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árka
Mierisová2,1 The Robert Steiner Magnetic Resonance Unit, Imperial College School of Medicine, Hammersmith Hospital, London W12 0HS, United Kingdom; and 2 Wihuri Research Institute, 00140 Helsinki, Finland
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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We used 1H-magnetic resonance spectroscopy to noninvasively determine total creatine (TCr), choline-containing compounds (Cho), and intracellular (IT) and extracellular (between-muscle fibers) triglycerides (ET) in three human skeletal muscles. Subjects' (n = 15 men) TCr concentrations in soleus [Sol; 100.2 ± 8.3 (SE) mmol/kg dry wt] were lower (P < 0.05) than those in gastrocnemius (Gast; 125.3 ± 9.2 mmol/kg dry wt) and tibialis anterior (TA; 123.7 ± 8.8 mmol/kg dry wt). The Cho levels in Sol (35.8 ± 3.6 mmol/kg dry wt) and Gast (28.5 ± 3.5 mmol/kg dry wt) were higher (P < 0.001 and P < 0.01, respectively) compared with TA (13.6 ± 2.4 mmol/kg dry wt). The IT values were found to be 44.8 ± 4.6 and 36.5 ± 4.2 mmol/kg dry wt in Sol and Gast, respectively. The IT values of TA (24.5 ± 4.5 mmol/kg dry wt) were lower than those of Sol (P < 0.01) and Gast (P < 0.05). There were no differences in ET [116.0 ± 11.2 (Sol), 119.1 ± 18.5 (Gast), and 91.4 ± 19.2 mmol/kg dry wt (TA)]. It is proposed that the differences in metabolite levels may be due to the differences in fiber-type composition and deposition of metabolites due to the adaptation of different muscles during locomotion.
free creatine; lipids; magnetic resonance spectroscopy; phosphocreatine
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INTRODUCTION |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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LEVELS OF ENDOGENOUS metabolites in human muscle are determined primarily through the biochemical analyses of muscle biopsies (5, 11, 18, 20, 22). Limitations of using these techniques include the difficulty in obtaining biopsy samples from deep muscles and a large variability in the results (40). More recently, magnetic resonance spectroscopy (MRS) techniques have been utilized to noninvasively quantitate levels of high-energy phosphates by using 31P-MRS (9, 10, 17), total creatine (TCr) with 1H-MRS (8, 30), glycogen with 13C-MRS (1, 35), and lipids again by using 1H-MRS (6, 30, 33). The advantages of the MRS techniques over the biopsy technique are that it is possible to select volumes of interest at different regions within a given muscle, as well as different muscle groups, and the results obtained show less variability (6, 30, 35). Previously, other investigators (27, 29) had observed quantitative differences in the levels of high-energy phosphates in animal muscles by using 31P-MRS. In addition, Boesch et al. (6), using 1H-MRS, showed qualitative differences of intracellular lipids in a number of human muscles. However, we are not aware of any study that has noninvasively determined quantitative differences in TCr and intracellular (IT) and extracellular triglycerides (ET) in human muscles. In the present study, we used 1H-MRS to quantitate individual levels of TCr, choline-containing compounds (Cho), IT, and ET in three different human muscles.
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METHODS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects
Fifteen male subjects (age range: 25-53 yr) participated in this study. Subjects' activity levels ranged from sedentary to highly trained. Subjects were informed of the experimental procedures, and written informed consent was obtained. This study was approved by the Ethics Committee of the Royal Postgraduate Medical School, Hammersmith Hospital, London (Rec. 96/5030).Magnetic Resonance (MR) Measurements
MR imaging and MRS. Imaging and spectroscopy data were acquired on a 1.5-T Picker prototype system by using a quadrature birdcage coil of 30-cm diameter. In each examination, subjects lay in a supine position with the left leg placed along the axis of the coil and immobilized by firm padding. The right leg was supported outside the coil. Transverse relaxation time-weighted MR images (repetition time 300, echo time 30 ms) were acquired to determine the placement of the 1H-MRS voxels, with a slice thickness of 10 mm, a 14-cm field of view, and 128 × 256 data matrix. Spectra were obtained from the soleus (Sol), medial gastrocnemius (Gast), and tibialis anterior (TA) muscles of the left leg, using a point-resolved spectroscopy sequence (7) with a repetition time-to-echo time ratio of 1,500/135 ms and an 8-cm3 voxel positioned within each of the muscles examined. The number of signal averages was 256, and the spectral collection time was 6.4 min.
Data analysis. The analyses of in vivo 1H-MRS data of calf muscle were performed in the time domain directly on free induction decays (FIDs). The water peaks were mathematically removed from the measured FIDs by means of Hankel Lanczos single-variable decomposition (HLSVD) (38), and then the signals free from the water resonances were analyzed by the variable projection method (VARPRO) (39). Six resonances, i.e., choline (Cho), TCr [free creatine (Cr) + phosphocreatine (PCr)], ET -(CH2)n- and -CH3- and IT -(CH2)n- and -CH3, were described by six Gaussian decaying sinusoids corresponding to six Gaussian peaks in the frequency domain. The Lorentzian line shape was also examined, but the fits were not as good as those obtained by using the Gaussian line shape. This finding was also confirmed by visual inspection of all the spectra from different muscles and different subjects. To increase the reliability of the fitted parameters, prior knowledge (16, 39) of the model parameters was incorporated.
The prior knowledge for the triglyceride resonances was obtained from 10 signals with good signal-to-noise ratios (4, 4, and 2 FIDs for Sol, Gast, and TA, respectively). For this purpose, only the signals with clearly separated ET and IT -(CH2)n- and -CH3 resonances were selected (this is possible due to variation in triglyceride content among subjects). After water removal by using HLSVD, these signals were analyzed by VARPRO with the prior knowledge of equal damping factors (Table 1). It should be emphasized here that there were no restrictions on the damping factor ratio between -(CH2)n- and -CH3. Subsequently, frequency shifts between -(CH2)n- and -CH3 resonances for ET and IT signals as well as damping factor ratios between -(CH2)n- and -CH3 resonances were calculated (Table 2). The prior knowledge calculated for the different muscles was found to be the same within the errors, and therefore the final prior knowledge (Table 2) applied to the present in vivo 1H-MR calf muscle data was calculated as an average over 10 signals selected. These values are consistent with the values found earlier (30). The zero-order phase correction was estimated by VARPRO, and the first-order phase correction was fixed to zero.
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Statistics
Differences between each muscle group for TCr, IT, and ET concentrations were determined by repeated-measures ANOVA. A post hoc Scheffé's F-test was used to analyze any significant difference. The level of significance was chosen at P < 0.05. All results are presented as means ± SE.| |
RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Figure 1 shows a typical
1H-MR spectrum of soleus muscle
fitted by VARPRO. Representative in vivo
1H-MR spectra from the three
muscle groups are shown in Fig. 2. Resonances from TCr, Cho, IT, and ET can be clearly observed. Although
similar resonances can be observed in each muscle, significant differences in the relative metabolite levels are apparent.
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Table 3 shows the levels of metabolites
quantified with 1H-MRS. By using
muscle water as an internal standard, subjects'
(n = 15) mean TCr concentrations in
Sol were significantly lower (P < 0.05) than those in Gast and TA. The concentrations of Cho in TA were
lower compared with Sol (P < 0.001)
and Gast (P < 0.01). Also, the IT
values of TA were significantly lower than those of Sol
(P < 0.01) and Gast
(P < 0.05). There were no
significant differences in levels of ET among the three muscle groups.
Levels of IT in Gast correlated moderately
(r = 0.52, P < 0.05) with Cho levels. A similar
trend was observed in Sol, although it did not reach significance
(P < 0.08). TCr levels did not
correlate significantly with IT concentration, although they showed a
significant correlation (r = 0.93;
P < 0.001) with Cho in
Sol.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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In this study we have used 1H-MRS to noninvasively investigate levels of TCr, Cho, IT, and ET in three different human muscles. The results of the study showed that Gast and TA contain higher concentrations of TCr than does Sol, whereas the levels of IT were lower in TA compared with Sol and Gast. The levels of ET were similar among the three muscles. An additional finding of the present study was the lower level of Cho in TA compared with Sol and Gast.
We are not aware of any study to date that has noninvasively quantified levels of TCr, IT, and ET in different muscle groups in human volunteers. The MRS techniques are of great value as they can be used to determine levels of these metabolites in deep muscles that are difficult to obtain with the biopsy technique. Assessments of IT and ET in different muscles are of significant value for a more in-depth understanding of human lipid metabolism. Also, the noninvasive determinations of TCr can enhance our understanding of Cr metabolism. The concentrations of IT in the three muscles examined in the present study were within the range of IT values obtained from biochemical analyses of biopsies of vastus lateralis muscle by Hurley et al. (24) (59 mmol/kg dry wt), Starling et al. (34) (35 mmol/kg dry wt), Cleroux et al. (14) (28 mmol/kg dry wt), Wendling et al. (40) (26 mmol/kg dry wt), and Kiens et al. (26) (22 mmol/kg dry wt). However, we observed larger IT concentrations in Sol and Gast muscles compared with TA. The levels of TCr in Sol, Gast, or TA observed in the present study were also similar to those obtained from biochemical analyses of muscle biopsies by Edström et al. (18) (Sol 100.6 mmol/kg dry wt), Bangsbo et al. (2) (Gast 119.8 mmol/kg dry wt), and Constantin-Teodosiu et al. (15) (TA 117 mmol/kg dry wt). From the values of these separate studies from different laboratories, it appeared that Sol contained less TCr than did Gast and TA. In the present study, we confirmed a significantly lower TCr content in human Sol compared with in Gast and TA. The differences observed in IT and TCr concentrations among the three muscles examined in the present study are likely to reflect true intermuscular differences.
It has been suggested that the training status of a subject can greatly influence the levels of IT (24-26). However, this does not explain the different levels of IT seen in the three muscles examined, as physical training would generally have a similar effect on all three muscles, unless there was some specific isolated muscle training. This is unlikely for the subjects in the present study. Diet is also a potential factor (34), although its influence should be similar for the three muscles examined. Another possible determinant in the storage of IT and TCr in muscles is the percentage of slow-twitch fibers (19, 27, 28). Interindividual differences in muscle metabolite concentrations can include adaptations to different activity patterns, diet, and fiber-type composition. However, intraindividual metabolite differences in metabolite concentrations of the three muscle observed are possibly due to differences in fiber-type composition.
The differences in metabolite levels due to fiber-type composition of the three muscles examined may be reflective of the chronic biological adaptations to locomotion. Some muscles might have developed to be more oxidative and fatigue resistant, whereas others are more glycolytic and less fatigue resistant, as a consequence of the fact that each of the muscles examined has a different functional role during locomotion. Human muscles contain mixtures of these two types of fibers and others that are classified as intermediate (oxidative-glycolytic). The Sol and Gast muscles are primarily involved in plantar flexion of the ankle joint, whereas the TA is used mostly during dorsiflexion, and the three muscles are used during free standing (3). The Gast is more involved in large contractions and in rapid development of tension compared with Sol (3). If chronic physical usage in endurance types of contraction of the different muscles is the primary factor in the end that influences the number of slow-twitch fibers, the oxidative potential, and the levels of IT (24-26), then we can conclude from the findings of this study that the load in aerobic activities in the human TA is less than that of the plantar flexor muscles during normal locomotion.
The higher levels of TCr in Gast and TA may be indicative of the larger percentage of fast-twitch fibers in these muscles as a likely adaptation of these muscles to more powerful contractions compared with Sol. PCr levels are higher in fast-twitch compared with slow-twitch fibers (27, 29, 32, 36). Also, the levels of PCr determine the power generated during muscle contraction (12). Additionally, PCr levels normally are much larger than those of free Cr in human muscle (12, 21, 23). Thus it is likely that the difference in TCr levels might be primarily due to larger levels of PCr in Gast and TA compared with Sol. In agreement with this hypothesis, Edström et al. (18) showed higher resting levels of PCr in human vastus lateralis compared with Sol. Vastus lateralis, Gast, and TA muscles have lower percentages of slow-twitch fibers compared with Sol (31).
An additional finding of the present study was the lower level of Cho in TA compared with Sol and Gast. Furthermore, Cho levels showed significant correlation with both IT (in Gast) and TCr (in Sol). Chung et al. (13) have previously shown that Cho resonance is a multicomponent peak with contributions from carnitine and glycerophosphorylcholine. The former is closely related to fatty acid metabolism. Therefore, the higher levels of carnitine and IT in Sol and Gast may reflect the higher potential for fat metabolism in theses muscles compared with TA. The significance of the correlations found between different metabolites needs to be explored.
In summary, the results of the present study suggest that IT levels are higher in Sol than in Gast and TA muscles and TCr levels are higher in TA and Gast compared with Sol in humans. On the other hand, the levels of ET are comparable. It is proposed that some of these differences are largely due to the diversity of fiber-type composition as a likely consequence of the selective biological adaptation of each muscle during locomotion.
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ACKNOWLEDGEMENTS |
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We thank Prof. Joseph V. Hajnal and Dr. Mika Ala-Korpela for invaluable help and Miquel Cabañas for kindly providing the MRUI software package (VARPRO).
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FOOTNOTES |
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This work was supported by The Medical Research Council and Picker International.
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. §1734 solely to indicate this fact.
Address for reprint requests and other correspondence: J. Rico-Sanz, Group of Biomedical Applications of Magnetic Resonance, Departament de Bioquimica i Biologia Molecular, Facultat de Ciencies, Universitat Autonoma de Barcelona, 08193 Bellaterra, Barcelona, Spain (E-mail: j.rico-sanz{at}proton.uab.es).
Received 24 February 1999; accepted in final form 23 August 1999.
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 D. B. Savage, G. D. Tan, C. L. Acerini, S. A. Jebb, M. Agostini, M. Gurnell, R. L. Williams, A. M. Umpleby, E. L. Thomas, J. D. Bell, et al. Human Metabolic Syndrome Resulting From Dominant-Negative Mutations in the Nuclear Receptor Peroxisome Proliferator-Activated Receptor-{gamma} Diabetes, April 1, 2003; 52(4): 910 - 917. [Abstract] [Full Text] [PDF]
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H. Howald, C. Boesch, R. Kreis, S. Matter, R. Billeter, B. Essen-Gustavsson, and H. Hoppeler Content of intramyocellular lipids derived by electron microscopy, biochemical assays, and 1H-MR spectroscopy J Appl Physiol, June 1, 2002; 92(6): 2264 - 2272. [Abstract] [Full Text] [PDF]
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J.-H. Hwang, J. W. Pan, S. Heydari, H. P. Hetherington, and D. T. Stein Regional differences in intramyocellular lipids in humans observed by in vivo 1H-MR spectroscopic imaging J Appl Physiol, April 1, 2001; 90(4): 1267 - 1274. [Abstract] [Full Text] [PDF]
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calculated). Cho, choline-containing compounds; TCr, total
creatine;
(-CH2)n-
and -CH3, resonances of
extramuscular (ET) and intramuscular (IT) triglyceride.
