Vol. 87, Issue 4, 1428-1432, October 1999
INVITED REVIEW
Hyperbaric bradycardia and hypoventilation in exercising men:
effects of ambient pressure and breathing gas
Dag
Linnarsson,
Anders
Östlund,
Folke
Lind, and
Carl
Magnus
Hesser
Section of Environmental Physiology, Department of Physiology
and Pharmacology, Karolinska Institutet, SE-171 77 Stockholm, Sweden
 |
ABSTRACT |
We sought to determine whether
hydrostatic pressure contributed to bradycardia and hypoventilation in
hyperbaria. Eight men were studied during exercise at 50, 150, and 250 W while breathing 1) air at 1 bar,
2) helium-oxygen
(He-O2) at 5.5 bar,
3) sulfur hexafluoride-oxygen
(SF6-O2)
at 1.3 bar, and 4) nitrogen-oxygen (N2-O2)
at 5.5 bar. Gas densities were pairwise identical in
1) and
2), and
3) and
4), respectively. Increased
hydrostatic pressure to 5.5 bar resulted in a modest but significant
relative bradycardia on the order of 6 beats/min, in both the absence
[1) vs.
2),
P = 0.0015] and presence
[3) vs.
4),
P = 0.029] of gases that are both denser than normal and mildly narcotic. In contrast, ventilatory responses appeared not to be influenced by hydrostatic pressure. Also,
the combined exposure to increased gas density and mild-to-moderate inert gas narcosis at a given hydrostatic pressure
[1) vs.
3), 2) vs.
4)] caused bradycardia
(P = 0.032 and 0.061, respectively) of
similar magnitude as 5.5-bar hydrostatic pressure. At the same time
there was relative hypoventilation at the two higher workloads. We
conclude that heart rate control, but not ventilatory control, is
sensitive to relatively small increases in hydrostatic pressure.
exercise; heart rate; hydrostatic pressure; density; inert gas
| |
INTRODUCTION |
BRADYCARDIA IS COMMONLY observed in divers both at rest
and during exercise (16). Apnea and head immersion are known to induce
bradycardia as an important part of the diving reflex (18). However,
also during dry compression and normal breathing, humans show
bradycardia at rest and during exercise (16). At pressures corresponding to extremely deep diving, a remarkable degree of bradycardia has been observed. Thus, for a given oxygen uptake (
O2) during exercise, Salzano
et al. (30) observed >30 beats/min lower heart rates (HR) at 31.6 bar
(1,000-ft seawater) than during surface control. Lafay et al. (17)
observed not only bradycardia but also other electrocardiographic
abnormalities in subjects during dry compression to 72 bar.
Because of the complexity of the hyperbaric environment, the cause of
the bradycardia is not obvious. Part of the bradycardia with hyperbaric
air has been shown to be caused by the hyperoxia (9), but substantial
degrees of bradycardia have also been observed in humans during
hyperbaric exposure with normoxic or near-normoxic gas mixtures (2, 16,
30). The non-O2-dependent bradycardia thus must be caused by other factors, such as the increased
hydrostatic pressure, the increased gas density, or the increased
partial pressure of metabolically inert gas(es) alone or in
combination. Other contributing factors could be the thermal
conductivity of the ambient gas and of the breathing gas, especially if
these gases are helium (He). The present study was undertaken in an
attempt to define the contribution of hydrostatic pressure in
hyperbaric bradycardia while maintaining constancy of breathing gas
density, ambient gas composition, and inspired gas temperature. All
measurements have been performed during normoxic exercise to
standardize metabolic conditions. The same approach has been used also
to study respiratory control. Although the effects of increased gas
density on respiration are fairly well understood, the possible
influences of hydrostatic pressure on respiration have hitherto not
been studied.
Our findings show that increased hydrostatic pressure causes relative
bradycardia in exercising men, but we found no influences of
hydrostatic pressure on concomitant ventilatory responses. The effects
of increased gas density and inert gas narcosis could not be separated,
but together they caused further bradycardia and a marked reduction in
ventilatory responses.
| |
METHODS |
Subjects.
Eight healthy male subjects were studied. Their age, weight, and height
ranged from 27 to 34 yr, 73 to 96 kg and 174 to 186 cm, respectively.
All had diving experience and had given their informed consent in
agreement with the procedures required for approval by the ethical
review board of Karolinska Institutet.
Equipment and procedure.
The experimental conditions with four different breathing gas mixtures
and three different ambient pressures are shown in Table
1, including partial pressures and
densities of inspired gases. All gas mixtures were normoxic and
contained either nitrogen (air;
N2-O2),
helium (He-O2), or sulfur
hexafluoride
(SF6-O2) as the inert dilutient gas. The
SF6 that was used in one of the breathing gas mixtures had undergone a special certification procedure, including batch analysis and bioassay, to acertain that no toxic impurities were present (Montefluos, Italy).
In each condition, the subject exercised continuously at three
successive workloads, 50, 150, and 250 W, on an electrically braked
cycle ergometer (Siemens Elema, Sweden). The duration of exercise at
each workload was 5 min, to attain a physiological steady state. All
experiments were performed in an
8-m3 hyperbaric chamber filled
with air. Subjects breathed the 37°C humidified premixed gas from a
Douglas bag by means of wide-bore tubing, a breathing valve, and a
mouthpiece. Exercise was preceded by 15 min washin of the gas mixture.
Ventilatory responses were measured as previously reported by Lind et
al. (20). In brief, inspired gas flow was measured with a Venturi-type
flowmeter, and an automatic pneumatic valve intermittently occluded the
inspiratory conduit to permit an assessment of central inspiratory
activity from inspiratory occlusion pressure after 0.1 s
(P0.1). HR was obtained from an
electrocardiogram by using precordial electrodes. Steady-state
recordings of ventilatory variables and HR were obtained during
minutes 4 and
5 of exercise at each workload.
Maximum voluntary ventilation (MVV) was determined 5 min before the
onset of exercise and during continued exercise at 250 W after
ventilatory and HR recordings had been completed. Each subject
participated in four experimental sessions on separate days, one for
each condition, and in random order.
Rationale of experimental design.
Basically, our purpose was to study effects of hydrostatic pressure in
the absence (1.0-bar air vs. 5.5-bar
He-O2) and presence (1.3-bar
SF6-O2
vs. 5.5-bar
N2-O2)
of a raised gas density and mild-to-moderate gas narcosis (Table 1).
Apart from HR and ventilation to quantify bradycardia and
hypoventilation, P0.1 and
exercise-induced changes in MVV were measured to assess possible
alterations of central inspiratory activity and exercise-induced
bronchodilation (14). The hyperbaric pressure level was chosen as that
giving a normoxic
N2-O2
mixture the same density as a normoxic
SF6 mixture in which
SF6 partial pressure
did not exceed atmospheric pressure. This limitation, in turn, was
dictated by our desire to avoid potential decompression problems with
SF6 after long-term exposure and
severe exercise. Also, 5.5 bar is the pressure at which a normoxic
He-O2 mixture has the same density
as air at 1.0 bar. An additional and more complex consideration were
the narcotic properties of the two high-density gas mixtures. In terms
of psychomotor performance, a significant impairment by 20-30%
would be expected with the present partial pressures of
SF6 and hyperbaric
N2 (27). Similar levels of inert
gas sedation have also been shown to be associated with alterations of
cardiovascular (6, 26) and temperature (23) control. Therefore, inert
gas sedation will be considered in our analysis, together with
hydrostatic pressure and density, as a possible cause of bradycardia
and hypoventilation.
Statistical analysis.
Data were analyzed by using a two-way, repeated-measures design of
analysis of variance (Statistica 5.1, Statsoft, Tulsa, OK). The
experimental design included two factors, exercise intensity (50, 150, and 250 W) and gas+pressure condition (1.0-bar air, 5.5-bar
He-O2, 1.3-bar
SF6-O2,
and 5.5-bar
N2-O2).
In case of significant effect of a factor, post hoc pairwise
comparisons were tested for significance by using Dunnett's test.
Significance was accepted at the P < 0.05 level.
| |
RESULTS |
Respiratory and HR responses to exercise with the four different
pressure and gas combinations are given in Table
2, and differences in ventilation
(I) and HR from air control are shown in
Figs. 1 and
2.
View larger version (20K):
[in this window]
[in a new window]
|
Fig. 1.
Differences in heart rate ( HR) between 1-bar air (control) and 3 gas+pressure conditions with normal (5.5-bar
He-O2) or 5.5 times increased
gas density (1.3-bar
SF6-O2,
5.5-bar
N2-O2).
Error bars, SE. There was no interaction between effects of
gas+pressure condition and exercise intensity on HR.
Inset: matrix of significances for
differences between gas+pressure conditions. n.s., Not significant.
|
|
View larger version (16K):
[in this window]
[in a new window]
|
Fig. 2.
Differences in exercise ventilation
(I)
between same conditions as in Fig. 1. Brackets indicate significance of
differences between normal-density (control, 5.5-bar
He-O2) and high-density conditions (1.3-bar
SF6-O2, 5.5-bar
N2-O2).
|
|
HR (Fig. 1) was reduced by ~11 beats/min with 5.5-bar
N2-O2
and by ~6 beats/min with 5.5-bar
He-O2 and 1.3-bar
SF6-O2
compared with 1.0-bar air. These pressure and gas effects did not
differ at different exercise intensities.
The general pattern of spontaneous ventilatory responses was that the
conditions with high-density and inert gas narcosis led to significant
and practically identical respiratory reductions compared with air
control, especially at the two higher exercise intensities. Respiratory
data obtained with 5.5-bar He-O2,
on the other hand, were identical to those in air control at 1.0 bar.
Therefore, respiratory variables will be analyzed in terms of a
comparison between high-density (1.3-bar
SF6-O2,
5.5-bar N2-O2)
and normal-density (1.0-bar air, 5.5-bar
He-O2) conditions.
Ventilation (Fig. 2) showed a significant interaction between exercise
condition and pressure+gas conditions
(P < 0.001), with reductions of 12 and 21% at 150 and 250 W, respectively, in the high-density conditions
compared with the normal-density conditions.
Respiratory rate (RR) (Table 2) showed a significant interaction
between exercise condition and pressure+gas conditions
(P = 0.002), with greater relative
reduction in RR in the high-density conditions as exercise intensity
was increased from 50 to 150 W
(P = 0.013) and 250 W
(P = 0.010).
Tidal volume and inspiratory time-to-total time ratio showed no
significant differences between pressure+gas conditions, so that
differences in
I between
high-density and normal-density conditions were entirely due to
proportional differences in RR, with equal changes in inspiratory and
expiratory durations.
P0.1 showed significant
interaction between exercise intensity and pressure+gas condition
(P = 0.049), with increasingly greater differences between normal-density and high-density conditions as
exercise intensity was increased from 50 (P = 0.002) to 150 (P = 0.012) and 250 W
(P = 0.005).
MVV in the high-density-conditions was markedly reduced to ~50% of
that in the normal-density conditions
(P < 0.001). Compared with resting
conditions, MVV increased on the average 15-19 l/min during
exercise, and there was no difference in this exercise-induced increase
between conditions.
| |
DISCUSSION |
Hydrostatic pressure.
The principal finding of this study was that increased hydrostatic
pressure per se induced a bradycardia in exercising men (Fig. 1). Such
bradycardia was observed both in the presence and in the absence of
concomitant mild-to-moderate inert gas narcosis and concomitantly
elevated gas density, as evidenced by a comparison between conditions
of equal gas density but with different hydrostatic pressures. A
hydrostatic pressure of 5.5 times normal ambient pressure represents a
very modest elevation compared with the conditions used in most animal
and tissue experiments in which hydrostatic-pressure-induced
alterations of the function of excitable tissues have been observed
(11, 12, 22, 24, 31, 32), but those researchers who have investigated
animal models in this relatively low range of hydrostatic pressure (1,
29, 31) have found marked changes in cardiac function at pressures as low as 5 atmospheres.
The observation that the difference in HR between conditions was
independent of work intensity suggests that a similar type of
bradycardia would also be observed at rest. Indeed, relative bradycardia is also commonly observed in resting divers (16). Bradley
et al. (2) found bradycardia of similar magnitude as in the present
He-O2 experiments in both resting
and exercising subjects breathing 0.3-bar
O2 in 4.3-bar He compared with
air-breathing control.
Our conclusion that increased hydrostatic pressure induces bradycardia
in exercising men rests on the presumption that the two low-density
conditions and the two high-density conditions differ in no other way
than in hydrostatic pressure. Thus the He atmosphere is presumed to
have no narcotic or other pharmacological effects at ~5-bar partial
pressure. This presumption is supported by the fact that He has never
been shown to exert any net narcotic effects even at pressures of
>100 bar in animal models (4). Against this presumption is the
observation that unanesthetized rats breathing He at atmospheric
pressure have bradycardia compared with air-breathing control animals
(19). Our interpretation, however, is strengthened by the observation
that a hydrostatic pressure increase from 1.3 bar with
SF6-O2
to 5.5 bar with
N2-O2 also causes bradycardia, clearly without any involvement of He.
Also, our conclusion that hydrostatic pressure causes bradycardia in
the combined presence of raised gas density and mild-to-moderate inert
gas narcosis rests on the presumption that the narcotic effect of
101-kPa SF6 is equivalent to that
of 525-kPa N2. Although not
studied with respect to possible influences on cardiac function, the
narcotic effect of SF6 in terms of
psychomotor impairment has been found to be approximately eight times
larger than that of N2 per unit
partial pressure (27). Thus the degree of inert gas narcosis was
similar but not identical in the two high-density conditions.
The present approach, with its comparison of conditions of equal gas
density and similar degrees of inert gas sedation, precludes the
establishment of a possible dose-response relationship between HR and
hydrostatic pressure. An alternative approach, however, has been
applied by Bradley et al. (2) and Salzano et al. (30). These authors
studied HR responses to exercise in a wide range of ambient pressures
up to 30.6 bar (30), where the gas densities of the near-normoxic
He-O2 breathing mixtures varied
with ambient pressure. On the assumption that HR was influenced by the
increased density in proportion to the
O2 cost of breathing the dense
gas, HR responses were analyzed as a function of
O2. For a given O2 during submaximal
exercise, HR was decreased by 6 beats/min at 4.6 bar (2), by 14-16
beats/min at 9.2-18.4 bar (2), and by 25-35 beats/min at 31.6 bar (30) These data support the notion of a dose-dependent effect of
hydrostatic pressure on HR.
Reasoning similar to that applied to HR can be used to explain the
respiratory responses (Fig. 2, Table 2). Conditions with identical gas
density showed practically identical responses at all three workloads
despite fivefold differences in hydrostatic pressure. This permits the
conclusion that differences in hydrostatic pressure between 1.0-bar air
and 5.5-bar He-O2 and 1.3-bar
SF6-O2 and 5.5-bar
N2-O2,
respectively, had no effect on respiratory responses. These respiratory
responses include exercise hyperpnea, load-compensatory increases in
central inspiratory activity, and exercise-induced enhancement of MVV.
Density and inert gas narcosis.
The present findings of reduced ventilation at the two higher workloads
and reduced MVV in the two high-density conditions agree well with
previous data obtained under similar conditions (8, 9, 15, 21). Even
though the present experimental design does not allow us to distinguish
the specific influences of density and narcotic properties of the
respired gas, data from other experiments in which degrees of inert gas
narcosis similar to those in the present experiments were obtained with
N2O inhalation while normal gas
density was maintained; Bradley and Dickson (3) and Fothergill and
Carlson (10) reported slightly increased ventilation in exercising
subjects during inhalation of 15-30% N2O. Fothergill and Carlson also
showed that the respiratory response to inspiratory flow-resistive
loading was unchanged with 23%
N2O compared with air breathing.
During resting conditions, responses to inspiratory loading have been
found to be maintained with 39% inspired
N2O (25). In summary, therefore,
on the assumption that N2O results
are representative for similar degrees of narcosis with
N2 and
SF6, inert gas narcosis is not
likely to have contributed to the relative hypoventilation in the
present high-density experiments.
Much less is known regarding possible effects of breathing gas
properties on circulatory responses. Apart from possible narcotic influences on central control or effector organ level (6, 26, 28),
there are multiple levels on which neural and mechanical outputs of
respiration may interact with cardiovascular function with primary or
secondary effects on HR. These levels include modulation by central
inspiratory activity on the vagal control of HR and effects of
breath-synchronous alterations of right ventricular diastolic filling
on left ventricular output, with secondary baroreflex-induced HR
variations (33). Several studies report data on HR during flow-resistive loading. Dressendorfer et al. (5) found no change in HR
when inspiratory flow-resistive loading was imposed on subjects during
submaximal exercise. Fothergill and Carlson (10) have shown similar
results. Hesser et al. (13) studied bradycardic responses to 6.3-bar
N2 in sitting and standing
subjects with and without
CO2-induced hyperpnea. They found
the same degree of hyperbaric bradycardia in normocapnic eupnea and
hypercapnic hyperpnea, suggesting that the increased respiratory neural
and mechanical output had no net effect on the hyperbaric bradycardia during concomitant hypercapnia. Furthermore, they found that the bradycardia associated with inhalation of 6.3-bar
N2 developed gradually over time
at a rate suggesting that uptake of
N2 in relatively slowly
equilibrating tissues influenced the degree of bradycardia. These
observations suggest that, apart from increased hydrostatic pressure,
it is the narcotic property of the inert gas rather than the density
and its associated effects on respiration that contributes to the
hyperbaric bradycardia. In contrast to these findings with hyperbaric
N2, measurements of steady-state exercise HR during inert gas narcosis with
N2O and normal gas density provide
little support for the notion that inert gas narcosis causes
bradycardia. Bradley and Dickson (3) found an unchanged HR with 15 and
30% N2O compared with air in
subjects exercising at 65 and 135 W. Fothergill and Carlson found no
differences in steady-state-exercise HR values between air and 23%
N2O. In a recent study in our
laboratory, subjects exercising at 100-W intensity had identical
steady-state HR and blood pressures with and without 30%
N2O in both upright and supine
postures (26).
In contrast to steady-state HR, HR responses to baroreflex stimuli have
been shown to be modified by inhalation of subanesthetic N2O concentrations. Thus Ebert (6)
demonstrated that, in resting humans, tachycardic responses to
hypotensive stimuli were attenuated, and Östlund et al. (28)
came to a similar conclusion. In exercising men, Östlund and
Linnarsson (26) found not only attenuations of HR responses to both
hyper- and hypotensive stimuli but also a prolongation of the
baroreflex response latency with inhalation of 30%
N2O. The observation by Hesser et
al. (13) that 6.3-bar N2 induces a
more marked bradycardic effect in the standing than in the sitting
position lends further support to the notion that attenuated baroreflex
responses of HR contribute to hyperbaric bradycardia. The consistent
absence of steady-state bradycardia with
N2O, in contrast to hyperbaric
N2, and, in the present study, also to SF6, might be explained by
the intrinsic sympathostimulatory effect of
N2O (7), which may offset any
bradycardic effects arising from baroreflex attenuation.
However, possible intrinsic sympathoexcitatory effects of
N2 and
SF6 have never been directly
analyzed. Therefore, the above tentative explanation of the mechanisms
for N2- and
SF6-induced relative bradycardia
and the absence of bradycardia in subjects breathing
N2O remains to be established experimentally.
Conclusions.
Elevated hydrostatic pressure evoked bradycardia in exercising men. A
narcotic influence of inert gas may contribute further to hyperbaric
bradycardia, but this latter effect cannot be separated from possible
influences of increased gas density. Ventilatory responses to exercise
appear not to be influenced by elevated hydrostatic pressure in the
present range.
| |
ACKNOWLEDGEMENTS |
This study was supported by Swedish Medical Research Council Grant 5020.
| |
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: D. Linnarsson,
Section of Environmental Physiology, Dept. of Physiology and
Pharmacology, Karolinska Institutet, SE-171 77 Stockholm, Sweden
(E-mail: Dag.Linnarsson{at}fyfa.ki.se).
Received 26 January 1999; accepted in final form 17 June 1999.
| |
REFERENCES |
1.
Ask, J. A.,
and
I. Tyssebotn.
Positive inotropic effect on the rat atrial myocardium compressed to 5, 10 and 30 bar.
Acta Physiol. Scand.
134:
277-283,
1988[Medline].
2.
Bradley, M. E.,
N. R. Anthonisen,
J. Vorosmarti,
and
P. G. Linaweaver.
Respiratory and cardiac responses to exercise in subjects breathing helium-oxygen mixtures at pressures from sea level to 19.2 atmospheres.
In: Underwater Physiology. Proceedings of the Fourth Symposium on Underwater Physiology, edited by C. J. Lambertsen. New York: Academic, 1971, p. 325-337.
3.
Bradley, M. E.,
and
J. G. Dickson, Jr.
The effects of nitrous oxide narcosis on the physiologic and psychologic performance of man at rest and during exercise.
In: Underwater Physiology V, edited by C. J. Lambertsen. Bethesda, MD: Fed. Am. Soc. Exp. Biol., 1976, p. 617-626.
4.
Brauer, R. W.,
P. M. Hogan,
M. Hugon,
A. G. MacDonald,
and
K. W. Miller.
Patterns of interaction of effects of light metabolically inert gases with those of hydrostatic pressure as such.
Undersea Biomed. Res.
9:
353-395,
1982[Medline].
5.
Dressendorfer, R. H.,
C. E. Wade,
and
E. M. Bernauer.
Combined effects of breathing resistance and hyperoxia on aerobic work tolerance.
J. Appl. Physiol.
42:
444-448,
1977[Abstract/Free Full Text].
6.
Ebert, T. J.
Differential effects of nitrous oxide on baroreflex control of heart rate and peripheral sympathetic nerve activity in humans.
Anesthesiology
72:
16-22,
1990[Medline].
7.
Ebert, T. J.,
and
J. P. Kampine.
Nitrous oxide augments sympathetic outflow: direct evidence from human peroneal nerve recordings.
Anesth. Analg.
69:
444-449,
1989[Abstract/Free Full Text].
8.
Fagraeus, L.
Maximal work performance at raised air and helium-oxygen pressures.
Acta Physiol. Scand.
91:
545-556,
1974[Medline].
9.
Fagraeus, L.,
C. M. Hesser,
and
D. Linnarsson.
Cardiorespiratory responses to graded exercise at increased ambient air pressure.
Acta Physiol. Scand.
91:
259-274,
1974[Medline].
10.
Fothergill, D. M.,
and
N. A. Carlson.
Effects of N2O narcosis on breathing and effort sensations during exercise and inspiratory resistive loading.
J. Appl. Physiol.
81:
1562-1571,
1996[Abstract/Free Full Text].
11.
Gennser, M.,
and
H. C. Örnhagen.
Effects of hydrostatic pressure, H2, N2, and He, on beating frequency of rat atria.
Undersea Biomed. Res.
16:
153-164,
1989[Medline].
12.
Gennser, M.,
and
H. Ch.
Örnhagen. Effects of hydrostatic pressure and inert gases on twitch tension.
Undersea Biomed. Res.
16:
415-426,
1989[Medline].
13.
Hesser, C. M.,
L. Fagraeus,
and
D. Linnarsson.
Respiratory gases and hyperbaric bradycardia.
Méd. Aéronautique Spatiale Méd. Subaquatique Hyperbare
17:
110-113,
1978.
14.
Hesser, C. M.,
F. Lind,
and
B. Faijerson.
Effect of exercise and raised air pressures on maximal voluntary ventilation.
In: Proceedings of the 5th Annual Scientific Meeting of the European Undersea Biomedical Society, edited by J. Grimstad. Bethesda, MD: Undersea Med. Soc., 1980, p. 203-212.
15.
Hesser, C. M.,
D. Linnarsson,
and
L. Fagraeus.
Pulmonary mechanics and work of breathing at maximal ventilation and raised air pressure.
J. Appl. Physiol.
50:
747-753,
1981[Abstract/Free Full Text].
16.
Hong, S. K.,
P. B. Bennett,
K. Shiraki,
Y.-C. Lin,
and
J. R. Claybaugh.
Mixed-gas saturation diving.
In: Handbook of Physiology. Environmental Physiology. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 4, vol. II, chapt. 44, p. 1023-1048.
17.
Lafay, V.,
P. Barthelemy,
B. Comet,
Y. Frances,
and
Y. Jammes.
ECG changes during the experimental human dive HYDRA 10 (71 atm/7,200 kPa).
Undersea Hyperbaric Med.
22:
51-60,
1995[Medline].
18.
Lin, Y.-C.,
and
S. K. Hong.
Hyperbaria: breath-hold diving.
In: Handbook of Physiology. Environmental Physiology. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 4, vol. II, chapt. 42, p. 979-998.
19.
Lin, Y.-C.,
and
E. N. Kato.
Effects of helium gas on heart rate and oxygen consumption in unanesthetized rats.
Undersea Biomed. Res.
1:
281-290,
1974[Medline].
20.
Lind, F. G.,
A. B. Truvé,
and
B. P. O. Lindborg.
Microcomputer-assisted on-line measurement of breathing pattern and occlusion pressure.
J. Appl. Physiol.
56:
235-239,
1984[Abstract/Free Full Text].
21.
Linnarsson, D.,
and
L. Fagraeus.
Maximal work performance in hyperbaric air.
In: Underwater Physiology V, edited by C. J. Lambertsen. Bethesda, MD: Fed. Am. Soc. Exp. Biol., 1976, p. 55-60.
22.
Lundgren, C. E. G.,
and
H. C. Örnhagen.
Heart rate and respiratory frequency in hydrostatically compressed, liquid-breathing mice.
Undersea Biomed. Res.
3:
303-320,
1976[Medline].
23.
Mekjavic, I. B.,
and
C. J. Sundberg.
Human temperature regulation during narcosis induced by inhalation of 30% nitrous oxide.
J. Appl. Physiol.
73:
2246-2254,
1992[Abstract/Free Full Text].
24.
Örnhagen, H. C.,
and
S. B. Sigurdsson.
Effects of high hydrostatic pressure on rat atrial muscle.
Undersea Biomed. Res.
8:
113-120,
1981[Medline].
25.
Östlund, A.,
and
D. Linnarsson.
Responses of respiratory drive and breathing pattern to inspiratory loading during nitrous oxide and isoflurane sedation.
Acta Anaesthesiol. Scand.
42:
1043-1049,
1998[Medline].
26.
Östlund, A.,
and
D. Linnarsson.
Slowing and attenuation of baroreflex heart rate control with nitrous oxide in exercising men.
J. Appl. Physiol.
87:
830-834,
1999[Abstract/Free Full Text].
27.
Östlund, A.,
D. Linnarsson,
F. Lind,
and
A. Sporrong.
Relative narcotic potency and mode of action of sulfur hexafluoride and nitrogen in humans.
J. Appl. Physiol.
76:
439-444,
1994[Abstract/Free Full Text].
28.
Östlund, A.,
P. Sundblad,
A. Demetriades,
and
D. Linnarsson.
Arterial baroreflex control during mild to moderate nitrous oxide narcosis.
Undersea Hyper. Med.
26:
15-20,
1999.
29.
Risberg, J.,
and
I. Tyssebotn.
Hyperbaric exposure to a 5 ATA He-N2-O2 atmosphere affects the cardiac function and organ blood flow distribution in awake trained rats.
Undersea Biomed. Res.
13:
77-90,
1986[Medline].
30.
Salzano, J.,
E. M. Overfield,
D. C. Rausch,
H. A. Saltzman,
J. A. Kylstra,
J. S. Kelley,
and
J. K. Summitt.
Arterial blood gases, heart rate, and gas exchange during rest and exercise in men saturated at a simulated seawater depth of 1,000 feet.
In: Underwater Physiology. Proceedings of the Fourth Symposium on Underwater Physiology, edited by C. J. Lambertsen. New York: Academic, 1971, p. 347-356.
31.
Stuhr, L. E. B.,
J. A. Ask,
and
I. Tyssebotn.
Increased cardiac contractility in rats exposed to 5 bar.
Acta Physiol. Scand.
136:
167-178,
1989[Medline].
32.
Stuhr, L. E. B.,
J. A. Ask,
and
I. Tyssebotn.
Cardiovascular changes in anesthetized rats during exposure to 30 bar.
Undersea Biomed. Res.
17:
383-393,
1990[Medline].
33.
Toska, K.,
and
M. Eriksen.
Respiration-synchronous fluctuations in stroke volume, heart rate and arterial pressure in humans.
J. Physiol. (Lond.)
472:
501-512,
1993[Abstract/Free Full Text].
J APPL PHYSIOL 87(4):1428-1432
8570-7587/99 $5.00
Copyright © 1999 the American Physiological Society
TOP
ABSTRACT
INTRODUCTION
