Orthostatic Tolerance, Cerebral Oxygenation, and Blood Velocity in Humans With Sympathetic Failure
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1 Orthostatic Tolerance, Cerebral Oxygenation, and Blood Velocity in Humans With Sympathetic Failure M.P.M. Harms, MD; W.N.J.M. Colier, PhD; W. Wieling, MD, PhD; J.W.M. Lenders, MD, PhD; N.H. Secher, MD, PhD; J.J. van Lieshout, MD, PhD 1 Background and Purpose Patients with orthostatic hypotension due to sympathetic failure become symptomatic when standing, although their capability to maintain cerebral blood flow is reported to be preserved. We tested the hypothesis that in patients with sympathetic failure, orthostatic symptoms reflect reduced cerebral perfusion with insufficient oxygen supply. Methods This study addressed the relationship between orthostatic tolerance, mean cerebral artery blood velocity (V mean, determined by transcranial Doppler ultrasonography), oxygenation (oxyhemoglobin [O 2 Hb], determined by nearinfrared spectroscopy), and mean arterial pressure at brain level (MAP MCA, determined by finger arterial pressure monitoring [Finapres]) in 9 patients (aged 37 to 70 years; 4 women) and their age- and sex-matched controls during 5 minutes of standing. Results Supine MAP MCA ( versus mm Hg) and V mean (84 21 versus cm s 1 ) were higher in the patients. After 5 minutes of standing, MAP MCA was lower in the patients (31 14 versus mm Hg), as was V mean (51 8 versus 59 9 cm s 1 ), with a larger reduction in O 2 Hb ( versus mol L 1 ). Four patients terminated standing after 1 to 3.5 minutes. In these symptomatic patients, the orthostatic fall in V mean was greater (45 6 versus cm s 1 ), and the orthostatic decrease in O 2 Hb ( versus mol L 1 ) tended to be larger. The reduction in MAP MCA was larger after 10 seconds of standing, and MAP MCA was lower after 1 minute (25 8 versus 40 6 mm Hg). Conclusions In patients with sympathetic failure, the orthostatic reduction in cerebral blood velocity and oxygenation is larger. Patients who become symptomatic within 5 minutes of standing are characterized by a pronounced orthostatic fall in blood pressure, cerebral blood velocity, and oxygenation manifest within the first 10 seconds of standing. (Stroke. 2000;31: ) Key Words: cardiac output hypotension, orthostatic posture ultrasonography, Doppler, transcranial When standing, humans adjust the cardiovascular system to the gravitational displacement of blood to the lower part of the body by increasing systemic vascular resistance through autonomic reflex activity, but patients with sympathetic failure lack this ability to modulate vascular tone in the upright body position. 1 3 Although their capability to maintain cerebral blood flow in response to a reduction in arterial pressure is reported to be preserved, 4 7 patients with sympathetic failure often develop symptoms such as lightheadedness and blurred vision when upright. We hypothesized that in patients with sympathetic failure, orthostatic symptoms reflect a reduced cerebral perfusion with an insufficiency of cerebral oxygen supply. Changes in cerebral tissue oxygenation can be assessed continuously and noninvasively by near-infrared spectroscopy (NIRS) This study addressed the relationship between orthostatic tolerance and estimates of cerebral perfusion in patients with sympathetic failure and healthy controls during orthostatic stress. The effect of standing on cerebral perfusion was evaluated by transcranial Doppler ultrasound (TCD) determined middle cerebral artery (MCA) mean blood velocity (V mean ) and by NIRS-determined cerebral oxygenation. Arterial pressure, central blood volume, and beat-to-beat cardiac output (CO) were measured to follow systemic circulatory responses. Subjects and Methods Subjects In 9 patients (age range, 37 to 70 years; 4 women), orthostatic hypotension was manifest as a fall 20 mm Hg in systolic arterial pressure and 5 mm Hg in diastolic pressure after 1 minute of standing. 11 Orthostatic hypotension was related to pure autonomic failure in 8 patients, while in 1 patient orthostatic intolerance was Received January 31, 2000; final revision received April 3, 2000; accepted April 12, From the Department of Internal Medicine, Academic Medical Center Amsterdam (M.P.M.H., W.W., J.J. van L.); Cardiovascular Research Institute, Amsterdam (M.P.M.H., W.W., J.J. van L.); Departments of Physiology (W.N.J.M.C.) and Internal Medicine (J.W.M.L.), University Hospital Nijmegen; and Department of Anesthesia, Copenhagen Muscle Research Center, Rigshospitalet, Copenhagen (N.H.S.), Denmark. Correspondence to J.J. van Lieshout, Department of Internal Medicine, Room F4-264, Academic Medical Center, University of Amsterdam, PO Box 22700, 1100 DE Amsterdam, Netherlands. j.j.vanlieshout@amc.uva.nl 2000 American Heart Association, Inc. Stroke is available at
2 Harms et al Cerebral Oxygenation in Sympathetic Failure 1609 TABLE 1. Patient Characteristics Patient Sex Disease Treatment BP Supine, mm Hg BP Standing, mm Hg Age, y Weight, kg Height, cm S1 M PAF None 156/68 97/ S2 M PAF HUT 175/101 76/ S3 F PAF None 175/99 85/ S4 F PAF NaCl/fludrocortisone 112/71 73/ S5 F PAF NaCl/fludrocortisone 163/98 75/ S6 M PAF Fludrocortisone 159/81 60/ S7 F PAF NaCl/fludrocortisone 145/92 74/ S8 M MSA Fludrocortisone/HUT 135/84 76/ S9 M PAF NaCl/fludrocortisone/HUT 192/102 68/ BP indicates blood pressure; PAF, pure autonomic failure; MSA, multiple system atrophy; HUT, sleeping 12 head-up tilt; and NaCl, dietary salt supplementation. subsequent to multiple system atrophy. No patient had symptoms or signs of organic heart disease (Table 1). Nine sex- (5 men) and age-matched (32 to 71 years) subjects with no orthostatic intolerance formed a control group. The protocol was approved by the ethics committee of the Academic Medical Center, and informed consent was obtained. Protocol At least 2 hours after a light breakfast without caffeine-containing beverages, the subjects were instrumented at 9 AM in a room with an ambient temperature of 22 C. A test run was performed to familiarize the subjects with the protocol. After 10 minutes of supine rest, the subjects were asked to stand in a relaxed position for 5 minutes. Standing was terminated if the subject developed symptoms of orthostatic intolerance such as blurred vision, dizziness, or nonresponsiveness. Measurements Cerebral oxygenation was monitored with NIRS. NIRS is based on the transparency of tissue to light in the near-infrared region and the O 2 status dependent changes in absorption in cerebral tissue caused by chromophores, ie, mainly oxyhemoglobin and deoxyhemoglobin (O 2 Hb and HHb, respectively). 12,13 With the use of a modified Lambert-Beer law, changes in light absorption at different wavelengths are measured, and tissue oxygenation is monitored. 14 To estimate the concentration changes in O 2 Hb and HHb, a differential path length factor of 6.0 was applied to account for the scattering of light in the tissue. 15,16 A continuous-wave NIRS instrument (Oxymon) with 3 wavelengths (901, 848, and 770 nm) and 10-Hz sampling time was used. The NIRS optodes were attached on the right side of the forehead, with the transmitting and receiving optodes placed 5.5 cm apart. Since there is no standard for cerebral oximetry, calibration is not possible. However, NIRS determined oxygenation changes in parallel with cerebral blood flow as determined by 133 Xe clearance, 17 and estimated cerebral O 2 saturation in humans during carotid clamping and declamping compares satisfactorily with jugular bulb venous O 2 saturation. 18 We therefore describe changes in O 2 Hb and HHb concentration (micromoles per liter), with supine control values as reference set at 0 mol L 1. Right MCA V mean was measured (Multidop X2, DWL) through the posterior temporal window. 19 Once the optimal signal-to-noise ratio was obtained, the probe was covered with an adhesive ultrasonic gel (Tensive, Parker Laboratories Inc) and secured with a head band. The V mean was obtained from the maximal TCD frequency shifts over 1 beat divided by the corresponding beat interval. As a reflection of PaCO 2, end-tidal CO 2 (PETCO 2 ) 20 was measured by an infrared CO 2 analyzer (Hewlett Packard 78345A). Arterial pressure was measured from the middle finger of the nondominant arm with a Finapres model 5 (Netherlands Organization for Applied Scientific Research, TNO-Biomedical Instrumentation). Finapres is based on the volume clamp method of Peñáz and the Physiocal criteria of Wesseling et al 21 and reflects blood pressure changes under conditions of orthostatic stress and arterial hypotension The cuffed finger was fixed in the anterior axillary line at heart level, maintaining a fixed distance to the TCD probe. Beat-to-beat changes in stroke volume were estimated by modeling flow from arterial pressure (Modelflow, TNO-Biomedical Instrumentation). This method computes an aortic flow waveform from a peripheral arterial pressure signal using a nonlinear 3-element model of the aortic input impedance. Peripheral arterial pressure appears sufficiently close to the aortic pressure to be applied in the model and to allow for reliable estimations of stroke volume (SV) from an arterial pressure signal. 25,26 Thus, SV is tracked from peripheral arterial pressure in patients with cardiovascular disease, 25 with septic shock, 26 and under conditions of orthostatic stress with a limited offset of 3 9 ml in comparison to a thermodilution-based estimate. 27,28 As an index of the central blood volume, thoracic electric impedance (TI) 29 was measured by an impedance cardiograph (Kardio-Dynagraph, Diefenbach GmbH). An event marker identified changes in posture. Data Acquisition and Analysis The signals of arterial pressure, the spectral envelope of MCA velocity, TI, PETCO 2, and marker were analog/digital converted at 100 Hz and stored on hard disk for off-line analysis. NIRS data were sampled at 10 Hz. Signals were routed through an interface providing electric isolation with offset and sensitivity adjustments when appropriate. Variables were also recorded on a polygraph on a thermo-writer (Graphtec WR7700, Western Graphtec Inc) for online inspection. The V mean was computed as the integral of the maximal frequency shifts over 1 beat divided by the corresponding beat interval. Mean arterial pressure (MAP) was the true integral of the arterial pressure wave over 1 beat divided by the beat interval. MAP at the MCA level (MAP MCA ) was calculated from MAP measured at heart level and the vertical finger-to-tcd probe distance. 30 Heart rate (HR) was computed as the inverse of the interbeat pressure interval and expressed in beats per minute. CO was the product of SV and HR, and total peripheral resistance (TPR) was MAP at heart level divided by CO. To allow for comparisons, beat-to-beat data were transformed to equidistantly resampled data at 2 Hz by polynomial interpolation. 31 Blood pressures, HR, V mean,petco 2, and TI are expressed in absolute values. Resting supine values for SV, CO, and TPR were set at 100% (control), and changes were expressed in percentages from control. Control values were the average of 60-second supine rest before standing. In the standing position, 20-second averages were calculated. Variables were tested for normality and are expressed as mean and SD or median with range. Responses to standing were examined by Friedman s repeated-measures ANOVA on ranks. Significant F
3 1610 Stroke July 2000 Figure 1. Cardiovascular and cerebral perfusion and oxygenation responses to standing in patients with sympathetic failure vs control subjects. The supine resting values (from 60 to 0 seconds) and the first (from 0 to 60 seconds) and the last minute of standing (from 60 to 0 seconds) are shown. Boxes indicate standing; bold lines, patients; and thin lines, healthy controls. ratios were subjected to Dunn s test to locate significant differences. Differences between patients and controls and between symptomatic and asymptomatic patients were analyzed by parametric or nonparametric tests where appropriate. A P value 0.05 was considered to indicate a statistically significant difference. Results Patients Versus Controls The control subjects tolerated standing without complaints. Orthostatic tolerance varied considerably between patients; 5 patients tolerated 5 minutes of standing without symptoms (asymptomatic), but 4 patients developed orthostatic complaints after 1 to 3.5 minutes of standing (symptomatic). In the supine position, blood pressure was higher in the patients but dropped during standing. The orthostatic fall in CO and MAP MCA was larger in the patients because of absence of an increase in TPR. Resting HR did not differ between the 2 groups, and on standing HR increased to a comparable magnitude. Additionally, the resting TI and its orthostatic changes were similar in the 2 groups of subjects. Resting PETCO 2 was comparable for patients and control subjects but became lower in the patients during standing. Supine MCA V mean was higher in the patients and decreased on standing but not in the controls. At the end of standing, the fall in O 2 Hb was larger in the patients. HHb increased in both groups, with the larger increase in the patients (Figures 1 and 2, Table 2). In the patients the correlation coefficient for MAP MCA and MCA V mean was 0.68 and for CO and MCA V mean was 0.48 (P 0.05). The correlation coefficient for MAP MCA and O 2 Hb was 0.41 and for CO and O 2 Hb was 0.36 (P 0.05). In the Figure 2. Relationship between MAP, CO, and cerebrovascular variables during standing in patients vs controls. The postural reductions during 2 minutes of standing in V mean and O 2 Hb and their relation to changes in MAP MCA and CO in patients and their controls are shown. Closed circles indicate patients; open circles, controls; closed line, regression patients; and dashed line, regression controls. control subjects these values for MAP MCA and MCA V mean were 0.18, for CO and MCA V mean 0.25, for MAP MCA and O 2 Hb 0.06, and for CO and HbO Asymptomatic Versus Symptomatic Patients In symptomatic patients supine blood pressure was higher, but V mean did not differ. In symptomatic patients the reduction in MAP MCA was greater after 10 and 30 seconds of standing. After 1 minute of standing the reduction in MAP MCA was versus mm Hg in asymptomatic patients, and it was accompanied by a slightly lower CO. In the symptomatic patients the orthostatic fall in V mean was larger, with a tendency for a larger postural reduction in O 2 Hb and a lower PETCO 2. There was a tendency toward a larger TI in symptomatic patients (Figure 3, Tables 3 and 4). Figure 4 shows representative examples of the reduction in V mean and O 2 Hb during standing in a control subject and in an asymptomatic versus a symptomatic patient. Discussion This study demonstrates that during orthostatic stress, the reduction in cerebral blood velocity and oxygenation in patients with sympathetic failure is larger than in healthy subjects. Patients who develop serious orthostatic complaints within 5 minutes of standing are characterized by a more pronounced orthostatic fall in blood pressure, cerebral blood velocity, and oxygenation manifest within 10 seconds of standing. This report quantifies the postural changes in cerebral artery blood velocity and oxygenation, as measured by TCD and NIRS, in patients with sympathetic failure. TCD is used to evaluate cerebrovascular dynamics, including its autoregulation, 32,33 in patients with sympathetic failure as well. 34,35 The diameter of the MCA remains constant over an
4 Harms et al Cerebral Oxygenation in Sympathetic Failure 1611 TABLE 2. Cardiovascular and Cerebral Perfusion and Oxygenation Responses in Patients vs Controls V mean,cm s 1 Supine Stand 60 s End of Standing Patients * 51 8* Controls MAP MCA,mmHg Patients * 31 14* Controls * 72 14* MAP heart,mmhg Patients * 52 13* Controls * O 2 Hb, mol L 1 Patients * * Controls * * HHb, mol L 1 Patients * * Controls * * PETCO 2,mmHg Patients * 33 6* Controls * 35 4 HR, bpm Patients 66 (49 79) 79 (63 105)* 81 (69 103)* Controls 60 (46 70) 75 (61 86)* 81 (68 93)* SV, % Patients (36 98)* 52 (41 66)* Controls (57 80)* 66 (46 80)* CO, % Patients (57 89)* 65 (46 84)* Controls (73 90)* 90 (73 104) TPR, % Patients (48 88)* 76 (48 101)* Controls ( )* 122 (99 142)* TI, Patients * 64 10* Controls * 65 12* MAP heart indicates mean arterial pressure at heart level. *P 0.05 in comparison to supine. P 0.05, patients vs controls. P 0.05, end of standing vs stand 60 s. 30 mm Hg range of blood pressure, with V mean reflecting changes in cerebral blood flow. 36 This requirement is considered to be fulfilled in upright healthy subjects given the relatively small changes in arterial pressure at brain level. It is, however, uncertain whether the MCA diameter remains stable at the low blood pressure levels developed in patients with sympathetic failure. Cerebral perfusion pressure decreases from the supine to the upright position. 37 In this study the reduction in cerebral blood velocity was accompanied by a fall in cerebral oxygenation under circumstances of considerable orthostatic hypotension. We consider that the fall in cerebral blood velocity and oxygenation was accompanied by complaints of cerebral hypoperfusion in the symptomatic Figure 3. Cerebral perfusion during standing in symptomatic vs asymptomatic patients. The supine resting values (from 60 to 0 seconds) and the first (from 0 to 60 seconds) and the last minute of standing (from 60 to 0 seconds) are shown. Boxes indicate standing; bold lines, symptomatic patients; and thin lines, asymptomatic patients. patients at a reduced arterial pressure and CO. We may speculate that under those circumstances the excessive fall in blood pressure might reduce the diameter of the MCA cerebral velocity and overestimate cerebral blood flow, 38 but the data regard changes in blood velocity, not flow, and cannot be said to reflect a decrease in flow, however suggestive. Given a constant arterial O 2 content, the cerebral tissue O 2 supply is predominantly a function of cerebral arterial blood flow. NIRS follows changes in cerebral oxygenation in parallel with cerebral blood flow as determined by 133 Xe clearance, 17 and estimated cerebral O 2 saturation in humans during carotid clamping and declamping compares satisfactorily with jugular bulb venous O 2 saturation. 18 The determination of cerebral tissue oxygenation by NIRS reflects the locally monitored cerebral cortex. Within the sampled volume, hemoglobin is contained in arterioles, capillaries, and venules, and the relative position of pigments determined by NIRS is unknown. From anatomic studies of brains, the ratio of venule to total vessel volume ranges from 2/3 to 4/5. 39 Only 5% of the blood is situated in the capillaries and 20% in the arterioles, and it may be argued that NIRS determines local SvO 2 rather than tissue O 2 content. Yet, resting values of O 2 Hb are higher than internal jugular SvO Thus, the O2Hb of the cerebral tissue measured by NIRS is not necessarily equal to the region perfused by the MCA, and it may be questioned whether the fall in the NIRS O 2 Hb signal can be taken to reflect a fall in MCA territory perfusion. In this study the reduction in MCA blood velocity was accompanied by a fall in cerebral oxygenation under circumstances of considerable orthostatic hypotension. We consider that during head-up tilt in healthy subjects, even when the reduction in MAP is limited, cerebrovascular oxygenation is related to cerebral perfusion, as determined by TCD, 13,40 and that NIRS properly reflects the reduction in O 2 Hb associated with fainting. 12 Comparable results have
5 1612 Stroke July 2000 TABLE 3. Cardiovascular and Cerebral Perfusion and Oxygenation Responses in Sympathetic Failure Supine Stand 60 s End of Standing MAP MCA,mmHg Symptomatic * (110 to 134) 25 8* (14 to 33) 19 4* (14 to 23) Asymptomatic 99 9 (85 to 108) 40 6 (34 to 47) (27 to 56) V mean,cm s 1 Symptomatic (64 to 123) 45 6*(39 to 53) 44 2* (42 to 47) Asymptomatic (68 to 114) (53 to 77) 56 7 (49 to 62) O 2 Hb, mol L 1 Symptomatic ( 15.6 to 7.8) ( 16.9 to 9.1) Asymptomatic ( 12.1 to 4.4) ( 14.7 to 4.2) HHb, mol L 1 Symptomatic (4.7 to 8.2) (5.1 to 10.9) Asymptomatic (1.1 to 6.9) (3.7 to 9.9) PETCO 2,mmHg Symptomatic 36 2 (32 to 38) 31 4 (25 to 35) 31 5 (25 to 35) Asymptomatic 38 8 (26 to 46) 36 8 (22 to 44) 35 6 (27 to 42) HR, bpm Symptomatic 70 5 (62 to 74) 76 6 (73 to 83) 76 6 (71 to 83) Asymptomatic (49 to 79) (63 to 105) (69 to 103) CO, % Symptomatic (57 to 82) (46 to 67) Asymptomatic (65 to 89) (57 to 84) TI, Symptomatic (56 to 89) (58 to 89) (60 to 89) Asymptomatic 55 7 (47 to 66) 61 4 (57 to 67) 62 5 (55 to 67) Values are mean SD (range). *P 0.05, symptomatic vs asymptomatic patients. been obtained during lower body negative pressure 41,42 and centrifuge studies. 43 At rest, blood pressure was elevated in the patients but fell considerably on standing because of a large reduction in SV and CO unopposed by an increase in TPR (Table 2 and Figure 1). The large reduction in V mean and O 2 Hb indicates that with a fall in arterial pressure of this magnitude, autoregulatory mechanisms are not capable of preventing a symptomatic decrease in cerebral perfusion, as reflected by TCD and NIRS. Apart from the considerable fall in blood pressure and CO (Figure 2), the reduction in PETCO 2 may also have contributed to the reduction in MCA V mean. 44 On standing, in healthy subjects a slight decrease in PETCO 2 is common 45 and can be explained by an increase in breathing rate in the upright position and changes of the ventilation-perfusion relationship. 46 TABLE 4. Cerebral Perfusion and Oxygenation Responses to Orthostatic Stress (First 30 Seconds) in Sympathetic Failure Duration of Standing 10 s 20 s 30 s MAP MCA,mmHg Symptomatic 60 13* ( 69 to 40) ( 88 to 61) 86 10* ( 97 to 73) Asymptomatic ( 45 to 12) ( 73 to 42) ( 80 to 42) V mean,cm s 1 Symptomatic ( 34 to 5) ( 56 to 4) ( 70 to 13) Asymptomatic ( 22 to 3.9) ( 34 to 9) ( 42 to 4) O 2 Hb, mol L 1 ) Symptomatic ( 7.0 to 1.7) ( 12.5 to 2.7) ( 10.5 to 4.7) Asymptomatic ( 4.0 to 1.4) ( 12.8 to 0.2) ( 12.4 to 1.1) Values are mean SD (range). Changes are in comparison to supine baseline values. *P 0.05, symptomatic vs asymptomatic patients.
6 Harms et al Cerebral Oxygenation in Sympathetic Failure 1613 dependent on venous return and the effective blood volume. 49,54 There is no specific treatment for sympathetic vasomotor failure, and therapy should be focused on alleviating the patient s orthostatic tolerance and reducing the orthostatic fall in CO by increasing the circulating volume. 50,55 Acknowledgment Dr Harms is a research fellow supported by the Netherlands Heart Foundation (grant ). Figure 4. Magnitude and time course of orthostatic reduction in cerebral blood velocity and oxygenation. Original tracings of arterial blood pressure (BP), cerebral blood velocity (CBV), and changes in O 2 Hb in a control subject (left), an asymptomatic patient (middle), and a symptomatic patient (right). With the subject standing, BP drops considerably; the decrease in V mean and O 2 Hb tends to be larger for patients during an equivalent period of standing. In symptomatic patients the rapidity of the reduction in CBV and oxygenation seems to already be larger during the first 30 seconds of standing. In subjects with orthostatic hypotension due to sympathetic failure, orthostatic tolerance varies considerably, but the underlying mechanism is not well understood. 47 In symptomatic recumbent patients, blood pressure but not MCA V mean was higher, suggesting a shift in the relationship between cerebral perfusion pressure and blood velocity comparable to that in chronic hypertensive patients. 48 The differences in MCA V mean between symptomatic and asymptomatic patients were relatively small (Table 3), but the effects on orthostatic tolerance were dramatic. We believe that when these patients are upright, cerebral blood flow is close to the critical lower level of cerebral perfusion, and an additional small reduction elicits symptoms of cerebral hypoperfusion. This is supported by a recognizably larger fall to lower values in blood pressure and MCA V mean in symptomatic patients, with cerebral oxygenation following this pattern. In patients with sympathetic failure, the postural fall in arterial pressure is amplified by the larger orthostatic fall in CO (Figure 1 and Table 2) because of enhanced venous pooling of blood, with an excessive reduction of venous return. 49,50 This is compatible with the tendency for higher values for thoracic electric impedance in symptomatic patients, suggesting a smaller central blood volume (Table 3). 29 In addition, the decrease in PETCO 2 on standing may have contributed to the cerebral hypoperfusion in the symptomatic patients. The fall in blood pressure, cerebral blood velocity, and oxygenation in the symptomatic patients was larger in the first 10 seconds of standing (Table 4 and Figures 3 and 4), suggesting that the rapidity of the reduction also contributes to trigger orthostatic symptoms. 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