Vol. 88, Issue 3, 957-965, March 2000
Carotid baroreflex control of heart rate and blood pressure
during ES leg cycling in paraplegics
Jacqui
Raymond1,
Glen M.
Davis1,
Martinus N.
van der Plas3,
Herbert
Groeller2, and
Scott
Simcox1
1 Rehabilitation Research Centre, University of
Sydney, Lidcombe, New South Wales 2141;
2 Department of Biomedical Science, University of
Wollongong, Wollongong, New South Wales 2522, Australia; and
3 Faculty of Human Movement Sciences, Vrije
University, 1081 BT Amsterdam, The Netherlands
 |
ABSTRACT |
This study investigated
control of heart rate (HR) and mean arterial pressure (MAP) at rest and
during electrical stimulation (ES) leg cycling exercise (LCE) in
paraplegics (Para). Seven men with complete spinal lesions
(T5-T11) and six able-bodied (AB) men
participated in this study. Beat-to-beat changes in HR and MAP were
recorded during carotid sinus perturbation. Carotid baroreflex function
curves were derived at rest and during ES-LCE for Para and during
voluntary cycling (Vol) for AB. From rest to ES-LCE, oxygen uptake
(
O2) increased (by 0.43 l/min) and HR rose (by 11 beats/min), yet MAP remained unchanged. In
AB, Vol increased O2 (by
0.53 l/min), HR (by 22 beats/min), and MAP (by 8 mmHg). ES-LCE did not
alter the carotid sinus pressure (CSP)-MAP relationship, but it
displaced the CSP-HR relationship upward relative to rest. No rightward
shift was observed during ES-LCE. Vol by AB produced an upward and
rightward displacement of the CSP-MAP and CSP-HR relationships relative
to rest. These findings suggested that the carotid sinus baroreflex was
not reset during ES-LCE in Para.
spinal cord injury; cardiovascular control; hemodynamic; functional
electrical stimulation
| |
INTRODUCTION |
IN ABLE-BODIED (AB) individuals, heart rate (HR) and
blood pressure rise with increasing dynamic leg exercise intensity
(23). The autonomic modulation of these alterations is mediated by
central command and reflex feedback via group III and IV skeletal
muscle afferent nerves (16, 25). In addition to these neural
mechanisms, the arterial baroreflex may also play a role in the
regulation of the cardiovascular responses during exercise. In intact
dogs (30), rabbits (7), and humans (20, 22), the carotid baroreflex stimulus-response curve is "reset" to higher operating pressures than at rest during graded intensities of dynamic exercise. Thus the
baroreflex contributes to elevating arterial pressure rather than
operating to oppose it (25). When exercise intensity is constant, the
baroreflex continuously regulates arterial pressure at its new point,
acting as a negative feedback system controlling fluctuations above and
below the operating point (25). The mechanism responsible for resetting
the arterial baroreflex during exercise has yet to be isolated (23).
However, it has been suggested to originate either as a centrally
generated signal (25) or from the mechanically sensitive skeletal
muscle afferent fibers (21).
Electrical stimulation (ES)-induced leg cycling exercise (LCE)
performed by people with spinal cord injuries produces inconsistent HR
and blood pressure responses. Whereas some studies demonstrated a
decrease in HR during ES exercise (1, 3), others have observed an
increase (2, 8, 11, 14) or no change (4, 29). Similarly, blood pressure
either was increased during ES-LCE (1, 8) or remained unchanged from
resting values (11, 14, 29).
In people with paraplegia (Para) who undertake ES-LCE, the spinal
lesion interrupts the transmission of afferent neural signals from the
exercising muscles. Furthermore, the nonvoluntary nature of ES-induced
muscle contractions allows such exercise to be performed in the absence
of central command (1, 4, 29). Therefore, this exercise paradigm
abolishes the action of central command and skeletal muscle afferent
feedback on the baroreflex while allowing the baroreceptors to remain
operational. On the basis of this paradigm, we hypothesized that ES-LCE
in Para would not elicit arterial baroreflex resetting. Therefore, the
purpose of this study was to investigate the carotid baroreflex control
of HR and mean arterial pressure (MAP) in Para at rest and during ES-LCE. The implications of the altered control of the cardiovascular responses during ES-LCE may assist in explaining the inconsistent HR
and blood pressure responses previously observed in Para.
| |
METHODS |
Subjects.
Seven men (37 ± 6 yr old) with clinically complete spinal lesions
between T5 and T11 (11 ± 7 yr since injury)
took part in this study. Before their participation, an independent
medical practitioner examined each subject for any contraindications to exercise. The subjects also underwent carotid duplex ultrasound scans
to screen for stenoses of the carotid arteries as interpreted by a
cardiologist. Subjects with stenosis >20% diameter of the carotid
artery or color Doppler evidence of hemodynamically significant plaque
were excluded. Six AB men of similar age (38 ± 5 yr) and physical
activity levels participated in this study as a cohort group. All
subjects abstained from caffeine and food intake for at least 3 h
before the experiment and avoided vigorous exercise in the previous 24 h.
Physiological measurements.
HR was monitored via a three-lead electrocardiogram (ECG; Portascope CR
55, Cardiac Recorders). Beat-to-beat changes in blood pressure were
assessed via finger photoplethysmography (Finapres 2300, Ohmeda,
Louisville, CO). The monitoring cuff was placed around the middle
finger of the right hand, and the forearm and hand were supported so
that the cuff was aligned at heart level. The analog signals of the ECG
and blood pressure waveforms were synchronized via computer software
(Labview 4.0, National Instruments, Austin, TX). The ECG was sampled at
1,000 Hz, and a value for systolic, diastolic, and mean arterial
pressures was collected at each QRS complex of the ECG. Finger
photoplethysmography measurements accurately track the beat-to-beat
changes in blood pressure both at rest and during exercise (9).
However, the absolute value for blood pressure from the Finapres may
not be as accurate (9), possibly because of cutaneous vasodilation
occurring with temperature regulation (19). Therefore, blood pressure
was also monitored on three occasions throughout each trial via
auscultation. The blood pressure recorded via the Finapres was
corrected for the blood pressure determined via auscultation.
During all trials, steady-state oxygen uptake
(O2) was averaged over 20-s
intervals via open-circuit spirometry (Sensormedics 2900 Metabolic
Cart, Sensormedics, Yorba Linda, CA). The mean value over 2 min of
collection was taken to represent the steady-state O2 for each trial.
Cycle ergometry.
Gel-backed surface electrodes (Empi, St. Paul, MN) were placed over the
neuromuscular motor points of the gluteal, quadriceps, and hamstring
muscle groups of Para subjects prior to their commencing ES-LCE (ERGYS
2, Therapeutic Alliances, Dayton, OH). During ES-LCE, monophasic
rectangular pulses were delivered at a frequency of 35 Hz and pulse
duration of 0.375 ms. The amplitude and timing of the stimulation were
preset by a microprocessor that received feedback based on crank
position and velocity. ES current output to the leg muscles was varied
by the microprocessor to maintain a cycling cadence of 50 revolutions/min. The maximum current output delivered to the muscle was
140 mA, and the minimum cycling cadence maintained was 35 revolutions/min. AB subjects performed leg cycling on the same
ergometer but under voluntary control at 50 revolutions/min.
Neck chamber.
A Silastic neck chamber (Engineering Development Laboratory),
previously described by Sprenkle et al. (28), was used to initiate
carotid sinus perturbation. The chamber encased the front half of the
neck, providing an airtight seal between the mandible and the clavicles
and sternum. Positive and negative pressures were delivered to the
carotid sinuses via a bellows system that was controlled by computer software.
The neck pressure/suction procedure used in this experiment was based
on that employed by Potts and co-workers (22) involving a randomly
selected sequence of 
70, 60, 40, 20, 0, 20, 30, and 40 mmHg pressures. The procedure involved delivering each positive or negative pressure to the carotid sinus region of the neck
50 ms after the R spike of the QRS complex. For the next 5 s, the
stimulus was renewed with each succeeding R spike, to maintain the
desired pressure in the face of any leakage from around the neck
chamber. After 5 s of carotid sinus perturbation, the pressure returned
to zero for 30 s, at which time the next pressure was selected in the
sequence. To ensure that the pressures were accurately delivered, the
level of neck pressure being generated was displayed on an oscilloscope
(Tektronix, model TDS 420, Wilsonville, OR).
Just before the onset, and for 5 s after each level of neck pressure,
the subject was instructed to hold his breath at end expiration. This
technique, used by Potts and colleagues (22), mitigated any influence
of respiration on HR and MAP. All subjects reported that, at rest and
during exercise, the breath-hold was not stressful and that no undue
strain was involved.
Procedures.
Subjects reported to the laboratory for a familiarization session and
two test sessions. The familiarization session involved habituation to
the procedures to be used on the subsequent test days. At this stage,
two Para and three AB subjects were excluded from the study because the
silastic neck chamber was unable to achieve an airtight seal.
The two test sessions followed the same procedures and were performed
at the same time of day, separated by at least 48 h. Each subject was
positioned on the leg cycle ergometer and instrumented for the
measurement of HR and blood pressure. Just before data collection commenced, the neck chamber was applied.
Both Para and AB subjects participated in three trials on each day. The
three Para trials comprised 1) rest; 2) passive leg cycling (passive), whereby an assistant turned the pedals of the cycle
ergometer; and 3) ES-LCE at 0 W. The three trials were always performed in the same order with rest preceding passive so that the
latter would not be influenced by prior exercise. The AB trials included 1) rest, 2) voluntary leg cycling at 18 W (Vol
18 W), and 3) voluntary leg cycling at 42 W (Vol 42 W). The two
exercise trials were performed in a randomized order but were always
preceded by the rest trial.
During each trial, three sequences of neck pressure and suction were
delivered to the carotid sinuses of the subject. The carotid sinus
perturbations were performed only when the subject had reached a steady
state (within 4-5 min of the start of the trial). Sequences were
separated by 3 min. Beat-to-beat changes in HR and MAP were collected
throughout each trial and stored to a personal computer for later
analysis. O2 was measured
for a 2-min period at the completion of the carotid sinus perturbations.
Data analysis.
During each carotid sinus perturbation, the peak HR and MAP responses
within 10 s of the onset of the stimulus were recorded (22). An example
of the HR and MAP responses during carotid sinus perturbation for a
typical Para subject at rest and during ES-LCE is shown in Fig.
1. The responses at each level of pressure for the three sequences performed during the trial were averaged for
each subject. The carotid sinus pressure (CSP) was calculated as MAP
minus the neck chamber pressure (100% transmission of pressure to the
carotid sinus was assumed). The HR or MAP response for each subject was
then fitted to a sigmoidal four-parameter logistic function equation
(12) by nonlinear least-squares regression
where
HR or MAP was the calculated variable and A1 was the
response range (maximum minimum), A2 was the gain
coefficient, A3 was the centering point or the CSP at which
equal increases or decreases in HR or MAP occurred, and A4
was the minimum HR or MAP response.
View larger version (23K):
[in this window]
[in a new window]
|
Fig. 1.
Changes in heart rate (HR) and mean arterial pressure (MAP) during neck
suction (40 mmHg) in 1 paraplegic (Para) subject at rest
(A and C) and during electrical stimulation leg cycling
exercise (ES-LCE; B and D). Duration of carotid sinus
perturbation is represented by heavy line. Responses to 3 different
pressure sequences are presented on each graph. Solid symbols represent
HR or MAP recorded as response to neck suction during that particular
sequence. Average of 3 solid symbols was calculated to represent HR or
MAP response to neck pressure (40 mmHg) for that trial.
|
|
In addition to the four parameters derived from the nonlinear
regression, other landmarks were also identified on the HR/MAP stimulus-response curves. These included the threshold and saturation points described by Chen and Chang (5) and the maximal gain (at
A3). Finally, the operating point was the point on the
stimulus-response curve around which the carotid baroreflex maintained
arterial pressure. We defined the operating point of the CSP-HR
relationship as the point on the curve that intersected with the
steady-state HR. The intersection of the line of identity with the
stimulus-response curve represented the operating point for the CSP-MAP
relationship (22, 26). The criterion for carotid baroreflex resetting
used in this study was determined a priori as a shift of the centering, operating, threshold, and saturation points to a higher CSP.
Statistical analysis.
A repeated-measures ANOVA was used to determine the test-retest
reproducibility of the variables between the two test sessions on
different days. This analysis revealed no effect for test session for
any of the variables. Therefore, for all subsequent analyses, data from
the two test days were averaged.
For each subject group, repeated-measures ANOVA were used to compare
the responses among the three trials. Bonferroni within-subjects contrasts were used for pairwise comparisons when Hotelling's T2 had previously established a significant
main effect for trial. The values for maximal gain were nonnormally
distributed. Therefore, a Friedman's nonparametric test was used to
compare the response among the three trials. To compare the responses
between Para and AB groups, a repeated-measures ANOVA was used to
determine an interaction effect. Rest and ES-LCE and rest and Vol 42 W
were used as the within-subjects measure for Para and AB, respectively. The higher of the two workloads was chosen for the AB group as it
elicited an O2 similar to
Para during ES-LCE at 0 W.
For all statistical analyses, results were considered significant at
the 95% confidence limit. The results are presented as means ± SD
(median and interquartile range for maximal gain), and all analyses
were performed by using a statistical software package (SPSS Version
8.0) on a personal computer.
| |
RESULTS |
Voluntary leg cycling.
In AB, HR was higher during Vol 18 W (73.6 ± 4.0 beats/min) and Vol
42 W (82.8 ± 7.7 beats/min) than at rest (61.3 ± 4.2 beats/min). MAP was also higher during exercise (Vol 18 W: 95.5 ± 8.5 mmHg; Vol
42 W: 97.8 ± 8.6 mmHg) compared with at rest (89.7 ± 7.6 mmHg). O2 was greater during Vol 18 W (0.51 ± 0.07 l/min) and Vol 42 W (0.80 ± 0.09 l/min) than at rest
(0.26 ± 0.05 l/min). During Vol 42 W, HR and
O2 were higher than during
Vol 18 W.
The four parameters calculated from the nonlinear regression of the
CSP-HR and CSP-MAP relationships for AB are presented in Table
1. Voluntary leg cycling
increased the centering point and the minimum HR or MAP response.
However, the response range and the slope coefficient were not altered
from rest to exercise in AB. There was also no significant difference
in maximal gain of the CSP-HR and CSP-MAP stimulus-response curves
among the three trials.
Voluntary leg cycling elicited an upward and rightward shift of the
CSP-HR and CSP-MAP relationships relative to rest (Fig. 2). Although the AB subjects performed two
levels of exercise in this study, clear evidence for resetting of the
carotid sinus baroreflex was only present at Vol 42 W. Figure
3 illustrates the sigmoidal curves fitted
to the mean CSP, HR, and MAP at rest and Vol 42 W. The four landmarks
used as criteria of carotid baroreflex resetting are also shown on the
curves. For both the CSP-HR and CSP-MAP relationships, the centering
and operating points occurred at significantly higher levels of CSP
during Vol 42 W than at rest. There was also a significant change in
the threshold and saturation points for the CSP-HR and CSP-MAP
relationships, respectively.
View larger version (19K):
[in this window]
[in a new window]
|
Fig. 2.
Stimulus-response curves for carotid sinus pressure (CSP)-HR
relationship (A) and CSP-MAP relationship (B) in
able-bodied (AB) group. Curves were fitted to the CSP and HR or MAP
responses at each pressure level. For clarity of presentation, the
average SD of all points is inset at bottom left. Range of SD
in A was 3.3-9.8 for HR and 5.6-10.0 for CSP. Range
of SD in B was 3.7-10.2 for MAP and 5.6-10.0 for CSP.
Vol 42 W and Vol 18 W, voluntary leg cycling at 42 and at 18 W,
respectively.
|
|
View larger version (19K):
[in this window]
[in a new window]
|
Fig. 3.
Stimulus-response curves for CSP-HR relationship (A) and
CSP-MAP relationship (B) in AB group at rest and during Vol 42 W. Landmarks that are indicators of baroreflex resetting are presented
on each stimulus-response curve as means ± SD. * CSP at which a
point occurs is significantly higher during Vol 42 W (P < 0.05).
|
|
Passive leg cycling.
In Para, passive decreased HR (69.3 ± 11.4 beats/min at rest vs. 62.7 ± 9.7 beats/min at passive) relative to rest, but did not alter MAP
(91.8 ± 6.2 mmHg at rest vs. 92.7 ± 7.0 mmHg at passive)
or O2 (0.22 ± 0.02 l/min at rest vs. 0.24 ± 0.03 l/min at passive). There was no
change in the four parameters calculated from the nonlinear regression
of either relationship except for an increase in the CSP at the
centering point and a decrease in the minimum response for the CSP-HR
relationship (Table 2). The maximal gain of
the stimulus-response curves was also unchanged from rest. Passive led
to a downward displacement of the CSP-HR relationship but did not
produce any alteration in the CSP-MAP relationship compared with rest
(Fig. 4).
View larger version (17K):
[in this window]
[in a new window]
|
Fig. 4.
Stimulus-response curves for CSP-HR relationship (A) and
CSP-MAP relationship (B) in Para group. Curves were fitted to
the mean CSP and HR or MAP responses at each pressure level. For
clarity of presentation, the average SD of all points is inset at
bottom left. Range of SD in A was 7.2-13.5 for HR
and 3.2-6.6 for CSP. Range of SD in B was 2.5-6.2 for
MAP and 3.2-6.6 for CSP. Passive, passive leg cycling with
assistant turning pedals of cycle ergometer.
|
|
ES-induced leg cycling.
O2 (0.65 ± 0.15 l/min) and HR (80.1 ± 11.1 beats/min) were higher during ES-LCE than
at rest or during passive. However, MAP (92.0 ± 7.8 mmHg) was not
altered during ES-LCE from its resting value.
Compared with results obtained at rest, ES-LCE did not elicit any
change in either maximal gain or the four nonlinear regression parameters for either the CSP-HR or the CSP-MAP relationships (Table
2). The CSP-HR relationship was displaced upward relative to rest;
however, the CSP-MAP relationship was not altered (Fig. 4). Figure
5 presents the sigmoidal curves fitted to
the mean CSP, HR, and MAP at rest and during ES-LCE. The threshold,
saturation, centering, and operating points are also displayed. ES-LCE
did not alter the CSP at which these points occurred for either the CSP-HR or CSP-MAP relationships. With the use of the same criteria for
baroreflex resetting that were applied to AB subjects, these data
indicated that ES-LCE did not elicit carotid baroreflex resetting in
Para subjects.
View larger version (20K):
[in this window]
[in a new window]
|
Fig. 5.
Stimulus-response curves for CSP-HR relationship (A) and
CSP-MAP relationship (B) in Para group at rest and during
ES-LCE. Landmarks that are indicators of baroreflex resetting are
presented on each stimulus-response curve as means ± SD. There was no
difference in CSP at which these points occurred between rest and
ES-LCE.
|
|
Para vs. AB differences.
Significant interaction (trial-by-group) effects were observed for
steady-state MAP and the centering, operating, and saturation points of
the CSP-MAP relationship. For the CSP-HR relationship, only the
centering point demonstrated a significant interaction effect. The
operating, threshold, and saturation points approached statistical
significance for a between-group interaction effect (P = 0.056, P = 0.059, P = 0.079, respectively).
| |
DISCUSSION |
Carotid baroreflex control during voluntary leg cycling.
The importance of the carotid baroreflex in regulating blood pressure
during exercise has been well established in animals (7, 30) and humans
(20, 22). Evidence that the baroreflex is reset to operate around a
higher CSP implies that this reflex contributes to an increase in blood
pressure during exercise rather than opposes it. The results of AB
subjects performing leg cycling in the present study supported the
concept of carotid sinus baroreflex resetting during voluntary
exercise. With an increase in
O2, the carotid baroreflex
reset to a higher sinus distending pressure as demonstrated by the
increase in CSP at which the centering, operating, threshold, and
saturation points occurred (Fig. 3).
The observations from AB data in this study agreed with previous
investigations (20, 22). Potts and colleagues (22) observed increases
in threshold, saturation, and centering point pressures of the
carotid-cardiac (CSP-HR) and carotid-vasomotor (CSP-MAP) function
curves from rest to exercise at power outputs eliciting 25% and 50%
peak O2
(O2 peak). Similarly,
Papelier and associates (20) observed a progressive rightward and
upward displacement of the CSP-HR and CSP-MAP function curves during leg cycling power outputs ranging from 60 to 240 W. In both studies, the gain of the carotid sinus baroreflex remained unchanged from resting values, suggesting that, during exercise, the baroreflex maintained appropriate sensitivity to control fluctuations in blood
pressure. In the present study, although the workloads performed by AB
were relatively low, there was clear evidence of resetting of the
CSP-HR and CSP-MAP relationships during Vol 42 W (Fig. 3). During
exercise, the CSPs at the operating, centering, threshold, and
saturation points were higher than at rest. The shift of these points
is consistent with the notion that the entire reflex has been centrally
modified to operate around a new prevailing blood pressure (24).
Carotid baroreflex control during ES-LCE.
ES-LCE performed by the Para group did not displace the CSP-HR or
CSP-MAP stimulus-response relationships rightward (Fig. 5), despite an
increase of O2 similar in
magnitude to their AB cohorts. However, similar to results in AB,
baroreflex sensitivity was unchanged in Para during exercise. These
observations suggested that the carotid baroreceptor reflex was not
reset during ES-LCE but remained functional near the resting level. In
one Para subject who could perform steady-state ES-LCE at 6 W (HR = 97 beats/min), the higher power output did not elicit a rightward shift of
the stimulus-response curves relative to rest or ES-LCE at 0 W (Fig. 6). This was in contrast to the AB group of
the present study and to earlier reports (20, 22), whereby increasing
exercise intensities led to progressive rightward displacement of the
CSP-HR and CSP-MAP relationships.
View larger version (18K):
[in this window]
[in a new window]
|
Fig. 6.
Stimulus-response curves for CSP-HR relationship (A) and
CSP-MAP relationship (B) in one Para subject. This subject
completed 2 levels of ES-LCE, at 0 and 6 W. Increasing workload
elicited a vertical displacement of CSP-HR relationship (A) but
no change in CSP-MAP relationship (B).
|
|
The precise stimulus initiating carotid baroreflex resetting is
unknown; however, both central command and skeletal muscle afferent
neural feedback have been implicated (21, 25). The lack of resetting in
Para is consistent with the evidence that signals arising from central
command and/or skeletal muscle afferent feedback alter the reflex's
interpretation of afferent information from the baroreceptors. In Para
with sensorimotor complete injuries, the spinal lesion interrupts the
ascending and descending neural traffic. Therefore, in the absence of
this neural traffic, and without central command, there was no stimulus
for carotid baroreceptor resetting during ES-LCE and the reflex thus
remained operational near resting levels.
Mechanisms for cardioacceleration in Para.
In the absence of central command or skeletal muscle afferent feedback,
our observations suggest that nonneural mechanism(s) mediate
cardioacceleration during ES-LCE in Para. Although it is unclear
precisely what this mechanism may be, Kjær and co-workers (14) have
suggested that humoral feedback may be an important stimulus for
cardioacceleration in the absence of central command and skeletal
muscle afferent feedback.
A second characteristic of the mechanism contributing to
cardioacceleration may be that it is time dependent. Although HR responses during ES-induced leg exercise have been inconsistent, those
studies that have detected cardioacceleration (2, 8, 11, 14, and the
present study) noted it after at least 10 min of exercise. Shorter
exercise trials were used in those investigations that observed no
change (4, 29) or a decrease (1, 3) in HR. The apparent time course of
cardioacceleration is consistent with the hypothesis of a blood-borne
stimulus, whereby this type of mechanism might have a minimal immediate
effect but would accumulate with time or intensity of exercise.
On the basis of the findings of the present investigation and those
from previous studies (3, 14), it is possible to reflect on why there
has been inconsistency in the HR response during ES-induced exercise in
Para. Inconsistent observations may be explained by the absence of
arterial baroreflex resetting coincident with nonneural mechanism(s)
mediating cardioacceleration during ES-LCE. We suggest that, at the
onset of ES-induced exercise blood pressure increases, and, in the
absence of arterial baroreflex resetting, this increase is interpreted
as hypertension. In turn, this elicits a reflex decrease in HR.
Notably, Brice and colleagues (3) observed an increase in arterial
blood pressure immediately followed by a decrease in HR in the
transition from rest to ES-induced leg exercise and again in the
transition to a higher work rate. As ES-induced leg exercise
progresses, we suggest that HR rises further not via increased central
command, afferent neural activity, or via the baroreflex (because
steady-state MAP remains unchanged) but rather is mediated by some
nonneural mechanism(s) that accumulates over time.
Another possible factor that may contribute to cardioacceleration in
Para subjects performing ES-LCE is an increase in blood temperature.
During a 30-min ES-LCE trial, Hjeltnes and co-workers (10) demonstrated
increases in rectal temperature after 12 min of cycling in subjects
with tetraplegia. However, whether the rise in temperature contributed
to cardioacceleration in their experiment was unclear, as the HR had
plateaued by 9 min in all but one subject.
MAP during ES-LCE.
MAP did not increase above rest during ES-LCE. This observation is
consistent with previous studies of Para subjects undertaking ES-induced leg exercise (1, 11, 14, 29). Moreover, the absence of a
pressor response supports the viewpoint that arterial pressure is
elevated during exercise via reflex changes arising from stimulation of
the chemosensitive muscle afferents in the active muscle (16, 25).
Kjær and co-workers (13) also found that MAP remained unchanged from
rest during ES-LCE in AB subjects whose legs were paralyzed following
epidural anesthesia at L3-L4. Conversely, when the same subjects
performed voluntary leg cycling at an equivalent
O2, MAP rose from
93 ± 4 mmHg at rest to 119 ± 4 mmHg during exercise. Further
evidence for the pressor reflex being mediated by afferent feedback
from the exercising muscles can be derived from experiments on AB
subjects performing ES-induced leg exercise (1, 29). Thomas and
colleagues (29) demonstrated a 39- to 44-mmHg increase in systolic
blood pressure in AB subjects undertaking ES-induced knee extension.
This increase in blood pressure was attributed to activation of the
muscle afferents based on the assumption that the muscle contractions
were elicited without an increase in central command.
Carotid baroreflex control during passive.
Passive was included in this study to determine whether limb movements
in the absence of muscle contractions might alter HR or MAP in Para
individuals. Such "sham exercise" was employed to delineate
between the effects of leg cycling motion vs. dynamic ES-induced muscle
contractions and also to eliminate the effect of knowledge of leg
movements. The lack of increase in HR during passive suggested that the
higher HR observed during ES-LCE was entirely due to neuromuscular recruitment.
Interestingly, passive elicited a decrease in HR of 7 beats/min. This
decrease is difficult to interpret on the basis of the measurements
made in this study; however, we can conclude that it was not a
baroreflex response, as MAP was unaltered. Muraki and colleagues (17)
noted that, in Para subjects, an increase in stroke volume occurred
during passive without a concurrent change in HR. This may suggest that
the decrease in HR observed in our study was due to an increase in
stroke volume. However, unpublished results from our laboratory
demonstrate that passive does not elevate stroke volume yet still
reduces HR. Similar observations have been made in people with
quadriplegia (18). Therefore, the mechanism explaining the decrease in
HR during passive has yet to be elucidated.
Potential limitations of the study.
The inherent limitations of the neck pressure/suction method have been
detailed elsewhere (20, 22). Briefly, these limitations include
1) the possibility that the reflex HR and MAP responses are
affected by the extracarotid baroreceptors (22) and 2) the incomplete transmission of positive and negative pressures to the
carotid sinuses (15). In addition to these factors, it is possible that
performing an end-expiratory breath-hold technique alters chemoreceptor
activity or provokes a Valsalva maneuver to influence HR and MAP during
the time of carotid sinus perturbation.
For all subjects, the peak change in HR generally occurred within 5 s
following either neck pressure or neck suction (e.g., Fig. 1). The peak
change in MAP typically occurred after the carotid sinus perturbation
had finished, representing the contribution of the slower,
sympathetically mediated changes in vascular resistance. However, the
recording of responses after the 5-s perturbation may allow for
increased counter effects from the extracarotid baroreceptors or
perhaps for a reduction in the magnitude of the response because the
stimulus was no longer being applied. However, the gains of our
stimulus-response curves were similar to those studies that employed
longer carotid sinus perturbation times. Papelier and co-workers (20)
employed 20-s periods of neck pressure/suction, and the maximal slope
of their MAP stimulus-response curves ranged from 0.23 to
0.29. In addition, Spaak and colleagues (27) used 15-s periods
of neck pressure/suction, and the maximal slope of their MAP
stimulus-response curves was 0.39. Furthermore, the range of
response was also similar to our study.
Another potential limitation was that the exercise levels used in this
experiment might have been insufficient to elicit baroreceptor resetting in Para. However, in defense of the relatively low ES-LCE workloads, the AB groups in the present study and in that of Potts and
colleagues (22) demonstrated significant baroreflex resetting at a
similar O2 to the Para
groups. In addition, as resetting appears to be a function of exercise
intensity (20), it could be argued that, with an inherently lower
O2 peak (6), Para subjects exercised at a higher percentage of their maximum capacity than their AB cohorts did. Unfortunately, in this study,
O2 peak was not
measured in either the Para or AB groups, precluding us from expressing
leg cycling workloads as a relative intensity of effort.
In conclusion, this study demonstrated that the carotid sinus
baroreflex was not reset to operate around a higher sinus pressure during ES-LCE in Para subjects. Instead, the carotid baroreflex responded to fluctuations in blood pressure with similar sensitivity to
rest and around a similar CSP. The lack of carotid baroreflex resetting
may assist in explaining the inconsistent HR responses previously
observed in these individuals during ES-induced leg exercise.
Furthermore, the lack of resetting in subjects with complete paraplegia
confirms the importance of central command and/or skeletal muscle
afferent feedback in modifying baroreflex control of cardiovascular
responses during voluntary dynamic exercise, as both these neural
pathways were absent during ES-LCE. A secondary conclusion of this
study was that the increase in HR observed during ES-LCE could be the
result of a nonneural mechanism mediating cardioacceleration in Para.
Finally, this study demonstrated the potential of the spinal
cord-injured individual to provide a human model of cardiovascular
control during exercise.
| |
ACKNOWLEDGEMENTS |
We acknowledge the technical efforts of Simone Poulter and the kind
assistance of Prof. Simon Gandevia in the early interpretation of this
work. The carotid duplex ultrasounds were performed by Jill Clarke
(School of Medical Radiation Technology) and were assessed by Dr. Geoff
Schembri. Our sincerest appreciation is also extended to the subjects
who volunteered for this study.
| |
FOOTNOTES |
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. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: G. M. Davis,
Rehabilitation Research Centre, Univ. of Sydney, PO Box 170, Lidcombe,
NSW 2141, Australia (E-mail: g.davis{at}cchs.usyd.edu.au).
Received 5 April 1999; accepted in final form 8 November 1999.
| |
REFERENCES |
1.
Adams, L.,
H. Frankel,
J. Garlick,
A. Guz,
K. Murphy,
and
S. J. G. Semple.
The role of spinal cord transmission in the ventilatory response to exercise in man.
J. Physiol. (Lond.)
355:
85-97,
1984[Abstract/Free Full Text].
2.
Barstow, T. J.,
A. M. E. Scremin,
D. L. Mutton,
C. F. Kunkel,
T. G. Cagle,
and
B. J. Whipp.
Gas exchange kinetics during functional electrical stimulation in subjects with spinal cord injury.
Med. Sci. Sports Exerc.
27:
1284-1291,
1995[ISI][Medline].
3.
Brice, A. G.,
H. V. Forster,
L. G. Pan,
A. Funahashi,
M. D. Hoffman,
C. L. Murphy,
and
T. F. Lowry.
Is the hyperpnea of muscular contractions critically dependent on spinal afferent?
J. Appl. Physiol.
64:
226-233,
1988[Abstract/Free Full Text].
4.
Brown, D. R.,
H. V. Forster,
L. G. Pan,
A. G. Brice,
C. L. Murphy,
T. F. Lowry,
S. M. Gutting,
A. Funahashi,
M. Hoffman,
and
S. Powers.
Ventilatory response of spinal cord-lesioned subjects to electrically induced exercise.
J. Appl. Physiol.
68:
2312-2321,
1990[Abstract/Free Full Text].
5.
Chen, H. I.,
and
K. C. Chang.
Assessment of threshold and saturation pressure in the baroreflex function curve: a mathematical analysis.
Jpn. J. Physiol.
41:
861-877,
1991[ISI][Medline].
6.
Davis, G. M.
Exercise capacity of individuals with paraplegia.
Med. Sci. Sports Exerc.
25:
423-432,
1993[ISI][Medline].
7.
DiCarlo, S. E.,
and
V. S. Bishop.
Onset of exercise shifts operating point of arterial baroreflex to higher pressures.
Am. J. Physiol. Heart Circ. Physiol.
262:
H303-H307,
1992[Abstract/Free Full Text].
8.
Figoni, S. F.,
M. M. Rodgers,
R. M. Glaser,
S. P. Hooker,
P. D. Faghri,
B. N. Ezenwa,
T. Mathews,
A. G. Suryaprasad,
and
S. C. Gupta.
Physiologic responses of paraplegics and quadriplegics to passive and active leg cycle ergometry.
J. Am. Paraplegia Soc.
13:
33-39,
1990[Medline].
9.
Gabriel, A.,
L. E. Lindblad,
and
C. Angleryd.
Non-invasive vs. invasive beat-to-beat monitoring of blood pressure.
Clin. Physiol.
12:
229-235,
1992[ISI][Medline].
10.
Hjeltnes, N.,
A. K. Aksnes,
K. I. Birkeland,
J. Johansen,
A. Lannem,
and
H. Wallberg-Henriksson.
Improved body composition after 8 wk of electrically stimulated leg cycling in tetraplegic patients.
Am. J. Physiol. Regulatory Integrative Comp. Physiol.
273:
R1072-R1079,
1997[Abstract/Free Full Text].
11.
Hooker, S. P.,
S. F. Figoni,
R. M. Glaser,
M. M. Rodgers,
B. N. Ezenwa,
and
P. D. Faghri.
Physiologic responses to prolonged electrically stimulated leg-cycle exercise in the spinal cord injured.
Arch. Phys. Med. Rehabil.
71:
863-869,
1990[ISI][Medline].
12.
Kent, B. B.,
J. W. Drane,
B. Blumenstein,
and
J. W. Manning.
A mathematical model to assess changes in the baroreceptor reflex.
Cardiology
57:
295-310,
1973.
13.
Kjær, M.,
G. Perko,
N. H. Secher,
R. Boushel,
N. Beyer,
S. Pollack,
A. Horn,
A. Fernandes,
T. Mohr,
S. F. Lewis,
and
H. Galbo.
Cardiovascular and ventilatory responses to electrically induced cycling with complete epidural anaesthesia in humans.
Acta Physiol. Scand.
151:
199-207,
1994[ISI][Medline].
14.
Kjær, M.,
F. Potts,
T. Mohr,
P. Linkis,
P. Tornøe,
and
N. H. Secher.
Heart rate during exercise with leg vascular occlusion in the spinal cord injured man.
J. Appl. Physiol.
86:
806-811,
1999[Abstract/Free Full Text].
15.
Ludbrook, J.,
G. Mancia,
A. Ferrari,
and
A. Zanchetti.
The variable-pressure neck chamber method for studying the carotid baroreflex in man.
Clin. Sci. Mol. Med.
53:
165-171,
1977[ISI][Medline].
16.
Mitchell, J. H.
Neural control of the circulation during exercise.
Med. Sci. Sports Exerc.
22:
141-154,
1990[ISI][Medline].
17.
Muraki, S.,
M. Yamasaki,
Y. Ehara,
K. Kikuchi,
and
K. Seki.
Cardiovascular and respiratory responses to passive leg cycle exercise in people with spinal cord injuries.
Eur. J. Appl. Physiol.
74:
23-28,
1996.
18.
Nash, M. S.,
M. S. Bilsker,
H. M. Kearney,
J. N. Ramirez,
B. Applegate,
and
B. A. Green.
Effects of electrically-stimulated exercise and passive motion on echocardiographically-derived wall motion and cardiodynamic function in tetraplegic persons.
Paraplegia
33:
80-89,
1995[ISI][Medline].
19.
Nijboer, J. A.,
J. C. Dorlas,
and
J. Lubbers.
The difference in blood pressure between upper arm and finger during physical exercise.
Clin. Physiol.
8:
501-510,
1988[ISI][Medline].
20.
Papelier, Y.,
P. Escourrou,
J. P. Gauthier,
and
L. B. Rowell.
Carotid baroreflex control of blood pressure and heart rate in men during dynamic exercise.
J. Appl. Physiol.
77:
502-506,
1994[Abstract/Free Full Text].
21.
Potts, J. T.,
and
J. H. Mitchell.
Rapid resetting of carotid baroreceptor reflex by input from skeletal muscle receptors.
Am. J. Physiol. Heart Circ. Physiol.
275:
H2000-H2008,
1998[Abstract/Free Full Text].
22.
Potts, J. T.,
X. R. Shi,
and
P. B. Raven.
Carotid baroreflex responsiveness during dynamic exercise in humans.
Am. J. Physiol. Heart Circ. Physiol.
265:
H1928-H1938,
1993[Abstract/Free Full Text].
23.
Raven, P. B.,
J. T. Potts,
and
X. Shi.
Baroreflex regulation of blood pressure during dynamic exercise.
Exerc. Sport Sci. Rev.
25:
365-389,
1997[Medline].
24.
Rowell, L. B.,
and
D. S. O'Leary.
Reflex control of the circulation during exercise: chemoreflexes and mechanoreflexes.
J. Appl. Physiol.
69:
407-418,
1990[Abstract/Free Full Text].
25.
Rowell, L. B.,
D. S. O'Leary,
and
D. L. Kellog.
Integration of cardiovascular control systems in dynamic exercise.
In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD: Am. Physiol. Soc, 1996, sect. 12, chapt. 17, p. 770-840.
26.
Sagawa, K.
Baroreflex control of systemic arterial pressure and vascular bed.
In: Handbook of Physiology. The Cardiovascular System. Peripheral Circulation and Organ Blood Flow. Bethesda, MD: Am. Physiol. Soc, 1983, sect. 2, vol. III, pt. 2, chapt. 14, p. 453-496.
27.
Spaak, J.,
P. Sundblad,
and
D. Linnarsson.
Human carotid baroreflex during isometric lower arm contraction and ischemia.
Am. J. Physiol. Heart Circ. Physiol.
275:
H940-H945,
1998[Abstract/Free Full Text].
28.
Sprenkle, J. M.,
D. L. Eckberg,
R. L. Goble,
J. J. Schelhorn,
and
H. C. Halliday.
Device for rapid quantification of human carotid baroreceptor-cardiac reflex responses.
J. Appl. Physiol.
60:
727-732,
1986[Abstract/Free Full Text].
29.
Thomas, A. J.,
G. M. Davis,
and
J. R. Sutton.
Cardiovascular and metabolic responses to electrical stimulation-induced leg exercise in spinal cord injury.
Methods Inf. Med.
36:
372-375,
1997[ISI][Medline].
30.
Walgenbach, S. C.,
and
D. E. Donald.
Inhibition by carotid baroreflex of exercise-induced increases in arterial pressure.
Circ. Res.
52:
253-262,
1983[Abstract/Free Full Text].
J APPL PHYSIOL 88(3):957-965
8570-7587/00 $5.00
Copyright © 2000 the American Physiological Society
TOP
ABSTRACT
INTRODUCTION
![HR or MAP = A<SUB>1</SUB> {1 + e[<SUP>A<SUB>2</SUB>(CSP−A<SUB>3</SUB>)</SUP>]}<SUP>−1</SUP> + A<SUB>4</SUB>](/content/vol88/issue3/fulltext/957/img001.gif)
