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Muscle fiber necrosis and regeneration induced by prolonged weight-lifting exercise in the cat.

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THE ANATOMICAL RECORD 211:133-141(1985)
Muscle Fiber Necrosis and Regeneration Induced
by Prolonged Weight-Lifting Exercise in the Cat
C.J. GIDDINGS, W.B. NEAVES, AND W.J. GONYEA
University of Texas Health Science Center, Department of Cell Biology, Dallas, TX 75235
For periods ranging from 26 to 87 weeks, the morphological charABSTRACT
acteristics of the flexor carpi radialis (FCR) muscle were examined in four cats
trained to perform weight-lifting exercise. Four untrained, sex and weight-matched
cats served as controls. The right FCR from each cat was surgically isolated, attached to a tension transducer, and set at its optimal 1ength.The forelimb was
perfused with 2% glutaraldehyde in 0.1 M cacodylate buffer. Small bundles of fibers
were teased from their origin and insertion tendons and embedded in Epon. Spaced
serial sections were used to examine the morphological features of the fibers for
trained and control animals. Ultrastructural examination revealed muscle fiber
degenerative changes, such as pyknotic nuclei, disruption of the sarcolemma, vacuolation, and disorganization of myofilaments. Such changes were observed a t a
higher frequency in trained muscle than in control muscle. Spaced serial sections of
fiber bundles showed that the degree of degeneration varied along the length of the
fiber. Fiber area measurements showed that trained muscle had both larger and
smaller fibers than control samples. The very small fibers observed in the trained
muscle were considered to be regenerating or “new” fibers since they had not
undergone degenerative changes. “Satellite-like” cells were observed in trained
muscle. Such cells resembled satellite cells but also contained developing myofilaments. Since evidence of degeneration-regeneration was observed in control samples,
but at a lower frequency, it was postulated that weight-lifting exercise accelerates
muscle fiber turnover in the cat FCR.
It is well known that skeletal muscle adapts differently to different forms of exercise. High resistance exercise such as weight-lifting induces increases in muscle
mass (hypertrophy) whereas endurance training usually
does not. Muscle hypertrophy has generally been attributed only to increases in muscle fiber size. However, it
has also been suggested that high resistance exercise
may increase fiber number (hyperplasia) (cf. Gonyea,
1980). Muscle biopsy studies in humans support the
concept of hyperplasia. Biopsies from elite (competition
class) bodybuilders and powerlifters showed no difference in fiber size when compared to control samples in
spite of large differences in elbow extension strength
and arm girth (MacDougall et al., 1982). Similar observations were reported by Tesch and Larsson (1982) in a
study comparing competition class bodybuilders to nonstrength-trained physical education students. Mean fiber area did not differ between the two groups in spite
of greater limb circumference and muscle mass shown
by the bodybuilders. These observations indicate that
hypertrophy of muscle fibers cannot account for the increased strength or limb circumference and that the
bodybuilders may possess a greater number of fibers
than control subjects. However, the concept of hyperplasia still remains controversial (Gollnick et al., 1981).
Recently, studies have shown that muscle fiber damage occurs with intense exercise. Acute eccentric exercise in rats running downhill resulted in necrosis of
muscle fibers (Armstrong et al., 1983).Disruption of the
0 1985 ALAN R.LISS, INC.
normal banding pattern occurred in some fibers. Later,
accumulations of monocytes and macrophages were observed in muscle fibers and in the interstitium. Necrosis
of muscle fibers also occurred in response to marathon
running in humans (Hikida et al., 1983).Ultrastructural
changes, most evident 1-3 days after a marathon, consisted of empty basal lamina tubes representing muscle
fiber remnants, disrupted sarcolemma, and infiltration
by phagocytic cells. These observations suggest inflammation may be a contributing factor in a n acute response to intense exercise.
Less is known about the long-term effects of exercise
on muscle morphology. A higher percentage of muscle
fibers from elite bodybuilders, who had trained intensively for a n average of 7 years, showed abnormalities
when compared to control individuals (MacDougall et
al., 1982). Central nuclei were present more frequently
in muscle fibers from the elite group. Enlarged cytoplasmic spaces and atrophied fibers were found only in
samples from the elite bodybuilders. The atrophied fibers exhibited no degenerative changes except that they
were reduced in size when compared to other normal
fibers in the biopsy sample. The presence of central
nuclei and small size strongly suggests fibers undergoing regeneration (Carlson, 1973; Carlson and Faulkner,
1983).
Received November 4, 1983; accepted September 11, 1984.
134
C.J. GIDDINGS, W.B. NEAVES, AND W.J. GONYEA
Preliminary data from cats trained to perform weightlifting exercise indicated that long-term high resistance
exercise may induce degenerative changes in muscle
along with regeneration which may provide a mechanism for hyperplasia (Gonyea et al., 1982). This study
was undertaken to examine the morphological characteristics of skeletal muscle after prolonged high resistance exercise (weight-lifting) in cats and to determine
the relationship of fiber size to morphological changes
in the exercised muscle.
METHODS
Four adult cats (three female and one male) were
trained to perform weight-lifting exercise for a food reward according to the method of Gonyea and Ericson
(1976). Four sex- and weight-matched untrained adult
cats served as control animals. The trained cats performed one arm curls by grasping a bar with their right
forelimb and moving the bar a specific distance. Weights
attached to the bar via a pulley were lifted as the bar
was moved. Additional weight was added weekly
throughout the training period which ranged from 2687 weeks (average 51 wks). The length of the training
period was determined by the ability of the cat to lift
increasing amounts of weight. When the cat had
achieved its maximum level and could not lift the next
increment of weight, it was anesthetized with sodium
pentobarbital (35 mgkg). The long insertion tendon of
the right flexor carpi radialis (FCR) muscle was surgically isolated from the forelimb of the animal and the
tendon was attached to a tension transducer. The muscle
was set at its optimal length following the procedure of
Gonyea and Bonde-Petersen (1977). The brachial artery
was cannulated and the forelimb was perfused with 50
ml minimal essential medium (MEM) followed by 50 ml
2% glutaraldehyde in 0.1 M cacodylate buffer (pH 7.3).
The FCR was then removed from the animal, weighed,
and stored in fresh fixative a t 4°C overnight. The right
FCR muscles from the untrained cats were perfused in
the same manner.
Muscle fiber bundles of 200-500 fibers were teased
from their origin and insertion tendons of the muscle
using microsurgical technique under a dissecting microscope. The bundles were postfixed in 1%osmium tetroxide, stained in uranyl acetate overnight, dehydrated,
and embedded in Epon 812. A modification of the technique used by Ontel (1977) of spaced serial ultrathin
sections was employed to examine the structural characteristics of the muscle fibers throughout their length.
The embedded bundles were cut transversely into 1-mm
segments and mounted on blank Epon blocks. Serial
transverse sections were cut a t 0.5 pm and 1.5 pm from
each block. The 0.5 pm sections were stained with toluidine blue and used for orientation to follow individual
fibers through their length. The 1.5 pm sections were
stained with p-phenylene diamine (Korneliussen, 1972)
and were used for fiber area measurements. Fiber areas
were determined from single cross sections near the
midregion of the fiber bundle. Photomicrographs ( x 25)
of the sections were taken and a Summagraphics digitizing tablet on line with a DEC 10 computer was used to
determine muscle fiber area. Spaced serial ultrathin
sections were taken from areas of interest observed during light microscopic evaluation of the 0.5 pm and 1.5
pm sections. The ultrathin sections were stained with
lead citrate and viewed using a Zeiss electron
microscope.
The data were analyzed statistically using Student’s t
test unless Bartlett’s test for equal variances demonstrated nonparametric analysis should be used, in which
case the Mann-Whitney test was used (Zar, 1974).Means
are expressed one standard error of the mean.
RESULTS
Mean body weight for trained and control cats did not
differ significantly and was 3.03 0.34 kg and 2.92 &
0.15 kg, respectively (mean 5 SE). The maximum weight
lifted by the four trained animals ranged from 1,140 to
1,760 gm (mean 1,375 gm). The mean weight of the right
FCR muscle from trained animals was 1.362 f 0.156
gm. This represented a 23.6% increase in muscle weight
when compared to the mean weight of the left FCR
muscle from the same animals (1.096 5 0.118 gm, P =
0.06). However, when the muscle mass of the right FCR
from the trained cats was compared to the muscle mass
of the right FCR from control cats (0.915 f 0.062 gm),
there was a significant increase in muscle weight of
48.6% in the trained animals (P < 0.05).
The average daily work and power outputs for the
trained cats are shown in Figures 1 and 2, which represent the mean of the four trained animals. Each individual cat showed a similar trend. There was a gradual
increase in power output from 100 gm to about 1,000 gm
of weight lifted. The power output then showed a greater
rise when heavier weights were lifted. The work performed by the cats increased until the animals were
lifting about 1,000 gm a t which time the work appeared
to level off.
Ultrastructural examination of the muscle samples
demonstrated degenerative morphological changes such
as disrupted sarcolemma, disorganization of myofilaments, vacuolation, and pyknotic nuclei. Such changes
were more frequently observed in trained muscle than
in control muscle. Fibers from trained and control animals were followed at 1 mm intervals. Areas of focal
necrosis occurred in about 5% of the muscle fibers examined in trained animals compared to less than 1%of
the control muscle fibers. This preliminary frequency
was based on a sample of 1,729 fibers from exercised
animals and 746 fibers from control cats. Central nuclei
were observed in trained and control muscle; however,
their frequency was not determined. Hypertrophic fibers
were observed only in trained muscle (Fig. 3). Ultrastructural examination of these fibers revealed disorganization of contractile elements (Fig. 4). The sarcolemma of some fibers was fragmented although the basal
lamina remained intact (Fig. 5). Some fibers had extensive regions of disrupted sarcolemma (Fig. 6). Membrane-bound vacuoles were observed in many necrotic
fibers (Fig. 7). Pyknotic nuclei were observed in fibers
undergoing degeneration. Occasionally, invasive cells
were found within a degenerating fiber (Fig. 8).
By examining spaced serial sections, the degree of
degeneration was determined to vary along the length
of the fibers. Figure 9 shows a group of fibers followed a
1-mm intervals through the middle region of the fibers.
A spectrum of degenerative changes can be seen in one
fiber of this group. This fiber has normal structural
features over a portion of its length (Fig. 9A). At this
level its sarcolemma is intact and myofilaments appear
135
MUSCLE FIBER TURNOVER
i
WORK OUTPUT
POWER OUTPUT
0+
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.
.
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1000
WEIGHT LIFTED IGRANS 1
Fig. 1. Average daily work output (joules) performed by four exercis-
ing cats.
Fig. 3. Light micrographs of hypertrophic fibers observed in trained
. Cross-sectional area of fiber = 5,642 pm2. B) Crossmuscle. ~ 9 5A)
500
1000
YEIGHT LIFTED C GRAHS )
Fig. 2. Average power output (joules per second) performed by four
exercising cats.
sectional area of fiber = 6,192 pm2. C) Cross-sectional area of fiber =
7,270 pm2. D) Cross-sectional area of fiber = 4,904pm2.
136
C.J.GIDDINGS, W.B. NEAVES, AND W.J. GONYEA
Fig. 4. Electron micrograph of a hypertropic fiber in cross section
from the middle region of the fiber. The fiber has lost the organization
of myofilaments. x 15,200.
Fig. 5. Electron micrograph of a necrotic (N) fiber in cross section.
Sarcolemma is disrupted (arrowhead) although basal lamina is intact.
Mitochondria appear swollen. A healthy fiber (M) is seen next to the
necrotic fiber. ~25,225.
Fig. 6. Electron micrograph of a necrotic fiber in cross section. Exten-
sive areas of disrupted sarcolemma can be seen (arrowhead). Basal
lamina is intact. Mitochondria are swollen. x 14,800.
Fig. 7. Electron micrograph of a necrotic fiber. Membrane-bound
vacuoles (V)and a pkynotic nucleus can be seen. X 14,100.
Fig. 8. Electron micrograph of a necrotic fiber (N) in longitudinal
section. An invasive cell (I) is observed within the fiber. A normal
muscle fiber (M) is adjacent to the necrotic fiber. X3,500.
MUSCLE FIBER TURNOVER
Fig. 9. Light micrographs of a group of fibers in cross section followed
at 1-mm intervals through the midregion of their length. One fiber
. the
(arrowheads) shows a spectrum of degenerative changes. ~ 9 6A)
fiber appears normal. B) The fiber shows vacuolation. C) The fiber is
enlarged. D) Only a basal lamina tube remains.
Fig. 10. Electron micrograph of the necrotic fiber seen in Figure 9C.
137
The fiber contains many swollen mitochondria (M). Sarcolemma is
fragmented. ~5,000.
Fig. 11. Electron micrograph of the necrotic fiber seen in Figure 9D.
Only a basal lamina tube remains containing a few swollen mitochondra (M).BL, basal lamina. ~ 2 , 2 5 0 .
138
C.J. GIDDINGS, W.B. NEAVES, AND W.J. GONYEA
.
0 -
FIBER AREA
-
-
TRAINED FCR
00:
0
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9-0
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4000
2000
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8( DO
FIBER AREA
In
FIBER AREA
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CONTROL FCR
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Fig. 12. Histograms of muscle fiber cross-sectional area of trained
and control samples.
organized. In the next segment, 1 mm away, the fiber
has a vacuolated appearance (Fig. 9B). Farther along its
length, the same fiber has a much greater cross-sectional area when compared to the previous sections (Fig.
9C). At this level the sarcolemma is fragmented and
there is a loss of organization of myofilaments. The
mitochondria also appear swollen and disrupted (Fig.
10).The most extreme degenerative changes are seen in
Figure 9D where the fiber consists of only a basal lamina tube containing a few swollen mitochondria (Fig.
11).
The histograms of fiber areas indicated that trained
muscle contained both larger and smaller fibers than
were observed in matched control samples (Fig. 12).
Many of the largest fibers exhibited degenerative
changes over a part of their length. The small fibers
observed in the trained muscle were considered to be
regenerating or "new" fibers since they were observed
not to contain degenerative morphological changes (Fig.
13). Figure 16 shows the ultrastructural characteristics
of a small fiber from trained muscle. The fiber has a
peripherally located euchromatic nucleus, the contractile elements appear organized and densely packed, and
there are no indications of atrophy or degeneration. Satellik cells were present under the basal lamina of control and trained muscle fibers (Fig. 14).In trained muscle
"satellite-like" cells were observed containing myofilaments and may represent the development of new fibers
(Fig. 15).These cells were observed infrequently. At this
point we have not systematically sampled for satellite
MUSCLE FIBER TURNOVER
Fig. 13.Light micrograph from trained muscle showing very small
regenerating or “new” muscle fibers. Compare with figure 16, which
shows the ultrastructural features of one fiber (asterisk) from this
group. x97.
Fig. 14. Electron micrograph of satellite cells beneath the basal
lamina (BL)of A) trained fibers ( x 8,430) and B) control fibers ( ~ 8 , 2 6 0 ) .
139
Fig. 15. A) Electron micrograph of a “satellite-like” cell (S)observed
in trained muscle. A myonucleus (MN) is seen next to it. ~ 8 , 3 6 0B)
. A
higher magnification of a portion of the satellite-like cell showing
developing myofilaments. ~21,200.
140
C.J. GIDDINGS, W.B. NEAVES, AND W.J. GONYEA
Fig. 16. Electron micrograph of a small fiber seen in Figure 13. The
fiber shows no degenerative changes and therefore, represents a regenerating or “new” fiber. X3,971.
cells to determine the frequency of those containing
myofilaments. Such cells were not observed in control
muscle.
DISCUSSION
Muscle fiber necrosis has been reported following acute
eccentric exercise (forceful stretching of the muscle) in
rats trained to run downhill on a treadmill (Armstrong
et al., 1983).It appeared that the necrosis was associated
with the acute inflammatory response observed during
the initial stage of training. Fiber necrosis was also
observed as a result of marathon running in humans
(Hikida et al., 1983). In contrast to these studies in
which a n acute response to exhaustive exercise was
reported, our study demonstrates for the first time that
muscle fibers undergo degeneration in response to longterm (chronic) high resistance exercise such as weightlifting in the cat. While downhill running produced eccentric muscle contractions, weight-lifting in the cat has
been shown to produce predominantly concentric (shortening of the muscle) in the FCR (Gonyea and BondePetersen, 1978). This study describes morphological
changes associated with chronic high resistance exercise.
Weight-lifting in cats induces muscle hypertrophy
(Gonyea and Ericson, 1976) and may also induce increases in muscle fiber number (Gonyea et al., 1983).
The right FCR mean weight from trained cats showed a
23.6% increase when compared to the left FCR from the
same animals (P = 0.06). However, since the cats use
their left limb a s a brace during weight lifting exercise,
the left FCR undergoes a n isometric training effect
(Gonyea and Ericson, 1976; Gonyea, 1980). This could
reduce differences observed in muscle mass when comparing the left FCR to the right FCR following training.
When the muscle mass of the right FCR from trained
cats was compared to sex- and weight-matched untrained control cats, there was a significant 48.6% increase in the trained muscle (P < 0.05).
Muscle hypertrophy has generally been attributed to
increases in muscle fiber size. However, in this study
fiber area measurements showed that the FCR muscles
from trained cats have both larger and smaller fibers
than do control samples (Fig. 12). We found that many
of the largest fibers had necrotic foci, although fiber
necrosis was not limited to a specific fiber size. This
would indicate that perhaps there is a limit to increases
in muscle fiber cross-sectional area (hypertrophy) at
which time fibers may undergo a degenerative process.
The largest fibers observed in this study showed degenerative changes such as disrupted sarcolemma, disorganization of myofilaments, pyknotic nuclei, and
vacuolation. It has been postulated that fiber necrosis
may be selective for a particular fiber type (Hikida et
al., 1983). Although fiber types were not determined in
this study, Gonyea and Bonde-Petersen (1978) found no
change in fiber type proportions in the FCR following
weight-lifting exercise. This would indicate that in the
cat FCR, muscle fiber necrosis is not fiber-type specific.
Although muscle fiber degeneration was observed a t a
higher frequency in trained muscles, neither fiber number nor strength decreases with exercise. In fact, our
preliminary results indicate that total fiber number in
the FCR increases in response to prolonged weighttraining exercise (Gonyea et al., 1983). Therefore, a
mechanism must exist to maintain or increase fiber
number. It is known that muscle regeneration occurs in
response to injury (Carlson and Faulkner, 1983). Previous studies on biopsy samples from elite bodybuilders
described small fibers as atrophic although no other
degenerative changes were noted (MacDougall et al.,
1982).Small fibers observed in this study did not appear
necrotic (Fig. 16) and, therefore, most likely represent
regenerating or “new” fibers. New fibers could originate
from muscle fiber splitting or through proliferation and
fusion of satellite cells (Allbrook, 1981; James, 1973; Van
Linge, 1962).
Branched fibers have been observed in serial frozen
sections following weight-lifting exercise in cats (Gonyea et al., 1977). In addition, direct counts of muscle
fibers following nitric acid digestion of the muscle have
shown that branched fibers can be found in both weighttrained and control muscles in the cat and also in weightoverloaded wing muscles and control muscles in chickens (Gonyea, manuscript in preparation; Gollnick et al.,
1983). However, the significance of branched fibers remains unclear. It has been postulated that branched
fibers might arise through longitudinal splitting of mature fibers (Gonyea et al., 1977; Ho et al., 1980; James,
1973; Van Linge, 1962). Fiber branches may also be the
result of defective myotube formation or from the fusion
of satellite fibers to mature fibers during regeneration
(James, 1973; Schmalbruch, 197613). Fiber branching
(splitting) was observed in this study and in rats after
weight-training (Ho et al., 1980). The mechanism by
which branching occurs and the role it might
play
- - in
hyperplasia hasyet to be determined.
141
MUSCLE FIBER TURNOVER
New fibers might also originate through profileration
and fusion of satellite cells (Allbrook, 1981). Satellite
cells have been shown to have myogenic potential in
tissue culture and in damaged muscle (Bischoff, 1979;
Schmalbruch, 1976a). Changes in satellite cell frequency in response to exercise remains to be determined. In this study, small cells which resembled
satellite cells and contained developing myofilaments
were observed in trained muscle. Fusion and growth of
such cells could provide a mechanism for hyperplasia.
The importance of satellite cells in the development of
“new” fibers in response to weight-lifting exercise must
await further analysis. Since muscle fiber degeneration
and regeneration are observed at very low frequencies
in control muscle, we postulate that high resistance
exercise accelerates muscle fiber turnover.
The mean power output (Fig. 1)of trained animals
indicated that there might be a threshold for changes
within the muscle. The power output showed much
steeper rise after the cats had exceeded the 1-kg increment of weight lifted. At this time, however, it is not
known whether this is correlated with an increase in
the degeneration-regeneration process. The work output
appears to level off a t higher weight lifted. This is consistent with previously reported work output in weighttraining cats by Gonyea (1980). Although the load the
cats lifted increased, the work output did not continue
to increase since the cats performed fewer events at the
higher weight.
Muscle consists of organized units called motor units
which are composed of a n alpha motoneuron and all the
fibers innervated by it (reviewed by Burke, 1981). It
could not be determined in this study if the degeneration
observed involved entire motor units or simply individual fibers of a muscle unit. Muscle fiber degeneration
could be due to denervation resulting from damage to
the nerve fibers or due to disruption of the sarcolemma
a t the neuromuscular junction. Although the structural
integrity of the neuromuscular junction has yet to be
examined in response to exercise, Ontell and Haller
(1980) have shown that the motor end plate remains
intact even with severe fiber necrosis in dystrophic mice.
Innervation of new fibers or reinnervation of regenerating fibers in response to weight-lifting exercise has not
been elucidated.
In summary, muscle fiber necrosis was observed in the
FCR muscle from cats trained to perform concentric
high resistance exercise. The trained muscles showed a
higher frequency of degenerative changes than did control muscles. The trained muscles also showed a wider
distribution of fiber cross-sectional area than did control
muscles. Small regenerating or “new” fibers were observed in the trained muscle; these may provide a mechanism for hyperplasia and account for a portion of the
increased strength in the trained cats.
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Armstrong, R.B., R.W. Ogilvie, and J.A. Schwane (1983)Eccentric
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Bischoff, R. (1979)Tissue culture studies on t h e origin of myogenic
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characteristics of muscle after prolonged weight-training in the
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number i n response to weight-lifting exercise. Med. Sci. Sports
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Costill (1983)Muscle fiber necrosis associated with human marathon runners. J. Neurol. Sci., 59:185-203.
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R.E. Carrow (1980)Skeletal muscle fiber splitting with weightlifting exercise in rats. Am. J. Anat., 157t433-440.
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ACKNOWLEDGMENTS
Tesch, P.A., and L. Larsson (1982)Muscle hypertrophy in bodybuilders.
We extend our appreciation to Ms. Barbara Barnes for
Eur. J. Appl. Physiol., 49t301-306.
her assistance in cat training and to Ms. Alicia Benitez Van Linge, B. (1962)The response of muscle to strenuous exercise. J.
Joint Surg., 44Br711-721.
for her assistance in preparing the manuscript. This Zar,Bone
J.H. (1974)Biostatistical Analysis. Prentice-Hall, Englewood Cliffs,
work was supported by grant AM17615 from the NaNJ.
tional Institute of Arthritis, Metabolism, and Digestive
Diseases.
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