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1 Department of Exercise and Sport Sciences and Physiology, Center for Exercise Science, University of Florida, Gainesville, Florida 32611; and 2 School of Sport Sciences and Technology, University of Hacettepe, Beytepe, Ankara, 06532, Turkey
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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This study
investigated the effects of exercise training duration on the myosin
heavy chain (MHC) isoform distribution in rat locomotor muscles. Female
Sprague-Dawley rats (120 days old) were assigned to either a sedentary
control group or to one of three endurance exercise training groups.
Trained animals ran on a treadmill at ~75% maximal
O2 uptake for 10 wk (4-5
days/wk) at one of three different exercise durations (30, 60, or 90 min/day). Training resulted in increases
(P < 0.05) in citrate synthase activity in the soleus and extensor digitorum longus in both the 60 and
90 min/day duration groups and in the plantaris (Pla) in all three
exercise groups. All durations of training resulted in a reduction
(P < 0.05) in the percentage of
MHCIIb and an increase (P < 0.05) in the percentage of
MHCIIa in the Pla. The magnitude of change in the percentage of
MHCIIb in the Pla increased as a
function of the training duration. In the extensor digitorum longus, 90 min of daily exercise promoted a decrease
(P < 0.05) in percentage of
MHCIIb and increases
(P < 0.05) in the percentages of
MHCI,
MHCIIa, and
MHCIId/x. Finally, training
durations 
60 min resulted in an increase
(P < 0.05) in the
percentage of MHCI and a
concomitant decrease (P < 0.05) in
the percentage of MHCIIa in the
soleus. These results demonstrate that increasing the training duration
elevates the magnitude of the fast-to-slow shift in MHC phenotype in
rat hindlimb muscles.
endurance exercise; muscle plasticity; fiber type; oxidative capacity
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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THE CONTRACTILE PROTEIN MYOSIN plays an important role in dictating the functional properties of skeletal muscle fibers. Myosin is known to exist as multiple isoforms in skeletal muscle as a result of polymorphic expression of both heavy and light chain components. Adult rat muscle fibers contain four major electrophoretically distinct myosin heavy chain (MHC) isoforms: three fast MHC isoforms (MHCIIb, MHCIId/x, and MHCIIa) and one slow MHC isoform (MHCI) (3, 28).
It is clear that endurance-exercise training promotes numerous adaptations in skeletal muscle, including enhancement of fiber oxidative and antioxidant capacities (10, 16, 22). Furthermore, the dose-response relationship between exercise intensity and duration and training-induced changes in muscle oxidative and antioxidant capacities is well established (9, 10, 22). In contrast, numerous questions remain regarding the effects of endurance training on muscle MHC isoforms. Although there is growing evidence that endurance training promotes changes in skeletal muscle myosin phenotype (5, 12, 15, 32), the dose-response relationship between exercise duration and muscle MHC phenotype remains relatively uninvestigated; this forms the rationale for the present study.
In contrast to the paucity of data on the influence of endurance exercise on MHC isoforms, many investigations have explored the effects of low-frequency (e.g., 10-Hz), chronic electrical stimulation (e.g., 10 h/day) on muscle fiber phenotype (see Refs. 20 and 21 for reviews). In this regard, electrical stimulation experiments demonstrate that this type of muscular activity can promote a significant transformation of fast MHC isoforms (i.e., MHCIIb, MHCIId/x, and MHCIIa) to the slow MHC isoform (MHCI) in specific experimental conditions (17, 31, 34, 35). These results could be interpreted as an indication that the exercise-induced MHC transformation process is primarily regulated by the total amount of contractile activity (reviewed in Ref. 19). On the basis of this assumption, it seems likely that increasing the daily training duration of animals performing whole body endurance exercise would result in greater MHC isoform shifts compared with those of exercise bouts of shorter duration.
To date, no studies have examined the relationship between whole body exercise training duration and the magnitude of MHC isoform transformation in skeletal muscle. Hence, by using three different daily durations of treadmill exercise, this study examines the exercise dose-response relationship as it pertains to skeletal muscle MHC transformation. We hypothesized that increasing the daily training duration would result in a greater fast-to-slow shift in MHC expression in skeletal muscles.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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This experiment was approved by the University Committee for use of animals in research and followed the guidelines established by the American Physiological Society.
Animals. Sixty-three female Sprague-Dawley rats (120 days old) were fed rat chow and water ad libitum and were maintained on a 12:12-h light-dark photoperiod. By investigating 4-mo-old rats (6.5 mo old at the date they were killed), we avoided the potential bias associated with myosin phenotype differences in muscle due to development (2). To avoid interanimal differences in physical activity of sedentary controls, animals were housed in standard cages for the duration of the experimental period. Similarly, trained animals were housed in the same standard cages during the experimental period.
Exercise training protocol.
Rats were selected by their willingness to run on a motorized treadmill
and were randomly assigned to either a sedentary control group
(n = 10) or one of three exercise
training groups: 1) 30 min/day
(n = 15),
2) 60 min/day
(n = 18), and
3) 90 min/day
(n = 20). The initial sample size in
the exercise training groups was varied to account for a loss of
animals from the study due to exercise-induced injury. The exercise
training protocols for the three training groups are outlined in Table
1. Briefly, to examine the effects of
duration of exercise training on the MHC isoforms, we examined three
durations (30, 60, and 90 min/day) of exercise training at the same
training intensity. This training intensity was designed to elicit
~70-75% maximal O2 uptake
(unpublished observations). The intensity of exercise was progressively
increased over the 10-wk training period in an effort to maintain the
same relative work rate throughout the training period (Table 1). We
have shown previously that this protocol results in a large and
duration-dependent increase in oxidative capacity in the plantaris (Pla) muscle (22). Electrical shocks were used sparingly to motivate
the animals to run.
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Tissue removal.
Twenty-four hours after the last training session, the animals were
killed with an intraperitoneal injection of 90 mg/kg pentobarbital sodium. The soleus (Sol), Pla, and extensor digitorum longus (EDL) muscles were quickly removed. Tissue for biochemical analysis was
quickly frozen in liquid nitrogen and then stored at 
80°C until assay. Furthermore, muscle samples to be used for histochemical analysis were immediately frozen (at an excised length) in isopentane cooled by liquid nitrogen. These samples were stored at also
80°C for subsequent histochemical analysis to determine
fiber type and fiber cross-sectional area (CSA).
Biochemical assays. After being thawed, muscle samples were quickly dissected free of fat and tendon before homogenization. Muscle samples from the left hindlimb were used to determine citrate synthase (CS) activity and protein concentration, and samples from right hindlimb were used to isolate myofibrillar protein.
For CS activity, muscle samples were homogenized in cold 100 mM phosphate buffer with 0.05% bovine serum albumin (1:20 wt/vol, pH 7.4). Homogenates were then centrifuged at 4°C for 10 min at 700 g. The resulting supernatant was decanted and assayed for enzyme activity and protein concentration. CS activity was determined at 25°C by using the procedure described by Srere (30) to document the increasing mitochondrial density and to prove the effectiveness of the exercise program. Samples were assayed in duplicate, and samples from all animals were assayed on the same day to reduce interassay variation. In our hands, the coefficient of variation was ~3%. Total protein in the homogenate was assayed by using the technique described by Bradford (6).Isolation of myofibrils. Muscle samples used for myofibrillar isolation were homogenized by using the technique modified by Baldwin et al. (2) from the original technique described by Solaro et al. (29). Myofibrillar protein concentration was determined by the Biuret method (14).
SDS-PAGE MHC analysis. MHC composition was assessed by using SDS-PAGE procedures described by Talmadge and Roy (33). Briefly, after determination of protein content, a sample of denaturated myofibrillar protein was loaded onto a 16-cm-long vertical gel (8% separating and 4% stacking gel; glycerol 30% wt/vol) and electrophoresed for 20 h at 8°C. To identify MHC bands, myosin standard (Sigma Chemical) and a mixture of myofibrillar protein from the Sol, Pla, and EDL were loaded on different cells throughout the gel. Gels were stained with Coomassie blue R-250 and destained by diffusion in a methanol-glacial acetic acid solution. On the basis of their migration pattern on SDS-PAGE, four different MHC bands, corresponding to ~205-kDa myosin standard, were identified as MHCI, MHCIIb, MHCIId/x, and MHCIIa. The relative concentrations of MHC isoforms were determined by scanning the gels by using a computerized densitometric image-analysis system.
Muscle fiber typing and morphometry. To evaluate the effects of training on muscle fiber CSA, we performed morphological analysis of the Sol, Pla, and EDL from the 90-min daily exercise group. This group was selected for analysis because we anticipated that, if exercise resulted in training-induced changes in fiber CSA, it would most likely occur in this treatment group. Therefore, muscle fiber type and morphological analysis was performed on randomly selected samples from the control (n = 4) and the 90 min/day training group (n = 4). This histological analysis was used to assist in our interpretation of the SDS-PAGE MHC data. For example, morphological assessment would determine whether a training-induced alteration in the percentage of MHC isoforms (observed by SDS-PAGE MHC analysis) was due to fiber type transformation or was simply due to selective changes in fiber CSA (e.g., increase in type I or decrease in type II fibers CSA).
Serial cross sections of each muscle were cut at 10 µm in a cryostat maintained at25°C. Muscle fibers were classified as type I,
IIa, IId/x, or IIb on the basis of their staining for myofibrillar
actomyosin ATPase by using techniques described by Sant'ana Pereira et
al. (27). The image of the muscle cross section was magnified by using
a Nikon light microscope (model Apaphot 2, Apaphot, Tokyo, Japan), and
an image was obtained via a computer image-processing
system. Fiber typing and the CSA of each fiber were
determined by using computerized planimetry (NIH Image 1.59 analysis
software) with the system being calibrated by using a stage micrometer
immediately before measurement. The proportions of fiber types were
determined from a sample of 500-700 fibers across the entire
section of each muscle.
Statistical analysis. Data were analyzed by using analysis of variance. When there was a significant F-ratio, a Tukey test was performed post hoc. Statistical significance was set at P < 0.05.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Animals that completed >90% of the prescribed exercise training sessions and were actively running during the last 2 wk of the training program were included in the data analysis (i.e., 30 min/day, n = 13; 60 min/day, n = 14; 90 min/day, n = 12).
Body weight. Initial and final body weights did not differ among groups [initial: control = 268.3 ± 6.5 (SE), 30 min/day = 260 ± 7.5; 60 min/day = 264 ± 4.3, and 90 min/day = 267.9 ± 5.5 g; and final: control = 298.9 ± 7, 30 min/day = 289 ± 3, 60 min/day = 294.4 ± 4, and 90 min/day = 293 ± 6 g].
Muscle CS activity.
Figure 1 shows the activities (means ± SE) of CS in the Sol, Pla, and EDL muscles. The 10-wk training program
resulted in a significant (P < 0.05) increase in CS activity (all durations) in Pla muscle and in
the 60 and 90 min/day groups in Sol and EDL muscles. In general, CS
activity increased as a function of exercise duration. In the 60 and 90 min/day groups, CS activity was significantly (P < 0.05) higher than the 30-min
group in all muscles studied.
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MHC isoform distribution.
Figure 2 shows the relative distribution of
MHC isoforms in all muscles, and Fig. 3
shows representative gels illustrating the endurance training-induced
changes in MHC. In the Sol, composed of only
MHCI and
MHCIIa, the percentage of
MHCI increased and MHCIIa decreased with training
durations 60 min. No differences (P > 0.05) existed between the 60- and 90-min training groups in the
percentage of either MHCI or
MHCIIa.
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Muscle morphometry.
Figure 4 shows the fiber number, fiber CSA,
and percentage of muscle CSA comprised by each fiber type in both the
control and 90 min/day training groups. First, in all muscles
investigated, the percentages of fiber CSA in both control and 90 min/day training groups were very similar to the percent distribution
of MHC analyzed by SDS-PAGE. Second, note that exercise training did
not significantly alter muscle fiber CSA in the Sol or Pla muscle, but
training did promote a small but significant increase in the CSA of
type IId/x fibers within the EDL. Third, note that endurance training promoted an increase in the number of both type IIa and IId/x fibers
(P < 0.05) and a concomitant
decrease in the number of IIb fibers
(P < 0.05) in both the Pla and EDL
muscles. Finally, there was a strong but nonsignificant trend
(P = 0.056) toward a training-induced
increase in the number of type I fibers in Sol muscle. This lack of
statistical significance was due to a small sample size (i.e., low
statistical power) because three of four Sol muscles from the 90 min/day training group expressed 100% type I fibers.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Overview of principal findings. To our knowledge, this is the first experiment to demonstrate that increasing the daily duration of exercise increases the magnitude of MHC isoform transformation in locomotor muscles. Our data indicate that whole body exercise training is capable of inducing a fast (type II)-to-slow (type I) shift in the MHC isoform pool within both "slow" and "fast" skeletal muscles. This shift in the total muscle MHC pool is not due to selective changes in fiber CSA but is due to a training-induced transformation in muscle MHC phenotype. Furthermore, the minimal amount of treadmill running required to induce changes in MHC isoforms varies across muscles.
Exercise-induced alterations in MHC composition. Because these experiments examined the effects of whole body exercise on skeletal muscle MHC isoform content, the interpretation of our results is more complex than that of electrical stimulation models where muscle activation can be applied on a continuous basis. For example, a key consideration is the way in which the increase in physical activity (i.e., treadmill running) is distributed among the numerous motor units of locomotor muscles. During exercise, motor units are normally recruited in an orderly fashion (e.g., size principle) (23). As a consequence, the primary training effects are observed in those motor units that are infrequently used during resting conditions (i.e., nonpostural muscles) (25, 26). Because we investigated locomotor muscles that differ in their initial MHC profiles and mechanical action, it would be predicted that these muscles would also vary in their recruitment pattern during exercise (23). Indeed, during short-term submaximal running, blood flow is greater in the Sol compared with that in both the Pla and EDL (1). Furthermore, during this type of exercise, blood flow is greater in the Pla compared with that in EDL (1). This finding has been interpreted as an indication of intermuscle differences in motor unit activity and metabolic rates (1). It follows that the training-induced changes in MHC profile should vary among muscles on the basis of these differences. Indeed, this was the case; a brief discussion of the training-induced changes in the MHC profile of each of the muscles investigated follows.
Sol. In the adult untrained Sprague-Dawley rats, the Sol muscle is primarily a slow muscle, which is composed of ~90% MHCI and ~10% is MHCIIa. Hence, endurance exercise-induced transformation in MHC pools would be restricted to a MHCIIa-to-MHCI shift. Our data reveal that 30 min of daily exercise did not significantly alter MHC content of the soleus. However, increasing the exercise duration to 60 or 90 min promoted a significant shift from MHCIIa to MHCI (Fig. 2). We interpret this observation as support for the notion that a minimal duration of exercise is required to promote changes in muscle myosin phenotype. The minimal duration concept has been discussed in detail by Salmons (24, 25); the idea is simply that there are specific levels of activity that must be exceeded for changes in myosin isoforms to occur.
Although a trend existed, our findings did not indicate that a statistically significant, stepwise, exercise duration-induced increase in MHCI content occurred in this muscle. Note, however, that the Sol muscle from five animals in the 90 min/day exercise group was composed of 100% MHCI. Hence, the failure to observe a stepwise exercise-induced shift in MHC content in the Sol may be due to the unique MHC composition of this muscle.Pla. The Pla is a fast muscle with >75% of its MHC pool existing as MHCIIb and MHCIId/x. Our results indicate that all durations of exercise training promoted a fast-to-slow shift in MHCs. We interpret these findings as an indication that the duration of running required for MHC transformation in the Pla muscle is relatively low compared with that in the Sol.
Furthermore, the training-induced decrease in the percentage of MHCIIb followed an exercise duration-dependent pattern. Indeed, there was a stepwise decrease in MHCIIb distribution with increasing exercise duration. For example, MHCIIb in the Pla of untrained animals comprised ~35% of the total MHC pool; this percent declined to ~30, 25, and 20% in the 30, 60, 90 min/day trained animals, respectively. Interestingly, although training tended to elevate the percentages of both MHCIId/x and MHCI within the Pla, these increases were not significant. In contrast, training promoted significant increases in MHCIIa.EDL. Of the muscles investigated, the EDL contained the highest percentage of fast MHC and the lowest percentage of MHCI. Although there tended to be a decrease in the percentage of MHCIIb content with increasing daily training duration, this difference was significant only in the 90 min/day training group. The reduction in MHCIIb isoform was accompanied by a concomitant increase in the percentages of MHCIId/x, MHCIIa, and MHCI. Therefore, compared with the Sol and Pla muscles, the EDL requires a longer daily duration of running to mediate a shift in MHC phenotype. The mechanism to explain this difference is unclear but could be related to the differences in the initial MHC profile and mechanical action (e.g., dorsiflexion vs. plantar flexion) of the EDL muscle. Furthermore, there is an altered recruitment pattern of motor units during prolonged exercise. In this regard, evidence exists that, during prolonged running at speeds that initially do not recruit all motor units of a muscle, there is a progressive recruitment of motor units to compensate for contractile fatigue. This results in the recruitment of more and more fast motor units over time (13).
Chronic, low-frequency electrical stimulation has been shown to promote an increase in the percentage of MHCI in both rabbit and rat skeletal muscles (31, 34, 35; see Ref. 21 for review). However, to our knowledge, this is the first investigation to demonstrate that high-intensity, prolonged-duration exercise is also capable of inducing an increase in the percentage of MHCI content in rat EDL muscle.Relationship between muscle fiber type and oxidative capacity. Increased muscular activity, as occurs during endurance training, brings about a variety of metabolic adaptations (see Ref. 16 for a review). In the studies where rats run daily on motor-driven treadmills for different durations, a new steady-state level of mitochondrial oxidative enzyme activities has been shown to be directly proportional to the exercise time (9, 10, 22). Similar to previous studies (9, 10, 22), the present study demonstrated that increase in the duration of exercise promotes a greater adaptive response in muscle oxidative capacity. In this regard, it has been shown that mitochondria obtained from muscles of endurance-trained animals exhibit a high level of respiratory control and tightly coupled oxidative phosphorylation, which indicates that the increase in oxidative capacity of muscles is accompanied by a corresponding increase in the capacity for regenerating of ATP via oxidative phosphorylation (16).
The present study reconfirms the postulate that the oxidative capacity of a muscle is related to its fiber type distribution. For example, when combining MHC data from both the Pla and EDL muscles, CS activity was negatively correlated with the percentage of MHCIIb (r =0.76,
P < 0.05) and positively correlated
with the percentage of MHCI
(r = 0.72, P < 0.05). On the basis of previous reports, it could be predicted that these observed training-induced changes in skeletal muscle metabolic properties would be associated with an improvement in muscle endurance (reviewed in Ref. 11)
Relationship between muscle fiber type and maximal shortening velocity (Vmax). Although the present study did not examine training-mediated changes in muscle Vmax, a brief comment regarding the potential impact of activity-induced MHC alterations on muscle Vmax is relevant. Although there are many factors that determine the Vmax of a muscle fiber, it is clear that ATP hydrolysis by myosin ATPase is a primary determinant (reviewed in Ref. 8). Indeed, muscle shortening velocity is significantly correlated with myosin ATPase activity (4).
Because Vmax is associated with myosin ATPase activity, it follows that any factor that influences muscle ATPase activity should alter Vmax. An important determinant of ATPase activity in muscle is the MHC composition. In this regard, it is well established that MHC isoforms differ in their ATPase activity, with type IIb MHC isforms containing the highest and type I MHC isoforms containing the lowest ATPase activity (reviewed in Ref. 18). In the present investigation, it seems likely that the training-induced decrease in type IIb MHC along with the increase in types IId/x, IIa, and I MHC in some muscles (i.e., EDL) could result in a decrease in muscle Vmax. Direct evidence for this type of response has been provided by studies in which the percentage of type IIb MHC was decreased and type I MHC increased in response to hypothyroidism (7).Regulation of MHC gene expression.
Although the purpose of the present experiments was not to delineate
the mechanism responsible for the exercise-induced change in MHC
phenotype, a brief discussion of potential regulating factors seems
warranted. The expression of myosin genes can be regulated in adult
skeletal muscle by a variety of factors, including neural innervation,
hormonal action, electrical stimulation, and mechanical activity (see
Ref. 20 for a review). For example,
MHCI can be induced in rat
skeletal muscle by a reduction in circulating thyroid hormone or
electrical stimulation of the muscle at a low frequency (20, 28).
Interestingly, MHC transitions appear to reflect an obligatory
pathway of MHC gene expression in the following order (20, 28, 35):
MHCI 
MHCIIa MHCIId/x MHCIIb. Changes in
contractile activity can drive the transformation in either direction
along the pathway (28). Experiments to determine those factors that
regulate MHC gene expression continue to be an active area of research.
Summary and conclusions. These experiments tested the hypothesis that increasing the daily training duration will result in a progressive fast-to-slow shift in the MHC content in skeletal muscles. The data clearly support this postulate and also demonstrate that whole body exercise training is capable of inducing a fast (type II)-to-slow (type I) shift in MHC isoforms within a specific skeletal muscle. Furthermore, our results indicate that the total amount of treadmill running required for transformation of MHC phenotype varies across locomotor skeletal muscles and presumably relates to the differences in recruitment pattern of fibers.
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ACKNOWLEDGEMENTS |
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The authors thank Dr. R. S. Staron for the thoughtful critique of this manuscript. We also thank Louise Fletcher and Iaonnis Vrabas for expert technical help.
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FOOTNOTES |
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This work is supported by National Institute on Aging Grant R03-AG-14779 awarded to S. K. Powers.
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: S. K. Powers, Dept. of Exercise and Sport Sciences and Physiology, Center for Exercise Science, Rm. 33, FLG, Univ. of Florida, Gainesville, FL 32611.
Received 2 April 1998; accepted in final form 12 November 1998.
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METHODS
RESULTS
DISCUSSION
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