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BASIC SCIENCES: Original Investigations

Effect of short-duration spaceflight on thigh and leg muscle volume

AKIMA, HIROSHI; KAWAKAMI, YASUO; KUBO, KEITARO; SEKIGUCHI, CHIHARU; OHSHIMA, HIROSHI; MIYAMOTO, AKIRA; FUKUNAGA, TETSUO

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Medicine & Science in Sports & Exercise: October 2000 - Volume 32 - Issue 10 - p 1743-1747
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Abstract

Due to limited access and the extreme cost of spaceflight research, scientists have utilized ground-based models to simulate exposure of the neuromuscular system to microgravity. It is well known that atrophy is induced by bed rest (1,4,6,8,11,13,16,17) or unilateral lower limb suspension (ULLS) (3,7,12) in human skeletal muscle. There are no data that support or refute the validity of these models. This probably arises from the fact that few studies have examined the influence of spaceflight upon human skeletal muscle, and no data concerning recovery of muscle size upon return to 1 G, to our knowledge, have been reported. As far as we know, there is one report concerning muscle volume changes after spaceflight. LeBlanc et al. (14) have shown a 6–8% of loss in thigh or leg muscle volume after 8 d of spaceflight. Edgerton et al. (9) recently reported 16–36% smaller fiber cross-sectional area after 11 d of spaceflight, indicating that atrophy probably accounts for the decline in muscle size. We have recently reported the effect of 20 d of bed rest on lower limb muscles in humans (1). Accordingly, the purposes of the present study were to investigate volume changes in thigh and leg muscles after spaceflight and to compare these with our bed rest data.

MATERIALS AND METHODS

Three subjects, A, B, and C, flew in space for approximately 9, 15, and 16 d. Informed written consent was obtained from each astronaut before data collection. Table 1 shows physical characteristics and flight duration for the subjects.

Table 1
Table 1:
Physical characteristics and flight duration of the subjects.

Magnetic resonance images (MRI) of the right thigh and calf were performed approximately 60 d before launch. After landing, images of each subject were taken four different times. These measurements were not at the same intervals because of schedule conflicts (Fig. 1). MR images were taken with a 1.5T imager (Signa Horizon, General Electric Medical Systems, Waukesha, WI) at the same hospital for all three subjects. Subjects were imaged in a prone position with the knee and ankle joints kept at 180° and ∼120°, respectively, with 180° being full extension. Coronal plane images were taken to identify the origin of the sartorius, the spina illiaca anterior superior, the most proximal muscle studied. Subsequently, spin-echo, axial-plane images (TR 1500 ms, TE 22 ms, matrix 256 × 256, field of view 400 mm, slice thickness 10 mm, interslice gap 0 mm, 1 NEX) were taken from the origin of m. sartorius to the ankle joint. The muscle groups investigated were the knee extensors (quadriceps femoris), knee flexors (hamstrings, sartorius, and gracilis), and plantar flexors (triceps surae). Each muscle group was outlined using the original film onto tracing paper, which was subsequently scanned to create a digital image. The digital images were transferred to a Macintosh computer (Power Macintosh 8600/200, Apple Computer, Cupertino, CA) for calculation of the cross-sectional area (CSA) using a public domain National Institute of Health (NIH) Image software package ver. 1.60/ppc (written by Wayne Rasband at the NIH and available from the Internet by anonymous ftp from zippy.nimh.nih.gov). Muscle volume was determined by summing the CSA of each image times the thickness (10 mm) of each section. For subject B, it was difficult to separate the knee flexor and adductor muscle groups in the thigh images, and the plantar and dorsi flexor muscle groups in the calf images. Therefore, this knee flexor data includes the adductor muscle group while the plantar and dorsi flexors were also combined.

Figure 1
Figure 1:
The schedule of spaceflight and MRI measurement for three subjects. Thearrows represent MRI measurement.

All data are presented as means ± standard deviation (SD).

RESULTS

The greatest decrease in volume of the knee extensor muscle group was found 4 d post flight for subjects A (−15.4%) and C (−11.6%), and 1 d after flight for subject B (−5.6%) (Fig. 2). The greatest muscle volume changes in the knee flexor group were found on these same days for subjects A (−14.1%), B (−11.6%), and C (−8.6%) (Fig. 2). Volume of the knee extensor and flexor muscle groups of subjects B and C were almost recovered at the third postflight measurement (21-d and 30-d after landing, respectively, (Fig. 2). Subject A, on the other hand, took between 30 and 120 d to recover.

Figure 2
Figure 2:
Relative muscle volume changes in the knee extensors and flexors and plantar flexors in three astronauts. Thebold line represents spaceflight.

Similar trends were noted for loss of volume of the plantar flexor muscle group in regards to relative magnitude and time (Fig. 2). Recovery seemed to differ from that of the thigh muscles; however, in that, subjects A and C took from between 30 and 120 d to recover, if at all.

Figure 3A. shows CSA of the knee extensor, knee flexor, and plantar flexor muscle groups in serial images of the subjects. At preflight and 4-d after landing, the greatest losses were noted. Decreases in CSA of the knee extensor and plantar flexor muscle groups were observed throughout the thigh and leg, respectively. In the knee flexors, however, decreases were most evident in the distal aspect of the thigh. Comparable results were found for subjects B and C (data not shown).

Figure 3
Figure 3:
Serial cross-sectional area (CSA) of the knee extensors and flexors and plantar flexors before and after spaceflight in subject

Figure 4 shows the greatest relative decline in muscle volume divided by flight duration for each subject and for our bed rest study (1). For all three subjects and for all three muscles, the % loss per day was greater for spaceflight than for bed rest. Normalized muscle volume loss (%·d1) for spaceflight appeared to be similar to or greater than the mean ± 1SD of the decline evoked by bed rest. On average, exposure to microgravity caused almost twice the loss.

Figure 4
Figure 4:
Normalized muscle volume changes by spaceflight or bed rest duration in the knee extensors and flexors and plantar flexors.

DISCUSSION

It is generally thought that atrophy of human skeletal muscles is induced by microgravity. However, only few studies have ever reported muscle morphological changes due to spaceflight in humans (9,14). LeBlanc et al. (14) reported a 6.0, 8.0, and 6.3% decrease in quadriceps femoris, hamstring, and calf muscle CSA, respectively, after 8 d of spaceflight. These responses correspond to 0.75, 1.00, and 0.79%·d1 loss of muscle size. In the present study, relative loss of volume in the knee extensor, knee flexor, and plantar flexor muscle groups was 15.4, 14.4, 12.2% for subject A (15 d), 5.6, 11.6, 8.4% for subject B (9 d), and 11.6, 8.6, 15.9% for subject C (16 d), respectively. Corresponding average values for muscle volume loss per day of flight were 0.80, 0.71, and 0.94%·d1, respectively. These are similar to those of LeBlanc and collaborators study (14).

The three subjects in this study showed variable relative decreases in muscle volume, even when values were expressed relative to flight duration. We also observed variability of muscle atrophy among individuals as the result of bed rest in our previous study (1). Edgerton et al. (9) have demonstrated that muscle fiber atrophy due to spaceflight also varied widely among individuals. They suggested that the extent of atrophy was inversely related to preflight fiber size. Subjects with the largest muscle fibers before flight (presumably the most active) showed the greatest atrophy, whereas the subject with the smallest fibers before the flight showed no atrophy. Variable atrophic responses may also be due to differences in physical activity during flight. Subject A was quite active before launch: resistance training, swimming, and/or running for about 40 min·d1 6 d a week. We speculate that subject A continued physical training frequently during flight, thereby attenuating the atrophic response to microgravity exposure. We have unpublished data which shows that isometric leg press resistance training (3-s contraction, 20 repetition·d1, every day) during 20 d of bed rest prevents muscle volume loss in the knee extensors. In the absence of physical conditioning, we speculated that the variability of muscle atrophy among individuals may be due to differences in muscle loading during their daily life; however, we have no data to support this speculation.

It is not clear whether there is a difference in the magnitude of muscle atrophy between spaceflight and simulated microgravity. Greater losses, i.e., muscle volume decrease per day (Fig. 4), appeared to be observed in all subjects in this study than in our previous bed rest data (1) in all muscle groups. In our bed rest study (1), muscle volume decreases in the thigh and calf muscles were ∼10% for 20 d or about 0.5%·d1. Convertino et al. (6) reported that CSA of thigh and calf muscle decreased 8.1% and 4.8% for 30-d bed rest. Ferrando et al. (10) reported a comparable change for bed rest (muscle volume of thigh and calf; −3.0 and −2.0% for 7 d), as have Berg et al. (4) and Hather et al. (12) for 6 wk of bed rest or ULLS. When taken together, these findings appear to demonstrate that greater muscle loss occurs as a result of spaceflight compared with simulated microgravity. This may be due to greater loading of skeletal muscle during simulated microgravity. Although bed rest has been considered to be one of the disuse models, we speculate that muscle was loaded even during bed rest because of the effect of gravity on the lower limbs. For example, when we move our legs or arms during bed rest or use the bed pan, skeletal muscles muscle act against some portion of body weight. In space, in contrast, movement occurs quite often, but there is no loading due to gravity.

Muscle atrophy occurred throughout the thigh and leg extensor muscles in subject A (Fig. 3). In contrast, atrophy was observed in the distal region of the knee flexor muscle group in subject A. Similar atrophic patterns were observed in subjects B and C. It has been demonstrated that atrophy occurs to the greatest extent around the region of peak CSA (1). It may be due to the differences of magnitude of muscle atrophy. Serial images from origin to insertion have also been used to examine changes in muscle shape due to training (2). Although the mechanism(s) is not understood, these results indicate that changes in muscle size are region specific (1,2,15). Thus, alterations in muscle size should be examined using multiple images, not a single slice.

Recovery of volume varied among subjects for a given muscle group, and even among muscle groups within a subject. The knee extensor and plantar flexor muscle groups of subjects B and C recovered to baseline within ∼30 d after spaceflight. We demonstrated a comparable response after 20 d of bed rest (1). However, all muscle groups for subject A and the knee flexor muscle groups for subjects B and C showed restoration of volume between 30 and 120 d after spaceflight, if they recovered. Although we have no explanation for the apparently prolonged recovery, this could lead to general weakness (subject A) and muscular imbalance about a given joint. Clearly, post flight assessments of muscle function and mass appear warranted based on these results. Moreover, recovery rate seems to greatly differ from that of subject B or C. As the muscle volume of the knee extensor and knee flexor muscle groups of subject A was the greatest, this could be the main factor in slow recovery of the knee extensor and knee flexor muscle groups in subject A. The plantar flexor muscle group did not recover for subject C even after 120 d of spaceflight. The reasons of this slow recovery were not clear. The recovery pattern in subject A was different to the other subject, i.e., the greatest muscle atrophy was observed at a few days later after launch. The mechanisms of this phenomenon were also unclear. Fluid shift due to acute posture change in human skeletal muscles has a great influence on muscle CSA as has been reported by Conley et al. (5); however, it is not the case in this study because the fluid shift effect on muscle volume seems to take up to 2 h (5).

In conclusion, we investigated that volume changes of the knee extensor, flexor, and plantar flexor muscle groups of three crew members before and after spaceflight of about 9, 15, and 16 d. Volume changes varied widely among individuals and muscle groups. Muscle volume changes per day appeared greater than those observed due to 20 d of bed rest. These results suggested that greater muscle losses might occur during short-duration spaceflight than bed rest in lower limb muscles.

We thank Dr. Gary A. Dudley, The University of Georgia, for helpful suggestions of this manuscript.

When we were submitting this manuscript, Widrick et al. (J. Physiol. 516:915–930, 1999) reported that “Effect of a spaceflight on contractile properties of human soleus muscle fibres”.

REFERENCES

1. Akima, H., S. Kuno, Y. Suzuki, A. Gunji, and T. Fukunaga. Effects of 20 days of bed rest on physiological cross-sectional area of human thigh and leg muscles evaluated by magnetic resonance imaging. J. Gravitat. Physiol. 4: 15–22, 1997.
2. Akima, H., S. Kuno, M. Inaki, H. Shimojo, and S. Katsuta. Effects of sprint cycle training on architectural characteristics, torque-velocity relationships, and power output in human skeletal muscles. Adv. Exerc. Sports Physiol. 3: 9–15, 1997.
3. Berg, H. E., G. A. Dudley, T. Häggmark, H. Ohlsèn, and P. A. Tesch. Effects of lower limb unloading on skeletal muscle mass and function in humans. J. Appl. Physiol. 70: 1882–1885, 1991.
4. Berg, H. E., L. Larsson, and P. A. Tesch. Lower limb muscle function after 6 wk of bed rest. J. Appl. Physiol. 82: 182–188, 1997.
5. Conley, M., J. M. Foley, L. L. Ploutz-Snyder, R. A. Meyer, and G. A. Dudley. Effect of acute head-down tilt on skeletal muscle cross-sectional area and proton transverse relaxation time. J. Appl. Physiol. 81: 1572–1577, 1996.
6. Convertino, V. A., D. F. Doerr, K. L. Mathes, S. L. Stein, and P. Buchanan. Changes in volume muscle compartment, and compliance of the lower extremities in man following 30 days of exposure to simulated microgravity. Aviat. Space Environ. Med. 60: 653–658, 1989.
7. Dudley, G. A., M. R. Duvoisin, G. R. Adams, R. A. Meyer, A. H. Belew, and P. Buchanan. Adaptations to unilateral lower limb suspension in humans. Aviat. Space Environ. Med. 63: 678–683, 1992.
8. Duvoisin, M. R., V. A. Convertino, P. Buchanan, P. D. Gollnick, and G. A. Dudley. Characteristics and preliminary observations of the influence of electromyostimulation on the size and function of human skeletal muscle during 30 days of simulated microgravity. Aviat. Space Environ. Med. 60: 671–678, 1989.
9. Edgerton, V. R., M.-Y. Zhou, Y. Ohira, et al. Human fiber size and enzymatic properties after 5 and 11 days of spaceflight. J. Appl. Physiol. 78: 1733–1739, 1995.
10. Ferrando, A. A., C. A. Stuart, D. G. Brunder, and G. R. Hillman. Magnetic resonance imaging quantitation of changes in muscle volume during 7 days of strict bed rest. Aviat. Space Environ. Med. 66: 976–981, 1995.
11. Ferretti, G., G. Antonutto, C. Denis, et al. The interplay of central and peripheral factors in limiting maximal O2 consumption in man after prolonged bed rest. J. Physiol. 501: 677–686, 1997.
12. Hather, B. M., G. R. Adams, P. A. Tesch, and G. A. Dudley. Skeletal muscle responses to lower limb suspension in humans. J. Appl. Physiol. 72: 1493–1498, 1992.
13. LeBlanc, A., E. Schonfeld, H. J. Evans, C. Pientok, R. Rowe, and E. Spector. Regional changes in muscle mass following 17 weeks of bed rest. J. Appl. Physiol. 73: 2172–2178, 1992.
14. LeBlanc, A., R. Rowe, Y. Schneider, H. Evans, and T. Hedrick. Regional muscles loss after short duration spaceflight. Aviat. Space Environ. Med. 66: 1151–1154, 1995.
15. Roman, W.J., J. Fleckenstein, J. Stray-Gunderson, S. E. Alway, R. Peshock, and W. J. Gonyea. Adaptations in the elbow flexors of elderly males after heavy-resistance training. J. Appl. Physiol. 74: 750–754.
16. Suzuki, Y., T. Murakami, Y. Haruna, et al. Effects of 10 and 20 days bed rest on leg muscle mass and strength in young subjects. Acta Physiol. Scand. 150 (Suppl. 616): 5–18, 1994.
17. Thornton W. E., and J. A. Rummel. Muscular deconditioning and its prevention in spaceflight. In:Biomedical Results from Skylab. R. S. Johnston and L. F. Dietlein (Eds.). Washington, DC: NASA. 1977: 191–197; NASA SP-377.
Keywords:

MAGNETIC RESONANCE IMAGING; SKELETAL MUSCLE; HUMAN; DISUSE

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