The maximal power of the lower limbs was determined in four astronauts (age 37–53 yr) 1) during maximal pushes of ∼250 ms on force platforms [“maximal explosive power” (MEP)] or2) during all-out bouts of 6–7 s on an isokinetic cycloergometer [pedal frequency 1 Hz: maximal cycling power (MCP)]. The measurements were done before and immediately after spaceflights of 31–180 days. Before flight, peak and mean values were 3.18 ± 0.38 and 1.5 ± 0.13 (SD) kW for MEP and 1.17 ± 0.12 and 0.68 ± 0.08 kW for MCP, respectively. After reentry, MEP was reduced to 67% after 31 days and to 45% after 180 days. MCP decreased less, attaining ∼75% of preflight level, regardless of the flight duration. The recovery of MCP was essentially complete 2 wk after reentry, whereas that of MEP was slower, a complete recovery occurring after an estimated time close to that spent in flight. In the same subjects, the muscle mass of the lower limbs, as assessed by NMR, decreased by 9–13%, irrespective of flight duration (J. Zange, K. Müller, M. Schuber, H. Wackerhage, U. Hoffmann, R. W. Günther, G. Adam, J. M. Neuerburg, V. E. Sinitsyn, A. O. Bacharev, and O. I. Belichenko.Int. J. Sports Med. 18,Suppl. 4: S308–S309, 1997). The larger fall in maximal power, compared with that in muscle mass, suggests that a fraction of the former (especially relevant for MEP) is due to the effects of weightlessness on the motor unit recruitment pattern.
- muscle power
- Euromir missions
since the beginning of the spaceflight era, weightlessness was shown to lead to substantial changes in muscle function (for a review, see Ref. 11). These changes, globally defined as deconditioning, consist mainly of loss of muscle mass and force, increased muscle fatigability, and abnormal reflex patterns (17, 19, 21, 27). They are likely due to an imbalance between muscle protein synthesis and catabolism, brought about by the absence of the constant pull of gravity, particularly in weight-bearing muscles, and similar to that observed during immobilization of fractured limbs or during prolonged bed rest without exercise (13, 23,28, 31, 32). Animal studies have also shown significant changes in rat muscle, as a consequence of 12.5–22 days of spaceflight. These changes consisted of reduction of mass and diameter of slow-twitch fibers and decrease in muscle force, as well as molecular rearrangements of myosin heavy chains occurring already within the first week of spaceflight (5, 6, 12, 24, 26).
In humans, muscle force and velocity were studied by using a Cybex dynamometer before and after the Skylab missions (2, 3, and 4 of 28, 59, and 84 days, respectively) during which the crews performed minimal to vigorous physical exercise to prevent muscular decay. Nevertheless, the leg extensor force was reduced by 25% after the 28-day Skylab-2 mission (35) and by 6.5% after the 84-day Skylab-4 mission (19). Isokinetic (eccentric and concentric) force was also measured before and after 5–11 days of spaceflight in 19 subjects. At reentry, concentric muscle force of the quadriceps, trunk flexors, and trunk extensors had decreased significantly (13, 10, and 23%, respectively) compared with preflight values (19). However, isovelocity muscle contractions never, or only seldom, occur in everyday life. We therefore set out to compare the effects of microgravity on maximal muscular power of the lower limbs of astronauts and cosmonauts during short efforts, in which either the velocity was imposed by the experimenters or both variables (force and velocity) were dependent on the subjects’ muscle action. The experiments were performed before and after the two missions, Euromir ’94 and ’95, jointly organized by the European and Russian space agencies.
MATERIALS AND METHODS
The procedures reported in the literature to determine the maximal power during very short all-out efforts in humans can be subdivided into two broad groups: 1) “instantaneous” methods, in which the power is assessed during a single, very short (<1-s) contraction of the extensor muscles of the lower limbs, such as a standing high jump off both feet; and2) “average” methods, in which the power is determined on a longer time basis (5–7 s) over an even number of contractions of the muscles of one limb at a time, such as pedaling maximally or running upstairs (for reviews, see Refs. 7 and13a). In this study we determined the maximal power according to both procedures by means of a newly developed instrument, the multipurpose ergometer dynamometer [MED (3, 37)], the technical characteristics of which are summarized below (seeMED).
Four male subjects (S1–S4), whose characteristics are reported in Table 1, were studied before and after spaceflights of 31- to 180-day duration. An additional subject (S5) has been studied only after reentry from the longest mission in manned spaceflight history so far (438 days).
The MED (Fig. 1) consists of two rectangular (3 × 0.9-m) metal frames hinged at one end. Two precision rails are fixed to the upper frame, which can be inclined by means of a hydraulic jack up to an angle of 30° with respect to the lower one. A seat is fixed on a carriage that is free to move by means of four ball bearings on the rails. An isokinetic cycloergometer, powered by a 4-kW electric motor, is fixed to the hinged end of the MED, between the rails. The electric motor is controlled by an inverter so that the pedaling frequency can be varied from 0.5 to 4 Hz. The power of the motor is large enough to avoid being overridden by the subject, even during an instantaneous all-out effort. A strain-gauge system (SRM Powermeter and Powercontrol II), mounted on the chain ring, yields continuous measurements of the force exerted by the subject on the pedals. The mechanical power, as given by the product of the torque times the angular velocity, is calculated on a 10-ms basis and displayed to the subject on the front panel for visual feedback control. When the MED is used as a cycloergometer, the carriage seat is fixed in a given position by means of adjustable electromagnetic blocks.
Two force platforms, which, when the MED is used as a cycloergometer, are tilted upward so as not to interfere with the movements of the pedals and of the lower limbs, are also fixed to the hinged end of the upper frame.
When the MED is used for instantaneous power assessment, the electromagnetic blocks are removed and the force platforms are tilted down so that the subject pushing on them can accelerate himself and the carriage seat (41.4 kg) backward. A couple of adjustable mechanical blocks can be appropriately positioned on the rails, thus setting the minimum distance between the carriage seat and the platforms. The backward movement of the carriage is stopped by two shock absorbers mounted on the back of the main frame. The force exerted on the force platforms is measured by two load cells (PA40 300, Laumas), indwelling in the platforms in such a way as to be unaffected by the point of application of the push. The backward velocity is recorded by means of a wire tachometer (PT8201, Celesco) connected to the carriage seat and fixed to the frame of the MED. The analog outputs of the force and velocity transducers are digitalized and recorded by means of a data-acquisition system (MP 100, Biopac) for subsequent analysis. The mechanical power (W˙) developed by the subject is obtained from the instantaneous product of the total force (F; sum of the two legs) times the backward speed (V ) Equation 1Before use, the MED was inspected and granted approval for use in human experiments by the appropriate European Space Agency committee (further details on the construction and operation of the MED can be found in Ref. 37).
The maximal power of the lower limbs was assessed after both an instantaneous and an average method as defined by Capelli and di Prampero (7). The instantaneous procedure consisted of a series of six maximal pushes with both feet on the force platforms, with a resting interval of 2 min between pushes. To optimize the force developed by the quadriceps femoris, the maximal pushes were performed from a knee angle of 110° (22, 25). The requested knee angle was obtained by adjusting the position of the mechanical blocks, which also prevented the motion of the carriage seat toward the platforms, thus impeding any countermovement and, consequently, recovery of elastic energy (37). The subjects sat on the carriage seat of the MED with arms on the handlebar and soles of the feet leaning against the platforms. The platforms were positioned perpendicularly to the rails, and the main frame was inclined 20° with respect to the horizontal position (see Fig. 1). The time course of force, velocity, and power (as calculated from Eq. 1 ) during a maximal instantaneous push is reported in Fig.2. Analysis of the time course ofW˙ allowed us to assess its peak (W˙peak, kW) and mean (W˙mean, kW) values. In turn,W˙mean was determined as Equation 2wheret W˙is the duration of the work phase. Throughout this report, the power assessed by means of this procedure will be defined “maximal explosive power” (MEP).
The average procedure was similar to that proposed by Ikuta and Ikai (18); it consisted of a bout of five to seven “all-out” pedal revolutions at the frequency of 1 Hz. These bouts were performed from a brief period of free wheel pedaling, either at rest or 5–7 min after mild aerobic exercise. The power developed over the three most forceful pedal revolutions during a single bout of 5- to 6-s duration was calculated as described above and averaged to yield what will be defined here as “maximal cycling power” (MCP). A typical tracing obtained during a maximal cycling bout is reported in Fig.3, which shows that the force exerted on the pedal shaft varies sinusoidally from zero, when the pedal is vertical, to a maximum, when the pedal is horizontal. The maximal force value is defined Fpeak, whereas the average force throughout one revolution is defined Fmean. Because the pedal frequency was constant (1 Hz), these two force values yielded two power values:W˙peak andW˙mean. It should be remembered that, in cycling, only one limb is active at a time instead of both simultaneously, as is the case for MEP, a fact that should be kept in mind when the absolute force or power values obtained by means of the two methods are compared.
The data were collected before flight [launch (L)] at days L − 230, L − 68, and L − 48 forS1 andS2; at days L − 75 and L − 15 for S3 andS4 and after flight [return (R); at days R+2, R+6, and R+11 for S1; R+3, R+8, and R+12 for S2; and R+2, R+6, R+12, R+14, and R+26, for S3 andS4]. As mentioned above (seeSubjects),S5 was tested after flight only, at days R+2, R+6, and R+11.
The experimental protocol was approved by the ethical committees and by the medical boards of the two Euromir missions, and all subjects signed an informed consent agreement.
The differences between the parameters observed in the different postflight baseline data collections were investigated by using an ANOVA. A post hoc Bonferroni test (Systat 5.2.1 for Macintosh) was then applied to determine the significance of the differences between the average values obtained pre- vs. postflight from repeated measures of any given parameter. The differences were considered significant forP < 0.05.
The average values (±1 SD) ofW˙peak andW˙mean for both MEP and MCP are reported in Table 2 in percentage of preflight values, together with the subjects’ body masses. In Table 2, the absolute preflight values ofW˙peakand W˙mean are reported in brackets for preflight conditions only.
In S1, the preflight baselines of MEP and MCP were calculated by averaging the values obtained in all experimental sessions. For S2, however, the data obtained at L − 48 were not considered because of his suboptimal physical status. In the case ofS3 andS4, we observed a learning or training effect between L − 75 and L − 15, on the order of 10% for both MEP and MCP for S3 and of 5 and 30% for MEP and MCP for S4, respectively. Therefore, in these subjects, the preflight baseline values retained for comparison were those recorded at L − 15.
S5 was not investigated before flight; in this case, therefore, preflight MEP, when expressed per kilogram of body mass, was assumed to be equal to the average observed preflight in the other subjects. MCP was not assessed in this subject.
Before flightW˙peak ranged from 3.74 to 2.88 kW for MEP and from 1.33 to 1.05 kW for MCP, whereasW˙mean ranged from 1.70 to 1.41 kW for MEP and from 0.79 to 0.59 kW for MCP. Table 2 shows that W˙peak andW˙mean for both MEP and MCP were substantially reduced, approximately by the same amount, after reentry.
Indeed, at R+2 (R+3) expressed as a percentage of preflight values, MEP amounted to ∼68% in S1 (31 days in microgravity) and to ∼50% in the three subjects who spent 169–180 days in microgravity (S2,S3, andS4). Furthermore in subjectS5, who remained in space for 438 days, MEP did not seem to fall below ∼50% of the preflight value. It should be remembered, however, that preflight MEP was not determined inS5: it was assumed to be equal (per kg body mass) to that observed on the other subjects.
After flight, MCP was reduced to a lesser extent than was MEP (see Table 2). In addition, the effects of the flight duration seemed to be less pronounced for MCP than for MEP. Indeed, MCP at R+2 (R+3) (average ofW˙peakand W˙mean) amounted to ∼81% of preflight after 31 days in microgravity (S1) and to ∼70% after 169–180 days (S2,S3, andS4).
The recovery of MCP after flight seemed to be rather fast. Indeed, with the possible exception of S4, it was essentially complete within 2 wk (Table 2). At variance with MCP, the recovery of MEP seemed to follow a slower time course and, as a first approximation, could be described by a monoexponential function (Fig.4) Equation 3wherey(d) is W˙mean (W/kg) at day d,A andA R+2 are the corresponding individual values assessed preflight or after reentry at R+2 (or R+3), and B is a time constant in days.
By using an iterative statistical package (Systat 5.2.1),Eq. 3 was solved for each subject.A andB, together with the determination coefficient (r 2) and the number of points (n) of each individual regression, are reported in Table3. Because the asymptote of an exponential is reached after about five time constants, the time (days) for complete recovery (R) was calculated as R = 5 ⋅ B and tends to be longer, the longer the duration of the preceding flight.
The instantaneous procedure yielding MEP allowed us to determine several other variables of physiological interest, such as peak force (Fpeak; kN), peak velocity (V peak; m/s); maximal acceleration during the backward movement [(dV/dt)max; m * s−2], and duration of the positive work phase (t w˙; s). These values are reported below in some detail. For simplicity, only nonsignificant differences are indicated by NS.
The preflight Fpeak ranged from 1.74 to 2.06 kN. It decreased by 11.7% after 31 days (S1 at R+2), 26.2% after 169 days (S2 at R+3), and 31.5 and 27.0% after 180 days of spaceflight (S3 andS4 at R+2, respectively). The recovery of Fpeak after reentry was faster for S1, who at R+6 and at R+11 had attained values of only ∼5% (NS) to 10% lower than preflight. On the contrary, in the three subjects who spent 169–180 days in microgravity, Fpeak was still 15–24% lower than preflight at R+11 and R+12, and, in subjectsS3 andS4, 12–22% lower at R+26.
The duration of the push phase immediately after spaceflight remained essentially unchanged in S1 (31 days in microgravity), whereas it increased on average by ∼12% after 169–180 days in space (S2,S3, andS4).
V peak attained during the push phase ranged from 2.76 to 2.29 m/s. It was substantially reduced in all subjects after reentry: −24.2% after 31 days (S1 at R+2) and −27.8 to −35.8% after 169–180 days (S2,S3, andS4 at R+2 or R+3). As was the case for Fpeak, the recovery ofV peak was faster in S1, who had attained the preflight value (actually 98.6%, NS) at R+11, than in the three other subjects. Indeed, S2 recovered only to −13.4% at R+12, whereas S3 andS4 were still below the preflight values (−5.7 and −24.0%, respectively) at R+26.
The preflight (dV/dt)maxvalues were close to 1 G (9.81 m * s−2) for all subjects (average value: 10.0 m * s−2). InS1, who spent 31 days in microgravity, (dV/dt)maxshowed only a nonsignificant decrease at R+2 (90.26%, NS) and a complete recovery at R+11 (103.4%, NS). In the three subjects who spent 169–180 days in microgravity, (dV/dt)maxdropped to 62.3, 68.4, and to 59.3% of preflight values at R+2 (R+3) and recovered only to 69.8, 85.6, and to 62.2% at R+12 (S2) and R+26 (S3 andS4), respectively.
Maximal muscle power was determined by two different means:1) an instantaneous procedure of ∼0.3-s duration, yielding MEP and2) an average procedure, consisting of a 5- to 6-s all-out pedaling bout on an isokinetic cycloergometer, yielding MCP.
Both procedures, despite their widely different duration, depend energetically on anaerobic alactic sources (mainly phosphocreatine splitting). In addition, in both cases the active muscles are essentially the same (primarily knee extensors), and the recovery of elastic energy is negligible, a fact that is obvious for MCP and that has been recently demonstrated for MEP (37). Thus the main difference between MEP and MCP is the velocity of movement, which is much higher for MEP. With this in mind, we will now briefly discuss the salient characteristics of both procedures with the purpose of drawing a comparison between the two.
The power developed during very short all-out efforts can be assumed to depend on 1) the active muscle mass,2) the intrinsic characteristics of the recruited motor units, and 3) a fast and coordinated recruitment pattern. If this is so, the decrease in MEP and MPC observed after spaceflight could be due to any of these three factors or to a combination thereof.
Morphological data obtained by Zange et al. (38), by means of nuclear magnetic resonance of the subjects’ calf muscles immediately after reentry, demonstrate a decrease in the muscle cross-sectional area (CSA) ranging from 9% in S1 to 13%, on average, for S2,S3, andS4. In addition, in two subjects (S3 andS4) the CSA of the thigh was estimated from measurements of the circumference 20 cm above the upper margin of the patella. The resulting changes in the CSA at R+2 were −9.0% for S3 and −17.8% for S4, with no differences between the left and right thigh. Because, at R+2, the body mass ofS3 andS4 had decreased by 6 and 3% only (see Table 2), respectively, the above changes in CSA of the thigh are due essentially to changes in muscle mass. These changes are on the same order as observed in the same subjects for the CSA of the calf, which amounted to −13 and −20% forS3 andS4, respectively (J. Zange, personal communication). Thus the percent changes observed by Zange et al. (38) in the calf can be assumed to be a measure of the changes in CSA of all active muscles. If an unchanged muscle length is assumed, the observed changes in CSA must be equal to the changes in muscle mass. Thus the percent MEP values observed after flight can be expressed relative to the muscle mass in percentage of preflight values. For MEP, these calculations at R+2 (R+3) amount to 0.67/0.91 = 0.74 forS1 and to 0.47/0.87 = 0.54 forS2,S3, andS4 (average).
It is therefore apparent that, in the case of MEP, the decrease in muscle mass is much smaller than the decrease in the power output throughout the investigated microgravity duration (31–180 days). It necessarily follows that other mechanisms must be responsible for the observed decline in MEP.
Under all experimental conditions, the fall in MEP was due to essentially equal declines in force and velocity (seeresults). For all subjects, with the exception of S1, the duration of the push increased after flight, this being presumably an attempt to reduce the fall in force by increasing its time of application. This set of observations can be tentatively attributed to either1) changes in the motor unit types, which tend to become slower; and/or2) a slower motor unit recruitment pattern.
The former possibility seems rather unlikely in view of the data obtained in animals after microgravity, which show the opposite trend (11, 12, 33). Similar “slow-to-fast” changes in muscle characteristics have been shown in humans as a consequence of spaceflights of short duration (15, 39).
We therefore think that, besides the above-mentioned decrease in muscle mass, the major factor responsible for the decline in MEP is a change in the motor unit recruitment patterns brought about by the absence of gravity. This hypothesis is similar to that put forward by other authors as “hypogravitational ataxia” (17). In essence, this state of affairs is the opposite of the early effects of muscle strength training, in which case the changes in muscle force precede, and are larger than, those in muscle mass, presumably because of more effective motor unit recruitment patterns (30). In addition, data recently reported by Koryak (20) suggest that the fall in maximal voluntary contraction force of the triceps surae after 7 days of simulated microgravity (“dry” water immersion) are mostly due to a reduction in motor drive.
Ferretti (16) has recently reported a 24% average reduction in the maximal power in 6 subjects during a standing high jump off both feet after 41 days of head-down tilt (−6°) bed rest, accompanied by a 13.4% mean decrease in the CSA of the extensor muscle groups. Thus, after 41 days of bed rest, the explosive power relative to the muscle mass amounted, on average, to 0.76/0.866 = 0.88, a value substantially larger than that of 0.74 observed inS1, who remained in space for a comparable period of time. The procedure utilized in this study to determine MEP is not directly comparable to standing high jumps off both feet, the latter, but not the former, permitting a substantial recovery of elastic energy (37). When it is considered that Ferretti’s bed rest study lasted 42 days with no exercise at all, compared with a spaceflight of 31 days with 2 h/day of aerobic exercise forS1, the large fall in MEP seems to be a specific characteristic of spaceflight that cannot be easily reproduced by bed rest.
The fall in MCP was substantially less than that of MEP, as indicated in Fig. 5, in which the MCP data lie above the identity line. In addition, when the MCP data are expressed per unit muscle mass, as was done above for MEP, the resulting values are 0.82/0.91 = 0.90 for S1 and ∼0.70/0.87 = 0.80 for S2,S3, andS4, i.e., substantially larger than those observed for MEP.
The different responses of MEP and MCP to microgravity presumably arise because, for MCP, the pedal frequency, and hence the speed, is imposed by the isokinetic cycloergometer, as opposed to MEP, where both force and velocity are set by muscle action. In addition, whereas in one case (MEP) the time from zero force (and speed) to peak force (and speed) was ∼200 ms (see Fig. 2), in the other (MCP) the time for full muscle activation was 500 ms (Fig. 3). The larger decline in MEP, compared with MCP, after spaceflight is consistent with the data reported by Thornton and Rummel (36) during torque-velocity tests performed on the extensor muscles of the legs and trunk of the astronauts participating in the Apollo project. Indeed, Thornton and Rummel showed a larger loss of force at the higher velocities of shortening. Any effects interfering with fast and coordinated motor unit recruitment are therefore likely to have a greater impact on MEP than on MCP.
To the authors’ knowledge, the data reported above are the first and only observations of the effects of microgravity on maximal muscular power. In contrast, the effects of microgravity on posture and muscle tone have been reported by numerous studies. These consistently show a generalized flexor prevalence (8-10), resulting from1) a greater inhibition of the extensors; 2) a greater facilitation of the flexors, arising from muscles and joints proprioceptors (14); and 3) the absence of the reflex activation of the extensor muscles, arising from the pressure of the pads of the feet on the floor as shown in simulated microgravity (1). This muscle tone resetting in the direction of a flexor bias is also shown by the “fetal” resting position in space, reported by Thornton et al. as early as 1977 (34) and persisting even after reentry on Earth (10). Finally, comparisons of pre- with postflight characteristics of gait and standing jump have shown postflight changes attributable to the effects of microgravity on locomotor coordination (4).
In summary, all these data indicate that the absence of gravity brings about a substantial rearrangement of muscle postural tone and of locomotor coordination. We propose that microgravity, favoring, as it does, smooth and delicately balanced muscle actions as opposed to forceful ones, brings about a rearrangement of the motor control system that is responsible, at least to a large extent, for the observed decline in the maximal muscular power during all-out, short-lasting muscle actions. We are not in the position of proposing at this stage any clear-cut hypothesis as to the mechanisms underlying these changes. However, recent data show that the fall in MEP after spaceflight is mirrored by a similar fall in electromyographic activity of the vastus lateralis, vastus medialis, and rectus femoris (2). In addition, the time course of the electromyographic recovery of the vastus medialis is much slower than that of the two other heads of the quadriceps femoris. Although these data were obtained in only one subject, they do support the hypothesis that microgravity interferes substantially with the normal motor unit recruitment patterns during very short all-out exercises.
The authors express their gratitude to the crews; their back-ups; the crew surgeons, Drs. Bernard Comet, Klaus Lohn, and Vladimir Nalishiti; Dr. Benny Elmann-Larsen, Dr. Eva König, and Gen. Sigmund Jähn of the European Space Agency; Paul Esser of Deutsche Forschungsanstalt für Luft und Raumfahrt; and Claudio Annoni and Ranieri Burelli of the Istituto Tecnico Industriale “A. Malignani” of Udine for their invaluable help.
Address for reprint requests: G. Antonutto, Dipartimento di Scienze e Tecnologie Biomediche dell’Università di Udine, via Gervasutta 48, I-33100 Udine, Italy (E-mail:).
This study has been financially supported by the Italian Space Agency (ASI) grants ASI-RS-100/140/172. P. E. di Prampero was the main investigator.
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.
- Copyright © 1999 the American Physiological Society