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

1Exercise 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


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
We performed two studies to determine the effect of a resistive training program comprised of fast vs. slow isokinetic lengthening contractions on muscle fiber 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 muscle lengthening contractions on muscle fiber and whole muscle cross-sectional area (CSA) of the elbow flexors was investigated in young men. Twelve subjects (23.8 ± 2.4 yr; means ± SD) performed maximal resistive lengthening isokinetic exercise with both arms for 8 wk (3 days/wk), during which they trained one arm at a Fast velocity while the contralateral arm performed an equivalent number of contractions at a Slow velocity. Before (Pre) and after (Post) the training, percutaneous muscle biopsies were taken from the midbelly of the 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. Type IIa and IIx muscle fiber CSA increased in both arms, but the increases were greater in the Fast- vs. the Slow-trained arm (P < 0.05). Elbow flexor CSA increased in Fast and Slow arms, with the increase in the Fast arm showing a trend toward being greater (P = 0.06). Maximum torque-generating capacity also increased to a greater degree (P < 0.05) in the Fast arm, regardless of testing velocity. In study II, we attempted to provide some explanation of the greater hypertrophy observed in study I by examining an indicator of protein remodeling (Z-line streaming), which we hypothesized would be greater in the Fast condition. Nine men (21.7 ± 2.4 yr) performed an acute bout (n = 30, 3 sets x 10 repetitions/set) of maximal lengthening contractions at Fast and Slow velocities used in the training study. Biopsies revealed that Fast lengthening contractions resulted in more (185 ± 1 7%; P < 0.01) Z-band streaming per millimeter squared muscle vs. the Slow arm. In conclusion, training using Fast (3.66 rad/s) lengthening contractions leads to greater hypertrophy and strength gains than Slow (0.35 rad/s) lengthening contractions. The greater hypertrophy seen in the Fast-trained arm (study I) may be related to a greater amount of protein remodeling (Z-band streaming; study II).

muscle damage; time under tension; Z-band disruption

HYPERTROPHY OF SKELETAL MUSCLE as a result of resistance training is due to a chronic summation of periods of positive net protein balance. The positive net protein balance arises due to the synergistic stimulatory effect of both resistive exercise and feeding on muscle protein synthesis (6, 7, 48). The increase in protein synthesis is directed toward remodeling and addition of cellular protein structures, in particular myofibrillar proteins, and is critical in the process of skeletal muscle hypertrophy. Most forms of resistive exercise also induce disruption of the protein ultrastructure, commonly observed as Z-line streaming and myofibrillar disorder, that is greater with lengthening vs. shortening contractions (17, 18).

Both lengthening and shortening contractions [terms used according to arguments outlined by Faulkner (14) but often referred to as eccentric and concentric contractions, respectively] induce what has been labeled as muscle protein ultrastructural damage, which is greater with lengthening contractions (17, 18). With repeated exposure to lengthening contractions, a combination of factors bring about a reduction in damage: the so-called "repeated-bout" effect (for review, see Ref. 8). Where hypertrophy is concerned, various studies have shown that resistive muscle training using isotonic (21, 26) and isokinetic (13, 23, 24, 27, 40) training protocols in the absence of lengthening contractions results in less hypertrophy, and smaller strength gains, than a corresponding condition consisting solely of shortening contractions or combinations of shortening and lengthening contractions. However, greater hypertrophy with isokinetic lengthening-only training programs is not always observed (9, 28, 31). Higher velocity lengthening contractions have been shown to increase muscular strength to a greater extent than slow contractions (13, 36); however, mechanism(s) responsible for this phenomenon remains unknown. Using B-mode ultrasound, Farthing and Chilibeck (13) showed that muscle thickness (i.e., hypertrophy) was greater with lengthening as opposed to shortening contractions, and that there was a tendency (~5% greater) for greater hypertrophy in fast (3.14 rad/s) vs. slow (0.52 rad/s) trained arms. Using their mixed design, these authors were likely underpowered to detect the difference between fast- and slow-trained arms (13). We hypothesized that the tendency for greater hypertrophy seen previously with faster vs. slower lengthening contractions (13) would be due to greater protein remodeling 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 curve, generate greater muscle forces, which may also stimulate a greater protein synthetic response resulting in greater muscle hypertrophy.

The purpose of the present study (study I) was to examine the early-phase adaptations in muscle fiber and whole muscle CSA of the elbow flexors, in young men after an isokinetic resistance training program with disparate lengthening contractile velocities [low velocity (Slow; 0.35 rad/s) and high velocity (Fast; 3.66 rad/s)]. We used naive untrained subjects to see a maximal response in terms of hypertrophy (2). Given the variability in the extent (32, 49) as well as time course (20) of resistance training-induced muscle hypertrophy and given that we only used a short-term study, and were trying to detect differences between two kinds of resistance training, we chose to use a within-subject design because this is a superior design compared with between-subject comparisons in terms of numbers of subjects needed to see a significant effect of the differing velocities. We also chose to use the biceps as the muscle for training because maximal lengthening actions during knee flexion would likely have resulted in subjects being able to exceed the maximal torque generating capacity of most dynamometers (405 N·m in our case), particularly after training. We hypothesized, in light of previous reports, that the Fast training would induce greater strength (12, 36) and hypertrophic (13) gains. The greater hypertrophy in the Fast trained arm would occur despite a substantially smaller torque-time integral vs. Slow training.

To examine the potential mechanisms underlying the differential effects of velocity on hypertrophy, we also conducted a separate study in which the acute changes in Z-line disruption were examined after Slow- and Fast-velocity lengthening contractions. Biopsies were taken, from a separate group of subjects from study I to examine the degree of Z-line disruption induced by a single acute bout of lengthening muscle contractions. Our hypothesis with this study was that Fast lengthening actions would induce greater Z-line disruption than Slow lengthening, which is indicative of protein remodeling, which may be a precursor to muscle hypertrophy (51, 52).


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Study I: Training Study

Subjects.   Twelve healthy men (age 23.8 ± 3.4 yr, height 178.5 ± 9.6 cm, weight 82.5 ± 10.3 kg) who were recreationally active (i.e., no weight training) participated in the 8-wk training study. Subjects were performing no more than 1–2 h/wk of structured physical activity, and none was, or had been for the previous 6 mo, engaging in resistance training. No subjects were taking protein or other supplements or potential ergogenic aids of any kind. Subjects were required to complete a routine medical screening questionnaire and based on the questionnaire and physical examination were deemed healthy. Subjects were advised of the purposes and risks associated with the study, and they gave written, informed consent. The project was approved by the Hamilton Health Sciences and McMaster University Research Ethics Board.

General Experimental Protocol

One week before the study start date, subjects attended a familiarization session on the testing and training apparatus (Biodex-System 3, Biodex Medical Systems, Shirley, NY). On the study start date, subjects had a scan taken at the midpoint of their biceps brachii in both arms by using high resolution peripheral quantitative computed tomography (pQCT). Subjects also underwent a series of pretraining (Pre) strength tests (see Strength measurements) on both arms independently. Using this procedure, and given that the elbow flexors are an easy muscle to recruit maximally with little to no training (33), it is not surprising that we consistently observed interclass correlation coefficients (ICC) of 0.95 and above for repeat testing of maximal torque within (ICC = 0.97) and between (ICC = 0.95) testing sessions. Five to seven days later, subjects reported back to the testing center and muscle biopsy samples were taken from the belly of the biceps brachii muscle of each arm. Arms were then randomly assigned (counterbalanced for dominance based on strength) to be trained using either fast (Fast) or slow (Slow) lengthening contractions.

Subjects commenced training after 1 wk of rest. For the next 8 wk, subjects reported to the testing center every Monday, Wednesday, and Friday for exercise training. During the first week, one set (10 repetitions/set) of maximal lengthening contractions was completed for both Fast and Slow velocities, and every week subsequent an additional set was added to a maximum of four, with 180 s of rest between each set. For the remaining 4 wk, subjects continued to complete four sets on every training day. All subjects completed 100% of the prescribed 24 training sessions.

After the 8-wk training protocol, subjects were again given 4 days of rest before posttraining (Post) testing for maximal torque generation. Post muscle biopsies were then obtained from a position ~4–5 cm superior or inferior (randomized counterbalanced) to the Pre biopsies.

Strength measurements.   Strength tests were performed both Pre and Post in a completely randomized order, with 4 min of rest in between, at various contraction speeds (0.35, 1.05, 2.10, 3.14, and 3.66 rad/s) and types (lengthening, concentric, and isometric). Subjects placed their elbow on a positioning pad so that the ulnar-humeral joint was at the axis of rotation of the Biodex machine, and they could comfortably grasp the lever arm handle, while their forearm was in a supinated position. Restraining straps were placed so as to secure the subject while seated in the dynamometer. Most importantly, a restraining strap was placed diagonally over the involved shoulder to omit the involvement of any other muscle groups, other than the elbow flexors, during performance of the maximal contractions.

Isometric torque.   Subjects performed three repetitions of a maximum voluntary contraction at 1.05 rad (120°) of elbow flexion. Each contraction was 5 s in duration with 30 s of rest between contractions. Maximum isometric torque was considered to be the highest peak torque of the three contractions.

Shortening torque.   Concentric torque was recorded as the highest peak torque of three repetitions through 1.57 rad (90°) range of 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, with maximal force to 1.48 rad (85°) of elbow flexion. Concentric torque was evaluated at the five different velocities: 0.35, 1.05, 2.10, 3.14, and 3.66 rad/s.

Lengthening torque.   Measurements of lengthening torque were made at the five testing velocities in a similar manner as for concentric torque. Lengthening torque was taken from the highest peak torque of three repetitions starting at 1.48 rad (85°) and concluding at 3.05 rad (175°) of elbow flexion. Each lengthening contraction, completed at five velocities (0.35, 1.05, 2.10, 3.14, and 3.66 rad/s), was completed by the subject maximally resisting the lever arm, which was returning to the resting position after the contraction.

pQCT scans.   The midline of the belly of the biceps brachii was determined by measuring halfway between midpoint of the antecubital and axilla areas. The arm was then inserted into a small cylinder that functions as the measurement area of the pQCT densitometer (Stratec XCT 2000 Densiometer, Norland Medical Systems, Fort Atkinson, WI). The subject's arm remained motionless for ~4 min while the scan (2.5 mm) was performed. Cross-sectional area (CSA) images were analyzed by using BonAlyze (Jyvaskyla, Finland), a software for processing computerized tomography scans that automatically identifies muscle tissue by assessing density and geometry. The BonAlyze software excludes intermuscular fat by quantifying pixels within a range corresponding to muscle density (35–160 mg/cm3) and excludes pixels that correspond to the density of intermuscular fat. In our laboratory, repeated scans of the midline of the biceps muscle CSA, analyzed by the same investigator, had a coefficient of variation <1.33% (12 repeat scans). Interinvestigator variation in assessing muscle CSA was never >2.6%; hence, to minimize variability, all scans for one subject were analyzed by one investigator who was blinded to condition.

Muscle biopsies.   Needle biopsy samples were obtained from each subject under local anesthesia (2% lidocaine) using manual suction. One biopsy was taken from the medial portion of the right and left biceps brachii Pre to establish a baseline measurement. Another biopsy sample was taken from each of the trained arms in the same manner Post. Samples were immediately dissected free of visible fat and connective tissue, and they were placed in optimum cutting temperature (OCT; Tissue Tech, Sakura Finetechnical) embedding medium with the muscle fibers oriented perpendicular to the plane in which the muscle was to be cut. The samples were then quick frozen in isopentane cooled by liquid nitrogen, and then they were stored at –80°C until subsequent analysis.

Histochemical analysis.   The frozen OCT-mounted muscle samples were serially cross-sectioned to 10 µm thick on a microtome cryostat (model HM500OM, MICROM International, Waldorf, Germany) for histochemical analysis. Myofibrillar adenosine triphosphatase (mATPase) histochemistry was performed using preincubation pH value 4.60 (50 mM potassium acetate and 17.5 mM calcium chloride) for 6.5 min to determine muscle fiber-type composition. Slides were then rinsed with distilled water and incubated in 3 mM ATP using an alkaline solution (75 mM glycine, 40.5 mM calcium chloride, 75 mM NaCl, and 67.5 mM NaOH, adjusted to pH 9.4) for 45 min at 37°C and agitated at regular intervals in a temperature-controlled incubator shaker. After the ATP incubation, a rinse with distilled water was done, and the samples were incubated in 1% CaCl2 for 3 min at room temperature. Slides were again rinsed with distilled water and incubated in 2% CoCl2 for 3 min at room temperature. Another rinse with distilled water and an incubation in 1% ammonium sulfide for 1 min at room temperature followed. Samples were rinsed with distilled water five times before being dehydrated by incubating for 2 min in each ethanol concentrations (70, 80, 90, 95, and 100%). Samples were then cleared using xylene. After the slides were dried, coverslips were mounted using Permount (Fisher SP15) and allowed to dry overnight.

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, Sterling Heights, MI) and visualized using SPOT software (V3.2.4 for Windows, SPOT Diagnostic Instruments). Images were analyzed by using both Image-J software (National Institute of Mental Health, Bethesda, MD) and Image Pro Plus (V4.0 for Windows, Media Cybernetics, Silver Spring, MD). The number of images taken at x200 magnification of each sample was between five and seven and was largely dependent on the quality of the serial sections. Each image contained ~30–50 fibers. Three fibers (type I, IIa, and IIx) were consistently distinguished using the Image-J software by setting cutoff limits resulting in the creation of optical density "bins" according to the darkest (type I), lightest (type IIa), and intermediate (type IIx) fibers, as previously described (44). The classification of fiber type is thus dependent on the intensity of the staining by the mATPase histochemical protocol. At pH 4.60, the light, intermediate, and dark fibers correspond to fiber type IIa, type IIx, and type I, respectively. Sample images were converted to 8-bit, 256 gray-scale images, which linearly scales each pixel and assigns a value from between 0 (black) to 255 (white). By setting lower and upper threshold values, optical density bins were created that were as follows: 0–95 for dark areas, 100–175 for intermediate areas, 180–255 for light areas. Using these cutoffs, the three fiber types were more objectively classified. A similar procedure was employed using the Image Pro Plus software. In comparing the ability of Image J and Image Pro Plus to classify the same images (n = 26 sample sets Pre and Post), we obtained an ICC of 0.985 (P < 0.001), and we also found that the ICC for repeated image analysis was 1.0 for both programs.

Direct tracings using the Image Pro Plus software determined fiber CSAs, which were expressed in micrometers squared. Fiber-type percent area (defined as total fiber area for one fiber type divided by summed total fiber area for all fiber types multiplied by 100), using the same cutoff thresholds and fiber-type distribution (number of one fiber type as a percentage of the total number of fibers examined) measurements were also calculated automatically using Image Pro.

MHC protocol.   Mixed-muscle myosin heavy chain (MHC) analysis was carried out as described previously (16). Briefly, four to six serial sections from the OCT-embedded muscle sample were cut (20 µm) and placed into microfuge tubes containing 250 µl of lysing buffer (10% wt/vol glycerol, 5% vol/vol 2-mercaptoethanol, and 2.3% wt/vol SDS in 62.5 mM Tris pH 6.8) and were heated for 10 min at 60°C. Approximately 4–6 µl of the lysed muscle extract were loaded into a 20-cm x 20-cm x 1.5-mm SDS-polyacrylamide gel, with Pre and Post samples adjacent to one another. The gel was poured and set in such a way that the top 25% of the gel was a 4% stacking gel, whereas the remaining 75% of the gel was a 4–8% acrylamide gradient. Samples were run overnight (19–21 h) at 120 V and subsequently stained with Coomassie blue. Three separate and distinct MHC isoforms (I, IIa, and IIx) were visually identified according to their masses (as compared with known standards). The gels were then scanned using a laser densitometer, the relative staining intensity (i.e., number of arbitrary densitometric units) of each band was calculated, and the intensity was expressed as a percentage of the total staining intensity (i.e., the summed arbitrary units of all three bands).

Statistical analysis (study I).   Muscle fiber size, fiber type, pQCT, and MHC data were analyzed by using a two-factor repeated-measures ANOVA, with time (Pre vs. Post), and condition (Fast vs. Slow) as the factors. Strength data were analyzed by using a four-factor repeated-measures ANOVA, with time (Pre vs. Post), condition (Fast vs. Slow), contraction (eccentric vs. concentric), and velocity (5 levels: 0.35, 1.05, 2.10, 3.14, and 3.66 rad/s) as the factors. All analyses were performed using SPSS (version 11.5, Chicago, IL). Statistical significance for all analyses was accepted as P < 0.05. Significant main effects and interactions, where seen in the ANOVA, were further analyzed by using Tukey's post hoc test. Values presented are means (SD).

Study II: Acute Study

Subjects.   Nine men (age 23.2 ± 2.4 yr, height 181.9 ± 6.1 cm, weight 81.1 ± 5.6 kg) who were recreationally active (i.e., no weight training and no more than 1 structured exercise bout per week) participated in the acute study protocol. Subjects were required to complete a routine medical screening questionnaire and based on the questionnaire and physical examination were deemed healthy. Subjects were advised of the purposes and risks associated with the study, and they gave written, informed consent. The project was approved by the Hamilton Health Sciences and McMaster University Research Ethics Board.

Experimental protocol.   For 1 wk before reporting to the testing center, subjects were instructed to refrain from any form of strenuous upper body activity. On the first study day, subjects had a muscle biopsy removed from the belly of biceps brachii of both right and left arms. Subjects also received instruction on the exercise protocol and use of the Biodex apparatus used for testing. For the week after the first biopsy, subjects were again asked to refrain from strenuous upper body activity. The next day, subjects returned to the Ivor Wynne Centre to repeat the contraction protocol and subsequently had the second biopsy sample from each arm taken. Subjects again returned to repeat the contraction protocol 24 and 72 h after the second biopsy session.

Exercise protocol.   The exercise protocol was completed on the Biodex dynamometer. Subjects placed their elbow on the Biodex positioning pad so that their forearm was in a supinated position, the ulnar-humeral joint was at the axis of rotation of the Biodex lever arm, and they could comfortably grasp the lever arm handle. A restraining strap was placed diagonally over the involved shoulder to omit involvement from other muscle groups. Each subject completed three sets (10 repetitions/set) of maximal lengthening contractions through 1.57 rad (90°) of arm flexion with 180 s of rest between sets. One arm was exercised at the Fast velocity (3.66 rad/s) while the other was exercised at the Slow velocity (0.35 rad/s).

Muscle sampling.   Needle biopsy samples were obtained from each subject under local anesthesia (2% lidocaine) using manual suction. One biopsy was taken from the medial portion of the right and left biceps brachii to establish a baseline measurement. Another biopsy sample was taken from each of the trained arms in the same manner 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 µm) and stained with toluidine blue.

Individual fibers from each longitudinal muscle section were studied under x1,000 magnification and examined for moderate (3–10 continuous and/or adjacent Z bands) and extreme (10 or more continuous 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 streaming using this method were also consistently >0.94, as reported previously (5, 45, 46). To reduce the variability, one investigator performed all of the analyses. Using this method, it has been shown 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 (x3,500–5,000 magnification), 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 microscopy were in fact areas of disruption as estimated. Damage estimated by light microscopy and by electron microscopy were highly correlated (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
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Study I: Training Study

Strength.   Training resulted in subjects being able to generate higher maximal torques during lengthening contractions, regardless of velocity, compared with shortening contractions (P < 0.05). Training also resulted in a main effect for training mode (Fast > Slow); hence, subjects were able to generate higher maximal torques after Fast training, regardless of velocity, compared with shortening contractions (P = 0.023). Fast training increased maximum torques across all velocities by an average of 11.3 ± 10.4 N·m, whereas Slow training only increased strength by 6.3 ± 12.0 N·m (P = 0.041; Fig. 1).



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  		Fig. 1. Peak torque before (Pre) and after (Post) 8 wk (24 sessions) of Fast (3.66 rad/s) and Slow (0.35 rad/s) training (study I). A: Slow arm. B: Fast arm. Values are means (SD) for 12 subjects. *Significant main effect for time, P < 0.05. {dagger}Significant time x condition interaction (Fast > Slow) at all testing velocities Post, P < 0.05.

 
pQCT.   Values for whole muscle CSA Pre and Post training are shown in Fig. 2. All changes are significantly different from zero (P < 0.01), with no significant difference between Fast and Slow (P = 0.060 for a time x condition interaction) and with a significant difference (P = 0.024) between Post Fast vs. Post Slow by post hoc test.



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  		Fig. 2. Whole muscle peripheral computed tomography pQCT scan for muscle cross-sectional area (CSA) before and after 8 wk of Fast and Slow training. Values are means (SD) for 12 subjects. *Significant main effect for time, P < 0.05. Time x condition interaction, P = 0.06.

 
Muscle fiber CSA.   Training resulted in a significant increase in the mean CSA of all fiber types (P = 0.016). Type I muscle fibers increased in size (P = 0.042; Fig. 3) by an average of 9.3 ± 5.0% (range Slow = 3–560 µm2, Fast = 94–1,300 µm2) with no significant differences between Fast or Slow (P = 0.19). The change in fiber area after training for only the type II fiber subtypes was greater in the Fast-trained (IIa: range = 279–1,548 µm2; IIx range = 963–1,730 µm2) vs. the Slow-trained arm (IIa: range = 57–966 µm2; IIx range = 205–1,124 µm2; all P = 0.007; Fig. 3).



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  		Fig. 3. Muscle fiber sizes in the Fast and Slow trained arms (study I) before and after 8 wk (24 training sessions) of isokinetic lengthening contractions. A: type I fibers. B: type IIa fibers. C: type IIx fibers. Values are means (SD) for 12 subjects. Note different scales for each graph. *Significantly different from Pre, P < 0.05. +Significantly different from Slow arm at the same time, P < 0.01.

 
Muscle fiber type.   A significant decrease was observed in the percent distribution of type IIx fibers (P = 0.031; Table 1), regardless of training. Although statistical significance was not reached, a trend was also observed toward a decrease in the percent area that type IIx fibers occupy (P = 0.056; Table 1). There was, however, a significant difference in the percent area 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).


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  		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

 
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).



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  		Fig. 4. Correlation between myosin heavy chain (MHC) isoform distribution by gel electrophoresis and percent area distribution from histochemistry (study I). Pearson's r = 0.95 (P < 0.001).

 
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 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 protocol (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.



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  		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 (see METHODS for details). Values are means (SD) for 9 subjects. *Significantly different from baseline (i.e., zero or no disruption), P < 0.001. +Significantly different from Slow, P < 0.01.

 

   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
GRANTS
 ACKNOWLEDGMENTS
 REFERENCES
 
The results of the present investigation show that a resistive training program consisting of fast isokinetic (3.66 rad/s) lengthening contractions resulted in a greater fiber hypertrophy, in type II fibers, vs. lengthening training performed at a slower isokinetic (0.35 rad/s) velocity. This conclusion is supported by a significantly greater increase in muscle fiber size as indicated by mATPase histochemical analysis. Additional support for the greater hypertrophy observed with fast lengthening training was demonstrated by our data measuring the CSA at the midline of the biceps brachii by pQCT. Although we did not observe a significant difference between the degree of change in the Fast and Slow arms using pQCT, there was a strong trend (P = 0.06) toward the Fast-trained arm having greater hypertrophy over the Slow-trained arm; hence, it is likely a type II statistical error that we are reporting no difference between the Fast and Slow trained arms in hypertrophy with pQCT.

A number of studies (13, 21, 23, 24, 26, 27, 40) have shown that training involving muscle lengthening contractions produces 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 demonstrated by LaStayo and colleagues (30), who used cycle ergometry 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 ergometry induced no change in fiber size or strength. In addition, compensatory hypertrophy after immobilization-induced atrophy has also been shown to be enhanced in terms of strength gains as well as fiber hypertrophy when lengthening as opposed to shortening, or even mixed, contractions were used in rehabilitation postimmobilization (25). Recently, Farthing and Chilibeck (13) found that training of the elbow flexors with fast lengthening contractions (3.14 rad/s) as opposed to fast or slow 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 shortcoming 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.

Adams et al. (1) recently showed that training using contractions that were isometric, lengthening, or shortening resulted in an equivalent hypertrophy in rats. The torque integrals for these three training modes were obviously quite different from each other. Despite similar degrees of hypertrophy, increases in mRNA expression for mechano-growth factor and insulin-like growth factor I (IGF-I), two proteins that have been implicated as playing a role in hypertrophic muscle growth (19), were increased only in the isometric and shortening contraction conditions (1). In humans, a single bout of lengthening resistive exercise resulted in a greater increase in IGF-I mRNA expression vs. a bout of shortening exercise (4). We observed, despite a >10-fold lower mean torque-time integral (Fig. 6), a greater degree of hypertrophy (Fig. 3) with a training protocol that involved only high velocity lengthening contractions. However, why we observed greater hypertrophy with Fast as opposed to Slow lengthening contractions when Adams et al. (1) observed quite similar hypertrophy with different contraction types and vastly dissimilar force-time integrals is not readily apparent. The difference in the model utilized in our study as opposed to that of Adams et al. may explain some of the differences: rats vs. humans, imposed vs. voluntary contractions, and the number of training bouts were greater in our study (24 vs. only 10 used by Adams et al.).



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  		Fig. 6. Torque tracings recorded during maximal torque testing Pre and Post training in an individual subject (study I). A: Fast-trained arm (torque-time integral 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.

 
Previously, our laboratory had labeled the ultrastructural observation of smeared or disrupted Z lines as muscle damage (5, 46), in accordance with others (15, 18, 39). Recently, it was reported that an acute bout of lengthening muscle actions, which would have resulted in severe muscle damage, resulted in no detectable disturbances of the myofiber protein structure (11). In fact, what we observed and labeled as Z-line streaming, and have previously called muscle damage (5, 46), has recently been reported not to be muscle damage but instead 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 contractions, 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 to the series of events outlined by Phillips (37), then this provides a basis for why we saw greater hypertrophy in the Fast-trained arms. Of course, we have no direct measurements 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). According 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 contralateral 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 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 effect for velocity (12, 36). Additionally, because the gains in maximal torque were greater in the Fast-trained arm, then any 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 a difference between the Fast and Slow arms in terms of strength gains is even more impressive and likely due to our use of a unilateral all-within-subject design.

The overall gains seen in maximal torque generation were quite moderate, and hence differences would have been more difficult to detect were they present. We suspect that the moderate strength gains may have been due to some residual fatigue from the training itself, despite several days of rest after the subjects' last training bout before strength assessment. In fact, Fig. 7 shows the mean peak torque on a week-to-week basis throughout the course of the study and shows that, during training, the weekly peak torque was actually depressed, likely as a result of muscle protein remodeling (see Ref. 50 for a review), for some time before recovering and eventually exceeding pretraining values only in the last week. This pattern of depressed force and yet substantial fiber remodeling, ultimately resulting in hypertrophy, is similar to that seen with chronic low-frequency stimulation in animals. In this model of extreme overload, force is persistently depressed, and yet fiber adaptations still occur while substantial fiber remodeling is still present (22). In two other studies in which differing lengthening velocities were used for training (12, 36), the gains in maximal torque were not large. For example, Paddon-Jones et al. (36) found no significant gains in maximal torque generation in a slow-trained arm performing lengthening contractions at 0.52 rad/s and a 5- to 10-N·m increase in the fast-trained (3.14 rad/s) arm. Farthing and Chilibeck (12) also reported the increments in maximal torque were in the range of 11–14 N·m.



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  		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 subjects. *Significantly different between Fast and Slow arms at the specified week, P < 0.05. a Different from week 1, P < 0.05. b Different from weeks 1–7, P < 0.05. c Different from week 7, P < 0.05.

 
Muscle fiber-type transitions that occur with resistance training have usually demonstrated a shift from IIx to IIa fibers (25, 42, 43). However, a recent observation of fiber-type distribution after fast lengthening training showed an increase in the percentage of type IIx fibers and a decrease in type I fibers found within muscle samples (36); on completion of the present study, no such changes were observed. In fact, a decrease was seen in type IIx fibers after both Fast and Slow lengthening training according to both mATPase histochemical and MHC gel electrophoretic analysis. Although the hypothesized concomitant increase in IIa fiber distribution was not seen, we did observe a significant increase in the total area occupied by type IIa fibers but in the Fast-trained arm only. A shift from IIx to IIa fibers was to be expected according to Andersen et al. (3), who hypothesized that the type IIx isoform is the "default" MHC that is expressed frequently in untrained subjects. However, when a resistance training protocol is implemented, the MHC isoforms shift toward an increase in type IIa fiber percent (25, 42, 43). Type IIa fibers, although they may have a lower maximal torque-generating capacity (29), do have a greater oxidative capacity, which confers on them a greater resistance to fatigue. Moreover, the increase fiber CSA of both the IIa and IIx fibers more than compensates for any small shift away from IIx to IIa.

To place our findings in some context with other resistance training protocols, it is interesting to note that the degree of hypertrophy we observed compared with other studies in which the elbow flexors have been trained have shown similar increases in muscle CSA (13), greater increases in CSA and individual muscle fiber area with longer training protocols (35, 38), or no change in fiber size-trained subjects who superimposed elbow flexor training on top of their normal routines (2). The increases in muscle CSA and fiber area that our laboratory and others have observed (13, 35, 38) tend to be larger than that seen in muscles such as the vastus lateralis (42, 43). Hence, our findings must be viewed in the context of a short-term training protocol of elbow flexor training and could differ if different subjects (i.e., trained) or muscles (i.e., lower body locomotor muscles) had been studied.

We observed that higher velocity (3.66 rad/s) isokinetic lengthening contractions are associated with greater muscular hypertrophy than slower (0.35 rad/s) velocity lengthening contractions. This finding occurred despite a >10-fold greater time under tension in the Fast- vs. the Slow-trained arms. We observed that acutely an isolated set of Fast contractions resulted in greater disruption to the muscle ultrastructure, which could be indicative of greater protein remodeling and potentially faster onset (34) and potentially a greater duration of protein synthesis. Over time, the greater protein synthesis may result in greater hypertrophy.


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This research was supported by a National Science and Engineering Research Council of Canada grant to S. M. Phillips. S. M. Phillips is the recipient of a Premier's Research Excellence Award and a Canadian Institutes of Health Research New Investigator Award.


   ACKNOWLEDGMENTS
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We thank the subjects for time and John Moroz for outstanding expertise in the set up and use of testing and training equipment.


   FOOTNOTES
 

Address for reprint requests and other correspondence: S. M. Phillips, Dept. of Kinesiology, IWC AB116, McMaster Univ., 1280 Main St. W., Hamilton, ON, Canada L8S 4K1 (E-mail: phillis{at}mcmaster.ca)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


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  1. Adams GR, Cheng DC, Haddad F, and Baldwin KM. Skeletal muscle hypertrophy in response to isometric, lengthening, and shortening training bouts of equivalent duration. J Appl Physiol 96: 1613–1618, 2004.[Abstract/Free Full Text]
  2. Alway SE, Grumbt WH, Stray-Gundersen J, and Gonyea WJ. Effects of resistance training on elbow flexors of highly competitive bodybuilders. J Appl Physiol 72: 1512–1521, 1992.[Abstract/Free Full Text]
  3. Andersen JL, Mohr T, Biering-Sorensen F, Galbo H, and Kjaer M. Myosin heavy chain isoform transformation in single fibres from m. vastus lateralis in spinal cord injured individuals: effects of long-term functional electrical stimulation (FES). Pflügers Arch 431: 513–518, 1996.[ISI][Medline]
  4. Bamman MM, Shipp JR, Jiang J, Gower BA, Hunter GR, Goodman A, McLafferty CL Jr, and Urban RJ. Mechanical load increases muscle IGF-I and androgen receptor mRNA concentrations in humans. Am J Physiol Endocrinol Metab 280: E383–E390, 2001.[Abstract/Free Full Text]
  5. Beaton LJ, Tarnopolsky MA, and Phillips SM. Contraction-induced muscle damage in humans following calcium channel blocker administration. J Physiol 544: 849–859, 2002.[Abstract/Free Full Text]
  6. Biolo G, Tipton KD, Klein S, and Wolfe RR. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol Endocrinol Metab 273: E122–E129, 1997.[Abstract/Free Full Text]
  7. Borsheim E, Tipton KD, Wolf SE, and Wolfe RR. Essential amino acids and muscle protein recovery from resistance exercise. Am J Physiol Endocrinol Metab 283: E648–E657, 2002.[Abstract/Free Full Text]
  8. Clarkson PM and Hubal MJ. Exercise-induced muscle damage in humans. Am J Phys Med Rehabil 81: S52–S69, 2002.[CrossRef][ISI][Medline]
  9. Colliander EB and Tesch PA. Effects of eccentric and concentric muscle actions in resistance training. Acta Physiol Scand 140: 31–39, 1990.[ISI][Medline]
  10. Colliander EB and Tesch PA. Effects of detraining following short term resistance training on eccentric and concentric muscle strength. Acta Physiol Scand 144: 23–29, 1992.[ISI][Medline]
  11. Crameri RM, Langberg H, Magnusson P, Jensen CH, Schroder HD, Olesen JL, Suetta C, Teisner B, and Kjaer M. Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J Physiol 558: 333–340, 2004.[Abstract/Free Full Text]
  12. Farthing JP and Chilibeck PD. The effect of eccentric training at different velocities on cross-education. Eur J Appl Physiol 89: 570–577, 2003.[CrossRef][ISI][Medline]
  13. Farthing JP and Chilibeck PD. The effects of eccentric and concentric training at different velocities on muscle hypertrophy. Eur J Appl Physiol 89: 578–586, 2003.[CrossRef][ISI][Medline]
  14. Faulkner JA. Terminology for contractions of muscles during shortening, while isometric, and during lengthening. J Appl Physiol 95: 455–459, 2003.[Abstract/Free Full Text]
  15. Friden J, Sjöstrom M, and Ekblom B. Myofibrillar damage following intense eccentric exercise in man. Int J Sports Med 4: 170–176, 1983.[ISI][Medline]
  16. Fry AC, Allemeier CA, and Staron RS. Correlation between percentage fiber type area and myosin heavy chain content in human skeletal muscle. Eur J Appl Physiol 68: 246–251, 1994.
  17. Gibala MJ, Interisano SA, Tarnopolsky MA, Roy BD, MacDonald JR, Yarasheski KE, and MacDougall JD. Myofibrillar disruption following acute concentric and eccentric resistance exercise in strength-trained men. Can J Physiol Pharmacol 78: 656–661, 2000.[CrossRef][ISI][Medline]
  18. Gibala MJ, MacDougall JD, Tarnopolsky MA, Stauber WT, and Elorriaga A. Changes in human skeletal muscle ultrastructure and force production after acute resistance exercise. J Appl Physiol 78: 702–708, 1995.[Abstract/Free Full Text]
  19. Goldspink G. Changes in muscle mass and phenotype and the expression of autocrine and systemic growth factors by muscle in response to stretch and overload. J Anat 194: 323–334, 1999.
  20. Green H, Goreham C, Ouyang J, Ball-Burnett M, and Ranney D. Regulation of fiber size, oxidative potential, and capillarization in human muscle by resistance exercise. Am J Physiol Regul Integr Comp Physiol 276: R591–R596, 1999.[Abstract/Free Full Text]
  21. Hather BM, Tesch PA, Buchanan P, and Dudley GA. Influence of eccentric actions on skeletal muscle adaptations to resistance training. Acta Physiol Scand 143: 177–185, 1991.[ISI][Medline]
  22. Hicks A, Ohlendieck K, Gopel SO, and Pette D. Early functional and biochemical adaptations to low-frequency stimulation of rabbit fast-twitch muscle. Am J Physiol Cell Physiol 273: C297–C305, 1997.[Abstract/Free Full Text]
  23. Higbie EJ, Cureton KJ, Warren GL, and Prior BM. Effects of concentric and eccentric training on muscle strength, cross-sectional area, and neural activation. J Appl Physiol 81: 2173–2181, 1996.[Abstract/Free Full Text]
  24. Hortobagyi T, Barrier J, Beard D, Braspennincx J, Koens P, Devita P, Dempsey L, and Lambert J. Greater initial adaptations to submaximal muscle lengthening than maximal shortening. J Appl Physiol 81: 1677–1682, 1996.[Abstract/Free Full Text]
  25. Hortobagyi T, Dempsey L, Fraser D, Zheng D, Hamilton G, Lambert J, and Dohm L. Changes in muscle strength, muscle fibre size and myofibrillar gene expression after immobilization and retraining in humans. J Physiol 524: 293–304, 2000.[Abstract/Free Full Text]
  26. Hortobagyi T, Devita P, Money J, and Barrier J. Effects of standard and eccentric overload strength training in young women. Med Sci Sports Exerc 33: 1206–1212, 2001.[CrossRef][ISI][Medline]
  27. Hortobagyi T, Hill JP, Houmard JA, Fraser DD, Lambert NJ, and Israel RG. Adaptive responses to muscle lengthening and shortening in humans. J Appl Physiol 80: 765–772, 1996.[Abstract/Free Full Text]
  28. Jones DA and Rutherford OM. Human muscle strength training: the effects of three different regimens and the nature of the resultant changes. J Physiol 391: 1–11, 1987.[Abstract/Free Full Text]
  29. Larsson L, Edstrom L, Lindegren B, Gorza L, and Schiaffino S. MHC composition and enzyme-histochemical and physiological properties of a novel fast-twitch motor unit type. Am J Physiol Cell Physiol 261: C93–C101, 1991.[Abstract/Free Full Text]
  30. Lastayo PC, Pierotti DJ, Pifer J, Hoppeler H, and Lindstedt SL. Eccentric ergometry: increases in locomotor muscle size and strength at low training intensities. Am J Physiol Regul Integr Comp Physiol 278: R1282–R1288, 2000.[Abstract/Free Full Text]
  31. Mayhew TP, Rothstein JM, Finucane SD, and Lamb RL. Muscular adaptation to concentric and eccentric exercise at equal power levels. Med Sci Sports Exerc 27: 868–873, 1995.[ISI][Medline]
  32. McCall GE, Byrnes WC, Dickinson A, Pattany PM, and Fleck SJ. Muscle fiber hypertrophy, hyperplasia, and capillary density in college men after resistance training. J Appl Physiol 81: 2004–2012, 1996.[Abstract/Free Full Text]
  33. Moore DR, Burgomaster KA, Schofield LM, Gibala MJ, Sale DG, and Phillips SM. Neuromuscular adaptations in human muscle following low intensity resistance training with vascular occlusion. Eur J Appl Physiol 92: 399–406, 2004.[CrossRef][ISI][Medline]
  34. Moore DR, Phillips SM, Babraj JA, Smith K, and Rennie MJ. Myofibrillar and collagen protein synthesis in human skeletal muscle after maximal shortening and lengthening contractions. Am J Physiol Endocrinol Metab. In press.
  35. O'Hagan FT, Sale DG, MacDougall JD, and Garner SH. Response to resistance training in young women and men. Int J Sports Med 16: 314–321, 1995.[ISI][Medline]
  36. Paddon-Jones D, Leveritt M, Lonergan A, and Abernethy P. Adaptation to chronic eccentric exercise in humans: the influence of contraction velocity. Eur J Appl Physiol 85: 466–471, 2001.[CrossRef][ISI][Medline]
  37. Phillips SM. Protein requirements and supplementation in strength sports. Nutrition 20: 689–695, 2004.[CrossRef][ISI][Medline]
  38. Roman WJ, Fleckenstein J, Stray-Gundersen J, Alway SE, Peshock R, and Gonyea WJ. Adaptations in the elbow flexors of elderly males after heavy-resistance training. J Appl Physiol 74: 750–754, 1993.[Abstract/Free Full Text]
  39. Roth SM, Martel GF, Ivey FM, Lemmer JT, Tracy BL, Hurlbut DE, Metter EJ, Hurley BF, and Rogers, MA. Ultrastructural muscle damage in young vs. older men after high-volume, heavy-resistance strength training. J Appl Physiol 86: 1833–1840, 1999.[Abstract/Free Full Text]
  40. Seger JY, Arvidsson B, and Thorstensson A. Specific effects of eccentric and concentric training on muscle strength and morphology in humans. Eur J Appl Physiol Occup Physiol 79: 49–57, 1998.[CrossRef][ISI][Medline]
  41. Shima N, Ishida K, Katayama K, Morotome Y, Sato Y, and Miyamura M. Cross education of muscular strength during unilateral resistance training and detraining. Eur J Appl Physiol 86: 287–294, 2002.[CrossRef][ISI][Medline]
  42. Staron RS, Karapondo DL, Kraemer WJ, Fry AC, Gordon SE, Falkel JE, Hagerman FC, and Hikida RS. Skeletal muscle adaptations during early phase of heavy-resistance training in men and women. J Appl Physiol 76: 1247–1255, 1994.[Abstract/Free Full Text]
  43. Staron RS, Leonardi MJ, Karapondo DL, Malicky ES, Falkel JE, Hagerman FC, and Hikida RS. Strength and skeletal muscle adaptations in heavy-resistance-trained women after detraining and retraining. J Appl Physiol 70: 631–640, 1991.[Abstract/Free Full Text]
  44. Stewart BG, Tarnopolsky MA, Hicks AL, McCartney N, Mahoney DJ, Staron RS, and Phillips SM. Treadmill training-induced adaptations in muscle phenotype in persons with incomplete spinal cord injury. Muscle Nerve 30: 61–68, 2003.[CrossRef]
  45. Stupka N, Lowther S, Chorneyko K, Bourgeois JM, Hogben C, and Tarnopolsky MA. Gender differences in muscle inflammation after eccentric exercise. J Appl Physiol 89: 2325–2332, 2000.[Abstract/Free Full Text]
  46. Stupka N, Tarnopolsky MA, Yardley NJ, and Phillips SM. Cellular adaptation to repeated eccentric exercise-induced muscle damage. J Appl Physiol 91: 1669–1678, 2001.[Abstract/Free Full Text]
  47. Tesch PA, Ekberg A, Lindquist DM, and Trieschmann JT. Muscle hypertrophy following 5-week resistance training using a non-gravity-dependent exercise system. Acta Physiol Scand 180: 89–98, 2004.[CrossRef][ISI][Medline]
  48. Tipton KD, Borsheim E, Wolf SE, Sanford AP, and Wolfe RR. Acute response of net muscle protein balance reflects 24-h balance after exercise and amino acid ingestion. Am J Physiol Endocrinol Metab 284: E76–E89, 2003.[Abstract/Free Full Text]
  49. Wang N, Hikida RS, Staron RS, and Simoneau JA. Muscle fiber types of women after resistance training—quantitative ultrastructure and enzyme activity. Eur J Appl Physiol 424: 494–502, 1993.
  50. Warren GL, Ingalls CP, Lowe DA, and Armstrong RB. Excitation-contraction uncoupling: major role in contraction-induced muscle injury. Exerc Sport Sci Rev 29: 82–87, 2001.[CrossRef][Medline]
  51. Yu JG, Carlsson L, and Thornell LE. Evidence for myofibril remodeling as opposed to myofibril damage in human muscles with DOMS: an ultrastructural and immunoelectron microscopic study. Histochem Cell Biol 121: 219–227, 2004.[CrossRef][ISI][Medline]
  52. Yu JG and Thornell LE. Desmin and actin alterations in human muscles affected by delayed onset muscle soreness: a high resolution immunocytochemical study. Histochem Cell Biol 118: 171–179, 2002.[CrossRef][ISI][Medline]



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