Exercise hemorheology: Moving from old simplistic paradigms to a more complex picture

Clinical Hemorheology and Microcirculation

Volumn 55, Issue 1, 2013, Pages 15-27

  Brun, Jean Frédéric ^a   Varlet Marie, Emmanuelle ^b,c   Romain, Ahmed Jérôme ^a   Guiraudou, M ^a   Raynaud De Mauverger, Eric ^a  

^a LAPEYRONIE HOSPITAL   (France)

^b UNIVERSITÉ DE PERPIGNAN   (France)

^c UNIV MONTPELLIER   (France)

Author keywords

blood viscosity; body fluids; erythrocyte aggregation; erythrocyte deformability; exercise; far mass; fat free mass; hematocrit; hemorheology; Insulin resistance; metabolic syndrome; plasma viscosity; training

Indexed keywords

GLUCOSE; INSULIN; LACTIC ACID;

ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHLETE; BLOOD FLOW; BLOOD PRESSURE; BLOOD RHEOLOGY; BLOOD VISCOSITY; BODY FAT; CALORIC RESTRICTION; CARBOHYDRATE INTAKE; CEREBROVASCULAR ACCIDENT; CIRCULATION; DIET; DOSE RESPONSE; ENDOTHELIAL DYSFUNCTION; ENDURANCE TRAINING; ERYTHROCYTE; ERYTHROCYTE DEFORMABILITY; EXERCISE; EXERCISE INTENSITY; FAT MASS; FEEDING BEHAVIOR; FITNESS; FOOD INTAKE; GENETIC POLYMORPHISM; GLUCOSE HOMEOSTASIS; GLYCEMIC INDEX; HEMATOCRIT; HUMAN; INSULIN RESISTANCE; ISCHEMIA; LIFESTYLE; MEAT; NONHUMAN; NUTRITION; OBESITY; PHYSICAL ACTIVITY; SEDENTARY LIFESTYLE; THROMBOSIS; VASODILATATION; WAIST HIP RATIO; WEIGHT REDUCTION;

BLOOD VISCOSITY; BODY FLUIDS; ERYTHROCYTE AGGREGATION; ERYTHROCYTE DEFORMABILITY; EXERCISE; FAR MASS; FAT-FREE MASS; HEMATOCRIT; HEMORHEOLOGY; INSULIN RESISTANCE; METABOLIC SYNDROME; PLASMA VISCOSITY; TRAINING;

BLOOD VISCOSITY; ERYTHROCYTE AGGREGATION; ERYTHROCYTE DEFORMABILITY; ERYTHROCYTES; EXERCISE; HEMATOCRIT; HEMORHEOLOGY; HUMANS; INSULIN RESISTANCE; METABOLIC SYNDROME X;

EID: 84887856106     PISSN: 13860291     EISSN: 18758622     Source Type: Journal    
DOI: 10.3233/CH-131686     Document Type: Article

References (96)

1. C. Aguer, J. Mercier, C.Y. Man, L. Metz, S. Bordenave, K. Lambert, E. Jean, L. Lantier, L. Bounoua, J.F. Brun, E. Raynaud de Mauverger, F. Andreelli, M. Foretz and M. Kitzmann, Intramyocellular lipid accumulation is associated with permanent relocation ex vivo and in vitro of fatty acid translocase (FAT)/CD36 in obese patients, Diabetologia 53(6) (2010), 1151-1163
2. T. Appelboom, C. Rouffin and E. Fierens, Sport and medicine in ancient Greece, Am J Sports Med 16(6) (1988), 594-596
3. C. Ayyad and T. Andersen, Long-term efficacy of dietary treatment of obesity: A systematic review of studies published between 1931 and 1999, Obes Rev 1 (2000), 113-119
4. E.J. Belin de Chantemele and D.W. Stepp, Influence of obesity and metabolic dysfunction on the endothelial control in the coronary circulation, J Mol Cell Cardiol 52(4) (2012), 840-847
5. A. Berrington de Gonzalez, P. Hartge, J.R. Cerhan, A.J. Flint, L. Hannan, R.J. MacInnis, S.C. Moore, G.S. Tobias, H. Anton- Culver, L.B. Freeman, W.L. Beeson, S.L. Clipp, D.R. English, A.R. Folsom, D.M. Freedman, G. Giles, N. Hakansson, K.D. Henderson, J. Hoffman-Bolton, J.A. Hoppin, K.L. Koenig, I.M. Lee, M.S. Linet, Y. Park, G. Pocobelli, A. Schatzkin, H.D. Sesso, E. Weiderpass, B.J. Willcox, A. Wolk, A. Zeleniuch-Jacquotte, W.C. Willett and M.J. Thun, Body-mass index and mortality among 1.46 million white adults, N Engl J Med 363(23) (2010), 2211-2219
6. S.N. Blair, H.W. Kohl and N.F. Gordon, R.S. Paffenbarger Jr, How much physical activity is good for health? Annu Rev Public Health 13 (1992), 99-126
7. S.N. Blair and J.C. Connelly, How much physical activity should we do? The case for moderate amounts and intensities of physical activity, Res Q Exerc Sport 67(2) (1996), 193-205
8. J.J. Bishop, P.R. Nance, A.S. Popel, M. Intaglietta and P.C. Johnson, Effect of erythrocyte aggregation on velocity profiles in venules, Am J Physiol Heart Circ Physiol 280 (2001), H222-H236
9. J.J. Bishop, P.R. Nance, A.S. Popel, M. Intaglietta and P.C. Johnson, Relationship between erythrocyte aggregate size and flow rate in skeletal muscle venules, Am J Physiol Heart Circ Physiol 286 (2004), H113-H120
10. J.C. Brand-Miller, H.J. Griffin and S. Colagiuri, The carnivore connection hypothesis: Revisited, J Obes 2012 (2012), 258624
11. M. Brochu, M.E. Mathieu, A.D. Karelis, E. Doucet, M.E. Lavoie, D. Garrel and R. Rabasa-Lhoret, Contribution of the lean body mass to insulin resistance in postmenopausal women with visceral obesity: A Monet study, Obesity 16 (2008), 1085-1093
12. G.A. Brooks and J. Mercier, Balance of carbohydrate and lipid utilization during exercise: The "crossover" concept, J Appl Physiol 76 (1994), 2253-2261
13. J.F. Brun, Le. LIPOXmax, un niveau d'exercice adapt'e par ses propri'et'es ́energ'etiques et comportementales au "ph'enotype ́econome" du syndrome m'etabolique: L'hypothèse du "healthy primitive lifestyle", Sci Sport (2012), in press.
14. J.F. Brun, M. Guiraudou, M.A.J. Romain, M. Pollatz, M.M. Mawunu, M.K. Bedjih, C. Fedou and J. Mercier, Effets chroniques de l'exercice cibl'e au niveau d'oxydation maximale des lipides (LIPOXmax) sur le comportement alimentaire de sujets obèses s'edentaires, Sci Sport (2012), in press.
15. J.F. Brun, E. Varlet-Marie, I. Aloulou, M. Sardinoux, E. Raynaud de Mauverger and J. Mercier, Hemorheology in Insulin Resistance. Microcirculation and Insulin Resistance. In: Nicolas Wiernsperger Eliete Bouskela & Luiz Guilherme Kraemer-Aguiar editors: Microcirculation and Insulin Resistance. Bentham Science publishing. Downloadable from http://www.benthamscience.com/ ebooks/9781608050574/contents.htm.
16. J.F. Brun, E. Varlet-Marie, P. Connes and I. Aloulou I, Hemorheological alterations related to training and overtraining, Biorheology 47 (2010), 95-115
17. J.F. Brun, E. Varlet-Marie, A.J. Romain and J. Mercier Measurement and physiological relevance of the maximal lipid oxidation rate during exercise (LIPOXmax), In: "Sports Medicine and Sports Injuries", InTech book, Vienne Austria 2011, ISBN 979-953-307-096-3
18. E.E. Calle, L.R. Teras and M.J. Thun, Obesity and mortality, N Engl J Med 353(20) (2005), 2197-2199
19. G. Caminiti, M. Volterrani, G. Marazzi, R. Massaro, C. Vitale, L. Gatta, C. Mammi, M. Miceli and G. Rosano, Metabolic syndrome predicts lower functional recovery in female but not in male patients after an acute cardiac event, Int J Cardiol 135(3) (2009), 296-301
20. J.O. Clausen, K. Borch-Johnsen, H. Ibsen, R.N. Bergman, P. Hougaard, K. Winther and O. Pedersen, Insulin sensitivity index, acute insulin response, and glucose effectiveness in a population-based sample of 380 young healthy Caucasians. Analysis of the impact of gender, body fat, physical fitness, and life-style factors, J Clin Invest 98(5) (1996), 1195-1209
21. S. Colagiuri and J.C. Brand Miller, The metabolic syndrome: From inherited survival trait to a health care problem, Exp Clin Endocrinol Diabetes 105(Suppl 2) (1997), 54-60
22. P. Connes, D. Bouix, G. Py, C. Caillaud, P. Kippelen, J.F. Brun, A. Varray, C. Prefaut and J. Mercier, Does exerciseinduced hypoxemia modify lactate influx into erythrocytes and hemorheological parameters in athletes? J Appl Physiol 97(3) (2004), 1053-1058
23. P. Connes, J.F. Brun and O.K. Baskurt, Blood Rheology and Exercise in "Exercise Physiology: From a Cellular to an Integrative Approach", In: Biomedical and Health Research, P. Connes, O. Hue and S. Perrey, ed., (2010), pp 213-229
24. J.P. Curtis, J.G. Selter, Y. Wang, S.S. Rathore, I.S. Jovin, F. Jadbabaie, M. Kosiborod, E.L. Portnay, S.I. Sokol, F. Bader and H.M. Krumholz, The obesity paradox: Body mass index and outcomes in patients with heart failure, Arch Intern Med 165(1) (2005), 55-61
25. S.G. Dasilva, L. Guidetti, C.F. Buzzachera, H.M. Elsangedy, K. Krinski, W. De Campos, F.L. Goss and C. Baldari, Gender-based differences in substrate use during exercise at a self- selected pace, J Strength Cond Res 25(9) (2011), 2544-2551
26. L. Dintenfass and B. Lake, Exercise fitness, cardiac work and blood viscosity factors in patients and normals, Eur Surg Res 8(2) (1976), 174-184
27. G.K. Driessen, C.W. Haest, H. Heidtmann, D. Kamp and H. Schmid-Schonbein, Effect of reduced red cell "deformability" on flow velocity in capillaries of rat mesentery, Pflugers Arch 388 (1980), 75-78
28. E. Ernst, Changes in blood rheology produced by exercise, JAMA 253(20) (1985), 24-31
29. E. Ernst, Influence of regular physical activity on blood rheology, Eur Heart J 8 (Suppl G) (1987), 59-62
30. S.K. Fried and S.P. Rao, Sugars, hypertriglyceridemia, and cardiovascular disease, AmJ Clin Nutr 78(4) (2003), 873S-880S.
31. K. Funai and C.F. Semenkovich, Skeletal muscle lipid flux: Running water carries no poison, Am J Physiol Endocrinol Metab 301(2) (2011), E245-251
32. O. Gögebakan, A.Kohl, M.A. Osterhoff, M.A. van Baak, S.A. Jebb, A. Papadaki, J.A. Martinez, T. Handjieva-Darlenska, P. Hlavaty, M.O. Weickert, C. Holst, W.H. Saris, A. Astrup, A.F. Pfeiffer and DiOGenes, Effects of weight loss and long-term weight maintenance with diets varying in protein and glycemic index on cardiovascular risk factors: The diet, obesity, and genes (DiOGenes) study: A randomized, controlled trial, Circulation 124(25) (2011), 2829-2838
33. H.L. Goldsmith, G.R. Cokelet and P. Gaehtgens, Robin Fåhraeus: Evolution of his concepts in cardiovascular physiology, Am J Physiol 257 (1989), H1005-H1015
34. E. Goyenechea, C. Holst, W.H. Saris, S. Jebb, A. Kafatos, A. Pfeiffer, S. Handjiev, P. Hlavaty, S. Stender, T.M. Larsen, A. Astrup, J.A. Martinez and on behalf of DIOGenes. Effects of different protein content and glycemic index of ad libitum diets on diabetes risk factors in overweight adults: The DIOGenes multicentre, randomised, dietary intervention trial, Diabetes Metab Res Rev (2011), doi: 10.1002/dmrr.1218
35. T.E. Graham and K.B. Adamo, Dietary carbohydrate and its effects on metabolism and substrate stores in sedentary and active individuals, Can J Appl Physiol 24(5) (1999), 393-415
36. A.C. Guyton and T.Q. Richardson, Effect of hematocrit on venous return, Circ Res 9 (1961), 157-161
37. A. Habbu, N.M. Lakkis and H. Dokainish, The obesity paradox: Fact or fiction? Am J Cardiol 1; (2006), 944- 948
38. A. Habbu, N.M. Lakkis and H. Dokainish, The obesity paradox: Fact or fiction? Am J Cardiol;98(7) (2006), 944- 948
39. C.N. Hales and D.J. Barker, Type 2 (non-insulin-dependent) diabetes mellitus: The thrifty phenotype hypothesis, Diabetologia 35 (1992), 595-601
40. M. Hamer and E. Stamatakis, Metabolically healthy obesity and risk of all-cause and cardiovascular disease mortality, J Clin Endocrinol Metab 97(7) (2012), 2482-2488
41. B.M. Holt, Mobility in Upper Paleolithic and Mesolithic Europe: Evidence from the lower limb, Am J Phys Anthropol 122(3) (2003), 200-215
42. B.M. Holt and V. Formicola, Hunters of the Ice Age: The biology of Upper Paleolithic people, Am J Phys Anthropol (Suppl 47) (2008), 70-99
43. J.A. Houmard, W.J. Pories and G.L. Dohm, Is there a metabolic program in the skeletal muscle of obese individuals? J Obes, 26 (2011), 250-496
44. J.A. Houmard, W.J. Pories and G.L. Dohm, Severe, Obesity: Evidence for a Deranged Metabolic Program in Skeletal Muscle? Exerc Sport Sci Rev 15 (2012
45. A.M. Johnstone, Safety and efficacy of high-protein diets for weight loss, Proc Nutr Soc (2012), 339-349
46. L.G. Jozsa, Obesity in the paleolithic era, Hormones 10(3) (2011), 241-244
47. D.K. Kaul, A. Koshkaryev, G. Artmann, G. Barshtein and S. Yedgar, Additive effect of red blood cell rigidity and adherence to endothelial cells in inducing vascular resistance, Am J Physiol Heart Circ Physiol 295 (2008), H1788-H1793
48. A.D. Karelis, Metabolically healthy but obese individuals, Lancet 372(9646) (2008), 1281-1283
49. A.D. Karelis, V. Messier, M. Brochu and R. Rabasa-Lhoret, Metabolically healthy but obese women: Effect of an energyrestricted diet, Diabetologia 51(9) (2008), 1752-1754
50. E. Kesse-Guyot, L. Fezeu, P. Galan, S. Hercberg, S. Czernichow and K. Castetbon, Adherence to French nutritional guidelines is associated with lower risk of metabolic syndrome, J Nutr 141(6) (2011), 1134-1139
51. E. Kilic-Toprak, F. Ardic, G. Erken, F. Unver-Kocak, V. Kucukatay, M. Bor-Kucukatay, Hemorheological responses to progressive resistance exercise training in healthy young males, Med Sci Monit 18(6) (2012), CR351-CR360
52. P. Kopelman, Health risks associated with overweight and obesity, Obes Rev 8(Suppl 1) (2007), 13-7
53. L. Langeron, Gynoid and android obesity; estrogenic hypercorticism, Presse Med 60(19) (1952), 389-390
54. M. Lainscak, S. von Haehling, W. Doehner and S.D. Anker, The obesity paradox in chronic disease: Facts and numbers, J Cachexia Sarcopenia Muscle 3(1) (2012), 1-4
55. T.M. Larsen, S.M. Dalskov, M. van Baak, S.A. Jebb, A. Papadaki, A.F. Pfeiffer, J.A. Martinez, T. Handjieva-Darlenska, M. Kunešov́a, M. Pihlsgård, S. Stender, C. Holst, W.H. Saris and A. Astrup, Diet, Obesity, and Genes (Diogenes) Project. Diets with high or low protein content and glycemic index for weight-loss maintenance, N Engl J Med 363(22) (2010), 2102-2113
56. C. Le Devehat, T. Khodabandehlou and M. Dougny, Hemorheological parameters in isolated obesity, Diabete Metab 18(1) (1992), 43-47
57. A. Lev-Ran, Human obesity: An evolutionary approach to understanding our bulging waistline, Diabetes Metab Res Rev 17(5) (2001), 347-362
58. P.S. Maclean, A. Bergouignan, M.A. Cornier and M.R. Jackman, Biology's response to dieting: The impetus for weight regain, Am J Physiol Regul Integr Comp Physiol 301(3) (2011), R581-R600
59. A.H. Manninen, A Statement of the American Heart Association Nutrition Committee on Dietary Protein and Weight Reduction: A Rigorous Rebuttal, Metabolic Syndrome and Related Disorders 2 (2004), 9-13
60. J. Martini, B. Carpentier, A.C. Negrete, J.A. Frangos, and M. Intaglietta, Paradoxical hypotension following increased hematocrit and blood viscosity, Am J Physiol Heart Circ Physiol 289 (2005), H2136-H2143
61. National Institutes of Health, National Heart, Lung, and Blood Institute, Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults: The evidence report, Obes Res 6 (1998), 51S-209S.
62. J.H. O'Keefe, R. Vogel, C.J. Lavie and L. Cordain L, Achieving hunter-gatherer fitness in the 21 (st) century: Back to the future, Am J Med 123(12) (2010), 1082-1086
63. J.H. O'Keefe, R. Vogel, C.J. Lavie and L. Cordain L, Exercise like a hunter-gatherer: A prescription for organic physical fitness, Prog Cardiovasc Dis 53(6) (2011), 471-479
64. K. Parthasarathi and H.H. Lipowsky, Capillary recruitment in response to tissue hypoxia and its dependence on red blood cell deformability, Am J Physiol Heart Circ Physiol 277 (1999), H2145-H2157
65. J. Perkkiö, L.J. Wurzinger and H. Schmid-Schönbein, Fåhraeus-Vejlens effect: Margination of platelets and leukocytes in blood flow through branches, Thromb Res 50(3) (1988), 357-364
66. A.R. Pries, D. Neuhaus and P. Gaehtgens, Blood viscosity in tube flow: Dependence on diameter and hematocrit, Am J Physiol 263 (1992), H1770-H1778
67. E. Raynaud, A. Ṕerez-Martin, J.F. Brun, C. F́edou and J. Mercier, Insulin sensitivity measured with the minimal model is higher in moderately overweight women with predominantly lower body fat, Horm Metab Res 31(7) (1999), 415- 417
68. G.M. Reaven, Banting lecture 1988. Role of insulin resistance in human disease, Diabetes 37 (1988), 1595-1607
69. G.M. Reaven, Why a cluster is truly a cluster: Insulin resistance and cardiovascular disease, Clin Chem 54(5) (2008), 785-787
70. R. Redeker "L'emprise sportive" (The grip of sport), F. Bourin, ed, Paris 2012
71. C.D. Reimers, G. Knapp and A.K. Reimers, Does Physical Activity Increase Life, Expectancy? A Review of the Literature, J Aging Res 2012 (2012), 243958
72. V. Richter, M.D. Savery, M. Gassmann, O. Baum, E.R. Damiano and A.R. Pries, High hematocrit may compromise the blood-endothelium interface in erythropoietin-overexpressing mice, Biorheology 49 (2012), 172-173
73. S.A. Ritchie and J.M. Connell, The link between abdominal obesity, metabolic syndrome and cardiovascular disease, Nutr Metab Cardiovasc Dis 17(4) (2007), 319-326
74. B.J. Rolls and E.A. Bell, Dietary approaches to the treatment of obesity, Med Clin North Am 84(2) (2000) 401-418
75. M. Rosenbaum, J. Hirsch, D.A. Gallagher and R.L. Leibel, Long-term persistence of adaptive thermogenesis in subjects who have maintained a reduced body weight, Am J Clin Nutr 88 (2008), 906-912
76. R. Ross, D. Dagnone, P.J. Jones, H. Smith, A. Paddags, R. Hudson and I. Janssen, Reduction in obesity and related comorbid conditions after diet-induced weight loss or exercise-induced weight loss in men. A randomized, controlled trial, Ann Intern Med 133(2) (2000), 92-103
77. N.J. Rothwell and M.J. Stock, Regulation of energy balance, Annu Rev Nutr 1 (1981), 235-256
78. B.Y. Salazar V́azquez, M. Intaglietta, M. Rodŕiguez- Moŕan and F. Guerrero-Romero, Blood pressure and hematocrit in diabetes and the role of endothelial responses in the variability of blood viscosity, Diabetes Care 29 (2006), 1523- 1528
79. P. Schnohr, Longevity and causes of death in male athletic champions, Lancet 2(7738) (1971), 1364-1366
80. K.G. Seshadri, Obesity: A Venusian story of Paleolithic proportions, Indian J Endocrinol Metab 16(1) (2012), 134-135
81. C.A. Slentz, J.A. Houmard and W.E. Kraus, Modest exercise prevents the progressive disease associated with physical inactivity, Exerc Sport Sci Rev 35(1) (2007), 18-23
82. C.A. Slentz, J.A. Houmard and W.E. Kraus, Exercise, abdominal obesity, skeletal muscle, and metabolic risk: Evidence for a dose response, Obesity 17(Suppl 3) (2009), S27-S33
83. S. Simchon, K.M. Jan and S. Chien, Influence of reduced red cell deformability on regional blood flow, Am J Physiol Heart Circ Physiol 253(4) (1987), H898-H903
84. C.A. Slentz, J.A. Houmard and W.E. Kraus, Exercise, abdominal obesity, skeletal muscle, and metabolic risk: Evidence for a dose response, Obesity 17(Suppl 3) (2009), S27-S33
85. S. Soenen, G. Plasqui, A.J. Smeets and M.S. Westerterp-Plantenga, Protein intake induced an increase in exercise stimulated fat oxidation during stable body weight, Physiol Behav 101(5) (2010), 770-774
86. S.T. St Jeor, B.V. Howard, T.E. Prewitt, V. Bovee, T. Bazzarre and R.H. Eckel, Dietary protein and weight reduction: A statement for healthcare professionals from the Nutrition Committee of the Council on Nutrition, Physical Activity, and Metabolism of the American Heart Association, Circulation 104 (2001), 1869-1874
87. P. Sumithran, L.A. Prendergast, E. Delbridge, K. Purcell, A. Shulkes, A. Kriketos and J. Proietto, Long-term persistence of hormonal adaptations to weight loss, N Engl J Med 365(17) (2011), 1597-1604
88. B. Surawicz and B.F. Waller, The enigma of sudden cardiac death related to dieting, Can J Cardiol 11(3) (1995), 228-231
89. J.L. Thompson, Conference on "Multidisciplinary approaches to nutritional problems". Symposium on "Performance, exercise and health". Exercise in improving health vs performance, Proc Nutr Soc 68(1) (2009), 29-33
90. R.B. Terry, M.L. Stefanick, W.L. Haskell and P.D. Wood, Contributions of regional adipose tissue depots to plasma lipoprotein concentrations in overweight men and women: Possible protective effects of thigh fat, Metabolism 40(7) (1991), 733-740
91. A. Tremblay and E. Doucet, Influence of intense physical activity on energy balance and body fatness, Proc Nutr Soc 58(1) (1999), 99-105
92. J. Vague, The distinction of android and gynoid obesities as the base for their prognosis; Sem Hop 31(66) (1955), 3503-3609
93. J. Vague, P. Vague, M. Tramoni and B. Vialettes, Clinical features of diabetogenic and atherogenic obesity, Tohoku J Exp Med 141(Suppl) (1983), 147-159
94. H. Vink, B. Eskens, H. Mooij, H. Cobelens and J. van Teeffelen, Loss of glycocalyx dimension is reflected by an increase of the erythrocyte perfused boundary region, Biorheology 49 (2012), 172
95. M. S. Westerterp-Plantenga, A. Nieuwenhuizen, D. Toḿe, S. Soenen and K.R. Westerterp, Dietary protein, weight loss, and weight maintenance, Annu Rev Nutr 29 (2009), 21-41
96. E. Wright Jr, J.L. Scism-Bacon and L.C. Glass, Oxidative stress in type 2 diabetes: The role of fasting and postprandial glycaemia, Int J Clin Pract 60(3) (2006), 308-314.