Methodological and physiological test–retest reliability of 13C‐MRS glycogen measurements in liver and in skeletal muscle of patients with type 1 diabetes and matched healthy controls

Glycogen is a major substrate in energy metabolism and particularly important to prevent hypoglycemia in pathologies of glucose homeostasis such as type 1 diabetes mellitus (T1DM). 13C‐MRS is increasingly used to determine glycogen in skeletal muscle and liver non‐invasively; however, the low signal‐to‐noise ratio leads to long acquisition times, particularly when glycogen levels are determined before and after interventions. In order to ease the requirements for the subjects and to avoid systematic effects of the lengthy examination, we evaluated if a standardized preparation period would allow us to shift the baseline (pre‐intervention) experiments to a preceding day.

[1]  C. Boesch,et al.  Fructose and galactose enhance postexercise human liver glycogen synthesis. , 2011, Medicine and science in sports and exercise.

[2]  R. Shulman,et al.  13C-NMR measurements of muscle glycogen during low-intensity exercise. , 1991, Journal of applied physiology.

[3]  G. Shulman,et al.  Hepatic glycogen metabolism in type 1 diabetes after long-term near normoglycemia. , 2002, Diabetes.

[4]  S. Van Huffel,et al.  Evaluation of signal processing methods for the quantification of a multi–exponential signal: the glycogen 13C‐1 NMR signal , 1996, NMR in biomedicine.

[5]  R. Kreis,et al.  Normal hepatic glycogen storage after fasting and feeding in children and adolescents with type 1 diabetes , 2003, Pediatric diabetes.

[6]  A Heerschap,et al.  Muscle glycogen recovery after exercise during glucose and fructose intake monitored by 13C-NMR. , 1996, Journal of applied physiology.

[7]  I. Gabriely,et al.  Role of hepatic glycogen breakdown in defective counterregulation of hypoglycemia in intensively treated type 1 diabetes. , 2006, Diabetes.

[8]  I. Macdonald,et al.  Variability in fasting lipid and glycogen contents in hepatic and skeletal muscle tissue in subjects with and without type 2 diabetes: a 1H and 13C MRS study , 2013, NMR in biomedicine.

[9]  Rolf Gruetter,et al.  A double‐quadrature radiofrequency coil design for proton‐decoupled carbon‐13 magnetic resonance spectroscopy in humans at 7T , 2015, Magnetic resonance in medicine.

[10]  K. Petersen,et al.  Impaired net hepatic glycogen synthesis in insulin-dependent diabetic subjects during mixed meal ingestion. A 13C nuclear magnetic resonance spectroscopy study. , 1995, The Journal of clinical investigation.

[11]  M. Tarnopolsky,et al.  Sex differences in carbohydrate metabolism , 2001, Current opinion in clinical nutrition and metabolic care.

[12]  G. Shulman,et al.  Lipid-dependent control of hepatic glycogen stores in healthy humans , 2001, Diabetologia.

[13]  R. Shulman,et al.  Validation of 13c nmr measurement of human skeletal muscle glycogen by direct biochemical assay of needle biopsy samples , 1992, Magnetic resonance in medicine.

[14]  Heerschap,et al.  Assessment of human muscle glycogen synthesis and total glucose content by in vivo13C MRS , 2000, European journal of clinical investigation.

[15]  H. King,et al.  Global Burden of Diabetes, 1995–2025: Prevalence, numerical estimates, and projections , 1998, Diabetes Care.

[16]  S. Gerrior,et al.  An Easy Approach to Calculating Estimated Energy Requirements , 2006, Preventing chronic disease.

[17]  D. Altman,et al.  STATISTICAL METHODS FOR ASSESSING AGREEMENT BETWEEN TWO METHODS OF CLINICAL MEASUREMENT , 1986, The Lancet.

[18]  D L Rothman,et al.  The Journal of Clinical Endocrinology & Metabolism Printed in U.S.A. Copyright © 2000 by The Endocrine Society Intramuscular Glycogen and Intramyocellular Lipid Utilization during Prolonged Exercise and Recovery in Man: A 13 C and 1 H Nuclear Magnetic Res , 1999 .

[19]  Vanhamme,et al.  Improved method for accurate and efficient quantification of MRS data with use of prior knowledge , 1997, Journal of magnetic resonance.

[20]  Ewald Moser,et al.  Absolute quantification of phosphorus metabolite concentrations in human muscle in vivo by 31P MRS: a quantitative review , 2007, NMR in biomedicine.

[21]  C. Boesch,et al.  Fuel metabolism during exercise in euglycaemia and hyperglycaemia in patients with type 1 diabetes mellitus—a prospective single-blinded randomised crossover trial , 2008, Diabetologia.

[22]  R. Mann,et al.  Effect of carbohydrate ingestion on glycogen resynthesis in human liver and skeletal muscle, measured by (13)C MRS. , 2000, American journal of physiology. Endocrinology and metabolism.

[23]  P. Greenhaff,et al.  Energy metabolism in single human muscle fibres during intermittent contraction with occluded circulation. , 1993, The Journal of physiology.

[24]  K. Petersen,et al.  Mechanism of impaired insulin-stimulated muscle glucose metabolism in subjects with insulin-dependent diabetes mellitus. , 1997, The Journal of clinical investigation.

[25]  A. Beckett,et al.  AKUFO AND IBARAPA. , 1965, Lancet.

[26]  K. Maruyama,et al.  13C MRS reveals a small diurnal variation in the glycogen content of human thigh muscle , 2015, NMR in biomedicine.

[27]  R. Haller,et al.  Reproducibility and Absolute Quantification of Muscle Glycogen in Patients with Glycogen Storage Disease by 13C NMR Spectroscopy at 7 Tesla , 2014, PloS one.

[28]  R. Shulman,et al.  13C NMR relaxation times of hepatic glycogen in vitro and in vivo. , 1990, Biochemistry.

[29]  R. Gruetter,et al.  Validation of 13C NMR measurements of liver glycogen in vivo , 1994, Magnetic resonance in medicine.

[30]  R. Shulman,et al.  NMR studies of muscle glycogen synthesis in insulin-resistant offspring of parents with non-insulin-dependent diabetes mellitus immediately after glycogen-depleting exercise. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Chris Boesch,et al.  Metabolic and hormonal response to intermittent high-intensity and continuous moderate intensity exercise in individuals with type 1 diabetes: a randomised crossover study , 2016, Diabetologia.

[32]  C. Boesch,et al.  Hepatic and intramyocellular glycogen stores in adults with type 1 diabetes and healthy controls. , 2015, Diabetes research and clinical practice.

[33]  G. Bassez,et al.  Evaluation of muscle glycogen content by 13C NMR spectroscopy in adult-onset acid maltase deficiency , 2003, Neuromuscular Disorders.

[34]  Postprandial and Fasting Hepatic Glucose Fluxes in Long-Standing Type 1 Diabetes , 2011, Diabetes.

[35]  D. Graveron-Demilly,et al.  Java-based graphical user interface for the MRUI quantitation package , 2001, Magnetic Resonance Materials in Physics, Biology and Medicine.

[36]  P. Styles,et al.  Daytime liver glycogen accumulation, measured by 13C magnetic resonance spectroscopy, in young children with Type 1 diabetes mellitus , 2001, Diabetic medicine : a journal of the British Diabetic Association.

[37]  R. Buchli,et al.  Noninvasive measurement of muscle high-energy phosphates and glycogen concentrations in elite soccer players by 31P- and 13C-MRS. , 1998, Medicine and science in sports and exercise.

[38]  E. Newsholme,et al.  The glucose fatty-acid cycle. Its role in insulin sensitivity and the metabolic disturbances of diabetes mellitus. , 1963, Lancet.

[39]  Physical activity/exercise and diabetes. , 2004, Diabetes care.