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1 Division of Clinical
Physiology, The acute metabolic response to sprint exercise
was studied in 20 male and 19 female students. We hypothesized that the
reduction of muscle glycogen content during sprint exercise would be
smaller in women than in men and that a possible gender difference in glycogen reduction would be higher in type II than in type I
fibers. The exercise-induced increase in blood lactate
concentration was 22% smaller in women than in men. A considerable
reduction of ATP (50%), phosphocreatine (83%), and glycogen (35%)
was found in type II muscle fibers, and it did not differ between the
genders. A smaller reduction of ATP (17%) and phosphocreatine (78%)
was found in type I fibers, and it did not differ between the genders. However, the exercise-induced reduction in glycogen content in type I
fibers was 50% smaller in women than in men. The hypothesis was indeed
partly confirmed: the exercise-induced glycogen reduction was
attenuated in women compared with men, but the gender difference was in
type I rather than in type II fibers. Fiber-type-specific and
gender-related differences in the metabolic response to sprint exercise
might have implications for the design of training programs for men and women.
anaerobic metabolism; vastus lateralis; Wingate test
SPRINT EXERCISE leads to a major reduction in muscle
ATP and phosphocreatine (PCr) content as well as a considerable
reduction in glycogen content and a subsequent accumulation of lactate
in both muscle and blood. These metabolic alterations seem
to be fiber type specific. For instance, during sprint exercise the type II fibers lose much more ATP and glycogen (6, 15, 29) than do type
I fibers. There are no studies, to our knowledge, in which
gender-related differences in the fiber-type-specific metabolic
response to sprint exercise have been addressed. It has been
demonstrated, at the systemic level, that women have lower
concentrations of blood lactate and plasma catecholamines than do men
after sprint exercise (13, 26). In addition, glycolytic enzyme
activities are lower in muscle from women than from men (10, 14, 31).
Thus gender-related differences in metabolic response to sprint
exercise, locally in the exercising muscle, are to be expected. We
hypothesized that the reduction of muscle glycogen content during
sprint exercise would be smaller in women than in men and that a
potential gender difference in glycogen reduction would be greater in
type II than in type I fibers. The latter hypothesis is based on the
observation that the glycogen reduction is greater in type II than in
type I fibers (15) and on the concept that women, to a lesser degree
than men, may recruit/activate their muscle fibers (e.g., Ref. 4),
especially type II fibers, during sprint exercise inasmuch as these
fibers have a higher activation threshold than do type I fibers (18).
To elucidate whether there are gender-related differences in the acute
metabolic response to sprint exercise, the exercise-induced reduction
of glycogen and high-energy phosphates was analyzed in type I and type
II fibers in both men and women.
Subjects.
Twenty men and nineteen women (students at a college for sports and
recreation instructors) volunteered for the study. None of the subjects
was at an elite or competitive athletic level. They did participate in
leisure-time sports (e.g., various ball games and jogging for the men
and mainly calisthenics, aerobics, and jogging for the women). During
class hours, all subjects took part in the same theoretical and
practical classes (physical exercises). A questionnaire was used to
estimate the physical activity level during leisure time. The subjects
answered nine different questions, from which an activity index
(minimum value 5.5 and maximum value 20.5) was calculated (22). As
estimated by this questionnaire, the physical activity level did not
differ between the genders (Table
1). Anthropometric data for
the subjects are given in Table 1. Fat-free mass was estimated from
skinfold measurements (triceps, biceps, and subscapula; Ref. 9).
ABSTRACT
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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INTRODUCTION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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METHODS
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ABSTRACT
INTRODUCTION
METHODS
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DISCUSSION
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Table 1.
Anthropometric, morphologic, and power output data
Experimental protocol. After familiarization, conducted at least 24 h before the experiment, a 30-s cycle sprint was performed (Wingate test; Ref. 1) on a mechanically braked cycle ergometer (Cardionics, Bredäng, Sweden). The subjects were instructed to pedal as fast as possible with an individual braking load set at 0.075 kp/kg body wt. A sensor-microprocessor assembly counted flywheel revolutions. The flywheel progression per pedal revolution was 6 m. Average power for 5-s periods was automatically printed. Peak power (i.e., the highest 5-s power) and mean power (the average power during the 30-s duration) were calculated. In addition, peak and mean power were adjusted for body mass and fat-free mass. This was done in a multiple-regression model, where peak or mean power was chosen as the dependent variable. Gender, together with body mass or fat-free mass, was chosen as independent variables (see also Statistics).
An indwelling catheter was inserted into an antecubital vein ~20 min before exercise. Two milliliters of blood were sampled ~2 min before exercise and subsequently at 3, 6, and 9 min after exercise (with the subjects in the supine position). Skeletal muscle biopsies were obtained from the vastus lateralis with the needle-biopsy technique (3) before and within 10 s of the cessation of exercise. Both biopsies were obtained from the same leg and skin incision, frozen in isopentane precooled with liquid nitrogen within a further 5 s, and stored at
70°C until later analysis.
Histochemical and morphological analyses. The biopsy taken before exercise was mounted in an embedding medium and analyzed histochemically for fiber types (I, IIA, IIB, and IIC) with a myofibrillar ATPase stain. Cross-sectional fiber area was measured morphologically by planimetry from an NADH-dehydrogenase stain. The relative number of the different fiber types (%type I, %type IIA, %type IIB, and %type IIC) and the relative area of the different fiber types (fiber type area) were calculated. In addition, mean type I, type IIA, and type IIB fiber areas; weighted mean fiber area of all fiber types combined; and weighted mean fiber area of the two type II fiber populations (IIA and IIB) were calculated. For more information about the histochemical and morphological analyses, see Jansson and Hedberg (22).
Single-muscle-fiber preparation procedures and analyses. After histochemical analysis of the preexercise biopsy, the rest of this biopsy and the one taken after exercise were freeze-dried, and ~100 single-fiber fragments were dissected from each biopsy. These were classified histochemically as fiber type I or II (12) and thereafter divided into separate pools of type I and type II. The mean weight of the pools was 40 µg (range 15-75 µg).
The fiber pools used for analysis of lactate, ATP, ADP, IMP, inosine, hypoxanthine, and PCr were extracted in 20-55 µl (depending on the weight of the pool) 0.4 M perchloric acid containing 0.06 M phenol red at 0°C. The pH of the extracts was brought to 8.2 by adding 1 M KOH. An HPLC technique, which has been described by Sellevold et al. (30), was used to determine the amounts of the metabolites in the fibers. The injection volume was 10 µl, and isocratic ion-pair reversed-phase assay (250 × 4.6-mm, 5-µm Nucleosil 120-C18 column) was used. The mobile phase used for separation consisted of 215 mM potassium dihydrogen phosphate (pH 5.6), containing 2.4 mM tetrabutylammonium hydrogen sulfate and 3.5% acetonitrile. ATP, ADP, IMP, inosine, and hypoxanthine were detected at 254 nm (model 440, Waters) and PCr at 206 nm (model 481, Waters) with two detectors connected in series. The fiber pools used for glycogen analysis were digested by adding 20 µl of 1 M KOH, and then glycogen was extracted by vigorously mixing and warming the samples for 15 min at 50°C. The extracts were neutralized by addition of 0.25 M HCl. Amyloglycosidase was added to break down glycogen to glycosyl units (17), which were then measured by a fluorometric enzymatic method (24).Blood analyses. Blood lactate was analyzed in neutralized perchloric acid extracts of whole blood by a fluorometric enzymatic method (24).
Methodological error. Methodological error (imprecision) for glycogen, ATP, ADP, IMP, and PCr was determined by analyzing extracts from two corresponding pools and was found to be between 5 and 8%.
Statistics. Unless otherwise stated, values in the text are means ± SD. The gender difference in exercise-induced blood lactate accumulation was tested by Student's t-test for groups. The exercise-induced accumulation of blood lactate was defined as the change between the preexercise and the peak value. The peak value was defined as the highest of the 3-, 6-, or 9-min postexercise value. For the single-muscle-fiber variables (ATP, ADP, IMP, PCr, glycogen, and lactate), an ANOVA was applied to compare the exercise-induced responses between genders and in different fiber types. Gender and muscle fiber type (I or II) were chosen as independent variables and exercise-induced changes in various muscle metabolites as dependent variables. If a significant (P < 0.05) interaction effect was found between gender and fiber type, a contrast analysis was applied to identify the interaction (7). Student's t-test was applied for paired observations or groups. The P values (all analyses) were accepted as statistically significant at P < 0.05.
Multiple-regression analyses were applied to analyze the influence of gender, body mass, and fat-free body mass (independent variables) on peak or mean power outputs (dependent variables). Multiple-regression analyses were also used to analyze the influence of gender, glycogen content before exercise, and exercise-induced increase in IMP or decrease in ATP content (independent variables) on the exercise-induced decrease in glycogen content and exercise-induced increase in muscle lactate content or muscle lactate content after exercise (dependent variables).| |
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Power output (Table 1). Absolute values of peak and mean power output were 27 and 30% lower, respectively, in women than in men. When peak and mean power output were adjusted for body mass, the women still presented lower peak (15% lower; P < 0.001) and mean power outputs (18% lower; P < 0.001) than did the men. When the power output was adjusted for fat-free body mass, there was a gender difference only for the mean power (8% lower in women than in men; P = 0.03).
Fiber types and size (Table 1). There were no gender differences in the relative numbers of different fiber types. The relative area of type II fibers was smaller in women than in men. The cross-sectional area of type I fibers, on the other hand, was not statistically different between the genders. The cross-sectional area of type IIA and type IIB fibers and the weighted mean fiber area was 33, 31, and 20% smaller, respectively, in women than in men.
Blood lactate.
The exercise-induced increase (peak value preexercise value) in
blood lactate concentration was 22% smaller in women than in men (Fig.
1).
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Metabolites in muscle: fiber-type comparisons (Table
2).
Before exercise, there were no differences in ATP, ADP,
IMP, or lactate content in the two fiber types. Glycogen content was ~1.2 times higher (P < 0.0001) and
PCr was 1.1 times higher (P = 0.02) in
type II than in type I fibers.
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Metabolites in muscle: gender comparison (Table 2, Fig.
2).
Before exercise, no gender differences were found for the assessed
substrates and metabolites in either type I or type II fibers.
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Correlations. Exercise-induced glycogen reduction correlated with glycogen content before exercise both in type I fibers (men, P = 0.003; women, P = 0.02) and in type II fibers (men, P = 0.02; and women, P = 0.004). However, in type I, but not in type II, fibers the regression lines were significantly different between men and women: at a given preexercise value of glycogen, the reduction in glycogen content was smaller in the women (P = 0.02).
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DISCUSSION |
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Our hypothesis that the reduction in glycogen content in the type II fiber pool would be attenuated in women compared with men during sprint exercise was not confirmed: sprint exercise reduced the glycogen content in type II fibers similarly in both men and women by ~140 mmol/kg dry muscle. Similarly, the exercise-induced lactate accumulation and the lactate content after exercise did not differ between the genders in type II fibers (~120 mmol/kg dry muscle). An extensive reduction of the ATP content in type II fibers to approximately one-half of the preexercise value occurred in both genders. The lack of a gender difference in exercise-induced metabolic changes in type II fibers indicates that an attenuated recruitment/activation of type II fibers in women compared with men during sprint exercise is not likely.
The finding that the exercise-induced reduction in glycogen content in type I fibers was smaller in women than in men was unexpected. The smaller glycogen reduction in type I fibers in women was supported by the lower lactate content in the same fibers after exercise. A lower muscle lactate content in women than men after a 30-s cycle sprint has earlier been shown in biopsies that were not dissected into single fibers (20). Bell and Jacobs (2) also found a gender difference in glycogen degradation in women, as estimated from a histochemical glycogen staining, during repeated bouts of maximal isokinetic knee extensions. However, they found lower degradation in women in both fiber types. The discrepancy between the results of the present study and those of Bell and Jacobs may be related to the different exercise protocols or to the different techniques used for quantification of glycogen.
It is thought that the rate of glycogenolysis increases as a response
to an increased ADP content and/or a decreased ATP content. An
increased IMP content most likely reflects such a disturbed energy
balance (e.g., Ref. 21). Therefore, the rate of glycogenolysis ought to
relate to the increase in IMP content. In fact, a strong correlation
was found between IMP and lactate accumulation during exercise in the
present study (Figs. 3 and
4). However, for type I fibers, the
regression lines describing the relationship between lactate and IMP
accumulation were significantly different for the male and female
subjects (different y-axis intercept).
This means that, for a given increase in IMP, the women demonstrated a
lower exercise-induced lactate content than did the men. This could be
due to a limiting phosphorylase activity in women by either lower
maximal velocity
(Vmax) or
higher Michaelis constant (Km) for the
enzyme or lower concentrations of alternative stimulators, such as cAMP
as discussed below. In type II fibers, however, no gender differences
were found either before or after adjustment for exercise-induced
accumulation of IMP.
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The gender difference in the average rate of glycogenolysis over the 30-s exercise in type I fibers occurred despite a lack of gender difference in net ATP or PCr reduction or IMP accumulation in these fibers. This would indicate that type I fibers were activated/recruited to a similar degree in the two genders. The similar metabolic activation of the high-threshold type II fibers in both men and women, together with the principle of orderly recruitment of motor units (18), makes it unlikely that there would be a gender difference in the recruitment/activation of the low threshold type I fibers. Therefore, we do not think that the smaller glycogen reduction in type I fibers in the women was due to a lower recruitment/activation of these fibers.
One possible explanation, however, for the lower rate of glycogenolysis in type I fibers in the women is the lower activity (lower Vmax or higher Km) of enzymes limiting the anaerobic ATP-regenerating pathway in women. Women are known to have lower Vmax activities of lactate dehydrogenase, phosphofructokinase, and glycogen phosphorylase (see Ref. 10). However, we have found that the greatest gender difference in lactate dehydrogenase activity is found in type II fibers (M. Esbjörnsson-Liljedahl, C. Sylvén, and E. Jansson, unpublished observations). Therefore, the lack of gender difference in the rate of glycogenolysis in type II fibers may argue against gender differences in glycolytic enzymes as the main explanation. The gender difference in activities of glycolytic or glycogenolytic enzymes may, to some extent, depend on the fact that women in general have a greater relative type I fiber area (10, 31). In turn, this may partly depend on the fact that women have larger type I compared with type II fibers than do men. Whether this gender difference in the relative proportion of the different contractile proteins explains the gender difference in glycogenolytic rate of the type I fibers is not known.
Another explanation could be that the gender difference in the rate of
glycogenolysis in type I fibers was related to a smaller increase in
plasma catecholamines during sprint exercise in women (5, 13, 26; M. Esbjörnsson-Liljedahl, K. Bodin, and E. Jansson, unpublished
observations). Muscle glycogenolysis is known to be stimulated by intracellularly derived ADP or AMP, by
Ca2+, or by a 
-receptor-induced
increase in cAMP (e.g., Ref. 23). Glycogenolysis may depend more on
-receptor stimulation in type I than in type II fibers (28) because
type I fibers have a threefold higher density of -receptors than do
type II fibers (25). This idea is supported by the finding that, during
electrical stimulation of vastus lateralis, the glycogen depletion in
type I fibers was more dependent on epinephrine than it was in type II
fibers (16). During aerobic exercise, an attenuated reduction of muscle
glycogen in women has also been demonstrated (27, 32). The cited
studies presented data only on mixed muscle. Therefore, no data were
available on fiber-type-specific gender difference in glycogen
reduction. In the study by Tarnopolsky et al. (32), it was suggested
that the attenuated glycogen reduction in the women was related to the
lower plasma epinephrine levels in the women than in the men. This is
in accordance with the explanation presented above. It has to be
considered, however, that the average rate of glycogenolysis is
~100-fold higher during a 30-s sprint than during 90 min of aerobic
exercise. Therefore, the metabolic responses to these two extremely
different exercise protocols must be compared with caution.
Finally, a highly significant positive correlation between preexercise glycogen content and the glycogen reduction during sprint exercise was found in the present study, both in type I and type II fibers. In a multiple-regression analysis, the glycogen reduction in type I fibers was found to be explained by both the glycogen content before exercise and the gender. This means that the smaller glycogen reduction in type I fibers in women could in part, but not fully, be explained by their somewhat lower glycogen content before exercise.
In a previous study, it was shown that the adaptation to a 4-wk period of sprint training was gender related and fiber type specific: the cross-sectional area of type II fibers increased in the women but not in the men (11). The extensive reduction of ATP, PCr, and glycogen content in type II fibers found in the present study did not differ between men and women. Thus the findings of a greater hypertrophy of type II fibers in women than in men after sprint training may not be due to a gender difference in the metabolic response of type II fibers during sprint exercise. However, the findings of a gender difference in the metabolic response of type I fibers to sprint exercise in the present study may have implications for the adaptation to sprint training.
The smaller increase in blood lactate concentration after sprint exercise in women than in men seems not to be explained by a smaller reduction in glycogen content in the type II fibers in women. However, the smaller reduction of glycogen content in type I fibers in women may be a contributing factor to the smaller increase in blood lactate concentration in women. The observed gender difference in blood lactate accumulation may also be explained by a lower muscle mass in women compared with that in men. However, the calculations below indicate that this is not the case. The leg muscle mass in the present study is estimated from the cross-sectional fiber areas, as measured in biopsies from each subject, and muscle length, which was approximated by the relative difference in body height. By this calculation the women had, on the average, 25% smaller leg muscle mass than did the men. Blood volume was not measured, but an estimation from height and weight showed that the women had an ~25% smaller blood volume than did the men (19). The resulting calculation of the gender difference in the relationship between the leg muscle mass and blood volume indicates that there is no gender difference in this relationship. Thus the muscle mass in relation to the blood volume did not seem to differ between men and women and thus could not explain the gender difference in blood lactate accumulation after sprint exercise.
The load chosen in the present study was 0.075 kp/kg body wt, as in our earlier sprint studies (10, 11). This load does not give an absolute maximal mean power, which is probably achieved at a load of ~0.09 kp/kg body wt for men and at a somewhat lower load for women (8). However, the curve describing the relationship between load and mean power is flat around the maximum point. Accordingly, the difference in the resulting mean power between 0.09 and 0.075 kp/kg body wt would be on average 5%, which is not very critical for the mean power (8). If anything, the gender difference may be underestimated at the load we have chosen. However, to make possible a comparison with our previous studies, we thought it was important to have the same load setting in the present study.
When attempting to identify gender-related differences in metabolic response during sprint exercise, it is important that the groups are comparable with respect to physical activity. In the present study, we selected physical education students at a boarding school. During the daytime, all subjects attended the same lectures, including both the theory and practice of different kinds of sports. According to the questionnaire-based activity index calculated in the present study, the level of leisure-time physical activity did not differ between the men and women. Thus the subjects in the present study can be considered well matched with respect to physical activity. Furthermore, all subjects of both genders were on similar diets, as all meals were served at the school.
Conclusions. We found a fiber-type-specific and gender-related difference in the metabolic response to sprint exercise and an interaction between fiber type and gender in that response.
The smaller sprint-exercise-induced reduction in glycogen content, in type I fibers, in women than in men may contribute to the smaller accumulation of blood lactate in women after sprint exercise. The lack of gender difference in the reduction of ATP, PCr, and glycogen content in type II fibers may argue against an attenuated recruitment/activation of these fibers in women compared with in men during sprint exercise. Knowledge about fiber-type-specific and gender-related difference in the metabolic response to sprint exercise may, besides being of basic scientific value, have implications for the design of training programs for men and women.| |
ACKNOWLEDGEMENTS |
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This study was supported by grants from the Swedish Center for Research in Sports and the Swedish Medical Research Council (no. 4494).
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: M. Esbjörnsson Liljedahl, Div. of Clinical Physiology, Dept. of Medical Laboratory Sciences and Technology, Huddinge Univ. Hospital, 141 86 Huddinge, Sweden (E-mail: Mona.Esbjornsson{at}labtek.ki.se).
Received 12 February 1999; accepted in final form 22 June 1999.
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