Evidence for structural sympathetic reinnervation after orthotopic cardiac transplantation in humans.
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BACKGROUND: Cardiac transplantation (CT) causes total cardiac denervation. METHODS AND RESULTS: To test directly for sympathetic reinnervation in humans, we measured the cardiac release of norepinephrine (NE) in response to tyramine (an agent that causes NE release from intact sympathetic nerve terminals) and sustained handgrip exercise (a reflex sympathetic stimulus) in 12 patients less than 5 months after CT, in 50 patients 1 year or more after CT, and in eight patients without CT. Plasma [NE] was measured in the aorta [( NE]Ao) and coronary sinus [( NE]CS) at rest, after tyramine administration (55 micrograms/kg, i.v.), and during sustained handgrip exercise. Cardiac NE release was determined by subtracting [NE]Ao from [NE]CS [( NE]CS-Ao). NE release was defined as [NE]CS-Ao during the intervention-[NE]CS-Ao at rest (delta [NE]CS-Ao). In patients studied within 5 months of CT, no significant NE release occurred after tyramine administration (delta [NE]CS-Ao, 33 +/- 18 pg/ml; range, -98 to 117 pg/ml) or handgrip exercise (delta [NE]CS-Ao, -34 +/- 10 pg/ml; range, -46 to 8 pg/ml; n = 10). Conversely, in 39 of 50 patients studied 1 year or more after CT, tyramine administration caused a significant cardiac NE release (delta [NE]CS-Ao, 500 +/- 59 pg/ml; range, -11 to 1,918 pg/ml), and handgrip exercise caused a significant NE release in 17 of 41 patients (delta [NE]CS-Ao, 189 +/- 34 pg/ml; range, -211 to 949 pg/ml). In normally innervated patients, tyramine caused an even larger NE release (delta [NE]Ao-CS, 1,943 +/- 210 pg/ml; range, 1,152 to 2,977 pg/ml), and handgrip exercise caused a significant NE release in two of seven patients (delta [NE]CS-Ao, 143 +/- 51 pg/ml; range, -15 to 338 pg/ml). CONCLUSIONS: Early after CT, neither tyramine nor handgrip exercise caused a significant cardiac release of NE, suggesting sympathetic denervation. Late after CT, most patients had a significant, but subnormal, NE release in response to pharmacological or reflex stimuli, suggesting that limited sympathetic reinnervation occurs in most patients after orthotopic CT.
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Most studies in humans of re-innervation of transplanted organs generally indicate that there is limited sympathetic fiber re-innervation by a year or more after transplant.
“Most studies in humans of re-innervation of transplanted organs (necessarily allogenic) generally indicate that there is limited sympathetic fiber re-innervation by a year or more after transplant [36], [37].”
From Sprouted Innervation into Uterine Transplants Contributes to the Development of Hyperalgesia in a Rat Model of Endometriosis (2012) · cites this paper as [36]
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Cites
A simplified radiometric assay for plasma norepinephrine and epinephrine
Passon, P. G., & Peuler, J. D. (1973) · Analytical Biochemistry · doi:10.1016/0003-2697(73)90517-4 · Cited by 637 · see citing works
L�ffelholz, K., & Muscholl, E. (1969) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf01417206 · Cited by 199 · see citing works
Glowniak, J. V., Turner, F. E., GRAY, L. L., Palac, R. T., Lagunas-Solar, M. C., & Woodward, W. R. (1989) · PubMed · Cited by 183 · see citing works
Hemodynamic Observations One and Two Years after Cardiac Transplantation in Man
Stinson, E. B., Griepp, R. B., SCHROEDER, J. S., Dong, E., & Shumway, N. E. (1972) · Circulation · doi:10.1161/01.cir.45.6.1183 · Cited by 182 · see citing works
Quigg, R. J., Rocco, M. B., Gauthier, D. F., Creager, M. A., Hartley, L. H., & Colucci, W. S. (1989) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(89)90183-6 · Cited by 120 · see citing works
Summing up: some implications of the neuron as a secreting cell
Smith, A. D. (1971) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1971.0076 · Cited by 109 · see citing works
Fallen, E. L., Kamath, M. V., Ghista, D. N., & FITCHETT, D. H. (1988) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(88)90094-x · Cited by 95 · see citing works
Synthesis, Binding, Release, and Metabolism of Norepinephrine in Normal and Transplanted Dog Hearts
Potter, L. T., Cooper, T., Willman, V. L., & WOLFE, D. E. (1965) · Circulation Research · doi:10.1161/01.res.16.5.468 · Cited by 91 · see citing works
Kontos, H. A., Thames, M. D., & Lower, R. R. (1970) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/s0022-5223(19)42475-6 · Cited by 77 · see citing works
Rowan, R. A., & Billingham, M. E. (1989) · PubMed · Cited by 73 · see citing works
Coronary vasodilator reserve after human orthotopic cardiac transplantation.
McGinn, A. L., Wilson, R. F., OLIVARI, M. T., Homans, D. C., & White, C. W. (1988) · Circulation · doi:10.1161/01.cir.78.5.1200 · Cited by 69 · see citing works
Self-citationReturn of neural responses after autotransplantation of the heart
Willman, V. L., Cooper, T., & Hanlon, C. (1964) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1964.207.1.187 · Cited by 69 · see citing works
Peiss, C. N., Cooper, T., Willman, V. L., & Randall, W. C. (1966) · Circulation Research · doi:10.1161/01.res.19.1.153 · Cited by 68 · see citing works
Heart Autotransplantation: Effect on Myocardial Catecholamine and Histamine
Cooper, T., Willman, V. L., Jellinek, M., & Hanlon, C. (1962) · Science · doi:10.1126/science.138.3536.40 · Cited by 66 · see citing works
Cardiac transplantation in man
Clark, D. A., SCHROEDER, J. S., Griepp, R. B., Stinson, E. B., Dong, E., Shumway, N. E., & Harrison, D. C. (1973) · The American Journal of Medicine · doi:10.1016/0002-9343(73)90114-9 · Cited by 63 · see citing works
Hosenpud, J. D., Morton, M. J., Wilson, R. A., Pantely, G. A., Norman, D. J., Cobanoglu, M. A., & STARR, A. M. (1989) · Circulation · doi:10.1161/01.cir.80.3.525 · Cited by 63 · see citing works
Self-citationCoronary artery spasm in the denervated transplanted human heart
Buda, A. J., Fowles, R. E., SCHROEDER, J. S., Hunt, S. A., Cipriano, P. R., Stinson, E. B., & Harrison, D. C. (1981) · The American Journal of Medicine · doi:10.1016/0002-9343(81)90890-1 · Cited by 60 · see citing works
Sinoatrial function after cardiac transplantation
Bexton, R. S., Nathan, A. W., Hellestrand, K. J., Cory-Pearce, R., Spurrell, R. A., English, T. A. H., & Camm, A. J. (1984) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(84)80247-8 · Cited by 59 · see citing works
DEGENERATION AND REGENERATION OF THE NERVES OF THE HEART AFTER TRANSPLANTATION
Norvell, J. E., & Lower, R. R. (1973) · Transplantation · doi:10.1097/00007890-197303000-00015 · Cited by 52 · see citing works
Kaye, M. P., Randall, W. C., Hageman, G. R., Geis, W. P., & PRIOLA, D. V. (1977) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1977.233.4.h431 · Cited by 50 · see citing works
Neural Responses Following Autotransplantation of the Canine Heart
Willman, V. L., Cooper, T., Cian, L. G., & Hanlon, C. (1963) · Circulation · doi:10.1161/01.cir.27.4.713 · Cited by 47 · see citing works
Exercise tachycardia not due to blood-borne agents in canine cardiac denervation
Donald, D., & Samueloff, S. (1966) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1966.211.3.703 · Cited by 45 · see citing works
Electrocardiography: Practical Applications with Vectorial Principles.
(1980) · Annals of Internal Medicine · doi:10.7326/0003-4819-93-4-650_4 · Cited by 44 · see citing works
Adverse effects of chronic cardiac denervation in conscious dogs with myocardial ischemia.
Lavallée, M., Amano, J., Vatner, S. F., Manders, W. T., Randall, W. C., & Thomas, J. X. (1985) · Circulation Research · doi:10.1161/01.res.57.3.383 · Cited by 40 · see citing works
Morphologic Findings in Human Cardiac Allografts
Milam, J. D., Shipkey, F. H., Cj, L., Nora, J. J., Leachman, R. D., Rochelle, D. G., Bloodwell, R. D., Hallman, G. L., & Cooley, D. A. (1970) · Circulation · doi:10.1161/01.cir.41.3.519 · Cited by 37 · see citing works
Pharmacologic quantitation of cardiac sympathetic reinnervation.
Ebert, P. A., & Dc, S. (1970) · PubMed · Cited by 15 · see citing works
Effect of tyramine on myocardial catecholamine release in coronary heart disease
Forman, M. B., Robertson, D., Goldberg, M., Bostick, D., Uderman, H. D., Perry, J., & Robertson, R. M. (1984) · The American Journal of Cardiology · doi:10.1016/0002-9149(84)90015-8 · Cited by 11 · see citing works
Coronary artery spasm in a denervated orthotopic transplanted human heart
Goldenberg, I. F., & Levine, T. B. (1986) · Catheterization and Cardiovascular Diagnosis · doi:10.1002/ccd.1810120111 · Cited by 8 · see citing works
Flagged first, then by citations
Research works printed but not linked: 9
- Feigel EO: Coronary physiology. Physiol Rev 1983;63:1-205
- Levy MN, Martin PJ: Neural control of the heart, in Berne RM (ed): Handbook of Physiology-Cardiovascular System I. Baltimore, Waverly Press, Inc, 1979
- Clark DA, Schroeder JS, Griepp RB, Stinson EB, Dong E, Shumway NE, Harrison DC: Cardiac transplantation: Review of first three years experience. Am J Med 1973;54:563-576
- Klein RL, Lagercrantz H, Zimmerman H: Chemical neuro- transmission -An introduction, in Klein RL, Lagercrantz H, Zimmerman H (eds): Neurotransmitter Vesicles. New York, Academic Press, Inc, 1982, pp 16-21
- Thureson-Klein A: Fine structure of the isolated norandren- ergic vesicles, in Klein RL, Lagercrantz H, Zimmerman H (eds): Neurotransmitter Vesicles. New York, Academic Press, Inc, 1982, pp 131-132
- Klein RL: Physiological and pharmacological properties of isolated norandrenergic vesicles, in Klein RL, Lagercrantz H, Zimmerman H (eds): Neurotransmitter Vesicles. New York, Academic Press, Inc, 1982, pp 209-210
- Gilbert EM, Eiswirth CC, Mealey PC, Larrabee P, Herrick CM, Bristow MR: ,B-Adrenergic supersensitivity of the trans- planted human heart is presynaptic in origin. Circulation 1989;79:344-349
- Hodgson JMB, Cohen MD, Szentpetery S, Thames MD: Effects of regional a-and 3-blockade on resting and hyper- emic coronary blood flow in conscious, unstressed humans. Circulation 1989;79:797-809
- Denniss AR, Marsh JD, Quigg RJ, Gordon JB, Colucci WS: /3-Adrenergic receptor number and adenylate cyclase function in denervated transplanted and cardiomyopathic human hearts. Circulation 1989;79:1028-1034
Cited by
Sorted by citations
Kohl, P. K., Hunter, P. J., & Noble, D. (1999) · Progress in Biophysics and Molecular Biology · doi:10.1016/s0079-6107(98)00038-8 · Cited by 293 · see citing works
Effect of Sympathetic Reinnervation on Cardiac Performance after Heart Transplantation
Bengel, F. M., Ueberfuhr, P., Schiepel, N., Nekolla, S. G., Reichart, B., & Schwaiger, M. (2001) · New England Journal of Medicine · doi:10.1056/nejmoa010519 · Cited by 292 · see citing works
Effects of cardiac sympathetic innervation on coronary blood flow
Di Carli, M. F., Tobes, M. C., Mangner, T., Levine, A. B., Muzik, O., Chakroborty, P., & Levine, T. B. (1997) · New England Journal of Medicine · doi:10.1056/nejm199704243361703 · Cited by 237 · see citing works
Stark, R. P., McGinn, A. L., & Wilson, R. F. (1991) · New England Journal of Medicine · doi:10.1056/nejm199106203242507 · Cited by 222 · see citing works
Self-citationVasovagal reactions may occur after orthotopic heart transplantation
Fitzpatrick, A. P., Banner, N., Cheng, A. B., Yacoub, M. H., & Sutton, R. (1993) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(93)90235-s · Cited by 214 · see citing works
Oh, S., Zhang, Y., Bibevski, S., Marrouche, N. F., Natale, A., & Mazgalev, T. N. (2006) · Heart Rhythm · doi:10.1016/j.hrthm.2006.02.020 · Cited by 180 · see citing works
Serial Assessment of Sympathetic Reinnervation After Orthotopic Heart Transplantation
Bengel, F. M., Ueberfuhr, P., Ziegler, S. I., Nekolla, S. G., Reichart, B., & Schwaiger, M. (1999) · Circulation · doi:10.1161/01.cir.99.14.1866 · Cited by 154 · see citing works
Early Denervation and Later Reinnervation of the Heart Following Cardiac Transplantation: A Review
Awad, M. A., Czer, L. S. C., Hou, M., Golshani, S. S., Goltche, M., Robertis, M. D., Kittleson, M. M., Patel, J. K., Azarbal, B., Kransdorf, E. P., et al. (2016) · Journal of the American Heart Association · doi:10.1161/jaha.116.004070 · Cited by 152 · see citing works
Bernardi, L., Bianchini, B., Spadacini, G., Leuzzi, S., Valle, F., Marchesi, E., Passino, C., Calciati, A., Viganò, M., Rinaldi, M., et al. (1995) · Circulation · doi:10.1161/01.cir.92.10.2895 · Cited by 150 · see citing works
Exercise Training in Solid Organ Transplant Recipients
Didsbury, M. S., McGee, R., Tong, A., Craig, J. C., Chapman, J. R., Chadban, S. J., & Wong, G. (2013) · Transplantation · doi:10.1097/tp.0b013e31827a3d3e · Cited by 143 · see citing works
Cardiac muscarinic receptors decrease with age. In vitro and in vivo studies.
Brodde, O., Konschak, U., Becker, K., Rüter, F., Poller, U., Jakubetz, J., Radke, J., & Zerkowski, H. R. (1998) · Journal of Clinical Investigation · doi:10.1172/jci1113 · Cited by 140 · see citing works
Miller, L. W., Schlant, R. C., KOBASHIGAWA, J. A., Kubo, S. H., & Renlund, D. G. (1993) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(93)90814-h · Cited by 140 · see citing works
Topography of cardiac ganglia in the adult human heart
Singh, S., Johnson, P. I., Lee, R. E., Orfei, E., Lonchyna, V. A., Sullivan, H. J., Montoya, A., Tran, H., Wehrmacher, W. H., & Wurster, R. D. (1996) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/s0022-5223(96)70094-6 · Cited by 135 · see citing works
Marco, T. D., Dae, M. W., Yuen-Green, M. S. F., Kumar, S. N., Sudhir, K., Keith, F. M., Amidon, T. M., Rifkin, C., Klinski, C. S., Lau, D. M., et al. (1995) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(94)00463-z · Cited by 134 · see citing works
Givertz, M. M., Hartley, L. H., & Colucci, W. S. (1997) · Circulation · doi:10.1161/01.cir.96.1.232 · Cited by 128 · see citing works
The surgically denervated, transplanted human heart.
Bristow, M. R. (1990) · Circulation · doi:10.1161/01.cir.82.2.658 · Cited by 127 · see citing works
Jacobsen, T. N., Morgan, B. J., Scherrer, U., Vissing, S. F., Lange, R. A., Johnson, N., Ring, W. S., Rahko, P. S., Hanson, P., & Victor, R. G. (1993) · Circulation Research · doi:10.1161/01.res.73.2.367 · Cited by 125 · see citing works
Current Status of Cardiac Transplantation
Hunt, S. A. (1998) · JAMA · doi:10.1001/jama.280.19.1692 · Cited by 115 · see citing works
Bengel, F. M., Ueberfuhr, P., Hesse, T., Schiepel, N., Ziegler, S. I., Scholz, S., Nekolla, S. G., Reichart, B., & Schwaiger, M. (2002) · Circulation · doi:10.1161/01.cir.0000025631.68522.9d · Cited by 113 · see citing works
Deficient acceleration of left ventricular relaxation during exercise after heart transplantation.
Paulus, W. J., Bronzwaer, J. G. F., Felice, H., Kishan, N., & Wellens, F. (1992) · Circulation · doi:10.1161/01.cir.86.4.1175 · Cited by 108 · see citing works
Exercise after heart transplantation: An overview
Nytrøen, K., & Gullestad, L. L. (2013) · World Journal of Transplantation · doi:10.5500/wjt.v3.i4.78 · Cited by 105 · see citing works
Vagal denervation and reinnervation after ablation of ganglionated plexi
Sakamoto, S., Schuessler, R. B., Lee, A. M., Aziz, A., Lall, S. C., & Damiano, R. J. (2009) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2009.04.056 · Cited by 105 · see citing works
Exercise Following Heart Transplantation
Braith, R. W., & Edwards, D. G. (2000) · Sports Medicine · doi:10.2165/00007256-200030030-00003 · Cited by 103 · see citing works
Anaesthesia for a patient with a cardiac transplant
Morgan‐Hughes, N. J., & Hood, G. (2002) · Continuing Education in Anaesthesia Critical Care & Pain · doi:10.1093/bjacepd/2.3.74 · Cited by 100 · see citing works
Patel, A. D., & Iskandrian, A. E. (2002) · Journal of Nuclear Cardiology · doi:10.1067/mnc.2002.121471 · Cited by 98 · see citing works
Burke, M. N., McGinn, A. L., Homans, D. C., Christensen, B. V., Kubo, S. H., & Wilson, R. F. (1995) · Circulation · doi:10.1161/01.cir.91.1.72 · Cited by 96 · see citing works
Self-citationThe Breuer-Hering Reflex in Humans. Effects of Pulmonary Denervation and Hypocapnia
Iber, C., Simon, P. M., Skatrud, J. B., Mahowald, M. W., & Dempsey, J. A. (1995) · American Journal of Respiratory and Critical Care Medicine · doi:10.1164/ajrccm.152.1.7599827 · Cited by 88 · see citing works
Functional significance of cardiac reinnervation in heart transplant recipients
Schwaiblmair, M., von Scheidt, W., Überfuhr, P., Ziegler, S. I., Schwaiger, M., Reichart, B., & Vogelmeier, C. F. (1999) · The Journal of Heart and Lung Transplantation · doi:10.1016/s1053-2498(99)00048-0 · Cited by 86 · see citing works
Natural History of Left Ventricular Mechanics in Transplanted Hearts
Eleid, M. F., Caracciolo, G., Cho, E. J., Scott, R. L., Steidley, D. E., Wilansky, S., Arabía, F. A., Khandheria, B. K., & Sengupta, P. P. (2010) · JACC. Cardiovascular imaging · doi:10.1016/j.jcmg.2010.07.009 · Cited by 84 · see citing works
The heart reinnervates after transplantation
Murphy, D. A., Thompson, G. W., Ardell, J. L., McCraty, R., Stevenson, R. S., SANGALANG, V. E., Cardinal, R., Wilkinson, M., Craig, S., Smith, F. M., et al. (2000) · The Annals of Thoracic Surgery · doi:10.1016/s0003-4975(00)01240-6 · Cited by 82 · see citing works
Long-term complications of cardiac transplantation
Miller, L. W. (1991) · Progress in Cardiovascular Diseases · doi:10.1016/0033-0620(91)90028-k · Cited by 79 · see citing works
Sympathetic Reinnervation of the Sinus Node and Exercise Hemodynamics After Cardiac Transplantation
Wilson, R. F., Johnson, T. H., Haidet, G. C., Kubo, S. H., & Mianuelli, M. (2000) · Circulation · doi:10.1161/01.cir.101.23.2727 · Cited by 76 · see citing works
Self-citationCoronary blood flow responses to physiological stress in humans
Momen, A., Mascarenhas, V., Gahremanpour, A., Gao, Z., Moradkhan, R., Kunselman, A. R., BOEHMER, J. P., Sinoway, L. I., & Leuenberger, U. A. (2009) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01075.2007 · Cited by 72 · see citing works
Reinnervation post-Heart transplantation
Grupper, A., Gewirtz, H., & Kushwaha, S. S. (2016) · European Heart Journal · doi:10.1093/eurheartj/ehw604 · Cited by 71 · see citing works
Grassi, B., Marconi, C., Meyer, M., Rieu, M., & Cerretelli, P. (1997) · Journal of Applied Physiology · doi:10.1152/jappl.1997.82.6.1952 · Cited by 71 · see citing works
Rabinovitch, M. A., Rose, C. P., Schwab, A., FITCHETT, D. H., Honos, G. N., Stewart, J. A., Chen, L. F., Castilla, E. P., Gomez, A. A., & Abrahamowicz, M. (1993) · PubMed · Cited by 70 · see citing works
Sympathetic Denervation and Reinnervation After Arterial Switch Operation for Complete Transposition
Kondo, C., Nakazawa, M., Momma, K., & Kusakabe, K. (1998) · Circulation · doi:10.1161/01.cir.97.24.2414 · Cited by 67 · see citing works
Überfuhr, P., Ziegler, S. I., Schwaiblmair, M., Reichart, B., & Schwaiger, M. (2000) · European Journal of Cardio-Thoracic Surgery · doi:10.1016/s1010-7940(99)00367-x · Cited by 67 · see citing works
Reinnervation of the transplanted human heart as evidenced from heart rate variability studies
Halpert, I., Goldberg, A. D., Levine, A. B., Levine, T. B., Kornberg, R. J., Kelly, C., & Lesch, M. (1996) · The American Journal of Cardiology · doi:10.1016/s0002-9149(96)90592-5 · Cited by 63 · see citing works
Long-term cardiorespiratory results of exercise training following cardiac transplantation
Kavanagh, T., Mertens, D. J., Shephard, R. J., Beyene, J., Kennedy, J., Campbell, R. B., Sawyer, P., & Yacoub, M. H. (2003) · The American Journal of Cardiology · doi:10.1016/s0002-9149(02)03108-9 · Cited by 61 · see citing works
McAllister, S. L., Dmitrieva, N., & Berkley, K. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031758 · Cited by 60 · see citing works
“Most studies in humans of reinnervation of transplanted organs (necessarily allogenic) generally indicate that there is limited sympathetic fiber re-innervation by a year or more after transplant [36,37].”
Different Evolutions in Heart Rate Variability after Heart Transplantation: 10-Year Follow-Up
Beckers, F., Ramaekers, D., Speijer, G., Ector, H., Vanhaecke, J., Verheyden, B., Cleemput, J. V., Droogné, W., de Werf, F. V., & AUBERT, A. E. (2004) · Transplantation · doi:10.1097/01.tp.0000141093.04132.41 · Cited by 58 · see citing works
Optimal Cardiac Pacing After Heart Transplantation
Melton, I., GILLIGAN, D. M., Wood, M. A., & Ellenbogen, K. A. (1999) · Pacing and Clinical Electrophysiology · doi:10.1111/j.1540-8159.1999.tb00356.x · Cited by 57 · see citing works
Anaesthesia for non-cardiac surgery in heart-transplanted patients
Cheng, D., & Ong, D. (1993) · Canadian Journal of Anesthesia/Journal canadien d anesthésie · doi:10.1007/bf03010103 · Cited by 56 · see citing works
Überfuhr, P., Frey, A. W., Ziegler, S. I., Reichart, B., & Schwaiger, M. (2000) · The Journal of Heart and Lung Transplantation · doi:10.1016/s1053-2498(00)00060-7 · Cited by 55 · see citing works
Radionuclide imaging of cardiac autonomic innervation
Ji, S. Y., & Travin, M. I. (2010) · Journal of Nuclear Cardiology · doi:10.1007/s12350-010-9239-x · Cited by 52 · see citing works
LORD, S. W., SENIOR, R. R., Das, M., Whittam, A. M., Murray, A., & McComb, J. M. (2001) · Clinical Science · doi:10.1042/cs20000111 · Cited by 52 · see citing works
Myocardial Efficiency and Sympathetic Reinnervation After Orthotopic Heart Transplantation
Bengel, F. M., Ueberfuhr, P., Schiepel, N., Nekolla, S. G., Reichart, B., & Schwaiger, M. (2001) · Circulation · doi:10.1161/01.cir.103.14.1881 · Cited by 52 · see citing works
Efficacy of augmented immunosuppressive therapy for early vasculopathy in heart transplantation
Lamich, R., Ballester, M., Vicens Martí, C., Brossa, V., Aymat, R. M., Carrió, I., Bernà, L., Campreciós, M., Puig, M., Estorch, M., et al. (1998) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(98)00234-4 · Cited by 51 · see citing works
Dobutamine Enhances Cardiodepressant Effects of Receptor-Mediated Coronary Endothelial Stimulation
Bartúnek, J., Shah, A. M., Vanderheyden, M., & Paulus, W. J. (1997) · Circulation · doi:10.1161/01.cir.95.1.90 · Cited by 51 · see citing works
Novel procedure- and device-based strategies in the management of systemic hypertension
Krum, H., Schlaich, M. P., Sobotka, P. A., Scheffers, I. J. M., Kroon, A. A., & de Leeuw, P. W. (2011) · European Heart Journal · doi:10.1093/eurheartj/ehq457 · Cited by 50 · see citing works
Arrowood, J. A., Goudreau, E., Minisi, A. J., Davis, A. B., & Mohanty, P. K. (1995) · Circulation · doi:10.1161/01.cir.92.3.402 · Cited by 49 · see citing works
von Scheidt, W., Böhm, M., Schneider, B., Reichart, B., Erdmann, E., & Autenrieth, G. (1992) · Circulation · doi:10.1161/01.cir.85.3.1056 · Cited by 49 · see citing works
Heart Rate Variability After Cardiac Transplantation in Humans
Ramaekers, D., Ector, H., Vanhaecke, J., Cleemput, J. V., & de Werf, F. V. (1996) · Pacing and Clinical Electrophysiology · doi:10.1111/j.1540-8159.1996.tb03286.x · Cited by 47 · see citing works
Role of ventricular vagal afferents in the vasovagal reaction
Waxman, M. B., CAMERON, D. A., & Wald, R. W. (1993) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(93)90236-t · Cited by 47 · see citing works
Überfuhr, P. (1997) · European Journal of Cardio-Thoracic Surgery · doi:10.1016/s1010-7940(97)00271-6 · Cited by 45 · see citing works
Cardiac sympathetic neuronal imaging using PET
Läutamaki, R., Tipre, D. N., & Bengel, F. M. (2007) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s00259-007-0442-1 · Cited by 45 · see citing works
Functional restitution of cardiac control in heart transplant patients
Toledo, E., Pinhas, I., Aravot, D. J., Almog, Y., & AKSELROD, S. (2002) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00467.2001 · Cited by 45 · see citing works
Neostigmine decreases heart rate in heart transplant patients
Backman, S. B., FOX, G. S., Stein, R. D., & Ralley, F. E. (1996) · Canadian Journal of Anesthesia/Journal canadien d anesthésie · doi:10.1007/bf03011717 · Cited by 44 · see citing works
Vagal reinnervation in the long term after orthotopic heart transplantation
Überfuhr, P., Frey, A. W., & Reichart, B. (2000) · The Journal of Heart and Lung Transplantation · doi:10.1016/s1053-2498(00)00181-9 · Cited by 44 · see citing works
Kazmirczak, F., Nijjar, P. S., Zhang, L. J., Hughes, A. N., Chen, K.-H. A., Okasha, O., Martin, C. M., Akçakaya, M., Farzaneh‐Far, A., & Shenoy, C. (2019) · Journal of Cardiovascular Magnetic Resonance · doi:10.1186/s12968-018-0515-2 · Cited by 43 · see citing works
Bengel, F. M., Ueberfuhr, P., Kärjä, J., SCHREIBER, K., Nekolla, S. G., Reichart, B., & Schwaiger, M. (2004) · European Heart Journal · doi:10.1016/j.ehj.2004.07.009 · Cited by 43 · see citing works
Palpitations and Cardiac Awareness After Heart Transplantation
BARSKY, A. J., Ahern, D. K., Brener, J. M., Surman, O. S., Ring, C., & DEC, G. W. (1998) · Psychosomatic Medicine · doi:10.1097/00006842-199809000-00007 · Cited by 41 · see citing works
Pašić, M., Musci, M., Siniawski, H., Grauhan, O., Edelmann, B., Tedoriya, T., Weng, Y., & Hetzer, R. (1999) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/s0022-5223(99)70219-9 · Cited by 41 · see citing works
Flyer, J. N., Zuckerman, W. A., Richmond, M. E., Anderson, B. R., Mendelsberg, T. G., McAllister, J., Liberman, L., Addonizio, L. J., & Silver, E. S. (2017) · Circulation · doi:10.1161/circulationaha.117.028087 · Cited by 39 · see citing works
Raczak, G. (1999) · The Journal of Heart and Lung Transplantation · doi:10.1016/s1053-2498(98)00071-0 · Cited by 38 · see citing works
Exercise and organ transplantation
Kjær, M., Beyer, N., & Secher, N. H. (1999) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/j.1600-0838.1999.tb00200.x · Cited by 38 · see citing works
de Lorgeril, M., Dureau, G., Boissonnat, P., Guidollet, J., Juhan-Vague, I., Bizollon, C., & Renaud, S. (1992) · Arteriosclerosis and Thrombosis A Journal of Vascular Biology · doi:10.1161/01.atv.12.2.222 · Cited by 38 · see citing works
Dobutamine myocardial scintigraphy for the prediction of cardiac events after heart transplantation
Hacker, M., Tausig, A., Romüller, B., Hoyer, X., Klauß, V., Stempfle, U., Reichart, B., Hahn, K. M., & Tiling, R. (2005) · Nuclear Medicine Communications · doi:10.1097/01.mnm.0000167908.30977.fe · Cited by 37 · see citing works
Ventilatory response to exercise after heart and lung denervation in humans
Grassi, B., Ferretti, G., Xi, L., Rieu, M., Meyer, M., Marconi, C., & Cerretelli, P. (1993) · Respiration Physiology · doi:10.1016/0034-5687(93)90014-2 · Cited by 37 · see citing works
Hayman, M. A., Nativi, J. N., Stehlik, J., McDaniel, J., Fjeldstad, A. S., Ives, S. J., Wray, D. W., Bader, F. M., Gilbert, E. M., & Richardson, R. S. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00580.2010 · Cited by 37 · see citing works
Kushwaha, S. S., Narula, J., Narula, N., Zervos, G. D., Semigran, M. J., Fischman, A. J., Alpert, N. M., Dec, G. W., & Gewirtz, H. (1998) · The American Journal of Cardiology · doi:10.1016/s0002-9149(98)00645-6 · Cited by 37 · see citing works
Chest Pain in Heart-Transplant Recipients
SCHROEDER, J. S., & Hunt, S. A. (1991) · New England Journal of Medicine · doi:10.1056/nejm199106203242509 · Cited by 37 · see citing works
Bengel, F. M., Ueberfuhr, P., Ziegler, S. I., Nekolla, S. G., Odaka, K., Reichart, B., & Schwaiger, M. (2000) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/s002590000366 · Cited by 36 · see citing works
Arrhythmias After Orthotopic Heart Transplantation
Stecker, E. C., Strelich, K. R., Chugh, S. S., Crispell, K. A., & McAnulty, J. H. (2005) · Journal of Cardiac Failure · doi:10.1016/j.cardfail.2005.02.005 · Cited by 35 · see citing works
Canine myocardial beta-adrenergic, muscarinic receptor densities after denervation: a PET study.
Valette, H., Deleuze, P., Syrota, A., Delforge, J., Crouzel, C., Fuseau, C., & Loisance, D. Y. (1995) · PubMed · Cited by 35 · see citing works
Re-innervation after heart transplantation: a multidisciplinary study
Page, J. C. G., Segovia, J., Alonso‐Pulpón, L., Alonso-Rodríguez, M., Salas, C., & Ortíz-Berrocal, J. (2004) · The Journal of Heart and Lung Transplantation · doi:10.1016/j.healun.2003.07.011 · Cited by 34 · see citing works
Kresh, J. Y., & Izrailtyan, I. (1998) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1998.275.3.r720 · Cited by 34 · see citing works
de Lorgeril, M., Boissonnat, P., MAMELLE, N., Martin, J., Monjaud, I., Guidollet, J., Dureau, G., Ninet, J., & Renaud, S. (1994) · Circulation · doi:10.1161/01.cir.89.6.2590 · Cited by 34 · see citing works
Exercise response after cardiac transplantation: correlation with sympathetic reinnervation.
Lord, S. W., Brady, S., Holt, N. D., Mitchell, L., Dark, J. H., & McComb, J. M. (1996) · Heart · doi:10.1136/hrt.75.1.40 · Cited by 32 · see citing works
Singh, T. P., Gauvreau, K., Rhodes, J., & Blume, E. D. (2007) · The Journal of Heart and Lung Transplantation · doi:10.1016/j.healun.2007.08.013 · Cited by 32 · see citing works
Anaesthesia for patients with a transplanted organ
Toivonen, H. J. (2000) · Acta Anaesthesiologica Scandinavica · doi:10.1034/j.1399-6576.2000.440708.x · Cited by 31 · see citing works
Hirose, R., Taguchi, T., Hirata, Y., Yamada, T., Nada, O., & Suita, S. (1995) · Surgery · doi:10.1016/s0039-6060(05)80256-9 · Cited by 31 · see citing works
Task force 4: Function of the heart trnsplant recipient
Young, J. B., Winters, W. L., Bourge, R. C., & Uretsky, B. F. (1993) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(93)90813-g · Cited by 31 · see citing works
Imamura, T., Kinugawa, K., Okada, I., Kato, N., Fujino, T., Inaba, T., Maki, H., Hatano, M., Kinoshita, O., Nawata, K., et al. (2015) · International Heart Journal · doi:10.1536/ihj.14-292 · Cited by 30 · see citing works
Thompson, D., Koster, M. J., Wagner, R. H., Heroux, A. L., & Barron, J. T. (2011) · European Heart Journal - Cardiovascular Imaging · doi:10.1093/ejechocard/jer270 · Cited by 30 · see citing works
Gürtner, C., Krause, B. J., Klepzig, H., Herrmann, G., Lelbach, S., Vockert, E. K., Hartmann, A., Maul, F. D., Kranert, T., Mutschler, E., et al. (1995) · European Journal of Nuclear Medicine and Molecular Imaging · doi:10.1007/bf00839059 · Cited by 29 · see citing works
The heart rate response to exercise and circulating catecholamines in heart transplant recipients
Ferretti, G., Marconi, C., Achilli, G., Caspani, E., FIOCCHI, R., Mamprin, F., Gamba, A., Ferrazzi, P., & Cerretelli, P. (2002) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s004240100701 · Cited by 29 · see citing works
Rudas, L., Pflugfelder, P. W., McKenzie, F., Menkis, A. H., Novick, R. J., & Kostuk, W. J. (1992) · The American Journal of Cardiology · doi:10.1016/0002-9149(92)91232-s · Cited by 29 · see citing works
Vanderlaan, R. D., Conway, J. L., Manlhiot, C., McCrindle, B. W., & Dipchand, A. I. (2012) · American Journal of Transplantation · doi:10.1111/j.1600-6143.2012.04046.x · Cited by 28 · see citing works
Outcomes and Complications After Heart Transplantation
Hoffman, F. M. (2005) · The Journal of Cardiovascular Nursing · doi:10.1097/00005082-200509001-00005 · Cited by 28 · see citing works
Kushwaha, S. S., Banner, N. R., Patel, N., Cox, A., Patton, H., & Yacoub, M. H. (1994) · Heart · doi:10.1136/hrt.71.5.431 · Cited by 28 · see citing works
Anatomy of the cardiac nervous system with clinical and comparative morphological implications
Kawashima, T. (2010) · Anatomical Science International · doi:10.1007/s12565-010-0096-0 · Cited by 27 · see citing works
RESPIRATORY SINUS DYSRHYTHMIA PERSISTS IN TRANSPLANTED HUMAN HEARTS FOLLOWING AUTONOMIC BLOCKADE
Slovut, D. P., Wenstrom, J. C., Moeckel, R. B., Wilson, R. F., Osborn, J. W., & Abrams, J. H. (1998) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.1998.tb02358.x · Cited by 27 · see citing works
Self-citationFarrukh, H. M., White, M., Port, J. D., Handwerger, D., Larrabee, P., Klein, J., Roden, R. A., Skerl, L., Renlund, D. G., Feldman, A. M., et al. (1993) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(93)90777-x · Cited by 27 · see citing works
Cardiac Neuronal Imaging at the Edge of Clinical Application
Travin, M. I. (2009) · Cardiology Clinics · doi:10.1016/j.ccl.2008.12.007 · Cited by 26 · see citing works
Function of the Transplanted Heart: Unique Physiology and Therapeutic Implications
Cotts, W., & Oren, R. M. (1997) · The American Journal of the Medical Sciences · doi:10.1016/s0002-9629(15)40190-9 · Cited by 26 · see citing works
Dobutamine Stress-Induced Angina in Patients With Denervated Cardiac Transplants
Akosah, K. O., Olsovsky, M. R., & Mohanty, P. K. (1995) · CHEST Journal · doi:10.1378/chest.108.3.695 · Cited by 26 · see citing works
Influence of post-surgery time after cardiac transplantation on exercise responses
Mercier, J. G., VILLE, N., Wintrebert, P., Caillaud, C., Varray, A. L., Albat, B., VENET, A. T., & FAUT, C. P. (1996) · Medicine & Science in Sports & Exercise · doi:10.1097/00005768-199602000-00003 · Cited by 26 · see citing works
Imamura, T., Kinugawa, K., Fujino, T., Inaba, T., Maki, H., Hatano, M., Kinoshita, O., Nawata, K., Kyo, S., & Ōno, M. (2014) · International Heart Journal · doi:10.1536/ihj.14-111 · Cited by 25 · see citing works
- Authors
- Wilson, R. F., Christensen, B. V., Olivari, M. T., Simon, A., White, C. W., & Laxson, D. D.
- Affiliations
- University of Minnesota (US)
- Venue
- Circulation
- Published
- 1991-04
- Volume
- 83
- Issue
- 4
- Pages
- 1210-1220
- ISSN
- 0009-7322 (ISSN-L)
- 1524-4539
- OpenAlex
- W1977408829
- Cited by
- 261
- References
- 28
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 1 · 2023: 2 · 2022: 4 · 2021: 4 · 2020: 3 · 2019: 3 · 2018: 3 · 2017: 5 · 2016: 7 · 2015: 4 · 2014: 2 · 2013: 3 · 2012: 6
- FWCI
- 22.20
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Circulation (publishedVersion)
- PubMed (publishedVersion)
- Funders
- American Heart Association
- University of Minnesota
- National Institutes of Health (5r01hl039185-03)
- National Heart, Lung, and Blood Institute (R01-HL39185)
- Topics
- Health Sciences › Medicine › Surgery › Transplantation: Methods and Outcomes
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
- Keywords
- orthotopic heart transplantation, cardiac denervation, noradrenaline release, tyramine, handgrip exercise, coronary sinus, sympathetic nerve terminals
- MeSH terms
- Electrocardiography, Heart, Cardiac Catheterization, Humans, Norepinephrine, Reflex, Sympathetic Nervous System, Time Factors, Tyramine, Exercise, Heart Transplantation
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