Age-matched comparison reveals early electrocardiography and echocardiography changes in dystrophin-deficient dogs

Neuromuscular Disorders

Volumn 21, Issue 7, 2011, Pages 453-461

  Fine, Deborah M ^a   Shin, Jin Hong ^b   Yue, Yongping ^b   Volkmann, Dietrich ^a   Leach, Stacey B ^a   Smith, Bruce F ^c   McIntosh, Mark ^b   Duan, Dongsheng ^b  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

^c AUBURN UNIVERSITY   (United States)

Author keywords

Cardiomyopathy canine; Dog; Duchenne muscular dystrophy; Dystrophin; ECG; Echocardiography; Electrocardiography; Golden retriever muscular dystrophy (GRMD); Heart; Labrador muscular dystrophy; Large animal model

Indexed keywords

CREATINE KINASE; DYSTROPHIN;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPSY; CARDIOMYOPATHY; CONTROLLED STUDY; CREATINE KINASE BLOOD LEVEL; DOG; ECHOCARDIOGRAPHY; ELECTROCARDIOGRAPHY; GROWTH RETARDATION; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART LEFT VENTRICLE SIZE; HISTOPATHOLOGY; MALE; NONHUMAN; PR INTERVAL; PRIORITY JOURNAL; PROSPECTIVE STUDY;

ANIMALS; CARDIOMYOPATHIES; CREATINE KINASE; DISEASE MODELS, ANIMAL; DOGS; DYSTROPHIN; ELECTROCARDIOGRAPHY; HEART; MUSCULAR DYSTROPHY, DUCHENNE; MYOCARDIUM;

EID: 79960089426     PISSN: 09608966     EISSN: 18732364     Source Type: Journal    
DOI: 10.1016/j.nmd.2011.03.010     Document Type: Article

References (65)

1. Lapidos K.A., Kakkar R., McNally E.M. The dystrophin glycoprotein complex: signaling strength and integrity for the sarcolemma. Circ Res 2004, 94:1023-1031.
2. Aartsma-Rus A., Van Deutekom J.C., Fokkema I.F., Van Ommen G.J., Den Dunnen J.T. Entries in the Leiden Duchenne muscular dystrophy mutation database: an overview of mutation types and paradoxical cases that confirm the reading-frame rule. Muscle Nerve 2006, 34:135-144.
3. Flanigan K.M., Dunn D.M., von Niederhausern A., et al. Mutational spectrum of DMD mutations in dystrophinopathy patients: application of modern diagnostic techniques to a large cohort. Hum Mutat 2009, 30:1657-1666.
4. Tuffery-Giraud S., Beroud C., Leturcq F., et al. Genotype-phenotype analysis in 2405 patients with a dystrophinopathy using the UMD-DMD database: a model of nationwide knowledgebase. Hum Mutat 2009, 30:934-945.
5. Towbin J.A. The role of cytoskeletal proteins in cardiomyopathies. Curr Opin Cell Biol 1998, 10:131-139.
6. Shin J.-H., Bostick B., Yue Y., Duan D. Duchenne cardiomyopathy gene therapy. Muscle gene therapy 2010, 141-162. Springer Science+Business Media, LLC, New York. D. Duan (Ed.).
7. Maron B.J., Towbin J.A., Thiene G., et al. Contemporary definitions and classification of the cardiomyopathies: an American Heart Association Scientific Statement from the Council on Clinical Cardiology, Heart Failure and Transplantation Committee; Quality of Care and Outcomes Research and Functional Genomics and Translational Biology Interdisciplinary Working Groups; and Council on Epidemiology and Prevention. Circulation 2006, 113:1807-1816.
8. Duan D. Challenges and opportunities in dystrophin-deficient cardiomyopathy gene therapy. Hum Mol Genet 2006, 15:R253-R261. [Spec No. 2].
9. McNally E.M. New approaches in the therapy of cardiomyopathy in muscular dystrophy. Annu Rev Med 2007, 58:75-88.
10. Bostick B., Yue Y., Long C., Duan D. Prevention of dystrophin-deficient cardiomyopathy in 21month-old carrier mice by mosaic dystrophin expression or complementary dystrophin/utrophin expression. Circ Res 2008, 102:121-130.
11. Bostick B., Yue Y., Lai Y., Long C., Li D., Duan D. Adeno-associated virus serotype-9 microdystrophin gene therapy ameliorates electrocardiographic abnormalities in mdx mice. Hum Gene Ther 2008, 19:851-856.
12. Yue Y., Skimming J.W., Liu M., Strawn T., Duan D. Full-length dystrophin expression in half of the heart cells ameliorates beta-isoproterenol-induced cardiomyopathy in mdx mice. Hum Mol Genet 2004, 13:1669-1675.
13. Shelton G.D., Engvall E. Canine and feline models of human inherited muscle diseases. Neuromuscul Disord 2005, 15:127-138.
14. Smith B.F., Yue Y., Woods P.R., et al. An intronic line-1 element insertion in the dystrophin gene aborts dystrophin expression and results in Duchenne-like muscular dystrphy in the corgi breed. La Invest 2011, 91:216-231.
15. Cooper B.J., Winand N.J., Stedman H., et al. The homologue of the Duchenne locus is defective in X-linked muscular dystrophy of dogs. Nature 1988, 334:154-156.
16. Kornegay J.N., Tuler S.M., Miller D.M., Levesque D.C. Muscular dystrophy in a litter of golden retriever dogs. Muscle Nerve 1988, 11:1056-1064.
17. Valentine B.A., Cooper B.J., de Lahunta A., O'Quinn R., Blue J.T. Canine X-linked muscular dystrophy An animal model of Duchenne muscular dystrophy: clinical studies. J Neurol Sci 1988, 88:69-81.
18. Smith BF, Kornegay JN, Duan D. Independent canine models of Duchenne muscular dystrophy due to intronic insertions of repetitive DNA. 10th Annual Meeting of the American Society of Gene Therapy, Seattle, WA 2007 May 30-June 3. 2007.
19. McNally E.M. Duchenne muscular dystrophy: how bad is the heart?. Heart 2008, 94:976-977.
20. Finsterer J., Stollberger C. The heart in human dystrophinopathies. Cardiology 2003, 99:1-19.
21. Diez-Prieto I., Garcia-Rodriguez M.B., Rios-Granja M.A., Cano-Rabano M.J., Pena-Penabad M., Perez-Garcia C.C. M-mode echocardiographic changes in growing beagles. J Am Assoc Lab Anim Sci 2010, 49:31-35.
22. Cornell C.C., Kittleson M.D., Della Torre P., et al. Allometric scaling of M-mode cardiac measurements in normal adult dogs. J Vet Intern Med 2004, 18:311-321.
23. Bartlett R.J., Winand N.J., Secore S.L., et al. Mutation segregation and rapid carrier detection of X-linked muscular dystrophy in dogs. Am J Vet Res 1996, 57:650-654.
24. Yue Y., Ghosh A., Long C., et al. A single intravenous injection of adeno-associated virus serotype-9 leads to whole body skeletal muscle transduction in dogs. Mol Ther 2008, 16:1944-1952.
25. Dukes-McEwan J., French A.T., Corcoran B.M. Doppler echocardiography in the dog: measurement variability and reproducibility. Vet Radiol Ultrasound 2002, 43:144-152.
26. Tilley L.P. Essentials of canine and feline electrocardiography: interpretation and treatment 1992, Lea & Febiger, Philadelphia. 3rd ed.
27. Thomas W.P., Gaber C.E., Jacobs G.J., et al. Recommendations for standards in transthoracic two-dimensional echocardiography in the dog and cat. Echocardiography Committee of the Specialty of Cardiology, American College of Veterinary Internal Medicine. J Vet Intern Med 1993, 7:247-252.
28. Rishniw M., Erb H.N. Evaluation of four 2-dimensional echocardiographic methods of assessing left atrial size in dogs. J Vet Intern Med 2000, 14:429-435.
29. Boon J.A. Manual of veterinary echocardiography 1998, Williams & Wilkins, Baltimore.
30. Ferasin L., Ferasin H., Little C.J. Lack of correlation between canine heart rate and body size in veterinary clinical practice. J Small Anim Pract 2010, 51:412-418.
31. Hanton G., Rabemampianina Y. The electrocardiogram of the Beagle dog: reference values and effect of sex, genetic strain, body position and heart rate. Lab Anim 2006, 40:123-136.
32. Bish L.T., Sleeper M.M., Brainard B., et al. Percutaneous transendocardial delivery of self-complementary adeno-associated virus 6 achieves global cardiac gene transfer in canines. Mol Ther 2008, 16:1953-1959.
33. Wang Z., Kuhr C.S., Allen J.M., et al. Sustained AAV-mediated dystrophin expression in a canine model of duchenne muscular dystrophy with a brief course of immunosuppression. Mol Ther 2007, 15:1160-1166.
34. Gregorevic P., Schultz B.R., Allen J.M., et al. Evaluation of vascular delivery methodologies to enhance rAAV6-mediated gene transfer to canine striated musculature. Mol Ther 2009, 17:1427-1433.
35. Townsend D., Turner I., Yasuda S., et al. Chronic administration of membrane sealant prevents severe cardiac injury and ventricular dilatation in dystrophic dogs. J Clin Invest 2010, 120:1140-1150.
36. Kornegay J.N., Li J., Bogan J.R., et al. Widespread muscle expression of an aav9 human mini-dystrophin vector after intravenous injection in neonatal dystrophin-deficient dogs. Mol Ther 2010, 18:1501-1508.
37. Moise N.S., Valentine B.A., Brown C.A., et al. Duchenne's cardiomyopathy in a canine model: electrocardiographic and echocardiographic studies. J Am Coll Cardiol 1991, 17:812-820.
38. Yugeta N., Urasawa N., Fujii Y., et al. Cardiac involvement in beagle-based canine X-linked muscular dystrophy in Japan (CXMDJ): electrocardiographic, echocardiographic, and morphologic studies. BMC Cardiovasc Disord 2006, 6:47.
39. Devaux J.Y., Cabane L., Esler M., Flaouters H., Duboc D. Non-invasive evaluation of the cardiac function in golden retriever dogs by radionuclide angiography. Neuromuscul Disord 1993, 3:429-432.
40. Chetboul V., Carlos C., Blot S., et al. Tissue Doppler assessment of diastolic and systolic alterations of radial and longitudinal left ventricular motions in golden retrievers during the preclinical phase of cardiomyopathy associated with muscular dystrophy. Am J Vet Res 2004, 65:1335-1341.
41. 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, 25:1934-1939.
42. Morrison S.A., Moise N.S., Scarlett J., Mohammed H., Yeager A.E. Effect of breed and body weight on echocardiographic values in four breeds of dogs of differing somatotype. J Vet Intern Med 1992, 6:220-224.
43. Crippa L., Ferro E., Melloni E., Brambilla P., Cavalletti E. Echocardiographic parameters and indices in the normal beagle dog. Lab Anim 1992, 26:190-195.
44. Valentine B.A., Cummings J.F., Cooper B.J. Development of Duchenne-type cardiomyopathy. Morphologic studies in a canine model. Am J Pathol 1989, 135:671-678.
45. Perloff J.K., Henze E., Schelbert H.R. Alterations in regional myocardial metabolism, perfusion, and wall motion in Duchenne muscular dystrophy studied by radionuclide imaging. Circulation 1984, 69:33-42.
46. Perloff J.K., Roberts W.C., de Leon A.C., O'Doherty D. The distinctive electrocardiogram of Duchenne's progressive muscular dystrophy. An electrocardiographic-pathologic correlative study. Am J Med 1967, 42:179-188.
47. Perloff J.K., de Leon A.C., O'Doherty D. The cardiomyopathy of progressive muscular dystrophy. Circulation 1966, 33:625-648.
48. Sanyal S.K., Johnson W.W. Cardiac conduction abnormalities in children with Duchenne's progressive muscular dystrophy: electrocardiographic features and morphologic correlates. Circulation 1982, 66:853-863.
49. Sanyal S.K., Johnson W.W., Thapar M.K., Pitner S.E. An ultrastructural basis for electrocardiographic alterations associated with Duchenne's progressive muscular dystrophy. Circulation 1978, 57:1122-1129.
50. Yotsukura M., Yamamoto A., Kajiwara T., et al. QT dispersion in patients with Duchenne-type progressive muscular dystrophy. Am Heart J 1999, 137:672-677.
51. Nigro G., Politano L., Santangelo L., et al. Is the value of QT dispersion a valid method to foresee the risk of sudden death? A study in Becker patients. Heart 2002, 87:156-157.
52. Fayssoil A. Holter electrocardiogram should be systematic in Duchenne muscular dystrophy. Int J Cardiol 2008, 128:442-443.
53. Sultan A., Fayaz M. Prevalence of cardiomyopathy in Duchenne and Becker's muscular dystrophy. J Ayub Med Coll Abbottabad 2008, 20:7-13.
54. Takami Y., Takeshima Y., Awano H., Okizuka Y., Yagi M., Matsuo M. High incidence of electrocardiogram abnormalities in young patients with duchenne muscular dystrophy. Pediatr Neurol 2008, 39:399-403.
55. Perloff J.K. Cardiac rhythm and conduction in Duchenne's muscular dystrophy: a prospective study of 20 patients. J Am Coll Cardiol 1984, 3:1263-1268.
56. Corrado G., Lissoni A., Beretta S., et al. Prognostic value of electrocardiograms, ventricular late potentials, ventricular arrhythmias, and left ventricular systolic dysfunction in patients with Duchenne muscular dystrophy. Am J Cardiol 2002, 89:838-841.
57. Thrush P.T., Allen H.D., Viollet L., Mendell J.R. Re-examination of the electrocardiogram in boys with Duchenne muscular dystrophy and correlation with its dilated cardiomyopathy. Am J Cardiol 2009, 103:262-265.
58. Urasawa N., Wada M.R., Machida N., et al. Selective vacuolar degeneration in dystrophin-deficient canine Purkinje fibers despite preservation of dystrophin-associated proteins with overexpression of Dp71. Circulation 2008, 117:2437-2448.
59. Wehling-Henricks M., Jordan M.C., Roos K.P., Deng B., Tidball J.G. Cardiomyopathy in dystrophin-deficient hearts is prevented by expression of a neuronal nitric oxide synthase transgene in the myocardium. Hum Mol Genet 2005, 14:1921-1933.
60. Colussi C., Berni R., Rosati J., et al. The histone deacetylase inhibitor suberoylanilide hydroxamic acid reduces cardiac arrhythmias in dystrophic mice. Cardiovasc Res 2010, 87:73-82.
61. Bostick B., Yue Y., Long C., et al. Cardiac expression of a mini-dystrophin that normalizes skeletal muscle force only partially restores heart function in aged Mdx mice. Mol Ther 2009, 17:253-261.
62. Martin M.W., Stafford Johnson M.J., Strehlau G., King J.N. Canine dilated cardiomyopathy: a retrospective study of prognostic findings in 367 clinical cases. J Small Anim Pract 2010, 51:428-436.
63. Nigro G., Comi L.I., Politano L., Bain R.J. The incidence and evolution of cardiomyopathy in Duchenne muscular dystrophy. Int J Cardiol 1990, 26:271-277.
64. Park O.Y., Ahn Y., Park W.S., et al. Rapid progression from hypertrophic cardiomyopathy to heart failure in a patient with Becker's muscular dystrophy. Eur J Heart Fail 2005, 7:684-688.
65. Bostick B., Yue Y., Duan D. Gender influences cardiac function in the mdx model of Duchenne cardiomyopathy. Muscle Nerve 2010, 42:600-603.