Cent Eur Neurosurg 2007; 68(2): 59-66
DOI: 10.1055/s-2007-980173
Original Article

© Georg Thieme Verlag KG Stuttgart · New York

Hypercapnia Impact on Vascular and Neuronal Reactivity in Patients Before and After Carotid Endarterectomy

Hyperkapnie Einfluß auf Vaskuläre und Neuronale Reaktivität bei Patienten vor und nach KarotisendarterektomieS. Ostrý 1 , L. Stejskal 1 , F. Kramár 1 , D. Netuka 1 , M. Mohapl 1 , V. Beneš 1
  • 1Department of Neurosurgery, Charles University, Prague, Czech Republic
Further Information

Publication History

Publication Date:
06 July 2007 (online)

Abstract

Hypothesis: Regional cerebral blood flow (rCBF) and vascular reactivity strongly affect neuronal function. The restoration of blood flow values in the cerebral vascular system may be another benefit of carotid endarterectomy (CEA) in a specific group of patients. Animal experiments in dogs have provided evidence of neuronal reactivity depending on rCBF and vascular reactivity. However, as yet, there are no reports on neuronal reactivity changes related to altered perfusion parameters in humans.

Material and Methods: The cohort under study consisted of 41 patients after transient ischaemic attack (TIA) or reversible ischaemic neurological deficit (RIND) whose neurological findings were normal (group A) and 17 patients after minor stroke with a mild degree of hemiparesis or hemihypesthesia (mRS≤2) (group B). All patients were examined 0-2 days before CEA, on postoperative days 3-7 and at 3 months after CEA. The tests included median nerve somatosensory evoked potentials (SEPs) and transcranial Doppler (TCD) at rest, during hypercapnia (et-CO2=7.0-7.5 kPa) and at rest after hypercapnia.

Results: Group A was found to have a significant increase in Vsys, Vmean and PI in response to hypercapnia in all periods (i.e., 0-2 days before CEA, on postoperative days 3-7 and at 3 months after CEA). N20/P25 amplitude decreased in response to hypercapnia before and early after CEA. Changes in other SEP parametres before and after hypercapnia were non-significant. Group B showed significant differences resulting from hypercapnia before and after CEA only in vasoreactivity (Vsys, Vmean, PI).

Conclusion: In the analysed group of patients high-grade carotid stenosis caused no haemodynamic impairment. Moreover, no evidence was found of artificially increased rCBF being accompanied by an equally significant change in somatosensory evoked scalp response.

Zusammenfassung

Hypothese: Die regionale cerebrale Blutzirkulation (cBZ) und die vaskuläre Reaktivität haben großen Einflussß auf die neuronale Funktion. Die Wiederherstellung des Blutflusses im cerebralen Gefäßsystem ist vermutlich ein weiterer Benefit der Karotisendarterektomie in einer selektiven Gruppe von Patienten. Tierexperimentelle Studien an Hunden lieferten den Beweis, dass die neuronale Aktivität vom cBZ und der vaskulären Reaktivität abhängig ist. Bis dato gibt es jedoch keine Berichte über Veränderungen der neuronalen Reaktivität in Zusammenhang mit der erhöhten Perfusion am Menschen.

Material und Methoden: In diese Studie wurden 41 Patienten nach einer transienten ischämischen Attacke oder prolongiertem reversiblem ischämischen Defizit (PRIND), deren neurologischer Status unauffällig war (Gruppe A), und 17 Patienten nach einem leichten Schlaganfall mit einer leichtgradigen Hemiparese oder Hemihypästhesie (mRS≤2) (Gruppe B), eingeschlossen. Alle Patienten wurden 0-2 Tage vor der CEA, am 3.-7. post-operativen Tag und 3 Monate nach CEA untersucht. Zu den Untersuchungsmethoden zählten somatosensibel evozierte Potentiale (SEPs) am N. medianus, eine transkranielle Doppleruntersuchung (TCD) in Ruhe, während Hyperkapnie (et-CO2=7.0-7.5 kPa) und in der Ruhephase nach Hyperkapnie.

Ergebnisse: Gruppe A hatte einen signifikanten Anstieg in Vsys, Vmean und PI aufgrund der Hyperkapnie zu allen Zeitpunkten (d. h. 0-2 Tage vor der CEA, 3.-7. post-op Tag und 3 Monate nach CEA). Die N20/P25 Amplitude fiel in Folge der Hyperkapnie vor und unmittelbar nach der CEA ab. Die Veränderungen der anderen SEP Parameter zeigten keine Signifikanz. Gruppe B zeigte signifikante Unterschiede in Folge der Hyperkapnie vor und unmittelbar nach der CEA nur in Bezug auf die Vasoreaktivität (Vsys, Vmean, PI).

Schlussfolgerung: Die hochgradige Karotisstenose verursachte keinerlei hämodynamische Beeinträchtigung in der untersuchten Gruppe der Patienten. Darüber hinaus konnte kein artifizieller Anstieg des cBZ begleitet von einer ebenso signifikanten Veränderung der SEPs nachgewiesen werden.

References

  • 1 Aaslid R, Markwalder TM, Nornes H. Non-invasive transcranial Doppler ultrasound recording of flow velocity in basal cerebral arteries.  J Neurosurg. 1982;  57 769-774
  • 2 Beneš V, Netuka D, Mandys V, Vrabec M, Mohapl M, Beneš V Jr, Kramár F. Comparison between degree of carotid stenosis observed at angiography and in histological examination.  Acta Neurochir (Wien). 2004;  146 671-677
  • 3 Bláha M, Ostrý S. Vliv kofeinu na prutok krve mozkem.  Čes a Slov Neurol a Neurochir. 2003;  66/99 335-337
  • 4 Branston NM, Symon L, Crockard HA, Pasztor E. Realtionship between cortical evoked potential and local cortical blood flow following acute middle cerebral artery occlusion in the baboon.  Exp Neurol. 1974;  95 195-208
  • 5 Derdeyn CP, Yundt KD, Videen TO, Carpenter DA, Grubb RL, Powers WJ. Increased oxygen extraction fraction is associated with prior ischemic events in patients with carotid occlusion.  Stroke. 1998;  29 754-758
  • 6 Derdeyn CP, Videen TO, Frisch SM, Carpenter DA, Grubb RL, Powers WJ. Compensatory mechanisms for chronic cerebral hypoperfusion in patients with carotid occlusion.  Stroke. 1999;  30 1019-1024
  • 7 Derdeyn CP, Videen TO, Yundt KD, Fritsch SM, Carpenter DA, Grubb RL, Powers WJ. Variability of cerebral blood flow and oxygen extraction: stages of cerebral haemodynamic impairment revisited.  Brain. 2002;  125 595-607
  • 8 Dienel GA, Pulsinelli WA, Duffy TE. Regional protein synthesis in rat brain following acute hemispheric ischemia.  J Neurochem. 1980;  35 1216-1226
  • 9 Erecinska M, Silver IA. Relationship between ions and energy metabolism: cerebral calcium movements during ischaemia and subsequent recovery.  Can J Physiol Pharmacol. 1992;  70 ((Suppl)) S190-S193
  • 10 European Carotid Stenosis Trialists’ Collaborative Group . Randomised trial of endarterectomy for recently symptomatic carotid stenosis: final results of MRC European Carotid Surgery Trial (ECST).  Lancet. 1998;  351 1379-1387
  • 11 Florence G, Guerit JM, Gueguen B. Electroencephalography (EEG) and somatosensory evoked potentials (SEP) to prevent cerebral ischaemia in the operating room.  Neurophysiol Clin.. 2004;  34 17-32
  • 12 Furuta S, Ohta S, Hatakeyama T, Nakamura K, Sakaki S. Recovery of protein synthesis in tolerance-induced hippocampal CA1 neurons after transient forebrain ischemia.  Acta Neuropathol (Berlin). 1993;  86 329-336
  • 13 Gosling RG, King DH. Arterial assessment by Doppler shift ultrasound.  Proc R Soc Med. 1974;  67 447-449
  • 14 Grond J van der , Balm R, Kappelle LJ, Eikelboom BC, Mali WP. Cerebral metabolism of patients with stenosis or occlusion of the internal carotid artery. A 1H-MR spectroscopic imaging study.  Stroke. 1995;  26 822-828
  • 15 Halsey JH, MacDowell HA, Gelmon S, Morawetz RB. Blood velocity in the middle cerebral artery and regional cerebral blood flow during carotid endarterectomy.  Stroke. 1989;  20 53-58
  • 16 Hatazawa J, Fujita H, Kanno I, Satoh T, Iida H, Miura S, Murakami M, Okudera T, Inugami A, Ogawa T. Regional cerebral blood flow, blood volume, oxygen extraction fraction, and oxygen utilization rate in normal volunteers measured by the autoradiographic technique and the single breath inhalation method.  Ann Nucl Med. 1995;  9 15-21
  • 17 Hossmann KA. Periinfarct depolarizations.  Cerebrovasc Brain Metab Rev. 1996;  8 195-208
  • 18 Hromada J. Patofyziologické mechanismy ischemických iktu. Abstrakta z Neurologického sjezdu v Hradci nad Moravicí.  Neurologie pro praxi. 2001;  2 ((Suppl. 2)) 9 , (abstr)
  • 19 Inao S, Tadokoro M, Nishino M, Mizutani N, Terada K, Bundo M, Kuchiwaki H, Yoshida J. Neural activation of the brain with hemodynamic insufficiency.  J Cereb Blood Flow Metab. 1998;  18 960-967
  • 20 Jenkins LW, Povlishock JT, Lewelt W, Miller JD, Becker DP. The role of postischemic recirculation in the development of ischemic neuronal injury following complete cerebral ischemia.  Acta Neuropathol (Berl). 1981;  55 205-220
  • 21 Kauppinen RA, Williams SR. Nuclear magnetic resonance spectroscopy studies of the brain.  Prog Neurobio.. 1994;  44 87-118
  • 22 Kontos HA. Validity of cerebral arterial blood flow calculations from velocity measurements.  Stroke. 1989;  20 1-3
  • 23 Kumar K, Goosmann M, Krause GS, Nayini NR, Estrada R, Hoehner TJ, White BC, Koestner A. Ultrastructural and ionic studies in global ischemic dog brain.  Acta Neuropathol (Berlin). 1987;  73 393-399
  • 24 Lee KS, Frank S, Vanderklish P, Arai A, Lynch G. Inhibition of proteolysis protects hippocampal neurons from ischemia.  Proc Natl Acad Sci USA. 1991;  88 7233-7237
  • 25 Lee KY, Sohn YH, Baik JS, Kim GW, Kim JS. Arterial pulsatility as an index of cerebral microangiopathy in diabetes.  Stroke. 2000;  31 1111-1115
  • 26 Markus HS. Cerebral perfusion and stroke.  J Neurol Neurosurg Psychiatry. 2004;  75 353-361
  • 27 Markus HS, Cullinane M. Severely impaired cerebrovascular reactivity predicts stroke and TIA risk in patients with carotid artery stenosis and occlusion.  Brain. 2001;  124 457-467
  • 28 Maruki Y, Koehler RC, Eleff SM, Traystman RJ. Intracellular pH during reperfusion influences evoked potential recovery after complete cerebral ischemia.  Stroke. 1993;  24 697-703
  • 29 MacPherson RW, Zeger S, Traystman RJ. Relationship of somatosensory evoked potentials and cerebral oxygen consumption during hypoxic hypoxia in dogs.  Stroke. 1986;  17 30-36
  • 30 MacPherson RW, Eimerl D, Traystman RJ. Interaction of hypoxia and hypercapnia on cerebral hemodynamics and brain electrical activity in dogs.  Am J Physiol. 1987;  253 H890-H897
  • 31 Meno JR, Nguyen TS, Jensen EM, Alexander WG, Groysman L, Kung DK, Ngai AC, Britz GW, Winn HR. Effect of caffeine on cerebral blood flow response to somatosensory stimulation.  J Cereb Blood Flow Metab. 2005;  25 775-784
  • 32 Nakagawa Y, Yamamoto YL, Meyer E, Hodge CP, Feindel W. Effect of hypercapnia on enhancement of decreased perfusion flow in non-infarcted brain tissues.  Stroke. 1981;  12 85-92
  • 33 Nakagawa Y, Ohtsuka K, Tsuru M, Nakamura N. Effects of mild hypercapnia on somatosensory evoked potentials in experimental cerebral ischemia.  Stroke. 1984;  15 275-278
  • 34 Nakagawara J, Sperling B, Lassen NA. Incomplete brain infarction of reperfused cortex may be quantitated with iomazenil.  Stroke. 1997;  28 124-132
  • 35 Netuka D, Beneš V, Mandys V, Hlásenská J, Burkert J, Beneš V Jr. Accuracy of angiography and Doppler ultrasonography in the detection of carotid stenosis: a histopathological study of 123 cases.  Acta Neurochir (Wien). 2006;  148 511-520
  • 36 North American Symptomatic Carotid Artery Trial Collaborators . Beneficial effect of carotid endarterectomy in symptomatic patients with high-grade carotid stenosis.  N Engl J Med. 1991;  325 445-453
  • 37 North American Symptomatic Carotid Endarterectomy Trial . Methods, patient characteristics, and progress.  Stroke. 1991;  22 711-720
  • 38 Powers WJ, Press GA, Grubb RL, Gado M, Raichle ME. The effect of hemodynamically significant carotid artery disease on the hemodynamic status of cerebral circulation.  Ann Int Medicine. 1987;  106 27-35
  • 39 Powers WJ. Cerebral hemodynamics in ischemic cerebrovascular disease.  Ann Neurol. 1991;  9 31-240
  • 40 Rami A, Kriegelstein J. Protective effects of calpain inhibitors against neuronal damage caused by cytotoxic hypoxia in vitro and ischemia in vivo.  Brain Res. 1993;  609 67-70
  • 41 Rehncrona S, Westerberg E, Akesson B, Siesjö BK. Brain cortical fatty acids and phospholipids during and following complete and severe incomplete ischemia.  J Neurochem. 1982;  38 84-93
  • 42 Roberts-Lewis JM, Siman R. Spectrin proteolysis in hippocampus is a biochemical marker for neuronal injury and neuroprotection.  Ann New York Acad Sci. 1993;  679 78-86
  • 43 Rossini PM, Altamura C, Ferretti A, Vernieri F, Zappasodi F, Caulo M, Pizella V, Del Gratta C, Romani GL, Tecchio F. Does cerebrovascular disease affect the coupling between neuronal activity and local haemodynamics?.  Brain. 2004;  127 99-110
  • 44 Rutgers DR, Klijn CJ, Kappelle LJ, Eikelboom BC, van Huffelen AC, van der Grond J. Sustained bilateral hemodynamic benefit of contralateral carotid endarterectomy in patients with symptomatic internal carotid artery occlusion.  Stroke. 2001;  32 728-734
  • 45 Saido TC, Yokota M, Nagao S, Yamamura I, Tani E, Tsuschiya, Suzuki K, Kawashima S. Spatial resolution of foldrin proteolysis in postischemic brain.  J Biol Chem. 1993;  268 25239-25243
  • 46 Seubert P, Lee K, Lynch G. Ischemia triggers NMDA receptor-linked cytoskeletal proteolysis in hippocampus.  Brain Res. 1989;  492 366-370
  • 47 Schlaepfer WW, Zimmerman UJ. Mechanisms underlying the neuronal response to ischemic injury. Calcium-activated proteolysis of neurofilaments.  Prog Brain Res. 1985;  63 185-196
  • 48 Schreiber SJ, Gottschalk S, Weih M, Villringer A, Valdueza JM. Assessment of blood flow velocity and diameter of the middle cerebral artery during the acetazolamide provocation test by use of transcranial Doppler sonography and MR imaging.  AJNR Am J Neuroradiol. 2000;  21 1207-1211
  • 49 Siesjö BK. Pathophysiology and treatment of focal cerebral ischemia. Part I: Pathophysiology.  J Neurosurg. 1992;  77 169-184
  • 50 Siesjö BK. Pathophysiology and treatment of focal cerebral ischemia. Part II: Mechanism of damage and treatment.  J Neurosurg. 1992;  77 337-354
  • 51 Stejskal L, Kramár F, Mohapl M, Beneš V Jr. Somatosenzorické evokované odpovedi pred a po karotické endarterektomii.  Ces a Slov Neurol Neurochir. 2001;  64/97 114-123
  • 52 Stejskal L, Štetkáová I, Kramár F. Evidence for perirolandic generators of median nerve SEPs from differential scalp recording.  Ces a Slov Neurol Neurochir. 2004;  67/100 29-32
  • 53 Strandgaard S, Paulson OB. Antihypertensive drugs and cerebral circulation.  Eur J Clin Invest. 1996;  26 625-630
  • 54 Valdueza JM, Draganski B, Hoffmann O, Dirnagl U, Einhäupl KM. Analysis of CO2 vasomotor reactivity and vessel diameter changes by simultaneous venous and arterial Doppler recordings.  Stroke. 1999;  30 81-86
  • 55 Vernieri F, Pasqualeni P, Passarelli F, Rossini PM, Silvestrini M. Outcome of carotid artery occlusion is predicted by cerebrovascular reactivity.  Stroke. 1999;  30 593-598
  • 56 White BC, Sullivan JM, Gracia DJ De, O’Neil BJ, Neumar RW, Grossman LI, Rafols JA, Krause GS. Brain ischemia and reperfusion: molecular mechanisms of neuronal injury.  J Neurol Sci. 2000;  179 1-33

Correspondence

Dr. S. Ostrý

Department of Neurosurgery

Charles University

U Vojenské nemocnice 1200

16902 Prague

Czech Republic

Phone: +420/973/20 29 63

Fax: +420/973/20 29 63

Email: svatopluk.ostry@uvn.cz