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Short-term high- vs. low-velocity isokinetic lengthening training results in

greater hypertrophy of the elbow flexors in young men

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Tim N. Shepstone, Jason E. Tang, Stephane Dallaire, Mark D. Schuenke, Robert S.
Staron and Stuart M. Phillips
J Appl Physiol 98:1768-1776, 2005. First published Jan 7, 2005; doi:10.1152/japplphysiol.01027.2004

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J Appl Physiol 98: 1768 –1776, 2005.
First published January 7, 2005; doi:10.1152/japplphysiol.01027.2004.

Short-term high- vs. low-velocity isokinetic lengthening training results in

greater hypertrophy of the elbow flexors in young men
Tim N. Shepstone,1 Jason E. Tang,1 Stephane Dallaire,1
Mark D. Schuenke,2 Robert S. Staron,2 and Stuart M. Phillips1
1
Exercise and Metabolism Research Group, Department of Kinesiology, McMaster University, Hamilton, Ontario, Canada;
and 2Department of Biomedical Sciences, College of Osteopathic Medicine, Ohio University, Athens, Ohio
Submitted 16 September 2004; accepted in final form 29 December 2004

Shepstone, Tim N., Jason E. Tang, Stephane Dallaire, Mark crease in protein synthesis is directed toward remodeling and
D. Schuenke, Robert S. Staron, and Stuart M. Phillips. Short- addition of cellular protein structures, in particular myofibrillar
term high- vs. low-velocity isokinetic lengthening training results proteins, and is critical in the process of skeletal muscle
in greater hypertrophy of the elbow flexors in young men. J Appl hypertrophy. Most forms of resistive exercise also induce
Physiol 98: 1768 –1776, 2005. First published January 7, 2005; disruption of the protein ultrastructure, commonly observed as
doi:10.1152/japplphysiol.01027.2004.—We performed two studies
to determine the effect of a resistive training program comprised of
Z-line streaming and myofibrillar disorder, that is greater with
fast vs. slow isokinetic lengthening contractions on muscle fiber lengthening vs. shortening contractions (17, 18).
Both lengthening and shortening contractions [terms used

Downloaded from jap.physiology.org on October 1, 2007

hypertrophy. In study I, we investigated the effect of fast (3.66
rad/s; Fast) or slow (0.35 rad/s; Slow) isokinetic high-resistance according to arguments outlined by Faulkner (14) but often
muscle lengthening contractions on muscle fiber and whole muscle referred to as eccentric and concentric contractions, respec-
cross-sectional area (CSA) of the elbow flexors was investigated in tively] induce what has been labeled as muscle protein ultra-
young men. Twelve subjects (23.8 ⫾ 2.4 yr; means ⫾ SD) performed structural damage, which is greater with lengthening contrac-
maximal resistive lengthening isokinetic exercise with both arms for tions (17, 18). With repeated exposure to lengthening contrac-
8 wk (3 days/wk), during which they trained one arm at a Fast velocity tions, a combination of factors bring about a reduction in
while the contralateral arm performed an equivalent number of con- damage: the so-called “repeated-bout” effect (for review, see
tractions at a Slow velocity. Before (Pre) and after (Post) the training, Ref. 8). Where hypertrophy is concerned, various studies have
percutaneous muscle biopsies were taken from the midbelly of the
shown that resistive muscle training using isotonic (21, 26) and
biceps brachii and analyzed for fiber type and CSA. Type I muscle
fiber size increased Pre to Post (P ⬍ 0.05) in both Fast and Slow arms. isokinetic (13, 23, 24, 27, 40) training protocols in the absence
Type IIa and IIx muscle fiber CSA increased in both arms, but the of lengthening contractions results in less hypertrophy, and
increases were greater in the Fast- vs. the Slow-trained arm (P ⬍ smaller strength gains, than a corresponding condition consist-
0.05). Elbow flexor CSA increased in Fast and Slow arms, with the ing solely of shortening contractions or combinations of short-
increase in the Fast arm showing a trend toward being greater (P ⫽ ening and lengthening contractions. However, greater hyper-
0.06). Maximum torque-generating capacity also increased to a trophy with isokinetic lengthening-only training programs is
greater degree (P ⬍ 0.05) in the Fast arm, regardless of testing not always observed (9, 28, 31). Higher velocity lengthening
velocity. In study II, we attempted to provide some explanation of the contractions have been shown to increase muscular strength to
greater hypertrophy observed in study I by examining an indicator of a greater extent than slow contractions (13, 36); however,
protein remodeling (Z-line streaming), which we hypothesized would mechanism(s) responsible for this phenomenon remains un-
be greater in the Fast condition. Nine men (21.7 ⫾ 2.4 yr) performed known. Using B-mode ultrasound, Farthing and Chilibeck (13)
an acute bout (n ⫽ 30, 3 sets ⫻ 10 repetitions/set) of maximal
lengthening contractions at Fast and Slow velocities used in the
showed that muscle thickness (i.e., hypertrophy) was greater
training study. Biopsies revealed that Fast lengthening contractions with lengthening as opposed to shortening contractions, and
resulted in more (185 ⫾ 1 7%; P ⬍ 0.01) Z-band streaming per that there was a tendency (⬃5% greater) for greater hypertro-
millimeter squared muscle vs. the Slow arm. In conclusion, training phy in fast (3.14 rad/s) vs. slow (0.52 rad/s) trained arms.
using Fast (3.66 rad/s) lengthening contractions leads to greater Using their mixed design, these authors were likely underpow-
hypertrophy and strength gains than Slow (0.35 rad/s) lengthening ered to detect the difference between fast- and slow-trained
contractions. The greater hypertrophy seen in the Fast-trained arm arms (13). We hypothesized that the tendency for greater
(study I) may be related to a greater amount of protein remodeling hypertrophy seen previously with faster vs. slower lengthening
(Z-band streaming; study II). contractions (13) would be due to greater protein remodeling
muscle damage; time under tension; Z-band disruption induced by fast contractions (51, 52). Additionally, high-
velocity lengthening contractions, due to the nature of muscle
mechanics on the lengthening portion of the force-velocity
HYPERTROPHY OF SKELETAL MUSCLE as a result of resistance curve, generate greater muscle forces, which may also stimu-
training is due to a chronic summation of periods of positive late a greater protein synthetic response resulting in greater
net protein balance. The positive net protein balance arises due muscle hypertrophy.
to the synergistic stimulatory effect of both resistive exercise The purpose of the present study (study I) was to examine
and feeding on muscle protein synthesis (6, 7, 48). The in- the early-phase adaptations in muscle fiber and whole muscle

Address for reprint requests and other correspondence: S. M. Phillips, Dept. The costs of publication of this article were defrayed in part by the payment
of Kinesiology, IWC AB116, McMaster Univ., 1280 Main St. W., Hamilton, of page charges. The article must therefore be hereby marked “advertisement”
ON, Canada L8S 4K1 (E-mail: [email protected]). in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

1768 8750-7587/05 $8.00 Copyright © 2005 the American Physiological Society http://www. jap.org
 VELOCITY OF LENGTHENING CONTRACTIONS AND HYPERTROPHY 1769
CSA of the elbow flexors, in young men after an isokinetic torque within (ICC ⫽ 0.97) and between (ICC ⫽ 0.95) testing
resistance training program with disparate lengthening contrac- sessions. Five to seven days later, subjects reported back to the testing
tile velocities [low velocity (Slow; 0.35 rad/s) and high veloc- center and muscle biopsy samples were taken from the belly of the
ity (Fast; 3.66 rad/s)]. We used naive untrained subjects to see biceps brachii muscle of each arm. Arms were then randomly assigned
(counterbalanced for dominance based on strength) to be trained using
a maximal response in terms of hypertrophy (2). Given the
either fast (Fast) or slow (Slow) lengthening contractions.
variability in the extent (32, 49) as well as time course (20) of Subjects commenced training after 1 wk of rest. For the next 8 wk,
resistance training-induced muscle hypertrophy and given that subjects reported to the testing center every Monday, Wednesday, and
we only used a short-term study, and were trying to detect Friday for exercise training. During the first week, one set (10
differences between two kinds of resistance training, we chose repetitions/set) of maximal lengthening contractions was completed
to use a within-subject design because this is a superior design for both Fast and Slow velocities, and every week subsequent an
compared with between-subject comparisons in terms of num- additional set was added to a maximum of four, with 180 s of rest
bers of subjects needed to see a significant effect of the between each set. For the remaining 4 wk, subjects continued to
differing velocities. We also chose to use the biceps as the complete four sets on every training day. All subjects completed
muscle for training because maximal lengthening actions dur- 100% of the prescribed 24 training sessions.
After the 8-wk training protocol, subjects were again given 4 days
ing knee flexion would likely have resulted in subjects being
of rest before posttraining (Post) testing for maximal torque genera-
able to exceed the maximal torque generating capacity of most tion. Post muscle biopsies were then obtained from a position ⬃4 –5
dynamometers (405 N 䡠m in our case), particularly after train- cm superior or inferior (randomized counterbalanced) to the Pre
ing. We hypothesized, in light of previous reports, that the Fast biopsies.
training would induce greater strength (12, 36) and hypertro- Strength measurements. Strength tests were performed both Pre

Downloaded from jap.physiology.org on October 1, 2007

phic (13) gains. The greater hypertrophy in the Fast trained arm and Post in a completely randomized order, with 4 min of rest in
would occur despite a substantially smaller torque-time inte- between, at various contraction speeds (0.35, 1.05, 2.10, 3.14, and
gral vs. Slow training. 3.66 rad/s) and types (lengthening, concentric, and isometric). Sub-
To examine the potential mechanisms underlying the differ- jects placed their elbow on a positioning pad so that the ulnar-humeral
ential effects of velocity on hypertrophy, we also conducted a joint was at the axis of rotation of the Biodex machine, and they could
separate study in which the acute changes in Z-line disruption comfortably grasp the lever arm handle, while their forearm was in a
supinated position. Restraining straps were placed so as to secure the
were examined after Slow- and Fast-velocity lengthening con- subject while seated in the dynamometer. Most importantly, a re-
tractions. Biopsies were taken, from a separate group of sub- straining strap was placed diagonally over the involved shoulder to
jects from study I to examine the degree of Z-line disruption omit the involvement of any other muscle groups, other than the
induced by a single acute bout of lengthening muscle contrac- elbow flexors, during performance of the maximal contractions.
tions. Our hypothesis with this study was that Fast lengthening Isometric torque. Subjects performed three repetitions of a maxi-
actions would induce greater Z-line disruption than Slow mum voluntary contraction at 1.05 rad (120°) of elbow flexion. Each
lengthening, which is indicative of protein remodeling, which contraction was 5 s in duration with 30 s of rest between contractions.
may be a precursor to muscle hypertrophy (51, 52). Maximum isometric torque was considered to be the highest peak
torque of the three contractions.
METHODS Shortening torque. Concentric torque was recorded as the highest
peak torque of three repetitions through 1.57 rad (90°) range of
Study I: Training Study motion. Every repetition began at 3.05 rad (175°) of elbow flexion and
concluded when the subject flexed his arm, and the Biodex lever arm,
Subjects. Twelve healthy men (age 23.8 ⫾ 3.4 yr, height 178.5 ⫾
with maximal force to 1.48 rad (85°) of elbow flexion. Concentric
9.6 cm, weight 82.5 ⫾ 10.3 kg) who were recreationally active (i.e.,
torque was evaluated at the five different velocities: 0.35, 1.05, 2.10,
no weight training) participated in the 8-wk training study. Subjects
3.14, and 3.66 rad/s.
were performing no more than 1–2 h/wk of structured physical
Lengthening torque. Measurements of lengthening torque were
activity, and none was, or had been for the previous 6 mo, engaging
made at the five testing velocities in a similar manner as for concentric
in resistance training. No subjects were taking protein or other
torque. Lengthening torque was taken from the highest peak torque of
supplements or potential ergogenic aids of any kind. Subjects were
three repetitions starting at 1.48 rad (85°) and concluding at 3.05 rad
required to complete a routine medical screening questionnaire and
(175°) of elbow flexion. Each lengthening contraction, completed at
based on the questionnaire and physical examination were deemed
five velocities (0.35, 1.05, 2.10, 3.14, and 3.66 rad/s), was completed
healthy. Subjects were advised of the purposes and risks associated
by the subject maximally resisting the lever arm, which was returning
with the study, and they gave written, informed consent. The project
to the resting position after the contraction.
was approved by the Hamilton Health Sciences and McMaster Uni-
pQCT scans. The midline of the belly of the biceps brachii was
versity Research Ethics Board.
determined by measuring halfway between midpoint of the antecubi-
General Experimental Protocol tal and axilla areas. The arm was then inserted into a small cylinder
that functions as the measurement area of the pQCT densitometer
One week before the study start date, subjects attended a familiar- (Stratec XCT 2000 Densiometer, Norland Medical Systems, Fort
ization session on the testing and training apparatus (Biodex-System Atkinson, WI). The subject’s arm remained motionless for ⬃4 min
3, Biodex Medical Systems, Shirley, NY). On the study start date, while the scan (2.5 mm) was performed. Cross-sectional area (CSA)
subjects had a scan taken at the midpoint of their biceps brachii in images were analyzed by using BonAlyze (Jyvaskyla, Finland), a
both arms by using high resolution peripheral quantitative computed software for processing computerized tomography scans that automat-
tomography (pQCT). Subjects also underwent a series of pretraining ically identifies muscle tissue by assessing density and geometry. The
(Pre) strength tests (see Strength measurements) on both arms inde- BonAlyze software excludes intermuscular fat by quantifying pixels
pendently. Using this procedure, and given that the elbow flexors are within a range corresponding to muscle density (35–160 mg/cm3) and
an easy muscle to recruit maximally with little to no training (33), it excludes pixels that correspond to the density of intermuscular fat. In
is not surprising that we consistently observed interclass correlation our laboratory, repeated scans of the midline of the biceps muscle
coefficients (ICC) of 0.95 and above for repeat testing of maximal CSA, analyzed by the same investigator, had a coefficient of variation

J Appl Physiol • VOL 98 • MAY 2005 • www.jap.org

1770 VELOCITY OF LENGTHENING CONTRACTIONS AND HYPERTROPHY

⬍1.33% (12 repeat scans). Interinvestigator variation in assessing Direct tracings using the Image Pro Plus software determined fiber
muscle CSA was never ⬎2.6%; hence, to minimize variability, all CSAs, which were expressed in micrometers squared. Fiber-type
scans for one subject were analyzed by one investigator who was percent area (defined as total fiber area for one fiber type divided by
blinded to condition. summed total fiber area for all fiber types multiplied by 100), using the
Muscle biopsies. Needle biopsy samples were obtained from each same cutoff thresholds and fiber-type distribution (number of one fiber
subject under local anesthesia (2% lidocaine) using manual suction. type as a percentage of the total number of fibers examined) measure-
One biopsy was taken from the medial portion of the right and left ments were also calculated automatically using Image Pro.
biceps brachii Pre to establish a baseline measurement. Another MHC protocol. Mixed-muscle myosin heavy chain (MHC) analysis
biopsy sample was taken from each of the trained arms in the same was carried out as described previously (16). Briefly, four to six serial
manner Post. Samples were immediately dissected free of visible fat sections from the OCT-embedded muscle sample were cut (20 ␮m)
and connective tissue, and they were placed in optimum cutting and placed into microfuge tubes containing 250 ␮l of lysing buffer
temperature (OCT; Tissue Tech, Sakura Finetechnical) embedding (10% wt/vol glycerol, 5% vol/vol 2-mercaptoethanol, and 2.3% wt/vol
medium with the muscle fibers oriented perpendicular to the plane in SDS in 62.5 mM Tris pH 6.8) and were heated for 10 min at 60°C.
which the muscle was to be cut. The samples were then quick frozen Approximately 4 – 6 ␮l of the lysed muscle extract were loaded into a
in isopentane cooled by liquid nitrogen, and then they were stored at 20-cm ⫻ 20-cm ⫻ 1.5-mm SDS-polyacrylamide gel, with Pre and
⫺80°C until subsequent analysis. Post samples adjacent to one another. The gel was poured and set in
Histochemical analysis. The frozen OCT-mounted muscle samples such a way that the top 25% of the gel was a 4% stacking gel, whereas
were serially cross-sectioned to 10 ␮m thick on a microtome cryostat the remaining 75% of the gel was a 4 – 8% acrylamide gradient.
(model HM500OM, MICROM International, Waldorf, Germany) Samples were run overnight (19 –21 h) at 120 V and subsequently
for histochemical analysis. Myofibrillar adenosine triphosphatase stained with Coomassie blue. Three separate and distinct MHC
(mATPase) histochemistry was performed using preincubation pH isoforms (I, IIa, and IIx) were visually identified according to their

Downloaded from jap.physiology.org on October 1, 2007

value 4.60 (50 mM potassium acetate and 17.5 mM calcium chloride) masses (as compared with known standards). The gels were then
for 6.5 min to determine muscle fiber-type composition. Slides were scanned using a laser densitometer, the relative staining intensity (i.e.,
then rinsed with distilled water and incubated in 3 mM ATP using an number of arbitrary densitometric units) of each band was calculated,
alkaline solution (75 mM glycine, 40.5 mM calcium chloride, 75 mM and the intensity was expressed as a percentage of the total staining
NaCl, and 67.5 mM NaOH, adjusted to pH 9.4) for 45 min at 37°C intensity (i.e., the summed arbitrary units of all three bands).
and agitated at regular intervals in a temperature-controlled incubator Statistical analysis (study I). Muscle fiber size, fiber type, pQCT,
shaker. After the ATP incubation, a rinse with distilled water was and MHC data were analyzed by using a two-factor repeated-mea-
done, and the samples were incubated in 1% CaCl2 for 3 min at room sures ANOVA, with time (Pre vs. Post), and condition (Fast vs. Slow)
temperature. Slides were again rinsed with distilled water and incu- as the factors. Strength data were analyzed by using a four-factor
bated in 2% CoCl2 for 3 min at room temperature. Another rinse with repeated-measures ANOVA, with time (Pre vs. Post), condition (Fast
vs. Slow), contraction (eccentric vs. concentric), and velocity (5
distilled water and an incubation in 1% ammonium sulfide for 1 min
levels: 0.35, 1.05, 2.10, 3.14, and 3.66 rad/s) as the factors. All
at room temperature followed. Samples were rinsed with distilled
analyses were performed using SPSS (version 11.5, Chicago, IL).
water five times before being dehydrated by incubating for 2 min in
Statistical significance for all analyses was accepted as P ⬍ 0.05.
each ethanol concentrations (70, 80, 90, 95, and 100%). Samples were
Significant main effects and interactions, where seen in the ANOVA,
then cleared using xylene. After the slides were dried, coverslips were
were further analyzed by using Tukey’s post hoc test. Values pre-
mounted using Permount (Fisher SP15) and allowed to dry overnight.
sented are means (SD).
Sections were viewed under light microscope (Olympus BX-60,
Olympus America, Melville, NY), and images were digitized using a
SPOT camera (model SP401-115, SPOT Diagnostic Instruments, Study II: Acute Study
Sterling Heights, MI) and visualized using SPOT software (V3.2.4 for Subjects. Nine men (age 23.2 ⫾ 2.4 yr, height 181.9 ⫾ 6.1 cm,
Windows, SPOT Diagnostic Instruments). Images were analyzed by weight 81.1 ⫾ 5.6 kg) who were recreationally active (i.e., no weight
using both Image-J software (National Institute of Mental Health, training and no more than 1 structured exercise bout per week)
Bethesda, MD) and Image Pro Plus (V4.0 for Windows, Media participated in the acute study protocol. Subjects were required to
Cybernetics, Silver Spring, MD). The number of images taken at complete a routine medical screening questionnaire and based on the
⫻200 magnification of each sample was between five and seven and questionnaire and physical examination were deemed healthy. Sub-
was largely dependent on the quality of the serial sections. Each image jects were advised of the purposes and risks associated with the study,
contained ⬃30 –50 fibers. Three fibers (type I, IIa, and IIx) were and they gave written, informed consent. The project was approved by
consistently distinguished using the Image-J software by setting cutoff the Hamilton Health Sciences and McMaster University Research
limits resulting in the creation of optical density “bins” according to Ethics Board.
the darkest (type I), lightest (type IIa), and intermediate (type IIx) Experimental protocol. For 1 wk before reporting to the testing
fibers, as previously described (44). The classification of fiber type is center, subjects were instructed to refrain from any form of strenuous
thus dependent on the intensity of the staining by the mATPase upper body activity. On the first study day, subjects had a muscle
histochemical protocol. At pH 4.60, the light, intermediate, and dark biopsy removed from the belly of biceps brachii of both right and left
fibers correspond to fiber type IIa, type IIx, and type I, respectively. arms. Subjects also received instruction on the exercise protocol and
Sample images were converted to 8-bit, 256 gray-scale images, which use of the Biodex apparatus used for testing. For the week after the
linearly scales each pixel and assigns a value from between 0 (black) first biopsy, subjects were again asked to refrain from strenuous upper
to 255 (white). By setting lower and upper threshold values, optical body activity. The next day, subjects returned to the Ivor Wynne
density bins were created that were as follows: 0 –95 for dark areas, Centre to repeat the contraction protocol and subsequently had the
100 –175 for intermediate areas, 180 –255 for light areas. Using these second biopsy sample from each arm taken. Subjects again returned to
cutoffs, the three fiber types were more objectively classified. A repeat the contraction protocol 24 and 72 h after the second biopsy
similar procedure was employed using the Image Pro Plus software. In session.
comparing the ability of Image J and Image Pro Plus to classify the Exercise protocol. The exercise protocol was completed on the
same images (n ⫽ 26 sample sets Pre and Post), we obtained an ICC Biodex dynamometer. Subjects placed their elbow on the Biodex
of 0.985 (P ⬍ 0.001), and we also found that the ICC for repeated positioning pad so that their forearm was in a supinated position, the
image analysis was 1.0 for both programs. ulnar-humeral joint was at the axis of rotation of the Biodex lever arm,

J Appl Physiol • VOL 98 • MAY 2005 • www.jap.org

 VELOCITY OF LENGTHENING CONTRACTIONS AND HYPERTROPHY 1771
that sections identified as having Z-band streaming were shown also
to have disrupted Z-bands by using electron microscopy (5, 45, 46).
We also confirmed, using electron microscopy (⫻3,500 –5,000 mag-
nification), in 30 randomly selected blocks (6 at rest, 12 at 24 h after
the Fast exercise, and 12 others at 24 h after the Slow exercise) that
Z-line streaming as identified using high-magnification light micros-
copy were in fact areas of disruption as estimated. Damage estimated
by light microscopy and by electron microscopy were highly corre-
lated (r ⫽ 0.98, P ⬍ 0.0001).
Statistical analysis (study II). Z-line streaming was analyzed as a
paired t-test, because no disrupted areas were seen in the baseline
biopsies; hence, values obtained were essentially a difference from
baseline (i.e., only a single value for Slow and Fast). All analyses
were performed using SPSS (version 11.5). Statistical significance
for all analyses was accepted as P ⬍ 0.05. Values presented are
means (SD).
RESULTS

Study I: Training Study

Strength. Training resulted in subjects being able to generate

Downloaded from jap.physiology.org on October 1, 2007

higher maximal torques during lengthening contractions, re-
gardless of velocity, compared with shortening contractions
(P ⬍ 0.05). Training also resulted in a main effect for training
Fig. 1. Peak torque before (Pre) and after (Post) 8 wk (24 sessions) of Fast mode (Fast ⬎ Slow); hence, subjects were able to generate
(3.66 rad/s) and Slow (0.35 rad/s) training (study I). A: Slow arm. B: Fast arm. higher maximal torques after Fast training, regardless of ve-
Values are means (SD) for 12 subjects. *Significant main effect for time, P ⬍ locity, compared with shortening contractions (P ⫽ 0.023).
0.05. †Significant time ⫻ condition interaction (Fast ⬎ Slow) at all testing
velocities Post, P ⬍ 0.05. Fast training increased maximum torques across all velocities
by an average of 11.3 ⫾ 10.4 N䡠m, whereas Slow training only
increased strength by 6.3 ⫾ 12.0 N䡠m (P ⫽ 0.041; Fig. 1).
pQCT. Values for whole muscle CSA Pre and Post training
and they could comfortably grasp the lever arm handle. A restraining
are shown in Fig. 2. All changes are significantly different from
strap was placed diagonally over the involved shoulder to omit
involvement from other muscle groups. Each subject completed three zero (P ⬍ 0.01), with no significant difference between Fast
sets (10 repetitions/set) of maximal lengthening contractions through and Slow (P ⫽ 0.060 for a time ⫻ condition interaction) and
1.57 rad (90°) of arm flexion with 180 s of rest between sets. One arm with a significant difference (P ⫽ 0.024) between Post Fast vs.
was exercised at the Fast velocity (3.66 rad/s) while the other was Post Slow by post hoc test.
exercised at the Slow velocity (0.35 rad/s). Muscle fiber CSA. Training resulted in a significant increase
Muscle sampling. Needle biopsy samples were obtained from each in the mean CSA of all fiber types (P ⫽ 0.016). Type I muscle
subject under local anesthesia (2% lidocaine) using manual suction. fibers increased in size (P ⫽ 0.042; Fig. 3) by an average of
One biopsy was taken from the medial portion of the right and left 9.3 ⫾ 5.0% (range Slow ⫽ 3–560 ␮m2, Fast ⫽ 94 –1,300 ␮m2)
biceps brachii to establish a baseline measurement. Another biopsy with no significant differences between Fast or Slow (P ⫽
sample was taken from each of the trained arms in the same manner
0.19). The change in fiber area after training for only the type
24 h after the two-set exercise protocol was completed. Samples were
immediately dissected free of fat and connective tissue, and they were
placed into a chilled (4°C) fixative (2% gluteraldehyde buffered with
0.1% sodium cacodylate) for staining with toluidine blue as described
previously (5, 45, 46).
Light microscopy. After initial fixation, the tissue samples were
postfixed in osmium tetroxide, dehydrated in graded baths of ethyl
alcohol, and embedded in an epoxy resin (Spurr’s) with the fibers
oriented longitudinally. Each block was then sectioned (0.5 ␮m) and
stained with toluidine blue.
Individual fibers from each longitudinal muscle section were stud-
ied under ⫻1,000 magnification and examined for moderate (3–10
continuous and/or adjacent Z bands) and extreme (10 or more con-
tinuous and/or adjacent Z bands) Z-band streaming as described
previously (5, 45, 46). Sample areas were calculated, and the amount
of Z-band streaming was expressed per millimeter squared of muscle.
All muscle sections were scored and viewed blind to the investigator
as to the treatment (Fast or Slow) and subject. ICCs for repeated
sample analysis with one investigator were consistently ⬎0.96 on 10
separate samples. In addition, interinvestigator estimates of Z-line Fig. 2. Whole muscle peripheral computed tomography pQCT scan for muscle
streaming using this method were also consistently ⬎0.94, as reported cross-sectional area (CSA) before and after 8 wk of Fast and Slow training.
previously (5, 45, 46). To reduce the variability, one investigator Values are means (SD) for 12 subjects. *Significant main effect for time, P ⬍
performed all of the analyses. Using this method, it has been shown 0.05. Time ⫻ condition interaction, P ⫽ 0.06.

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1772 VELOCITY OF LENGTHENING CONTRACTIONS AND HYPERTROPHY

of type IIa fibers from Pre to Post but only in the Fast-trained
arm (P ⫽ 0.05; Table 1). The percent area occupied by IIa
fibers was also significantly greater in the Fast vs. the Slow arm
(P ⫽ 0.041; Table 1).
MHC content. The percentage of MHC isoforms expressed
showed a significant decrease in the percentage of type IIx
isoform expressed in both Fast and Slow arms after training
(P ⫽ 0.033; Table 1). Similarly, there was an increase in the
percentage of type IIa isoforms present after training that
was greater in the Fast vs. the Slow arm. The percentage of
MHC isoforms expressed according to gel electrophoresis
correlated well with the percent area for each fiber type as
analyzed by mATPase histochemistry (r ⫽ 0.95, P ⫽
0.0006; Fig. 4).

Study II: Acute Study

Z-line streaming. The extent of moderate Z-band disruption
(expressed per mm2 of muscle) seen in all muscle samples
from the postexercise time point was greater (P ⬍ 0.001) than

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baseline samples, in which no damage could be identified.
Z-band disruption was greater (185 ⫾ 17%) after the Fast
exercise protocol than that seen after the Slow exercise proto-
col (P ⫽ 0.002; Fig. 5). The extent of extreme, compared with
moderate, Z-band streaming (defined as encompassing ⬎10
serially or longitudinally adjacent sarcomeres with damage)
(17, 18) was not significantly different (P ⫽ 0.096) between
Fast- and Slow-exercised arms (Fast ⫽ 0.10 ⫾ 0.15 and
Slow ⫽ 0.04 ⫾ 0.11 areas of extreme damage per mm2 of
muscle), but it was observed in six of nine Fast samples and
only two of nine Slow samples.

Table 1. Percentage muscle fiber composition and muscle

fiber area by histochemistry, as well as percentage myosin
heavy chain from biopsies taken before and after training
Type I Type IIa Type IIx

Fiber, %
Fast
Pre 46.9 (15.6) 46.0 (12.8) 9.1 (8.7)
Post 42.3 (10.0) 50.9 (9.0) 6.8 (6.6)*
Slow
Pre 45.2 (12.8) 43.5 (12.5) 11.3 (9.7)
Fig. 3. Muscle fiber sizes in the Fast and Slow trained arms (study I) before Post 49.8 (3.3) 42.8 (10.4) 7.4 (5.9)*
and after 8 wk (24 training sessions) of isokinetic lengthening contractions. Area, %
A: type I fibers. B: type IIa fibers. C: type IIx fibers. Values are means (SD)
Fast
for 12 subjects. Note different scales for each graph. *Significantly differ-
Pre 33.3 (11.8) 58.2 (13.2) 8.5 (7.6)
ent from Pre, P ⬍ 0.05. ⫹Significantly different from Slow arm at the same
Post 27.8 (7.6) 66.6 (9.0)*† 5.6 (6.2)
time, P ⬍ 0.01.
Slow
Pre 32.5 (11.8) 58.1 (12.8) 9.3 (6.9)
Post 34.1 (8.7) 59.8 (8.7) 6.1 (4.8)
II fiber subtypes was greater in the Fast-trained (IIa: range ⫽ MHC, %
279 –1,548 ␮m2; IIx range ⫽ 963–1,730 ␮m2) vs. the Slow- Fast
trained arm (IIa: range ⫽ 57–966 ␮m2; IIx range ⫽ 205–1,124 Pre 37.3 (8.0) 54.1 (13.1) 8.0 (6.2)
␮m2; all P ⫽ 0.007; Fig. 3). Post 30.3 (7.3) 65.6 (7.3)*† 4.1 (4.5)*
Slow
Muscle fiber type. A significant decrease was observed in the Pre 37.0 (10.8) 53.4 (12.8) 6.7 (8.0)
percent distribution of type IIx fibers (P ⫽ 0.031; Table 1), Post 34.1 (7.6) 61.3 (6.3)* 4.6 (7.8)*
regardless of training. Although statistical significance was not
Values are means (SD) for 12 subjects. Fast, fast trained arm (3.66 rad/s);
reached, a trend was also observed toward a decrease in the Slow, slow trained arm (0.35 rad/s); Pre, before training; Post, after training;
percent area that type IIx fibers occupy (P ⫽ 0.056; Table 1). MHC, myosin heavy chain. *Significantly different from Pre, P ⬍ 0.05.
There was, however, a significant difference in the percent area †Significantly different from Slow at the same time point, P ⬍ 0.05.

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 VELOCITY OF LENGTHENING CONTRACTIONS AND HYPERTROPHY 1773
shortening (3.14 and 0.52rad/s) muscle training promoted a
greater degree of hypertrophy. In addition, the difference in
hypertrophy between the degree of hypertrophy induced by
training with fast and slow (0.52 rad/s) lengthening conditions,
whereas not statistically different, was 5% (13); their mixed-
factor design likely lacked the statistical power to detect this
difference. In our study, we attempted to address this short-
coming by using a completely within-subject design and by
using two lengthening conditions that were more disparate in
velocity: 10-fold vs. only a 6-fold used by Farthing and
Chilibeck, thinking that a greater difference in velocity may
play a role in emphasizing differences in protein remodeling
and thus hypertrophy, according to our hypothesis.
Fig. 4. Correlation between myosin heavy chain (MHC) isoform distribution
Adams et al. (1) recently showed that training using con-
by gel electrophoresis and percent area distribution from histochemistry (study tractions that were isometric, lengthening, or shortening re-
I). Pearson’s r ⫽ 0.95 (P ⬍ 0.001). sulted in an equivalent hypertrophy in rats. The torque integrals
for these three training modes were obviously quite different
DISCUSSION from each other. Despite similar degrees of hypertrophy, in-
creases in mRNA expression for mechano-growth factor and

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The results of the present investigation show that a resistive insulin-like growth factor I (IGF-I), two proteins that have
training program consisting of fast isokinetic (3.66 rad/s) been implicated as playing a role in hypertrophic muscle
lengthening contractions resulted in a greater fiber hypertro- growth (19), were increased only in the isometric and short-
phy, in type II fibers, vs. lengthening training performed at a ening contraction conditions (1). In humans, a single bout of
slower isokinetic (0.35 rad/s) velocity. This conclusion is lengthening resistive exercise resulted in a greater increase in
supported by a significantly greater increase in muscle fiber IGF-I mRNA expression vs. a bout of shortening exercise (4).
size as indicated by mATPase histochemical analysis. Addi- We observed, despite a ⬎10-fold lower mean torque-time
tional support for the greater hypertrophy observed with fast integral (Fig. 6), a greater degree of hypertrophy (Fig. 3) with
lengthening training was demonstrated by our data measuring a training protocol that involved only high velocity lengthening
the CSA at the midline of the biceps brachii by pQCT. contractions. However, why we observed greater hypertrophy
Although we did not observe a significant difference between with Fast as opposed to Slow lengthening contractions when
the degree of change in the Fast and Slow arms using pQCT, Adams et al. (1) observed quite similar hypertrophy with
there was a strong trend (P ⫽ 0.06) toward the Fast-trained arm different contraction types and vastly dissimilar force-time
having greater hypertrophy over the Slow-trained arm; hence, integrals is not readily apparent. The difference in the model
it is likely a type II statistical error that we are reporting no utilized in our study as opposed to that of Adams et al. may
difference between the Fast and Slow trained arms in hyper- explain some of the differences: rats vs. humans, imposed vs.
trophy with pQCT. voluntary contractions, and the number of training bouts were
A number of studies (13, 21, 23, 24, 26, 27, 40) have shown greater in our study (24 vs. only 10 used by Adams et al.).
that training involving muscle lengthening contractions pro-
duces greater hypertrophy, and oftentimes greater strength
gains, than a condition in which shortening contractions or a
combination of shortening and lengthening contractions were
used. We also acknowledge that greater hypertrophy with
lengthening-only vs. shortening-only or mixed contractions is
not always observed (9, 28, 31). However, we believe that the
balance of evidence favors the idea that there is something
intrinsically unique with muscle lengthening contractions that
promotes hypertrophy. For example, the ability of lengthening
contractions to promote hypertrophy was elegantly demon-
strated by LaStayo and colleagues (30), who used cycle er-
gometry exercise to induce hypertrophy, but this occurred only
when performed eccentrically. Eccentric ergometry induced a
52% increase in muscle fiber area and a 36% increase in
isometric leg strength, whereas traditional concentric ergom-
etry induced no change in fiber size or strength. In addition,
compensatory hypertrophy after immobilization-induced atro-
phy has also been shown to be enhanced in terms of strength
gains as well as fiber hypertrophy when lengthening as op-
posed to shortening, or even mixed, contractions were used in Fig. 5. Moderate Z-band disruption (study II: see METHODS for details) seen in
biopsy samples 24 h after an acute lengthening isokinetic exercise protocol
rehabilitation postimmobilization (25). Recently, Farthing and (see METHODS for details). Values are means (SD) for 9 subjects. *Significantly
Chilibeck (13) found that training of the elbow flexors with fast different from baseline (i.e., zero or no disruption), P ⬍ 0.001. ⫹Significantly
lengthening contractions (3.14 rad/s) as opposed to fast or slow different from Slow, P ⬍ 0.01.

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1774 VELOCITY OF LENGTHENING CONTRACTIONS AND HYPERTROPHY

of protein turnover, synthesis or breakdown, in this study, so

this theory remains speculative.
Training increased muscle strength at all tested velocities,
regardless of training mode; however, the overall gain in
maximal torque generation was greater in the Fast arm at all
velocities (i.e., a main effect of training mode; Fig. 1). This
result is most likely at least in part a consequence of the greater
hypertrophy seen within the Fast-trained arm (Fig. 3). Accord-
ing to previous reports (24, 25, 27), however, strength gains are
typically dependent on training modes. Hence, when training
with lengthening-only muscle contractions, it is expected that
lengthening strength would increase more then concentric
strength. There is also the possibility of cross-education, that
is, an effect of one training protocol impacting on the con-
tralateral arm (10, 41, 47). However, when both limbs are
training simultaneously, it is impossible to estimate how the
strength gains in one limb would transfer to the other limb. In
other studies we examined, strength was variably altered in an
untrained limb (41) or remained unchanged (47); hence, in our

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design where both limbs are training, it appears that strength
gains that transfer from one limb to other would be minimal,
compared with the transfer of strength to a nontrained limb.
We acknowledge that training mode may have been transferred
to the contralateral limb, but evidence for this phenomenon in
simultaneously training limbs indicates similar results to what
we observed, that is an overall generally greater increase in
strength with lengthening muscle actions with no specificity
Fig. 6. Torque tracings recorded during maximal torque testing Pre and Post effect for velocity (12, 36). Additionally, because the gains in
training in an individual subject (study I). A: Fast-trained arm (torque-time integral maximal torque were greater in the Fast-trained arm, then any
Pre ⫽ 19.1 and Post ⫽ 23.8). B: Slow-trained arm (torque-time integral Pre ⫽
213.3 and Post ⫽ 303.1). Note that time scales on the graphs are different.
cross-education in terms of strength gains would be to increase
strength gains in the Slow-trained arm in which we observed
“inferior” strength gains (Fig. 1). Hence, the fact that we saw
Previously, our laboratory had labeled the ultrastructural a difference between the Fast and Slow arms in terms of
observation of smeared or disrupted Z lines as muscle damage strength gains is even more impressive and likely due to our
(5, 46), in accordance with others (15, 18, 39). Recently, it was use of a unilateral all-within-subject design.
reported that an acute bout of lengthening muscle actions, The overall gains seen in maximal torque generation were quite
which would have resulted in severe muscle damage, resulted moderate, and hence differences would have been more difficult
in no detectable disturbances of the myofiber protein structure to detect were they present. We suspect that the moderate strength
(11). In fact, what we observed and labeled as Z-line stream- gains may have been due to some residual fatigue from the
ing, and have previously called muscle damage (5, 46), has training itself, despite several days of rest after the subjects’ last
recently been reported not to be muscle damage but instead training bout before strength assessment. In fact, Fig. 7 shows the
myofibrillar remodeling (11, 51, 52). This conclusion was
based on an elegant and detailed immunohistochemcial and
electron miscroscopic examination of the protein composition
of amorphous or smeared Z lines (11). These authors showed
that the smeared Z lines from damaged muscle were quite
dissimilar from their normal protein composition, containing
instead higher than normal quantities of actin and desmin,
which the authors concluded was an indication of fiber protein
remodeling and not damage (51, 52). With this interpretation in
mind (51, 52), then our data indicate that, in the Fast training
condition, which as our acute study showed was accompanied
by greater “Z-line streaming” (Fig. 5), there would have been
greater fiber remodeling. Our laboratory has recently observed
that lengthening contractions, as opposed to shortening con-
tractions, are associated with a more rapid rise in myofibrillar
protein synthesis (34). If a greater protein synthetic response
were to result in greater protein accretion over time, according Fig. 7. Mean peak torque values for training sessions (study I) averaged by
week throughout the 8-wk training protocol. Values are means (SD) for 12
to the series of events outlined by Phillips (37), then this subjects. *Significantly different between Fast and Slow arms at the specified
provides a basis for why we saw greater hypertrophy in the week, P ⬍ 0.05. a Different from week 1, P ⬍ 0.05. b Different from weeks
Fast-trained arms. Of course, we have no direct measurements 1–7, P ⬍ 0.05. c Different from week 7, P ⬍ 0.05.

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 VELOCITY OF LENGTHENING CONTRACTIONS AND HYPERTROPHY 1775
mean peak torque on a week-to-week basis throughout the course under tension in the Fast- vs. the Slow-trained arms. We
of the study and shows that, during training, the weekly peak observed that acutely an isolated set of Fast contractions
torque was actually depressed, likely as a result of muscle protein resulted in greater disruption to the muscle ultrastructure,
remodeling (see Ref. 50 for a review), for some time before which could be indicative of greater protein remodeling and
recovering and eventually exceeding pretraining values only in the potentially faster onset (34) and potentially a greater duration
last week. This pattern of depressed force and yet substantial fiber of protein synthesis. Over time, the greater protein synthesis
remodeling, ultimately resulting in hypertrophy, is similar to that may result in greater hypertrophy.
seen with chronic low-frequency stimulation in animals. In this
model of extreme overload, force is persistently depressed, and ACKNOWLEDGMENTS
yet fiber adaptations still occur while substantial fiber remodeling We thank the subjects for time and John Moroz for outstanding expertise in
is still present (22). In two other studies in which differing the set up and use of testing and training equipment.
lengthening velocities were used for training (12, 36), the gains in
GRANTS
maximal torque were not large. For example, Paddon-Jones et al.
(36) found no significant gains in maximal torque generation in a This research was supported by a National Science and Engineering
Research Council of Canada grant to S. M. Phillips. S. M. Phillips is the
slow-trained arm performing lengthening contractions at 0.52 recipient of a Premier’s Research Excellence Award and a Canadian Institutes
rad/s and a 5- to 10-N䡠m increase in the fast-trained (3.14 rad/s) of Health Research New Investigator Award.
arm. Farthing and Chilibeck (12) also reported the increments in
maximal torque were in the range of 11–14 N䡠m. REFERENCES
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