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Service de Cardiologie, Hôpital Beaujon, 92110 Clichy, France
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ABSTRACT |
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 Top
 Abstract
 Introduction
Methods
Results
Discussion
References
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Recent studies have suggested that the increased ventilatory response during exercise in patients with chronic heart failure was related to the activation of muscle metaboreceptors. To address this issue, 23 patients with heart failure and 7 normal subjects performed arm and leg bicycle exercises with and without cuff inflation around the arms or the thighs during recovery. Obstruction slightly reduced ventilation and gas exchange variables at recovery but did not change the kinetics of recovery of these parameters compared with nonobstructed recovery: half-time of ventilation recovery was 175 ± 54 to 176 ± 40 s in patients and 155 ± 66 to 127 ± 13 s in controls (P < 0.05, patients vs. controls, not significant within each group from baseline to obstructed recovery). We conclude that muscle metaboreceptor activation does not seem to play a role in the exertion hyperventilation of patients with heart failure.
ventilation; metaboreceptors
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INTRODUCTION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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PATIENTS WITH CHRONIC HEART failure (CHF) have an excessive ventilation during exercise (36) and recovery (9). Such exertional hyperventilation does not seem to be related to increased pulmonary capillary pressure (13). Increased pulmonary dead space (33), bronchial hyperreactivity (2), and heavy respiratory muscle work (22) have also been suggested as possible mechanisms. A classical view links the increased ventilatory response to exercise to stimulation of the carotid chemoreceptors by CO2 produced by the muscles during exercise (31); it was recently suggested that muscle ergoreceptors may mediate the hyperventilation response during and after exercise in CHF (6, 28) and that the decreased ventilation brought about by training was due to their decreased stimulation (29). Ergoreceptors are receptors sensitive to physical stimuli, e.g., pressure and tension ("mechanoreceptors"), or to metabolic stimuli, e.g., H+, lactate, and K+ ("metaboreceptors"), that stimulate ventilation via excitation of myelinated type III and nonmyelinated type IV muscle fibers (26, 30).
We undertook this study to assess the role of ergoreceptor stimulation in exertional dyspnea of patients with CHF. If ergoreceptor stimulation plays a role in exercise hyperventilation, trapping the products of local metabolism within the muscle by cuff inflation should excite them. Inasmuch as CHF patients exhibit marked histological (23) and metabolic muscle abnormalities (21), greater decrease in intracellular pH (21) and increase in K+ (1) during exercise should excite metaboreceptors, whereas increased venous pressure and capillary filtration (19) should stimulate ergoreceptors. Thus the contribution of muscle ergoreceptors to hyperventilation should be greater in CHF patients than in normal subjects. Our hypothesis was that circulatory occlusion, maintaining metabolites within the muscle, would retard the normal decrease of ventilation after exercise in CHF patients. We sought also to determine whether a regional heterogeneity was present in the ergoreceptor response, inasmuch as it is now clearly demonstrated that muscle abnormalities exhibit regional differences, as recently demonstrated for muscle vascular reactivity (20), perhaps because of differential deconditioning (4).
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METHODS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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We used two protocols to assess the ergoreceptor response of the legs and arms.
Protocol 1. Protocol 1 was designed to assess the ergoreceptor responses of the lower limbs.
All exercise tests were performed in the morning after a light breakfast. We used an upright graded bicycle exercise with workload increments of 10 W/min for the patients and 20 W/min for the control group, after a similar initial workload of 20 W. Patients and control subjects were regularly encouraged to exercise until exhaustion. The bicycle was an Ergoline 900 ergometer, the calibration of which was regularly checked; subjects pedaled at a constant rate of 40-50 rpm. At maximal exercise the load was removed and the subjects were asked to stop pedaling. Respiratory gas analysis was carried out with a CPX-D Medical Graphics system (St. Paul, MN). Calibration of the system was performed with standard gas of known concentration before each test. Subjects were asked to remain still for 3 min before exercising to stabilize resting gas measurements. A standard 12-lead electrocardiogram was continuously recorded, allowing determination of heart rate each minute. Blood pressure was measured by a sphygmomanometer every 2 min. O2 consumption (
O2),
CO2 production
(CO2), minute ventilation
(E),
breathing rate, respiratory exchange ratio, ventilatory
equivalents for O2
(E/O2)
and CO2
(E/CO2), and end-tidal PO2
(PETO2) and
PCO2 (PETCO2) were measured on a
breath-by-breath basis. The results were averaged using a
moving-average filter every seven breaths, with the highest and lowest
values excluded at each breath to reduce the breath-by-breath noise.
They were thereafter averaged every 15 s and printed. Peak
O2 was defined as the
highest O2 obtained at the
end of the test; it was expressed in milliliters per minute and in
milliliters per minute per kilogram. Indexed peak
O2 (percent) was calculated
as peak O2 divided by
maximal predicted O2 with
use of the values reported by Wasserman et al. (34). The ventilatory
threshold was determined by classical methods (8, 35).
Ventilation response was assessed during recovery by means of the
half-time of recovery
(t1/2) of
ventilatory variables with use of a previously reported method (9). The
kinetics of recovery of gas exchange and ventilatory variables
(O2,
CO2, E) fit a
single-exponential curve (3, 12, 14, 16). The single-exponential
regression between O2,
CO2, and
E and time
during the first 4 min of recovery was described by the slope
(k) of the relationship as follows:
y(t) = Ae
kt + C, where
k (the rate constant) is the slope of
the curve, A is a parameter, and
C is the asymptotic baseline value. We
then derived 
, the constant of time, defined as = 1/k and
t1/2(exp) = 0.693. We also characterized recovery kinetics by simply
measuring t1/2,
i.e., the time required for a 50% fall in the peak value, as
previously reported (9). The coefficients of variation of these
variables were recently found to be 6 and 12% (9). Results obtained by
these two methods were here again highly correlated; therefore, only
those obtained by the exponential method are reported here.
On the next day, patients and subjects underwent the same test at the
same time of day. A large cuff was positioned around the lower part of
the thighs before the test and inflated for 30 s to evaluate the
tolerance to inflation. All patients were able to endure the occlusion.
After 10 min, subjects underwent the graded exercise test. At peak
exercise the cuffs were rapidly inflated at suprasystemic pressure
(i.e., the systolic pressure measured at peak exercise during the
preliminary test). Subjects were asked to have their legs extended
during recovery to ensure perfect occlusion of circulation. Circulatory
occlusion was maintained during 3 min of recovery, then released.
Protocol 2. Protocol 2 was performed to assess the role of the upper limb muscle ergoreceptors.
Exercise was performed with the arms by using a specially designed cycle ergometer. The patient was seated, with the chest at the level of the ergometer. Work rate was increased by 5 W/min after an initial work rate of 10 W in patients and by 10 W/min after an initial work rate of 20 W in normal subjects. All subjects performed exercise to a maximum effort while gas exchange was measured on-line. Circulatory occlusion was made during a second test, at peak exercise, with two smaller cuffs inflated around the upper part of the arm. However, inflation pressure was 40-50 mmHg only, because no subject could tolerate an inflation at suprasystemic pressure. Thus this level of inflation was considered sufficient to induce venous, but not arterial, occlusion. The kinetics of ventilation were assessed as described for protocol 1.Subjects.
Twenty-three men with mild to moderate CHF (57 ± 6 yr of age) and 7 normal men (50 ± 2 yr of age) participated in the study. Patients
with CHF were categorized as New York Heart Association functional
class II (n = 13) or III
(n = 10). All had performed at least
one preliminary exercise test, which was terminated because of fatigue
and/or dyspnea. The causes of heart failure were ischemic (n = 11) or idiopathic
(n = 12) cardiopathies. Mean left
ventricular ejection fraction was 27 ± 13%. None of the patients
had valve disease or respiratory insufficiency. All patients were
receiving diuretics and angiotensin-converting enzyme inhibitors, and
one-half of them were receiving digitalis; none was receiving a
-blocker. Ongoing treatments were not stopped before the exercise
test. None of the control subjects had clinical signs of heart failure or echographic evidence of left ventricular dysfunction or pulmonary disease.
Statistical analysis.
Values are means ± SD. Comparison of
t1/2 values was
carried out with paired or unpaired Student's
t-test as appropriate. ANOVA for
repeated measurements was used to compare change in E,
E/O2,
E/CO2,
PETO2, and
PETCO2 with and without cuff
inflation at recovery. P < 0.05 was
considered significant.
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RESULTS |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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Protocol 1.
Patients and subjects reached comparable work rates and peak
O2 during the two tests
(Table 1). Cuff inflation could be maintained during recovery in all subjects. The
t1/2 of
ventilatory variables of the patients was within values previously
reported (9, 10).
O2,
CO2, and
E recovery
rates were lower in patients than in normal subjects
(P < 0.05). Although values were slightly lower at each level during circulatory occlusion (Fig. 1), there was no significant difference in the
t1/2 of
E, O2, or
CO2 with and without cuff
inflation in patients and in normal subjects.
E/O2,
E/ CO2,
PETO2, and PETCO2 courses were
unaffected by cuff inflation (Fig. 2).
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Protocol 2.
Both tests were also well reproducible. Here again, no difference in
the kinetics of recovery was observed in any variable with and without
cuff inflation (Table 2).
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DISCUSSION |
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Top
Abstract
Introduction
Methods
Results
Discussion
References
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The main finding of this study is that circulatory occlusion did not affect the ventilatory response in CHF patients more than in normal subjects after exercise, suggesting that a greater stimulatory response from the muscle ergoreceptors does not explain the exertional ventilation observed in CHF patients.
Circulatory occlusion produced by cuff inflation decreases ventilation at each level of exercise, as demonstrated previously (11, 15, 18, 31). These results have been interpreted as showing that trapping blood in the exercised legs during exercise recovery accelerates the ventilatory decline to resting levels. In these studies, however, the rate of ventilatory recovery was not directly calculated. Moreover, these studies were performed during constant submaximal work rate exercise, whereas our study used graded maximal exercise.
Our findings do not necessarily contradict the previous studies (11,
15, 18, 31) because of differences in protocol and in the way in which
the recovery rate of ventilation was assessed. The absolute decrease in
ventilatory level was far greater in the study of Haouzi et al. (15),
who used supra-anaerobic constant work rate exercise, than in that of
Innes et al. (18), who used a moderate level of exercise. The fact that
ventilation levels after circulatory occlusion were only moderately
decreased (Fig. 1) compared with the control test may also be due to
the fact that we occluded only the lower parts of the thighs.
Therefore, the muscle mass excluded from circulation was less than in
previous studies. The fact that no significant change in
PETCO2 or
E/CO2
was observed during the obstructed recovery, despite changes in
E, as in
previous studies in normal subjects (15, 31), suggests that
E still
responded in proportion to the CO2 from the exercising muscles.
Recently, Piepoli and co-workers (28, 29) suggested that abnormalities
of muscle metabolism play a major role in the exertional dyspnea of
patients with CHF, launching the attractive "muscle hypothesis"
of exertional dyspnea (6, 7). These authors found that circulatory
occlusion virtually totally impeded the decrease of exertional
hyperventilation after peak exercise, until cuffs were deflated. They
concluded that circulatory occlusion, by trapping locally the products
of metabolism, led to an increased stimulation of muscle ergoreceptors.
This result was also found in normal subjects (28), in contrast to
previous studies (15, 18). It is difficult to reconcile our findings
with their results. We used maximal graded exercise, whereas they used
handgrip. The level of exercise was also much lower in their study
(peak exercise O2 was <500
ml/min) than in ours, which was done maximally, because we expected the
metabolites trapped within the muscles to be at the highest possible
concentration. Their exercise tests were performed with the arms and
with cuffs inflated at suprasystemic pressure. We used leg and arm
exercise, but we were unable to achieve circulatory occlusion of the
arms at suprasystemic pressure after exercise, because this maneuver
was extremely painful, and neither patients nor normal subjects
tolerated it for >30 s. However, 40-50 mmHg seems sufficient to
block venous return in the arm and to trap metabolites within the
muscles, which was the aim of the protocol. Piepoli et al. (28, 29)
stated that stimulation of nociceptive fibers could not explain the
persistent ventilatory response, inasmuch as heart rate did not
decrease more slowly with than without cuff inflation; however, the
fact that blood pressure during recovery was greater after cuff
inflation may suggest that pain indeed elicited a nociceptive response
that could by itself explain hyperventilation.
O2 and mainly
CO2 were also increased after
cuff inflation, which was in opposition to what others have found;
finally, this increased CO2
response at recovery could not be reproduced in the second study
performed in CHF patients. The relative level of persistent
hyperventilation in normal subjects and in CHF patients was compared
and found to be greater in CHF patients.
Despite the fact that the rate of decrease of ventilation after
exercise was not affected by cuff inflation, ventilation tended to be
lower than without cuff inflation at each measurement during recovery.
These results are thus in accordance with those reported by Rowell et
al. (31), Innes et al. (18), and Haouzi et al. (15). The mechanism of
reduction in E
during circulatory occlusion is still debated. It is classically
attributed to reduction of flow of known or unknown metabolites to the
arterial or central chemoreceptors (17).
H+ and
K+ have been incriminated, but a
discrepancy between the rate of lactate removal and ventilatory decline
has been usually found (27) and other mechanisms probably also operate.
Recently, it was demonstrated that chemoreceptor sensitivity was
increased in CHF patients (5), which may explain the greater
ventilatory response of CHF patients for a given amount of
CO2. NMR spectroscopy studies
demonstrated that the decrease in tissue pH is greater at peak exercise
in CHF patients than in normal subjects, suggesting greater production
of acid products (21, 24, 25). A recent work suggested that
ergoreceptor stimulation, assessed by microneurographic response, is
lower in CHF patients than in normal subjects (32). Therefore, a
decreased sensitivity of the muscle receptor in CHF may explain the
lower microneurographic response, despite increased production of
metabolites within the muscles.
Subjects were studied according to a fixed sequence with a test with cuff occlusion always following the baseline test without cuff occlusion. It is, however, unlikely that this has biased the study, inasmuch as most of the patients and subjects had been regularly exercised on a bicycle for other studies or in the setting of the regular evaluation of their disease. A familiarization effect was thus unlikely to have occurred. It is also unlikely that the difference in protocol between normal subjects and CHF patients may have confounded our results. Our study was not aimed at elucidating the various mechanisms responsible for the exertional dyspnea in CHF patients. Our results favor the hypothesis suggested by Rowell et al. (31) and Wasserman et al. (34, 35) of a predominant role of hyperventilation linked to CO2 production by a still unknown mechanism. The decrease in ventilation at a similar level of exercise found after training in CHF patients and attributed to improvement in muscle metabolism may be explained by reduced stimulation of aortic and carotid chemoreceptors secondary to reduced central delivery of CO2.
Conclusion. Cuff inflation of the legs or the arms at peak exercise does not retard the decline of ventilation in CHF patients or in normal subjects. This argues against a significant role of muscle ergoreceptors in genesis of the exercise hyperventilation of patients with CHF.
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ACKNOWLEDGEMENTS |
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The authors acknowledge the remarks and comments of Karlman Wasserman and Philippe Haouzi.
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FOOTNOTES |
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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: A. Cohen-Solal, Service de Cardiologie, Hôpital Beaujon, 100 Blvd. du General Leclerc, 92110 Clichy, France (E-mail: alain.cohen-solal{at}bjn.ap-hop-ap.fr).
Received 11 August 1998; accepted in final form 10 November 1998.
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Top
Abstract
Introduction
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Discussion
References
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