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Published in: Cardiovascular Diabetology 1/2008

Open Access 01-12-2008 | Original investigation

Effect of streptozotocin-induced diabetes on myocardial blood flow reserve assessed by myocardial contrast echocardiography in rats

Authors: Bernard Cosyns, Steven Droogmans, Sophie Hernot, Céline Degaillier, Christian Garbar, Caroline Weytjens, Bram Roosens, Danny Schoors, Tony Lahoutte, Philippe R Franken, Guy Van Camp

Published in: Cardiovascular Diabetology | Issue 1/2008

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Abstract

Abstract

The role of structural and functional abnormalities of small vessels in diabetes cardiomyopathy remains unclear. Myocardial contrast echocardiography allows the quantification of myocardial blood flow at rest and during dipyridamole infusion. The aim of the study was to determine the myocardial blood flow reserve in normal rats compared with Streptozotocin-induced diabetic rats using contrast echocardiography.

Methods

We prospectively studied 40 Wistar rats. Diabetes was induced by intravenous streptozotocin in 20 rats. All rats underwent baseline and stress (dipyridamole: 20 mg/kg) high power intermittent imaging in short axis view under anaesthesia baseline and after six months. Myocardial blood flow was determined and compared at rest and after dipyridamole in both populations. The myocardial blood flow reserve was calculated and compared in the 2 groups. Parameters of left ventricular function were determined from the M-mode tracings and histological examination was performed in all rats at the end of the study.

Results

At six months, myocardial blood flow reserve was significantly lower in diabetic rats compared to controls (3.09 ± 0.98 vs. 1.28 ± 0.67 ml min-1 g-1; p < 0.05). There were also a significant decrease in left ventricular function and a decreased capillary surface area and diameter at histology in the diabetic group.

Conclusion

In this animal study, diabetes induced a functional alteration of the coronary microcirculation, as demonstrated by contrast echocardiography, a decrease in capillary density and of the cardiac systolic function. These findings may offer new insights into the underlying mechanisms of diabetes cardiomyopathy.
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Literature
2.
go back to reference Fang ZY, Prins JB, Marwick TH: Diabetic Cardiomyopathy: Evidence, Mechanisms, and Therapeutic Implications. Endocr Rev. 2004, 25 (4): 543-567. 10.1210/er.2003-0012.CrossRefPubMed Fang ZY, Prins JB, Marwick TH: Diabetic Cardiomyopathy: Evidence, Mechanisms, and Therapeutic Implications. Endocr Rev. 2004, 25 (4): 543-567. 10.1210/er.2003-0012.CrossRefPubMed
3.
go back to reference Cosyns B, Droogmans S, Weytjens C, Lahoutte T, Van Camp G, Schoors D, Franken PR: Effect of streptozotocin-induced diabetes on left ventricular function in adult rats: an in vivo Pinhole Gated SPECT study. Cardiovasc Diabetol. 2007, 6: 30-10.1186/1475-2840-6-30.PubMedCentralCrossRefPubMed Cosyns B, Droogmans S, Weytjens C, Lahoutte T, Van Camp G, Schoors D, Franken PR: Effect of streptozotocin-induced diabetes on left ventricular function in adult rats: an in vivo Pinhole Gated SPECT study. Cardiovasc Diabetol. 2007, 6: 30-10.1186/1475-2840-6-30.PubMedCentralCrossRefPubMed
4.
go back to reference Strauer BE, Motz W, Vogt M, Schwartzkopff B: Impaired coronary flow reserve in NIDDM: a possible role for diabetic cardiopathy in humans. Diabetes. 1997, 46 Suppl 2: S119-24.CrossRefPubMed Strauer BE, Motz W, Vogt M, Schwartzkopff B: Impaired coronary flow reserve in NIDDM: a possible role for diabetic cardiopathy in humans. Diabetes. 1997, 46 Suppl 2: S119-24.CrossRefPubMed
5.
go back to reference Nitenberg A, Valensi P, Sachs R, Dali M, Aptecar E, Attali JR: Impairment of coronary vascular reserve and ACh-induced coronary vasodilation in diabetic patients with angiographically normal coronary arteries and normal left ventricular systolic function. Diabetes. 1993, 42 (7): 1017-1025. 10.2337/diabetes.42.7.1017.CrossRefPubMed Nitenberg A, Valensi P, Sachs R, Dali M, Aptecar E, Attali JR: Impairment of coronary vascular reserve and ACh-induced coronary vasodilation in diabetic patients with angiographically normal coronary arteries and normal left ventricular systolic function. Diabetes. 1993, 42 (7): 1017-1025. 10.2337/diabetes.42.7.1017.CrossRefPubMed
6.
go back to reference Nitenberg A, Foult JM, Blanchet F, Zouioueche S: Multifactorial determinants of reduced coronary flow reserve after dipyridamole in dilated cardiomyopathy. Am J Cardiol. 1985, 55 (6): 748-754. 10.1016/0002-9149(85)90150-X.CrossRefPubMed Nitenberg A, Foult JM, Blanchet F, Zouioueche S: Multifactorial determinants of reduced coronary flow reserve after dipyridamole in dilated cardiomyopathy. Am J Cardiol. 1985, 55 (6): 748-754. 10.1016/0002-9149(85)90150-X.CrossRefPubMed
7.
go back to reference Treasure CB, Vita JA, Cox DA, Fish RD, Gordon JB, Mudge GH, Colucci WS, Sutton MG, Selwyn AP, Alexander RW: Endothelium-dependent dilation of the coronary microvasculature is impaired in dilated cardiomyopathy. Circulation. 1990, 81 (3): 772-779.CrossRefPubMed Treasure CB, Vita JA, Cox DA, Fish RD, Gordon JB, Mudge GH, Colucci WS, Sutton MG, Selwyn AP, Alexander RW: Endothelium-dependent dilation of the coronary microvasculature is impaired in dilated cardiomyopathy. Circulation. 1990, 81 (3): 772-779.CrossRefPubMed
8.
go back to reference Durante W, Sunahara FA, Sen AK: Effect of diabetes on metabolic coronary dilatation in the rat. Cardiovasc Res. 1989, 23 (1): 40-45. 10.1093/cvr/23.1.40.CrossRefPubMed Durante W, Sunahara FA, Sen AK: Effect of diabetes on metabolic coronary dilatation in the rat. Cardiovasc Res. 1989, 23 (1): 40-45. 10.1093/cvr/23.1.40.CrossRefPubMed
9.
go back to reference Wei K, Ragosta M, Thorpe J, Coggins M, Moos S, Kaul S: Noninvasive quantification of coronary blood flow reserve in humans using myocardial contrast echocardiography. Circulation. 2001, 103 (21): 2560-2565.CrossRefPubMed Wei K, Ragosta M, Thorpe J, Coggins M, Moos S, Kaul S: Noninvasive quantification of coronary blood flow reserve in humans using myocardial contrast echocardiography. Circulation. 2001, 103 (21): 2560-2565.CrossRefPubMed
10.
go back to reference Jayaweera AR, Wei K, Coggins M, Bin JP, Goodman C, Kaul S: Role of capillaries in determining CBF reserve: new insights using myocardial contrast echocardiography. Am J Physiol. 1999, 277 (6 Pt 2): H2363-72.PubMed Jayaweera AR, Wei K, Coggins M, Bin JP, Goodman C, Kaul S: Role of capillaries in determining CBF reserve: new insights using myocardial contrast echocardiography. Am J Physiol. 1999, 277 (6 Pt 2): H2363-72.PubMed
11.
go back to reference Van Camp G, Ay T, Pasquet A, London V, Bol A, Gisellu G, Hendrickx G, Rafter P, Melin JA, Vanoverschelde JL: Quantification of myocardial blood flow and assessment of its transmural distribution with real-time power modulation myocardial contrast echocardiography. J Am Soc Echocardiogr. 2003, 16 (3): 263-270. 10.1067/mje.2003.55.CrossRefPubMed Van Camp G, Ay T, Pasquet A, London V, Bol A, Gisellu G, Hendrickx G, Rafter P, Melin JA, Vanoverschelde JL: Quantification of myocardial blood flow and assessment of its transmural distribution with real-time power modulation myocardial contrast echocardiography. J Am Soc Echocardiogr. 2003, 16 (3): 263-270. 10.1067/mje.2003.55.CrossRefPubMed
12.
go back to reference Vogel R, Indermuhle A, Reinhardt J, Meier P, Siegrist PT, Namdar M, Kaufmann PA, Seiler C: The quantification of absolute myocardial perfusion in humans by contrast echocardiography: algorithm and validation. J Am Coll Cardiol. 2005, 45 (5): 754-762. 10.1016/j.jacc.2004.11.044.CrossRefPubMed Vogel R, Indermuhle A, Reinhardt J, Meier P, Siegrist PT, Namdar M, Kaufmann PA, Seiler C: The quantification of absolute myocardial perfusion in humans by contrast echocardiography: algorithm and validation. J Am Coll Cardiol. 2005, 45 (5): 754-762. 10.1016/j.jacc.2004.11.044.CrossRefPubMed
13.
go back to reference 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. 1998, 97 (5): 473-483.CrossRefPubMed 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. 1998, 97 (5): 473-483.CrossRefPubMed
14.
go back to reference Weytjens C, Franken PR, D'Hooge J, Droogmans S, Cosyns B, Lahoutte T, Van Camp G: Doppler myocardial imaging in the diagnosis of early systolic left ventricular dysfunction in diabetic rats. Eur J Echocardiogr. 2008, 9 (3): 326-333. 10.1093/ejechocard/jen123.CrossRefPubMed Weytjens C, Franken PR, D'Hooge J, Droogmans S, Cosyns B, Lahoutte T, Van Camp G: Doppler myocardial imaging in the diagnosis of early systolic left ventricular dysfunction in diabetic rats. Eur J Echocardiogr. 2008, 9 (3): 326-333. 10.1093/ejechocard/jen123.CrossRefPubMed
15.
go back to reference Oshita A, Ohmori K, Yu Y, Kondo I, Takeuchi H, Takagi Y, Wada Y, Yukiiri K, Mizushige K, Kohno M: Myocardial blood flow measurements in rats with simple pulsing contrast echocardiography. Ultrasound Med Biol. 2002, 28 (4): 459-466. 10.1016/S0301-5629(02)00481-7.CrossRefPubMed Oshita A, Ohmori K, Yu Y, Kondo I, Takeuchi H, Takagi Y, Wada Y, Yukiiri K, Mizushige K, Kohno M: Myocardial blood flow measurements in rats with simple pulsing contrast echocardiography. Ultrasound Med Biol. 2002, 28 (4): 459-466. 10.1016/S0301-5629(02)00481-7.CrossRefPubMed
16.
go back to reference Iltis I, Kober F, Desrois M, Dalmasso C, Lan C, Portha B, Cozzone PJ, Bernard M: Defective myocardial blood flow and altered function of the left ventricle in type 2 diabetic rats: a noninvasive in vivo study using perfusion and cine magnetic resonance imaging. Invest Radiol. 2005, 40 (1): 19-26.PubMed Iltis I, Kober F, Desrois M, Dalmasso C, Lan C, Portha B, Cozzone PJ, Bernard M: Defective myocardial blood flow and altered function of the left ventricle in type 2 diabetic rats: a noninvasive in vivo study using perfusion and cine magnetic resonance imaging. Invest Radiol. 2005, 40 (1): 19-26.PubMed
17.
go back to reference Bland JM, Altman DG: Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 1986, 1 (8476): 307-310.CrossRefPubMed Bland JM, Altman DG: Statistical methods for assessing agreement between two methods of clinical measurement. Lancet. 1986, 1 (8476): 307-310.CrossRefPubMed
18.
go back to reference Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, Reichek N: Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol. 1986, 57 (6): 450-458. 10.1016/0002-9149(86)90771-X.CrossRefPubMed Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, Reichek N: Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol. 1986, 57 (6): 450-458. 10.1016/0002-9149(86)90771-X.CrossRefPubMed
19.
go back to reference Shafrir E: Diabetes in animals: Contribution to the understanding of diabetes by study of its etiopathology in animal models in D. Porte, R.S. Sherwin and A. Baron,Diabetes mellitus. Diabetes mellitus. Edited by: D. Porte RSSAB. 2003, NewYork , McGraw-Hill, 231–255. Shafrir E: Diabetes in animals: Contribution to the understanding of diabetes by study of its etiopathology in animal models in D. Porte, R.S. Sherwin and A. Baron,Diabetes mellitus. Diabetes mellitus. Edited by: D. Porte RSSAB. 2003, NewYork , McGraw-Hill, 231–255.
20.
go back to reference Li XS, Tanz RD, Chang KS: Effect of age and methacholine on the rate and coronary flow of isolated hearts of diabetic rats. Br J Pharmacol. 1989, 97 (4): 1209-1217.PubMedCentralCrossRefPubMed Li XS, Tanz RD, Chang KS: Effect of age and methacholine on the rate and coronary flow of isolated hearts of diabetic rats. Br J Pharmacol. 1989, 97 (4): 1209-1217.PubMedCentralCrossRefPubMed
21.
go back to reference Nicholl TA, Lopaschuk GD, McNeill JH: Effects of free fatty acids and dichloroacetate on isolated working diabetic rat heart. Am J Physiol. 1991, 261 (4 Pt 2): H1053-9.PubMed Nicholl TA, Lopaschuk GD, McNeill JH: Effects of free fatty acids and dichloroacetate on isolated working diabetic rat heart. Am J Physiol. 1991, 261 (4 Pt 2): H1053-9.PubMed
22.
go back to reference Hoit BD, Castro C, Bultron G, Knight S, Matlib MA: Noninvasive evaluation of cardiac dysfunction by echocardiography in streptozotocin-induced diabetic rats. J Card Fail. 1999, 5 (4): 324-333. 10.1016/S1071-9164(99)91337-4.CrossRefPubMed Hoit BD, Castro C, Bultron G, Knight S, Matlib MA: Noninvasive evaluation of cardiac dysfunction by echocardiography in streptozotocin-induced diabetic rats. J Card Fail. 1999, 5 (4): 324-333. 10.1016/S1071-9164(99)91337-4.CrossRefPubMed
23.
go back to reference Crystal GJ, Downey HF, Bashour FA: Small vessel and total coronary blood volume during intracoronary adenosine. Am J Physiol. 1981, 241 (2): H194-201.PubMed Crystal GJ, Downey HF, Bashour FA: Small vessel and total coronary blood volume during intracoronary adenosine. Am J Physiol. 1981, 241 (2): H194-201.PubMed
24.
go back to reference Eliasen P, Amtorp O: Effect of intracoronary adenosine upon regional blood flow, microvascular blood volume and hematocrit in canine myocardium. Int J Microcirc Clin Exp. 1984, 3 (1): 3-12.PubMed Eliasen P, Amtorp O: Effect of intracoronary adenosine upon regional blood flow, microvascular blood volume and hematocrit in canine myocardium. Int J Microcirc Clin Exp. 1984, 3 (1): 3-12.PubMed
25.
go back to reference Kawaguchi M, Asakura T, Saito F, Nemoto O, Maehara K, Miyake K, Sugai N, Maruyama Y: [Changes in diameter size and F-actin expression in the myocytes of patients with diabetes and streptozotocin-induced diabetes model rats]. J Cardiol. 1999, 34 (6): 333-339.PubMed Kawaguchi M, Asakura T, Saito F, Nemoto O, Maehara K, Miyake K, Sugai N, Maruyama Y: [Changes in diameter size and F-actin expression in the myocytes of patients with diabetes and streptozotocin-induced diabetes model rats]. J Cardiol. 1999, 34 (6): 333-339.PubMed
26.
go back to reference Jesmin S, Zaedi S, Shimojo N, Iemitsu M, Masuzawa K, Yamaguchi N, Mowa CN, Maeda S, Hattori Y, Miyauchi T: Endothelin antagonism normalizes VEGF signaling and cardiac function in STZ-induced diabetic rat hearts. Am J Physiol Endocrinol Metab. 2007, 292 (4): E1030-40. 10.1152/ajpendo.00517.2006.CrossRefPubMed Jesmin S, Zaedi S, Shimojo N, Iemitsu M, Masuzawa K, Yamaguchi N, Mowa CN, Maeda S, Hattori Y, Miyauchi T: Endothelin antagonism normalizes VEGF signaling and cardiac function in STZ-induced diabetic rat hearts. Am J Physiol Endocrinol Metab. 2007, 292 (4): E1030-40. 10.1152/ajpendo.00517.2006.CrossRefPubMed
27.
go back to reference Pitkanen OP, Nuutila P, Raitakari OT, Ronnemaa T, Koskinen PJ, Iida H, Lehtimaki TJ, Laine HK, Takala T, Viikari JS, Knuuti J: Coronary flow reserve is reduced in young men with IDDM. Diabetes. 1998, 47 (2): 248-254. 10.2337/diabetes.47.2.248.CrossRefPubMed Pitkanen OP, Nuutila P, Raitakari OT, Ronnemaa T, Koskinen PJ, Iida H, Lehtimaki TJ, Laine HK, Takala T, Viikari JS, Knuuti J: Coronary flow reserve is reduced in young men with IDDM. Diabetes. 1998, 47 (2): 248-254. 10.2337/diabetes.47.2.248.CrossRefPubMed
28.
go back to reference Litwin SE, Raya TE, Anderson PG, Daugherty S, Goldman S: Abnormal cardiac function in the streptozotocin-diabetic rat. Changes in active and passive properties of the left ventricle. J Clin Invest. 1990, 86 (2): 481-488. 10.1172/JCI114734.PubMedCentralCrossRefPubMed Litwin SE, Raya TE, Anderson PG, Daugherty S, Goldman S: Abnormal cardiac function in the streptozotocin-diabetic rat. Changes in active and passive properties of the left ventricle. J Clin Invest. 1990, 86 (2): 481-488. 10.1172/JCI114734.PubMedCentralCrossRefPubMed
29.
go back to reference Akula A, Kota MK, Gopisetty SG, Chitrapu RV, Kalagara M, Kalagara S, Veeravalli KK, Gomedhikam JP: Biochemical, histological and echocardiographic changes during experimental cardiomyopathy in STZ-induced diabetic rats. Pharmacol Res. 2003, 48 (5): 429-435. 10.1016/S1043-6618(03)00191-9.CrossRefPubMed Akula A, Kota MK, Gopisetty SG, Chitrapu RV, Kalagara M, Kalagara S, Veeravalli KK, Gomedhikam JP: Biochemical, histological and echocardiographic changes during experimental cardiomyopathy in STZ-induced diabetic rats. Pharmacol Res. 2003, 48 (5): 429-435. 10.1016/S1043-6618(03)00191-9.CrossRefPubMed
30.
go back to reference Mihm MJ, Seifert JL, Coyle CM, Bauer JA: Diabetes related cardiomyopathy time dependent echocardiographic evaluation in an experimental rat model. Life Sci. 2001, 69 (5): 527-542. 10.1016/S0024-3205(01)01141-9.CrossRefPubMed Mihm MJ, Seifert JL, Coyle CM, Bauer JA: Diabetes related cardiomyopathy time dependent echocardiographic evaluation in an experimental rat model. Life Sci. 2001, 69 (5): 527-542. 10.1016/S0024-3205(01)01141-9.CrossRefPubMed
31.
go back to reference Irlbeck M, Zimmer HG: Functional responses of the left and right heart of diabetic rats to alpha- and beta-adrenergic receptor stimulation. Diabetes Res Clin Pract. 1996, 31 Suppl: S79-86. 10.1016/0168-8227(96)01234-X.CrossRefPubMed Irlbeck M, Zimmer HG: Functional responses of the left and right heart of diabetic rats to alpha- and beta-adrenergic receptor stimulation. Diabetes Res Clin Pract. 1996, 31 Suppl: S79-86. 10.1016/0168-8227(96)01234-X.CrossRefPubMed
32.
go back to reference Konduracka E, Gackowski A, Rostoff P, Galicka-Latala D, Frasik W, Piwowarska W: Diabetes-specific cardiomyopathy in type 1 diabetes mellitus: no evidence for its occurrence in the era of intensive insulin therapy. Eur Heart J. 2007, 28 (20): 2465-2471. 10.1093/eurheartj/ehm361.CrossRefPubMed Konduracka E, Gackowski A, Rostoff P, Galicka-Latala D, Frasik W, Piwowarska W: Diabetes-specific cardiomyopathy in type 1 diabetes mellitus: no evidence for its occurrence in the era of intensive insulin therapy. Eur Heart J. 2007, 28 (20): 2465-2471. 10.1093/eurheartj/ehm361.CrossRefPubMed
33.
go back to reference Litwin SE, Katz SE, Weinberg EO, Lorell BH, Aurigemma GP, Douglas PS: Serial echocardiographic-Doppler assessment of left ventricular geometry and function in rats with pressure-overload hypertrophy. Chronic angiotensin-converting enzyme inhibition attenuates the transition to heart failure. Circulation. 1995, 91 (10): 2642-2654.CrossRefPubMed Litwin SE, Katz SE, Weinberg EO, Lorell BH, Aurigemma GP, Douglas PS: Serial echocardiographic-Doppler assessment of left ventricular geometry and function in rats with pressure-overload hypertrophy. Chronic angiotensin-converting enzyme inhibition attenuates the transition to heart failure. Circulation. 1995, 91 (10): 2642-2654.CrossRefPubMed
34.
go back to reference Pires MD, Salemi VM, Cestari IA, Picard MH, Leirner AA, Mady C, Cestari IN: Noninvasive assessment of hemodynamic parameters in experimental stenosis of the ascending aorta. Artif Organs. 2003, 27 (8): 695-700. 10.1046/j.1525-1594.2003.07276.x.CrossRefPubMed Pires MD, Salemi VM, Cestari IA, Picard MH, Leirner AA, Mady C, Cestari IN: Noninvasive assessment of hemodynamic parameters in experimental stenosis of the ascending aorta. Artif Organs. 2003, 27 (8): 695-700. 10.1046/j.1525-1594.2003.07276.x.CrossRefPubMed
35.
go back to reference Slama M, Ahn J, Varagic J, Susic D, Frohlich ED: Long-term left ventricular echocardiographic follow-up of SHR and WKY rats: effects of hypertension and age. Am J Physiol Heart Circ Physiol. 2004, 286 (1): H181-5. 10.1152/ajpheart.00642.2003.CrossRefPubMed Slama M, Ahn J, Varagic J, Susic D, Frohlich ED: Long-term left ventricular echocardiographic follow-up of SHR and WKY rats: effects of hypertension and age. Am J Physiol Heart Circ Physiol. 2004, 286 (1): H181-5. 10.1152/ajpheart.00642.2003.CrossRefPubMed
36.
go back to reference Watson LE, Sheth M, Denyer RF, Dostal DE: Baseline echocardiographic values for adult male rats. J Am Soc Echocardiogr. 2004, 17 (2): 161-167. 10.1016/j.echo.2003.10.010.CrossRefPubMed Watson LE, Sheth M, Denyer RF, Dostal DE: Baseline echocardiographic values for adult male rats. J Am Soc Echocardiogr. 2004, 17 (2): 161-167. 10.1016/j.echo.2003.10.010.CrossRefPubMed
37.
go back to reference Joffe II, Travers KE, Perreault-Micale CL, Hampton T, Katz SE, Morgan JP, PS. D: Abnormal cardiac function in the streptozotocin-induced non-insulin-dependent diabetic rat: noninvasive assessment with doppler echocardiography and contribution of the nitric oxide pathway. J Am Coll Cardiol. 1999, 34 (7): 2111-2119. 10.1016/S0735-1097(99)00436-2.CrossRefPubMed Joffe II, Travers KE, Perreault-Micale CL, Hampton T, Katz SE, Morgan JP, PS. D: Abnormal cardiac function in the streptozotocin-induced non-insulin-dependent diabetic rat: noninvasive assessment with doppler echocardiography and contribution of the nitric oxide pathway. J Am Coll Cardiol. 1999, 34 (7): 2111-2119. 10.1016/S0735-1097(99)00436-2.CrossRefPubMed
38.
go back to reference Mihm MJ, Seifert JL, Coyle CM, Bauer JA: Diabetes related cardiomyopathy time dependent echocardiographic evaluation in an experimental rat model. Life Sci. 2001, 69 (5): 527-542. 10.1016/S0024-3205(01)01141-9.CrossRefPubMed Mihm MJ, Seifert JL, Coyle CM, Bauer JA: Diabetes related cardiomyopathy time dependent echocardiographic evaluation in an experimental rat model. Life Sci. 2001, 69 (5): 527-542. 10.1016/S0024-3205(01)01141-9.CrossRefPubMed
39.
go back to reference Nemoto O, Kawaguchi M, Yaoita H, Miyake K, Maehara K, Maruyama Y: Left ventricular dysfunction and remodeling in streptozotocin-induced diabetic rats. Circ J. 2006, 70 (3): 327-334. 10.1253/circj.70.327.CrossRefPubMed Nemoto O, Kawaguchi M, Yaoita H, Miyake K, Maehara K, Maruyama Y: Left ventricular dysfunction and remodeling in streptozotocin-induced diabetic rats. Circ J. 2006, 70 (3): 327-334. 10.1253/circj.70.327.CrossRefPubMed
40.
go back to reference Bollano E: Cardiac remodeling rather than disturbed myocardial energy metabolism isassociated with cardiac dysfunction in diabetic rats. International Journal of Cardiology. 2007, 114: 195 – 201-10.1016/j.ijcard.2006.01.027.CrossRefPubMed Bollano E: Cardiac remodeling rather than disturbed myocardial energy metabolism isassociated with cardiac dysfunction in diabetic rats. International Journal of Cardiology. 2007, 114: 195 – 201-10.1016/j.ijcard.2006.01.027.CrossRefPubMed
41.
go back to reference Joffe, Travers KE, Perreault-Micale CL, Hampton T, Katz SE, Morgan JP, Douglas PS: Abnormal cardiac function in the streptozotocin-induced non-insulin-dependent diabetic rat: noninvasive assessment with doppler echocardiography and contribution of the nitric oxide pathway. J Am Coll Cardiol. 1999, 34 (7): 2111-2119. 10.1016/S0735-1097(99)00436-2.CrossRefPubMed Joffe, Travers KE, Perreault-Micale CL, Hampton T, Katz SE, Morgan JP, Douglas PS: Abnormal cardiac function in the streptozotocin-induced non-insulin-dependent diabetic rat: noninvasive assessment with doppler echocardiography and contribution of the nitric oxide pathway. J Am Coll Cardiol. 1999, 34 (7): 2111-2119. 10.1016/S0735-1097(99)00436-2.CrossRefPubMed
42.
go back to reference Al-Shafei AI, Wise RG, Gresham GA, Carpenter TA, Hall LD, Huang CL: Magnetic resonance imaging analysis of cardiac cycle events in diabetic rats: the effect of angiotensin-converting enzyme inhibition. J Physiol. 2002, 538 (Pt 2): 555-572. 10.1113/jphysiol.2001.012857.PubMedCentralCrossRefPubMed Al-Shafei AI, Wise RG, Gresham GA, Carpenter TA, Hall LD, Huang CL: Magnetic resonance imaging analysis of cardiac cycle events in diabetic rats: the effect of angiotensin-converting enzyme inhibition. J Physiol. 2002, 538 (Pt 2): 555-572. 10.1113/jphysiol.2001.012857.PubMedCentralCrossRefPubMed
43.
go back to reference Loganathan R, Bilgen M, Al-Hafez B, Alenezy MD, Smirnova IV: Cardiac dysfunction in the diabetic rat: quantitative evaluation using high resolution magnetic resonance imaging. Cardiovasc Diabetol. 2006, 5: 7-10.1186/1475-2840-5-7.PubMedCentralCrossRefPubMed Loganathan R, Bilgen M, Al-Hafez B, Alenezy MD, Smirnova IV: Cardiac dysfunction in the diabetic rat: quantitative evaluation using high resolution magnetic resonance imaging. Cardiovasc Diabetol. 2006, 5: 7-10.1186/1475-2840-5-7.PubMedCentralCrossRefPubMed
44.
go back to reference Nemoto O, Kawaguchi M, Yaoita H, Miyake K, Maehara K, Maruyama Y: Left ventricular dysfunction and remodeling in streptozotocin-induced diabetic rats. Circ J. 2006, 70 (3): 327-334. 10.1253/circj.70.327.CrossRefPubMed Nemoto O, Kawaguchi M, Yaoita H, Miyake K, Maehara K, Maruyama Y: Left ventricular dysfunction and remodeling in streptozotocin-induced diabetic rats. Circ J. 2006, 70 (3): 327-334. 10.1253/circj.70.327.CrossRefPubMed
45.
go back to reference Rodrigues B, Cam MC, Kong J, Goyal RK, McNeill JH: Strain differences in susceptibility to streptozotocin-induced diabetes: effects on hypertriglyceridemia and cardiomyopathy. Cardiovasc Res. 1997, 34 (1): 199-205. 10.1016/S0008-6363(97)00045-X.CrossRefPubMed Rodrigues B, Cam MC, Kong J, Goyal RK, McNeill JH: Strain differences in susceptibility to streptozotocin-induced diabetes: effects on hypertriglyceridemia and cardiomyopathy. Cardiovasc Res. 1997, 34 (1): 199-205. 10.1016/S0008-6363(97)00045-X.CrossRefPubMed
46.
go back to reference Jackson CV, McGrath GM, Tahiliani AG, Vadlamudi RV, McNeill JH: A functional and ultrastructural analysis of experimental diabetic rat myocardium. Manifestation of a cardiomyopathy. Diabetes. 1985, 34 (9): 876-883. 10.2337/diabetes.34.9.876.CrossRefPubMed Jackson CV, McGrath GM, Tahiliani AG, Vadlamudi RV, McNeill JH: A functional and ultrastructural analysis of experimental diabetic rat myocardium. Manifestation of a cardiomyopathy. Diabetes. 1985, 34 (9): 876-883. 10.2337/diabetes.34.9.876.CrossRefPubMed
Metadata
Title
Effect of streptozotocin-induced diabetes on myocardial blood flow reserve assessed by myocardial contrast echocardiography in rats
Authors
Bernard Cosyns
Steven Droogmans
Sophie Hernot
Céline Degaillier
Christian Garbar
Caroline Weytjens
Bram Roosens
Danny Schoors
Tony Lahoutte
Philippe R Franken
Guy Van Camp
Publication date
01-12-2008
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2008
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/1475-2840-7-26

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