Meal-induced activation of the sympathetic nervous system and its cardiovascular and thermogenic effects in man

Physiology and Behavior

Volumn 94, Issue 2, 2008, Pages 178-186

  van Baak, Marleen A ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Blood flow; Food; Macronutrient composition; Nutrient; Postprandial; Vagal afferents

Indexed keywords

INSULIN; LEPTIN;

ADRENERGIC ACTIVITY; ADRENERGIC SYSTEM; ARTICLE; BRAIN; CARDIOVASCULAR EFFECT; CARDIOVASCULAR RESPONSE; CHEMORECEPTOR; COMORBIDITY; FOOD COMPOSITION; FOOD INTAKE; GASTROINTESTINAL TRACT; HUMAN; INTESTINE; LIVER; MEAL INDUCED ACTIVATION; NUTRIENT; OBESITY; OSMORECEPTOR; PATHOGENESIS; PORTAL VEIN; PRESSORECEPTOR; PRIORITY JOURNAL; SENSORY RECEPTOR; SYMPATHETIC TONE; THERMOGENESIS;

EID: 42949113565     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2007.12.020     Document Type: Article

References (112)

1. G. Grassi Sympathetic overdrive and cardiovascular risk in the metabolic syndrome Hypertens Res Clin Exp 29 11 2006 839 847
2. L. Landsberg A teleological view of obesity, diabetes and hypertension Clin Exp Pharmacol Physiol 33 9 2006 863 867
3. G. Mancia P. Bousquet J.L. Elghozi M. Esler G. Grassi S. Julius The sympathetic nervous system and the metabolic syndrome J Hypertens 25 5 2007 909 920
4. C.L. Gentile J.S. Orr B.M. Davy K.P. Davy Modest weight gain is associated with sympathetic neural activation in nonobese humans Am J Physiol, Regul Integr Comp Physiol 292 5 2007 R1834 R1838
5. K. Masuo H. Mikami T. Ogihara M.L. Tuck Sympathetic nerve hyperactivity precedes hyperinsulinemia and blood pressure elevation in a young, nonobese Japanese population Am J Hypertens 10 1 1997 77 83
6. R.J. Huggett A.J. Hogart A.F. Mackintosh D.A. Mary Sympathetic nerve hyperactivity in non-diabetic offspring of patients with type 2 diabetes mellitus Diabetologia 49 11 2006 2741 2744
7. W. Kopp Pathogenesis and etiology of essential hypertension: role of dietary carbohydrate Med Hypotheses 64 4 2005 782 787
8. M.B. Sidery A.J. Cowley I.A. MacDonald Cardiovascular responses to a high-fat and a high-carbohydrate meal in healthy elderly subjects Clin Sci (Lond) 84 3 1993 263 270
9. M.B. Sidery I.A. Macdonald The effect of meal size on the cardiovascular responses to food ingestion Br J Nutr 71 6 1994 835 848
10. M.T. Kearney A.J. Cowley T.A. Stubbs A.J. Perry I.A. MacDonald Central and peripheral haemodynamic responses to high carbohydrate and high fat meals in human cardiac transplant recipients Clin Sci (Lond) 90 6 1996 473 483
11. U. Hoost H. Kelbaek H. Rasmusen M. Court-Payen N.J. Christensen U. Pedersen-Bjergaard Haemodynamic effects of eating: the role of meal composition Clin Sci (Lond) 90 4 1996 269 276
12. Z. Guo D.D. Hensrud C.M. Johnson M.D. Jensen Regional postprandial fatty acid metabolism in different obesity phenotypes Diabetes 48 8 1999 1586 1592
13. A.F. Muller L. Fullwood M. Hawkins A.J. Cowley The integrated response of the cardiovascular system to food Digestion 52 3–4 1992 184 193
14. M.B. Sidery I.A. Macdonald P.E. Blackshaw Superior mesenteric artery blood flow and gastric emptying in humans and the differential effects of high fat and high carbohydrate meals Gut 35 2 1994 186 190
15. P.J. Matheson M.A. Wilson R.N. Garrison Regulation of intestinal blood flow J Surg Res 93 1 2000 182 196
16. A. Fugmann J. Millgard M. Sarabi C. Berne L. Lind Central and peripheral haemodynamic effects of hyperglycaemia, hyperinsulinaemia, hyperlipidaemia or a mixed meal Clin Sci (Lond) 105 6 2003 715 721
17. E.M. Scott J.P. Greenwood G. Vacca J.B. Stoker S.G. Gilbey D.A. Mary Carbohydrate ingestion, with transient endogenous insulinaemia, produces both sympathetic activation and vasodilatation in normal humans Clin Sci (Lond) 102 5 2002 523 529
18. M. Vaz A. Turner B. Kingwell J. Chin E. Koff H. Cox Postprandial sympatho-adrenal activity: its relation to metabolic and cardiovascular events and to changes in meal frequency Clin Sci (Lond) 89 4 1995 349 357
19. A. Astrup J. Bulow N.J. Christensen F. Quaade Facultative thermogenesis induced by carbohydrate: a skeletal muscle component mediated by epinephrine Am J Physiol 250 2 Pt 1 1986 E226 E229
20. A. Hernandez Mijares M.D. Jensen Contribution of blood flow to leg glucose uptake during a mixed meal Diabetes 44 10 1995 1165 1169
21. M.B. Sidery I.A. Macdonald A.J. Cowley L.J. Fullwood Cardiovascular responses to high-fat and high-carbohydrate meals in young subjects Am J Physiol 261 5 Pt 2 1991 H1430 H1436
22. T.J. Ulahannan F. Karpe S.M. Humphreys D.R. Matthews K.N. Frayn Effects of acute administration of doxazosin on fasting and postprandial haemodynamics and lipid metabolism in healthy subjects Horm Metab Res 34 9 2002 499 503
23. J. Bulow A. Astrup N.J. Christensen J. Kastrup Blood flow in skin, subcutaneous adipose tissue and skeletal muscle in the forearm of normal man during an oral glucose load Acta Physiol Scand 130 4 1987 657 661
24. M. Elia P. Folmer A. Schlatmann A. Goren S. Austin Carbohydrate, fat, and protein metabolism in muscle and in the whole body after mixed meal ingestion Metabolism 37 6 1988 542 551
25. M. Elia K. Khan G. Jennings Effect of mixed meal ingestion on fuel utilization in the whole body and in superficial and deep forearm tissues Br J Nutr 81 5 1999 373 381
26. D. Kelley A. Mitrakou H. Marsh F. Schwenk J. Benn G. Sonnenberg Skeletal muscle glycolysis, oxidation, and storage of an oral glucose load J Clin Invest 81 5 1988 1563 1571
27. L.A. Lipsitz S.M. Ryan J.A. Parker R. Freeman J.Y. Wei A.L. Goldberger Hemodynamic and autonomic nervous system responses to mixed meal ingestion in healthy young and old subjects and dysautonomic patients with postprandial hypotension Circulation 87 2 1993 391 400
28. L. Simonsen J. Bulow A. Astrup J. Madsen N.J. Christensen Diet-induced changes in subcutaneous adipose tissue blood flow in man: effect of beta-adrenoceptor inhibition Acta Physiol Scand 139 2 1990 341 346
29. L.K. Summers J. Callow J.S. Samra I.A. Macdonald D.R. Matthews K.N. Frayn The effect on adipose tissue blood flow of isoenergetic meals containing different amounts and types of fat Int J Obes Relat Metab Disord 25 9 2001 1294 1299
30. F. Karpe B.A. Fielding J.L. Ardilouze V. Ilic I.A. Macdonald K.N. Frayn Effects of insulin on adipose tissue blood flow in man J Physiol 540 Pt 3 2002 1087 1093
31. J.L. Ardilouze B.A. Fielding J.M. Currie K.N. Frayn F. Karpe Nitric oxide and beta-adrenergic stimulation are major regulators of preprandial and postprandial subcutaneous adipose tissue blood flow in humans Circulation 109 1 2004 47 52
32. B. Samnegard T. Brundin Renal extraction of insulin and C-peptide in man before and after a glucose meal Clin Physiol 21 2 2001 164 171
33. P.S. Avasthi E.R. Greene W.F. Voyles Noninvasive Doppler assessment of human postprandial renal blood flow and cardiac output Am J Physiol 252 6 Pt 2 1987 F1167 F1174
34. A.M. Bernstein L. Treyzon Z. Li Are high-protein, vegetable-based diets safe for kidney function? A review of the literature J Am Diet Assoc 107 4 2007 644 650
35. R.R. Baliga L.L. Burden M.K. Sidhu M.W. Rampling J.S. Kooner Effects of components of meals (carbohydrate, fat, protein) in causing postprandial exertional angina pectoris Am J Cardiol 79 10 1997 1397 1400
36. W.Y. Chung D.W. Sohn Y.J. Kim S. Oh I.H. Chai Y.B. Park Absence of postprandial surge in coronary blood flow distal to significant stenosis: a possible mechanism of postprandial angina J Am Coll Cardiol 40 11 2002 1976 1983
37. B.A. Waaler M. Eriksen Post-prandial cardiovascular responses in man after ingestion of carbohydrate, protein or fat Acta Physiol Scand 146 3 1992 321 327
38. G.R. Dagenais A. Oriol M. McGregor Hemodynamic effects of carbohydrate and protein meals in man: rest and exercise J Appl Physiol 21 4 1966 1157 1162
39. D. Gentilcore K.L. Jones D.G. O'Donovan M. Horowits Postprandial hypotension — novel insights into pathophysiology and therapeutic implications Curr Vasc Pharmacol 4 2 2006 161 171
40. R. Muniyappa M. Montagnani K.K. Koh M.J. Quon Cardiovascular actions of insulin Endocr Rev 28 5 2007 463 491
41. L. Tappy Thermic effect of food and sympathetic nervous system activity in humans Reprod Nutr Dev 36 4 1996 391 397
42. E.A. Sims E. Danforth Jr. Expenditure and storage of energy in man J Clin Invest 79 4 1987 1019 1025
43. K.J. Acheson Influence of autonomic nervous system on nutrient-induced thermogenesis in humans Nutrition 9 4 1993 373 380
44. K.J. Acheson E. Ravussin J. Wahren E. Jequier Thermic effect of glucose in man. Obligatory and facultative thermogenesis J Clin Invest 74 5 1984 1572 1580
45. T. Brundin J. Wahren Influence of a mixed meal on splanchnic and interscapular energy expenditure in humans Am J Physiol 260 2 Pt 1 1991 E232 E237
46. L. Simonsen C. Ryge J. Bulow Glucose-induced thermogenesis in splanchnic and leg tissues in man Clin Sci (Lond) 88 5 1995 543 550
47. M.D. Jensen C.M. Johnson P.E. Cryer M.J. Murray Thermogenesis after a mixed meal: role of leg and splanchnic tissues in men and women Am J Physiol 268 3 Pt 1 1995 E433 E438
48. H.S. Cox D.M. Kaye J.M. Thompson A.G. Turner G.L. Jennings C. Itsiopoulos Regional sympathetic nervous activation after a large meal in humans Clin Sci (Lond) 89 2 1995 145 154
49. A. Astrup L. Simonsen J. Bulow J. Madsen N.J. Christensen Epinephrine mediates facultative carbohydrate-induced thermogenesis in human skeletal muscle Am J Physiol 257 3 Pt 1 1989 E340 E345
50. G. Grassi M. Esler How to assess sympathetic activity in humans J Hypertens 17 6 1999 719 734
51. G. Eisenhofer Sympathetic nerve function-assessment by radioisotope dilution analysis Clin Auton Res 15 4 2005 264 283
52. J.B. Young J.W. Rowe J.A. Pallotta D. Sparrow L. Landsberg Enhanced plasma norepinephrine response to upright posture and oral glucose administration in elderly human subjects Metabolism 29 6 1980 532 539
53. S. Welle U. Lilavivathana R.G. Campbell Increased plasma norepinephrine concentrations and metabolic rates following glucose ingestion in man Metabolism 29 9 1980 806 809
54. R.S. Schwartz L.F. Jaeger S. Silberstein R.C. Veith Sympathetic nervous system activity and the thermic effect of feeding in man Int J Obes 11 2 1987 141 149
55. J.N. Patel G. Eisenhofer S.W. Coppack J.M. Miles Norepinephrine spillover in forearm and subcutaneous adipose tissue before and after eating J Clin Endocrinol Metab 84 8 1999 2815 2819
56. J. Fagius C. Berne Increase in muscle nerve sympathetic activity in humans after food intake Clin Sci (Lond) 86 2 1994 159 167
57. P. Penev K. Spiegel T. Marcinkowski E. Van Cauter Impact of carbohydrate-rich meals on plasma epinephrine levels: dysregulation with aging J Clin Endocrinol Metab 90 11 2005 6198 6206
58. I. Marques-Lopes L. Forga J.A. Martinez Thermogenesis induced by a high-carbohydrate meal in fasted lean and overweight young men: insulin, body fat, and sympathetic nervous system involvement Nutrition 19 1 2003 25 29
59. N. Tentolouris C. Tsigos D. Perea E. Koukou D. Kyriaki E. Kitsou Differential effects of high-fat and high-carbohydrate isoenergetic meals on cardiac autonomic nervous system activity in lean and obese women Metabolism 52 11 2003 1426 1432
60. N. Nagai N. Sakane T. Hamada T. Kimura T. Moritani The effect of a high-carbohydrate meal on postprandial thermogenesis and sympathetic nervous system activity in boys with a recent onset of obesity Metabolism 54 4 2005 430 438
61. N. Nagai N. Sakane T. Moritani Metabolic responses to high-fat or low-fat meals and association with sympathetic nervous system activity in healthy young men J Nutr Sci Vitaminol (Tokyo) 51 5 2005 355 360
62. N. Nagai N. Sakane T. Moritani Impact of aging and beta3-adrenergic-receptor polymorphism on thermic and sympathetic responses to a high-fat meal J Nutr Sci Vitaminol (Tokyo) 52 5 2006 352 359
63. P.P. Jones R.E. Van Pelt D.G. Johnson D.R. Seals Role of sympathetic neural activation in age- and habitual exercise-related differences in the thermic effect of food J Clin Endocrinol Metab 89 10 2004 5138 5144
64. A.S. Oberman M.M. Gagnon D.K. Kiely J.C. Nelson L.A. Lipsitz Autonomic and neurohumoral control of postprandial blood pressure in healthy aging J Gerontol, Ser A, Biol Sci Med Sci 55 8 2000 M477 M483
65. S. Welle U. Lilavivat R.G. Campbell Thermic effect of feeding in man: increased plasma norepinephrine levels following glucose but not protein or fat consumption Metabolism 30 10 1981 953 958
66. J.F. Potter D. Heseltine G. Hartley J. Matthews I.A. MacDonald O.F. James Effects of meal composition on the postprandial blood pressure, catecholamine and insulin changes in elderly subjects Clin Sci (Lond) 77 3 1989 265 272
67. D. Heseltine J.F. Potter G. Hartley I.A. Macdonald O.F. James Blood pressure, heart rate and neuroendocrine responses to a high carbohydrate and a high fat meal in healthy young subjects Clin Sci (Lond) 79 5 1990 517 522
68. N.K. Fukagawa Protein-induced changes in energy expenditure in young and old individuals Am J Physiol 260 3 Pt 1 1991 E345 E352
69. S.F. Morrison Differential regulation of sympathetic outflows to vasoconstrictor and thermoregulatory effectors Ann N Y Acad Sci 940 2001 286 298
70. M. Tanida A. Niijima J. Shen T. Nakamura K. Nagai Olfactory stimulation with scent of essential oil of grapefruit affects autonomic neurotransmission and blood pressure Brain Res 1058 1–2 2005 44 55
71. J. Shen A. Niijima M. Tanida Y. Horii K. Maeda K. Nagai Olfactory stimulation with scent of lavender oil affects autonomic nerves, lipolysis and appetite in rats Neurosci Lett 383 1–2 2005 188 193
72. M. Tanida A. Yamatodani A. Niijima J. Shen T. Todo K. Nagai Autonomic and cardiovascular responses to scent stimulation are altered in cry KO mice Neurosci Lett 413 2 2007 177 182
73. J. Shen A. Niijima M. Tanida Y. Horii T. Nakamura K. Nagai Mechanism of changes induced in plasma glycerol by scent stimulation with grapefruit and lavender essential oils Neurosci Lett 416 3 2007 241 246
74. J. LeBlanc M. Cabanac P. Samson Reduced postprandial heat production with gavage as compared with meal feeding in human subjects Am J Physiol 246 1 Pt 1 1984 E95 E101
75. J. LeBlanc L. Brondel Role of palatability on meal-induced thermogenesis in human subjects Am J Physiol 248 3 Pt 1 1985 E333 E336
76. D. Grundy Signalling the state of the digestive tract Auton Neurosci 125 1–2 2006 76 80
77. P.L. Andrews G.J. Sanger Abdominal vagal afferent neurones: an important target for the treatment of gastrointestinal dysfunction Curr Opin Pharmacol 2 6 2002 650 656
78. A.J. Verberne M. Saita D.M. Sartor Chemical stimulation of vagal afferent neurons and sympathetic vasomotor tone Brain Res Rev 41 2–3 2003 288 305
79. H.E. Raybould Sensing of glucose in the gastrointestinal tract Auton Neurosci 133 1 2007 86 90
80. H.E. Raybould J. Glatzle S.L. Freeman K. Whited N. Darcel A. Liou Detection of macronutrients in the intestinal wall Auton Neurosci 125 1–2 2006 28 33
81. P. Rossi G.I. Andriesse P.L. Oey G.H. Wieneke J.M. Roelofs L.M. Akkermans Stomach distension increases efferent muscle sympathetic nerve activity and blood pressure in healthy humans J Neurol Sci 161 2 1998 148 155
82. N.P. van Orshoven P.L. Oey L.J. van Schelven J.M. Roelofs P.A. Jansen L.M. Akkermans Effect of gastric distension on cardiovascular parameters: gastrovascular reflex is attenuated in the elderly J Physiol 555 Pt 2 2004 573 583
83. C.M. Brown L. Barberini A.G. Dulloo J.P. Montani Cardiovascular responses to water drinking: does osmolality play a role? Am J Physiol, Regul Integr Comp Physiol 289 6 2005 R1687 R1692
84. S.R. Raj I. Biaggioni B.K. Black A. Rali J. Jordan I. Taneja Sodium paradoxically reduces the gastropressor response in patients with orthostatic hypotension Hypertension 48 2 2006 329 334
85. E.R. Peskind A. Radant D.J. Dobie J. Hughes C.W. Wilkinson C. Sikkema Hypertonic saline infusion increases plasma norepinephrine concentrations in normal men Psychoneuroendocrinology 18 2 1993 103 113
86. W.B. Farquhar M.M. Wenner E.P. Delaney A.V. Prettyman M.E. Stillabower Sympathetic neural responses to increased osmolality in humans Am J Physiol Heart Circ Physiol 291 5 2006 H2181 H2186
87. H. Katagiri T. Yamada Y. Oka Adiposity and cardiovascular disorders: disturbance of the regulatory system consisting of humoral and neuronal signals Circ Res 101 1 2007 27 39
88. T. Yamada H. Katagiri Avenues of communication between the brain and tissues/organs involved in energy homeostasis Endocr J 2007
89. R.J. Grekin A.P. Vollmer R.S. Sider Pressor effects of portal venous oleate infusion. A proposed mechanism for obesity hypertension Hypertension 26 1 1995 193 198
90. A. Randich D.S. Spraggins J.E. Cox S.T. Meller G.R. Kelm Jejunal or portal vein infusions of lipids increase hepatic vagal afferent activity NeuroReport 12 14 2001 3101 3105
91. R.J. Grekin C.O. Ngarmukos D.M. Williams M.A. Supiano Renal norepinephrine spillover during infusion of nonesterified fatty acids Am J Hypertens 18 3 2005 422 426
92. T. Osaka M. Endo M. Yamakawa S. Inoue Energy expenditure by intravenous administration of glucagon-like peptide-1 mediated by the lower brainstem and sympathoadrenal system Peptides 26 9 2005 1623 1631
93. T.P. Vahl M. Tauchi T.S. Durler E.E. Elfers T.M. Fernandes R.D. Bitner GLP-1 receptors expressed on nerve terminals in the portal vein mediate the effects of endogenous GLP-1 on glucose tolerance in rats Endocrinology 2007
94. J.M. Lavoie The contribution of afferent signals from the liver to metabolic regulation during exercise Can J Physiol Pharm 80 11 2002 1035 1044
95. K. Uno H. Katagiri T. Yanada Y. Ishigaki T. Ogihara J. Imai Neuronal pathway from the liver modulates energy expenditure and systemic insulin sensitivity Science 312 5780 2006 1656 1659
96. C. Berne J. Fagius T. Pollare P. Hjemdahl The sympathetic response to euglycaemic hyperinsulinaemia. Evidence from microelectrode nerve recordings in healthy subjects Diabetologia 35 9 1992 873 879
97. E.A. Anderson R.P. Hoffman T.W. Balon C.A. Sinkey A.L. Mark Hyperinsulinemia produces both sympathetic neural activation and vasodilation in normal humans J Clin Invest 87 6 1991 2246 2252
98. J. Fagius C. Berne The increase in sympathetic nerve activity after glucose ingestion is reduced in type I diabetes Clin Sci (Lond) 98 5 2000 627 632
99. K. Rahmouni M.L. Correia W.G. Haynes A.L. Mark Obesity-associated hypertension: new insights into mechanisms Hypertension 45 1 2005 9 14
100. D.P. van Aggel-Leijssen M.A. van Baak R. Tenenbaum L.A. Campfield W.H. Saris Regulation of average 24 h human plasma leptin level; the influence of exercise and physiological changes in energy balance Int J Obes Relat Metab Disord 23 2 1999 151 158
101. D. Robertson D. Wade R.M. Robertson Postprandial alterations in cardiovascular hemodynamics in autonomic dysfunction states Am J Cardiol 48 6 1981 1048 1052
102. T. Brundin A.K. Aksnes J. Wahren Whole body and splanchnic metabolic and circulatory effects of glucose during beta-adrenergic receptor inhibition Am J Physiol 272 4 Pt 1 1997 E678 E687
103. C. De Mey D. Enterling I. Meineke Cardiovascular effects of eating, atenolol and their interaction: beta1-adrenergic modulation does not play a predominant role in the genesis of postprandial effects Br J Clin Pharmacol 36 5 1993 427 435
104. A.V. Astrup N.J. Christensen L. Simonsen J. Bulow Effects of nutrient intake on sympathoadrenal activity and thermogenic mechanisms J Neurosci Methods 34 1–3 1990 187 192
105. S. Welle R.G. Schwartz M. Statt Reduced metabolic rate during beta-adrenergic blockade in humans Metabolism 40 6 1991 619 622
106. L. De Jonge D.R. Garrel Role of the autonomic nervous system in the thermogenic response to food in lean individuals Am J Physiol 272 5 Pt 1 1997 E775 E780
107. J.B. Morgan D.A. York T.J. Wilkin Influence of propranolol on the acute thermic effect of feeding in man Ann Nutr Metab 30 6 1986 386 392
108. M. Boschmann J. Steiniger U. Hille J. Tank F. Adams A.M. Sharma Water-induced thermogenesis J Clin Endocrinol Metab 88 12 2003 6015 6019
109. C.M. Brown A.G. Dulloo J.P. Montani Water-induced thermogenesis reconsidered: the effects of osmolality and water temperature on energy expenditure after drinking J Clin Endocrinol Metab 91 9 2006 3598 3602
110. M.A. van Baak The peripheral sympathetic nervous system in human obesity Obes Rev 2 1 2001 3 14
111. E.E. Blaak M.A. van Baak A.D. Kester W.H. Saris Beta-adrenergically mediated thermogenic and heart rate responses: effect of obesity and weight loss Metabolism 44 4 1995 520 524
112. D.R. Seals C. Bell Chronic sympathetic activation: consequence and cause of age-associated obesity? Diabetes 53 2 2004 276 284