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(Stroke. 1997;28:1564-1568.)
© 1997 American Heart Association, Inc.

Articles

Cerebrovascular and Cardiovascular Measurements During Neurally Mediated Syncope Induced by Head-Up Tilt

Ronald Schondorf, PhD, MD; Julie Benoit, MSc Theodore Wein, MD

From the Autonomic Reflex Laboratory, Department of Neurology, McGill University, Sir Mortimer B. Davis Jewish General Hospital, Montreal, Quebec, Canada.

	Abstract

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Background and Purpose This study examines changes in systemic hemodynamics and in cerebral blood velocity that occur during neurally mediated syncope (NMS) to determine whether cerebral autoregulation is intact or impaired in patients with recurrent NMS.

Methods Beat-to-beat recordings of heart rate, blood pressure (volume clamp photoplethysmography), stroke volume (impedance cardiography), and right middle cerebral artery blood velocity (transcranial Doppler sonography) were performed at rest and during 80° head-up tilt. Twelve patients with NMS and 10 healthy control subjects were studied.

Results Baseline values and the initial response to head-up tilt of control subjects and patients with NMS were similar. The mean latency to onset of syncope was 11.8±11.1 minutes. At syncope, heart rate, systolic and diastolic blood pressure, and diastolic cerebral blood velocity decreased significantly, whereas systolic cerebral blood velocity did not change. Calculated cerebrovascular resistance was significantly reduced from 1.85±0.60 to 1.32±0.27 mm Hg/cm per second, whereas the pulsatility index increased from 0.92±0.16 to 1.52±0.21. We never observed a change in cerebral blood velocity before the rapid decline in blood pressure, nor did we observe any significant change in respiratory pattern.

Conclusions The decrease in cerebrovascular resistance during NMS indicates that the integrity of cerebrovascular autoregulation is maintained even when syncope is imminent. The selective loss of diastolic flow during syncope and the increase in pulsatility index are likely caused by collapse of downstream vessels as diastolic blood pressure decreases below the critical closing pressure of cerebral vessels.

Key Words: autoregulation • cerebral blood flow • syncope • transcranial Doppler

	Introduction

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The most common form of syncope encountered in clinical practice is vasovagal or neurally mediated syncope.^{1 2} NMS is often not indicative of abnormal cardiovascular physiology and can be elicited in almost any normal subject if central blood volume is reduced sufficiently.^{3 4 5 6 7} Those with recurrent NMS may have symptoms provoked by lesser levels of orthostatic stress such as head-up tilt with footrest support. In both groups there are often small declines in BP and TPR associated with malaise and premonitory symptoms that occur before the cardiovascular collapse of syncope.^{3 8 9} The trigger of this abrupt decrease in SBP, DBP, TPR, and HR is unknown.^{8 10 11}

Although the pathophysiology of NMS in patients and in normal control subjects may differ, it is likely that the loss of consciousness during syncope results from cerebral hypoperfusion.^{3 12 13} Rapidly responding cerebrovascular autoregulatory mechanisms might be expected to partially counter the hemodynamic collapse during syncope.^{14 15 16} Some have suggested, however, that cerebral vasoconstriction rather than vasodilatation may occur during NMS.^{5 17 18} Others have observed only a minimal cerebral vasoconstriction during syncope that was induced in normal subjects by incremental lower body negative pressure.^{19 20} In these latter studies much larger cerebral vasoconstriction was elicited by hyperventilation, although no impairment in consciousness was ever observed during this maneuver.

The suggestion that a unique derangement of cerebral autoregulation exists in patients with recurrent NMS requires further investigation. It clearly does not correlate with clinical observations of maintained patient consciousness despite significant hypotension during HUT. Moreover, in some of the studies mentioned above, BP and respiration were not continuously monitored so that the precise relationship between systemic and cardiovascular hemodynamics could not be established.^{17 18} The specific aim of this study was to examine changes that occur in cerebral circulation during HUT in normal control subjects and in patients with recurrent NMS. We hypothesized that cerebral autoregulation is not impaired in patients with NMS and that a reduction in CVR would partially offset the cerebral hypoperfusion during impending syncope.

	Subjects and Methods

Top Abstract Introduction Subjects and Methods Results Discussion References

 
Twelve patients with recurrent NMS were included in this study. Two patients were referred for recurrent syncope without warning, and 10 were referred for evaluation of symptomatic orthostatic intolerance that included multiple episodes of near syncope or syncope. Many had symptoms of presyncope that were exacerbated by exposure to heat or prolonged standing. In all 12 patients history, physical examination, routine clinical chemistry, complete blood count, Holter monitor, electroencephalogram, electrocardiogram, and echocardiographic evaluation did not reveal the cause of syncope. No patient took medication of any kind. Eleven had a previous HUT test without TCD measurements in our laboratory, and all fainted (mean latency to syncope, 12.5±10.1; range, 4 to 40 minutes). Ten healthy subjects of similar age, weight, and height with no history of syncope or orthostatic intolerance served as the initial control group. One who fainted during HUT was excluded from analysis.

The HUT test protocols were approved by the hospital internal review board, and informed consent was obtained from all subjects. All patients were supine for 30 to 45 minutes before recordings. The HUT protocol consisted of a 10-minute resting period in the supine position, 40-minutes of 80° HUT with footrest support, and a second 5-minute period with the subject supine. The HUT was ended if a subjective sensation of impending syncope was associated with a clear precipitous drop in BP or HR. The episodes of syncope during HUT were preceded by or associated with lightheadedness, nausea, blurred vision, and sweating. All 12 patients fainted during this test.

BP was continuously recorded from the third finger of the left hand with a volume clamp photoplethysmograph (Finapres model 2300, Ohmeda Monitoring Systems) and was also intermittently measured from the brachial artery with a sphygmomanometer. During the recording period, the subject's hand was warmed with a heated pad to prevent finger vasoconstriction.^{8 21} The arm was maintained at the level of the heart. Respiratory movements were measured with a nasal thermistor. SV and CO were monitored with an impedance cardiograph (BoMed NCCOM3 R-7, BoMed Medical Manufacturing). The right MCA was insonated through the temporal window at depths ranging between 45 and 55 mm with a 2-MHz Doppler probe (Eden Medical Equipment TC-64) that was firmly strapped in place with an adjustable headband to ensure a fixed angle of insonation. The analog ECG, BP, spectral envelope of CBV, and respiratory signals were sampled at 200 Hz and fed to a PC equipped with an eight-channel analog/digital acquisition card and software (Windaq, Dataq Instruments). SV and CO values, averaged every 16 cardiac cycles, were serially transferred to the PC via the RS232 port of the impedance cardiograph.

Beat-to-beat HR, systolic and diastolic BP, and CBV were derived off-line with an automatic peak and trough detection algorithm. In all cases placement of the cursors was verified by visual inspection of the waveforms. The data were then resampled at 2 Hz with a linear interpolation algorithm. CVR was initially calculated as MBP/MCBV. A conservative correction of CVR that accounted for the hydrostatic reduction in MBP at the level of insonation during standing was calculated as (MBP-15 mm Hg)/MCBV.²² Both of these calculations assume that MCA caliber remains constant so that CBV is an accurate reflection of CBF. CBV is considered to be an index of CBF because changes in cerebral artery lumen area of the insonated vessel are minimal²³ and because carotid blood flow is closely correlated with MCA velocity.^{24 25} Gosling's PI, expressed as (SCBV-DCBV)/MCBV, which is used by some as an index of CVR, was also continuously derived.²⁶ To obtain a smoothed profile of the hemodynamic response of control and syncopal subjects to HUT, sequential segments of 60 seconds of data were averaged. A detailed profile of the events preceding syncope was constructed by averaging each of the last 240 interpolated data points taken from all 12 patients with NMS (120 seconds) before the patients were returned to the supine position. Nonparametric statistical tests (Mann-Whitney U test) were used to assess the statistical significance of paired and unpaired data. Data are expressed as mean±SD. Statistical significance was defined as P<.05.

	Results

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The anthropomorphic characteristics of the 10 control subjects and 12 patients with NMS are provided in the top portion of Table 1. Sample recordings from one control subject and from one patient with NMS are shown in Figs 1 and 2. In both groups the initial cardiovascular response to HUT consisted of an increase in HR and DBP, a decrease in SV and CO, and a variable small change in SBP. The initial cerebrovascular response to HUT was a small decrease in SCBV, DCBV, and MCBV, whereas PI did not change. During HUT CVR appeared to increase when MBP measured at heart level was used. When the correction for hydrostatic reduction in MBP at the level of insonation of the MCA was applied, CVR diminished slightly or did not change. The averaged values of 10 minutes of data recorded while the patient was supine and during the first 3 minutes of HUT are shown in the bottom portion of Table 1. All parameters were similar except for baseline HR, which was increased in the NMS group. This small difference in baseline HR has been noted previously.⁸

View this table: [in this window] [in a new window]   Table 1. Characteristics of Control Subjects and Patients With Syncope

View larger version (39K): [in this window] [in a new window]   Figure 1. Profile of the beat-to-beat cardiovascular and cerebrovascular responses to HUT (performed at 5 minutes) of a normal control subject. In this and in all subsequent figures CVR was not corrected for the discrepancy between MBP recorded at heart level and the reduced pressure actually expected at the point of insonation.

View larger version (34K): [in this window] [in a new window]   Figure 2. Profile of the beat-to-beat cardiovascular and cerebrovascular responses to HUT (performed at 5 minutes) of a patient with NMS.

The mean latency to onset of syncope (11.8±11.1 minutes; range, 3 to 38 minutes) during the second HUT with TCD did not differ from the latency to onset of syncope during the original HUT. Fig 3 depicts the detailed temporal profile of the cardiovascular and cerebrovascular responses during NMS obtained by back-averaging the last 240 points (2 minutes) of resampled beat-to-beat data from the trough of the SBP (end of the syncopal response). At syncope there was a sudden decrease in SBP, DBP, HR, and DCBV, whereas SCBV did not change (Fig 2). This response was observed in all 12 patients and in the one control subject who fainted during HUT. In no case was any change in CBV observed before the rapid decline in BP, nor was any significant change in respiratory pattern ever noted. A comparison of the magnitudes of the responses obtained at the trough of the syncope with those obtained 1 minute before syncope is shown in Table 2.

View larger version (25K): [in this window] [in a new window]   Figure 3. Detailed averaged profile of presyncope of all 12 patients.

View this table: [in this window] [in a new window]   Table 2. Comparison of Presyncope and End Syncope

In all cases there was a much greater drop in MBP than in MCBV, suggesting that CVR must be decreasing, as would be expected from an intact cerebrovascular autoregulation. Coincident with the reduction in CVR was an increase in PI, which was almost completely due to the drop in DCBV. Although not shown, the change in morphology of the spectral envelope of the TCD signals during syncope was entirely comparable to those published by other investigators.^{7 17 20}

	Discussion

Top Abstract Introduction Subjects and Methods Results Discussion References

 
The purpose of this study was to evaluate whether a derangement of cerebral autoregulation exists in patients with recurrent NMS. Autoregulation is defined as the intrinsic ability of the brain to maintain CBF during changes of arterial and cerebral perfusion pressure.²⁶ Many of the initial studies of cerebral autoregulation used radioactive tracer techniques that assume a quasi–steady state condition and hence are unable to assess rapid changes in CBF. TCD represents the only technology currently available that permits noninvasive prolonged monitoring of rapidly changing CBV. The latency to onset of dynamic autoregulation is very brief, and under certain conditions restoration of CBV may be complete within 5 seconds.²⁷ For example, rapid deflation of large cuffs previously placed around the upper thigh¹⁵ or performance of the Valsalva maneuver²⁸ may evoke a prolonged decrease in MBP but only a transient decrease in MCBV. The calculated CVR as defined by Ohm's law may serve as a useful index of this autoregulation.^{14 27 29}

We measured beat-to-beat changes in CBV, BP, and HR at rest and throughout HUT to the point of impending syncope. On the basis of the data cited above, we hypothesized that any impairment of dynamic cerebral autoregulation must manifest as an increase in calculated CVR, ie, as a decrease in CBV in excess of that expected from the rapid MBP reduction at syncope.⁸ CVR decreased in all patients and in one control subject who fainted during HUT, suggesting that the integrity of cerebrovascular autoregulation was maintained even when syncope was imminent. Our findings are also in accord with the observation of maintained cerebral oxygen saturation during HUT-induced central hypovolemia in normal control subjects until BP was critically reduced.³⁰

During syncope the rapid reduction in MBP was due to a decrease in both SBP and DBP. In contrast, the reduction in MCBV was almost entirely due to a decrease in DCBV, whereas SCBV did not change. The changes in CBV that we observed in our study agree completely with those reported previously by Grubb et al.¹⁷ These investigators inferred that cerebral vasoconstriction occurred during NMS because PI increased. If BP and HR are relatively stable, a rise in distal vascular resistance may increase flow pulsatility.^{26 31} In many instances, however, there is a clear divergence between PI and CVR. In an experimental rabbit model of syncope, drug-induced hypotension or hypotensive hemorrhage provokes a significant decrease in CVR and a concomitant increase in PI.³¹ Similarly, PI is increased during postprandial hypotension in the elderly³² and during orthostatic hypotension in patients with pandysautonomia,³³ although in both groups CVR is expected to decrease. Indeed, it is often remarked that because orthostatic tolerance is often maintained despite severe hypotension, these patients must maintain an intact cerebral autoregulation. Therefore, although under stable conditions a qualitative relationship does exist between pulsatility and CVR, it is doubtful that PI can serve as an adequate index of CVR during the rapid BP decrease of syncope.

Our data show that the rise in PI is due exclusively to a decrease in DCBV and occurs despite a sharp drop in calculated CVR. Severe hemorrhagic hypotension that provokes an electroencephalographic burst suppression is associated with a characteristic decrease in DCBV to zero.³⁴ Similarly, zero diastolic velocity or even diastolic flow reversal has been observed in some patients at syncope,⁷ during severe orthostatic hypotension,¹² and during cough syncope.¹³ None of our patients actually lost consciousness because for ethical reasons they were rapidly returned to the supine position once the typical hemodynamic profile of syncope was evident.⁵ It is likely, however, that the selective loss of diastolic flow in all cases is due to a common mechanism: collapse of downstream vessels as DBP decreases below the critical closing pressure of cerebral vessels.^{27 35 36} In these collapsible vessels, reduced flow is not a consequence of increased CVR but rather a sudden reduction in the driving force of cerebral perfusion pressure as arterial critical closing pressure exceeds cerebral venous pressure.³⁷ It is therefore to be expected that as cerebral perfusion pressure decreases, critical closing pressure is reached and the autoregulatory decrease in CVR that maintains flow will be unable to overcome the diminution of flow. Moreover, as critical closing pressure is reached pulsatility of flow will increase, although CVR does not change.³⁸ The downward trend of DCBV also suggests that critical closing pressure of all cerebral vessels is not uniform.

In conclusion, our data demonstrate that cerebrovascular autoregulation functions to significantly limit the reduction of CBF during syncope. Ultimately diastolic CBF will diminish as critical closing pressure of cerebral vasculature is reached, and loss of consciousness will occur. The reduction in diastolic CBF and increased PI can easily be explained without postulating a paradoxical increase in CVR or disordered cerebral autoregulation during syncope.^{5 17}

	Selected Abbreviations and Acronyms

 

BP = blood pressure CBF = cerebral blood flow CBV = cerebral blood velocity CO = cardiac output CVR = cerebrovascular resistance DBP = diastolic blood pressure DCBV = diastolic cerebral blood velocity HR = heart rate HUT = head-up tilt MBP = mean blood pressure MCBV = mean cerebral blood velocity MCA = middle cerebral artery NMS = neurally mediated syncope PI = pulsatility index SBP = systolic blood pressure SCBV = systolic cerebral blood velocity SV = stroke volume TCD = transcranial Doppler sonography TPR = total peripheral resistance

	Acknowledgments

 
This study was supported by grants from the CFIDS Association of America and the Fonds de la Recherche en Santé du Québec (Dr Schondorf).

	Footnotes

 
Reprint requests to Ronald Schondorf, PhD, MD, Department of Neurology, Sir Mortimer B. Davis Jewish General Hospital, 3755 chemin de la Côte Ste Catherine, Montreal, Quebec, Canada H3T 1E2.

Received February 26, 1997; revision received May 14, 1997; accepted May 14, 1997.

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