Glucose uptake by the brain on chronic high-protein weight-loss diets with either moderate or low amounts of carbohydrate

British Journal of Nutrition

Volumn 111, Issue 4, 2014, Pages 586-597

  Lobley, Gerald E ^a   Johnstone, Alexandra M ^a   Fyfe, Claire ^a   Horgan, Graham W ^b   Holtrop, Grietje ^b   Bremner, David M ^a   Broom, Iain ^c   Schweiger, Lutz ^d   Welch, Andy ^d  

^a ROWETT RESEARCH INSTITUTE   (United Kingdom)

^b BIOMATHEMATICS AND STATISTICS SCOTLAND   (United Kingdom)

^c ROBERT GORDON UNIVERSITY   (United Kingdom)

^d UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Brain; Glucose kinetics; Ketogenic diets; Ketone body metabolism; Positron emission tomography

Indexed keywords

ADULT; APPETITE REGULATION; BODY MASS INDEX; BRAIN; CARBON ISOTOPES; CROSS-OVER STUDIES; DIET, CARBOHYDRATE-RESTRICTED; DIET, REDUCING; DIETARY CARBOHYDRATES; DIETARY PROTEINS; ENERGY INTAKE; GLUCOSE; HUMANS; KETOGENIC DIET; KETONES; MALE; MIDDLE AGED; OBESITY;

ARGININE; BRANCHED CHAIN AMINO ACID; FLUORODEOXYGLUCOSE F 18; GLUCOSE; GLUTAMIC ACID; GLUTAMINE; HISTIDINE; KETONE; PROLINE; SERINE; THREONINE; TRYPTOPHAN; TYROSINE; UREA; VALINE;

ADULT; AGED; AMINO ACID BLOOD LEVEL; ARTICLE; BODY MASS; BRAIN METABOLISM; BRAIN REGION; CARBOHYDRATE INTAKE; CLINICAL EFFECTIVENESS; COMPOSITE HUNGER SCORE; CONTROLLED STUDY; CROSSOVER PROCEDURE; FOOD COMPOSITION; FOOD INTAKE; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HUMAN; IMAGE ANALYSIS; MALE; NEUROIMAGING; NORMAL HUMAN; POSITRON EMISSION TOMOGRAPHY; PROTEIN DIET; RANDOMIZED CONTROLLED TRIAL; SCORING SYSTEM; WEIGHT REDUCTION;

EID: 84894202457     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114513002900     Document Type: Article

References (61)

1. WHO (2000) Obesity: preventing and managing the global epidemic. Report of a WHO consultation. World Health Organ Tech Rep Ser 894, 1-253, (i-xii).
2. Haslam DW & James WP (2005) Obesity. Lancet 366, 1197-1209.
3. Atkins RC (2002) Dr. Atkins' New Diet Revolution. New York, NY: Harper Collins Publishers.
4. Weigle DS, Breen PA, Matthys CC, et al. (2005) A high-protein diet induces sustained reductions in appetite, ad libitum caloric intake, and body weight despite compensatory changes in diurnal plasma leptin and ghrelin concentrations. Am J Clin Nutr 82, 41-48.
5. Foster GD, Wyatt HR, Hill JO, et al. (2003) A randomized trial of a low-carbohydrate diet for obesity. N Engl J Med 348, 2082-2090.
6. Soenen S, Bonomi AG, Lemmens SG, et al. (2012) Relatively high-protein or 'low-carb' energy-restricted diets for body weight loss and body weight maintenance? Physiol Behav 107, 374-380.
7. Johnstone AM, Horgan GW, Murison SD, et al. (2008) Effects of a high-protein ketogenic diet on hunger, appetite, and weight loss in obese men feeding ad libitum. Am J Clin Nutr 87, 44-55.
8. Anderson JW, Konz EC & Jenkins DJ (2000) Health advantages and disadvantages of weight-reducing diets: a computer analysis and critical review. J Am Coll Nutr 19, 578-590.
9. Feinman RD, Vernon MC & Westman EC (2006) Low carbohydrate diets in family practice: what can we learn from an internet-based support group. Nutr J 5, 26.
10. Ahima RS & Antwi DA (2008) Brain regulation of appetite and satiety. Endocrinol Metab Clin North Am 37, 811-823.
11. Reinmuth OM, Scheinberg P & Bourne B (1965) Total cerebral blood flow and metabolism. Arch Neurol 12, 49-66.
12. Hasselbalch SG, Knudsen GM, Jakobsen J, et al. (1994) Brain metabolism during short-term starvation in humans. J Cereb Blood Flow Metab 14, 125-131.
13. Hawkins RA, Mans AM & Davis DW (1986) Regional ketone body utilization by rat brain in starvation and diabetes. Am J Physiol 250, E169-E178.
14. Morton GJ, Cummings DE, Baskin DG, et al. (2006) Central nervous system control of food intake and body weight. Nature 443, 289-295.
15. Blomqvist G, Thorell JO, Ingvar M, et al. (1995) Use of R-beta-[1-11C]hydroxybutyrate in PET studies of regional cerebral uptake of ketone bodies in humans. Am J Physiol 269, E948-E959.
16. Pan JW, Rothman TL, Behar KL, et al. (2000) Human brain beta-hydroxybutyrate and lactate increase in fasting-induced ketosis. J Cereb Blood Flow Metab 20, 1502-1507.
17. Johnstone AM, Lobley GE, Horgan GW, et al. (2011) Effects of a high-protein, low-carbohydrate v. high-protein, moderate-carbohydrate weight-loss diet on antioxidant status, endothelial markers and plasma indices of the cardiometabolic profile. Br J Nutr 106, 282-291.
18. Balasse EO (1979) Kinetics of ketone body metabolism in fasting humans. Metabolism 28, 41-50.
19. Huang S-C & Phelps ME (1986) Principles of tracer kinetic modeling in positron emission tomography and autoradiography. In Positron Emission Tomography and Autoradiography: Principles and Applications for the Brain and Heart, pp. 287-346 [ME Phelps, JC Mazziotta and HR Schelbert, editors]. New York, NY: Raven Press.
20. Wu HM, Bergsneider M, Glenn TC, et al. (2003) Measurement of the global lumped constant for 2-deoxy-2-[18F]fluoro-Dglucose in normal human brain using [15O]water and 2-deoxy-2-[18F]fluoro-D-glucose positron emission tomography imaging. A method with validation based on multiple methodologies. Mol Imaging Biol 5, 32-41.
21. Avogaro A,Valerio A, Gnudi L, et al. (1992) The effects of different plasma insulin concentrations on lipolytic and ketogenic responses to epinephrine in normal and type 1 (insulindependent) diabetic humans. Diabetologia 35, 129-138.
22. Nosadini R, Datta H, Hodson A, et al. (1980) A possible mechanism for the anti-ketogenic action of alanine in the rat. Biochem J 190, 323-332.
23. Cobelli C, Toffolo G, Avogaro A, et al. (1990) On the measurement of ketone body turnover. Am J Physiol 259, E890.
24. Li PK, Lee JT, MacGillivray MH, et al. (1980) Direct, fixed-time kinetic assays for beta-hydroxybutyrate and acetoacetate with a centrifugal analyzer or a computer-backed spectrophotometer. Clin Chem 26, 1713-1717.
25. Des RC, Montgomery JA, Desrochers S, et al. (1988) Interference of 3-hydroxyisobutyrate with measurements of ketone body concentration and isotopic enrichment by gas chromatography-mass spectrometry. Anal Biochem 173, 96-105.
26. Calder AG, Garden KE, Anderson SE, et al. (1999) Quantitation of blood and plasma amino acids using isotope dilution electron impact gas chromatography/mass spectrometry with U-(13)C amino acids as internal standards. Rapid Commum Mass Spectrom 13, 2080-2083.
27. Wilson FA, van den Borne JJ, Calder AG, et al. (2009) Tissue methionine cycle activity and homocysteine metabolism in female rats: impact of dietary methionine and folate plus choline. Am J Physiol Endocrinol Metab 296, E702-E713.
28. Patterson BW, Carraro F & Wolfe RR (1993) Measurement of 15N enrichment in multiple amino acids and urea in a single analysis by gas chromatography/mass spectrometry. Biol Mass Spectrom 22, 518-523.
29. Cobelli C, Nosadini R, Toffolo G, et al. (1982) Model of the kinetics of ketone bodies in humans. Am J Physiol 243, R7-R17.
30. Bougneres PF & Ferre P (1987) Study of ketone body kinetics in children by a combined perfusion of 13C and 2H3 tracers. Am J Physiol 253, E496-E502.
31. Ader M, Ni TC & Bergman RN (1997) Glucose effectiveness assessed under dynamic and steady state conditions. Comparability of uptake versus production components. J Clin Invest 99, 1187-1199.
32. Cherrington AD, Edgerton D & Sindelar DK (1998) The direct and indirect effects of insulin on hepatic glucose production in vivo. Diabetologia 41, 987-996.
33. Chaput JP, Gilbert JA, Gregersen NT, et al. (2010) Comparison of 150-mm versus 100-mm visual analogue scales in free living adult subjects. Appetite 54, 583-586.
34. Landau BR, Wahren J, Chandramouli V, et al. (1996) Contributions of gluconeogenesis to glucose production in the fasted state. J Clin Invest 98, 378-385.
35. Meyer C, Stumvoll M, Welle S, et al. (2003) Relative importance of liver, kidney, and substrates in epinephrine-induced increased gluconeogenesis in humans. Am J Physiol Endocrinol Metab 285, E819-E826.
36. Gerich JE, Meyer C, Woerle HJ, et al. (2001) Renal gluconeogenesis: its importance in human glucose homeostasis. Diabetes Care 24, 382-391.
37. Wolff JE & Bergman EN (1972) Gluconeogenesis from plasma amino acids in fed sheep. Am J Physiol 223, 455-460.
38. Owen OE, Morgan AP, Kemp HG, et al. (1967) Brain metabolism during fasting. J Clin Invest 46, 1589-1595.
39. Yudkoff M, Daikhin Y, Nissim I, et al. (2004) Ketogenic diet, brain glutamate metabolism and seizure control. Prostaglandins Leukot Essent Fatty Acids 70, 277-285.
40. Volek JS, Sharman MJ, Gomez AL, et al. (2003) An isoenergetic very low carbohydrate diet improves serum HDL cholesterol and triacylglycerol concentrations, the total cholesterol to HDL cholesterol ratio and postprandial pipemic responses compared with a low fat diet in normal weight, normolipidemic women. J Nutr 133, 2756-2761.
41. Batterham RL, Heffron H, Kapoor S, et al. (2006) Critical role for peptide YY in protein-mediated satiation and bodyweight regulation. Cell Metab 4, 223-233.
42. Veldhorst M, Smeets A, Soenen S, et al. (2008) Proteininduced satiety: effects and mechanisms of different proteins. Physiol Behav 94, 300-307.
43. Potier M, Darcel N & Tome D (2009) Protein, amino acids and the control of food intake. Curr Opin Clin Nutr Metab Care 12, 54-58.
44. Lopez M, Tovar S, Vazquez MJ, et al. (2007) Peripheral tissue-brain interactions in the regulation of food intake. Proc Nutr Soc 66, 131-155.
45. Solomon A, De Fanti BA & Martinez JA (2007) Peripheral ghrelin interacts with orexin neurons in glucostatic signalling. Regul Pept 144, 17-24.
46. LaManna JC, Salem N, Puchowicz M, et al. (2009) Ketones suppress brain glucose consumption. Adv Exp Med Biol 645, 301-306.
47. Blomqvist G, Alvarsson M, Grill V, et al. (2002) Effect of acute hyperketonemia on the cerebral uptake of ketone bodies in nondiabetic subjects and IDDM patients. Am J Physiol Endocrinol Metab 283, E20-E28.
48. Bentourkia M, Tremblay S, Pifferi F, et al. (2009) PET study of 11C-acetoacetate kinetics in rat brain during dietary treatments affecting ketosis. Am J Physiol Endocrinol Metab 296, E796-E801.
49. Hasselbalch SG, Madsen PL, Hageman LP, et al. (1996) Changes in cerebral blood flow and carbohydrate metabolism during acute hyperketonemia. Am J Physiol 270, E746-E751.
50. Veldhorst MA, Westerterp KR, van Vught AJ, et al. (2010) Presence or absence of carbohydrates and the proportion of fat in a high-protein diet affect appetite suppression but not energy expenditure in normal-weight human subjects fed in energy balance. Br J Nutr 104, 1395-1405.
51. Johnston CS, Tjonn SL, Swan PD, et al. (2006) Ketogenic low-carbohydrate diets have no metabolic advantage over nonketogenic low-carbohydrate diets. Am J Clin Nutr 83, 1055-1061.
52. De Silva A, Salem V, Matthews PM, et al. (2012) The use of functional MRI to study appetite control in the CNS. Exp Diabetes Res 2012, 764017.
53. Lizarbe B, Benitez A, Sanchez-Montanes M, et al. (2012) Imaging hypothalamic activity using diffusion weighted magnetic resonance imaging in the mouse and human brain. Neuroimage 64, 448-457.
54. Rosenbaum M, Sy M, Pavlovich K, et al. (2008) Leptin reverses weight loss-induced changes in regional neural activity responses to visual food stimuli. J Clin Invest 118, 2583-2591.
55. Marty N, Dallaporta M & Thorens B (2007) Brain glucose sensing, counterregulation, and energy homeostasis. Physiology (Bethesda) 22, 241-251.
56. Levin BE, Routh VH, Kang L, et al. (2004) Neuronal glucosensing: what do we know after 50 years? Diabetes 53, 2521-2528.
57. Page KA, Seo D, Belfort-DeAguiar R, et al. (2011) Circulating glucose levels modulate neural control of desire for highcalorie foods in humans. J Clin Invest 121, 4161-4169.
58. Volkow ND, Wang GJ, Telang F, et al. (2009) Inverse association between BMI and prefrontal metabolic activity in healthy adults. Obesity (Silver Spring) 17, 60-65.
59. Le DS, Pannacciulli N, Chen K, et al. (2006) Less activation of the left dorsolateral prefrontal cortex in response to a meal: a feature of obesity. Am J Clin Nutr 84, 725-731.
60. Gautier JF, Chen K, Salbe AD, et al. (2000) Differential brain responses to satiation in obese and lean men. Diabetes 49, 838-846.
61. Tataranni PA, Gautier JF, Chen K, et al. (1999) Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. Proc Natl Acad Sci USA 96, 4569-4574.