Vol. 91, Issue 5, 2199-2204, November 2001
Changes in cerebral oxygenation and blood flow during LBNP in
spinal cord-injured individuals
Sibrand
Houtman1,
Jorge M.
Serrador2,
Willy N. J. M.
Colier1,
Derek W.
Strijbos1,
Kevin
Shoemaker2, and
Maria T. E.
Hopman1
1 Department of Physiology, University Medical Center
Nijmegen, 6500 HB Nijmegen, The Netherlands; and
2 Neurovascular Research Laboratory, School of
Kinesiology, University of Western Ontario, London, Ontario, Canada
N6A 3K7
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ABSTRACT |
Spinal cord-injured (SCI) individuals,
having a sympathetic nervous system lesion, experience hypotension
during sitting and standing. Surprisingly, they experience
few syncopal events. This suggests adaptations in cerebrovascular
regulation. Therefore, changes in systemic circulation, cerebral
blood flow, and oxygenation in eight SCI individuals were compared with
eight able-bodied (AB) individuals. Systemic circulation was
manipulated by lower body negative pressure at several levels down to
60 mmHg. At each level, we measured steady-state blood pressure,
changes in cerebral blood velocity with transcranial Doppler, and
cerebral oxygenation using near-infrared spectroscopy. We found
that mean arterial pressure decreased significantly in SCI but not in
AB individuals, in accordance with the sympathetic impairment in the
SCI group. Cerebral blood flow velocity decreased during orthostatic stress in both groups, but this decrease was significantly greater in
SCI individuals. Cerebral oxygenation decreased in both groups, with a
tendency to a greater decrease in SCI individuals. Thus present data do
not support an advantageous mechanism during orthostatic stress in the
cerebrovascular regulation of SCI individuals.
tetraplegia; postural syncope; lower body negative pressure
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INTRODUCTION |
SPINAL
CORD-INJURED (SCI) individuals have part of their sympathetic
nervous system isolated from brain stem control. Consequently, SCI individuals show a lesser or absent increase of sympathetic activity during orthostatic challenges (41), thus
impairing vasoconstriction in the legs and splanchnic area below the
level of the lesion. Resting blood pressure in individuals with
tetraplegia is lower than in able-bodied (AB) individuals
(9). Furthermore, during head-up tilt, blood pressure
(7) and stroke volume (4) settle at lower
values in SCI compared with AB individuals. Despite the greater fall of
blood pressure during orthostatic stress in SCI individuals, they seem
to have a surprisingly low incidence of syncope (30). This
suggests that cerebral blood flow (CBF) is maintained during lowered
blood pressure and has thus raised the idea of an improved
cerebrovascular regulation in SCI individuals (30).
Few studies have reported on cerebral circulation in SCI individuals.
Gonzalez and co-workers (13), using transcranial Doppler, reported that in orthostatic tolerant and intolerant individuals with
tetraplegia, cerebral autoregulation, and not maintenance of systemic
blood pressure, was crucial in the prevention of syncope symptoms
during head-up tilt. However, Gonzalez et al. made no comparison with
AB individuals. Nanda and co-workers (31), using 133Xe, reported similar cerebral autoregulation in SCI and
AB individual, but they manipulated blood pressure by comparing sitting
with supine position, which may bear relevance for everyday life but may not have been enough of a challenge to the circulation to reveal
differences between groups. In addition, the 133Xe
technique does not discriminate between intra- and extracranial circulation. Therefore, conclusive evidence for an improved cerebral autoregulation in SCI individuals is lacking.
Nevertheless, the fact that SCI individuals show normal orthostatic
tolerance, despite lowered blood pressure during orthostatic stress,
deserves further study. It has been argued that the sympathetic nervous
system may increase cerebral vascular resistance during orthostatic
stress in healthy individuals (12, 24, 28). Previous
studies indicate that sympathetically mediated cerebral vasoconstriction is at least in part mediated through the upper cervical ganglia. These upper cervical ganglia receive preganglionic innervation emerging from the first to fourth thoracic spinal cord
segment (37). Consequently, SCI individuals with these, or
higher, lesion levels may lack the disadvantageous increase in
cerebrovascular resistance during orthostatic stress, thus contributing
to the remarkable orthostatic tolerance in SCI individuals.
Although most studies on orthostatic tolerance assessed cerebral flow
by use of the 133Xe or transcranial Doppler method,
cerebral oxygenation is the final common pathway leading to syncope.
Cerebral oxygenation may be assessed using near-infrared spectroscopy
(NIRS) (35) and may thus present additional information on
the maintenance of an adequate cerebral perfusion.
The aim of this study was to compare lower body negative pressure
(LBNP)-induced changes in systemic circulation and cerebral flow
velocity (CFV) and oxygenation between SCI and AB individuals. We
hypothesized that SCI individuals would not increase cerebrovascular resistance (CVR) during orthostatic stress as observed in AB
individuals and that this lack of cerebral vasoconstriction might
compensate for the greater fall in blood pressure in SCI individuals,
thus resulting in a similar decrease in cerebral oxygenation in both groups.
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MATERIALS AND METHODS |
Ten SCI and ten AB individuals matched for gender (9 men, 1 woman), weight, and age participated in this study after an informed consent was signed. All spinal cord lesions were caused by trauma >2
yr previously. Eight of the lesions were above T1, two at
T4. All spinal cord lesions were complete except for one
individual with a C5-C6 lesion, who had some
sensitivity in the right leg but no voluntary motor control (classified
as American Spinal Injury Association B). None of the participants
suffered from cardiovascular diseases or hypertension, nor did any
participant suffer from orthostatic intolerance. Three SCI individuals
used baclofen to minimize muscle spasms. The Faculty Ethics Committee of the University of Nijmegen Medical Center approved the study.
Protocol.
The experiment started after ~20 min of supine rest. The
participant's lower body, i.e., distally from the iliac crest, was positioned in a homebuilt LBNP box. During this period, data collection instruments were connected and calibrated. Participants were not allowed to speak, sleep, or move during the experiment. The
experimental protocol consisted of multiple stepwise decreases of the
barometric pressure inside this LBNP box, as depicted in Fig.
1. Each LBNP level lasted 5 min to allow
development of a steady-state response. Three recovery or baseline
periods, two lasting 10 min and one lasting 5 min, were scheduled.
During the 10-min baseline measurements, participants were allowed to
speak and move a little from minutes 3 to 5. The
major advantage of the protocol used lies in the fact that the repeated
maneuvers analyzed with a repeated measures ANOVA decreases the type 2 error.
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Fig. 1.
Scheme showing lower body negative pressure (LBNP)
stages. The last 2 min of each level of LBNP were used for data
analysis.
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Measurements.
Mean arterial pressure (MAP) and heart rate were measured continuously
with Portapres (TNO-BMI, Amsterdam, The Netherlands), the portable
version of Finapres. This instrument samples finger arterial pressure
at 200 Hz on the basis of the method of Penaz. It has been
shown that changes in arterial blood pressure are accurately reflected
by Finapres and Portapres during orthostatic challenges
(21). Stroke volume and cardiac output were calculated off-line using Modelflow, a pulse contour method described by Wesseling
and co-workers (44, 45). This method requires
knowledge of the compliance of the individual's aorta, which may be
estimated from information on the height, weight, gender, and age of
each subject. However, because our main interest was to examine the LBNP-induced alterations, all cardiovascular variables calculated by
Modelflow during LBNP were expressed relative to the baseline measurement directly before the LBNP. Modelflow has been
reported to calculate changes in stroke volume very accurately from
Portapres blood pressure data (16).
CFV was measured in the middle cerebral artery using transcranial
Doppler (Medasonics, Newark, NJ), with a 2-MHz pulsed flat probe
located over the temporal bone. The middle cerebral artery was gated to
a depth of 45-60 mm. The probe was attached with Velcro headbands
for the duration of the test after an optimum signal was found. The
transcranial Doppler signal was sampled at 10 kHz. Off-line data
analysis was performed with customized data analysis software
(25). The peak velocity envelope of the transcranial
Doppler waveform was taken to represent the instantaneous CFV of the
middle cerebral artery.
During the entire experiment, cerebral oxygenation was assessed by
measuring changes in oxy- and deoxyhemoglobin concentration ([O2Hb] and [HHb], respectively) using NIRS. NIRS
monitors changes in light absorption of tissue in vivo, which is mainly
caused by oxygenation-dependent [O2Hb] and [HHb]
changes. The sum of [O2Hb] and [HHb] changes represents
a measure of the total blood volume ([tHb]) change in the monitored
tissue, whereas the difference between [O2Hb] and [HHb]
changes is a measure of tissue oxygenation {oxygenation index
([OI])} (2). This noninvasive method has been
described in greater detail in earlier studies (2, 3) and
has been reported to reflect the changes in cerebral oxygenation accurately (35). Optodes were placed above the
left eyebrow, using an interoptode distance of 55 mm. This optode
distance ensures a deep enough penetration of the near-infrared light
into the frontal lobe cortex to exclude significant influence of
extracranial circulation (10, 17). A pathlength factor of
six was used. The NIRS equipment (Oxymon, Depts. of Physiology and
Instrumentation, Univ. of Nijmegen, Nijmegen, The Netherlands) used was
a three-wavelength, continuous-wave instrument (43). NIRS
data were sampled at 10 Hz, displayed in real time, and stored on disk
for off-line analysis. The NIRS optodes were firmly fixed to the
forehead to avoid movement artifacts.
Respiratory rate and the end-tidal PCO2
(PETCO2) were measured using a combined
capnograph-pulse oximeter (model N1000, Nellcor-Puritan Bennet, Tucson, AZ).
Analysis.
All data of the measured variables during the different levels of LBNP
and recovery or baseline periods were averaged over the last 2 min of
each period, provided a steady state existed. Variables obtained during
different levels of LBNP were expressed as change from the previous
recovery or baseline level in absolute ([OI], [tHb]) or relative
(MAP, stroke volume, cardiac output, CFV) units. MAP, heart rate, and
PETCO2 were expressed as the actual
absolute values. An indication of the change in regional CVR in the
distribution of the middle cerebral artery was calculated as
Statistics.
All variables were normally distributed. The effect of LBNP on measured
variables was evaluated within and between groups using a
repeated-measures ANOVA.
The differences between no LBNP and the nine stages with LBNP in
circulatory and cerebral oxygenation variables were tested post hoc to
be different from 0 (95% confidence interval). Also, differences
between 0 mmHg and the nine stages with LBNP in SCI and AB were
evaluated post hoc using a Student's t-test, with a
P value <0.05 being taken to indicate a significant
difference. Significant differences found with these post hoc tests are
indicated in the figures.
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RESULTS |
Initially, 10 SCI and 10 AB individuals participated in this
study. However, two SCI individuals with lesions above T1
and two AB individuals fainted during the first stage of 45 mmHg LBNP, resulting in a premature end of those experiments. The results of these
individuals were completely omitted from further analysis because we
were interested in the mechanism behind orthostatic tolerance.
Consequently, results are based on eight SCI [age 32 ± 6 (SE)
yr; weight 69 ± 14 kg] and eight AB individuals (age 34 ± 10 yr; weight 76 ± 10 kg).
Stroke volume decreased significantly with increasing LBNP
(P < 0.001), indicating that the orthostatic stress
impaired venous return. The relative change in stroke volume was
similar in both groups (Fig. 2). The
increase in heart rate during LBNP, similar in both groups, did not
fully compensate for the decrease in stroke volume. Consequently,
cardiac output decreased (P < 0.001) by a similar
percent in both groups during LBNP (up to 14 ± 13 and 12 ± 14% in SCI and AB individuals, respectively, during 60 mmHg LBNP;
Fig. 2).
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Fig. 2.
Percent change ( ) in stroke volume and cardiac output
secondary to LBNP manipulation for able-bodied (AB) and spinal
cord-injured (SCI) individuals. Values are means ± SE. * SCI
significantly different from baseline, P < 0.05. # AB significantly different from baseline,
P < 0.05.
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MAP during 0 mmHg LBNP increased over the consecutive recovery or
baseline periods in AB individuals (from 82 ± 13 to 89 ± 11 mmHg; P = 0.01) and tended to rise in SCI individuals
(79 ± 12 to 97 ± 19 mmHg; P = 0.08) (Fig.
3, top). The other variables, including heart rate, did not show a significant gradual change in any
group during the experiment. The effect of LBNP on MAP was different in
each group (P = 0.009): during LBNP, MAP decreased in
six of eight SCI individuals but remained stable or increased in AB
individuals (Fig. 3, bottom).
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Fig. 3.
Averaged mean arterial pressure (MAP; top) and
the averaged changes in MAP relative to the 0 mmHg LBNP levels
(bottom) secondary to LBNP manipulation for AB and SCI
individuals. Values are means ± SE. * SCI significantly
different from baseline, P < 0.05. # AB
significantly different from baseline, P < 0.05.  Significant difference between groups,
P < 0.05.
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During LBNP, PETCO2 decreased in both AB
and SCI individuals (P < 0.001), and no difference
between groups was found. In AB individuals,
PETCO2 decreased from 5.4 ± 0.4 kPa
during 0 mmHg LBNP to 5.0 ± 0.3 kPa during 60 mmHg LBNP; in SCI
individuals, it decreased from 5.3 ± 0.5 kPa to 4.9 ± 0.6 kPa.
The CFV was assessed successfully in six of the eight SCI and matched
AB individuals. The baseline CFV was 65 ± 17 and 54 ± 11 cm/s in AB and SCI individuals, respectively. CFV of middle cerebral
artery decreased (P = 0.004) during orthostatic stress in SCI and AB individuals (Fig. 4). The
CFV decreased more in SCI than in AB individuals (P = 0.04) during LBNP. The CVR downstream the middle cerebral artery
increased in both AB and SCI individuals during LBNP (P < 0.001).
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Fig. 4.
Percent change in the middle cerebral artery flow
velocity (CFV) and regional cerebrovascular resistance (CVR) secondary
to LBNP manipulation for AB and SCI individuals. Values are means ± SE. * SCI significantly different from baseline,
P < 0.05. # AB significantly different
from baseline, P < 0.05. Significant difference between groups,
P < 0.05.
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LBNP caused cerebral [OI] to decrease in both AB and SCI individuals
(P = 0.006; Fig. 5), and
this decrease, although not quite significantly different
(P = 0.08), tended to be larger in SCI than AB
individuals. Whereas cerebral [OI] decreased to 4.9 ± 3.3 and
9.2 ± 7.1 µmol/l in AB and SCI individuals, respectively, [tHb] decreases were smaller and similar in AB (down to 1.5 ± 1.9 µmol/l) and SCI individuals (down to 2.3 ± 1.9 µmol/l)
(Fig. 5).
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Fig. 5.
Averaged changes in oxygenation index ([OI]) and total
hemoglobin concentration ([tHb]) secondary to LBNP manipulation for
AB and SCI individuals. Values are means ± SE. * SCI
significantly different from baseline, P < 0.05. # AB significantly different from baseline,
P < 0.05.
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DISCUSSION |
To explain the remarkable orthostatic tolerance despite a lowered
blood pressure in SCI individuals, we hypothesized that SCI individuals
would show reduced cerebral vasoconstriction during orthostatic stress.
However, both AB and SCI individuals increased CVR, and, consequently,
cerebral oxygenation tended to a greater decrease in SCI than in AB
individuals during LBNP.
Cardiovascular responses.
Stroke volume and cardiac output decreased during LBNP in accordance
with findings reported for AB (1) and by a similar extent
in both groups (Fig. 2), suggestive of a similar orthostatic challenge
in both groups. A previous study (20) reported a similar decrease in cerebral [OI], despite great differences in MAP in AB and
SCI individuals during head-up tilt, thus supporting present hypothesis. However, this study (20) was exploratory and
therefore less well controlled. For example, the orthostatic stress
indicated by the change in stroke volume was different between groups,
which may have affected the results.
MAP during rest periods (0 mmHg LBNP) increased during the experiment
in AB individuals and tended to do so in SCI individuals (Fig. 3,
top), which was confirmed with manually measured blood pressure. The blood pressure rise in AB individuals may have been caused by increasing plasma renin, vasopressin, and norepinephrine levels secondary to repetitive orthostatic stress without enough recovery time (33). In SCI individuals, the gradual
increase in blood pressure is most likely explained by an increase in
plasma renin independent from the sympathetic nervous system
(22, 23).
The changes in MAP during LBNP seemed fairly repeatable (Fig. 3,
bottom). MAP remained stable or increased slightly in AB individuals during LBNP (Fig. 3, bottom), as has been
reported by others (1), but decreased in SCI individuals.
Regarding the similar changes in cardiac output (Fig. 2), this may be
explained by the sympathetically mediated vasoconstriction in AB but
not in SCI individuals during the orthostatic challenge evoked by LBNP.
This decreased ability of SCI individuals with a lesion above
T4 to maintain blood pressure during orthostatic challenges is well documented (7, 14, 22, 30). However, SCI
individuals showed great variation in the measured responses to LBNP.
This is a common finding in SCI individuals and is probably due to the
great variation in the exact lesion. Because this variation seemed
independent of lesion level or medication, SCI individuals were
regarded as one group.
CBF.
Because the middle cerebral artery does not appear to change in
diameter during LBNP or arterial PCO2
(PaCO2) manipulation (12, 40), relative
changes in cerebral blood flow may be calculated from changes in
erythrocyte velocity (26).
In AB individuals, CFV decreased in the face of a maintained or
increased MAP during LBNP, whereas SCI individuals, in contrast to our
expectations, showed similar cerebral vasoconstriction in addition to a
falling perfusion pressure (i.e., MAP), resulting in a greater fall in
CFV than in AB individuals.
In healthy individuals, CVR has been found to increase during
orthostatic stress, causing a decrease in cerebral flow. From these
findings, it was hypothesized that this vasoconstriction may be caused
by the sympathetic nervous system (12, 28). Jordan and
co-workers (24) decreased sympathetic activity, using phentolamine, in individuals with idiopathic orthostatic intolerance and found increased CBF during head-up tilt and improved orthostatic tolerance. Recently, Sandor (38) suggested that the
sympathetic nervous system effect on the cerebral circulation may have
been grossly underestimated. Thus the CVR increase in AB individuals may have been caused by sympathetic activity, which is not fully compensated by cerebral autoregulation. In accordance with neuroanatomy (37, 38), earlier reports suggested that sympathetic
nerves pass through the upper paravertebral ganglia (42)
before reaching the cerebral vessels. Thus we hypothesized that, in
contrast to AB individuals, the brain stem cannot induce a
sympathetically mediated vasoconstriction in the cerebral vessels of
SCI individuals. However, assuming intact cerebral autoregulation in
SCI individuals (46), the calculated CVR in the present
study suggest reasonably similar changes in cerebral vasoconstriction
in both groups (Fig. 4). Therefore, the observed cerebral
vasoconstriction in SCI individuals may be caused by sympathetic fibers
that short circuit the cervical ganglia (37), or,
alternatively, cerebral vasoconstriction in SCI individuals could
conceivably be caused by the altered endocrine response to orthostatic
stress (22, 23, 29, 39).
The small decreases in PETCO2, reflecting
PaCO2, during LBNP were very similar in both groups.
Obviously, because changes in PaCO2 in the present
study occurred simultaneously with orthostatic stress, the pressure and
PaCO2 effects could not be differentiated. Even small
changes in PaCO2 may affect CBF (36).
However, assuming a normal PaCO2 responsiveness
(31, 32, 46) in SCI individuals [although some reports
have suggested an attenuated (5, 6, 8, 27, 34)
PaCO2 responsiveness in the broader group of individuals with a sympathetic nervous system impairment], the effect
of the decreased PETCO2 during LBNP has
probably been similar in both AB and SCI individuals.
Cerebral oxygenation.
Cerebral [OI] decreased during LBNP in both AB and SCI individuals.
This decrease, although not significant, tended to be greater in SCI
than in AB individuals (P = 0.08). In previous studies,
our laboratory found similar decreases of cerebral oxygenation in
syncope-free SCI (20) and AB (19, 20)
individuals during head-up tilt. The changes in
[O2Hb], i.e., ~50% of the [OI] change (<5
µmol/l), and in [tHb] (<3 µmol/l) found in the present study were very small (4-6%) compared with the estimated total blood flow in the cerebrum of ~70-100 µmol/l
(18). The detection of such small changes in
[OI] and related variables may in part explain the absence of
presyncope complaints with a significantly lowered [OI].
The tendency for a greater decrease in cerebral [OI] in SCI than in
AB individuals is in keeping with the greater decrease in CFV in SCI
than AB individuals, assuming a steady arterial O2 content
and cerebral O2 consumption. Obviously, it is not clear whether the decrease in CFV is matched to the decrease in cerebral [OI]; i.e., the latter variable may, or may not, have been buffered against the effect of a decreased CFV. For example, changes in CBF
distribution distally from the conductance artery may have influenced
the frontal lobe oxygenation as measured by NIRS.
The tendency for a greater fall in cerebral [OI] in SCI than in AB
individuals, and with cerebral oxygenation being the final common
pathway to syncope, suggests that SCI may have a slightly diminished
orthostatic tolerance compared with AB individuals. Pure autonomic
failure (PAF) patients have a sympathetic nervous system impaired at
the synapse and commonly experience postural hypotension and
orthostatic intolerance. In accordance, in PAF patients, MAP and both
CBV and cerebral oxygenation seem to decrease further than in SCI
individuals during orthostatic stress, resulting in a statistical
significant difference between controls and PAF patients
(16).
In conclusion, in contrast to our hypothesis, SCI individuals increased
CVR, as did AB individuals, during orthostatic stress. In
addition, SCI individuals showed a greater fall in MAP than did AB
individuals. Consequently, CFV decreased more in SCI than in AB
individuals, whereas cerebral oxygenation decreased in both groups.
This study does not support the idea that orthostatic tolerance in SCI
individuals may be explained by a lesser cerebral vasoconstriction
during orthostatic stress.
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ACKNOWLEDGEMENTS |
J. K. Shoemaker was supported by the Natural Sciences and
Research Council of Canada. J. M. Serrador was supported by a
Natural Sciences and Research Council of Canada Postgraduate Scholarship.
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FOOTNOTES |
Address for reprint requests and other correspondence: S. Houtman, Dept. of Physiology 237, Univ. Medical Center Nijmegen, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands (E-mail:
S.Houtman{at}fysio.kun.nl).
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 20 February 2001; accepted in final form 2 July 2001.
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