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Evidence for structural sympathetic reinnervation after orthotopic cardiac transplantation in humans.
Open accessAbstract
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 (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
L�ffelholz, K., & Muscholl, E. (1969) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf01417206 · Cited by 199
Glowniak, J. V., Turner, F. E., GRAY, L. L., Palac, R. T., Lagunas-Solar, M. C., & Woodward, W. R. (1989) · PubMed · Cited by 183
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
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
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
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
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
Rowan, R. A., & Billingham, M. E. (1988) · PubMed · Cited by 86
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
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
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Items 201–260 of 260
Heart rate variability, exercise capacity, and o2 uptake kinetics in heart transplant recipients
Mettauer, B., Fouillot, J.-P., Epailly, É., Zhao, Q. M., Charloux, A., Lampert, E., Heitz-Naegelen, B., Rieu, M., & Lonsdorfer, J. (1998) · Transplantation Proceedings · doi:10.1016/s0041-1345(98)00484-9 · Cited by 3
Caring for Transplant Recipients in a Nontransplant Setting
Hoffman, F. M., Nelson, B. J., Drangstveit, M. B., Flynn, B., Watercott, E. A., & Zirbes, J. M. (2006) · Critical Care Nurse · doi:10.4037/ccn2006.26.2.53 · Cited by 3
Dynamical Analysis of Heartbeat Interval Time Series After Cardiac Transplantation
Meyer, M., Marconi, C., Ferretti, G., FIOCCHI, R., Mamprin, F., Skinner, J. E., & Cerretelli, P. (1998) · Birkhäuser Basel eBooks · doi:10.1007/978-3-0348-8936-0_10 · Cited by 3
Packard, R. R. S., & Maddahi, J. (2017) · Journal of Nuclear Cardiology · doi:10.1007/s12350-016-0763-1 · Cited by 3
Wyller, V. B., Nygaard, S., Christensen, A. H., Rolid, K., Nytrøen, K., Gullestad, L. L., Fiane, A. E., Thaulow, E., Døhlen, G., & Saul, J. P. (2021) · European Journal of Applied Physiology · doi:10.1007/s00421-020-04586-0 · Cited by 3
β-Adrenoceptor desensitization despite cardiac denervation in human failing transplanted myocardium
Reithmann, C., von Scheidt, W., & Werdan, K. (1996) · International Journal of Cardiology · doi:10.1016/0167-5273(96)02709-x · Cited by 3
Cugini, P., Lucia, P., Scibilia, G., Palma, L. D., Cioli, A. R., Ciamei, A., Luca, A. D., & Marino, B. (1993) · Chronobiology International · doi:10.3109/07420529309059701 · Cited by 3
Heart neuronal imaging with carbon-11- and fluorine-18-labeled tracers
Wieland, D. M. (1992) · Developments in cardiovascular medicine · doi:10.1007/978-94-011-2456-0_31 · Cited by 3
Physiology and Pharmacology of the Transplanted Heart
Young, J. B. (2007) · Springer eBooks · doi:10.1007/978-0-585-34287-0_27 · Cited by 3
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Oh, S. (2024) · Korean Circulation Journal · doi:10.4070/kcj.2024.0050 · Cited by 2
Farid, T., Omer, M. A., GOSCH, K. L., Moser, A. R., Austin, B. A., Magalski, A., & Wimmer, A. P. (2017) · Journal of Interventional Cardiac Electrophysiology · doi:10.1007/s10840-017-0226-x · Cited by 2
Severe coronary artery spasm presenting as Prinzmetal's angina following cardiac transplantation
Parikh, P. B., Clerkin, K. J., MANCINI, D. M., & Kirtane, A. J. (2018) · Cardiovascular revascularization medicine · doi:10.1016/j.carrev.2018.06.019 · Cited by 2
Benefits of exercise in solid organ transplant recipients
Hernández-Sánchez, S. (2018) · Dialnet (Universidad de la Rioja) · Cited by 2
Mercier, J. G., Wintrebert, P., Caillaud, C., Varray, A. L., Albat, B., & Thévenet, A. (1994) · Science & Sports · doi:10.1016/s0765-1597(05)80161-3 · Cited by 2
Transplant-Associated Coronary Artery Disease: From Chronic Disease to Acute Myocardial Infarction
Hauptman, P. J., Ting, H. H., & Stone, P. H. (1995) · Annals of Emergency Medicine · doi:10.1016/s0196-0644(17)30482-1 · Cited by 2
Interventionelle Therapiestrategien bei resistenter Hypertonie
Linnenweber-Held, S., Schmidt, B. M. W., & Menne, J. (2011) · Der Nephrologe · doi:10.1007/s11560-011-0543-5 · Cited by 1
Coronary Vasomotor Response to Phenylephrine in Heart Transplant Patients
Aptecar, E., Corvoisier, P. L., Teíger, E., Dupouy, P. J., Vermès, E., Sediame, S., Hittinger, L., Loisance, D. Y., Dubois‐Randé, J., & Montagne, O. (2006) · The Journal of Heart and Lung Transplantation · doi:10.1016/j.healun.2006.03.001 · Cited by 1
Cardiac Transplantation: Denervation, Reinnervation, and Myocardial Blood Flow
Grupper, A., Gewirtz, H., & Kushwaha, S. S. (2016) · Springer eBooks · doi:10.1007/978-3-319-45800-7_10 · Cited by 1
You've got some nerve (after heart transplantation)
Tchoukina, I. F., & Shah, K. B. (2022) · The Journal of Heart and Lung Transplantation · doi:10.1016/j.healun.2022.02.024 · Cited by 1
Autonomic Nervous System Repair and Regeneration
Muratori, L., Fregnan, F., Carta, G., & Geuna, S. (2022) · Reference series in biomedical engineering · doi:10.1007/978-3-030-21052-6_2 · Cited by 1
Heart Transplantation: Indications, Outcome, and Long-Term Complications
Miller, L. W. (2007) · Springer eBooks · doi:10.1007/978-1-84628-715-2_67 · Cited by 1
Renal Denervation Therapy (RDT) in Resistant Hypertension
Amin, M. G., & Haque, H. F. (2012) · BIRDEM Medical Journal · doi:10.3329/birdem.v2i2.12325 · Cited by 1
Diagnosis and Management of Cardiac Allograft Vasculopathy (Chronic Rejection)
Miller, L. W., Donahue, T. A., Wolford, T. L., & Drury, J. H. (2007) · Springer eBooks · doi:10.1007/978-0-585-34287-0_35 · Cited by 1
Exercise-Induced Diastolic Left Ventricular Dysfunction after Heart Transplantation
Paulus, W. J. (1998) · KARGER eBooks · doi:10.1159/000061729 · Cited by 1
Lord, S., & McComb, J. M. (1996) · Heart · doi:10.1136/hrt.75.2.213 · Cited by 1
Gaer, J. A., Gordon, L., Wharton, J., Polak, J. M., Taylor, K. M., McKenna, W. J., & Parker, D. J. (1993) · Heart · doi:10.1136/hrt.70.6.574 · Cited by 1
Zusammenfassung: Spinale Schmerzverarbeitung
Waldvogel, H. H. (1996) · Springer eBooks · doi:10.1007/978-3-642-97649-0_5 · Cited by 1
Cardiovascular and Metabolic Responses to Exercise in Heart Transplanted Children
Marconi, C., Marzorati, M., FIOCCHI, R., Mamprin, F., Ferrazzi, P., Ferretti, G., & Cerretelli, P. (1996) · Springer eBooks · doi:10.1007/978-1-4615-5887-3_29 · Cited by 1
Transplanted Organs: Autonomous Reinnervation or Not?
Carr, F., & Bernard Swynghedauw, A. (1998) · KARGER eBooks · doi:10.1159/000061738
Innovative Therapieoptionen bei therapieresistenter arterieller Hypertonie
Linnenweber-Held, S., Haller, H. G., & Menne, J. (2012) · Journal für Kardiologie (Krause & Pachernegg GmbH)
Varray, A. L., Barthe, V., Mercier, J. G., Wintrebert, P., Albat, B., Thévenet, A., & PREFAUT, C. G. (1994) · Springer eBooks · doi:10.1007/978-4-431-68272-1_31
Hacker, M. (2002) · Elektronische Hochschulschriften der LMU München (Ludwig-Maximilians-Universität München) · doi:10.5282/edoc.153
Pathology and the Transplant Patient
Marboe, C. C., & Alobeid, B. (2004) · Humana Press eBooks · doi:10.1007/978-1-59259-758-1_6
Cardiac Transplantation: A Review for Critical Care Nurses
Ohler, L., Morris, K. H., McCauley, M. F., & DiSanto, P. (1994) · Journal of Intensive Care Medicine · doi:10.1177/088506669400900501 · Cited by 1
Présentation au service des urgences de patients ayant subi une transplantation cardiaque
Vranckx, M., Lheureux, P. E. R., Vachiéry, J., & Askenasi, R. (1998) · Réanimation Urgences · doi:10.1016/s1164-6756(98)80142-4
Moskopp, D., Kehl, H.-G., Horch, C., Pusk�s, Z., Wassmann, H., Schuierer, G. R., & Fingerhut, D. (1994) · Neurosurgical Review · doi:10.1007/bf00698772
Kreuder, J. G., Netz, H., Paul, T., Müller, A., Bauer, J. M., & Repp, R. (1996) · Cardiology in the Young · doi:10.1017/s1047951100003188
Evaluation of Sympathetic Reinnervation Using 123I-MIBG Scintigraphy in Cardiac Transplants
Kim, J. H., Shin, M., Hwang, K. H., Han, S. H., Koh, K. K., Ahn, T. H., Choi, I. S., Park, C. H., Park, K. Y., & Shin, E. K. (2003) · Korean Circulation Journal · doi:10.4070/kcj.2003.33.10.909
Lönnerholm, S. (2002) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
Pathology of Cardiac Transplantation
Tan, C. D., Halushka, M. K., & Rodríguez, E. R. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-420219-1.00016-1
Rehabilitación en pacientes con trasplante cardíaco
Lomelí, H. I. (2006) · Revista Portuguesa de Pneumologia
Autonomic Imaging in Heart Transplantation
Bengel, F. M. (2014) · Springer eBooks · doi:10.1007/978-3-662-45074-1_17
Cardiac Transplantation for Ischaemic Heart Disease
Yacoub, M. H. (1994) · Springer eBooks · doi:10.1007/978-3-642-78637-2_23
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Kinderkardiologie, A. D. A. F. (2010)
Interventionelle Therapiestrategien bei resistenter Hypertonie
Haller, H. G. (2011)
Krum, H., Schlaich, M. P., & Sobotka, P. A. (2012) · Elsevier eBooks · doi:10.1016/b978-1-4377-2766-1.00025-9
Johnson, M. R., Kao, W., Winkel, E., Bobadilla, J. L., Kohmoto, T., & Edwards, N. M. (2011) · doi:10.1002/9781444391770.ch8
EFFECT OF SYMPATHETIC REINNERVATION ON CARDIAC PERFORMANCE AFTER HEART TRANSPLANTATION
Engel, M., Eberfuhr, P. E. U., Chiepel, N. I. S., Ekolla, G. N., Eichart, B. R. R., & Chwaiger, M. A. S. (2001)
EFFECTS OF CARDIAC SYMPATHETIC INNERVATION ON CORONARY BLOOD FLOW
Arli, F. D. I. C., Ichael, M., Obes, C. T., Angner, T. H. M., Evine, B. L., Uzik, O. T. M., Hakroborty, P. U. C., & Evine, T. B. A. L. (1997)
Backman, S. B., Stein, R. D., Ralley, F. E., & FOX, G. S. (1996)
Allard, R. V., Hatzakorzian, R., Deschamps, A., & Backman, S. B. (2004)
von Scheidt, W. (2000) · Springer eBooks · doi:10.1007/978-3-662-12156-6_87
Cheng, D. (1994) · Canadian Journal of Anesthesia/Journal canadien d anesthésie · doi:10.1007/bf03010013
Bhaktavatsalam, B. J., Hambly, P., Ferguson, J. Y., Day, J., & Galitzine, S. V. (2022) · International Journal of Medical Anesthesiology · doi:10.33545/26643766.2022.v5.i1a.341
Physiology of the Transplanted Heart
Nikolova, A. (2025) · Springer eBooks · doi:10.1007/978-3-031-88290-6_10
Heart Failure, Pulmonary Hypertension, and Heart Transplantation
Dymarkowski, S., & Bogaert, J. (2005) · Springer eBooks · doi:10.1007/3-540-26997-5_10
Franchi, F., Marianello, D., Bianchi, C., Biuzzi, C., Gottin, L., Peluso, L., Maccherini, M., Cameli, M., Vendramin, I., Scolletta, S., et al. (2026) · Clinical Transplantation · doi:10.1111/ctr.70710
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Galeone, A., Mazzeo, G., Moretti, M., Munari, E., Gambaro, A., Capovilla, T. M., Brunelli, M., & Luciani, G. B. (2026) · Medicina · doi:10.3390/medicina62101987
Anästhesiologische Besonderheiten bei Patienten nach Herztransplantation
Weiss, B., & Schmid, E. R. (1991) · Klinische Anästhesiologie und Intensvtherapie · doi:10.1007/978-3-642-51139-4_23
Metadata
- 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 › Physiology (medical) › 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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