Abstract
To clarify the luteal-follicular and male–female differences in ventilatory and heart rate responses at the onset of exercise, seven women and seven men performed voluntary exercise and passive movement for 20 s (brief voluntary exercise and brief passive movement) and voluntary exercise for 3 min (long voluntary exercise) in a sitting position. Voluntary exercise consisted of alternate flexion-extensions of both lower legs with a weight corresponding to about 2.5% of the subjects' body mass attached to each ankle, at a frequency of about 60 times min−1. Passive movement was carried out without weights by experimenters pulling ropes attached to both of the subjects' ankles, in the same way as voluntary exercise. During these exercises and movements, minute inspiratory ventilation (V̇ I) and heart rate (HR) were continuously measured by breath-by-breath and beat-to-beat techniques. We calculated relative changes of V̇ I and HR (ΔV̇ I and ΔHR). Additionally, we averaged ΔV̇ I and ΔHR obtained during the exercise and movement for each subject, and performed a correlation analysis between the averaged ΔV̇ I and ΔHR. It was clarified that: (1) ΔV̇ I and ΔHR in the follicular phase were almost equal to those in the luteal phase; (2) there were no significant male–female differences in these parameters; (3) significant positive correlations were found in both genders only during brief voluntary exercise. We conclude that ventilatory and HR responses at the onset of voluntary exercise and passive movement are not affected by the menstrual cycle or gender.
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Introduction
In understanding physiological phenomena, gender difference is a very interesting and important topic. For example, White et al. (1983) observed lower ventilatory responses to hypoxia and hypercapnia in women than in men. Jones et al. (1999) reported that gender appeared to influence sympathetic and cardiovascular responses to various conditions (10, 12, 50%) of inspired oxygen levels. There have also been many studies about the effect of gender on minute ventilation and heart rate (HR) at the anaerobic threshold (AT) or at peak exercise in young people (Younis et al. 1990; Ogawa et al. 1992; Helgerud 1994; Rickli et al. 1997; Nindl et al. 1998). According to the results of those studies, while no gender effect seems to exist for HR at AT or peak levels of exercise, a male–female comparison of minute ventilation has been reported with various results.
It is a well-known physiological reaction that the transition from rest to light or moderate exercise is accompanied by a rapid increase in minute ventilation and HR. It has been shown that this abrupt increase in ventilation and HR usually occurs from the first breath (Eldridge and Waldrop 1991) and lasts for about 20 s, and is termed phase I (Whipp et al. 1982). This phase I response, from the first breath and lasting for about 20 s, is observed not only during voluntary exercise but also during passive movement following electrically induced muscle contractions or flexion-extensions of the lower legs with ropes (Adams et al. 1987; Miyamura et al. 1992). In past studies, it has been reported that the phase I response is influenced by various factors, e.g., posture (Weiler-Ravell et al. 1983), exercise frequency (Kelsey and Duffin 1992), exercise intensity (Miyamura et al. 1992), age (Ishida et al. 2000; Sato et al. 2000) and so on. To our knowledge, however, no study about the effect of gender on phase I response has been done.
Many investigators have pursued mechanisms that are responsible for the phase I response. At present, it is considered that two neural mechanisms, central command and peripheral reflex, mainly trigger the increase in ventilation and HR that appears at the onset of exercise (Mitchell 1990; Mateika and Duffin 1995). Central command arises from the activation of the cerebral cortex and hypothalamus (Goodwin et al. 1972). In contrast, peripheral reflex originates in the stimulation of group III (mechanoreceptor) and IV (metaboreceptor) muscle afferents (McCloskey and Mitchell 1972; Kaufman et al. 1983). Recently, Rabinowicz et al. (2002) have clarified the existence of gender difference in the structure of the human cerebral cortex. Hinojosa-Laborde et al. (1999), from previous reports about the sympathetic nervous system, suggest that females limit the activation or enhance the inhibition of the sympathetic nervous system more effectively than males. As it is thought that structure and function usually accompany each other, this male–female constructive difference in the cerebral cortex may have an effect on ventilatory and HR responses at the onset of exercise, and gender difference in the sympathetic nervous system may affect these responses.
However, in evaluating the phase I response in women, the menstrual cycle cannot be ignored because it is reported that female sex hormones act on the central nervous system. It has been shown in experiments with cats that progesterone exerts a respiratory effect on the hypothalamus (Bayliss et al. 1990) and that estrogen (17β-estradiol) attenuates the cardiovascular and ventilatory responses not to peripheral reflex but to central command (Hayes et al. 2002).
The purpose of the present study, therefore, was to clarify whether or not ventilatory and HR responses at the onset of voluntary exercise and passive movement differ (1) between the luteal and follicular phase and (2) between women and men.
Methods
Subjects
Seven women and seven men volunteered to participate in the present study. All women reported having a normal history of menstrual cycles. No subjects had a history of cardiorespiratory diseases, took medications that seriously affected cardiorespiratory responses and the menstrual cycle, or smoked. The subjects were informed of the experimental protocol and possible risks involved in this study before giving written consent. The ethics committee of the Research Center of Health, Physical Fitness and Sports at Nagoya University approved this study. The physical characteristics of the subjects are summarized in Table 1.
Menstrual cycle
In the current study, the timing of the menstrual cycle was initially indicated by a menstrual cycle history questionnaire. Secondly, it was confirmed by applying the methods described by Cunningham et al. (1978) and Frye and Kamon (1981), which are based on menses and ovulation. Although the aforementioned researchers estimated the dates of ovulation by a rise in basal temperature, we made our estimations not only through basal oral temperature measurements but also by the use of a Dotest LH ovulation predictor test kit (Rohto Pharmaceutical, Japan). This kit accurately detects the subject's luteinizing hormone (LH) surge by measuring their urinary LH concentration. The subjects were verbally told to test their urine right after waking up in the morning. They continued testing their urine every morning until the test indicated that they had a high concentration of LH, reflecting an LH surge, which predicted the subsequent occurrence of ovulation (Varma et al. 1983). The luteal phase and the follicular phase were defined as a period from the estimated date of ovulation to menses and from menses to the estimated date of ovulation, respectively.
Experimental procedure
The experimental procedure was designed by referring to methods of our previous studies (Miyamura et al. 1992; Ishida et al. 2000; Sato et al. 2000).
Voluntary exercise and passive movement
Subjects sat with their backs against an experimental chair with an electrogoniometer attached to the right knee joint during the experiment. During brief voluntary exercise, two weight belts, each equivalent to about 2.5% of subject's body mass, were bound around each ankle. These weights were given to equalize the relative load to muscles among the subjects. The subjects extended and relaxed both lower legs in an alternating pattern from ∼110° to 20° with an anatomically flexed position defined as 0°. The start of this exercise was signaled by the experimenter's voice before the start of inspiratory periods, and the exercise was made up of sets which continued for 20 s. Each set was 1 s and consisted of an extension and relaxation of first the right limb and then the left limb. The starting point, just before the start of the inspiratory periods, was determined by the respiratory flow curve monitored on an oscilloscope. Subjects were instructed to keep the upper body as still as possible.
Brief passive movement was achieved without weights by the experimenter alternately pulling ropes that were connected to the subject's ankles at the same pace, for the same length of time, and in the same posture as in the brief voluntary exercise. All subjects were directed to relax and not to resist the motion and care was taken to immobilize the body as much as possible to avoid motion artifacts.
Protocol
Preliminary testing was carried out to familiarize the subjects with the experimental procedures. The subjects practiced the brief voluntary exercise and the brief passive movement several times so as not to respond suddenly to experimenter's voice and the movement. The actual experiment was performed at least 2 h after each subject's last meal on a day different from the preliminary testing once for men and twice for women – once during the luteal phase and once during the follicular phase. The women participated in the experiment during the luteal and follicular phases which were also chosen in a random order. Each mode of brief voluntary exercise and passive movement was conducted after the subjects' HR and respiration were stable. Both brief voluntary exercise and passive movement were repeated seven times. To avoid a sequence effect, all the subjects performed brief voluntary exercise and passive movement in a random order. Finally, to evaluate actual exercise intensity during voluntary exercise, long voluntary exercise was conducted one time for 3 min in the same way as brief voluntary exercise, and the mean of the last 30 s (STD; 3 min steady-state value) of every cardiorespiratory parameter was analyzed. All parameters were measured in the same way as in brief voluntary exercise.
Measurements
Inspiratory minute ventilation (V̇ I), tidal volume (V T), inspiratory and expiratory period, and partial pressure of end-tidal carbon dioxide (P ETCO2) were measured by the breath-by-breath technique. A hot-wire flowmeter (Minato Ika-gaku, RF-H, Japan) was attached to a respiratory face mask. It was calibrated prior to each experiment using a 2-l calibration pump at different flow rates. The dead space of the respiratory face mask was about 100 ml. Respiratory gases were sampled using a thin vinyl tube (inner diameter 1 mm) inserted into the face mask, with the tip being positioned as close to each subject's mouth as possible. P ETCO2 was calculated from end-tidal CO2 %, which was obtained by analyzing gas samples being drawn continuously through the vinyl tube with the use of a gas analyzer (Minato Ika-gaku, MG-360, Japan). HR was measured beat-to-beat from the R spike using an electrocardiogram connected to a bioamplifier (Nihon Kohden, AB-621G, Japan).
All ventilatory and ECG signals were continuously displayed on the screen of an oscilloscope. They were converted from analogue to digital using an A-D converter (Canopus, ADX-98H, Japan) at a sampling frequency of 100 Hz throughout one set of voluntary exercise and passive movement. V T was determined by digitally integrating the airflow signals. Respiratory frequency (f) was calculated from total respiratory time. V̇ I was obtained as the product of V T and f. These data were stored on a hard disk unit, and analyzed afterwards on a personal computer (NEC, PC-9821Xa, Japan).
Data analysis and statistics
Measured values were expressed with means (SE). First, breath-by-breath and beat-to-beat data were aligned with the onset of brief voluntary exercise and passive movement and linearly interpolated between each breath and beat to yield data points at 1-s intervals. Then the mean values were calculated for each subject. Thereafter, the mean values for men, the luteal phase, and the follicular phase were computed from the average values of the individuals. The values for women were defined as the average values of the luteal and follicular phases. From the above analyses, we obtained absolute changes during brief voluntary exercise and passive movement for women and men. We also calculated the increasing rates of V̇ I and HR. They were obtained by dividing STD by resting values (Rest) and the values were defined as an index of exercise intensity. Rest was defined as the averages of the 30-s values before brief voluntary exercise and passive movement.
Second, we calculated relative changes of V̇ I and HR (ΔV̇ I and ΔHR) during brief voluntary exercise and passive movement for women and men. ΔV̇ I and ΔHR in brief voluntary exercise were expressed as a fraction (%) of absolute changes to STD. In this case STD was defined as 100%. ΔV̇ I and ΔHR in brief passive movement were obtained by calculating a ratio (%) of absolute changes to resting values (Rest), which was defined as 0%. ΔV̇ I and ΔHR were defined as ventilatory and HR responses at the onset of voluntary exercise and passive movement in the present study. In addition, response time (RT) was calculated to investigate the kinetics of V̇ I and HR by referring to the methods reported by Ishida et al. (2000). They obtained RT by calculating the time to reach one-half of the gain, which was the value of the relative change at 15 s after the start of exercise and movement. In the present study, RT was defined as the time to reach one-half of the differences between ΔV̇ I at 15 s and ΔV̇ I at 0 s, and between ΔHR at 15 s and ΔHR at 0 s. To confirm whether or not absolute changes were significant when compared to Rest, one-way ANOVA with repeated measures was conducted and Dunnet's t-test (post hoc) was carried out for parameters in which significant differences were recognized. To evaluate differences between the luteal and follicular phase, a Wilcoxon signed rank test was used. In comparing women with men, Mann-Whitney's U test was used. The comparisons between the luteal and follicular phase and between women and men consisted of three analyses: (1) comparing ΔV̇ I and ΔHR, (2) comparing Rest, STD, and the increasing rate, and (3) RT.
Finally, to investigate whether or not gender differences were recognized in the relationship between ΔV̇ I and ΔHR, we calculated the averages of 20 s ΔV̇ I and ΔHR values (aΔV̇ I and aΔHR) for brief voluntary exercise and passive movement for each subject, displayed them as a scatter plot, and performed linear regression and correlation analysis. These statistical analyses were calculated by computer software (SPSS 10.0, SPSS) and the level of significance (significant P level) was set at 5%.
Results
Absolute changes
Figure 1 shows absolute changes of V̇ I and HR during brief voluntary exercise and passive movement in the luteal and follicular phases. Both V̇ I and HR significantly (P<0.05) increased in both phases at 1 s after the onset of brief voluntary exercise and passive movement, compared with Rest. P ETCO2 did not significantly change in either phase from Rest [luteal phase: 37.6 (1.0) mmHg, means (SE); follicular phase: 37.7 (1.0) mmHg] during brief voluntary exercise. Similar results were observed during brief passive movement, when Rest was 37.5 (0.67) mmHg in the luteal phase and 37.3 (1.3) mmHg in the follicular phase.
Figure 2 indicates absolute changes of V̇ I and HR during brief voluntary exercise and passive movement in women and men. V̇ I in the female group significantly rose from 6.98 (0.43) to 8.92 (0.53) l min−1 at 1 s after the onset of brief voluntary exercise. Similarly, a significant increase in V̇ I in the male group was recognized at 1 s after the onset of brief voluntary exercise, compared with Rest [from 8.27 (0.35) to 10.1 (0.60) l min−1]. P ETCO2 did not significantly change in either gender when compared with Rest [women: 37.7 (0.84) mmHg, men: 39.1 (1.1) mmHg]. A significant absolute change in V̇ I was observed at 1 s after the onset of brief passive movement for women and at 2 s for men, compared with Rest [women: from 6.49 (0.32) to 7.43 (0.46) l min−1, men: from 7.50 (0.29) to 9.12 (0.48) l min−1]. HR significantly increased at 1 s after the onset of brief voluntary exercise in both genders, compared with Rest [women: from 67.2 (3.6) to 76.4 (3.7) beats min−1, men: 69.2 (4.8) to 80.4 (4.9) beats min−1]. On the other hand, during brief passive movement, a significant absolute change in HR was observed at 1 s after the onset of brief passive movement in the female group and at 2 s in the male group, compared with Rest [women: 65.0 (3.8) to 69.5 (4.1) beats min−1, men: from 68.1 (5.1) to 75.6 (4.9) beats min−1]. No significant changes were detected for P ETCO2 when compared with Rest [women: 37.4 (0.67) mmHg, men: 38.1 (1.2) mmHg].
Rest, STD, and the increasing rate
Table 2 describes Rest, STD, and the increasing rate of V̇ I and HR during voluntary exercise. There was no significant difference in Rest of V̇ I between the luteal and follicular phases [luteal phase: 7.00 (0.56) l min−1, follicular phase: 6.96 (0.33) l min−1]. Similarly, significant luteal–follicular differences were not recognized for STD or for the increasing rate of V̇ I. Rest of V̇ I in women was not significantly different from that in men. In addition, although there was a gap in the increasing rate of V̇ I between women and men, the gap was not significant. However, a significant male–female difference was recognized in STD of V̇ I [women: 13.1 (1.2) l min−1, men: 19.8 (2.4) l min−1, P<0.05]. No luteal–follicular or male–female differences were detected in any calculation related to HR.
Rest of V̇ I and HR during brief passive movement were similar between the luteal and follicular phases [V̇ I; luteal phase: 6.39 (0.44) l min−1, follicular phase: 6.59 (0.28) l min−1, HR; luteal phase: 64.0 (4.0) beats min−1, follicular phase: 66.0 (4.2) beats min−1]. There were no significant differences in Rest of V̇ I or HR during brief passive movement between women and men [V̇ I; women: 6.49 (0.32) l min−1, men: 7.50 (0.29) l min−1, HR; women: 65.0 (3.8) beats min−1, men: 68.1 (5.1) beats min−1]. No luteal–follicular or male–female differences in P ETCO2 at rest were detected in either brief voluntary exercise or passive movement.
Relative changes
Figure 3 identifies relative changes of V̇ I and HR (ΔV̇ I and ΔHR) during brief voluntary exercise and passive movement in the luteal and follicular phases. No significant luteal–follicular differences were detected in any of the parameters.
Similarly, ΔV̇ I and ΔHR in the female group and in the male group are indicated in Fig. 4. Except for the point marking 2 s in the comparison between women and men for ΔHR in brief passive movement [women: 4.6 (1.9)%, men: 11.5 (2.9)%, P<0.05], no significant male–female differences were detected in any of the parameters.
Response time
Figure 5 shows the response time (RT) of V̇ I and HR. RT of V̇ I in the luteal phase during brief voluntary exercise [1.96 (1.06) s] and brief passive movement [1.37 (0.33) s] was not significantly different from that in the follicular phase during brief voluntary exercise [1.17 (0.51) s] or brief passive movement [1.30 (0.35) s]. No luteal–follicular difference in RT of HR was detected during either brief voluntary exercise [luteal phase: 1.24 (0.30) s, follicular phase: 1.97 (0.61) s] or brief passive movement [luteal phase: 1.01 (0.38) s, follicular phase: 1.20 (0.51) s]. There were no significant differences in RT of V̇ I or HR during brief voluntary exercise between women and men [V̇ I; women: 1.57 (0.48) s, men: 2.19 (0.59) s, HR; women: 2.10 (0.55) s, men: 2.43 (0.54) s]. In addition, when comparing them between women and men during brief passive movement, no significant differences were observed [V̇ I; women: 1.31 (0.33) s, men: 1.87 (0.56) s, HR; women: 0.90 (0.35) s, men: 1.87 (1.23) s].
Relationships between ventilatory and HR responses
Figure 6 represents the results of calculating the averages of ΔV̇ I and ΔHR (aΔV̇ I and aΔHR) during brief voluntary exercise and passive movement for each subject, displaying aΔV̇ I and aΔHR as a scatter plot, and, additionally, performing a linear regression and correlation analysis between them. In brief voluntary exercise, significant positive correlations between aΔV̇ I and aΔHR were found in both genders [women: r=0.92; P<0.01, men: r=0.82; P<0.05]. No significant male–female differences were observed between regression lines [women: aΔHR=0.39·aΔV̇ I+63.4, men: aΔHR=0.37·aΔV̇ I+64.3]. In brief passive movement, no significant correlations were recognized but a tendency for correlation was found in women (P=0.07).
Discussion
In the present study, ventilatory and HR responses at the onset of voluntary exercise and passive movement were evaluated using ΔV̇ I and ΔHR because, in spite of there being no significant differences, there were gaps in increasing rates of V̇ I and HR, indices of exercise intensity, between women and men particularly in the increasing rate of V̇ I during voluntary exercise. Similarly, these responses were evaluated in brief passive movement with ΔV̇ I and ΔHR. Two major findings were identified. First, ventilatory and HR responses at the onset of voluntary exercise and passive movement were not affected by the menstrual cycle when ΔV̇ I and ΔHR were regarded as an index of these responses. Second, these responses did not differ between women and men when ΔV̇ I and ΔHR in women were compared with those in men. Additionally, there were no significant differences in the response time (RT) as an index of V̇ I and HR kinetics between the luteal and follicular phases or between women and men.
Effect of menstrual cycle
In the present study, there were no significant differences in resting ventilation or P ETCO2 between the luteal and follicular phases. This result does not agree with many reports that say resting ventilation was elevated and resting PCO2 (P ETCO2,arterial PCO2, or alveolar PCO2) was lower during the luteal phase of the menstrual cycle (Regensteiner et al. 1989; Tatsumi et al. 1995; Beidleman et al. 1999; Loeppky et al. 2001). However, several studies (White et al. 1983; Chen and Tang 1989; Edwards et al. 1996) do not report any significant luteal–follicular differences in resting ventilation. Among them, White et al. (1983) identified significantly lower resting P ETCO2 in the luteal phase compared with the follicular phase. In contrast, Edwards et al. (1996) observed no significant difference in resting P ETCO2 between the luteal and follicular phases. Although, at present, we cannot explain this discrepancy based on the physiological backgrounds, the differences in experimental designs may have led to this discrepancy. In addition, the present study observed no significant luteal–follicular differences in resting HR. This result coincides with studies of Edwards et al. (1996), whereas Hessemer and Brück (1985) observed significantly higher resting HR in the luteal phase than in the follicular phase. Further investigation is needed about the effect of the menstrual cycle on resting ventilation and HR.
In the present study, two forms of exercise were performed: one was voluntary exercise and the other was passive movement. It is considered that brief voluntary exercise mobilizes not only peripheral reflex but also central command and that brief passive movement is a form of movement in which peripheral reflex functions almost exclusively (Miyamura et al. 1992; Ishida et al. 2000). Recently, Hayes et al. (2002) administered estrogen (17β-estradiol) to decerebrate male cats and examined the cardiovascular and ventilatory responses while stimulating parts related to central command and peripheral reflex for 60 s every 15 min. They reported that estrogen attenuated these responses to central command but not to peripheral reflex. However, no significant differences in ΔV̇ I and ΔHR were observed between the luteal and follicular phases for either voluntary exercise or passive movement (Fig. 3). One possible reason for the discrepancy between the Hayes et al. (2002) study and the present study is related to the differences in experimental design. Their experiment dramatically increased the concentration of estrogen over a short of time by giving it to the male cats as a bolus. This type of increase may be necessary to facilitate the attenuating effect of estrogen on the cardiovascular and ventilatory responses to central command. They also suspect from their results that the effects of estrogen on neural functions are maximized by their approach. Another possible reason for this discrepancy is that the effect of this attenuation on ventilatory and heart rate responses is small over a short period of exercise and movement. That is, even an attenuated central command might be able to cause the cardiovascular and ventilatory responses observed at the onset of exercise. Ettinger et al. (1998) investigated whether cardiovascular and muscle sympathetic nerve activity (MSNA) responses differed between the menstrual and follicular phases when women performed 2 min of static handgrip exercise at 30% maximal voluntary contraction (MVC), and observed no influence of the menstrual cycle on HR response. However, further investigations about the effects of estrogen on cardiorespiratory responses are necessary.
Gender difference
In previous studies, it has been frequently reported that gender does not affect HR at AT or during maximal exercise in young people, whereas the results of studies about the effect of gender on minute ventilation at AT and maximal exercise have been conflicting (Younis et al. 1990; Ogawa et al. 1992; Helgerud 1994; Rickli et al. 1997; Nindl et al. 1998). In the present study, it was demonstrated, for the first time, that ventilatory and HR responses at the onset of voluntary exercise and passive movement did not differ between women and men.
To our knowledge, there have been no studies about the difference in ventilatory response between women and men either at the onset of exercise or during exercise over a 2- or 3-min period. However, Ettinger et al. (1996) compared women's cardiovascular and MSNA responses with men's when subjects performed a 2-min static handgrip exercise at 30% MVC. The result was that the HR response of women was not different from that of men throughout the exercise. The results of the present study and Ettinger et al. (1996) indicate that ventilatory and circulatory responses to a short period of exercise and movement would not be affected by gender. In other words, it is suggested that an input from central command and peripheral reflex to the cardiorespiratory center would not differ between women and men when voluntary exercise and passive movement are performed for short amounts of time.
We investigated whether or not gender difference existed in the relationship between ventilatory response and HR response. As shown in Fig. 6, significant correlations between aΔV̇ I and aΔHR during brief voluntary exercise were recognized both in women (r=0.92, P<0.01) and in men (r=0.82, P<0.05), but not during brief passive movement. Fontana et al. (1993) observed significant positive correlations between the increase in V̇ I and that in HR during the final 30 s of 3 min of static handgrip exercises at 25% and 30% MVC but not at 15% MVC. Their study and the present study demonstrate that a relationship like this is observed not only during static exercise for a few minutes but also at the onset of voluntary exercise and that it is not recognized unless exercise over a certain intensity is performed. However, the linear regression equation of brief voluntary exercise for women (aΔHR=0.39·aΔV̇ I+63.4) was almost equal to that for men (aΔHR=0.37·aΔV̇ I+64.3) (Fig. 6). We have no information to explain this point. Nevertheless, Fontana et al. (1993) suggest that the relationship between ventilatory response and HR response is caused by a considerable degree of coordination and integration of respiratory and cardiovascular functions at a central level, despite the possibility of a differential control. If so, it would be possible that this coordination and integration of respiratory and circulatory centers occurred to the same extent in women and men.
In conclusion, the present study aimed to clarify whether or not ventilatory and HR responses at the onset of voluntary exercise and passive movement differed (1) between the luteal and follicular phase and (2) between women and men. It has been found that they are not affected by the menstrual cycle and that these responses in women are similar to those in men.
References
Adams L, Guz A, Innes JA, Murphy K (1987) The early circulatory and ventilatory response to voluntary and electrically induced exercise in man. J Physiol (Lond) 383:19–30
Bayliss DA, Cidlowski JA, Millhorn DE (1990) The stimulation of respiration by progesterone in ovariectomized cat is mediated by an estrogen-dependent hypothalamic mechanism requiring gene expression. Endocrinology 126:519–527
Beidleman BA, Rock PB, Muza SR, Fulco CS, Forte VA Jr, Cymerman A (1999) Exercise V̇ E and physical performance at altitude are not affected by menstrual cycle phase. J Appl Physiol 86:1519–1526
Chen H, Tang Y (1989) Effects of the menstrual cycle on respiratory muscle function. Am Rev Respir Dis 140:1359–1362
Cunningham DJ, Stolwijk JAJ, Wenger CB (1978) Comparative thermoregulatory responses of resting men and women. J Appl Physiol 45:908–915
Edwards N, Wilcox I, Polo OJ, Sullivan CE (1996) Hypercapnic blood pressure response is greater during the luteal phase of the menstrual cycle. J Appl Physiol 81:2142–2146
Eldridge FL, Waldrop TG (1991) Neural control of breathing during exercise. In: Whipp BJ, Wasserman K (eds) Exercise: pulmonary physiology and pathology. Marcel Dekker, New York, pp 309–370
Ettinger SM, Silber DH, Collins BG, Gray KS, Sutliff G, Whisler SK, McClain JM, Smith MB, Yang QX, Sinoway LI (1996) Influences of gender on sympathetic nerve responses to static exercise. J Appl Physiol 80:245–251
Ettinger SM, Silber DH, Gray KS, Smith MB, Yang QX, Kunselman AR, Sinoway LI (1998) Effects of the ovarian cycle on sympathetic neural outflow during static exercise. J Appl Physiol 85:2075–2081
Fontana GA, Pantaleo T, Bongianni F, Cresci F, Manconi R, Panuccio P (1993) Respiratory and cardiovascular responses to static handgrip exercise in humans. J Appl Physiol 75:2789–2796
Frye AJ, Kamon E (1981) Responses to dry heat of men and women with similar aerobic capacities. J Appl Physiol 50:65–70
Goodwin GM, McCloskey DI, Mitchell JH (1972) Cardiovascular and respiratory responses to changes in central command during isometric exercise at constant muscle tension. J Physiol (Lond) 226:173–190
Hayes SG, Pino NB, Kaufman MP (2002) Estrogen attenuates the cardiovascular and ventilatory responses to central command in cats. J Appl Physiol 92:1635–1641
Helgerud J (1994) Maximal oxygen uptake, anaerobic threshold and running economy in women and men with similar performances level in marathons. Eur J Appl Physiol 68:155–161
Hessemer V, Brück K (1985) Influence of menstrual cycle on thermoregulatory, metabolic, and heart rate responses to exercise at night. J Appl Physiol 59:1911–1917
Hinojosa-Laborde C, Chapa I, Lange D, Haywood JR (1999) Gender differences in sympathetic nervous system regulation. Clin Exp Pharmacol Physiol 26:122–126
Ishida K, Sato Y, Katayama K, Miyamura M (2000) Initial ventilatory and circulatory responses to dynamic exercise are slowed in the elderly. J Appl Physiol 89:1771–1777
Jones PP, Davy KP, Seals DR (1999) Influence of gender on the sympathetic neural adjustments to alterations in systemic oxygen levels in humans. Clin Physiol 19:153–160
Kaufman MP, Longhurst JC, Rybicki KJ, Wallach JH, Mitchell JH (1983) Effects of static muscular contraction on impulse activity of groups III and IV afferents in cats. J Appl Physiol 55:105–112
Kelsey CJ, Duffin J (1992) Changes in ventilation in response to ramp changes in treadmill exercise load. Eur J Appl Physiol 65:480–484
Loeppky JA, Scotto P, Charlton GC, Gates L, Icenogle M, Roach RC (2001) Ventilation is greater in women than men, but the increase during acute altitude hypoxia is the same. Respir Physiol 125:225–237
Mateika JH, Duffin J (1995) A review of the control of breathing during exercise. Eur J Appl Physiol 71:1-27
McCloskey DI, Mitchell JH (1972) Reflex cardiovascular and respiratory responses originating in exercising muscle. J Physiol (Lond) 224:173–186
Mitchell JH (1990) Neural control of the circulation during exercise. Med Sci Sports Exerc 22:141–154
Miyamura M, Ishida K, Yasuda Y (1992) Ventilatory response to the onset of passive and active exercise in human subjects. Jpn J Physiol 42:607–615
Nindl BC, Sharp MA, Mello RP, Rice VJ, Murphy MM, Patton JF (1998) Gender comparison of peak oxygen uptake: repetitive box lifting versus treadmill running. Eur J Appl Physiol 77:112–117
Ogawa T, Spina RJ, Martin WH III, Kohrt WM, Schechtman KB, Holloszy JO, Ehsani AA (1992) Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation 86:494–503
Rabinowicz T, Petetot J McD-C, AIBMS, Gartside PS, Sheyn D, Sheyn T, de Courten-Myers GM (2002) Structure of the cerebral cortex in men and women. J Neuropathol Exp Neurol 61:46–57
Regensteiner JG, Woodard WD, Hagerman JV, Weil JV, Pickett CK, Bender PR, Moore LG (1989) Combined effects of female hormones and metabolic rate on ventilatory drives in women. J Appl Physiol 66:808–813
Rickli H, MacCarter DJ, Maire R, Amann FW, Candinas R (1997) Age and sex related changes in heart rate to ventilation coupling: implications for rate adaptive pacemaker algorithms. PACE 20:104–111
Sato Y, Katayama K, Ishida K, Miyamura M (2000) Ventilatory and circulatory responses at the onset of voluntary exercise and passive movement in children. Eur J Appl Physiol 83:516–523
Tatsumi K, Hannhart B, Moore LG (1995) Influences of sex steroids on ventilation and ventilatory control. In: Dempsey JA, Pack AI (eds) Regulation of breathing, 2nd end. Marcel Dekker, New York, pp 829–864
Varma TR, Patel RH, Everard DM (1983) The correlation between LH determination in the urine (Hi-Gonavis) and serum LH, FSH, oestradiol, progesterone, prolactin levels, and vaginal cytology at midcycle. Int J Fertil 28:243–246
Weiler-Ravell D, Cooper DM, Whipp BJ, Wasserman K (1983) Control of breathing at the start of exercise as influenced by posture. J Appl Physiol 55:1460–1466
Whipp BJ, Ward SA, Lamarra N, Davis JA, Wasserman K (1982) Parameters of ventilatory and gas exchange dynamics during exercise. J Appl Physiol 52:1506–1513
White DP, Douglas NJ, Pickett CK, Weil JV, Zwillich CW (1983) Sexual influence on the control of breathing. J Appl Physiol 54:874–879
Younis LT, Melin JA, Robert AR, Detry JMR (1990) Influence of age and sex on left ventricular volumes and ejection fraction during upright exercise in normal subjects. Eur Heart J 11:916–924
Acknowledgements
We appreciate the cooperation of the subjects in the present study. We also would like to thank Miss H. Shirafuji for assistance with the present study and Mr. J. Myerson for reviewing the English in the manuscript. This research was supported in part by a Grant-in-Aid for Science Research from the Japanese Ministry of Education, Science and Culture (Grant no. 12480009, 13680020, and 13878007).
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Matsuo, H., Katayama, K., Ishida, K. et al. Effect of menstrual cycle and gender on ventilatory and heart rate responses at the onset of exercise. Eur J Appl Physiol 90, 100–108 (2003). https://doi.org/10.1007/s00421-003-0873-8
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DOI: https://doi.org/10.1007/s00421-003-0873-8