic changes in patients with severe stenosis of the internal carotid artery. Stroke. 1996 Nov;27(11):2026–2032. doi: 10.1161/01.str.27.11.2026. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Neurology, Neurosurgery, and Psychiatry are provided here courtesy of BMJ Publishing Group

RESOURCES