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Clinical Investigations: GENDER |

Gender Differences in the Oxygen Transport System During Maximal Exercise in Hypertensive Subjects* FREE TO VIEW

Tony Reybrouck, PhD; Robert Fagard, MD, PhD
Author and Funding Information

*From the Hypertension and Cardiovascular Rehabilitation Unit, Department of Molecular and Cardiovascular Research, University of Leuven, University Hospital Gasthuisberg, Leuven, Belgium.



Chest. 1999;115(3):788-792. doi:10.1378/chest.115.3.788
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Study objectives: To analyze gender differences in the oxygen transport system at peak exercise with particular emphasis on the difference in systemic arteriovenous oxygen extraction and in mixed venous oxygen saturation.

Patients and methods: Cardiopulmonary graded exercise testing and hemodynamic assessment were performed on a cycle ergometer in 64 hypertensive patients (32 female and 32 male) varying in age from 23 to 64 years. Female and male patients were matched for age and BP.

Measurements and results: Peak oxygen uptake was significantly lower in women than in men, and when expressed in absolute units (L/min: −39%) and when normalized for body mass (mL/min/kg: −33%) or statistically adjusted for height and weight (−29%). This resulted essentially from a significantly lower cardiac output in women, both when expressed in absolute units and when adjusted for body size. At the peripheral level, female patients had a lower arteriovenous oxygen content difference at peak exercise, which resulted from a lower hemoglobin concentration and the inability to decrease mixed venous oxygen saturation to the same level as in men.

Conclusion: The lower peak oxygen uptake of women results from both central and peripheral factors. The significantly higher value for mixed venous oxygen saturation, which contributes to the lower arteriovenous oxygen difference of women, could result from their smaller muscle mass, lower capillary density, and lower oxidative potential.

Abbreviations: (av)o2 = arteriovenous oxygen content difference; NS = not significant; R = respiratory gas exchange ratio; V̇co2 = carbon dioxide output; V̇o2 = oxygen uptake (units per minute)

Figures in this Article

Aerobic power is lower in women than in men. This has been shown not only in healthy subjects1,,2 but also in patients with hypertension,3chronic heart failure,4or with congenital heart disease.5 The difference can be explained at least partially by anthropometric differences, but it is still significant after adjusting for body size.2,,3,,4 Peak oxygen uptake (V̇o2) is the product of heart rate, stroke volume, and the arteriovenous oxygen content difference [(av)o2]. It has been shown that peak heart rate is similar in both sexes,,2 but women have a lower stroke volume and a lower (av)o2 than men.,6This is due at least partly to the lower hemoglobin concentration of women,7 but it has not been well studied whether the oxygen saturation of mixed venous blood differs between the sexes at peak exercise. Most hemodynamic studies on gender differences have been performed in normal subjects. In the present study, we analyzed the role of peripheral oxygen extraction in the gender difference in peak V̇o2 in a sample of hypertensive men and women, matched for age and BP, in whom hemodynamic measurements were performed.

Among patients referred for the investigation of hypertension, including hemodynamic studies at rest and during exercise, 32 women and 32 men matched for age and BP were selected for the present analysis. BP had exceeded 140 mm Hg for systolic pressure or 90 mm Hg for diastolic pressure, or both, on several occasions. The patient characteristics are presented in Table 1. Ages ranged from 23 to 64 years. Patients with heart or renal failure or with nonhypertensive cardiac, hematologic, or hepatic disease were excluded from this study. All patients were hospitalized. They had never been treated for hypertension or had not taken antihypertensive medication for at least 3 weeks. Two men and two women had ECG evidence of left ventricular hypertrophy, defined as the sum of the S wave in V1 and the R wave in V6 > 3.4 mV and a flat or inverted T wave in the left precordial leads. The patients (female and male) had a sedentary lifestyle. No patient was engaged in formal sport participation. A few days after admission to the hospital, patients were introduced to the exercise laboratory, where the exercise testing procedure was explained. They also performed some preliminary exercise testing to get accustomed to the procedures. The experimental protocol had been approved by the local medical ethical committee on clinical human research, and informed consent was obtained from the subjects after the experimental procedure was fully explained and demonstrated.

Exercise testing was performed in an air-conditioned laboratory (18 to 22°C and humidity 40 to 60%). Right heart catheterization was performed by percutaneous puncture of an antecubital vein with a flow-directed Swan-Ganz catheter. The catheter was positioned in the pulmonary artery to sample mixed venous blood and to measure pulmonary artery and pulmonary capillary wedge pressures. Another catheter was introduced in the brachial artery by percutaneous puncture to measure intra-arterial pressure. Pressures were measured using pressure transducers (Elema-Schönander; Stockholm, Sweden} that were positioned 5 cm below the sternal angle. Mean pressures were obtained by electrical damping. Samples of arterial and mixed venous blood were drawn slowly and simultaneously for determination of oxygen saturation by reflection oximetry (Kipp Haemoreflector; the Netherlands). At rest and at all different exercise levels, hemoglobin concentration was determined on arterial blood by the cyanmethemoglobin method.8 Oxygen content was calculated as the product of hemoglobin concentration, the oxygen saturation, and the combining factor 1.34. The (av)o2 was calculated as the difference between arterial and mixed venous values.

Gas exchange was measured by the open circuit method. Expired air was collected in a 5-L mixing box, and minute volume was measured continuously with a pneumotachograph (at body temperature and pressure, and saturated with water vapor). The gas analyzers were calibrated before each exercise test with precise gas mixtures.

o2 and carbon dioxide output (V̇co2) were reduced to standard temperature, pressure, and dry conditions. The respiratory gas exchange ratio (R) was calculated as V̇co2 divided by V̇o2. Cardiac output was determined by the direct Fick method for O2, from the ratio of V̇o2 to (av)o2. Stroke volume was calculated as cardiac output divided by heart rate. Heart rate was derived continuously from the ECG. Hemodynamic measurements were performed with the subject at rest in the supine position 30 min after introduction of the catheters and after the subject had been sitting on the bicycle ergometer for 10 min. The exercise test was performed on a electromagnetically braked bicycle ergometer, with the subject in the upright position. Exercise was started at 20 W. The work rate was increased by 30 W every 4 min until exhaustion. Hemodynamic measurements were performed at 50 W, 110 W, and 170 W, or every work rate after the patient had reached an R value of 1.0. This was done in an attempt to determine cardiac output at the highest exercise level that the subject could maintain during 4 min.

Statistical Analysis

Software (SAS; SAS Institute Inc; Cary, NC) was used for the statistical analysis. The data are reported as means and SDs. Differences between the mean values were assessed by using Student’s t test. To account for differences in anthropometric characteristics, volumetric hemodynamic data were also analyzed with adjustment for height and weight. This was done by using height and weight as covariates in the statistical analyses when comparing data from men and women. Associations between variables were studied by use of single regression analysis. A two-tailed p value of < 0.05 was considered significant.

Exercise Performance and Central Hemodynamics

Cardiopulmonary exercise data obtained at peak exercise are listed in Table 2. The highest achieved work load was lower in women than in men, whereas R exceeded 1.0 and was similar in both genders (1.10 ± 0.11 in women and 1.09 ± 0.14 in men). Peak V̇o2 was significantly lower in women than in men, both before and after adjustment for height and weight. When simply divided by body weight, V̇o2 averaged 20.0 ± 4.8 mL/min/kg in women and 29.8 ± 5.3 mL/min/kg in men (p < 0.001). Peak V̇o2 was 39% lower in women than in men when expressed in absolute values, 33% when expressed per kilogram of body weight, and 29% after controlling for height and weight. The significantly lower value for peak V̇o2 in women resulted from a lower cardiac output, both when expressed in absolute units and when adjusted for body size, and from a smaller peak (av)o2. The lower cardiac output in women was due to a smaller stroke volume, both in absolute values and after controlling for height and weight, but peak heart rate was similar in women and men.

Oxygen-Carrying Capacity

Peak exercise arterial oxygen saturation was slightly higher in women than in men (p < 0.05); the gender difference was more pronounced for the mixed venous oxygen saturation (Fig 1). The arteriovenous difference in oxygen saturation was 56.5 ± 7.2% in women, compared with 60.0 ± 8.0% in men (p < 0.07). Fig 2 illustrates that the mixed venous oxygen saturation at peak exercise was inversely related to peak V̇o2 in the total study population (r = −0.46; p < 0.001). When analyzed within each gender, the relationship was significant in women (r = −0.52; p < 0.01) and tended to be significant in men (r = −0.28; p = 0.13). Mixed venous oxygen saturation was not related to peak R, neither in women (p = 0.67) nor in men (p = 0.35). When arterial oxygen content was calculated from hemoglobin concentration and oxygen saturation, a significantly (p < 0.001) lower value was found in women compared with men (Fig 1). This resulted mainly from the lower value for hemoglobin concentration at peak exercise in women (14.3 ± 1.3 g/dL) compared with men (16.5 ± 1.3 g/dL) (p < 0.001). For mixed venous oxygen content, no significant difference was found between both genders.

Systemic and Pulmonary Artery Pressures

Mean brachial artery pressure at peak exercise averaged 145 ± 23 mm Hg in women and 151 ± 23 mm Hg in men (not significant [NS]). Mean pulmonary artery pressure and mean pulmonary capillary wedge pressure were similar in the two genders and amounted, respectively, to 25.1 ± 8.7 and 9.4 ± 7.2 mm Hg in women and to 26.0 ± 6.2 and 9.4 ± 4.2 mm Hg in men.

The components of the Fick equation were analyzed to assess gender differences in the oxygen transport system at peak exercise in hypertensive subjects. Measurements were performed at the end of a graded uninterrupted exercise test until exhaustion. Since a plateau in V̇o2 with increasing exercise intensity is not often reached during clinical exercise testing, there was no objective evidence that the subjects studied reached a true V̇o2max. However, the maximal value for heart rate and R were similar to the normal criteria for attainment of a physiologic end point during exercise testing.9 Therefore, it can be concluded that the subjects of the present study performed a physiologic maximal exercise test, which was the case for both men and women.

The mean value for peak V̇o2 in both genders was at the lower limit of the 95% confidence limits of the predicted normal values, as published by Wasserman et al.10This can be ascribed to the lower peak aerobic power of hypertensives when compared to normotensives11 and the sedentary lifestyle of the studied patients. The data of the present study show that the lower peak V̇o2 value in female hypertensive patients is attributable to gender differences in both the central and peripheral circulation. At the central level, a lower value for peak cardiac output was found in female hypertensive patients, which is in agreement with previous studies in normal women.,1,,6 Similarly to data obtained in normal subjects, the lower value for cardiac output at peak exercise can be ascribed to a lower value for stroke volume while no gender differences were found for peak heart rate.6 To eliminate the confounding effects of height and weight on volumetric hemodynamic data,2 these variables were also analyzed by using height and weight as covariates. Even after adjusting for the effects of height and weight, significantly lower values were still observed for cardiac output and stroke volume at peak exercise in the women. Assessments of body fat were not performed, so that we cannot exclude that differences in body composition may have affected the results. However, the magnitude of the difference in stroke volume between both genders seems to be more pronounced than differences in body composition might explain in addition to differences in body size. Furthermore, no patient reached the degree of obesity that has been reported in hemodynamic studies comparing values for stroke volume and end-diastolic volume between obese patients and normal control subjects, eg, body mass index was elevated by 50 ± 14% in the study of Alaud-din et al,,12and the percent overweight averaged 54 ± 23% in the study of Nakajima et al.13 As to the peripheral level, a significantly lower (av)o2 was found in female patients compared with male patients. This resulted mainly from the lower hemoglobin concentration in the women, which is in agreement with previous studies.,7,,14,,15

At the arterial side, the lower hemoglobin concentration results in a lower oxygen-carrying capacity of the blood in the female subjects, which contributes to the significantly lower value for peak V̇o2 in women compared with men.1,,2,,7 However, in experimental studies in which the hemoglobin concentration of male subjects was reduced to the same value as in female subjects by withdrawal of blood, the decrease of V̇o2max (L/min) was not proportional to the reduction of hemoglobin concentration.,7 This intervention reduced gender differences in V̇o2max by 7.5% when expressed in liters per minute and by 6.9% when expressed in milliliters per minute per kilogram, but even for equal hemoglobin concentrations, V̇o2max, expressed in liters per minute, and maximal ride time on the cycle ergometer were still significantly higher in men compared with women. This suggests that apart from differences in stroke volume and hemoglobin concentration, other factors should be operational to explain gender differences in maximal aerobic exercise performance, such as differences in mixed venous O2 saturation at maximal exercise and differences in muscle structure and capillary density.

At the venous side, a significantly higher value was found for mixed venous oxygen saturation in the female hypertensive subjects. This correlated with the smaller muscle fiber size in women compared with men.2,,16 Even in female track athletes, the size of the individual muscle fibers was only 70 to 80% of the size found in male athletes.17 Together with the lower muscle mass in women compared with men, gender differences have been reported in the metabolic profile, muscle fiber composition, and capillary supply per fiber. In muscle biopsy specimens of the quadriceps muscle, Saltin et al16 found a lower cross-sectional area of muscle fibers in the quadriceps muscle in women compared with men and female subjects had a slightly lower concentration of the oxidative enzyme succinic dehydrogenase, compared with male subjects. Furthermore, a close correlation has been reported between the number of capillaries per muscle fiber and the V̇o2max. Capillary density was found to be lower in women than in men.,16 These factors would lead to a lesser muscular oxygen extraction in women and can explain the higher value for mixed venous oxygen saturation. However, other explanations should also be considered. For example, it is possible that men and women just reached the same lower limit for mixed venous oxygen content (about 70 mL/L) (Fig 1), below which no further reduction in oxygen content would be possible. Moreover, although all subjects had a sedentary lifestyle, it cannot totally be excluded that habitual physical activity and fitness were lower in women than in men, which might have contributed to the lower peak V̇o2 and the higher mixed venous oxygen saturation in the women through a lesser redistribution of blood flow to the active muscles. The significant inverse correlation between mixed venous oxygen saturation at peak exercise and peak V̇o2 could support this hypothesis, though the significant correlation cannot be considered proof of a cause-and-effect relationship. Finally, although desaturation of mixed venous blood is also related to the motivation to perform maximal exercise during incremental exercise testing, a difference in motivation to perform maximal exercise is unlikely, since R values were similar in women and men at peak exercise.

Gender differences in (av)o2 during maximal exercise have been reported in normal subjects.1,,2 This resulted essentially from the lower blood hemoglobin concentration in the female subjects. At maximal exercise, no significant difference was found for mixed venous O2 content between female and male subjects in the studies of Hossack and Bruce,1and Mitchell et al.2 No values were reported for mixed venous O2 saturation in these studies. However, since mixed venous oxygen content is the product of oxygen saturation and hemoglobin concentration, and both factors change in opposite direction during exercise, mixed venous O2 content does not adequately reflect the rate of O2 extraction of the exercising muscles. Therefore, mixed venous oxygen saturation is a better estimate of the rate of oxygen extraction in the exercising muscles.

The present study has some limitations, since factors that could influence the O2 dissociation curve, such as a reduction of pH, an increase of 2,3 DPG, and an increase in body temperature,18,,19 were not determined on arterial and mixed venous blood samples. However, when the degree of metabolic acidosis was indirectly estimated from the rate of CO2 elimination vs V̇o2 during exercise,20 and expressed by the respiratory gas exchange ratio, no significant difference was found between women and men, which suggests that the influence of this factor was not different between both genders.

This study shows that peak V̇o2 in female hypertensive patients is significantly lower than in male patients, related to differences in central hemodynamic factors and peripheral metabolic potential. At the central level, a significantly lower value was found for cardiac output in women, compared with men, even after adjusting for differences in body mass and height, which resulted from a significantly lower stroke volume. At the peripheral level, female patients could not reach the same maximal value for (av)o2 as male patients. This was due to their lower hemoglobin concentration and also to the inability to lower mixed venous oxygen saturation to the same level as the male subjects, which could result from a lower oxidative potential and lower capillary density per muscle fiber in the female subjects. This could implicate that female hypertensive patients have a lower potential to increase (av)o2 in conditions of heart disease or when treated with antihypertensive agents that lower cardiac output, such asβ -blockers.

Dr. Fagard is holder of the Professor Amery Chair in Hypertension Research, founded by Merck Sharp and Dohme (Belgium).

Correspondence to: Tony Reybrouck, PhD, Cardiovascular Rehabilitation, Department of Physical Medicine and Rehabilitation, Gasthuisberg University Hospital, Herestraat, 3000 Leuven, Belgium; e-mail tony.reybrouck@uz.kuleuven.ac.be

Table Graphic Jump Location
Table 1. Characteristics of the Subjects*
* 

Values are means ± SD. BMI = body mass index; HR = heart rate; SBAP, DBAP = systolic, diastolic arterial pressure; MPAP = mean pulmonary artery pressure; MPCWP = mean pulmonary capillary wedge pressure.

Table Graphic Jump Location
Table 2. Hemodynamic Data at Peak Exercise*
* 

Values are means ± SD.

 

Adjusted for height and weight.

Figure Jump LinkFigure 1.  Comparison of hemoglobin oxygen saturation (top) and oxygen content (bottom) between men (M) and women (F), in arterial and mixed venous blood. Asterisk = p < 0.05; three asterisks = p < 0.001.Grahic Jump Location
Figure Jump LinkFigure 2.  Relationship between mixed venous oxygen saturation at peak exercise and peak V̇o2 in the total study population. Open circles represent men; closed circles represent women.Grahic Jump Location

ACKNOWLEDGMENT: The authors gratefully acknowledge the help of J. Delsupehe and J. Romont during the hemodynamic investigations.

Hossack, KF, Bruce, RA (1982) Maximal cardiac function in sedentary normal men and women: comparison of age-related changes.J Appl Physiol53,799-804. [PubMed]
 
Mitchell, JH, Tate, C, Raven, P, et al Acute response and chronic adaptation to exercise in women.Med Sci Sports Exerc1992;24(suppl),S258-S265
 
Fagard, RH, Thijs, LB, Amery, AK The effect of gender on aerobic power and exercise hemodynamics in hypertensive adults.Med Sci Sports Exerc1995;27,29-34. [PubMed]
 
Pardaens, K, Vanhaecke, J, Fagard, RH Impact of age and gender on peak oxygen uptake in chronic heart failure.Med Sci Sports Exerc1997;29,733-737. [PubMed] [CrossRef]
 
Legett, ME, Kuusisto, J, Healy, NL, et al Gender differences in left ventricular function at rest and with exercise in asymptomatic aortic stenosis.Am Heart J1996;131,94-100. [PubMed]
 
Fagard, R, Staessen, J, Amery, A Hemodynamic aspects of human essential hypertension. Zanchetti, A Mancia, GL eds.Handbook of hypertension (vol 17): pathophysiology of hypertension1997,213-240 Elsevier Science. New York, NY:
 
Cureton, K, Bishop, P, Hutchinson, P, et al Sex differences in maximal oxygen uptake: effect of equating haemoglobin concentrations.Eur J Appl Physiol1986;54,656-660
 
Dacie, JV, Lewis, SM Practical haematology.1963,36 Churchill. London, UK:
 
Myers, J, Froelicher, V Hemodynamic determinants of exercise capacity in chronic heart failure.Ann Intern Med1991;115,377-386. [PubMed]
 
Wasserman, K, Hansen, JE, Sue, DY, et al. Exercise testing and interpretation. 1994; Lea & Febiger. Philadelphia, PA:.
 
Fagard, R, Amery, A Physical exercise in hypertension. Laragh, JH Brenner, BM eds.Hypertension: pathophysiology, diagnosis and management1995,2669-2681 Raven Press. New York, NY:
 
Alaud-din, A, Meterissian, S, Lisboa, R, et al Assessment of cardiac function in patients who were morbidly obese.Surgery1990;108,809-820. [PubMed]
 
Nakajima, T, Fujioka, S, Tokunaga, K, et al Correlation of intra-abdominal fat accumulation and left ventricular performance in obesity.Am J Cardiol1989;64,369-373. [PubMed]
 
Astrand PO, Rodahl K. Textbook of work physiology: physiological bases of exercise. 3rd ed. New York, NY: McGraw-Hill, 1–756, 1986.
 
Pate, R, Barnes, C, Miller, W A physiological comparison of performance-matched female and male distance runners.Res Q1985;56,245-250
 
Saltin, B, Henriksson, J, Nygaard, E, et al Fiber types and metabolic potentials of skeletal muscles in sedentary man and endurance runners.Ann N York Acad Sci1977;301,3-29
 
Costill, DL, Daniels, J, Evans, W, et al Skeletal muscle enzymes and fiber composition in male and female track athletes.J Appl Physiol1976;40,149-152. [PubMed]
 
Perego, GB, Marenzi, GC, Guazzi, M, et al Contribution of Po2, P50 and Hb to changes in arteriovenous O2content during exercise in heart failure.J Appl Physiol1986;80,623-631
 
Johnson, RL, Heigenhauser, GJF, Hsia, CCN, et al Determinants of gas exchange and acid-base balance during exercise. Rowell, LB Shepherd, T eds.Handbook of physiology, section 12: exercise: regulation and integration of multiple systems1996,515-584 Oxford University Press. New York, NY:
 
Reybrouck, T, Mertens, L, Kalis, N, et al Dynamics of respiratory gas exchange after correction of congenital heart disease.J Appl Physiol1996;80,458-463. [PubMed]
 

Figures

Figure Jump LinkFigure 1.  Comparison of hemoglobin oxygen saturation (top) and oxygen content (bottom) between men (M) and women (F), in arterial and mixed venous blood. Asterisk = p < 0.05; three asterisks = p < 0.001.Grahic Jump Location
Figure Jump LinkFigure 2.  Relationship between mixed venous oxygen saturation at peak exercise and peak V̇o2 in the total study population. Open circles represent men; closed circles represent women.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1. Characteristics of the Subjects*
* 

Values are means ± SD. BMI = body mass index; HR = heart rate; SBAP, DBAP = systolic, diastolic arterial pressure; MPAP = mean pulmonary artery pressure; MPCWP = mean pulmonary capillary wedge pressure.

Table Graphic Jump Location
Table 2. Hemodynamic Data at Peak Exercise*
* 

Values are means ± SD.

 

Adjusted for height and weight.

References

Hossack, KF, Bruce, RA (1982) Maximal cardiac function in sedentary normal men and women: comparison of age-related changes.J Appl Physiol53,799-804. [PubMed]
 
Mitchell, JH, Tate, C, Raven, P, et al Acute response and chronic adaptation to exercise in women.Med Sci Sports Exerc1992;24(suppl),S258-S265
 
Fagard, RH, Thijs, LB, Amery, AK The effect of gender on aerobic power and exercise hemodynamics in hypertensive adults.Med Sci Sports Exerc1995;27,29-34. [PubMed]
 
Pardaens, K, Vanhaecke, J, Fagard, RH Impact of age and gender on peak oxygen uptake in chronic heart failure.Med Sci Sports Exerc1997;29,733-737. [PubMed] [CrossRef]
 
Legett, ME, Kuusisto, J, Healy, NL, et al Gender differences in left ventricular function at rest and with exercise in asymptomatic aortic stenosis.Am Heart J1996;131,94-100. [PubMed]
 
Fagard, R, Staessen, J, Amery, A Hemodynamic aspects of human essential hypertension. Zanchetti, A Mancia, GL eds.Handbook of hypertension (vol 17): pathophysiology of hypertension1997,213-240 Elsevier Science. New York, NY:
 
Cureton, K, Bishop, P, Hutchinson, P, et al Sex differences in maximal oxygen uptake: effect of equating haemoglobin concentrations.Eur J Appl Physiol1986;54,656-660
 
Dacie, JV, Lewis, SM Practical haematology.1963,36 Churchill. London, UK:
 
Myers, J, Froelicher, V Hemodynamic determinants of exercise capacity in chronic heart failure.Ann Intern Med1991;115,377-386. [PubMed]
 
Wasserman, K, Hansen, JE, Sue, DY, et al. Exercise testing and interpretation. 1994; Lea & Febiger. Philadelphia, PA:.
 
Fagard, R, Amery, A Physical exercise in hypertension. Laragh, JH Brenner, BM eds.Hypertension: pathophysiology, diagnosis and management1995,2669-2681 Raven Press. New York, NY:
 
Alaud-din, A, Meterissian, S, Lisboa, R, et al Assessment of cardiac function in patients who were morbidly obese.Surgery1990;108,809-820. [PubMed]
 
Nakajima, T, Fujioka, S, Tokunaga, K, et al Correlation of intra-abdominal fat accumulation and left ventricular performance in obesity.Am J Cardiol1989;64,369-373. [PubMed]
 
Astrand PO, Rodahl K. Textbook of work physiology: physiological bases of exercise. 3rd ed. New York, NY: McGraw-Hill, 1–756, 1986.
 
Pate, R, Barnes, C, Miller, W A physiological comparison of performance-matched female and male distance runners.Res Q1985;56,245-250
 
Saltin, B, Henriksson, J, Nygaard, E, et al Fiber types and metabolic potentials of skeletal muscles in sedentary man and endurance runners.Ann N York Acad Sci1977;301,3-29
 
Costill, DL, Daniels, J, Evans, W, et al Skeletal muscle enzymes and fiber composition in male and female track athletes.J Appl Physiol1976;40,149-152. [PubMed]
 
Perego, GB, Marenzi, GC, Guazzi, M, et al Contribution of Po2, P50 and Hb to changes in arteriovenous O2content during exercise in heart failure.J Appl Physiol1986;80,623-631
 
Johnson, RL, Heigenhauser, GJF, Hsia, CCN, et al Determinants of gas exchange and acid-base balance during exercise. Rowell, LB Shepherd, T eds.Handbook of physiology, section 12: exercise: regulation and integration of multiple systems1996,515-584 Oxford University Press. New York, NY:
 
Reybrouck, T, Mertens, L, Kalis, N, et al Dynamics of respiratory gas exchange after correction of congenital heart disease.J Appl Physiol1996;80,458-463. [PubMed]
 
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