CME. Triceps Brachii Strength and Regional Body Composition Changes After Detraining Quantified by MRI. Original Research

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1 CME JOURNAL OF MAGNETIC RESONANCE IMAGING 33: (2011) Original Research Triceps Brachii Strength and Regional Body Composition Changes After Detraining Quantified by MRI Jelena Z. Popadic Gacesa, MD, PhD, 1 * Kozic B. Dusko, MD, PhD, 2 and Nikola G. Grujic, MD, PhD 1 Purpose: To determine the triceps brachii functional adaptation and regional body composition changes after 12 months of detraining. Materials and Methods: Seventeen healthy young men ( y, body mass index kg/m 2 ) were put in the detraining regimen for 12 months after completing a 12-week exercise protocol on isoacceleration dynamometer (5 times a week, 5 daily series with 10 maximal elbow extensions, 1 min rest between sets). Triceps brachii muscle strength was measured by isoacceleration dynamometry, using identical protocol as during the training. Muscle volumes, subcutaneous adipose tissue (SCAT), and intermuscular adipose tissue (IMAT) at midhumerus were assessed by using MRI. Results: Long-term detraining resulted in the significant decrease of 17% and 19% in endurance strength and fatigue rate, respectively. Maximal muscle strength slightly changed, and its 4% decrease was not significant. Triceps brachii volumes of both arms returned to their pretraining values ( cm 3 for right arm, and cm 3 for left arm). IMAT depots in upper arm significantly increased by 14% after 12 months of detraining, when compared with baseline values (P < 0.05). Conclusion: Long-term detraining leads to triceps brachii adaptation with endurance strength decrease, volume return to its baseline values, and significant IMAT accumulation. IMAT values after 12 months of detraining exceed baseline, pretraining values, which is significant accumulation as a result of physiologically decreased muscle activity. 1 Laboratory for Functional Diagnostics, Department of Physiology, Medical School, University of Novi Sad, Serbia. 2 Centre for Imaging Diagnostics, Institute of Oncology, Sremska Kamenica, Serbia. Contract grant sponsor: the Provincial Secretariat for Science and Technological Development, Autonomous Province of Vojvodina, Serbia; Contract grant number: Responses of the Human Body to Physical Stress and Limits of Compensatory Mechanisms # / *Address reprint requests to: J.Z.P.G., Department of Physiology, Medical School, University of Novi Sad, 3, Hajduk Veljko St., Novi Sad, Serbia. jpopadic@uns.ac.rs Received November 18, 2010; Accepted February 9, DOI /jmri View this article online at wileyonlinelibrary.com. Key Words: MRI; detraining; intermuscular adipose tissue; skeletal muscle J. Magn. Reson. Imaging 2011;33: VC 2011 Wiley-Liss, Inc. LONG-TERM DETRAINING is defined as a period of more than 4 weeks of insufficient training stimuli (1). Cessation of physical activity detraining is typically associated with a diminished physiological function of a muscle, as a result of morphological and neural strength component changes. There are numerous reports concerning the reduction in maximal voluntary muscle strength after detraining (2 4). In contrast, some studies have reported partially preserved gains in dynamic muscle strength when resistance training was followed by 6 12 weeks (5,6) and even weeks of detraining (7,8). Long-term detraining has been known to decrease muscle fiber cross-sectional areas (3,9 11), muscle mass (9,10,12), and lean body mass (13) in trained and untrained individuals. Regional body composition changes as a result of programmed physical activity or decreased activity, detraining, include not only muscle, but also an adipose tissue (AT) changes. One less-well studied depot is the AT that lies below the subcutaneous adipose tissue (SCAT) fascial plane, called intermuscular adipose tissue (IMAT) (14,15). It was also observed that the amount of this tissue decreased significantly after diet and exercise protocols. In the case of inactivity or immobilization (16), the significant accumulation of this tissue has been observed, together with muscle strength decrease. Imaging methods such as computerized tomography and MRI have been used to quantify muscle volume accurately (17 21). The use of MRI in evaluation of muscle volumes and quantifying IMAT depot allows researchers to determine the morphological adaptation of skeletal muscles and regional body composition changes as a result of programmed physical activity or decreased activity in detraining. Functional and morphological adaptation changes of triceps brachii after 6 and 12 weeks of maximal, self-perceived resistance training have been recently reported (21,22). The extent of regional body VC 2011 Wiley-Liss, Inc. 1114

2 Triceps Brachii Muscle and Fat Changes 1115 composition changes, as well as decrease in functional muscle properties in healthy young nonathletes as a result of long-term detraining remained unknown. Therefore, the aim of this study was to determine the triceps brachii functional adaptation changes and regional body composition changes as a result of 12 months of detraining, after completing a 12-week training protocol of elbow extensors. MATERIALS AND METHODS Subjects Seventeen healthy young men ( years, body weight kg, body height cm, body mass index kg/m 2 ), who did not take part in any formal resistance exercise regimen for 12 months after completing 12-week exercise protocol, volunteered for this study. All subjects were given an oral and written explanation of the study before signing a written informed consent form. The study was approved by the Research Ethics Committee and the investigation was performed according to the principles outlined in the Declaration of Helsinki. Muscle Volume Measurements A series of cross-sectional images of the triceps brachii muscles were obtained by MRI scans with an extremity coil on the Magnetom Avanto TIM Siemens, 1.5 Tesla (T) (Siemens, Erlangen, Germany). Multislice sequences of T1-weighted, flash (gradient echo) axial images of both arms were obtained, starting from the humerus head to the medial epicondiles, and each arm was imaged separately. MRI parameters were: repetition time (TR), 232 ms; echo time (TE), 4.76 ms; field of view (FOV), mm; and the matrix size; Slice thickness was 10 mm with an interslice interval of 3 mm. Data processing was conducted using the Medical Image Processing, Analysis and Visualization (MIPAV) software, version 2.6 (Center for Information Technology, National Institutes of Health, Bethesda, MD). The MIPAV software was used to analyze images on a personal computer workstation (23). This program calculates the surface area (in mm 2 ) of the manually selected region of interest (i.e., triceps brachii CSA) in every axial image from the first section closest to the superior border of the humerus to a point where the muscle group is no longer reliably distinguishable (24,25). The same number of sections distal from the humerus was measured for a particular subject before, after 12 weeks of training, and after 12 months of detraining, to ensure within subject measurement replication. The biceps brachii and brachialis muscle CSA were analyzed simultaneously on each slice. All sequences were analyzed by the same person (J.P.G.). The investigator was blinded to subject identification, date of scan, and training status, for both baseline, after training and detraining analyses. The intraclass correlation coefficient for repeated measurements was Cronbach s a reliability coefficient for repeated measures on the same Figure 1. Preprocessed image of a slice located at mid-humerus. After determining gray-level intensity (threshold value) of the adipose tissue, and removing the bone and subcutaneous adipose tissue, values of IMAT were calculated before training, after 12 weeks of triceps brachii strength training, and after 12 months of detraining. participant was 0.98 for triceps brachii, 0.96 for biceps brachii, and 0.93 for brachialis muscle. The final muscle volume (V m ) was calculated using the truncated cone formula, as previously reported (20). IMAT and SCAT Measurements In every MRI sequence, slice from mid-arm was chosen for IMAT calculation. Mid-arm was determined by mid-humeral diaphysis calculation (from scout image). MIPAV was also used to analyze images on a personal computer workstation (23). IMAT was defined as the visible high-signal intensity (light) pixels between muscle groups and within muscle fascia. We used a modified version of previously described strategies for measuring adipose tissue (16,24 26). We first used a well-established nonparametric nonuniform intensity normalization (N3) algorithm that corrects smoothly varying shading caused by poor radiofrequency coil uniformity or gradient-driven eddy currents (27). Next, bone was removed and a rectangular region of interest has been drawn containing 50% muscle and 50% subcutaneous adipose tissue. The rectangles were placed at seven different areas around the upper arm producing seven bimodal distributions of muscle and subcutaneous fat signal intensity peaks. The average gray-level intensity (threshold value) of the adipose tissue in the SCAT region was determined and used as a reference. This threshold value was reduced by 20% to identify the IMAT threshold (20). For every participant, three IMAT values were obtained, before the training, after 12 weeks of strength training and 12 months after cessation of training. All images were read in random order, and one investigator (J.P.G.) performed the analysis (see

3 1116 Popadic Gacesa et al. All data were presented as mean 6 SD unless otherwise indicated. The difference in muscle volumes between left and right arm, as well as in the volume change between left and right arm were assessed using Wilcoxon s test. All measured variables were compared with those measured before training baseline values, after training, and after detraining using analysis of variance. Pearson s correlation coefficient was used to assess the relationship between muscle volumes and strength parameters. Statistical significance was indicated if P < All calculations were performed using SPSS, version 10.0 (SPSS, Inc., Chicago, IL). Figure 2. Strength parameters after 12 months of detraining following a 12-week period of strength training and baseline values. Fig. 1). The technical error of identifying the signal intensity threshold, which allows separation of fat from muscle, was CV ¼ 2.7%. Dynamometry Measurements and Training Protocol Strength measurements were performed on the isoacceleration dynamometer Concept 2 Dyno (Concept 2, Inc. Morrisville, VT). Each participant performed five sets of 10 maximal elbow extensions following 15 min of a general warm-up, with a 1-min resting period between each set. The measurements were the same as daily training sessions, as previously reported (22). The training protocol lasted for 12 weeks, with a frequency of five sessions per week. Each training session included five sets of 10 maximal elbow extensions following 15 min of an identical general warmup. A 1-min resting period was allowed between each set. Each contraction was performed in the sitting bench press position with the full elbow extension of both arms against the resistance to maintain a central acceleration during the whole range of movement. Training sessions were monitored to precisely measure load of each contraction daily throughout training. Training was individually dosed, as each participant performed maximally according to personal perception. Maximal strength (MS) was defined as the highest daily scored result in Newtons (N). Endurance strength (ES) was calculated as a mean value of all 50 repetitions (expressed in N). Fatigue rate (FR) was defined as difference in the average values of muscle strength between the first and fifth training series, calculated as the percentage ratio of the fifth training series in the first one. RESULTS Muscle Strength Changes The average decrease in upper arm extensors ES was 17% after detraining (from N after training to N in detraining), but it was still 40% higher than before training ( N) (P < 0.01). MS decreased only 4% compared with values after the training and it was not significant (from N after the training to N) (P > 0.05). The values were 24% higher than before training (pretraining values were N) (P < 0.01). The difference between the first and the last series (FR) changed from N after the training to N after detraining, P < The percentage ratio of the fifth training series in the first one decreased from 90% at the end of the 12 weeks of training to 71% in detraining. Still, it was better than pretraining value of 55% (Fig. 2). The trend of the muscle strength averages in all five series before the training, at the end of training and after a 12 month of detraining is presented in Figure 3. Muscle Volumes Following 12 months of detraining, the volume of triceps brachii muscle (V m ) decreased by 8% compared with values after the training, and returned to its pretraining values, from to cm 3 (pretraining cm 3 ) for the right, and by 7.8%, from to cm 3 (pretraining ) for the left arm (P < 0.01). After detraining no significant difference was found Statistical Analysis Figure 3. Average triceps muscle strength values trend in five sets of repetition after 12 months of detraining (compared with the same values before and after the training). Diamonds ¼ pretraining; triangles ¼ after 12 weeks of training; squares ¼ after 12 months of detraining.

4 Triceps Brachii Muscle and Fat Changes 1117 Table 1 IMAT and SCAT Values in 17 non-athletes Prior to the Training, After 12 Weeks of Maximal Strength Training, and After 12 Months of Consequent Detraining BMI (kg/m 2 ) SCAT (cm 2 ) IMAT (cm 2 ) % IMAT Pre-training After training b b After detraining a a a P < P < between left and right arm in the upper arm extensor volumes, nor in the V m decrease. The volumes of antagonistic muscles (m. biceps brachii and m. brachialis) did not change significantly after detraining compared with pretraining values and values after 12 weeks of training (P > 0.05). A nonsignificant difference was found between left and right arm of the antagonist muscles as well (P > 0.05). IMAT and SCAT Changes Values of IMAT and SCAT before training, after completing 12 weeks of training and after 12 months of detraining are presented in Table 1. It is noticeable that IMAT decreased significantly after 12 weeks of training (P < 0.01). After 12 months of detraining, IMAT accumulation increased significantly compared with posttraining, as well as pretraining values (P < 0.05). The percentage of IMAT in the upper arm muscle CSA (% IMAT) decreased significantly compared with the posttraining, as well as the pretraining values (P < 0.05). SCAT did not change significantly after training, nor after long-term detraining (P > 0.05). Correlations The MS and ES were highly correlated with the volume of m. triceps brachii after 12 months of detraining (r 2 ¼ 0.82, r 2 ¼ 0.70, P < 0.01). There was no significant correlation between V m and the FR after detraining (r 2 ¼ 0.21, P > 0.05). Significant negative correlation has been observed between triceps volume increase after training and triceps volume decrease after detraining (when comparing with the pretraining values), r 2 ¼ 0.44, P < Significant correlation was registered between the decrease in endurance strength and decrease in triceps brachii volume as a result of long-term detraining (r ¼ 0.547, P < 0.05) (see Fig. 4). There was no significant correlation between muscle volumes and IMAT before, after the training and after detraining, as well (P > 0.05). There was no significant correlation found between maximal muscle strength and IMAT for baseline, posttraining and detraining values (r ¼ 0.01, 0.20, and 0.31, respectively). Also, there was no significant correlation between endurance strength and IMAT before, after training and after detraining (r ¼ 0.02, 0.13, and 0.28, respectively). However, the positive correlation has been established between change in fatigue rate and change in IMAT before and after the training (r ¼ 0.41, P < 0.05), and between change in fatigue rate and change in IMAT before training and after detraining (r ¼ 0.43; P < 0.05), as well. DISSCUSION The aim of this study was to determine upper arm extensors functional and morphological changes as a result of 12 months of detraining, after completing 12 weeks of maximal, self-perceived strength training. Additionally, we investigated changes in adipose tissue depots: subcutaneous and intermuscular adipose tissue CSA in upper arm (SCAT and IMAT). Long-term detraining resulted in endurance strength and fatigue rate decrease. Maximal muscle strength slightly changed, and its 4% decrease was not significant. Triceps brachii volumes of both arms returned to their pretraining values. Adipose tissue depots in muscles changed significantly as a result of increased or decreased muscle activity. Triceps brachii muscle strength partially changed after 12 months of detraining. The parameter of maximal muscle strength stayed preserved after long-term cessation of physical activity, while endurance muscle strength and fatigue rate decreased significantly, by 17% and 19%, respectively. No significant decrease in Figure 4. Correlation between triceps brachii volumes for both arms and endurance muscle strength (ES) after training and consequent detraining in nonathletes

5 1118 Popadic Gacesa et al. elbow extensors maximal strength may be explained by the learning effect, because all training sessions have been identical as were testing sessions for muscle strength measurements (using the same methodology and equipment). There are numerous factors that influence muscle strength, and muscle volume is only one of them. Partial or complete preservation of muscle strength after some period of detraining has been observed by many researchers (4,8,28) and it can be explained by some neural influences. Repetition of the same movement during training and testing sessions (when performed on the identical training and testing device) is a part of learning effect in central nervous system that leads to preservation of muscle strength even after a longer period of decreased muscle activity, detraining (29). Previous investigations reported that strength in young men (4,7) can be maintained from 4 to 32 weeks following the training. The force production of strength-trained athletes has been shown to decline by only 7 to 12% during inactivity periods ranging from 8 to 12 weeks (2,9,11). This force decline appears to be related to a decreased electromyogram activity, (2,11) in addition to the above mentioned reductions in fiber areas and muscle mass. High percentages of recently acquired strength gains are also maintained for at least 12 weeks, despite the discontinuation of training (3,4,8,28,30 33). Of interest, it has been suggested that performing eccentric muscle actions during training is essential to promote greater and longer lasting neural adaptations to training (4). Andersen and associates discovered that quadriceps femoris eccentric strength gains were fully preserved after 3 months of detraining; however, the concentric muscle strength, which had also increased after 3 months of resistance training, decreased to pretraining levels (34). Of interest, the strength decrease after detraining registered throughout all five series shows similar trendline function as before the training (Fig. 3). Muscle strength decrease during five testing series after detraining has been significantly higher than after the completion of training. This suggests that, although maximal muscle strength is preserved, the endurance and fatigability have returned to their pretraining values. Our study showed that triceps brachii muscle volumes of both arms, after initial 8% increase as a result of a 12-week maximal, self-perceived resistance training, decreased to pretraining values after a 12- month detraining period. Other researches mostly report data for CSA changes and some of them showed similar results. Andersen et al (34) found that m. quadriceps femoris CSA at mid-femur increased by 10% after 3 months of resistance training, and muscle CSA decreased to pretraining levels after 3 months of detraining. Narici et al (3) found decrease in quadriceps mean CSA after long-term detraining in previously untrained individuals. Smith and Stransky (13) also reported decrease in muscle mass in young women after detraining. Correlation between muscle volume and strength remained significant after long-term detraining. We also found that decrease in triceps brachii volume after detraining is in significant positive correlation with the decrease in endurance strength, compared with its posttraining values. These findings indicate that endurance strength parameter changes after the cessation of physical activity can be explained partially by the muscle volume loss. At the same time, maximal muscle strength change did not correlate with triceps brachii volume decrease, because other factors influence this muscle strength parameter. Significant negative correlation has been observed between triceps volume increase after training and triceps volume decrease after detraining. It is noticeable that muscle volume increase throughout training and its decrease after training cessation does not show identical mathematical function and dynamics. There are few possible explanations. The muscles that hypertrophied in higher extent showed higher adaptation capacity and therefore decrease was lower, when compared with pretraining values. Before training our participants had different volumes of triceps brachii. If some of them had some previous muscle activity in the past, their starting volumes will be bigger, and volume increase will be smaller. Situation can be similar with detraining, as well. Also, it must be emphasized that this correlation is significant, but not highly. In our study, there are significant changes in IMAT after training and consequent long-term detraining. We discovered that 12 weeks of training led to significant decrease of 16% in upper arm IMAT. Reduction of physical activity for 12 months, long-term detraining, had significantly increased regional IMAT accumulation in healthy, previously untrained young males. This accumulation exceeded baseline values, measured before training activity, by 14%. These findings indicate that the decrease in muscle activity (detraining) after the increased activity (strength training) significantly accumulates IMAT to a similar extent as when it occurs after a short immobilization. This increased accumulation is also observed through the increase in IMAT related to skeletal muscle CSA. Changes in subcutaneous adipose tissue were not observed and it was in agreement with other researchers (16). Because most researches on the morphologic changes that occur with the reductions in physical activity focus on muscle mass, the accumulation of IMAT after detraining has not been clearly studied in healthy young, previously untrained adults. There are several reports about IMAT changes after a period of inactivity. Two studies showed increased levels of subcutaneous adipose tissue after 30 d of immobilization (plaster casting) and 42 d of bed rest in healthy males (35,36). Increase in thigh IMAT was observed 8 y after a spinal cord injury, when compared with weight-matched healthy control subjects (37). Manini and associates (16) added to these models, without pathological interference, that 4 weeks of reduced activity (leg immobilization) in healthy young men and women causes substantial (15 20%) increases in IMAT without changes in subcutaneous adipose tissue.

6 Triceps Brachii Muscle and Fat Changes 1119 Our data suggest that decreased muscle activity after increased activity, detraining, leads to IMAT increased accumulation compared with baseline values. Mechanism that can explain this phenomenon is probably similar to the one explained in the literature, which directly suggests altered fat oxidation as being responsible for inactivity-induced IMAT accumulation (16,38,39). The accumulation of IMAT after a reduction in activity arises from either an excess triacylglycerol influx from the vasculature or altered fat oxidation in the muscle. Recent evidence suggests that physical inactivity blocks the uptake of plasma triacylglycerols by down-regulating lipoprotein lipase activity, which directly implicates altered fat oxidation as being responsible for inactivity-induced IMAT accumulation (16,38,39). The larger increase in IMAT relative to muscle loss supports a shift in fuel metabolism away from lipid toward glucose usage commonly observed after inactivity (16). Nonexistence of significant correlation between maximal muscle strength and IMAT in our participants can be explained by the fact that physiological fat accumulation does not influence maximal muscle strength or its changes, as it may be in the pathological cases (16). There has been some positive correlation between IMAT change and fatigue rate change before and after the training, and before training and after detraining as well. Similar correlation has not been established for maximal and endurance strength change in our participants. This positive relation between functional muscle properties and IMAT can be explained by the fact that IMAT accumulation in a muscle can lead to its increased fatigability. Decrease in muscle functional properties may be due to change in metabolic function and, as suggested by Manini and associates, due to an increase in IMAT that provides an inhospitable environment for contractile dysfunction (16). However, the reduction in activity in previous studies was extreme and/or combined with pathological conditions. On the other hand, our results show IMAT changes in young, healthy adults with decreased muscle activity after previously increased activity, but within the physiological boundaries. It certainly suggests that physical activity levels are involved in the etiology of IMAT, but further work is needed to verify this hypothesis. The current study provides new data on effects of long-term decreased activity, detraining, in the general population that may involve in short-term training, especially using MRI in quantifying a depot of fat that is commonly associated with insulin resistance and glucose intolerance in different clinical population. 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