Background

It is well known that food intake influences several physiological parameters. For example, food intake increases metabolism and body temperature [1,2,3]. This is the so-called postprandial thermogenesis or thermic effect of food. We recently reported that food intake also influences the respiratory response at rest [1]—i.e., food intake increases minute ventilation (VE) in resting young individuals. In that study, we speculated that this elevation in VE was caused by an elevation in the H+ ion concentration related to increases in CO2 output (VCO2) and the plasma noradrenaline concentration [4], which can be induced by an increase in sympathetic nervous system activity [5]. Young adults in that study exercised at 50% of peak oxygen uptake 90 min after food intake, and the increase in metabolism elicited by the food intake was still present during the subsequent exercise. Interestingly, we found that although VCO2 and end-tidal PCO2 (PETCO2) were increased by food intake during exercise, VE was not [1]. On the other hand, when we previously compared the ventilatory responses during exercise with participants breathing CO2-enriched air or room air, we found that breathing CO2-enriched air elevated PCO2 and VE [6]. We have thus obtained differing results regarding the impact of CO2 on VE.

It has also been reported that respiratory chemosensitivity is subject to alteration by several factors. For example, it was reported that exercise (at 19%, 26%, and 34% of maximal oxygen uptake) increased respiratory chemosensitivity to CO2 relative to the resting state [7] and that a rise in body temperature of > 0.7 °C increased respiratory chemosensitivity to CO2 [8]. From these findings, it is plausible that respiratory chemosensitivity to CO2 is increased during exercise after food intake. However, our previous study [1] did not reveal higher VE during exercise after food intake. From that finding, we hypothesized that VE remains steady as a result of redundant compensatory mechanisms [1, 9]. On the other hand, Durand et al. [10] tested the effect of feeding on respiratory responses in the newborn infant and reported that feeding suppresses respiratory chemosensitivity to CO2. It is therefore possible that food intake suppresses respiratory chemosensitivity to CO2 in infants, though it remains unclear whether food intake changes respiratory chemosensitivity in adults. To address this issue, we compared respiratory chemosensitivity to CO2 measured before and after food intake in young adults.

Material and methods

Participants

Eleven healthy participants [four males and seven females, mean age = 21 ± 2 (SD) year; height = 169.0 ± 7.4 cm; weight = 59.7 ± 8.5 kg] participated in the study. None of the participants were smokers, and none were taking any medication. All of the female participants were studied within 10 days of menstruation, and none were taking oral contraceptives, which contain female hormones. The study was approved by the Research Ethics Committee of the University of Shizuoka and conformed to the provisions of the Declaration of Helsinki. Written informed consent was obtained from all participants.

Test meal

Test meals were designed for each participant. After estimating the basal metabolic rate for each subject using the equation of Ganpule et al. [11], we estimated the total energy expenditure by multiplying the estimated basal metabolic rate by the estimated average physical activity level [12]. For six of the participants, that factor was 1.75; for the remaining five, it was 2. The amounts of carbohydrate, protein, and fat in the meals were based on the Dietary Reference Intakes for the Japanese [13]. As a result, test meals contained 117.6 ± 17.4 g of carbohydrate, 30.9 ± 8.8 g of protein, and 20.2 ± 5.4 g of fat. The total energy content was 3332 ± 633 kJ.

Experimental design

The experiment was conducted in the morning, and the participants were all asked to abstain from strenuous exercise and not to consume any food or alcohol during the 12 h prior to the experiment. After each subject came to the laboratory, they voided urine, were weighed, and sat in a chair to rest for 30 min. During this period, a heart rate (HR) monitor (S810i, Polar, Finland) was attached. HR was recorded every 5 s during the experiment and was averaged over 30-s periods. Just before the measurements were begun, sublingual temperature (Tsl) data were collected via copper-constantan thermocouples, which were sampled every 1 s using a data logger system (WE7000, Yokogawa, Japan) and averaged over 30-s periods. A mass-flow sensor and a gas-sampling tube were then connected to the mask, after which respiratory chemosensitivity to CO2 was measured using a rebreathing method [14, 15]. Participants consumed test meals after the measurement. Tsl and respiratory chemosensitivity were then measured 90 min after eating using the same procedure. The experiments were carried out in an experimental laboratory maintained at 25 °C and 40–60% relative humidity.

Rebreathing test

The participants wore a mask connected to a closed one-way circuit with a 6-l rubber bag containing the test gas (7% CO2, 43% O2, 50% N2). For the first 5 min with the stopcock open (“the one-way rebreathing circuit”), the participants breathed room air to measure control ventilation values. The stopcock was then closed, and rebreathing was begun. Rebreathing was terminated when the inspired CO2 fraction reached 9.2%. Rebreathing time ranged from 4 to 6 min in each participant. Respiratory parameters and gas concentrations were monitored breath-to-breath (AE-310S, Minato Medical Science, Japan). This test was performed twice with a 20-min recovery period between tests, and the mean values were evaluated for respiratory chemosensitivity, which was calculated as the slope of the regression line relating PETCO2 to VE. Because a ventilatory recruitment threshold was observed at around PETCO2 = 45 mmHg in several participants, regression analyses were conducted with data for PETCO2 > 50 mmHg. Previous studies showed that there is no significant difference in respiratory chemosensitivity to CO2 between steady-state and rebreathing methods when they are used under normal acid-base conditions [16, 17]. Therefore, the present results are comparable to results obtained using steady-state methods.

Statistical analysis

All values are reported as means ± SD. Paired t tests were used to compare the “before food intake” and “after food intake” sessions among the measured variables. Values of P < 0.05 were considered significant.

Results

Baseline Tsl, HR, oxygen uptake (VO2), VCO2, VE, respiratory frequency (fR), and PETCO2 were all significantly higher during the session after food intake (Table 1). The baseline respiratory exchange ratio, tidal volume (VT), and end-tidal PO2 did not significantly differ between sessions.

Table 1 Baseline levels of the measured parameters
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Figure 1 shows the respiratory chemosensitivity to CO2. There was no significant between-session difference in respiratory chemosensitivity to CO2 (1.60 ± 0.62 l min−1 mmHg−1 in the before food intake session vs. 1.53 ± 0.77 l min−1 mmHg−1 in the after food intake session, P = 0.59, effect size d = 0.13). However, six of the 11 participants showed higher chemosensitivity before food intake.

Fig. 1
figure 1

Mean (± SD) respiratory chemosensitivity to CO2 before (blue circle) and after (red circle) food intake. Gray circles and lines depict individual data

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Conclusions

The present study showed that food intake leads to increases in Tsl, VO2, VCO2, VE, and PETCO2, which is consistent with earlier studies [1,2,3]. Moreover, the results suggest that the elevated VE is not caused by a change in respiratory chemosensitivity, and they support our earlier speculation that the elevation in VE is caused by increases in the H+ ion concentration and plasma noradrenaline concentration [1].

Our results showed that food intake did not influence respiratory chemosensitivity to CO2, which is in contrast to an earlier report [10]. It may be that this discrepancy reflects the difference in the type of food eaten by the participants. The infants who participated in the earlier study took in milk, while the young adults participating in the present study ate test meals containing rice, chicken, and other things. To test this idea, it will be necessary to examine the effect of different food types on respiration. Furthermore, food intake elicited an elevation in Tsl of only 0.3 °C in the present study. It is likely that no change in respiratory chemosensitivity can be explained by this small elevation in Tsl. Nonetheless, in infants, respiratory chemosensitivity to CO2 was changed by feeding, which suggests this change cannot be explained simply based on body temperature. To understand this discrepancy, it will be necessary to clarify the differences relating to respiration between young adults and infants.

González-Castillo et al. [18] compared the changes in gene expression that occur in the ventral respiratory column of the ventrolateral medulla, which is involved in determining respiratory rhythm and central chemoreception, between adult and neonatal rats. Their analysis confirmed the differential expression of 84 genes involved in the expression of neuronal ion (K+, Na+, and Ca2+) channels. Although it is not clear how these genes relate to respiratory chemosensitivity to CO2, it may be that the differences their expression relate to the different responses to CO2 in neonates and adults. Further study will be necessary to clarify the differences in respiratory control and to determine how respiratory chemosensitivity changes with aging.

In summary, our results suggest that food intake does not suppress respiratory chemosensitivity to CO2 in young adults, which is different from the situation in infants and suggests that respiratory chemosensitivity does not directly influence ventilatory responses after food intake. These observations do not support the hypothesis that blunted respiratory chemosensitivity to CO2 underlies the attenuation of the increase in VE during exercise after food intake. On the other hand, these results support the hypothesis that VE remains steady during exercise after food intake as a result of redundant mechanisms.