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Department of Physiology, McGill University, Montreal, Quebec, Canada H3G 1Y6
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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In a previous
study in conscious normoxic newborn rats, we found that the strength of
the Hering-Breuer reflex (HB reflex) was greater (188%) at high
(36°C) than at low (24°C) ambient temperature (Ta; D. Merazzi and J. P. Mortola.
Pediatr. Res. 45: 370-376, 1999).
We now asked what the effect would be of changes in
Ta during hypoxia. Rat pups at
3-4 days of age were studied in a double-chamber airflow
plethysmograph. The HB reflex was induced by negative body surface
pressures of 5 or 10 cmH2O and
quantified from the inhibition of breathing during maintained lung
inflation. Rats were first studied at
Ta = 32°C in normoxia,
followed by hypoxia (10% O2
breathing). During hypoxia, oxygen consumption (
O2) averaged 47%, and HB
reflex 115%, of the corresponding normoxic values, confirming that in
the newborn, differently from the adult, hypoxia does not decrease the
strength of the HB reflex. As hypoxia was maintained, lowering
Ta to 24°C or increasing it to
36°C, on average, had no significant effects on
O2 and the HB reflex.
However, with 5-cmH2O inflations,
the HB reflex during the combined hypoxia and hyperthermia was
significantly stronger than in normoxia. We conclude that in conscious
newborn rats during normoxia the
Ta sensitivity of the HB reflex is
largely mediated by the effects of
Ta on thermogenesis and
O2; in hypoxia, because thermogenesis is depressed and
O2 varies little with
Ta, the HB reflex is
Ta independent. The observation
that the reflex response to lung inflations during hypoxic hyperthermia
can be greater than in normoxia may be of importance in the
pathophysiology of apneas during the neonatal period.
control of breathing; neonatal respiration; thermoregulation; vagal reflexes
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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SINCE THE STUDIES BY HERING and Breuer 130 years ago,
it has been clear that vagal inputs from the lungs play a crucial role in the control of the breathing pattern. As inspiration progresses, the
gradual recruitment and increase in activity of the airway stretch
receptors inhibit inspiratory, and promote expiratory, activity,
culminating in the termination of inspiration and the onset of the
expiratory phase. When lung volume is maintained above the
end-expiratory level, the expiratory facilitation persists with an
absence of inspiratory movements [Hering-Breuer
expiratory-promoting reflex (HB reflex)] (28). The magnitude of
the reflex vagal inhibition of ventilation during the maintained
inflation reflects the interplay of numerous factors. In addition to
the degree of stimulation of the airways receptors, the hypoxic and
hypercapnic stimuli that gradually build during the ventilatory
inhibition are important in offsetting the vagal inputs (27). This
chemical "drive" results from the tissue oxygen consumption
(O2) and carbon dioxide
production (CO2); hence, the
level of metabolism should also play a role in determining the strength
of the HB reflex. Indeed, changes in metabolic rate and
chemosensitivity could explain why anesthesia and hypoxia were found
to, respectively, increase and decrease the effect of the vagal
inhibition in adult animals (i.e., Refs. 1, 20). In normoxic rat pups,
a rise in ambient temperature
(Ta) from 32 to 36°C
determined a drop in metabolic rate and an increase of the HB reflex;
the opposite occurred when temperature decreased (12). Therefore, these
results were also compatible with the possibility that changes in
metabolic rate played an important role in the temperature-mediated
changes in vagal inhibition.
In the present work we investigated the effects of changes in Ta on the HB reflex of the newborn during hypoxia. Differently from what is known to occur in adults, in 2- and 5-day-old newborn rats studied at thermoneutrality, hypoxia and hypercapnia failed to reduce the intensity of the HB reflex (11), presumably because of the low chemosensitivity in the early postnatal days (4, 11). Our interest in the interaction between hypoxia and temperature on vagal ventilatory inhibition was also motivated by reports that inhibition of breathing and fatal apnea in infants (sudden infant death syndrome) are often associated with signs of hypoxia and of hyperthermic conditions (24, 26).
In hypoxia in newborns, as in adults, the temperature set point of thermoregulation changes to a lower value (16). In fact, what is a normal thermal environment in a newborn during normoxia can be perceived as a hyperthermic condition during hypoxia (18, 21). As such, one may expect that an increase in temperature during hypoxia could enhance the HB reflex even more than in normoxia. On the other hand, because hypoxia depresses thermogenesis, changes in Ta result in much smaller changes in the rate of metabolism than during normoxia (14). Hence, if metabolic rate were a variable of major importance in determining the strength of the HB reflex, one could hypothesize that changes in Ta during hypoxia would affect the HB reflex much less than in normoxia. We tested this hypothesis in newborn rats during hypoxic conditions at Ta of 24, 32, and 36°C.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Experiments were performed in 85 newborn Sprague-Dawley rats from 20 litters, at 3 and 4 days of age (day 0 = day of birth), in either the morning or afternoon. Experiments were approved by the Animal Ethics Committee of McGill University. The pregnant dams had free access to food and water and were maintained in individual cages at Ta between 20 and 25°C, relative humidity of 50-53%, and a 12:12-h dark-light cycle.
The main group of rats was used for measurements of the HB reflex.
Separate groups of rats were used for measurements of body temperature
(Tb) and gaseous metabolism.
These measurements were performed at
Ta of 32°C, which is slightly
below thermoneutrality for rats of this age (14), first in normoxia for
20 min, followed by 20 min in hypoxia. Measurements were then continued
for a third period of 20 min, with hypoxia maintained, with one-half of
the rats at Ta = 24°C ("cold") and the
other one-half at Ta = 36°C ("warm"). Numbers of
animals, or sets of animals in the case of metabolic measurements, used
for each experiment are given in Table 1
and in the pertinent sections of
RESULTS.
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HB reflex.
The animal was placed in the rear chamber of a double-chamber
plethysmograph, identical to that previously adopted (11, 12). The
animal's head emerged into the front chamber by passing through
multiple layers of paraffin sealing film (Parafilm), which provided
complete separation of the rear from the front chamber. The front
chamber (~15 ml) was for measuring the airflow () via a small pneumotachograph connected to a differential pressure transducer (Validyne, Northridge, CA). Tidal volume
(VT) was obtained by
electronic integration of the signal. A steady
flow of 80 ml/min, controlled by a flowmeter, was continuously
delivered through the anterior chamber, to avoid any accumulation of
expired air. This flow consisted of either air, for the normoxic runs, or hypoxia, obtained by connecting the anterior chamber to an anesthesia bag filled with a calibrated 10%
O2 gas mixture.
, VT, P)
were recorded on paper (Gould pen recorder) at a speed of 25 mm/s (Fig.
1). Temperature was measured in both the
front and rear chambers by a small tungsten-constantan thermocouple
(DP30, Omega, Stamford, CT).
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Gaseous metabolism.
O2 and
CO2 were measured with an
open-flow system, with a setup and a methodology similar to that
previously adopted (12, 14). Rat pups were studied in sets of four
animals, with separators to impede huddling, the magnitude of which
influences metabolic rate and is affected by hypoxia (15, 22). The pups
were in the metabolic chamber, which was preset at
Ta = 32°C; 20 min in hypoxia
followed, and an additional 20 min of hypoxia in cold or warm
conditions. Gases were passed through a drying column, sampled by appropriate gas analyzers for measuring the
O2 and CO2 concentrations, and the values
were continuously displayed on a computer monitor.
O2 and
CO2 were computed over
several minutes as the product of the inflow-outflow gas concentration difference and the steady gas flow (235 ml/min) delivered through the
chamber. Metabolic data are presented normalized by the weight (in kg),
at STPD conditions. At the end,
Tb was measured in each pup.
Effects of changes of Ta on Tb. The animals were placed in the double-chamber plethysmograph, preset at 32°C, used for the measurements of the HB reflex. Rectal temperature was measured with a very fine tungsten-constantan thermocouple inserted about 15 mm in the rectum, and its value was taken as representative of Tb. Ta and Tb measurements were registered every 2 min for the entire 1-h experiment, i.e., 20 min in normoxia, 20 min in hypoxia, and an additional 20 min in hypoxia in either warm or cold conditions.
Statistical analysis. Data are presented as group means ± SE. The statistical significance of differences between two groups of data from the same animals was evaluated by two-tailed paired t-test. Comparisons between normoxia and hypoxia at each of the three temperatures (32, 36, and 24°C) were performed, first, by ANOVA; post hoc Bonferroni limitations were then applied to assess the statistical significance for the four comparisons of interest, i.e., each of the three hypoxic conditions vs. normoxia, and hypoxia-cold vs. hypoxia-warm. In all cases, a significant difference was considered at P < 0.05.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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HB reflex at 32°C: normoxia and hypoxia.
As expected (28), the IR was greater at 10 than at 5 cmH2O inflation pressures. On
average, the IR value in hypoxia was 115 ± 5% of normoxia, a
difference that was not statistically significant. When the two
inflation pressures were individually considered, IR at 5 cmH2O was significantly greater in
hypoxia than in normoxia (7.2 vs. 6.1, P < 0.05, Fig.
2), whereas at the higher pressure IR did
not differ significantly (14.7 vs. 14.6).
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HB reflex in hypoxia: effect of changes in Ta. During hypoxia, the effect of changes in Ta on the HB reflex varied depending on the inflation pressure (Fig. 2). At 5 cmH2O inflation, the reflex was significantly stronger in the warm than in the cold condition. In addition, in the warm condition, the reflex was stronger than during the control normoxic phase. At 10 cmH2O inflation, warming tended to have an opposite effect, i.e., that of reducing the strength of the reflex in comparison to cold, although it did not differ significantly from normoxia. On average, therefore, changes in Ta during hypoxia had minimal and insignificant effects on IR, which at 36°C averaged only 2% more than at 24°C.
In summary, IR during hypoxia was slightly greater than during normoxia at 32°C (Fig. 3, solid symbols) and by approximately the same amount at various Ta (+12% at 24°C, +15% at 32°C, +14% at 36°C). None of these changes, individually taken, reached statistical significance; only when all the results at the three Ta were combined did the overall effect of hypoxia indicate a significant increase in IR, on average by 14 ± 3% (P < 0.01). For comparison purposes, Fig. 3 also presents the data previously obtained in same-age rats during normoxia (12); with warming, IR increased, and in the cold condition it decreased, compared with the value at 32°C, and at 36°C it averaged 188% of the value at 24°C.
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Gaseous metabolism.
At 32°C, O2 in normoxia
averaged 55 ± 3 ml · kg
1 · min1;
during hypoxia it dropped to 26 ± 1 ml · kg1 · min1
(P < 0.01), or ~47% of normoxia.
This hypoxic value was not significantly altered by changes in
Ta. In fact, in cold and in warm
conditions, O2 averaged 24 ± 2 and 28 ± 2 ml · kg1 · min1,
respectively, with no significant difference between the two (Fig.
4).
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Effects of changes of Ta on
Tb.
At Ta = 32°C,
Tb was similar between normoxia
and hypoxia (33.5 ± 0.3 and 34.3 ± 0.3°C, respectively). At
the end of the warm and cold hypoxic phases,
Tb averaged 37.2 ± 0.2 and
29.7 ± 0.6°C, respectively (Fig. 5,
"basal measurements," 
). Similar
Tb values were recorded after the
measurements of metabolic rate and HB reflex (Fig. 5, filled symbols).
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The results of this study confirmed that, in conscious newborn rats, hypoxia does not reduce the strength of the HB reflex. They also indicated that during hypoxia temperature has very little effect on the intensity of the reflex. This latter result is in sharp contrast to the temperature sensitivity of the HB reflex during normoxia (Fig. 3).
During the apnea of the maintained lung inflation, oxygen is consumed and carbon dioxide is produced at a rate that depends on the metabolic processes. The animal's chemosensitivity eventually dictates the level of arterial hypoxia and hypercapnia at which the chemical drive overcomes the inhibitory inputs from the pulmonary stretch receptors. Hence, the HB reflex, quantified as the apnea during maintained lung inflation, reflects the balance between the stretch receptors' inhibition on breathing and the stimulation of breathing by the increasing chemical drive. The former depends on the magnitude of lung inflation and the degree of adaptation of the stretch receptors. The latter depends on chemosensitivity and metabolic rate. The interplay of these factors has been studied in conscious and anesthetized adult animals. A depression of chemosensitivity or a reduction in metabolic rate, as during anesthesia, increases the strength of vagal reflexes (1, 7, 19, 20). On the other hand, stimulation by hypoxia or hypercapnia reduces the HB reflex (1). In a previous study in conscious newborn rats at Ta = 32-34°C, the strength of the HB reflex was reduced by hypoxia at postnatal day 8, whereas it was not affected or even slightly increased in younger rats (11). Similarly, in the 3- and 4-day-old rats in the present study, hypoxia did not lessen, but, in fact, slightly increased, the strength of the HB reflex. The insensitivity of the HB reflex to hypoxia in the early neonatal period probably reflects the combination of the low ventilatory chemosensitivity and the hypometabolic response to hypoxia (4, 9, 13).
During hypoxia, increasing Ta to 36°C or lowering it to 24°C had insignificant effects on the HB reflex, which, at either of the above Ta, averaged approximately those at 32°C (Fig. 3, solid symbols). This lack of sensitivity to changes in Ta during hypoxia differs markedly from what has been previously observed in rats of the same age during normoxia (12), where the HB reflex significantly decreased in cold and increased in warm conditions (Fig. 3, open symbols). In fact, during normoxia at 36°C, IR averaged 188% of the value at 24°C, whereas during hypoxia at 36°C it was only 102% of, and not significantly different from, the value at 24°C. Hence, in the newborn rat, the temperature sensitivity of the HB reflex depends on the level of oxygenation, being very pronounced in normoxia and absent in hypoxia. Several factors, and their interplay, are likely to be responsible for this difference.
The Tb values presently observed in the hypoxic rats (Fig. 5) in cold and warm conditions are very similar to those previously measured in warm and cold conditions during normoxia (12). The changes in Tb with Ta and their similarities between normoxia and hypoxia are not surprising. In fact, in small newborn mammals, including the rat, Ta is of overwhelming importance in determining Tb, and the presence (i.e., in normoxia) or absence (i.e. in hypoxia) of the metabolic response to cold does not make any appreciable difference to the effect of Ta on Tb (14). The fact that, at the various Ta, Tb was approximately the same between normoxia and hypoxia, whereas the HB reflex was very different, should imply that Tb is not an important parameter in determining the strength of the HB reflex. This is surprising. In fact, temperature influences neuronal activity and could affect the HB reflex at multiple sites of the reflex loop, including the stretch receptors' sensitivity to lung inflation (2, 25) and the central effectiveness of vagal inputs (3, 5, 8, 29). Changes in temperature modify the breathing pattern and its response to chemical stimuli (10, 12, 16, 17); also, in normoxic cats under barbiturate anesthesia, changes in Tb have been shown to modify the central integration of the vagal reflexes (5, 6). One might postulate that Tb in the normoxic newborn, as in the adult, also has a direct effect on the intensity of the HB reflex and that this effect is shadowed by the large changes in metabolic level, which was very high in the cold and low in the warm condition. This interpretation, however, would not hold during hypoxia; in fact, in hypoxia, the metabolic level and the strength of the HB reflex were essentially constant and independent of temperature, despite the large changes in Tb. Hence, it seems reasonable to conclude that in the conscious newborn rat the effects of cooling and warming temperatures on the strength of the HB reflex cannot be attributable to the changes in Tb per se, but, rather, to the corresponding changes in metabolic rate. In normoxic conditions cooling stimulates and warming lowers metabolic rate, and the reflex becomes weaker and stronger, respectively. With hypoxia, the chemical stimuli from the peripheral chemoreceptors should reduce the strength of the HB reflex compared with normoxia, as it happens in adults (1, 20), but the drop in metabolic level offsets this effect. Finally, during hypoxia, because the metabolic responses to changes in temperature are suppressed, ambient cooling and warming have negligible effects on the intensity of the reflex.
The combined analysis of the results at the two inflation pressures revealed a small trend for the HB reflex to increase in hypoxia, independently of temperature. However, when the effects of raising Ta were separately analyzed at each of the two inflation pressures, a significant trend emerged indicating an increase in the reflex response to small inflations, and a slight drop with large inflations (Fig. 2). Airway tension is the stimulus activating the stretch receptors (23), and changes in the mechanical properties of the airways with temperature may have altered the pressure-tension relationship, but it is difficult to see how this could have resulted in opposite effects at the two inflation pressures. It is more likely that the higher pressures also stimulated the rapidly adapting irritant receptors, which are facilitatory in breathing (28), hence reducing the inhibition from the stretch receptors.
The observation that in the newborn rat hypoxia not only did not decrease but also could actually strengthen the intensity of the HB reflex when the temperature increased is of considerable interest. In fact, it implies that the vagal inhibition on ventilation in the early neonatal period can be increased when hypoxia is combined with hyperthermia, an association that has been often suspected in the pathophysiology of sudden infant death (24, 26). This could be important in the pathophysiology of neonatal apneas, particularly if one considers that hypoxia lowers the set point of thermoregulation; hence, even values of temperatures considered normal in normoxia can act as hyperthermic conditions during hypoxia (18, 21).
In conclusion, the present results in newborn rats have indicated that hypoxia did not decrease the intensity of the HB reflex and that changes in Ta between 24 and 36°C had no significant effects, contrary to what was previously observed during normoxia. The most likely interpretation is that, in addition to chemosensitivity, changes in metabolic rate play a most important role in determining the magnitude of the reflex and its Ta sensitivity. Finally, the observation that the reflex response to small lung inflations during hypoxic hyperthermia can actually be greater than in normoxia may be of importance in the pathophysiology of apneas during the neonatal period.
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ACKNOWLEDGEMENTS |
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The authors thank Lina Naso for technical assistance and Teresa Trippenbach for critical reading of the manuscript.
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FOOTNOTES |
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This study was supported by funds from the Medical Research Council of Canada. D. Merazzi was financially supported at McGill University by a grant from the Fondo J. Miglierina, Varese, Italy, and was on leave from Hospital S. Anna, Como, Italy.
Present address of D. Merazzi: Div. of Neonatology, Neonatal Intensive Care Unit, S. Anna Hospital, via Napoleona 60, 22100 Como, Italy.
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 correspondence: J. P. Mortola, Dept. Physiology, McGill Univ., McIntyre Basic Sciences Bldg., Rm. 1121, 3655 Drummond St., Montreal, Quebec, Canada H3G 1Y6 (E-mail: jacopo{at}med.mcgill.ca).
Received 30 December 1998; accepted in final form 29 June 1999.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Significantly
different from 24°C, P < 0.05.
), 32 (
), and 36°C (
). Open symbols, mean IR values previously
measured in same-age rats during normoxia: at 24 (
), equally expressed in percentage of corresponding values at
32°C (
