• 1. Butler WJ, Ostrander L Jr, Carman WJ, et al. Mortality from coronary heart disease in the Tecumseh study. Long-term effect of diabetes mellitus, glucose tolerance and other risk factors. Am J Epidemiol 1985;121:541547.

    • Search Google Scholar
    • Export Citation
  • 2. Kannel WB, McGee D. Diabetes and glucose tolerance as risk factors for cardiovascular disease: the Framingham study. Diabetes Care 1979;2:120126.

    • Search Google Scholar
    • Export Citation
  • 3. Fein FS, Sonnenblick EH. Diabetic cardiomyopathy. Prog Cardiovasc Dis 1985;27:255270.

  • 4. Picano E. Diabetic cardiomyopathy the importance of being earliest. J Am Coll Cardiol 2003;42:454457.

  • 5. Rubler S, Dlugash J, Yuceoglu YZ, et al. New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 1972;30:595602.

    • Search Google Scholar
    • Export Citation
  • 6. Bertoni AG, Tsai A, Kasper EK, et al. Diabetes and idiopathic cardiomyopathy: a nationwide case-control study. Diabetes Care 2003;26:27912795.

    • Search Google Scholar
    • Export Citation
  • 7. Boyer JK, Thanigaraj S, Schechtman KB, et al. Prevalence of ventricular diastolic dysfunction in asymptomatic, normotensive patients with diabetes mellitus. Am J Cardiol 2004;93:870875.

    • Search Google Scholar
    • Export Citation
  • 8. From AM, Scott CG, Chen HH. The development of heart failure in patients with diabetes mellitus and pre-clinical diastolic dysfunction: a population-based study. J Am Coll Cardiol 2010;55:300305.

    • Search Google Scholar
    • Export Citation
  • 9. Poornima IG, Parikh P, Shannon RP. Diabetic cardiomyopathy: the search for a unifying hypothesis. Circ Res 2006;98:596605.

  • 10. Schannwell CM, Schneppenheim M, Perings S, et al. Left ventricular diastolic dysfunction as an early manifestation of diabetic cardiomyopathy. Cardiology 2002;98:3339.

    • Search Google Scholar
    • Export Citation
  • 11. Liu JE, Palmieri V, Roman MJ, et al. The impact of diabetes on left ventricular filling pattern in normotensive and hypertensive adults: the Strong Heart Study. J Am Coll Cardiol 2001;37:19431949.

    • Search Google Scholar
    • Export Citation
  • 12. Boudina S, Abel ED. Diabetic cardiomyopathy revisited. Circulation 2007;115:32133223.

  • 13. Candido R, Forbes JM, Thomas MC, et al. A breaker of advanced glycation end products attenuates diabetes-induced myocardial structural changes. Circ Res 2003;92:785792.

    • Search Google Scholar
    • Export Citation
  • 14. Clark RJ, McDonough PM, Swanson E, et al. Diabetes and the accompanying hyperglycemia impairs cardiomyocyte calcium cycling through increased nuclear O-GlcNAcylation. J Biol Chem 2003;278:4423044237.

    • Search Google Scholar
    • Export Citation
  • 15. Nelson RW, Reusch CE. Animal models of disease: classification and etiology of diabetes in dogs and cats. J Endocrinol 2014;222:T1T9.

    • Search Google Scholar
    • Export Citation
  • 16. Muñana KR. Long-term complications of diabetes mellitus. Part I: retinopathy, nephropathy, neuropathy. Vet Clin North Am Small Anim Pract 1995;25:715730.

    • Search Google Scholar
    • Export Citation
  • 17. Chetboul V, Escriou C, Tessier D, et al. Tissue Doppler imaging detects early asymptomatic myocardial abnormalities in a dog model of Duchenne's cardiomyopathy. Eur Heart J 2004;25:19341939.

    • Search Google Scholar
    • Export Citation
  • 18. Wess G, Keller LJ, Klausnitzer M, et al. Comparison of longitudinal myocardial tissue velocity, strain, and strain rate measured by two-dimensional speckle tracking and by color tissue Doppler imaging in healthy dogs. J Vet Cardiol 2011;13:3143.

    • Search Google Scholar
    • Export Citation
  • 19. Kasner M, Westermann D, Steendijk P, et al. Utility of Doppler echocardiography and tissue Doppler imaging in the estimation of diastolic function in heart failure with normal ejection fraction: a comparative Doppler-conductance catheterization study. Circulation 2007;116:637647.

    • Search Google Scholar
    • Export Citation
  • 20. Di Bonito P, Moio N, Cavuto L, et al. Early detection of diabetic cardiomyopathy: usefulness of tissue Doppler imaging. Diabet Med 2005;22:17201725.

    • Search Google Scholar
    • Export Citation
  • 21. Struble AL, Feldman EC, Nelson RW, et al. Systemic hypertension and proteinuria in dogs with diabetes mellitus. J Am Vet Med Assoc 1998;213:822825.

    • Search Google Scholar
    • Export Citation
  • 22. Sahn DJ, DeMaria A, Kisslo J, et al. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 1978;58:10721083.

    • Search Google Scholar
    • Export Citation
  • 23. Bonagura JD, Schober K. Can ventricular function be assessed by echocardiography in chronic canine mitral valve disease? J Small Anim Pract 2009;50(suppl 1):1224.

    • Search Google Scholar
    • Export Citation
  • 24. Hansson K, Häggström J, Kvart C, et al. Left atrial to aortic root indices using two-dimensional and M-mode echocardiography in Cavalier King Charles Spaniels with and without left atrial enlargement. Vet Radiol Ultrasound 2002;43:568575.

    • Search Google Scholar
    • Export Citation
  • 25. Dickson D, Caivano D, Patteson M, et al. The times they are a-changin': two-dimensional aortic valve measurements throughout diastole. J Vet Cardiol 2016;18:1525.

    • Search Google Scholar
    • Export Citation
  • 26. Fang ZY, Yuda S, Anderson V, et al. Echocardiographic detection of early diabetic myocardial disease. J Am Coll Cardiol 2003;41:611617.

    • Search Google Scholar
    • Export Citation
  • 27. Poirier P, Bogaty P, Garneau C, et al. Diastolic dysfunction in normotensive men with well-controlled type 2 diabetes importance of maneuvers in echocardiographic screening for preclinical diabetic cardiomyopathy. Diabetes Care 2001;24:510.

    • Search Google Scholar
    • Export Citation
  • 28. Gul K, Celebi AS, Kacmaz F, et al. Tissue Doppler imaging must be performed to detect early left ventricular dysfunction in patients with type 1 diabetes mellitus. Eur J Echocardiogr 2009;10:841846.

    • Search Google Scholar
    • Export Citation
  • 29. Jackson CV, McGrath GM, Tahiliani AG, et al. A functional and ultrastructural analysis of experimental diabetic rat myocardium: manifestation of a cardiomyopathy. Diabetes 1985;34:876883.

    • Search Google Scholar
    • Export Citation
  • 30. Chetboul V, Sampedrano CC, Testault I, et al. Use of tissue Doppler imaging to confirm the diagnosis of dilated cardiomyopathy in a dog with equivocal echocardiographic findings. J Am Vet Med Assoc 2004;225:18771880.

    • Search Google Scholar
    • Export Citation
  • 31. Ommen SR, Nishimura RA, Appleton CP, et al. Clinical utility of Doppler echocardiography and tissue Doppler imaging in the estimation of left ventricular filling pressures: a comparative simultaneous Doppler-catheterization study. Circulation 2000;102:17881794.

    • Search Google Scholar
    • Export Citation
  • 32. Ballo P, Quatrini I, Giacomin E, et al. Circumferential versus longitudinal systolic function in patients with hypertension: A nonlinear relation. J Am Soc Echocardiogr 2007;20:298306.

    • Search Google Scholar
    • Export Citation
  • 33. Mizuguchi Y, Oishi Y, Miyoshi H, et al. The functional role of longitudinal, circumferential, and radial myocardial deformation for regulating the early impairment of left ventricular contraction and relaxation in patients with cardiovascular risk factors: a study with two-dimensional strain imaging. J Am Soc Echocardiogr 2008;21:11381144.

    • Search Google Scholar
    • Export Citation
  • 34. Fang ZY, Leano R, Marwick TH. Relationship between longitudinal and radial contractility in subclinical diabetic heart disease. Clin Sci 2004;106:5360.

    • Search Google Scholar
    • Export Citation
  • 35. Fein FS, Strobeck JE, Malhotra A, et al. Reversibility of diabetic cardiomyopathy with insulin in rats. Circ Res 1981;49:12511261.

  • 36. Ilercil A, Devereux RB, Roman MJ, et al. Associations of insulin levels with left ventricular structure and function in American Indians the strong heart study. Diabetes 2002;51:15431547.

    • Search Google Scholar
    • Export Citation
  • 37. From AM, Scott CG, Chen HH. Changes in diastolic dysfunction in diabetes mellitus over time. Am J Cardiol 2009;103:14631466.

  • 38. Malhotra A, Penpargkul S, Fein FS, et al. The effect of streptozotocin-induced diabetes in rats on cardiac contractile proteins. Circ Res 1981;49:12431250.

    • Search Google Scholar
    • Export Citation
  • 39. Vadlamudi RV, Rodgers RL, McNeill JH. The effect of chronic alloxan-and streptozotocin-induced diabetes on isolated rat heart performance. Can J Physiol Pharmacol 1982;60:902911.

    • Search Google Scholar
    • Export Citation
  • 40. Grandi AM, Piantanida E, Franzetti I, et al. Effect of glycemic control on left ventricular diastolic function in type 1 diabetes mellitus. Am J Cardiol 2006;97:7176.

    • Search Google Scholar
    • Export Citation
  • 41. Berg TJ, Snorgaard O, Faber J, et al. Serum levels of advanced glycation end products are associated with left ventricular diastolic function in patients with type 1 diabetes. Diabetes Care 1999;22:11861190.

    • Search Google Scholar
    • Export Citation
  • 42. Posner J, Ilya R, Wanderman K, et al. Systolic time intervals in diabetes. Diabetologia 1983;24:249252.

  • 43. Mathew P, John L, Jose J, et al. Assessment of left ventricular diastolic function in young diabetics—a two dimensional echo Doppler study. Indian Heart J 1992;44:2932.

    • Search Google Scholar
    • Export Citation
  • 44. Blair E. Anatomy of the ventricular coronary arteries in the dog. Circ Res 1961;9:333341.

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Evaluation of tissue Doppler ultrasonographic and strain imaging for assessment of myocardial dysfunction in dogs with type 1 diabetes mellitus

Yun-Hye Kim MS, DVM1, Jung-Hyun Kim DVM, PhD2, and Chul Park DVM, PhD3
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  • 1 BK21 Plus Team and Department of Veterinary Internal Medicine, College of Veterinary Medicine, Chonbuk National University, Iksan, Jeonbuk 54596, South Korea.
  • | 2 Department of Veterinary Internal Medicine, Veterinary Medical Teaching Hospital, Konkuk University, Seoul 143-701, South Korea.
  • | 3 BK21 Plus Team and Department of Veterinary Internal Medicine, College of Veterinary Medicine, Chonbuk National University, Iksan, Jeonbuk 54596, South Korea.

Abstract

OBJECTIVE To investigate cardiac structural and functional changes by tissue Doppler imaging (TDI) and strain imaging in dogs with spontaneous type 1 diabetes mellitus.

ANIMALS 30 client-owned dogs, of which 10 had normotensive type 1 diabetes mellitus and 20 were healthy.

PROCEDURES All dogs underwent physical examination, laboratory analyses, standard echocardiography, and TDI.

RESULTS On TDI and strain imaging, transmitral peak early diastolic velocity (E)-to-tissue Doppler–derived peak early diastolic velocity at basal segment (E') of septum ratio, E:lateral E’ ratio, and septal tissue Doppler–derived peak late diastolic velocity at basal segment (A') were significantly higher and the septal E':A’ ratio and lateral longitudinal strain were significantly lower for diabetic dogs than for control dogs. Furthermore, in diabetic dogs, serum glucose and fructosamine concentrations after a 12-hour period of food withholding were positively correlated with regional systolic functional variables (septal and lateral longitudinal strain) and left ventricular filling pressure indices (E:septal E’ and E:lateral E’ ratios) but were negatively correlated with diastolic functional variables (E:transmitral peak late diastolic velocity and septal and lateral E':A’ ratios).

CONCLUSIONS AND CLINICAL RELEVANCE Results indicated that myocardial function in diabetic dogs may be altered before the development of clinical heart-associated signs and that the change may be more readily detected by TDI and strain imaging than by conventional echocardiography. In addition, findings indicated that hyperglycemia could have detrimental effects on myocardial function, independent of hypertension, other cardiac diseases, and left ventricular hypertrophy, in dogs with type 1 diabetes.

Contributor Notes

Address correspondence to Dr. Park (chulpark0409@jbnu.ac.kr).