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Department of Exercise Science, The University of Georgia, Athens, Georgia 30602; and Departments of Physical Education and of Physiology and Radiology, Michigan State University, East Lansing, Michigan 48824
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Conley, Michael S., Jeanne M. Foley, Lori L. Ploutz-Snyder,
Ronald A. Meyer, and Gary A. Dudley. Effect of acute head-down tilt on skeletal muscle cross-sectional area and proton transverse relaxation time. J. Appl. Physiol.
81(4): 1572-1577, 1996.
This study investigated changes in
skeletal muscle cross-sectional area (CSA) evoked by fluid shifts that
accompany short-term 6° head-down tilt (HDT) or horizontal bed
rest, the time course of the resolution of these changes after
resumption of upright posture, and the effect of altered muscle CSA, in
the absence of increased contractile activity, on proton transverse
relaxation time (T2). Average
muscle CSA and T2 were determined
by standard spin-echo magnetic resonance imaging. Analyses were
performed on contiguous transaxial images of the neck and calf. After a
day of normal activity, 24 h of HDT increased neck muscle CSA 19 ± 4 (SE)% (P < 0.05) while
calf muscle CSA decreased 14 ± 3%
(P < 0.05). The horizontal posture
(12 h) induced about one-half of these responses: an 11 ± 2%
(P < 0.05) increase in neck muscle
CSA and an 8 ± 2% decrease (P < 0.05) in the calf. Within 2 h after resumption of upright posture, neck
and calf muscle CSA returned to within 0.5% (P > 0.05) of the values assessed
after a day of normal activity, with most of the change occurring
within the first 30 min. No further change in muscle CSA was observed
through 6 h of upright posture. Despite these large alterations in
muscle CSA, T2 was not altered by
more than 1.1 ± 0.6% (P > 0.05)
and did not relate to muscle size. These results suggest that postural
manipulations and subsequent fluid shifts modeling microgravity elicit
marked changes in muscle size. Because these responses were not
associated with alterations in muscle
T2, it does not appear that simple movement of water into muscle can explain the contrast shift observed after exercise.
simulated microgravity; magnetic resonance imaging; posture; skeletal muscle size
INTRODUCTION REDISTRIBUTION OF FLUID from the lower to upper body is
a generally accepted response to spaceflight. Similar responses are observed during the head-down-tilt (HDT) model of microgravity (14, 24,
26), suggesting that gravity-dependent alterations in hydrostatic
pressure are involved in the redistribution of fluid. The ensuing
changes in capillary hydrostatic pressure likely result in fluid
movement between the vasculature and interstitium. A possible
consequence of this fluid movement is an alteration in tissue volume.
Previous data suggest that regional fluid shifts alter limb volume (9,
14, 22, 36), and it has recently been shown that moving from the
upright to horizontal posture decreased lower limb muscle size assessed
by transaxial computed tomography (5). This response was larger in more
distal muscle (5), likely because of a greater change in capillary
hydrostatic pressure the more distally located the tissue. It seems
likely that neck and calf muscle would demonstrate even larger
increases and decreases, respectively, in size during HDT, compared
with horizontal bed rest, because this model of microgravity should evoke greater fluid shifts than horizontal posture. This could confound
determination of the atrophic response of skeletal muscle to unloading
independent of net protein loss, depending on the extent and time
course of these fluid shifts.
Magnetic resonance (MR) imaging is frequently used for noninvasive
anatomic visualization. More recently, MR imaging has been used to
examine the intensity and pattern of muscle use during physical
activity (1, 7, 10, 13, 17, 27-29, 39). Exercise has been shown to
increase proton transverse (spin-spin) relaxation time
(T2) in MR images of muscle
(11). These exercise-induced shifts in
T2 have been shown to be
correlated with integrated electromyographic activity (1)
and increase with exercise intensity (1, 10, 13, 17), and the
cross-sectional area (CSA) of muscle demonstrating such a shift has
been shown to relate to isometric torque during electromyostimulation
(2). Because proton-weighted MR images are based on signals from
hydrogen atoms, it is believed that the exercise-induced shift in
T2 is the result of water movement
into muscle (6, 11-13). If simple movement of water into muscle is
responsible for the exercised-induced contrast shift, regional fluid
shifts resulting from postural changes that increase muscle size should
be accompanied by increased T2.
The purpose of this investigation was to examine the extent and time
course of changes in neck and calf muscle CSA evoked by the fluid
shifts that accompany short-term HDT. A secondary interest was to
determine whether such changes in skeletal muscle CSA, in the absence
of increased contractile activity, alter transverse relaxation time of
skeletal muscle.
METHODS General protocol. Eleven healthy
college students served as subjects. Six were exposed to HDT and five
to horizontal (Hor) bed rest. In the evening after a day of normal
activities, MR images of the neck and calf in HDT were obtained. The
next morning, HDT began 24 h of 6° HDT at the MR imaging facility.
MR images of the neck and calf were collected in HDT after 24 h of HDT. HDT subsequently moved to an upright posture, and MR images were collected 30 min, 2 h, and 6 h later. Hor subjects reported to the MR
imaging facility in the evening after a day of normal activities. MR
images of the neck and calf were collected at this time, after 12 h of
horizontal bed rest, and at 30 min, 2 h, and 6 h after the subjects
moved to an upright posture. Subjects remained at the MR imaging
facility throughout bed rest and resumption of upright posture.
Subjects. Ten males and one female
volunteered to serve as subjects. After the purpose of the study and
its risks and benefits had been explained, each subject provided
informed written consent to participate. Subjects volunteered for the
HDT [21 ± 1 (SD) yr, 177 ± 9 cm, 77 ± 17 kg] or
Hor (21 ± 1 yr, 181 ± 6 cm, 82 ± 12 kg) group. They
consumed at least 2 liters of water during the day preceding the start
of data collection in an effort to ensure that they started bed rest
fully hydrated. For the 48 h preceding data collection and while at the
MR imaging facility, subjects did not exercise or consume any substance
known to affect fluid homeostasis. Food and beverages were provided
while subjects were at the MR imaging facility. Urine was collected and
measured during bed rest to determine whether a microgravity stimulus
was evoked. The protocol of the study was approved by the Institutional Research Review Board at Michigan State University and at The University of Georgia.
MR image collection and analysis.
Standard spin-echo MR images of the neck and calf were collected by
using a 1.5-T super conducting magnet (General Electric, Milwaukee, WI)
and analyzed essentially as described previously (1, 2, 7, 27-29). Briefly, contiguous transaxial MR images (repetition time = 2,000 ms; 30 echo times = 30 and 60 ms; field of view = 24 cm) 1-cm thick were obtained with a 0.5-cm gap between slices. This
image-acquisition protocol was used to provide high spatial resolution
in a reasonable time (4 min 40 s) and to allow direct comparison with
most studies of exercise-induced increases in
T2, which have utilized similar two-echo collections. Two echoes will likely not provide an exact fit
to the exponential signal decay, but the use of four in the conventional spin-echo technique would add little to the curve fit.
Echo-planar imaging, for example, allows for numerous echo times and
provides more complete curve fit, but this advanced imaging technique
does not allow for direct comparison to most previous studies, nor is
it widely avaliable. Ink marks on the calf and on the bridge of the
nose aligned with the crosshairs of the imager allowed for similar
positioning in the magnet bore for each scan. Digitized MR images were
transferred to a computer for calculation of muscle CSA and
T2 by using a modified version of
the public domain National Institutes of Health (NIH) Image program
(written by Wayne Rasband at the NIH and available from the Internet by
anonymous ftp from ftp://zippy.nimh.nih.gov or on floppy disk from NTIS, 5285 Port Royal Rd., Springfield, VA 22161, part number PB93-504868),
as done previously (2, 7, 27-29). After spatial calibration, a
region of interest was defined by tracing the outline of each muscle or
muscle group used in analyses. The CSA and average
T2 were determined for each region
of interest. To avoid inclusion of visible nonmuscle tissue, nine
regions for the neck (trapezius, splenius capitis, levator scapulae,
longissimus capitis and cervicis, scalenus medius and anterior,
sternocleidomastoid, semispinalis capitis, semispinalis cervicis and
multifidus, and longus capitis and colli muscles) and eight regions for
the calf (extensor digitorum longus, extensor hallucis longus, peroneus
brevis, flexor hallucis longus, soleus, gastrocnemius, tibialis
anterior, and tibialis posterior) were used. The CSA and
T2 of these regions were averaged
over four contiguous images of the neck and seven to nine images of the calf. For all bed-rest image collections, subjects were lifted on a
backboard and transported to the imager on a gurney set either 6°
head down or horizontal to minimize any effect of movement or change in
posture.
Statistics. Data were analyzed with a
three-way analysis of variance (treatment × muscle group × time) with repeated measures over time. If there were significant
three-way or two-way interactions, appropriate simple effects were
determined. Where results indicated that the assumption of spherecity
of the within-subject factor may not have been met ( RESULTS Urine excretion was higher (P < 0.05) in HDT than in Hor group [1,376 ± 119 vs. 689 ± 52 (SE) ml, respectively] for the first 12 h of bed rest, suggesting
that a simulated microgravity response was evoked by HDT. No change
(P > 0.05) in body weight was
observed for either group during bed rest (77 ± 7 to 77 ± 7 kg
for HDT vs. 82 ± 5 to 82 ± 5 kg for Hor). There was a treatment × muscle group × time interaction for muscle CSA
(P < 0.05) (Fig.
1). Subsequent analyses of simple effects
showed a muscle group × time interaction (P < 0.05) and treatment, muscle
group, and time effects (P < 0.05).
After a day of normal activity, 24 h of HDT increased neck muscle CSA
19 ± 4% (P < 0.05) and
concomitantly decreased calf muscle CSA 14 ± 3%
(P < 0.05). The horizontal position
induced about one-half of these responses: an 11 ± 2%
(P < 0.05) increase in neck muscle
CSA and an 8 ± 2% decrease in the calf. By 2 h after resumption of
upright posture, neck and calf muscle CSA for HDT and Hor had returned
to within 0.5% (P > 0.05) of the values assessed after a day of normal activity, with most of the change
occurring within the first 30 min. No further changes in muscle CSA
were observed through 6 h of upright posture in either group. Despite
these large changes in muscle CSA, no interactions or main effects were
observed for muscle T2
(P > 0.05; Fig.
2). Overall, muscle
T2 was not altered by more than
1.1 ± 0.6% as a result of postural changes in either group and did
not relate to muscle size.
DISCUSSION The most striking result of this study was the marked increase (19%)
and decrease (14%) in neck and calf muscle CSA, respectively, evoked
by 24 h of HDT after the subjects had been upright the previous day.
While the possible effect of posture on anthropometric measurements has
long been acknowledged (9, 36), most investigations have utilized girth
or fluid displacement measures of the lower limb. Nixon et al. (24)
reported a decrease in leg volume from 7.5 to 7.1, 6.9, 7.0, and 7.1 liters after 0.5, 2, 6, and 24 h, respectively, of HDT. Hargens et al.
(14) found a decrease in calf circumference from 36.9 to 36.7 cm when
the subjects were moved from upright to horizontal posture. Calf
circumference did not change after 0.5 h of 5° HDT but decreased to
35.7 cm by 4 h. No further change was observed after 8 h. These results
were closely paralleled by water displacement measures also made by Hargens et al. (14). Thornton et al. (35) recently observed a 4.5%
decrease in calf circumference after 2.5 h of 6° HDT. Taken together, these results show an ~5% decrease in lower limb girth during HDT, with most of the response occurring within the first few
hours. A 5% decrease in circumference (cir = 2 The effect of posture on skeletal muscle CSA has been examined by Berg
et al. (5) using computed tomography. In the evening after a day of
normal activities, 2 h of horizontal bed rest decreased thigh and calf
CSA 1.9 and 5.5%, respectively. Most of the change occurred within the
first 60 min of supine posture. The decrease for the calf is comparable
to that found in the present study (8%). Taken together, these results
demonstrate the potential confounding influence that changes from the
vertical to horizontal posture exert on muscle CSA and suggest that
posture should be standardized when evaluating muscle size. For
example, short-term resistance training in young adults for 8-10
wk may increase muscle size 10%. If estimates of calf muscle size were
made in the morning after a night's sleep pretraining and in the
evening after a day of regular activity posttraining, this could lead
to an overestimation of hypertrophy because fluid accumulation during
the day would increase calf muscle size by as much as 8%. Also, the
results of the present study suggest that the effect of fluid shifts
due to postural changes on muscle size could also confound
determination of atrophy after unloading. The decreases in lower limb
muscle size of 5-15% after short-term unloading that have been
reported (see Ref. 28) may reflect net protein loss. However, the
finding in this study that 24 h of HDT decreased calf muscle size to
the same extent suggests that future studies of real or simulated microgravity should fully appreciate the potentially confounding effect
of fluids shifts on muscle morphology.
The reciprocal nature of the changes in upper vs. lower body skeletal
muscle size found in the present study suggests that gravity-dependent
alterations in hydrostatic pressure and subsequent exchange of fluid
between the vasculature and tissue alter the size ot the latter. It has
been shown that alterations in posture result in greater relative
changes in limb circumference (35) and muscle CSA (5) in more distal
body regions. This is likely due to a greater change in the height of
the hydrostatic column of blood the more distal the tissue, thereby
resulting in greater regional capillary filtration. Unlike exercise,
the postural manipulations used in the present study are not associated
with production and accumulation of osmotically active substances.
Therefore, net capillary filtration is believed to be initially
regulated by vascular and extravascular hydrostatic forces, with
osmotic and oncotic forces involved subsequent to hemoconcentration
and/or extravascular dilution. Hargens et al. (14) reported
that 8 h of 5° HDT decreased soleus water content by 3.4% and
interstitial fluid pressure from 4.6 to The secondary interest of the present study was to determine whether
marked alterations in muscle size, presumably due to accumulation or
loss of extracellular water (21), alter muscle T2. This arose from the wealth of
controversial literature purporting the mechanisms responsible for
contrast shift in MR images. The multiexponential nature of
T2 in skeletal muscle suggests
that multiple water fractions, e.g., extracellular water
(T2 196 ms), intracellular free
water (T2 40-45 ms), and
intracellular bound water (T2
<16 ms), contribute to the single apparent first-order rate constant
typically reported (15, 19). It has been suggested that
exercise-induced contrast shift is mainly the result of extracellular fluid accumulation in muscle (3, 6, 11-13). This seems to be
supported by the finding that muscles demonstrating an increase in
T2 after exercise also increase in
size (attributed to fluid influx), whereas those not demonstrating an
increase in T2 do not (29).
Dynamic exercise has been shown to elevate extracellular and
intracellular water in skeletal muscle depending on exercise intensity.
At low workloads (50-70% maximal oxygen uptake), extracellular water primarily increases, whereas at higher workloads (120% maximal oxygen uptake), mainly intracellular water accumulates (32, 33). This
suggests that the transition from rest to moderate exercise should
profoundly affect muscle T2
because of the long relaxation attributed to extracellular water (196 ms). However, moderate exercise evokes only small increases (2-4
ms) in T2 (1, 10) and signal
intensity (17). Moreover, postural alterations result in changes in
interstitial and extracellular water with almost no change in
intracellular water (21). Nevertheless, the marked alterations
(14-19%) in muscle size observed with HDT in the present study
were not accompanied by changes in
T2. Taken together, these results
suggest that simple movement of water into the extracellular space of
muscle cannot explain the contrast shift evoked by exercise.
What then might explain exercise-induced contrast shift? Increased
muscle perfusion has been proposed (8). However, Archer et al. (4)
reported that exercise with vascular occlusion increased muscle
T2 and that postexercise
reperfusion was associated with a decrease of
T2. These results also raise issue
with the suggestion of Yue et al. (39) that the exercise-induced
increase in T2 is related to the
level of oxygenation of blood. Yue et al. suggest that increased blood
flow immediately after exercise reduces the relative deoxyhemoglobin
content of blood, thereby increasing T2. The finding that patients with
myophosphorylase deficiency do not show contrast shift postexercise
(12, 16) has been used to suggest that increases in
T2 are related to glycogenolysis. Specifically, the absence of lactate-mediated water translocation into
muscle accounted for the lack of
T2 increase. However, Jehenson et
al. (16) reported no increase in
T2 after exercise in patients with
certain mitochondrial myopathies, who exhibit elevated lactate at rest
and postexercise. Because these patients are believed to have enhanced
intracellular buffering, Jehenson et al. suggested that the absence of
elevated H+ concentration
([H+]) accounted for
the lack of T2 increase. A role
for [H+] is supported
by the finding that muscle T2 is
correlated negatively with pH and positively with the inorganic
phosphate-to-phosphocreatine ratio postexercise (37). However, Cheng et
al. (6) observed increases in muscle
T2 that preceded elevation of
[H+] and more rapid
recovery of [H+] than
T2 postexercise. Thus it appears
that T2 is related to muscle
metabolism, but a causal effect of cytosolic
[H+] has not been
demonstrated. In this regard, many of the metabolic events associated
with exercise may alter the structure of proteins. These could affect
the intracellular water order, resulting in an increase in the free
water fraction and thereby T2
(18). For example, Oplatka (25) has proposed that changes in the
hydration shell of actomyosin are required for cross-bridge cycling and force generation. Other events associated with contractile activity such as elevated temperature (20, 23), decreased pH (see Ref. 38), and
increased cytosolic calcium (30) with subsequent confromational changes
of thin filament proteins may also alter macromolecular hydration
shells.
We have previously reported that the semispinalis and multifidus
muscles have a "high" T2 in
the absence of voluntary exercise compared with other neck muscles and
suggested that this reflects their role as antigravity muscles of the
head and neck during upright posture (7). If this were the case, bed
rest would be expected to reduce their postural role and, consequently,
their contractile activity and T2.
Even though there was no overall effect of bed rest on muscle
T2 in the present study,
examination of the semispinalis cervicis and multifidus muscles alone
showed a decrease with bed rest (P < 0.05) in HDT (32.1 ± 1.1 to 28.4 ± 0.8 ms) and Hor (31.9 ± 1.2 to 28.6 ± 1.1 ms). Moreover, these values returned to those
observed after a day of normal activity (P > 0.05) within 30 min after
resumption of upright posture. These results add further support to the
suggestion that the semispinalis cervicis and multifidus muscles serve
an antigravity role during upright posture and, consequently, may be
predisposed to atrophy during microgravity or bed rest. They also show
that muscle T2 can decrease while
muscle size increases due to accumulation of extracellular fluid evoked
by bed rest.
In summary, these results show that acute exposure to HDT or moving
from upright to horizontal posture elicit marked changes in muscle size
that are likely caused by the accumulation of fluid and not net protein
loss. These changes appear to be resolved within 2 h after the
resumption of upright position. These results demonstrate that posture
should be controlled when assessing muscle size. The lack of
T2 change despite the marked
alteration in muscle size, likely reflecting accumulation or loss of
extracellular water, suggests that simple movement of fluid into muscle
cannot explain the increase in T2
postexercise.
< 0.7), a
Huynh-Feldt adjustment was performed. Means contrast analyses, with a
Bonferroni adjustment for multiple comparisons, were used to determine
specific differences over time. The level of significance was set at
P < 0.05.
Fig. 1.
Muscle cross-sectional area (CSA) for the head-down tilt (HDT) and
horizontal bed rest (Hor) groups. 
, HDT calf; 
, HDT neck; 
,
Hor calf; 
, Hor neck. Values are means ± SE. UPall, after a day
of regular activity; ENDbr, end of bed rest. UP.5h, UP2h, UP6h,
resumption of upright posture with data collected 0.5, 2, and 6 h
thereafter, respectively. * Treatment difference
(P < 0.05);
+ different from UPall in
Hor (P < 0.05);
# different from UPall in
HDT (P < 0.05).
[View Larger Version of this Image (17K GIF file)]
Fig. 2.
Muscle proton transverse relaxation time
(T2) for HDT and Hor groups.
, HDT calf; , HDT neck; , Hor calf; , Hor neck. Values are
mean ± SE. No significant effects
(P > 0.05) were observed.
[View Larger Version of this Image (12K GIF file)]
r) reflects an ~10% decrease
in area (area = r2). These
changes can account for about two-thirds of the 14% decrease in calf
muscle CSA found in the present study. This apparent discrepancy may
reflect the tendency for an increase in lower limb cutaneous blood flow
during short-term HDT (34) to mask fluid loss from muscle and the
inclusion of tissues such as bone that are likely insensitive to fluid
shifts. It also suggests that alterations in skeletal muscle size
evoked by fluid shifts that accompany postural changes may not be
reflected by measures of limb volume. Finally, the magnitude of the
change in muscle size found in the present study suggests that this
tissue is a major compartmental reservoir for fluid redistribution
associated with postural manipulations.
2.8 mmHg. Conversely,
Parazynski et al. (26) reported an increase in intramuscular
interstitial fluid pressure in the sternocleidomastoid after 4 and 8 h
of 6° HDT. These results support the concept that changes in muscle size resulting from HDT are due to regional shifts in transcapillary pressure gradients. It is interesting that neck muscle demonstrated a
greater relative change in CSA (+19%) than calf muscle (14%) in the present study after 24 h of HDT. It has been proposed (3, 26,
31) that intracapillary pressure of the neck is lower and less affected
by postural changes than that of the feet because the neck is closer to
the heart. Thus the microvasculature of the neck may be less adapted to
counter the increases in pressure associated with HDT.
ACKNOWLEDGEMENTS
The authors thank the subjects for their participation and Roop Jayaraman for technical assistance throughout data collection.
FOOTNOTES
Address for reprint requests: G. A. Dudley, Dept. of Exercise Science, Ramsey Center, The Univ. of Georgia, Athens, GA 30602 (E-mail: gdudley{at}uga.cc.uga.edu).
Received 22 March 1996; accepted in final form 6 June 1996.
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