Effects of ephedrine, dobutamine and dopexamine on cerebral haemodynamics: transcranial Doppler studies in healthy volunteers

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1 British Journal of Anaesthesia 92 (1): 39±44 (2004) DOI: /bja/aeh014 Effects of ephedrine, dobutamine and dopexamine on cerebral haemodynamics: transcranial Doppler studies in healthy volunteers I. K. Moppett 1 *, M. J. Wild 2, R. W. Sherman 2, J. A. Latter 2, K. Miller 3 and R. P. Mahajan 12 1 University Department of Anaesthesia, Queen's Medical Centre, Nottingham, UK. 2 Nottingham City Hospital, Nottingham, UK. 3 Medical School, Nottingham University, Nottingham, UK *Corresponding author. iain.moppett@nottingham.ac.uk Background. Sympathomimetic drugs are assumed to have no direct effects on cerebral haemodynamics on the basis of animal experiments; there is little evidence of their direct effects in humans. This study aimed to address this issue. Methods. The effects of ephedrine, dobutamine, and dopexamine on cerebral autoregulation, cerebral vascular reactivity to carbon dioxide, estimated cerebral perfusion pressure, and zero ow pressure (ZPF) were studied in 10 healthy volunteers using transcranial Doppler ultrasound. The strength of autoregulation was measured using the transient hyperaemic response test. The reactivity to carbon dioxide was measured as the change in middle cerebral artery ow velocity with a step change in end-tidal carbon dioxide. For the estimated cerebral perfusion pressure and the ZFP, established formulae were used which utilized instantaneous values of arterial pressure and middle cerebral artery ow velocity. Measurements were made at baseline and after i.v. infusion of the study drug to an endpoint of 25% increase in mean arterial pressure (MAP) (ephedrine, dobutamine) or cardiac index (dopexamine). Results. There was no signi cant change in the strength of autoregulation (from (mean (SD)) 1.07 (0.16) to 1.07 (0.18); from 1.07 (0.16) to 1.03 (0.19); from 1.04 (0.12) to 1.04 (0.25)), reactivity to carbon dioxide (from 40% (8) to 36 (10); from 37 (12) to 37 (11); from 45 (12) to 43 (11)) with ephedrine, dobutamine, or dopexamine, respectively. Despite a clinically signi cant increase in MAP with ephedrine and dobutamine and a clinically signi cant increase in cardiac index with dopexamine, the estimated cerebral perfusion pressure did not change signi cantly (from 81 (38) to 60 (16) mm Hg with ephedrine; from 67 (22) to 63 (11) mm Hg with dobutamine; from 87 (27) to 79 (17) mm Hg with dopexamine). The ZFP increased signi cantly with ephedrine (from 29 (10) to 44 (11) mm Hg) and dobutamine (from 35 (14) to 43 (10) mm Hg) but not dopexamine (from 3 (23) to 11 (22) mm Hg). Conclusions. Sympathomimetic agents do not signi cantly change cerebrovascular homeostasis as assessed by the transient hyperaemic response test, reactivity to carbon dioxide and estimated cerebral perfusion pressure. Br J Anaesth 2004; 92: 39±44 Keywords: blood, ow, zero ow pressure; measurement techniques, transcranial Doppler; sympathetic nervous system, beta-sympathomimetic Accepted for publication: July 14, 2003 Sympathomimetic drugs are used widely in intensive care and anaesthesia to manipulate cardiovascular variables. Many of these patients have a disordered cerebral circulation either because of trauma, 1 sepsis, 2 sub-arachnoid haemorrhage, 3 or pre-existing cerebrovascular disease. 4 Although sympathomimetic drugs are assumed to have little direct effect on the cerebral circulation, 5±7 the effects of these drugs on cerebral autoregulation, reactivity to carbon dioxide, estimated cerebral perfusion pressure and zero ow pressure (ZFP), as assessed by transcranial Doppler ultrasonography are not well documented. A knowledge of any such effects is important for judicious Ó The Board of Management and Trustees of the British Journal of Anaesthesia 2004

2 Moppett et al. use of these drugs in patients with neurological disorders. Alteration of cerebrovascular tone can affect cerebral autoregulation 8 and can also in uence estimated cerebral perfusion pressure and ZFP; 910 cerebral perfusion pressure may therefore be changed independently of changes in intracranial pressure. 10 The overall effects of sympathomimetic agents are dependent on their balance of a, b, and dopaminergic effects, and their mode of action. Before assessing the effects of these drugs in subjects with neurological disorders, it is rst necessary to know what effect they might have in healthy subjects. In the present study, we aimed to assess the effects of clinically signi cant doses of ephedrine, dobutamine, and dopexamine, all commonly used, predominantly b agonists, at steady state on cerebral autoregulation, reactivity to carbon dioxide, estimated cerebral perfusion pressure, and ZFP in healthy volunteers. Methods To allow for the relative lack of pressor effect of dopexamine, two slightly different protocols were followed. Protocol A assessed the effects of ephedrine and dobutamine; protocol B assessed dopexamine. The local Ethics Committee approved the study. All subjects were enrolled after giving informed, written consent. Subjects were healthy volunteers. Criteria for exclusion were: age less than 18 yr or more than 40 yr; history of hypertension (or measured arterial pressure >130/ 85 mm Hg) or neurological disease; drugsðany vaso-active substances, for example calcium channel blockers, antidepressants; history of migraine; smokers; pregnancy/potential pregnancy. The 10 subjects for protocol A were different subjects to the 10 for protocol B as the studies were carried out on different sites. Subjects were studied in the supine position (protocol A) or sat at 45 (protocol B). Cerebral blood ow is not known to be in uenced by position. The subjects sat up in protocol B for comfort and ease of positioning of the Doppler probe. Each subject lay with his or her head in a comfortable position on a pillow. The left middle cerebral artery was identi ed using standard criteria, 7 via the subjects' temporal window, using a 2 MHz pulsed transcranial Doppler ultrasonography probe (SciMed PCDop 842 (protocol A) and QVL (protocol B), SciMed, Bristol, UK). The position of the probe was held constant throughout the study by the application of a headband, to ensure a constant angle of insonation. The middle cerebral artery ow velocity waveform was recorded continuously onto digital audiotape for subsequent analysis using speci c software (SciMed). Following application of a nose clip, constant end-tidal carbon dioxide monitoring was instituted via a mouthpiece connected to a capnograph (Datex Capnomac (protocol A) or Marquette (protocol B)). The arterial pressure was measured non-invasively at 1-min intervals for the duration of the test (Dinamap (protocol A) or Marquette (protocol B)). Further monitoring consisted of continuous pulse oximetry and electrocardiography. For protocol B, the cardiac index was determined using a transoesophageal Doppler probe (Deltex, Chichester) inserted nasally under local anaesthesia. All transcranial Doppler ultrasonography measurements were taken with the probe removed to avoid confounding effects of discomfort from the probe. Middle cerebral artery ow velocity, cerebral autoregulation, reactivity to carbon dioxide, and arterial pressure were measured with the subject receiving no drug (baseline values) and then following titration of the drug to a predetermined cardiovascular endpoint. Each drug was studied on a separate day. For protocol A, the order of drug was chosen at random, and the endpoint was an increase in mean arterial pressure (MAP) of 25% above baseline values. For protocol B, dopexamine was titrated to an increase in cardiac index of 25% over baseline. The drugs were studied in an open label fashion as pilot studies had shown that subjects were likely to be aware of the drug infusion as a result of peripheral b-stimulation leading to tremulousness. The starting infusion rate was 0.3 mg kg ±1 min ±1 for ephedrine, 1.25 mgkg ±1 min ±1 for dobutamine and mg kg ±1 min ±1 for dopexamine. Each drug was titrated to the arterial pressure or cardiac index endpoint by increasing the rate of infusion every 2±5 min. Cerebral haemodynamic measurements were repeated only after achieving a steady state at the cardiac index or arterial pressure endpoint; steady state was de ned as less than 5 mm Hg change in MAP on successive recordings or less than 0.1 litre min ±1 m ±2 change in cardiac index over 5 min. Transcranial Doppler ow velocity measurements Cerebral autoregulation. This was assessed by performing the transient hyperaemic response test. The details of this test have been described previously. 11±13 Brie y, it consists of compression of the common carotid artery ipsilateral to the insonated middle cerebral artery for 10 s and then sudden release; with intact autoregulation a transient hyperaemic response is seen at the release of compression. The criteria for the acceptance of a transient hyperaemic response test were: (i) a sudden and maximal decrease in ow velocity at the onset of compression; (ii) stable heart rate for the period of compression; (iii) steady Doppler signal for the duration of compression; and (iv) absence of ow transients following release of compression. 13 Two indices were calculated to assess autoregulation, the transient hyperaemic response ratio and the strength of autoregulation. Analysis was performed by selecting three waveforms from each period of compression: (i) the middle cerebral artery waveform immediately before compression, 40

3 Beta-agonists and cerebral circulation F1; (ii) the rst waveform following compression, F2; and (iii) the waveform immediately following release of compression, F3. 13 The time-averaged mean of the outer envelope of the ow velocity pro le was used for performing the analysis. The transient hyperaemic response ratio (THRR) was calculated as: THRR=F3/F1 (1) The strength of autoregulation (SA) was calculated as: SA=(F33P2)/(MAP3F1) (2) where, P2 is the greater value of either the estimated arterial pressure in the middle cerebral artery at the onset of common carotid artery compression, as calculated by: P2=MAP3F2/F1 (3) or 60 mm Hg (the assumed lower limit of autoregulation). Details of the derivation of these formulae have been published previously. 13 The strength of autoregulation is considered to be a better measure of autoregulation as it takes into account the variable decrease in perfusion pressure on compression as a result of (i) variable amounts of ow around the circle of Willis and (ii) incomplete occlusion of the carotid artery. Reactivity to carbon dioxide. After baseline measurements of arterial pressure, end tidal carbon dioxide and middle cerebral artery ow velocity breathing room air, subjects were asked either to raise or lower their end tidal carbon dioxide. To lower the end tidal carbon dioxide, subjects were asked to increase the rate and depth of their breathing suf cient to reduce their end tidal carbon dioxide by 1 kpa from baseline. Once this had been achieved at steady state (1 min of lowered end tidal carbon dioxide) repeated measurements of arterial pressure, end tidal carbon dioxide and middle cerebral artery ow velocity were made. To raise end tidal carbon dioxide subjects breathed through a Mapleson D circuit with low ows of air and oxygen to allow a degree of re-breathing suf cient to increase end tidal carbon dioxide by 1 kpa. Again, once this had been achieved at steady state (1 min of raised end tidal carbon dioxide) repeated measurements of arterial pressure, end tidal carbon dioxide and middle cerebral artery ow velocity were made. The order of hypo- or hypercapnia was made at random. Subjects were allowed to breath room air to normalise their end tidal carbon dioxide between measurements. The reactivity to carbon dioxide was calculated as the percentage change of mean middle cerebral artery ow velocity per kpa change in end tidal carbon dioxide. 13 Estimated cerebral perfusion pressure and ZFP. These were calculated using the method described by Belfort. 14 Simultaneous measurements of arterial pressure and transcranial Doppler ultrasonography velocities were recorded. The estimated cerebral perfusion pressure, ecpp, was derived from: ecpp=[mfv/(mfv ± DFV)]3(MAP ± DAP) (4) where, MAP and DAP are mean and diastolic arterial pressures, and MFV and DFV are mean and diastolic middle cerebral artery ow velocities. ZFP was calculated using the following formula: ZFP=MAP ± ecpp (5) Statistics The calculated range for strength of autoregulation in healthy volunteers is 0.88±1.12 with a coef cient of variation of less than 10% on repetitive measurements within the same subject We calculated that 10 subjects would be required to detect an absolute difference of 0.15 in strength of autoregulation with a power of 0.8 and a of This is a clinically relevant change of similar magnitude to that seen with impairment of autoregulation with inhalation anaesthetics. 11 Post hoc testing indicated that the study had the same power to detect clinically signi cant differences in reactivity to carbon dioxide (30% relative change). Changes of up to 50% may be seen with high doses of anaesthetics, 11 cerebrovascular disease, 16 and traumatic brain injury. 17 The data were tested for normality of distribution using the Anderson±Darling test. Cerebrovascular and cardiovascular variables were analysed using multivariate ANOVA comparing data before and after administration of each drug for each subject. Where the null hypothesis was rejected, signi cant differences between the means were analysed using Tukey's test. All statistical analyses were performed using SPSS 11.0 for Windows. Control measurements were always from the period immediately preceding the administration of the study drug. Results Subjects were aged between 22 and 38 yr. In protocol A, seven were males, three females: all were males in protocol B. The endpoint of increase in MAP or cardiac index was reached in all subjects (Table 1). The oxygen saturation was greater than or equal to 98% for all subjects throughout the study. The median dose (range) of drug required was: ephedrine 30 (9±54) mg kg ±1 min ±1, dobutamine 12.5 (10± 25) mg kg ±1 min ±1, dopexamine 0.25 (0.125±0.5) mg kg ±1 min ±1. The median (range) time to reach steady state was: ephedrine 15 (11±33) min, dobutamine 15 (6±24) min, and dopexamine 20 (15±35) min. There were no adverse events. Some subjects reported slight tremulousness with ephedrine, dobutamine, and dopexamine. The effects of each drug on middle cerebral artery ow velocity, transient hyperaemic response ratio, strength of autoregulation, reactivity to carbon dioxide, estimated 41

4 Moppett et al. Table 1. The effect of experimental drugs on cerebrovascular and haemodynamic. Variables: CI, cardiac index; CPP, cerebral perfusion pressure; CR, compression ratio; CRCO 2, cerebral vascular reactivity to carbon dioxide; HR, heart rate; MCAFV, time-averaged mean middle cerebral artery ow velocity; SA, strength of autoregulation; THRR, transient hyperaemic response ratio. All values are given as mean (SD) All results are non-signi cant unless stated otherwise. *P<0.05 vs control values Ephedrine Dobutamine Dopexamine Control Drug Control Drug Control Drug HR (beats min ±1 ) 69 (5) 71 (9) 67 (10) 76 (12) 64 (6) 70 (9) MAP (mm Hg) 86 (9) 104 (9) 89 (9) 106 (8) 89 (11) 90 (9) CI (litre min ±1 m ±2 ) NA NA NA NA 2.2 (0.3) 2.8 (0.3) MCAFV (cm s ±1 ) 57 (18) 56 (13) 52 (11) 56 (13) 59 (5) 62 (7) CRCO 2 (%/kpa) 40 (8) 36 (10) 37 (12) 37(11) 45 (12) 43 (11) THRR 1.43 (0.15) 1.52 (0.13) 1.52 (0.20) 1.54 (0.12) 1.28 (0.29) 1.31 (0.17) SA 1.07 (0.16) 1.07 (0.18) 1.07 (0.16) 1.03 (0.19) 1.04 (0.12) 1.07 (0.25) CPP (mm Hg) 56 (12) 60 (16) 53 (22) 63 (11) 87 (27) 79 (17) ZFP (mm Hg) 29 (10) 44 (11)* 35 (21) 43 (10)* 3 (23) 11 (22) cerebral perfusion pressure, and ZFP are detailed in Table 1. The middle cerebral artery ow velocity, strength of autoregulation, transient hyperaemic response ratio, and reactivity to carbon dioxide remained within the normal range before and during infusion of each drug. None of the drugs had a statistically signi cant effect on the strength of autoregulation, reactivity to carbon dioxide, or estimated cerebral perfusion pressure. The ZFP increased signi cantly with ephedrine and dobutamine, but not dopexamine. Discussion We have shown that the sympathomimetic drugs tested in this study have little effect on the strength of autoregulation or reactivity to carbon dioxide in healthy volunteers. In addition, we have shown that despite having achieved a clinically signi cant increase in MAP, ephedrine and dobutamine did not signi cantly increase estimated cerebral perfusion pressure, and were associated with statistically signi cant increases in ZFP suggesting an increase in the tone of the cerebral vasculature. There is an abundant sympathetic innervation of the cerebral vasculature. 18 In animals with normal blood±brain barriers, adrenergic drugs have been shown to have no effect on cerebral blood ow measured by xenon clearance, thermoclearance, and tissue gas tensions. 19±21 If the blood± brain barrier is disrupted or bypassed, the effects of such agents can be either vasodilatory (b) or vasoconstrictive (a) depending upon the drug pro le and the size of the vessels. 22 Chronic cervical sympathectomy in baboons reduces the lower limit of autoregulation suggesting a role for the sympathetic nervous system in modulating cerebrovascular tone indirectly Acute cervical sympathectomy in baboons reduces the upper limit of the autoregulatory plateau. In humans, the evidence for the effect of sympathomimetic agents is less direct. Some of the methods of assessing cerebral autoregulation rely on pharmacological means of manipulating arterial pressure. 7 The results of these tests could be taken to be confounded by the direct effects of vasoactive agents, unless it is assumed that these agents have no direct effect on cerebral autoregulation. Berre and colleagues 25 showed that dobutamine (10 mg kg ±1 min ±1 ) given to septic patients with an altered conscious level increased middle cerebral artery ow velocity in parallel with increases in cardiac index and MAP. In contrast to much of the animal work, b-block in humans has no effect on cerebral blood ow measured by xenon clearance or transcranial Doppler ultrasonography suggesting that, at least in normal individuals, b-adrenergic stimulation is not important. 26 The transient hyperaemic response test provides an ideal opportunity to study direct effects of vasoactive agents on cerebral autoregulation. Unlike some other commonly used tests of autoregulation 7 the transient hyperaemic response test does not rely on the use of vasoactive substances to change systemic arterial pressure. Therefore, its use avoids any confounding interactions between the direct effects of a drug and autoregulatory in uences on the vascular tone. We found no statistically signi cant change in the strength of autoregulation with any of the drugs. Cerebral vascular reactivity to carbon dioxide is a marker of the ability of the cerebral vasculature to respond to metabolic demands, normally independent of perfusion pressure. 27 Patients with head injuries may have reduced reactivity to carbon dioxide, which in some may show a return of reactivity to carbon dioxide to normal with increased MAP. 17 Using transcranial Doppler ultrasonography experiments with changes in carbon dioxide and head up tilt/ganglionic block to augment/diminish sympathetic tone, Jordan and colleagues 28 suggested that sympathetic tone may attenuate the carbon dioxide-induced increase in cerebral blood ow. Studies in patients with autonomic neuropathy secondary to diabetes mellitus show increased reactivity to carbon dioxide in the presence of postural hypotension and decreased reactivity to carbon dioxide in its absence. 29 However, labetalol does not affect reactivity to carbon dioxide in volunteers

5 Beta-agonists and cerebral circulation Our results suggest that b-sympathomimetic drugs do not cause a signi cant change in reactivity to carbon dioxide in normal, young subjects. The difference between our results and those of Jordan and colleagues 28 may be a result of difference in experimental technique. We gave steady-state infusions of single drugs, whereas Jordan and colleagues assessed the effect of sympathetic activation or block, which is a more subtle process. The same arguments apply to the results found in diabetic autonomic neuropathy. 29 The labetalol results are consistent with ours, although again this is a pharmacological rather than physiological approach. There is no single accepted de nition of cerebral perfusion pressure. Taking the orthodox view of: CPP=MAP ± (greater of) ICP or CVP (6) where, CPP is cerebral perfusion pressure, ICP is intracranial pressure and CVP is central venous pressure, any increase in MAP will increase cerebral perfusion pressure provided intracranial pressure or central venous pressure remain unchanged; indeed, in clinical practice vasopressors are used to increase cerebral perfusion pressure by increasing MAP. 31 However, recently it has been shown that in patients/subjects with normal intracranial pressure, cerebrovascular tone is the major determinant of the downstream component of cerebral perfusion pressure. 910 Thus, a more general concept of ZFP has been introduced, where ZFP is de ned as the pressure at which ow in a vessel would cease. In the cerebral circulation the ZFP is a function of intracranial pressure, central venous pressure, and vascular tone 30±33 and the cerebral perfusion pressure can be estimated from the difference between MAP and ZFP. In conditions of relatively low intracranial pressure and central venous pressure, vascular tone may be the dominant component of ZFP. Thus, if a drug or manoeuvre, which is designed to increase MAP also results in a similar increase in ZFP, it will fail to have any effect on estimated cerebral perfusion pressure. In the present study, both ephedrine and dobutamine, despite causing signi cant increases in MAP, failed to increase estimated cerebral perfusion pressure presumably a result of simultaneous increases in ZFP. The increase in ZFP with ephedrine and dobutamine suggests that use of these drugs is associated with increased cerebrovascular tone. Given the lack of effect on reactivity to carbon dioxide, an indirect effect as a result of changes in MAP is the most likely explanation, although a direct effect of these drugs on the vascular bed cannot be excluded. Whatever the cause, this is an interesting nding as it tends to challenge the frequently recommended use of vasopressors to increase cerebral perfusion pressure. 34 However, further studies are required with different vasoactive drugs in healthy subjects and in patients with head injury to de ne the place of estimated cerebral perfusion pressure. We have used the term b-sympathomimetics within this study as that re ects the predominant action of these drugs. The choice of drugs used in this study was based on their common clinical use and spectrum of associated a-receptor activity; dopexamine is known to have no effect on a receptors, dobutamine has some a-agonistic effect, and ephedrine has signi cant a-agonistic effect. We used two different endpoints (MAP or cardiac index) for drug titration. This was appropriate because dopexamine could not be expected to signi cantly increase MAP. Furthermore, the aim of the endpoint was to reach a measurable, repeatable and clinically relevant cardiovascular change with each drug. The range of drug doses required was relatively wide, but this re ects clinical and experimental experience. We chose not to attempt to de ne a dose± response relationship for each drug as using smaller cardiovascular changes was even less likely to produce cerebrovascular change and 25±30% changes are commonly used in cerebrovascular studies. Transoesophageal Doppler estimation of cardiac output has been validated against indicator dilution methods; 35 changes correlate better than absolute values. 35 This study was not designed to investigate the effects of sympathomimetic agents in head injury or sepsis, but rather to clarify what is `normal'. Extrapolation of these results to patients with neurological disease will be inappropriate. However, these results will serve as the point of reference for further studies in patients with neurological disorders. In conclusion, we have found that a range of b- sympathomimetic agents, given systemically, do not affect the cerebral haemodynamics as assessed by transient hyperaemic response tests, cerebral reactivity to carbon dioxide, or cerebral perfusion pressure using transcranial Doppler studies. If changes in these variables are seen in pathological states when using these drugs then clinicians should seek the cause. Acknowledgements The Transcranial Doppler ultrasound equipment was purchased with a grant from the Association of Anaesthetist of Great Britain and Ireland. The Oesophageal Doppler probes were kindly donated by Deltex Medical, UK. References 1 Czosnyka M, Matta BF, Smielewski P, Kirkpatrick PJ, Pickard JD. Cerebral perfusion pressure in head-injured patients: a noninvasive assessment using transcranial Doppler ultrasonography. J Neurosurg 1998; 88: 802±8 2 Bowie RA, O'Connor PJ, Mahajan RP. Cerebrovascular reactivity to carbon dioxide in sepsis syndrome. Anaesthesia 2003; 58: 261±5 3 Lam JM, Smielewski P, Czosnyka M, Pickard JD, Kirkpatrick PJ. Predicting delayed ischemic de cits after aneurysmal subarachnoid hemorrhage using a transient hyperemic response test of cerebral autoregulation. Neurosurgery 2000; 47: 819±25 4 Lam JM, Smielewski P, al-rawi P, et al. Prediction of cerebral ischaemia during carotid endarterectomy with preoperative CO 2 -reactivity studies and angiography. Br J Neurosurg 2000; 14: 441±8 5 Giller CA, Bowman G, Dyer H, Mootz L, Krippner W. Cerebral 43

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J Neurosurg Anesth 2000; 12: 210±6 11 Bedforth NM, Girling KJ, Harrison JM, Mahajan RP. The effects of sevo urane and nitrous oxide on middle cerebral artery blood ow velocity and transient hyperemic response. Anesth Analg 1999; 89: 170±4 12 Harrison JM, Girling KJ, Mahajan RP. Effects of target-controlled infusion of propofol on the transient hyperaemic response and carbon dioxide reactivity in the middle cerebral artery. Br J Anaesth 1999; 83: 839±44 13 Mahajan RP, Cavill G, Simpson EJ. Reliability of the transient hyperemic response test in detecting changes in cerebral autoregulation induced by the graded variations in end-tidal carbon dioxide. Anesth Analg 1998; 87: 843±9 14 Belfort MA, Saade GR, Grunewald C, et al. Association of cerebral perfusion pressure with headache in women with preeclampsia. Br J Obstet Gynaecol 1999; 106: 814±21 15 Sherman RW, Bowie RA, Henfrey MM, Mahajan RP, Bogod D. Cerebral haemodynamics in pregnancy and pre-eclampsia as assessed by transcranial Doppler ultrasonography. Br J Anaesth 2002; 89: 687±92 16 Thiel A, Zickmann B, Stertmann WA, Wyderka T, Hempelmann G. Cerebrovascular carbon dioxide reactivity in carotid artery disease. Relation to intraoperative cerebral monitoring results in 100 carotid endarterectomies. Anesthesiology 1995; 82: 655±61 17 Steiger HJ, Ciessinna E, Seiler RW. Identi cation of posttraumatic ischemia and hyperperfusion by determination of the effect of induced arterial hypertension on carbon dioxide reactivity. Stroke 1996; 27: 2048±51 18 Duckles SP. Innervation of the cerebral vasculature. Ann Biomed Eng 1983; 11: 599± MacKenzie ET, McCulloch J, O'Kean M, Pickard JD, Harper AM. Cerebral circulation and norepinephrine: relevance of the bloodbrain barrier. Am J Physiol 1976; 231: 483±8 20 McCalden TA, Eidelman BH. Cerebrovascular response to infused noradrenalin and its modi cation by a catecholamine metabolism blocker. Neurology 1976; 26: 987±91 21 Raichle ME, Hartman BK, Eichling JO, Sharpe LG. Central noradrenergic regulation of cerebral blood ow and vascular permeability. Proc Natl Acad Sci USA 1975; 72: 3726±30 22 Wei EP, Raper AJ, Kontos HA, Patterson JL jr. Determinants of response of pial arteries to norepinephrine and sympathetic nerve stimulation. Stroke 1975; 6: 654±8 23 MacKenzie ET, McGeorge AP, Graham DI, Fitch W, Edvinsson L, Harper AM. Effects of increasing arterial pressure on cerebral blood ow in the baboon: in uence of the sympathetic nervous system. P ugers Arch 1979; 378: 189±95 24 Edvinsson L, Hardebo JE, Owman C. In uence of the cerebrovascular sympathetic innervation on regional ow, autoregulation, and blood-brain barrier function. Ciba Found Symp 1978; 56: 69±95 25 Berre J, De Backer D, Moraine JJ, Melot C, Kahn RJ, Vincent JL. Dobutamine increases cerebral blood ow velocity and jugular bulb hemoglobin saturation in septic patients. Crit Care Med 1997; 25: 392±8 26 Schroeder T, Schierbeck J, Howardy P, Knudsen L, Skafte-Holm P, Gefke K. Effect of labetalol on cerebral blood ow and middle cerebral arterial ow velocity in healthy volunteers. Neurol Res 1991; 13: 10±2 27 Maeda H, Matsumoto M, Handa N, et al. Reactivity of cerebral blood ow to carbon dioxide in various types of ischemic cerebrovascular disease: evaluation by the transcranial Doppler method. Stroke 1993; 24: 670±5 28 Jordan J, Shannon JR, Diedrich A, et al. Interaction of carbon dioxide and sympathetic nervous system activity in the regulation of cerebral perfusion in humans. Hypertension 2000; 36: 383±8 29 Tantucci C, Bottini P, Fiorani C, et al. Cerebrovascular reactivity and hypercapnic respiratory drive in diabetic autonomic neuropathy. J Appl Physiol 2001; 90: 889±96 30 Michel E, Hillebrand S, von Twickel J. Frequency dependence of cerebrovascular impedence in pre-term neonates: a different view on critical closing pressure. 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