Techniques to measure microcirculatory parameters in insulin resistant states in humans

Microcirculation and Insulin Resistance

Volumn , Issue , 2009, Pages 14-30

  Kraemer Aguiar, Luiz Guilherme ^a   Bouskela, Eliete ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Insulin resistance; Microcirculation; Techniques

Indexed keywords

EID: 84855893707     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.2174/978160805057410901010014     Document Type: Chapter

References (142)

1. Levy BI, Ambrosio G, Pries AR, Struijker-Boudier HA: Microcirculation in hypertension: a new target for treatment? Circulation 104:735-740, 2001.
2. Feihl F, Liaudet L, Waeber B, Levy BI: Hypertension: a disease of the microcirculation? Hypertension 48:1012-1017, 2006.
3. Sax FL, Cannon RO, III, Hanson C, Epstein SE: Impaired forearm vasodilator reserve in patients with microvascular angina. Evidence of a generalized disorder of vascular function? N Engl J Med 317:1366-1370, 1987.
4. Fichtlscherer S, Breuer S, Zeiher AM: Prognostic value of systemic endothelial dysfunction in patients with acute coronary syndromes: further evidence for the existence of the "vulnerable" patient. Circulation 110:1926-1932, 2004.
5. Johnson PC: Active and passive determinants of capillary density: a historical perspective. Int J Microcirc Clin Exp 15:218-222, 1995.
6. Verdant C, De BD: How monitoring of the microcirculation may help us at the bedside. Curr Opin Crit Care 11:240-244, 2005.
7. Haslam DW, James WP: Obesity. Lancet 366:1197-1209, 2005.
8. Mokdad AH, Bowman BA, Ford ES, Vinicor F, Marks JS, Koplan JP: The continuing epidemics of obesity and diabetes in the United States. JAMA 286:1195-1200, 2001.
9. Singleton JR, Smith AG, Russell JW, Feldman EL: Microvascular complications of impaired glucose tolerance. Diabetes 52:2867-2873, 2003.
10. van Leiden HA, Dekker JM, Moll AC, Nijpels G, Heine RJ, Bouter LM, Stehouwer CD, Polak BC: Blood pressure, lipids, and obesity are associated with retinopathy: the hoorn study. Diabetes Care 25:1320-1325, 2002.
11. de Jongh PE, Verhave J.C., Pinto-Siestma S.J., Hillege H.L.: Obesity and target organ damage: the kidney. Int J Obes Relat Metab Disord 26:S21-S24, 2002.
12. Kenchaiah S, Gaziano JM, Vasan RS: Impact of obesity on the risk of heart failure and survival after the onset of heart failure. Med Clin North Am 88:1273-1294, 2004.
13. Clark MG, Wallis MG, Barrett EJ, Vincent MA, Richards SM, Clerk LH, Rattigan S: Blood flow and muscle metabolism: a focus on insulin action. Am J Physiol Endocrinol Metab 284:E241-E258, 2003.
14. de Jongh RT, Serne EH, Ijzerman RG, de VG, Stehouwer CD: Impaired microvascular function in obesity: implications for obesity-associated microangiopathy, hypertension, and insulin resistance. Circulation 109:2529-2535, 2004.
15. Serne EH, Ijzerman RG, Gans RO, Nijveldt R, de VG, Evertz R, Donker AJ, Stehouwer CD: Direct evidence for insulin-induced capillary recruitment in skin of healthy subjects during physiological hyperinsulinemia. Diabetes 51:1515-1522, 2002.
16. Serne EH, Stehouwer CD, ter Maaten JC, ter Wee PM, Rauwerda JA, Donker AJ, Gans RO: Microvascular function relates to insulin sensitivity and blood pressure in normal subjects. Circulation 99:896-902, 1999.
17. Vollus GC, Bradley EA, Roberts MK, Newman JM, Richards SM, Rattigan S, Barrett EJ, Clark MG: Graded occlusion of perfused rat muscle vasculature decreases insulin action. Clin Sci (Lond) 112:457-466, 2007.
18. Barac A, Campia U, Panza JA: Methods for evaluating endothelial function in humans. Hypertension 49:748-760, 2007.
19. Holowatz LA, Thompson-Torgerson CS, Kenney WL: The human cutaneous circulation as a model of generalized microvascular function. J Appl Physiol 105:370-372, 2008.
20. Johnson PC: Active and passive determinants of capillary density: a historical perspective. Int J Microcirc Clin Exp 15:218-222, 1995.
21. Wright CI, Kroner CI, Draijer R: Non-invasive methods and stimuli for evaluating the skin's microcirculation. J Pharmacol Toxicol Methods 54:1-25, 2006.
22. Leahy MJ, de Mul FF, Nilsson GE, Maniewski R: Principles and practice of the laser-Doppler perfusion technique. Technol Health Care 7:143-162, 1999.
23. Kubli S, Waeber B, Leave A, Feihl F: Reproducibility of laser Doppler imaging of skin blood flow as a tool to assess endothelial function. J Cardiovasc Pharmacol 36:640-648, 2000.
24. Newton DJ, Khan F, Belch JJ: Assessment of microvascular endothelial function in human skin. Clin Sci (Lond) 101:567-572, 2001.
25. Cracowski JL, Minson CT, Salvat-Melis M, Halliwill JR: Methodological issues in the assessment of skin microvascular endothelial function in humans. Trends Pharmacol Sci 27:503-508, 2006.
26. Khan F, Elhadd TA, Greene SA, Belch JJ: Impaired skin microvascular function in children, adolescents, and young adults with type 1 diabetes. Diabetes Care 23:215-220, 2000.
27. Kruger A, Stewart J, Sahityani R, O'Riordan E, Thompson C, Adler S, Garrick R, Vallance P, Goligorsky MS: Laser Doppler flowmetry detection of endothelial dysfunction in end-stage renal disease patients: correlation with cardiovascular risk. Kidney Int 70:157-164, 2006.
28. Ijzerman RG, de Jongh RT, Beijk MA, van Weissenbruch MM, Delemarre-van de Waal HA, Serne EH, Stehouwer CD: Individuals at increased coronary heart disease risk are characterized by an impaired microvascular function in skin. Eur J Clin Invest 33:536-542, 2003.
29. Pierzga JM, Frymoyer A, Kenney WL: Delayed distribution of active vasodilation and altered vascular conductance in aged skin. J Appl Physiol 94:1045-1053, 2003.
30. Wong BJ, Wilkins BW, Holowatz LA, Minson CT: Nitric oxide synthase inhibition does not alter the reactive hyperemic response in the cutaneous circulation. J Appl Physiol 95:504-510, 2003.
31. Holowatz LA, Thompson CS, Kenney WL: L-Arginine supplementation or arginase inhibition augments reflex cutaneous vasodilatation in aged human skin. J Physiol 574:573-581, 2006.
32. Minson CT, Holowatz LA, Wong BJ, Kenney WL, Wilkins BW: Decreased nitric oxide- and axon reflexmediated cutaneous vasodilation with age during local heating. J Appl Physiol 93:1644-1649, 2002.
33. Thompson-Torgerson CS, Holowatz LA, Flavahan NA, Kenney WL: Cold-induced cutaneous vasoconstriction is mediated by Rho kinase in vivo in human skin. Am J Physiol Heart Circ Physiol 292:H1700-H1705, 2007.
34. Abahji TN, Nill L, Ide N, Keller C, Hoffmann U, Weiss N: Acute hyperhomocysteinemia induces microvascular and macrovascular endothelial dysfunction. Arch Med Res 38:411-416, 2007.
35. Minson CT, Berry LT, Joyner MJ: Nitric oxide and neurally mediated regulation of skin blood flow during local heating. J Appl Physiol 91:1619-1626, 2001.
36. Lorenzo S, Minson CT: Human cutaneous reactive hyperaemia: role of BKCa channels and sensory nerves. J Physiol 585:295-303, 2007.
37. Kvandal P, Stefanovska A, Veber M, Kvernmo HD, Kirkeboen KA: Regulation of human cutaneous circulation evaluated by laser Doppler flowmetry, iontophoresis, and spectral analysis: importance of nitric oxide and prostaglandines. Microvasc Res 65:160-171, 2003.
38. Celermajer DS: Statins, skin, and the search for a test of endothelial function. J Am Coll Cardiol 42:78-80, 2003.
39. Stefanovska A, Bracic M, Kvernmo HD: Wavelet analysis of oscillations in the peripheral blood circulation measured by laser Doppler technique. IEEE Trans Biomed Eng 46:1230-1239, 1999.
40. Abularrage CJ, Sidawy AN, Aidinian G, Singh N, Weiswasser JM, Arora S: Evaluation of the microcirculation in vascular disease. J Vasc Surg 42:574-581, 2005.
41. Boignard A, Salvat-Melis M, Carpentier PH, Minson CT, Grange L, Duc C, Sarrot-Reynauld F, Cracowski JL: Local hyperemia to heating is impaired in secondary Raynaud's phenomenon. Arthritis Res Ther 7:R1103-R1112, 2005.
42. Fagrell B, Intaglietta M: Microcirculation: its significance in clinical and molecular medicine. J Intern Med 241:349-362, 1997.
43. Fagrell B: Microcirculatory methods for the clinical assessment of hypertension, hypotension, and ischemia. Ann Biomed Eng 14:163-173, 1986.
44. Braverman IM: The cutaneous microcirculation: ultrastructure and microanatomical organization. Microcirculation 4:329-340, 1997.
45. Shore AC: Capillaroscopy and the measurement of capillary pressure. Br J Clin Pharmacol 50:501-513, 2000.
46. Bollinger A, Saesseli B, Hoffmann U, Franzeck UK: Intravital detection of skin capillary aneurysms by videomicroscopy with indocyanine green in patients with progressive systemic sclerosis and related disorders. Circulation 83:546-551, 1991.
47. Moneta G, Brulisauer M, Jager K, Bollinger A: Infrared fluorescence videomicroscopy of skin capillaries with indocyanine green. Int J Microcirc Clin Exp 6:25-34, 1987.
48. Bollinger A, Butti P, Barras JP, Trachsler H, Siegenthaler W: Red blood cell velocity in nailfold capillaries of man measured by a television microscopy technique. Microvasc Res 7:61-72, 1974.
49. Fagrell B, Fronek A, Intaglietta M: A microscope-television system for studying flow velocity in human skin capillaries. Am J Physiol 233:H318-H321, 1977.
50. Kraemer de Aguiar LG, Laflor CM, Bahia L, Villela NR, Wiernsperger N, Bottino DA, Bouskela E: Metformin improves skin capillary reactivity in normoglycaemic subjects with the metabolic syndrome. Diabet Med 24:272-279, 2007.
51. Kraemer-Aguiar LG, Laflor CM, Bouskela E: Skin microcirculatory dysfunction is already present in normoglycemic subjects with metabolic syndrome. Metabolism 57:1740-1746, 2008.
52. Montagna W, Carlisle K: Structural changes in aging human skin. J Invest Dermatol 73:47-53, 1979.
53. de Jongh RT, Ijzerman RG, Serne EH, Voordouw JJ, Yudkin JS, de Waal HA, Stehouwer CD, van Weissenbruch MM: Visceral and truncal subcutaneous adipose tissue are associated with impaired capillary recruitment in healthy individuals. J Clin Endocrinol Metab 91:5100-5106, 2006.
54. Shamim-Uzzaman QA, Pfenninger D, Kehrer C, Chakrabarti A, Kacirotti N, Rubenfire M, Brook R, Rajagopalan S: Altered cutaneous microvascular responses to reactive hyperaemia in coronary artery disease: a comparative study with conduit vessel responses. Clin Sci (Lond) 103:267-273, 2002.
55. Antonios TF, Kaski JC, Hasan KM, Brown SJ, Singer DR: Rarefaction of skin capillaries in patients with anginal chest pain and normal coronary arteriograms. Eur Heart J 22:1144-1148, 2001.
56. Pasqui AL, Puccetti L, Di RM, Bruni F, Camarri A, Palazzuoli A, Biagi F, Servi M, Bischeri D, Auteri A, Pastorelli M: Structural and functional abnormality of systemic microvessels in cardiac syndrome X. Nutr Metab Cardiovasc Dis 15:56-64, 2005.
57. Schiessler C, Schaudig S, Harris AG, Christ F: [Orthogonal polarization spectral imaging--a new clinical method for monitoring of microcirculation]. Anaesthesist 51:576-579, 2002.
58. Lupi O, Semenovitch I, Treu C, Bouskela E: Orthogonal polarization technique in the assessment of human skin microcirculation. Int J Dermatol 47:425-431, 2008.
59. Turek Z, Cerny V, Parizkova R: Noninvasive in vivo assessment of the skeletal muscle and small intestine serous surface microcirculation in rat: sidestream dark-field (SDF) imaging. Physiol Res 57:365-371, 2008.
60. De BD, Dubois MJ: Assessment of the microcirculatory flow in patients in the intensive care unit. Curr Opin Crit Care 7:200-203, 2001.
61. Cerny V, Turek Z, Parizkova R: Orthogonal polarization spectral imaging. Physiol Res 56:141-147, 2007.
62. Groner W, Winkelman JW, Harris AG, Ince C, Bouma GJ, Messmer K, et al: Orthogonal polarization spectral imaging: A new method for study of the microcirculation. Nature Medicine 5:1209-1213, 1999.
63. Milner SM, Bhat S, Gulati S, Gherardini G, Smith CE, Bick RJ: Observations on the microcirculation of the human burn wound using orthogonal polarization spectral imaging. Burns 31:316-319, 2005.
64. Erdmann D, Sweis R, Wong MS, Eyler CE, Olbrich KC, Levin LS, Germann G, Klitzman B: [Current perspectives of orthogonal polarization spectral imaging in plastic surgery]. Chirurg 73:827-832, 2002.
65. Chierego M, Verdant C, De BD: Microcirculatory alterations in critically ill patients. Minerva Anestesiol 72:199-205, 2006.
66. Lipowsky HH, Sheikh NU, Katz DM: Intravital microscopy of capillary hemodynamics in sickle cell disease. J Clin Invest 80:117-127, 1987.
67. De BD: OPS techniques. Minerva Anestesiol 69:388-391, 2003.
68. Pahernik S, Harris AG, Schmitt-Sody M, Krasnici S, Goetz AE, Dellian M, Messmer K: Orthogonal polarisation spectral imaging as a new tool for the assessment of antivascular tumour treatment in vivo: a validation study. Br J Cancer 86:1622-1627, 2002.
69. Harris AG, Sinitsina I, Messmer K: The Cytoscan Model E-II, a new reflectance microscope for intravital microscopy: comparison with the standard fluorescence method. J Vasc Res 37:469-476, 2000.
70. Harris AG, Sinitsina I, Messmer K: Validation of OPS imaging for microvascular measurements during isovolumic hemodilution and low hematocrits. Am J Physiol Heart Circ Physiol 282:H1502-H1509, 2002.
71. Mathura KR, Vollebregt KC, Boer K, De Graaff JC, Ubbink DT, Ince C: Comparison of OPS imaging and conventional capillary microscopy to study the human microcirculation. J Appl Physiol 91:74-78, 2001.
72. Langer S, Harris AG, Biberthaler P, von DE, Messmer K: Orthogonal polarization spectral imaging as a tool for the assessment of hepatic microcirculation: a validation study. Transplantation 71:1249-1256, 2001.
73. Lascasas-Porto CL, Milhomens AL, Virgini-Magalhaes CE, Fernandes FF, Sicuro FL, Bouskela E: Use of microcirculatory parameters to evaluate clinical treatments of chronic venous disorder (CVD). Microvasc Res 76:66-72, 2008.
74. Moncada S, Higgs A: The L-arginine-nitric oxide pathway. N Engl J Med 329:2002-2012, 1993.
75. Ludmer PL, Selwyn AP, Shook TL, Wayne RR, Mudge GH, Alexander RW, Ganz P: Paradoxical vasoconstriction induced by acetylcholine in atherosclerotic coronary arteries. N Engl J Med 315:1046-1051, 1986.
76. Werns SW, Walton JA, Hsia HH, Nabel EG, Sanz ML, Pitt B: Evidence of endothelial dysfunction in angiographically normal coronary arteries of patients with coronary artery disease. Circulation 79:287-291, 1989.
77. Zeiher AM, Drexler H, Wollschlager H, Just H: Endothelial dysfunction of the coronary microvasculature is associated with coronary blood flow regulation in patients with early atherosclerosis. Circulation 84:1984-1992, 1991.
78. Gould KL, Martucci JP, Goldberg DI, Hess MJ, Edens RP, Latifi R, Dudrick SJ: Short-term cholesterol lowering decreases size and severity of perfusion abnormalities by positron emission tomography after dipyridamole in patients with coronary artery disease. A potential noninvasive marker of healing coronary endothelium. Circulation 89:1530-1538, 1994.
79. Aengevaeren WR, Uijen GJ, Jukema JW, Bruschke AV, van der WT: Functional evaluation of lipidlowering therapy by pravastatin in the Regression Growth Evaluation Statin Study (REGRESS). Circulation 96:429-435, 1997.
80. Hokanson DE, Sumner DS, Strandness DE, Jr.: An electrically calibrated plethysmograph for direct measurement of limb blood flow. IEEE Trans Biomed Eng 22:25-29, 1975.
81. Anderson TJ: Assessment and treatment of endothelial dysfunction in humans. J Am Coll Cardiol 34:631-638, 1999.
82. Linder L, Kiowski W, Buhler FR, Luscher TF: Indirect evidence for release of endothelium-derived relaxing factor in human forearm circulation in vivo. Blunted response in essential hypertension. Circulation 81:1762-1767, 1990.
83. Panza JA, Quyyuml AA, Brush Jr JE, Epstein SE: Abnormal endothelium-dependent vascular relaxation in patients with essential hypertension. New England Journal of Medicine 323:22-27, 1990.
84. Creager MA, Cooke JP, Mendelsohn ME, Gallagher SJ, Coleman SM, Loscalzo J, Dzau VJ: Impaired vasodilation of forearm resistance vessels in hypercholesterolemic humans. J Clin Invest 86:228-234, 1990.
85. Johnstone MT, Creager SJ, Scales KM, Cusco JA, Lee BK, Creager MA: Impaired endothelium-dependent vasodilation in patients with insulin-dependent diabetes mellitus. Circulation 88:2510-2516, 1993.
86. Chowienczyk PJ, Watts GF, Cockcroft JR, Ritter JM: Impaired endothelium-dependent vasodilation of forearm resistance vessels in hypercholesterolaemia. Lancet 340:1430-1432, 1992.
87. Williams SB, Cusco JA, Roddy MA, Johnstone MT, Creager MA: Impaired nitric oxide-mediated vasodilation in patients with non-insulin-dependent diabetes mellitus. J Am Coll Cardiol 27:567-574, 1996.
88. Anderson TJ, Uehata A, Gerard MD, Meredith IT, Knab S, Delagrange D, et al: Close relation of endothelial function in the human coronary and peripheral circulations. Journal of the American College of Cardiology 26:1235-1241, 1995.
89. Celermajer DS, Sorensen KE, Bull C, Robinson J, Deanfield JE: Endothelium-dependent dilation in the systemic arteries of asymptomatic subjects relates to coronary risk factors and their interaction. J Am Coll Cardiol 24:1468-1474, 1994.
90. Clarkson P, Celermajer DS, Donald AE, Sampson M, Sorensen KE, Adams M, Yue DK, Betteridge DJ, Deanfield JE: Impaired vascular reactivity in insulin-dependent diabetes mellitus is related to disease duration and low density lipoprotein cholesterol levels. J Am Coll Cardiol 28:573-579, 1996.
91. Lambert J, Aarsen M, Donker AJ, Stehouwer CD: Endothelium-dependent and -independent vasodilation of large arteries in normoalbuminuric insulin-dependent diabetes mellitus. Arterioscler Thromb Vasc Biol 16:705-711, 1996.
92. Schachinger V, Britten MB, Zeiher AM: Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation 101:1899-1906, 2000.
93. Suwaidi JA, Hamasaki S, Higano ST, Nishimura RA, Holmes DR, Jr., Lerman A: Long-term follow-up of patients with mild coronary artery disease and endothelial dysfunction. Circulation 101:948-954, 2000.
94. Lind L, Hall J, Johansson K: Evaluation of four different methods to measure endothelium-dependent vasodilation in the human peripheral circulation. Clin Sci (Lond) 102:561-567, 2002.
95. Lind L, Hall J, Larsson A, Annuk M, Fellstrom B, Lithell H: Evaluation of endothelium-dependent vasodilation in the human peripheral circulation. Clin Physiol 20:440-448, 2000.
96. Laakso M, Edelman SV, Brechtel G, Baron AD: Decreased effect of insulin to stimulate skeletal muscle blood flow in obese man. A novel mechanism for insulin resistance. J Clin Invest 85:1844-1852, 1990.
97. Baron AD, Laakso M, Brechtel G, Edelman SV: Reduced capacity and affinity of skeletal muscle for insulin-mediated glucose uptake in noninsulin-dependent diabetic subjects. Effects of insulin therapy. J Clin Invest 87:1186-1194, 1991.
98. Baron AD, Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G: Insulin-mediated skeletal muscle vasodilation contributes to both insulin sensitivity and responsiveness in lean humans. J Clin Invest 96:786-792, 1995.
99. Cleland SJ, Petrie JR, Ueda S, Elliott HL, Connell JM: Insulin-mediated vasodilation and glucose uptake are functionally linked in humans. Hypertension 33:554-558, 1999.
100. Wilkinson IB, Webb DJ: Venous occlusion plethysmography in cardiovascular research: methodology and clinical applications. Br J Clin Pharmacol 52:631-646, 2001.
101. Joannides R, Bellien J, Thuillez C: Clinical methods for the evaluation of endothelial function-- a focus on resistance arteries. Fundam Clin Pharmacol 20:311-320, 2006.
102. Dahn I, Hallbook T: Simultaneous blood flow measurements by water and strain gauge plethysmography. Scand J Clin Lab Invest 25:419-428, 1970.
103. Webb DJ: The pharmacology of human blood vessels in vivo. J Vasc Res 32:2-15, 1995.
104. Gilligan DM, Guetta V, Panza JA, Garcia CE, Quyyumi AA, Cannon RO, III: Selective loss of microvascular endothelial function in human hypercholesterolemia. Circulation 90:35-41, 1994.
105. Higashi Y, Sasaki S, Kurisu S, Yoshimizu A, Sasaki N, Matsuura H, Kajiyama G, Oshima T: Regular aerobic exercise augments endothelium-dependent vascular relaxation in normotensive as well as hypertensive subjects: role of endothelium-derived nitric oxide. Circulation 100:1194-1202, 1999.
106. Taddei S, Virdis A, Ghiadoni L, Mattei P, Sudano I, Bernini G, Pinto S, Salvetti A: Menopause is associated with endothelial dysfunction in women. Hypertension 28:576-582, 1996.
107. Joyner MJ, Dietz NM, Shepherd JT: From Belfast to Mayo and beyond: the use and future of plethysmography to study blood flow in human limbs. J Appl Physiol 91:2431-2441, 2001.
108. DeSouza CA, Shapiro LF, Clevenger CM, Dinenno FA, Monahan KD, Tanaka H, Seals DR: Regular aerobic exercise prevents and restores age-related declines in endothelium-dependent vasodilation in healthy men. Circulation 102:1351-1357, 2000.
109. Taddei S, Galetta F, Virdis A, Ghiadoni L, Salvetti G, Franzoni F, Giusti C, Salvetti A: Physical activity prevents age-related impairment in nitric oxide availability in elderly athletes. Circulation 101:2896-2901, 2000.
110. Sasaki S, Higashi Y, Nakagawa K, Kimura M, Noma K, Sasaki S, Hara K, Matsuura H, Goto C, Oshima T, Chayama K: A low-calorie diet improves endothelium-dependent vasodilation in obese patients with essential hypertension. Am J Hypertens 15:302-309, 2002.
111. Taddei S, Virdis A, Ghiadoni L, Magagna A, Salvetti A: Vitamin C improves endothelium-dependent vasodilation by restoring nitric oxide activity in essential hypertension. Circulation 97:2222-2229, 1998.
112. de Aguiar LG, Bahia LR, Villela N, Laflor C, Sicuro F, Wiernsperger N, Bottino D, Bouskela E: Metformin improves endothelial vascular reactivity in first-degree relatives of type 2 diabetic patients with metabolic syndrome and normal glucose tolerance. Diabetes Care 29:1083-1089, 2006.
113. Bahia L, Aguiar LG, Villela N, Bottino D, Godoy-Matos AE, Geloneze B, Tambascia M, Bouskela E: Adiponectin is associated with improvement of endothelial function after rosiglitazone treatment in nondiabetic individuals with metabolic syndrome. Atherosclerosis 195:138-146, 2007.
114. Pasimeni G, Ribaudo MC, Capoccia D, Rossi F, Bertone C, Leonetti F, Santiemma V: Non-invasive evaluation of endothelial dysfunction in uncomplicated obesity: relationship with insulin resistance. Microvasc Res 71:115-120, 2006.
115. Takeshita A, Mark AL: Decreased vasodilator capacity of forearm resistance vessels in borderline hypertension. Hypertension 2:610-616, 1980.
116. Conway J: A vascular abnormality in hypertension. A study of blood flow in the forearm. Circulation 27:520-529, 1963.
117. Folkow B: Physiological aspects of primary hypertension. Physiol Rev 62:347-504, 1982.
118. Julius S, Mejia A, Jones K, Krause L, Schork N, van d, V, Johnson E, Petrin J, Sekkarie MA, Kjeldsen SE, .: "White coat" versus "sustained" borderline hypertension in Tecumseh, Michigan. Hypertension 16:617-623, 1990.
119. Brown E, Greenfield DM, Goei JS, Plassaras G: Filling and emptying of the low-pressure blood vessels of the human forearm. J Appl Physiol 21:573-582, 1966.
120. Gamble J, Gartside IB, Christ F: A reassessment of mercury in silastic strain gauge plethysmography for microvascular permeability assessment in man. J Physiol 464:407-422, 1993.
121. Roberts DH, Tsao Y, Breckenridge AM: The reproducibility of limb blood flow measurements in human volunteers at rest and after exercise by using mercury-in-Silastic strain gauge plethysmography under standardized conditions. Clin Sci (Lond) 70:635-638, 1986.
122. Cooke JP, Dzau VJ: Nitric oxide synthase: role in the genesis of vascular disease. Annu Rev Med 48:489-509, 1997.
123. Petrie JR, Ueda S, Morris AD, Murray LS, Elliott HL, Connell JM: How reproducible is bilateral forearm plethysmography? Br J Clin Pharmacol 45:131-139, 1998.
124. Walker HA, Jackson G, Ritter JM, Chowienczyk PJ: Assessment of forearm vasodilator responses to acetylcholine and albuterol by strain gauge plethysmography: reproducibility and influence of strain gauge placement. Br J Clin Pharmacol 51:225-229, 2001.
125. Chou CC, Hsieh CP, Yu YM, Kvietys P, Yu LC, Pittman R, Dabney JM: Localization of mesenteric hyperemia during digestion in dogs. Am J Physiol 230:583-589, 1976.
126. Wei K, Jayaweera AR, Firoozan S, Linka A, Skyba DM, Kaul S: Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion. Circulation 97:473-483, 1998.
127. Krix M, Weber MA, Krakowski-Roosen H, Huttner HB, Delorme S, Kauczor HU, Hildebrandt W: Assessment of skeletal muscle perfusion using contrast-enhanced ultrasonography. J Ultrasound Med 24:431-441, 2005.
128. Clark MG, Rattigan S, Barrett EJ, Vincent MA: Point: There is capillary recruitment in active skeletal muscle during exercise. J Appl Physiol 104:889-891, 2008.
129. Wei K, Skyba DM, Firschke C, Jayaweera AR, Lindner JR, Kaul S: Interactions between microbubbles and ultrasound: in vitro and in vivo observations. J Am Coll Cardiol 29:1081-1088, 1997.
130. Dawson D, Vincent MA, Barrett EJ, Kaul S, Clark A, Leong-Poi H, Lindner JR: Vascular recruitment in skeletal muscle during exercise and hyperinsulinemia assessed by contrast ultrasound. Am J Physiol Endocrinol Metab 282:E714-E720, 2002.
131. Vincent MA, Clerk LH, Lindner JR, Price WJ, Jahn LA, Leong-Poi H, Barrett EJ: Mixed meal and light exercise each recruit muscle capillaries in healthy humans. Am J Physiol Endocrinol Metab 290:E1191-E1197, 2006.
132. Mahajan H, Richards SM, Rattigan S, Clark MG: Local methacholine but not bradykinin potentiates insulin-mediated glucose uptake in muscle in vivo by augmenting capillary recruitment. Diabetologia 47:2226-2234, 2004.
133. Rattigan S, Clark MG, Barrett EJ: Hemodynamic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes 46:1381-1388, 1997.
134. Vincent MA, Clerk LH, Lindner JR, Klibanov AL, Clark MG, Rattigan S, Barrett EJ: Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. Diabetes 53:1418-1423, 2004.
135. Zhang L, Vincent MA, Richards SM, Clerk LH, Rattigan S, Clark MG, Barrett EJ: Insulin sensitivity of muscle capillary recruitment in vivo. Diabetes 53:447-453, 2004.
136. Mahajan H, Kolka CM, Newman JM, Rattigan S, Richards SM, Clark MG: Vascular and metabolic effects of methacholine in relation to insulin action in muscle. Diabetologia 49:713-723, 2006.
137. Rattigan S, Zhang L, Mahajan H, Kolka CM, Richards SM, Clark MG: Factors influencing the hemodynamic and metabolic effects of insulin in muscle. Curr Diabetes Rev 2:61-70, 2006.
138. Coppack SW, Persson M, Miles JM: Phenylalanine kinetics in human adipose tissue. J Clin Invest 98:692-697, 1996.
139. Kjellmer I, Lindbjerg I, Prerovsky I, Tonnesen H: The relation between blood flow in an isolated muscle measured with the Xe133 clearance and a direct recording technique. Acta Physiol Scand 69:69-78, 1967.
140. Lalande S, Gusso S, Hofman PL, Baldi JC: Reduced leg blood flow during submaximal exercise in type 2 diabetes. Med Sci Sports Exerc 40:612-617, 2008.
141. Hachiya T, Blaber AP, Saito M: Near-infrared spectroscopy provides an index of blood flow and vasoconstriction in calf skeletal muscle during lower body negative pressure. Acta Physiol (Oxf) 193:117-127, 2008.
142. Heinonen I, Nesterov SV, Kemppainen J, Nuutila P, Knuuti J, Laitio R, Kjaer M, Boushel R, Kalliokoski KK: Role of adenosine in regulating the heterogeneity of skeletal muscle blood flow during exercise in humans. J Appl Physiol 103:2042-2048, 2007.