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Department of Biology, Marquette University, Milwaukee, Wisconsin 53201-1881
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Bangart, J. J., J. J. Widrick, and R. H. Fitts. Effect
of intermittent weight bearing on soleus fiber force-velocity-power and
force-pCa relationships. J. Appl.
Physiol. 82(6): 1905-1910, 1997.
Rat
permeabilized type I soleus fibers displayed a 33% reduction in peak
power output and a 36% increase in the free
Ca2+ concentration required for
one-half maximal activation after 14 days of hindlimb non-weight
bearing (NWB). We examined the effectiveness of intermittent weight
bearing (IWB; consisting of four 10-min periods of weight bearing/day)
as a countermeasure to these functional changes. At peak power output,
type I fibers from NWB animals produced 54% less force and shortened
at a 56% greater velocity than did type I fibers from control
weight-bearing animals while type I fibers from the IWB rats produced
26% more absolute force than did fibers from the NWB group and
shortened at a velocity that was only 80% of the NWB group mean. As a
result, no difference was observed in the average peak power of fibers from the IWB and NWB animals. Hill plot analysis of force-pCa relationships indicated that fibers from the IWB group required similar
levels of free Ca2+ to reach
half-maximal activation in comparison to fibers from the weight-bearing
group. However, at forces <50% of peak force, the force-pCa curve
for fibers from the IWB animals clearly fell between the relationships
observed for the other two groups. In summary, IWB treatments
1) attenuated the NWB-induced
reduction in fiber Ca2+
sensitivity but 2) failed to prevent
the decline in peak power that occurs during NWB because of opposing
effects on fiber force (an increase vs. NWB) and shortening velocity (a
decrease vs. NWB).
isotonic contractile properties; hindlimb suspension; muscle
atrophy; countermeasures
INTRODUCTION THE REMOVAL of normal weight-bearing activity leads to
rapid changes in the function of single fibers obtained from rat
hindlimb extensor muscles. Soleus fibers expressing the type I myosin
heavy chain (MHC) isoform are particularly susceptible to prolonged non-weight bearing. When activated with saturating levels of free Ca2+, chemically permeabilized
type I soleus fibers from hindlimb-suspended rats display a substantial
increase in their maximal unloaded shortening velocity (8, 17, 23, 27).
At relative loads less than ~50% of peak isometric force, these
fibers shorten at considerably greater velocities than do fibers
obtained from weight-bearing animals (16). However, type I soleus
fibers from non-weight-bearing animals produce considerably less
absolute force than do fibers from weight-bearing controls (8, 16, 17,
23, 27), and, as a result, their peak power is reduced by up to 50%
(16).
Attention is now being directed to the development of procedures to
attenuate or prevent non-weight-bearing-induced alterations in
mammalian lower limb extensor muscle function. It is thought that these
countermeasures will have important applications in the manned space
program, where a reduction in voluntary ankle extensor muscle torque
during isokinetic movements has been documented after spaceflight (13),
and in ground-based clinical settings, where similar functional changes
have been observed in human knee extensor performance after prolonged
bed rest (6).
One of the simplest countermeasures used to date has been to provide
non-weight-bearing animals with brief, intermittent periods of standing
weight support (5, 22, 26, 27). Our laboratory (27) previously reported
that four 10-min intermittent weight-bearing sessions per day during 14 days of hindlimb suspension attenuated changes in the peak isometric
force and maximal unloaded shortening velocity (determined from slack
test measurements) of single type I soleus fibers.
However, isometric and/or unloaded contractions are not the
predominant forms of muscle action during animal locomotion. Instead,
muscle fibers shorten while under tension to produce the mechanical
work and power required for movement. In the present study, we examined
the effect of intermittent weight-bearing treatments on the isotonic
contractile properties of type I soleus fibers.
The dependence of force development on
Ca2+ is altered by prolonged
non-weight bearing. Type I fibers from non-weight-bearing animals
require a significantly greater free
Ca2+ concentration than do fibers
obtained from weight-bearing controls to attain 50% of their peak
isometric force (8, 18). Therefore, an additional objective of this
study was to determine whether intermittent weight bearing attenuated
this reduction in fiber Ca2+
sensitivity.
METHODS This study was approved by the Animal Care Committee at Marquette
University. Adult male Sprague-Dawley rats were divided into three
groups: normal caged weight bearing, 14 days of non-weight bearing, and
14 days of intermittent weight bearing. Hindlimb weight-bearing
activity of both the non-weight-bearing and the intermittent
weight-bearing animals was eliminated by a tail-suspension procedure
(27). Four times each day (at 0, 4, 8, and 11.75 h of the light cycle),
the intermittent weight-bearing animals were removed from hindlimb
suspension and placed in an upright standing position on a horizontal
surface. To prevent extensive ambulatory activity, a small
wire enclosure was placed over each animal during the intermittent
weight-bearing period. This enclosure was large enough to allow the
animal to turn about but too small to allow walking activity. After 10 min of weight bearing, the intermittent weight-bearing animals were
resuspended.
At the conclusion of the experimental treatments, soleus muscle bundles
were prepared as previously described (27). These bundles were stored
for up to 28 days at The composition of the relaxing and
Ca2+-activating solutions used for
the single fiber functional experiments was determined by using the
computer program of Fabiato and Fabiato (7) and the apparent stability
constants (corrected for temperature, pH, and ionic strength) reported
by Godt and Lindley (10). Each solution contained (in mM): 7 EGTA, 20 imidazole, 10 caffeine, 14.5 creatine phosphate, 1 free
Mg2+, and 4 free MgATP. The
relaxing solution contained a free
Ca2+ concentration of pCa 9.0 (where pCa is On the day of an experiment, a muscle bundle was transferred into cold
relaxing solution, and a single soleus fiber segment was isolated,
transferred into an experimental chamber filled with relaxing solution,
and mounted between an isometric force transducer (model 400, Cambridge
Technology, Watertown MA) and a direct-current position motor (model
300B, Cambridge Technology) by using small monofilament posts and 10.0 suture. Sarcomere length was adjusted to 2.5 µm by using an eyepiece
micrometer (×800). The length of the fiber was measured and
recorded. A photograph was taken of the fiber while it was briefly
suspended in air. Fiber width was determined at three points along the
length of the photo. The mean of these measurements was taken as fiber
diameter and used to calculate fiber cross-sectional area under the
assumption that the fiber forms a circular cross section when suspended
in air (19). The fiber was briefly bathed in relaxing solution containing 0.5% (wt/vol) Brij 58 (polyoxyethylene 20 cetyl
ether, Sigma Chemical, St. Louis, MO) to inhibit any sarcoplasmic
reticulum Ca2+ uptake activity.
Detailed descriptions of the mounting procedure and experimental
apparatus have been presented in previous papers (8, 16, 27).
Contractions were induced by rapidly transferring the mounted fiber
into an adjacent chamber filled with a
Ca2+-activating solution. Outputs
from the force transducer and position motor were directed to a digital
storage oscilloscope, amplified, and then interfaced to a personal
computer via a Lab Master input-output board (Scientific Solutions,
Solon, OH). Activating and relaxing solutions were
maintained at 15°C during all experiments.
All fibers were subjected to a series of isotonic contractions as
follows. The fiber was activated in pCa 4.5, and after peak isometric
force was attained, the position motor, operating via a servomechanism
similar to that described by Julian and Moss (15), stepped the fiber to
three submaximal isotonic loads. Each isotonic contraction lasted
between 100 and 150 ms. At the conclusion of the final isotonic load,
the fiber was slackened to a length Force-pCa relationships were determined by recording peak isometric
force during maximal (pCa 4.5) and submaximal (pCa 6.8-4.7) Ca2+ activation. Periodic
activations were conducted at pCa 4.5 to monitor preparation viability.
All submaximal forces (Pr) were expressed relative to the peak force obtained at pCa 4.5; i.e., Pr is ratio of peak force in given pCa to peak force in pCa
4.5. Force-pCa data were fit to Hill plots {where log
[Pr/(1 After the contractile measurements, the fiber was solubilized in 10 µl of 1% sodium dodecyl sulfate sample buffer (for composition, see
Ref. 27) and stored at Results are presented as means ± SE. A one-way analysis of variance
was used to determine significant differences between the three
experimental groups. When a significant
F-ratio was obtained, the
Student-Newman-Keuls post hoc procedure was used to determine
differences between specific means. Statistical significance was
accepted at P < 0.05.
RESULTS
20°C in skinning solution containing
(in mM) 125 K propionate, 20 imidazole (pH 7.0), 2 ethylene
glycol-bis(
-aminoethyl
ether)-N,N,N
,N-tetraacetic acid (EGTA), 4 ATP, and 1 MgCl2
and 50% glycerol vol/vol.
log Ca2+
concentration) and the activating solution a free
Ca2+ concentration of pCa 4.5. Sufficient KOH and KCl were present in both solutions to achieve a pH
of 7.0 and a total ionic strength of 180 mmol/l. Submaximal activating
solutions, ranging from pCa 7.0 to 4.7, were made by mixing appropriate
volumes of relaxing and maximal activating solutions to attain the
required free Ca2+ concentration.
20% of fiber length and was
transferred back into relaxing solution where it was reextended to its
original fiber length. The entire procedure was repeated so that each
fiber was subjected to 15-18 different isotonic loads. Custom
software determined the peak isometric force and the average force and
average velocity over the final half of each isotonic step. The force
baseline was defined as the resting force recorded while the fiber was in relaxing solution immediately before activation. Force-velocity data
were fit with the hyperbolic Hill equation (14) by an iterative curve-
fitting algorithm (Marquardt algorithm). For each individual fiber, the
force-velocity parameters
Vmax
[y-intercept of the relationship
in fiber lengths/s (FL/s)],
a/Po
(where a is a constant with dimensions
of force and Po is peak isometric
force), and peak isometric force were used to calculate peak absolute
power (µN · FL · s
1)
and peak normalized power
(kN · m2 · FL · s1).
Force-velocity parameters were used to construct force-velocity and
force-power relationships for each fiber (28). Velocity (and power)
values corresponding to 101 separate force bins (0-100% of peak
isometric force) for each individual relationship were summed across
fibers to obtain a single composite relationship for all fibers making
up a particular group (28).
Pr)] is plotted against
pCa} by using least squares regression analysis. Two Hill plots
were obtained for each fiber: one from data points <0.5
Pr (Hill plot coefficient
n2) and another
using data points >0.5 Pr (Hill
plot coefficient
n1). The value
for the free Ca2+ concentration
eliciting one-half maximal activation was calculated as the mean
abscissal intercept of the plots. The
Ca2+-activation threshold was
calculated as the free Ca2+
concentration corresponding to an ordinal value of 2.5 for the Hill plot by using data points <0.5
Pr.
80°C. Later, ~0.5 nl of fiber
volume was run on a Hoefer SE 600 gel-electrophoresis system,
consisting of a 3% (wt/vol) acrylamide stacking gel and a 5%
(wt/vol) separating gel as previously described (27). Gels were
silver stained according to the procedures described by Giulian et al.
(9). Representative gels illustrating MHC identification in single rat
soleus fibers have been presented in previous work from this laboratory
(8, 16, 27).
Table 1.
Animal and soleus mass
Variable
WB Group
NWB Group
IWB Group
n
8
7
8
Body mass, g
356 ± 6
383 ± 12
361 ± 11
Soleus mass, g
177 ± 7
107 ± 7*
118 ± 5*
Soleus/body mass, mg/g
0.50 ± 0.02
0.28 ± 0.01*
0.33 ± 0.01*,
Values are means ± SE; n, no. of animals. WB, weight
bearing; NWB, non-weight bearing; IWB, intermittent weight bearing.
*
P < 0.05 vs. WB mean.
P < 0.05 vs. NWB
mean.
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Neither non-weight bearing nor intermittent weight bearing affected a/Po, which specifies the curvature of the force-velocity relationship (Table 2). Consequently, there were no differences in the relative load associated with the peak power output of type I fibers from each experimental group (19 ± 0.3, 18 ± 0.4, and 19 ± 0.5% of peak isometric force for the weight-bearing, non-weight-bearing, and intermittent weight-bearing groups, respectively; P > 0.05). However, because non-weight bearing and intermittent weight bearing both reduced peak isometric force while elevating Vmax in comparison to the weight-bearing condition, the absolute forces and shortening velocities associated with peak power output differed between the three treatments. Fibers from the non-weight-bearing group produced 54% less absolute force and 24% less normalized force at peak power output than did fibers from the weight-bearing animals. Compared with the non-weight-bearing condition, the intermittent weight-bearing treatments served to elevate both the absolute (26%) and normalized force (16%) produced at peak power. However, this countermeasure did not restore these forces to weight-bearing levels because fibers from the intermittent weight-bearing group still produced 41% less absolute force and 12% less force per fiber cross-sectional area at peak power output than fibers from the weight-bearing animals. At the submaximal force associated with peak power output, non-weight-bearing type I fibers shortened on average 56% faster than type I fibers from the weight-bearing group. Intermittent weight bearing served to reduce this non-weight-bearing-induced rise in shortening velocity by ~45%. However, type I fibers obtained from the intermittent weight-bearing rats still shortened at a velocity that exceeded the shortening velocity of type I fibers from the weight-bearing animals by 25%. Non-weight bearing reduced the average peak absolute power output (µN · FL · s
1)
of type I soleus fibers by 33% (Table 2). Intermittent weight bearing
had no significant effect on this non-weight-bearing-induced reduction
in peak absolute power. Figure 2
illustrates that at essentially all relative forces (Fig.
2A), type I fibers from both the
non-weight-bearing and intermittent weight-bearing groups produced
substantially less power than did type I fibers from the weight-bearing
animals. These differences in power output were even more evident when
the force-power results were plotted on an absolute force axis (Fig.
2B).
When peak power was normalized for differences in fiber size (kN · m
2 · FL · s1),
single fibers from the non-weight-bearing animals produced slightly
greater peak power than did fibers from the intermittent weight-bearing
group, which in turn produced slightly greater peak power than did
fibers from the weight-bearing rats. However, these differences were
not statistically significant.
Force-pCa relationships.
Force-pCa relationships (Fig. 3) and Hill
plot analysis (Table 3) were used to assess the
dependence of force production on free
Ca2+ levels in single
fibers. Non-weight bearing shifted the force-pCa relationship to the right so that a significantly greater free Ca2+ concentration was required to
achieve one-half maximal activation. In all groups, there was a steeper
rise in force at free Ca2+
concentrations eliciting <50% of peak force
(n2) in
comparison to levels of Ca2+
activation producing >50% of relative force
(n1).
Non-weight bearing had no effect on the slope of the Hill plots for
data below or above 50% of peak force, nor did this treatment affect the free Ca2+ concentration
required for the onset of force (activation threshold). Compared with
fibers from the non-weight-bearing animals, intermittent weight bearing
shifted the force-pCa relationship to the left. Nevertheless, at
submaximal forces <50% of peak force, the force-pCa relationship for
fibers from the intermittent weight-bearing animals fell between the
curves observed for fibers from the weight-bearing and
non-weight-bearing groups. Hill plot analysis indicated that the free
Ca2+ concentration required for
one-half maximal activation was statistically similar for fibers
obtained from the weight bearing and intermittent weight-bearing
animals.
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DISCUSSION
20% vs.
non-weight-bearing mean). Because these changes in fiber force
production and shortening velocity have opposing effects on peak power,
the average peak power output of type I fibers after the intermittent
weight-bearing treatments remained at the non-weight-bearing level.
These results have important implications concerning the effectiveness
of intermittent weight bearing as a countermeasure to
non-weight-bearing-induced soleus atrophy. Preliminary results from our
laboratory indicate that 17 days of non-weight bearing reduce the peak
power of human type I soleus fibers (25). While it is not entirely
clear as to whether a loss of soleus power would hamper the physical
performance of humans during the microgravity conditions of
spaceflight, these reductions would be expected to limit work capacity
on a return to a gravity environment (4). In the case of bed rest, it
is likely that the ability to resume a normal lifestyle on the
resumption of ambulatory activity would be compromised by a loss of
muscle power. The inability of intermittent weight-bearing treatments
to reduce non-weight-bearing-induced losses in peak power brings into
question the practical effectiveness of this countermeasure. What
appears to be required is a modified procedure that
1) restores peak force to a greater
extent than the present protocol and/or
2) does not affect the elevation in type I fiber shortening velocity that occurs during non-weight bearing.
Fiber Ca2+
sensitivity.
Fiber Ca2+ sensitivity is thought
to be regulated by differences in thin filament regulatory protein
isoforms (12, 21) and the kinetics of cross-bridge attachment and
detachment (1). In addition to these regulatory mechanisms, the
relationship between force and
Ca2+ concentration is highly
sensitive to the spacing between the thin and thick myofilaments (11).
In agreement with previous results (8, 18), 14 days of non-weight
bearing reduced the Ca2+
sensitivity of single fibers. This is evident by the rightward shift of
the force-pCa relationship for forces <50% of peak force and by the
significantly greater free Ca2+
concentration required to attain half-maximal activation. The mechanism(s) responsible for this rightward shift in the force-pCa relationship is not presently known. Non-weight bearing is associated with an increase in the fast isoforms of troponin T (TnT) and troponin
I (3). Single intermediate- and fast-velocity fibers expressing a fast
TnT isoform have a lower Ca2+
sensitivity than do slow-velocity fibers expressing the slow TnT
isoform (12). However, it is not known what effect fast TnT expression
in a slow fiber would have on the force-pCa relationship. Electron
micrographs demonstrating a disproportionate loss of thick filaments
(24) raise the possibility that the ultrastructural geometry of the
myofilament lattice could be altered during non-weight bearing. While
it is not known whether changes in filament geometry actually occur, an
increase in the distance between thin and thick filaments,
and/or a change in the angle at which myosin binds to
actin, is consistent with a rightward shift in the force-pCa relationship (11).
Based on the Hill plot analysis results in Table 3, one could conclude
that intermittent weight-bearing treatments restored fiber
Ca2+ sensitivity to the
weight-bearing level. However, an examination of the force-pCa
relationships (Fig. 3) indicates that at forces <50% of peak force,
the relationship for fibers from the intermittent weight-bearing
animals fell between the relationships observed for the other two
groups. Taken together, these results indicate that fiber
Ca2+ sensitivity may not have been
completely restored by the intermittent weight-bearing treatments. If
changes in the expression of thin filament regulatory proteins are
responsible for the rightward shift in the force-pCa relationship after
non-weight bearing, then the intermittent weight-bearing treatments may
have worked to partially reduce the expression of these isoforms.
Alternatively, if the rightward shift was due to changes in lattice
spacing, intermittent weight bearing may have attenuated these changes in ultrastructural geometry. This second hypothesis is attractive because it could also explain the reduction in fiber
Vmax and the
increase in peak normalized force that occurred with the intermittent weight-bearing treatments (20).
Conclusions.
The stimulus provided by intermittent weight-bearing treatments, which
is presumed to be the restoration of normal weight-bearing activity by
the hindlimb extensor muscles, attenuated a non-weight-bearing-induced reduction in fiber Ca2+
sensitivity. However, this countermeasure had no effect on the decline
in type I fiber peak power output that occurs during 14 days of
non-weight bearing. Intermittent weight bearing was ineffective in this
regard because it had opposing effects on fiber force (an increase vs.
the non-weight-bearing mean) and fiber shortening velocity (a decrease
vs. the non-weight-bearing mean). This inability to attenuate
reductions in type I peak power output is a shortcoming of intermittent
weight bearing as a countermeasure to non-weight-bearing-induced soleus
atrophy.
ACKNOWLEDGEMENTS
This study was supported by a Wisconsin Space Grant Consortium scholarship to J. J. Bangart, National Aeronautics and Space Administration (NASA) Postdoctoral Space Biology Research Associate Award SBRA93-06 to J. J. Widrick, and NASA Grants NAG2-212 and NAGW-4376 to R. H. Fitts.
FOOTNOTES
Address for reprint requests: R. H. Fitts, Marquette Univ., Dept. of Biology, Wehr Life Sciences Bldg., P.O. Box 1881, Milwaukee, WI 53201-1881.
Received 30 September 1996; accepted in final form 7 February 1997.
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J. Caruso, J. Hamill, M. Yamauchi, D. Mercado, T. Cook, B. Higginson, S. O'Meara, J. Elias, and S. Siconolfi Albuterol aids resistance exercise in reducing unloading-induced ankle extensor strength losses J Appl Physiol, May 1, 2005; 98(5): 1705 - 1711. [Abstract] [Full Text] [PDF]
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 D. A. Riley, J. L. W. Bain, J. G. Romatowski, and R. H. Fitts Skeletal muscle fiber atrophy: altered thin filament density changes slow fiber force and shortening velocity Am J Physiol Cell Physiol, February 1, 2005; 288(2): C360 - C365. [Abstract] [Full Text] [PDF]
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D. V. Baewer, M. Hoffman, J. G. Romatowski, J. L. W. Bain, R. H. Fitts, and D. A. Riley Passive stretch inhibits central corelike lesion formation in the soleus muscles of hindlimb-suspended unloaded rats J Appl Physiol, September 1, 2004; 97(3): 930 - 934. [Abstract] [Full Text] [PDF]
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J. C. Gallegly, N. A. Turesky, B. A. Strotman, C. M. Gurley, C. A. Peterson, and E. E. Dupont-Versteegden Satellite cell regulation of muscle mass is altered at old age J Appl Physiol, September 1, 2004; 97(3): 1082 - 1090. [Abstract] [Full Text] [PDF]
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J. E. Hurst and R. H. Fitts Hindlimb unloading-induced muscle atrophy and loss of function: protective effect of isometric exercise J Appl Physiol, October 1, 2003; 95(4): 1405 - 1417. [Abstract] [Full Text] [PDF]
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L.-F. Zhang, B. Sun, X.-S. Cao, C. Liu, Z.-B. Yu, L.-N. Zhang, J.-H. Cheng, Y.-H. Wu, and X.-Y. Wu Effectiveness of intermittent -Gx gravitation in preventing deconditioning due to simulated microgravity J Appl Physiol, July 1, 2003; 95(1): 207 - 218. [Abstract] [Full Text] [PDF]
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K. Yamashita-Goto, R. Okuyama, M. Honda, K. Kawasaki, K. Fujita, T. Yamada, I. Nonaka, Y. Ohira, and T. Yoshioka Maximal and submaximal forces of slow fibers in human soleus after bed rest J Appl Physiol, July 1, 2001; 91(1): 417 - 424. [Abstract] [Full Text] [PDF]
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R. H. Fitts, D. R. Riley, and J. J. Widrick Physiology of a Microgravity Environment Invited Review: Microgravity and skeletal muscle J Appl Physiol, August 1, 2000; 89(2): 823 - 839. [Abstract] [Full Text] [PDF]
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J. J. Widrick, K. M. Norenberg, J. G. Romatowski, C. A. Blaser, M. Karhanek, J. Sherwood, S. W. Trappe, T. A. Trappe, D. L. Costill, and R. H. Fitts Force-velocity-power and force-pCa relationships of human soleus fibers after 17 days of bed rest J Appl Physiol, November 1, 1998; 85(5): 1949 - 1956. [Abstract] [Full Text] [PDF]
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E. E. Dupont-Versteegden, M. Knox, C. M. Gurley, J. D. Houle, and C. A. Peterson Maintenance of muscle mass is not dependent on the calcineurin-NFAT pathway Am J Physiol Cell Physiol, June 1, 2002; 282(6): C1387 - C1395. [Abstract] [Full Text] [PDF]
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