Multiparametric Aging Study Across Adulthood in the Leg Through Quantitative MR Imaging, 1H Spectroscopy, and 31P Spectroscopy at 3T
Alfredo L. Lopez KolkovskyBéatrice MatotPierre‐Yves BaudinEricky Caldas de Almeida AraújoHarmen ReyngoudtBenjamin MartyYves Fromes
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Background Improved characterization of healthy muscle aging is needed to establish early biomarkers in age‐related diseases. Purpose To quantify age‐related changes on multiple MRI and clinical variables evaluated in the same cohort and identify correlations among them. Study Type Prospective. Population 70 healthy subjects (30 men) from 20 to 81 years old. Field Strength/Sequence 3T/water T 2 (multiecho SE, multi‐TE STEAM), water T 1 (GRE MR Fingerprinting), fat‐fraction (multiecho GRE, multi‐TE STEAM), carnosine (PRESS), multicomponent water T 2 (ISIS‐CPMG SE train), and 31 P pulse‐acquire spectroscopy. Assessment Age‐ and sex‐related changes on: Imaging: fat‐fraction (FF MRI ), water T 1 (T 1‐H2O ), and T 2 (T 2‐H2O‐MRI ) and their heterogeneities ΔT 1‐H2O and ΔT 2‐H2O‐MRI in the posterior compartment (PC) and anterior compartment (AC) of the leg. 1 H spectroscopy: Carnosine concentration, pH, water T 2 components (T 2‐H2O‐CPMG ), fat‐fraction (FF MRS ), and water T 2 (T 2‐H2O‐MRS ) in the gastrocnemius medialis. 31 P spectroscopy: Phosphodiesters (PDE), phosphomonoesters, inorganic phosphates (Pi), and phosphocreatine (PCr) normalized to adenosine triphosphate (ATP) and pH in the calf. Clinical evaluation: Body‐mass index (BMI), gait speed (GS), plantar flexion strength, handgrip strength (HS), HS normalized to wrist circumference (HS norm ), physical activity assessment. Statistical Tests Multilinear regressions with sex and age as fixed factors. Spearman correlations calculated between variables. Benjamini–Hochberg procedure for false positives reduction (5% rate). A P < 0.05 significance level was used. Results Significant age‐related increases were found for BMI ( ρ Age = 0.04), HS norm ( ρ Age = −0.01), PDE/ATP ( ρ Age = 2.8 × 10 −3 ), Pi/ATP ( ρ Age = 2.0 × 10 −3 ), Pi/PCr ( ρ Age = 0.3 × 10 −3 ), T 2‐H2O‐MRS ( ρ Age = 0.051 msec), FF MRS ( ρ Age = 0.036) the intermediate T 2‐H2O‐CPMG component time ( ρ Age = 0.112 msec), and fraction ( ρ Age = −0.3 × 10 −3 ); and in both compartments for FF MRI ( ρ Age = 0.06, PC; ρ Age = 0.06, AC), T 2‐H2O‐MRI ( ρ Age = 0.05, PC; ρ Age = 0.05, AC; msec), ΔT 2‐H2O‐MRI ( ρ Age = 0.02, PC; ρ Age = 0.02, AC; msec), T 1‐H2O ( ρ Age = 1.08, PC; ρ Age = 1.06, AC; msec), and ΔT 1‐H2O ( ρ Age = 0.22, PC; ρ Age = 0.37, AC; msec). The best age predictors, accounting for sex‐related differences, were HS norm ( R 2 = 0.52) and PDE/ATP ( R 2 = 0.44). In both leg compartments, the imaging measures and HS norm were intercorrelated. In PC, T 2‐H2O‐MRS and FF MRS also showed numerous correlations to the imaging measures. PDE/ATP correlated to T 1‐H2O, T 2‐H2O‐MRI , ΔT 2‐H2O‐MRI , FF MRI , FF MRS , the intermediate T 2‐H2O‐CPMG , BMI, Pi/PCr, and HS norm . Data Conclusion Our multiparametric MRI approach provided an integrative view of age‐related changes in the leg and revealed multiple correlations between these parameters and the normalized HS. Level of Evidence 1 Technical Efficacy Stage 3Keywords:
Carnosine
Phosphorus nuclear magnetic resonance (31P NMR) spectroscopy is a non-destructive analytical laboratory technique that, due to recent technical advances, has become applicable to the study of high-energy phosphate metabolism in both animal and human extremity muscles (in vivo). 31P NMR can assay cellular phosphocreatine, ATP, inorganic phosphate, the phosphorylated glycolytic intermediates, and intra-cellular pH in either resting or exercising muscle, in a non-invasive manner. NMR uses non-perturbing levels of radio-frequency energy as its biophysical probe and can therefore safely study intact muscle in a repeated fashion while exerting no artifactual influence on ongoing metabolic processes. Compared with standard tissue biopsy and biochemical assay techniques, NMR possesses the advantages of being non-invasive, allowing serial in situ studies of the same tissue sample, and providing measurements of only active (unbound) metabolites. NMR studies of exercising muscle have yielded information regarding fatigue mechanisms at the cellular level and are helping resolve long-standing questions regarding the metabolic control of glycolysis, oxidative phosphorylation, and post-exercise phosphocreatine re-synthesis. NMR is also being utilized to measure enzymatic reaction rates in vivo. In the near future, other forms of NMR spectroscopy may also permit the non-invasive measurement of tissue glycogen and lactate content.
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This study reports the MR spectroscopic patterns of two patients with bithalamic glioma. In one patient, phosphorus (31P) MR spectroscopy was performed. In both patients, the proton MR spectroscopic scans showed an increased creatine-phosphocreatine peak in the tumor. In the patient who underwent 31P-MR spectroscopy, an increased phosphocreatine peak was also observed. This group of thalamic tumors may be distinguished from other gliomas clinically, radiologically, and metabolically.
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A 40-year-old female with a recurrent mixed astrocytoma/oligodendroglioma was treated with intra-arterial BCNU at six week intervals. Phosphorus magnetic resonance spectroscopy was performed before, and on two occasions after her third treatment. Before treatment, phosphodiesters were 25% less than normal and intracellular pH was 7.14 (normal 6.97 +/- 0.02). Eight hours following treatment phosphocreatine and phosphodiesters were reduced by approximately 40% and pHi increased to 7.24. Thirty-two hours after treatment, phosphocreatine and phosphodiesters had reversed their decline, but pHi had increased further to 7.35. MRI and x-ray CT scans did not show any change during this period. This study demonstrates that chemical changes can be observed in a glioma by magnetic resonance spectroscopy shortly after chemotherapy in a clinical setting and before changes are observable by imaging modalities. This approach evidently offers a possible means of monitoring the acute metabolic response of tumours to chemotherapy or other forms of treatment by a non-invasive repeatable quantitative method.
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Sapega, A. A., D. P. Sokolow, T. J. Graham, and B. Chance. Phosphorus nuclear magnetic resonance: a non-invasive technique for the study of muscle bioenergetics during exercise. Med. Sci. Sports Exerc., Vol. 19, No. 4, pp. 410–420, 1987. Phosphorus nuclear magnetic resonance (31P NMR) spectroscopy is a non-destructive analytical laboratory technique that, due to recent technical advances, has become applicable to the study of high-energy phosphate metabolism in both animal and human extremity muscles (in vivo). 31P NMR can assay cellular phosphocreatine, ATP, inorganic phosphate, the phosphorylated glycolytic intermediates, and intra-cellular pH in either resting or exercising muscle, in a non-invasive manner. NMR uses non-perturbing levels of radio-frequency energy as its biophysical probe and can therefore safely study intact muscle in a repeated fashion while exerting no artifactual influence on ongoing metabolic processes. Compared with standard tissue biopsy and biochemical assay techniques, NMR possesses the advantages of being non-invasive, allowing serial in situ studies of the same tissue sample, and providing measurements of only active (unbound) metabolites. NMR studies of exercising muscle have yielded information regarding fatigue mechanisms at the cellular level and are helping resolve longstanding questions regarding the metabolic control of glycolysis, oxidative phosphorylation, and post-exercise phosphocreatine re-synthesis. NMR is also being utilized to measure enzymatic reaction rates in vivo. In the near future, other forms of NMR spectroscopy may also permit the non-invasive measurement of tissue glycogen and lactate content.
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Involvement of the autonomic system in multiple sclerosis (MS) may concur with dysfunction of the cardiovascular system. The introduction of potentially cardiotoxic immunosuppressive drugs like Mitoxantrone into the treatment of MS warrants proper assessment of preexisting heart disease. However, systematic analyses of functional and metabolic derangements in MS are missing. Using quantitative 31P-MR-spectroscopy (MRS) and MR-imaging (MRI) metabolic and functional parameters were analyzed in patients with MS in comparison to healthy volunteers.14/15 patients with MS could be included in the study, as the MRS examination of one patient had to be excluded from analysis due to movement during the examination. Using chemical shift imaging (CSI) and AMARES, phosphocreatine (PCr) to adenosine triphosphate (ATP) ratios, characterizing myocardial high-energy phosphate metabolism, were determined. Additionally, absolute concentrations of PCr and ATP were calculated by SLOOP (Spatial Localization with Optimal Pointspread Function). Analysis of functional changes was performed by Cine-MRI. 14 healthy volunteers matched for age and gender served as control.A significant decrease of absolute PCr concentration was observed in patients with MS compared to matched volunteers (p < 0.05), whereas ATP concentrations showed no significant changes (p = 0.27). Metabolite ratios calculated by SLOOP or AMARES showed a tendency to be reduced in patients, however, did not reach significance (p = 0.08, SLOOP; p = 0.47, AMARES). Using volunteers' mean values +/- 2 x SD as cut off value revealed PCr changes in 5 of 14 patients, whereas only 2 also had pathologic PCr/ATP ratios. Functional analysis by MRI depicted depressed left ventricular ejection fraction in 4 patients.The reduction in cardiac high-energy phosphates in some patients with MS points to a subclinical involvement of the heart. This may be important for treatment with potentially cardiotoxic drugs. Longitudinal studies are need to understand the clinical relevance of our findings.
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Sapega, A. A., D. P. Sokolow, T. J. Graham, and B. Chance. Phosphorus nuclear magnetic resonance: a non-invasive technique for the study of muscle bioenergetics during exercise. Med. Sci. Sports Exerc., Vol. 19, No. 4, pp. 410–420, 1987. Phosphorus nuclear magnetic resonance (31P NMR) spectroscopy is a non-destructive analytical laboratory technique that, due to recent technical advances, has become applicable to the study of high-energy phosphate metabolism in both animal and human extremity muscles (in vivo). 31P NMR can assay cellular phosphocreatine, ATP, inorganic phosphate, the phosphorylated glycolytic intermediates, and intra-cellular pH in either resting or exercising muscle, in a non-invasive manner. NMR uses non-perturbing levels of radio-frequency energy as its biophysical probe and can therefore safely study intact muscle in a repeated fashion while exerti no artifactual influence on ongoing metabolic processes. Compare with standard tissue biopsy and biochemical assay techniques, NMR possesses the advantages of being non-invasive, allowing serial in situ studies of the same tissue sample, and providing measurements of only active (unbound) metabolites. NMR studies of exercising muscle have yielded information regarding fatigue mechanisms at the cellular level and are helping resolve longstanding questions regarding the metabolic control of glycolysis, oxidative phosphorylation, and post-exercise phosphocreatine re-synthesis. NMR is also being utilized to measure enzymatic reaction rates in vivo. In the near future, other forms of NMR spectroscopy may also permit the non-invasive measurement of tissue glycogen and lactate content.
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