Evidence for differential sympathetic and parasympathetic reinnervation after heart transplantation in humans

Journal of the Autonomic Nervous System

Volumn 67, Issue 3, 1997, Pages 176-183

  Tio, René A ^a   Reyners, An K L ^a   Van Veldhuisen, Dirk J ^a   Van den Berg, Maarten P ^a   Brouwer, René M H J ^a   Haaksma, Jaap ^a   Smit, Andries J ^a   Crijns, Harry J G M ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Autonomic testing; Heart rate variability; Heart transplantation; Human; Reinnervation

Indexed keywords

ADULT; ARTICLE; AUTONOMIC NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; FUNCTION TEST; HEART FUNCTION TEST; HEART RATE; HEART RATE VARIABILITY; HEART TRANSPLANTATION; HUMAN; HYPERPNEA; MALE; MENTAL STRESS; PARASYMPATHETIC INNERVATION; PRIORITY JOURNAL; REINNERVATION; SYMPATHETIC FUNCTION; SYSTOLIC BLOOD PRESSURE; VALSALVA MANEUVER;

ADULT; FEMALE; HEART; HEART RATE; HEART TRANSPLANTATION; HUMANS; MALE; MIDDLE AGED; NERVE REGENERATION; PARASYMPATHETIC NERVOUS SYSTEM; POSTOPERATIVE PERIOD; SYMPATHETIC NERVOUS SYSTEM;

EID: 0031565128     PISSN: 01651838     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0165-1838(97)00104-5     Document Type: Article

References (50)

1. Pope S.E., Stinson E.B., Daughters G.T., Schroeder J.S., Ingels N.B., Alderman E.L. Exercise response of the denervated heart in long-term cardiac transplant recipients. Am. J. Cardiol. 46:1980;213-218.
2. Quigg R.J., Rocco M.B., Gauthier D.F., Creager M.A., Hartley L.H., Colucci W. Mechanism of the attenuated peak heart rate response to exercise after orthotopic cardiac transplantation. J. Am. Coll. Cardiol. 14:1989;338-344.
3. Rudas L., Pflugfelder P.W., Menkis A.H., Novick R.J., McKenzie F.N., Kostuk W.J. Evolution of heart rate responsiveness after orthotopic cardiac transplantation. Am. J. Cardiol. 68:1991;232-236.
4. Arrowood J.A., Goudreau E., Minisi A.J., Davis A.B., Mohanty P.K., Rudas L., Pflugfelder P.W., Menkis A.H., Novick R.J., McKenzie F.N., Kostuk W.J. Evidence against reinnervation of cardiac vagal afferents after human orthotopic cardiac transplantation. Evolution of heart rate responsiveness after orthotopic cardiac transplantation. Circulation. 68:1991;232-236.
5. Dong D. Performance of the heart two years after autotransplantation. Surgery. 56:1964;270-274.
6. Willman V.L., Cooper T., Hanlon C. Return of autonomic responses following autotransplantation of the canine heart. Am. J. Physiol. 207:1964;187-189.
7. Peiss C.N., Cooper T., Willman V.L., Randall W.C. Circulatory responses to electrical and reflex activation of the nervous system after cardiac denervation. Circ. Res. 19:1966;153-166.
8. Seki S., Danielson G.K. Characteristics of cardiac reinnervation in growing calves. J. Thorac. Cardiovasc. Surg. 62:1971;602-607.
9. Kondo Y., Matheny J.L., Hardy J.D. Autonomic reinnervation of cardiac transplants: Further observations in dogs and Rhesus monkeys. Ann. Surg. 176:1972;42-48.
10. Kaye M.P., Wells D.J., Tyce G.M. Nerve growth factor-enhanced reinnervation of surgically denervated canine heart. Am. J. Physiol. 236:1979;H624-H628.
11. Mohanty P.K., Themes M.D., Capehart J.R., Kawaguchi A., Ballon B., Lower R. Afferent reinnervation of the autotransplanted heart in dogs. J. Am. Coll. Cardiol. 7:1986;414-418.
12. Norvell J.E., Lower R.R. Degeneration and regeneration of the nerves of the heart after transplantation. Transplantation. 15:1973;337-344.
13. Milam J.D., Shipkey F.H. Jr., Lind C.J. Jr., Nora J.J., Leachman R.D., Rochelle D.G., Bloodwell R.D., Hallman G.L., Cooley D.A. Morphologic findings in human cardiac allografts. Circulation. 41:1970;519-535.
14. Wilson R.F., Christensen B.V., Olivari M.T., Simon A., White C.W., Laxson D. Evidence for structural sympathetic reinnervation after orthotopic cardiac transplantation in humans. Circulation. 83:1991;1210-1220.
15. Schwaiger M., Hutchins G.D., Kalff V., Rosenspire K., Haka M.S., Mailette S., Deeb G.M., Abrams G.D., Wieland D. Evidence for regional catecholamine uptake and storage sites in the transplanted human heart by positron emission tomography. J. Clin. Invest. 87:1991;1681-1690.
16. Kaye D.M., Esler M., Kingwell B., McPherson G., Esmore D., Jennings G. Functional and neurochemical evidence for partial cardiac sympathetic reinnervation after cardiac transplantation in humans. Circulation. 88:1993;1110-1118.
17. De Marco T., Dae M., Yuen Green M.S., Kumar S., Sudhir K., Keith F., Amidon T.M., Rifkin C., Klinski C., Lau D.et al. Iodine-123 metaiodobenzylquanidine scintigraphic assessment of the transplanted human heart: Evidence for late reinnervation. J. Am. Coll. Cardiol. 25:1995;927-931.
18. Fallen E.L., Kamath M.V., Ghista D.N., Fitchett D. Spectral analysis of heart rate variability following human heart transplantation: Evidence for functional reinnervation. J. Auton. Nerv. Syst. 23:1988;199-206.
19. Fitzpatrick A.P., Banner N., Cheng A., Yacoub M., Sutton R. Vasovagal reactions may occur after orthotopic heart transplantation. J. Am. Coll. Cardiol. 21:1993;1132-1137.
20. Le Guludec D., Delforge J., Syrota A., Desruennes M., Valette H., Gandjbakhch I., Merlet P. In viva quantification of myocardial muscarinic receptors in heart transplant patients. Circulation. 90:1994;172-178.
21. Wesseling K.H., DeWit B., Settels J.J., Klaver W.H. On the direct registration of finger blood pressure after Penaz. Funkt. Biol. Med. 1:1982;245-250.
22. Ewing D.J., Martyn C.N., Young R.J., Clarke B.F. The value of cardiovascular autonomic function tests: 10 years experience in diabetes. Diabetes Care. 8:1985;491-498.
23. Eckberg D.L. Parasympathetic cardiovascular control in human disease: A critical review of methods and results. Am. J. Physiol. 239:1980;H581-H593.
24. Arnold R.W., Dyer J.A., Gould A.B. Jr., Hohberger G.G., Low P.A. Sensitivity to vasovagal maneuvers in normal children and adults. Mayo Clin. Proc. 66:1991;797-804.
25. Mickley H., Hansen K.N., Oxhoj H., Moller M. The effect of carotid sinus massage is independent of posture in patients with heart disease. Eur. Heart J. 10:1989;459-463.
26. Ng A.V., Callister R., Johnson D.G., Seals D.R. Sympathetic neural reactivity to stress does not increase with age in healthy humans. Am. J. Physiol. 267:1994;H344-H353.
27. Aars H., Brodin P., Andersen E. A study of cholinergic and beta-adrenergic components in the regulation of blood flow in the tooth pulp and gingiva in man. Acta. Physiol. Scand. 148:1993;441-447.
28. Brod J., Fencl V., Hejl Z., Jirka J. Circulatory changes underlying blood pressure elevation during acute emotional stress (mental arithmetic) in normotensive and hypertensive subjects. Clin. Sci. 50:1959;565-576.
29. Locatelli A., Franzetti I., Lepore G., Maglio M.L., Gaudio E., Caviezel F., Pozza G. Mental arithmetic stress as a test for evaluation of diabetic sympathetic autonomic neuropathy. Diabetic Med. 6:1989;490-495.
30. Jern S., Pilhall M., Jern C. Effect of cholinergic blockade on heart rate, blood pressure and plasma catecholamine responses to mental stress in normal subjects. Clin. Auton. Res. 1:1991;225-231.
31. Martin C.E., Shaver J.A., Leon D.F., Thompson M.E., Reddy P.S., Leonard J.J. Autonomic mechanisms in hemodynamic responses to isometric exercise. J. Clin. Invest. 54:1974;104-115.
32. Perondi R., Saino A., Tio R.A., Pomidossi G., Gregorini L., Alessio P., Morganti A., Zanchetti A., Mancia G. ACE inhibition attenuates sympathetic coronary vasoconstriction in patients with coronary artery disease. Circulation. 85:1992;2004-2013.
33. Heistadd D.D., Abboud F.M., Eckstein J.W. Vasoconstrictor response to simulated diving in man. J. Appl. Physiol. 25:1968;542-549.
34. Navarro X., Kennedy W.R., Ferrer M.T. Cardiovascular responses to tilting in healthy and diabetic subjects. J. Neurol. Sci. 104:1991;39-45.
35. Task force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology, Heart rate variability: Standards of measurement, physiological interpretation and clinical use, Circulation 93 (1996) 1043-1065.
36. D.J. Ewing, Analysis of heart rate variability and other non-invasive tests with special reference to diabetes mellitus, in: R. Bannister, C.J. Mathias (Eds.), Autonomic Failure. A Textbook of Clinical Disorders of the Autonomic Nervous System, 3rd ed., Oxford University Press, Oxford, 1992, pp. 312-333.
37. Akselrod S., Gordon D., Madwed J.B., Snidman N.C., Shannon D.C., Cohen R. Hemodynamic regulation: Investigation by spectral analysis. Am. J. Physiol. 249:1985;H867-H875.
38. Wharton J., Polak J.M., Gordon L., Banner N.R., Springall D.R., Rose M., Khagani A., Wallwork J., Yacoub M.H. Immunohistochemical demonstration of human cardiac innervation before and after transplantation. Circ. Res. 66:1990;900-912.
39. Regitz V., Bossaller C., Strasser R., Schuler S., Hetzer R., Fleck E. Myocardial catecholamine content after heart transplantation. Circulation. 82:1990;620-623.
40. Bristow M.R. The surgically denervated, transplanted human heart. Circulation. 82:1990;658-660.
41. Stark R.P., McGinn A.L., Wilson R.F. Chest pain in cardiac-transplant recipients. Evidence of sensory reinnervation after cardiac transplantation. N. Engl. J. Med. 324:1991;1791-1794.
42. Casadei B., Pipilis A., Sessa F., Conway J., Sleight P. Low doses of scopolamine increase cardiac vagal tone in the acute phase of myocardial infarction. Circulation. 88:1993;353-357.
43. Floras J.S. Clinical aspects of sympathetic activation and parasympathetic withdrawal in heart failure. J. Am. Coll. Cardiol. 22:1993;72A-84A.
44. Malik M., Camm A.J. Heart rate variability and clinical cardiology. Br. Heart J. 71:1994;3-6.
45. Fei L., Anderson M.H., Katritsis D., Sneddon J., Statters D.J., Malik M., Camm A.J. Decreased heart rate variability in survivors of sudden cardiac death not associated with coronary artery disease. Br. Heart J. 71:1994;16-21.
46. Valkama J.O., Huikuri H.V., Koistinen M.J., Yli Mayry S., Airaksinen K.E., Myerburg R.J. Relation between heart rate variability and spontaneous and induced ventricular arrhythmias in patients with coronary artery disease. J. Am. Coll. Cardiol. 25:1995;437-443.
47. Burke M.N., McGinn A.L., Homans D.C., Christensen B.V., Kubo S.H., Wilson R. Evidence for functional sympathetic reinnervation of left ventricle and coronary arteries after orthotopic cardiac transplantation in humans. Circulation. 91:1995;72-78.
48. Benvenuti C., Aptecar E., Mazzucotelli J.P., Jouannot P., Loisance D., Nitenberg A. Coronary artery response to cold-pressor test is impaired early after operation in heart transplant recipients. J. Am. Coll. Cardiol. 26:1995;446-451.
49. D.K. Berke, A.F. Graham, J.S. Schroeder, D.C. Harrison, Arrhythmias in the denervated transplanted human heart, Circulation 48 (Suppl. 5) (1973).
50. de Jonge N., Jambroec G., Lahpor J.R., Woolley S.R. Ventricular fibrillation during acute rejection after heart transplantation. J. Heart Lung Transplant. 11:1992;797-798.