Over the years, evidence has accumulated to suggest that ovarian hormones may influence performance and substrate metabolism during rest and during exercise. Numerous empirical data have been provided, referring to changes in metabolic and cardiorespiratory variables (4,9,10,12-14,23,30-34,37,40,44,46) associated with the menstrual cycle.
During the menstrual cycle, specifically the follicular phase (FP) and the luteal phase (LP), the effects on maximal performance capacity (5,23) have only been reported in a few cases. A study by Brutsaert et al. (5), who investigated native women at high altitude (3600 m), reports a higher maximal power output in the LP compared with the FP. Another investigation by Jurkowski et al. (23) reports longer exercise duration in LP during constant-load tests at 90% V˙O2max. The majority of investigations document no significant changes in maximal performance or maximal exercise duration (4,10,13,30,34,40) during the menstrual cycle. Bemben et al. (4) and McCracken et al. (30) found no changes in running time to exhaustion during a maximal treadmill test between FP and LP. Other studies using cycle ergometry to exhaustion have not revealed significant differences in maximal power output (10,34) or time to exhaustion (4,13,40). Maximal oxygen consumption (V˙O2max) determined in test protocols (treadmill, cycle ergometry) has produced only limited evidence (16) of an influence of menstrual cycle phases on V˙O2max. Most of the investigations have not found statistically significant changes in V˙O2max during FP and LP (4,10,12,13,23,34,40,44).
Our interest focus was on ventilatory drive and blood lactate concentration (LA), because endurance capacity is often based on cardiorespiratory and LA measures. Schoene et al. (37) found a higher ventilatory drive (for V˙E and V˙E/V˙O2) at rest, at different submaximal stages, and at maximal load in LP. A similar result (higher V˙E and V˙E/V˙O2 in the LP) has been reported by Takase (40) during rest and during peak exercise. Dombovy et al. (13) have demonstrated significantly higher V˙E and V˙E/V˙CO2 in LP when performing constant-load exercise bouts of 4 min on a cycle ergometer at several submaximal loads (highest intensity: 75% V˙O2max). Williams and Krahenbuhl (44) have presented a significantly higher V˙E in the LP during treadmill running at 55 and 80% of V˙O2max. Redman et al. (34) found higher maximal V˙CO2 and V˙E in LP and no difference in V˙O2max. In contrast, De Souza et al. (12) report no influence of menstrual cycle on V˙E during treadmill running at maximal effort versus 80% V˙O2max.
Research literature addressing lactate concentration throughout the menstrual cycle is also inconsistent. Redman et al. (34) report no significant differences in LA at rest, at lactate threshold (LT), and at the end of the exercise when comparing LA responses in FP with those in LP. They only found a significantly higher LA in FP when changes in LA were modeled as a single exponential function. Jurkowski et al. (23) observed higher LA levels in FP during rest and at exhaustion, but not at constant-load exercise (one third and two thirds of maximal power output). McCracken et al. (30) found significantly higher values for LA at 3 and 30 min of recovery in FP after exhaustive exercise on a treadmill. Others have reported a significant increase in LA in the FP during maximal and submaximal work when subjects ran at 80% V˙O2max on a treadmill (12) and during rowing ergometer performance at fixed exercise intensities (8). Numerous investigators have reported no changes in lactate concentration during the menstrual cycle (4,10,12). Dean et al. (10) found no differences in LA at rest, at the respective anaerobic threshold (AT), or at exhaustion when comparing early FP, mid FP, and mid LP. Others have reported no changes in LA (FP vs LP) at rest and postexercise LA, using a treadmill test to exhaustion (4) during constant submaximal exercise for 60 min at 60% V˙O2max (25) and during treadmill running at maximal performance at an intensity of 80% V˙O2max (12). The above-listed divergences in literature regarding energy supply in the course of menstrual cycle may have been influenced by methodological procedures, such as nutrition before and during exercise testing (45).
Contrasting the inconsistencies in research literature, it is reasonable to ask whether cycle phases should be considered when testing eumenorrheic women. Only a few investigations have focused on the determination of the aerobic-anaerobic transition during different cycle phases (4,10,14,34,46). Dean et al. (10), Redman et al. (34), and Zderic et al. (46) have determined the LT to be the last workload before an upward shift in plasma LA occurred. In other investigations (4,14), the ventilatory AT has been determined using the methodology presented by Wasserman et al. (43). On the basis of the determination of individual thresholds of energy supply, these investigators did not find significant differences in threshold performance.
From the physiological point of view, the LT, as well as the AT, represent the first breakpoint of metabolic energy supply (the transition from the aerobic to the aerobic-anaerobic transition phase). In our investigation, an additional approach was used; it was based on two three-phase models of the aerobic-anaerobic transition as described by Skinner and McLellan (39). Using the three-phase models for both LA and respiratory gas-exchange measures (2,35,39,43), we additionally determined two second breakpoints, which demarcate the second phase of energy supply (the "compensated phase" of aerobic-anaerobic energy supply) from the third phase (the decompensation phase (2,35,39,43)). These second breakpoints are termed the respiratory compensation point (RCP) (2,39,43) and the lactate turnpoint 2 (LTP2) (35).
However, these breakpoints of aerobic-anaerobic transition (AT, LTP1, RCP, LTP2) represent alterations in energy substrate mobilization and use (2,35,39,43). As exercise intensity increases, these energy substrate alterations indicate important implications for exercise science, as well as occupational, preventive, and rehabilitative medicine. Evidence suggests that the second breakpoints of aerobic-anaerobic transition (RCP and LTP2), which occur at higher intensities than AT or LT, may be influenced by menstrual cycle phases. We based our reasoning on previous findings that have reported changes in LA with increasing load intensities. Zderic et al. (46) found no significant differences in LA during constant-load exercise at 70% of measured LT, but differences reached significance at 90% of LT with higher values in FP. Redman et al. (34) investigated 20 min of constant-load cycle ergometry exercise at 25 and 75% of V˙O2max and did not find differences in LA response at 25% V˙O2max, but they found significantly higher LA after 15 and 20 min of exercise at 75% V˙O2max in the FP.
Considering the empirical data described above, the aims of this study were 1) to study the metabolic and cardiorespiratory responses during different phases of energy supply in the FP and LP of the menstrual cycle on the basis of strict dietary control, and 2) to examine whether the results of exercise testing based on different physiological variables and different methods of breakpoint determination are influenced by a normal menstrual cycle. In contrast to previous studies, we also investigated two three-phase models of energy supply. To our knowledge, these models have not been investigated using this methodological approach.
Twenty-two eumenorrheic healthy women volunteered for this study. Only women who reported a regular menstrual cycle during the last 6 months were recruited. Further exclusion criteria included the use of oral contraceptives during the last 6 months, or pregnancy. During the study, three subjects had to be excluded, two because sex hormone concentrations were outside the normal range in LP (27) before exercise testing, and the other because of pregnancy. The remaining 19 subjects (mean ± SD: age 26.6 ± 2.0 yr; height 167.4 ± 3.0 cm) reported an average weekly training time of 353.3 ± 206.4 min·wk−1. Subjects participated in a wide spectrum of sports activities. Endurance sports were most frequently reported, encompassing 219.0 ± 195.0 min·wk−1, or approximately 62% of all sports activities. The weight of subjects was 63.1 ± 6.4 kg in the FP and 63.0 ± 6.3 kg in the LP. All participants were fully informed of the study's purpose and possible risks before signing a consent form. The university ethics committee of the University of Vienna approved the study.
Menstrual Cycling Monitoring
The order of testing was randomized. Information about previous menstrual cycles and basal body temperature was used to identify ovulation and phases. Blood samples for determination of sex hormone concentrations were collected immediately before each incremental test.
Incremental Tests and Blood Sex Hormone Concentration Measurements
Two identical incremental tests were conducted in the FP and LP of the menstrual cycle. The tests consisted of an initial workload of 0.2 W·kg−1, with a 0.2-W·kg−1 increase every minute until voluntary exhaustion of the subjects. Subjects pedaled at a rate of 80 rpm. The order of testing was counterbalanced for both cycle phases. The tests were performed at the same time of day in both cases (FP and LP). Blood samples from a hyperemic earlobe, in the amount of 20 μL, were collected at the end of each stage and immediately at the end of each test; these were analyzed for LA. Before the incremental tests, blood samples of 8.0 mL were obtained from the antecubital vein and were analyzed for progesterone and estradiol levels via immunoassay tests, to confirm the menstrual cycle phase for FP (low estradiol and low progesterone) and LP (high concentrations of both hormones). Although it would have been interesting to investigate the ovulatory phase (high estradiol and low progesterone), we had to refrain from this method because of the high organizational effort of precise ovulation monitoring.
Study Variables and Method of Determination
The following variables were studied: power output (W·kg−1), V˙O2 (mL·kg−1·min−1), HR (bpm), blood LA concentration (mM), respiratory exchange ratio (RER), V˙E (L·min−1), the ventilatory equivalent for oxygen (V˙E/V˙O2), and the ventilatory equivalent for carbon dioxide (V˙E/V˙CO2). These variables were determined at rest, during all stages of the incremental test, at maximal workload, and at different thresholds, which are described as follows.
Lactate turnpoint determination.
Lactate turnpoint 1 (LTP1) and LTP2 were introduced and described by Ribeiro et al. (35). The blood LA values were plotted against time, and three straight lines were fitted so that two breakpoints were defined by means of a linear-regression breakpoint method. The LTP1 was defined as the point immediately before blood lactate levels began to increase systematically above resting values. The LTP2 was defined as the second breakpoint, immediately before the abrupt increase in blood lactate (35).
Ventilatory threshold determination consisted of the identification of the AT and the RCP as described by Wasserman (43). The AT is characterized by the following criteria: a faster increase in V˙E and V˙CO2 in contrast to V˙O2, an upward inflection of V˙E/V˙O2 with no increase in V˙E/V˙CO2, and an upward inflection of PETO2. The RCP was detected by an upward inflection of V˙E/V˙CO2 and a downward inflection of PETCO2. The determination of the AT and RCP was assessed by an experienced evaluator (intraclass correlation AT: r = 0.96; RCP: r = 0.97).
All exercise tests were performed on an electronically braked cycle ergometer (Lode Excalibur Sport, Groningen, Netherlands). Respiratory gas-exchange measures were determined in breath-by-breath mode using an open-air spirometry system (Jäger Oxycon Alpha, Würzburg, Germany). Volume and gas calibration was conducted before each test, according to manufacturer's guidelines. Respiratory gas-exchange measures were recorded in breath-by-breath mode, averaged for eight breaths, recorded, and stored for subsequent analysis. LA was determined by fully enzymatic-amperometric method (Eppendorf ESAT 6666, Hamburg, Germany). HR was recorded every 5 s with a Sporttester PE4000 (Polar Electro, Kempele, Finland). Analysis of sex hormones was performed via electrochemiluminescence-immunoassay (Modula E170, Roche Diagnostics GmbH, Mannheim, Germany).
Diet and Workload
To reduce the influence of diet on metabolic and ventilatory responses, diet was standardized during the day before the incremental tests in both FP and LP and on the morning before testing. It consisted of two components: 1) a diet plan identical for all subjects with an energy content of 7.05 MJ (1684 kcal) per day, and 2) a total energy intake of resting metabolic rate (RMR) × 1.6 per day. The RMR was estimated according to an equation presented by Schofield (38). A sport drink containing 7.0% carbohydrate was used to obtain the desired energy intake. The supply of this sport drink ranged between 662 and 1539 mL·d−1. Additional fluid intake was administered without energy content.
Food was weighed, prepared, and apportioned by a nutritional scientist. Subjects fasted overnight. The tests were conducted in the morning between 9:00 a.m. and 12:00 p.m. for both incremental tests. On test days, a defined breakfast was consumed 2 h before the incremental tests. Drinks containing carbohydrates were not allowed on the test day before or during the incremental tests. Subjects abstained from caffeine and nicotine-containing substances on test days. A diet protocol for both FP and LP was handed to participants, and subjects were required to adhere to the specific schedule and food and fluid intake, to reach nearly identical nutritional intake. On the day before the exercise tests, no physical activities, or only light to very light activities, were allowed. Subjects were also asked to avoid changes in training regimen between the two tests. The training was documented, and no significant differences were found in comparison with training sessions reported before our test series.
Statistical analyses were conducted using Statistica software (Version 5.1 StaSoft, Inc., Tulsa, OK). The results were expressed as means ± SD. Repeated-measures analysis of variance (RMANOVA) was used to evaluate differences between FP and LP. Differences between datasets (power output, V˙O2, HR, LA, RER, V˙E, V˙E/V˙O2, and V˙E/V˙CO2) at rest, at maximal work, and at different thresholds were obtained via LSD post hoc analysis tests (least significant differences test). RMANOVA and LSD post hoc analysis tests were also used to calculate changes between FP and LP during the course of the aerobic-anaerobic transition. A paired t-test was used to determine differences between datasets (power output, V˙O2, HR, LA, RER, V˙E, V˙E/V˙O2, and V˙E/V˙CO2) at the different intensities of exercise testing. The level of significance was set at P < 0.05.
Duration of cycle phases and sex hormone concentrations.
The average cycle length was 28 ± 2 d (calculated from the first day of menses). The incremental tests were performed, on average, on day 9 ± 1 in FP and on day 25 ± 2 in LP. Sex hormone concentrations were used to evaluate the different cycle phases. Mean values for female sex hormones were 55.37 ± 29.49 pg·mL−1 for estradiol and 0.71 ± 0.20 ng·mL−1 for progesterone in FP, and 124.28 ± 51.16 pg·mL−1 for estradiol and 8.62 ± 4.33ng·mL−1 for progesterone in LP. Dataset values for measured sex hormones for subjects included in our study were within normal reference ranges during both the FP and LP (27).
Power output, oxygen uptake, and heart rate.
The average values ± SD for power output and V˙O2 at maximal load and at different thresholds are presented in Table 1. We found no significant difference when comparing power output, V˙O2, and HR at rest, at maximal workload, and at different thresholds (LTP1, LTP2, AT, RCP) in FP versus LP (Table 1). No changes were observed at any exercise intensity during the incremental tests.
Lactate and respiratory exchange ratio.
We found no significant differences when comparing LA and RER values between the cycle phases at maximal workload, at any exercise intensity, or at any threshold value (Table 2).
Ventilatory equivalents and minute ventilation.
In contrast to power output, V˙O2, HR, LA, RER, and the ventilatory equivalents for oxygen (V˙E/V˙O2), carbon dioxide (V˙E/V˙CO2), and minute ventilation (V˙E) revealed significant differences between FP versus LP. We found higher values for V˙E/V˙O2, V˙E/V˙CO2, and V˙E that were significant at rest, at maximal workload, at thresholds (Fig. 1A-C), and at different stages of incremental tests (Fig. 2A and B, Fig. 3)
To determine the course of the aerobic-anaerobic transition, we calculated the delta values between the two breakpoints of energy supply (LTP2 vs LTP1 and RCP vs AT, respectively) for our study variables (W·kg−1, HR, V˙O2, V˙E, V˙E/V˙O2, and V˙E/V˙CO2) during FP and LP. When comparing results of FP and LP (RMANOVA), we did not find any significant differences.
In past decades, it repeatedly has been suggested that estrogen and progesterone fluctuation during the menstrual cycle may influence energy supply and substrate metabolism. Changes in fuel availability during exercise have been reported as a potential factor. Evidence has been presented to suggest that estrogen may enhance fatty acid oxidation (1,11,18,19,22,26,28). This effect has been attributed to estrogen-mediated changes on lipoprotein lipase and hepatic lipase activity (1,36) and to the effects of estrogen on growth hormone, cortisol, and catecholamines (1,3,11). Following these considerations, an increase in free fatty acid oxidation as an energy source may also result in a glycogen-sparing effect.
Furthermore, it has been suggested that sex steroids may influence carbohydrate metabolism through alterations in key enzyme activity and membrane permeability, or indirectly via changes in insulin, glucagon, cortisol, growth hormone, and catecholamine levels and sensitivity (6). Evidence has been offered that estrogen and progesterone may influence glucose uptake, glucose transport, glucose storage, and sensitivity of stored carbohydrate in response to epinephrine as well as gluconeogenesis and glycogenolysis (6-8,11,17). Results of these studies suggest that performance and lactate dynamics during prolonged exercise may be influenced by the menstrual cycle. These considerations are also supported by changes in plasma volume, hematocrit, and hemoglobin exhibited during the menstrual cycle (15,42).
Thermoregulatory changes between FP and LP are caused mainly by increased progesterone concentration in the LP. Throughout the menstrual cycle, body temperature (BT) increases by approximately 0.3-0.5°C after ovulation and remains elevated throughout the LP (22,41), because progesterone seems to decrease the activity of warm sensitive neurons and to increase the activity of cold sensitive neurons (29). Furthermore, the changes in body temperature (6), together with changes in plasma volume and blood viscosity, have been suggested to be responsible for possible changes in heart rate between FP and LP (31,32). Additionally, changes in body temperature and progesterone (33) have been considered to cause changes in minute ventilation (increase in FP vs LP) observed in numerous studies (5,13,33,34,37,40,44). However, the literature addressing the above-mentioned influences of menstrual cycle on fat and carbohydrate metabolism, and also on plasma volume, hematocrit, and hemoglobin during the menstrual cycle, is rather inconsistent.
In view of our data, our results are not in agreement with previous reports suggesting changes in performance, blood LA, and HR response between FP and LP (5,13,14,23,30-34,37,40,44,46). We did not find any significant differences at rest when comparing V˙O2, HR (Table 1), LA, and RER (Table 2), at maximal workload or at any of the thresholds (LTP1, LTP2, AT, RCP), between FP and LP among our eumenorrheic subjects. No changes in power output were observed at maximal workload or at any of the thresholds in FP versus LP. The absence of significant differences suggests that the results of our exercise tests were not affected by FP or LP, using our methodological approach.
Results of our power-output measures (Table 1) are comparable with those of other studies that have documented no significant changes in maximal performance, maximal power output, or maximal exercise duration (4,5,10,13,23,30,34,40). In contrast, a study conducted with native women residing at 3600 m produced a higher maximal power output in the LP than in the FP (5). Despite significant differences in maximal power output, investigators found similar, and not significantly different, values for V˙O2max when comparing FP with LP. Jurkowski et al. (23) report that longer exercise duration was found in LP during constant-load tests at 90% V˙O2max; however, no changes are reported for maximal power output measured during an incremental test. Our data support the view of no influence of menstrual cycle on maximal performance capacity.
Similar to maximal power output, V˙O2max was also unchanged between FP and LP. These findings are in agreement with the results of other investigations (4,10,12,13,23,34,40,44). Thus, we cannot confirm the data determined by Lebrun et al. (28), who report that V˙O2max was slightly but significantly (P < 0.04) lower in LP versus FP when using the absolute V˙O2 values for comparison. However, when converting V˙O2 to body weight, the significant difference disappeared in the above-mentioned study.
Previous studies also have reported changes in HR between FP and LP (31,32). Considering that endurance training is often based on HR, changes could result in inappropriate training intensities. However, on the basis of our investigation, we cannot affirm the influence of the menstrual cycle on HR during incremental exercise testing. HR was unchanged at rest, at maximal load, at any threshold, and at any given exercise intensity of the incremental tests.
Our interest focused on variables that are often used to interpret individual endurance capacity. Therefore, in contrast to previous investigations, we additionally used two LT to determine markers of performance. Assessing power output, V˙O2, HR (Table 1), LA, and RER (Table 2), no influence of menstrual cycle was detected at rest, at maximal workload, or at the any of the previously mentioned thresholds in either FP or LP in our eumenorrheic subjects. Our observation at the LTP1 was comparable with previous investigations (10,34,46) that have reported no changes in power output or V˙O2 at the LT.
Previous investigations have shown an influence of the menstrual cycle on LA dynamics and fuel supply with increasing exercise intensities (23,34,46). Therefore, we also investigated changes associated with the LTP2 (35,39,43), which appears at higher exercise intensities than the LTP1. At the LTP2, the power output, V˙O2, HR (Table 1), LA, and RER (Table 2) were unchanged in both FP and LP. We were unable to find any comparable data with respect to influences of menstrual cycle hormones on the LTP2.
When assessing the influence of female sex hormones on lactate dynamics, we were not able to detect any influences on LA concentrations at any stage of the two incremental tests. These findings, which show no change in LA concentrations between FP and LP, are also supported by other investigators (10,12,16). Dean et al. (10) report no significant differences at LT or at maximal power output during an incremental test. Galliven et al. (16), who tested eumenorrheic women on a treadmill, found no changes in LA levels at 70 and 90% of V˙O2max.
The research literature addressing lactate kinetics and energy supply in the time course of the menstrual cycle is inconsistent. Zderic (46) found no significant differences in LA when their subjects cycled for 25 min at a constant load of 70% of the respective LT, but differences reached significance at 90% of the LT with higher values in the FP. Redman et al. (34) report no significant differences in LA at the LT, at rest, or at the end of the exercise when comparing the FP with the LP. In contrast to our results, they found a significantly lower LA in the LP when changes in LA were modeled as a single exponential function. Jurkowski et al. (23) observed higher LA levels in the FP during rest and at exhaustion, but not at constant-load exercise when performed at one third and two thirds of maximal power output. McCracken et al. (30) report that resting LA levels were not different between the FP and LP; however, they found significantly higher values of LA concentration at 3 and 30 min of recovery after exhaustive exercise on a treadmill in the FP. A study by Forsyth and Reilly (14) reports changes in lactate concentrations at preexercise and at fixed exercise intensities before and during a rowing ergometry, with significantly higher LA in the FP compared with the LP.
The premise of a greater reliance on fat as an energy source and, thus, a lower LA in the LP, is supported by findings of a lower RER in the LP (13,17,34,46). However, there are also reports of unchanged RER between the cycle phases, contradicting the findings of a shift to fat use during the LP (5,12,21,40). In our investigation, RER was not significantly different between the cycle phases at maximal load, at any of the determined thresholds (Table 2), or at any given exercise intensity. These data are in agreement with the results of a previous tracer study (24) that has reported unchanged fat metabolism and whole-body fuel oxidation during exercise when comparing the FP with the LP.
Probing for explanations for the inconsistent findings in the literature for LA and fuel supply during the menstrual cycle, the results of some studies may have been partly influenced by methodological differences, such as test protocols, test equipment, control of cycle phases, age, fitness status, menstrual cycle length, menstrual history, and nutritional status. The absence of dietary control also may be considered a possible source of the obscure results (45). Only a few studies (5,14,21,28,34,46) have been based on strict dietary control.
We also investigated the respiratory thresholds AT and RCP (39,43). This was of interest because of the evidence that there is a change in ventilatory responses dependent on the menstrual cycle (13,34,37,40,44). Similar to the threshold determination used in our study, we did not find significant differences in ventilatory response for power output, V˙O2, HR (Table 1), LA, and RER (Table 2). These results are similar to those reported by Bemben et al. (4) and Forsyth and Reilly (14) regarding AT determination. To our knowledge, there are no data for RCP available to compare with those of our study.
During the three phases of aerobic-anaerobic transition, we calculated the delta values between the two breakpoints of energy supply (LTP2 vs LTP1 and RCP vs AT, respectively) for our study variables (W·kg−1, HR, V˙O2, V˙E, V˙E/V˙O2, V˙E/V˙CO2) in the FP and LP. The lack of significant differences between the FP and LP observed in all variables suggests no influence of the menstrual cycle on the aerobic-anaerobic transition, using our methods.
The tendency toward increased V˙E/V˙O2 (Fig. 1A), V˙E/V˙CO2 (Fig. 1B), and V˙E (Fig. 1C), which we observed at rest, at maximal load, at determined breakpoints of the aerobic-anaerobic transition (AT, LTP1, RCP, LTP2), and at several stages of incremental tests (Fig. 2A and B, Fig. 3), are in agreement with previous results (3,7,20,21,24,27,29). The higher ventilatory drive in the LP seems to be caused by progesterone, a known respiratory stimulant (20). However, significant ventilatory differences between the two phases (V˙E/V˙O2 and V˙E/V˙CO2) disappear with increasing workload (Fig. 1A and B, Fig. 2A and B). Altogether, the higher ventilatory drive observed during LP did not result in significant changes in ventilatory threshold determination or oxygen costs of exercise.
The results of our incremental cycle ergometer tests conducted during the two different phases of menstrual cycle (follicular and luteal phase) suggest the following: 1) the study variables used to assess the performance capacity of our eumenorrheic subjects (power output, V˙O2, HR, and LA) were not significantly altered by the menstrual cycle, either at maximal load or at any selected threshold. The main finding of our investigation was the lack of influence of a regular menstrual cycle on performance in our subjects in this study. 2) Our data do not support the assumption of a change in energy supply during exercise throughout the time course of the menstrual cycle. 3) Our findings support the results of previous investigations reporting a higher ventilatory drive during the LP of the menstrual cycle.
1. Ashley, C. D., M. L. Kramer, and P. Bishop. Estrogen and substrate metabolism. A review of contradictory research. Sports Med
. 29:221-227, 2000.
2. Beaver, W. L., K. Wasserman, and B. J. Whipp. A new method for detecting anaerobic threshold
by gas exchange. J. Appl. Physiol
. 60:2020-2027, 1986.
3. Bemben, D. A., R. A. Boileau, J. M. Bahr, R. A. Nelson, and J. E. Misner. Effects of oral contraceptives on hormonal and metabolic responses during exercise. Med. Sci. Sports Exerc
. 24:434-441, 1992.
4. Bemben, D. A., P. C. Salm, and A. J. Salm. Ventilatory and blood lactate responses to maximal treadmill exercise during the menstrual cycle. J. Sports Med. Phys. Fitness
5. Brutsaert, T. D., H. Spielvogel, E. Caceres, M. Araoz, R. T. Chatterton, and V. J. Vitzthum. Effect of menstrual cycle phase on exercise performance of high-altitude native women at 3600 m. J. Exp. Biol
. 205:233-239, 2002.
6. Bunt, J. C. Metabolic actions of estradiol: significance for acute and chronic exercise responses. Med. Sci. Sports Exerc
. 22:286-290, 1990.
7. Campbell, S. E., and M. A. Febbraio. Effects of ovarian hormones on exercise metabolism. Curr. Opin. Clin. Nutr. Metab. Care
8. Carter, S., S. McKenzie, M. Mourtzakis, D. J. Mahoney, and M. A. Tarnopolsky. Short-term 17beta-estradiol decreases glucose R(a) but not whole body metabolism during endurance exercise. J. Appl. Physiol
. 90:139-146, 2001.
9. Constantini, N. W., G. Dubnov, and C. M. Lebrun. The menstrual cycle and sport performance. Clin. Sports. Med
. 24:e51-e82, 2005.
10. Dean, T. M., L. Perreault, R. S. Mazzeo, and T. J. Horton. No effect of menstrual cycle phase on lactate threshold
. J. Appl. Physiol
. 95:2537-2543, 2003.
11. D'Eon, T., and B. Braun. The roles of estrogen and progesterone in regulating carbohydrate and fat utilization at rest and during exercise. J. Womens Health Gend. Based Med
. 11:225-237, 2002.
12. De Souza, M. J., M. S. Maguire, K. R. Rubin, and C. M. Maresh. Effects of menstrual phase and amenorrhea on exercise performance in runners. Med. Sci. Sports Exerc
. 22:575-580, 1990.
13. Dombovy, M. L., H. W. Bonekat, T. J. Williams, and B. A. Staats. Exercise performance and ventilatory response in the menstrual cycle. Med. Sci. Sports Exerc
. 19:111-117, 1987.
14. Forsyth, J. J., and T. Reilly. The combined effect of time of day and menstrual cycle on lactate threshold
. Med. Sci. Sports Exerc
. 37:2046-2053, 2005.
15. Fortney, S. M., C. Turner, L. Steinmann, T. Driscoll, and C. Alfrey. Blood volume responses of men and women to bed rest. J. Clin. Pharmacol
. 34:434-439, 1994.
16. Galliven, E. A., A. Singh, D. Michelson, S. Bina, P. W. Gold, and P. A. Deuster. Hormonal and metabolic responses to exercise across time of day and menstrual cycle phase. J. Appl. Physiol
. 83:1822-1831, 1997.
17. Hackney, A. C. Influence of oestrogen on muscle glycogen utilization during exercise. Acta Physiol. Scand
. 167:273-274, 1999.
18. Hamadeh, M. J., M. C. Devries, and M. A. Tarnopolsky. Estrogen supplementation reduces whole body leucine and carbohydrate oxidation and increases lipid oxidation in men during endurance exercise. J. Clin. Endocrinol. Metab
. 90:3592-3599, 2005.
19. Hatta, H., Y. Atomi, S. Shinohara, Y. Yamamoto, and S. Yamada. The effects of ovarian hormones on glucose and fatty acid oxidation during exercise in female ovariectomized rats. Horm. Metab. Res
. 20:609-611, 1988.
20. Hessemer, V., and K. Bruck. Influence of menstrual cycle on shivering, skin blood flow, and sweating responses measured at night. J. Appl. Physiol
. 59:1902-1910, 1985.
21. Horton, T. J., E. K. Miller, D. Glueck, and K. Tench. No effect of menstrual cycle phase on glucose kinetics and fuel oxidation during moderate-intensity exercise. Am. J. Physiol. Endocrinol. Metab
. 282:E752-E762, 2002.
22. Janse de Jonge, X. A. Effects of the menstrual cycle on exercise performance. Sports Med
. 33:833-851, 2003.
23. Jurkowski, J. E., N. L. Jones, C. J. Toews, and J. R. Sutton. Effects of menstrual cycle on blood lactate, O2 delivery, and performance during exercise. J. Appl. Physiol
. 51:1493-1499, 1981.
24. Kanaley, J. A., R. A. Boileau, J. A. Bahr, J. E. Misner, and R. A. Nelson. Substrate oxidation and GH responses to exercise are independent of menstrual phase and status. Med. Sci. Sports Exerc
. 24:873-880, 1992.
25. Kendrick, Z. V., C. A. Steffen, W. L. Rumsey, and D. I. Goldberg. Effect of estradiol on tissue glycogen metabolism in exercised oophorectomized rats. J. Appl. Physiol
. 63:492-496, 1987.
26. Lamont, L. S. Lack of influence of menstrual cycle on blood lactate. Phys. Sportmed
. 14:159-163, 1986.
27. Landgren, B. M., A. L. Unden, and E. Diczfalusy. Hormonal profile of the cycle in 68 normally menstruating women. Acta Endocrinol
. 94:89-98, 1980.
28. Lebrun, C. M., D. C. McKenzie, J. C. Prior, and J. E. Taunton. Effects of menstrual cycle phase on athletic performance. Med. Sci. Sports Exerc
. 27:437-444, 1995.
29. Marrone, B. L., R. T. Gentry, and G. N. Wade. Gonadal hormones and body temperature in rats: effects of estrous cycles, castration and steroid replacement. Physiol. Behav
. 17:419-425, 1976.
30. McCracken, M., B. Ainsworth, and A. C. Hackney. Effects of the menstrual cycle phase on the blood lactate responses to exercise. Eur. J. Appl. Physiol. Occup. Physiol
. 69:174-175, 1994.
31. Moran, V. H., H. L. Leathard, and J. Coley. Cardiovascular functioning during the menstrual cycle. Clin. Physiol
. 20:496-504, 2000.
32. Pivarnik, J. M., C. J. Marichal, T. Spillman, and J. R. Morrow JR. Menstrual cycle phase affects temperature regulation during endurance exercise. J. Appl. Physiol
. 72:543-548, 1992.
33. Preston, R. J., A. P. Heenan, and L. A. Wolfe. Physicochemical analysis of phasic menstrual cycle effects on acid-base balance. Am. J. Physiol. Regul. Integr. Comp. Physiol
. 280:R481-R487, 2001.
34. Redman, L. M., G. C. Scroop, and R. J. Norman. Impact of menstrual cycle phase on the exercise status of young, sedentary women. Eur. J. Appl. Physiol
. 90:505-513, 2003.
35. Ribeiro, J. P., V. Hughes, R. A. Fielding, W. Holden, W. Evans, and H. G. Knuttgen. Metabolic and ventilatory responses to steady state exercise relative to lactate thresholds. Eur. J. Appl. Physiol
. 55:215-221, 1986.
36. Schaefer, E. J., S. Lamon-Fava, D. Spiegelman, et al. Changes in plasma lipoprotein concentrations and composition in response to a low-fat, high-fiber diet are associated with changes in serum estrogen concentrations in premenopausal women. Metabolism
37. Schoene, R. B., H. T. Robertson, D. J. Pierson, and A. P. Peterson. Respiratory drives and exercise in menstrual cycles of athletic and nonathletic women. J. Appl. Physiol
. 50:1300-1305, 1981.
38. Schofield, W. N. Predicting basal metabolic rate, new standards and review of previous work. Hum. Nutr. Clin. Nutr
. 39(Suppl. 1):5-41, 1985.
39. Skinner, J. S., and T. H. McLellan. The transition from aerobic to anaerobic metabolism. Res. Q. Exerc. Sport
40. Takase, K., T. Nishiyasu, and K. Asano. Modulating effects of the menstrual cycle on cardiorespiratory responses to exercise under acute hypobaric hypoxia. Jpn. J. Physiol
. 52:553-560, 2002.
41. Tankersley, C. G., W. C. Nicholas, D. R. Deaver, D. Mikita, and W. L. Kenney. Estrogen replacement in middle-aged women: thermoregulatory responses to exercise in the heat. J. Appl. Physiol
. 73:1238-1245, 1992.
42. Vellar, O. D. Changes in hemoglobin concentration and hematocrit during the menstrual cycle. I. A cross-sectional study. Acta Obstet. Gynecol. Scand
. 53:243-246, 1974.
43. Wasserman, K., J. E. Hansen, D. Y. Sue, W. W. Stringer, R. Casaburi, and B. J. Whipp. Physiology of exercise. In: Principles of Execise Testing and Interpretation
, 3rd ed., K. Wasserman, J. E. Hansen, D. Y. Sue, W. W. Stringer, R. Casaburi, and B. J. Whipp (Eds.). Balimore, MD: Lippincot Williams & Wilkins, pp. 10-61, 1999.
44. Williams, T. J., and G. S. Krahenbuhl. Menstrual cycle phase and running economy. Med. Sci. Sports Exerc
. 29:1609-1618, 1997.
45. Yoshida, T. Effect of dietary modifications on lactate threshold
and onset of blood lactate accumulation during incremental exercise. Eur. J. Appl. Physiol. Occup. Physiol
. 53:200-205, 1984.
46. Zderic, T. W., A. R. Coggan, and B. C. Ruby. Glucose kinetics and substrate oxidation during exercise in the follicular and luteal phases. J. Appl. Physiol
. 90:447-453, 2001.