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Evidence for time-dependent autonomic cardiac reinnervation in children subsequent to transplantation of the heart

Published online by Cambridge University Press:  19 August 2008

Joachim Kreuder ,
Heinrich Netz ,
Thomas Paul ,
Andreas Müller ,
Jürgen Bauer  and
Reinald Repp
Joachim Kreuder*
Affiliation:
From the Departments of Pediatric Cardiology, Justus-Liebig University, Giessen, Ludwig-Maximilians University, München and University Medical School, Hannover
Heinrich Netz
Affiliation:
From the Departments of Pediatric Cardiology, Justus-Liebig University, Giessen, Ludwig-Maximilians University, München and University Medical School, Hannover
Thomas Paul
Affiliation:
From the Departments of Pediatric Cardiology, Justus-Liebig University, Giessen, Ludwig-Maximilians University, München and University Medical School, Hannover
Andreas Müller
Affiliation:
From the Departments of Pediatric Cardiology, Justus-Liebig University, Giessen, Ludwig-Maximilians University, München and University Medical School, Hannover
Jürgen Bauer
Affiliation:
From the Departments of Pediatric Cardiology, Justus-Liebig University, Giessen, Ludwig-Maximilians University, München and University Medical School, Hannover
Reinald Repp
Affiliation:
From the Departments of Pediatric Cardiology, Justus-Liebig University, Giessen, Ludwig-Maximilians University, München and University Medical School, Hannover
*
Dr. Joachim Kreuder, Children's Hospital, Justus-Liebig University, Feulgenstraße 12, D-35385 Giessen, Germany. Tel. 49 641 702 4400; Fax. 49 641 702 4489.
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Abstract

Autonomic denervation has been assumed to persist after orthotopic heart transplantation. Analyzing spontaneous and induced variations of heart rate, the status of autonomic cardiac innervation was investigated in six children 19–37 months after cardiac transplantation. The age at the time of transplantation varied from three weeks to 15.4 years. Heart rate variability was assessed on 24-hour Holter recordings by calculating time-domain indices (standard deviation of all RR intervals; standard deviation of the mean RR intervals from successive five-minute periods; mean of the standard deviations of RR intervals from successive five-minute periods; proportion of adjacent RR intervals > 50 msec different; square root of mean square successive differences in RR intervals) and frequency-domain variables (low frequency power, high frequency power and total spectrum power). Sinus node recovery time, sinoatrial conduction time and post-pacing cycle lengths were examined at different rates of endocardial atrial pacing. After the first year subsequent to transplantation, standard deviation of the mean RR intervals reached the normal range in four patients, whereas the other time-domain variables became normal in two patients. Both patients displayed normal or near-normal power spectrums of heart rate with normal day-to-night variations. For the remaining patients, spectrums of heart rate failed to show the main frequency peaks. Only the patient with normal variability in heart rate exhibited a decrease in corrected sinus node recovery time at higher stimulation rates, shortening of the first recovery cycle below the pre-pacing level, and a rapid decline of the accelerated post-pacing heart rate as described in innervated hearts. These results suggest the evolution of time-dependent efferent autonomic reinnervation after cardiac transplantation in children.

Keywords

Heart transplantationheart rate variabilityautonomic nervous system
Type
Original Manuscripts
Information
Cardiology in the Young , Volume 6 , Issue 1 , January 1996 , pp. 12 - 19
Copyright
Copyright © Cambridge University Press 1996

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References

1. Kontos, HA, Thames, MD, Lower, RR. Responses to electrical and reflex autonomic stimulation in dogs with cardiac transplantation before and after reinnervation. J Thorac Cardiovasc Surg 1970; 59: 382–392.Google Scholar
2. Kaye, MP, Randall, WC, Hageman, GR, Geis, WP, Priola, DV. Chronology and mode of reinnervation of the surgically denervated canine heart: functional and chemical correlates. Am J Physiol 1977; 233: H431–H437.Google ScholarPubMed
3. Pope, SE, Stinson, EB, Daughters, GT, Schroeder, JS, Ingels, NB, Alderman, EL. Exercise response of the denervated heart in long-term cardiac transplant recipients. Am J Cardiol 1980; 46: 213–218.Google Scholar
4. Savin, WM, Haskell, WL, Schroeder, JS, Stinson, EB. Cardiorespiratory responses of cardiac transplant patients to graded, symptom-limited exercise. Circulation 1980; 26: 55–60.Google Scholar
5. Fallen, EL, Kamath, MV, Ghista, DN, Fitchett, D. Spectral analysis of heart rate variability following human heart transplantation: evidence of functional reinnervation. J Auton Nerv Syst 1988; 23: 199–206.Google Scholar
6. Wilson, RF, Christensen, BV, Olivari, MT, Simon, A, White, CW, Laxson, DD. Evidence of structural sympathetic reinnervation after orthotopic cardiac transplantation in humans. Circulation 1991; 83: 1210–1220.CrossRefGoogle ScholarPubMed
7. Schwaiger, M, Hutchins, GD, Kalff, V, Rosenspire, K, Haka, MS, Mallette, S, Deeb, GM, Abrams, GD, Wieland, D. Evidence for regional catecholamine uptake and storage sites in the transplanted human heart by positron emission tomography. J Clin Invest 1991; 87: 1681–1690.CrossRefGoogle ScholarPubMed
8. Fitzpatrick, AP, Banner, N, Cheng, A, Yacoub, M, Sutton, R. Vasovagal reactions may occur after orthotopic heart transplantation. J Am Coll Cardiol 1993; 21: 1132–1137.CrossRefGoogle ScholarPubMed
9. Akselrod, S, Gordon, D, Madwed, JB, Snidman, NC, Shannon, DC, Cohen, RJ. Hemodynamic regulation: investigation by spectral analysis. Am J Physiol 1985; 249: H867–H875.Google Scholar
10. Appel, ML, Berger, RD, Saul, P, Smith, JM, Cohen, RJ. Beat to beat variability in cardiovascular variables: noise or music? J Am Coll Cardiol 1989; 14: 1139–1148.Google Scholar
11. Stein, PK, Bosner, MS, Kleiger, RE, Conger, BM. Heart rate variability: a measure of cardiac autonomic tone. Am Heart J 1994; 127: 1376–1381.CrossRefGoogle ScholarPubMed
12. Malliani, A, Pagani, M, Lombardi, F, Cerutti, S. Cardiovascular neural regulation explored in the frequency domain. Circulation 1991; 84: 482–492.Google Scholar
13. Malik, M, Camm, AJ. Heart rate variability and clinical cardiology. Br Heart J 1994; 71: 3–6.CrossRefGoogle ScholarPubMed
14. Mason, JW. Overdrive suppression in the transplanted heart: effect of the autonomic nervous system on human sinus node recovery. Circulation 1980; 62: 688–696.Google Scholar
15. Bexton, RS, Nathan, AW, Hellestrand, KJ, Cory-Pearce, R, Spurrell, RAJ, English, TAH, Camm, AJ. Sinoatrial function after cardiac transplantation. J Am Coll Cardiol 1984; 3: 712–723.Google Scholar
16. Nalos, PC, Deng, Z, Rosenthal, ME, Gang, ES, Oseran, DS, Mandel, WJ, Peter, T. Hemodynamic influences on sinus node recovery time: effects of autonomic blockade. J Am Coll Cardiol 1986; 7: 1079–1086.CrossRefGoogle ScholarPubMed
17. Kugler, JD. Sinus node dysfunction. In: Gillette, PC, Garson, A (eds). Pediatric Arrhythmias, Electrophysiology & Pacing. W.B. Saunders, Philadelphia, 1990, pp 250–300.Google Scholar
18. Malik, M, Farrell, T, Cripps, T, Camm, AJ. Heart rate variability in relation to prognosis after myocardial infarction: Selection of optimal processing techniques. Eur Heart J 1989; 10: 1060–1074.Google Scholar
19. Van Hoogenhuyze, D, Weinstein, N, Martin, GJ, Weiss, JS, Schaad, JW, Sahyouni, N, Fintel, D, Remme, WJ, Singer, DH. Reproducibility and relation to mean heart rate of heart rate variability in normal subjects and in patients with congestive heart failure secondary to coronary heart disease. Am J Cardiol 1991; 68: 1668–1676.Google Scholar
20. Martin, GJ, Magid, NM, Myers, G, Barnett, PS, Schaad, JW, Weiss, JS, Lesch, M, Singer, DH. Heart rate variability and sudden death secondary to coronary artery disease during ambulatory electrocardiographic monitoring. Am J Cardiol 1987; 60: 86–89.Google Scholar
21. Bigger, JT, Kleiger, RE, Fleiss, JL, Rolnitzky, LM, Steinman, RC, Miller, JP. Components of heart rate variability measured during healing of acute myocardial infarction. Am J Cardiol 1988; 61: 208–215.CrossRefGoogle ScholarPubMed
22. Bigger, JT, Albrecht, P, Steinman, RC, Rolnitzky, L, Fleiss, JL, Cohen, RJ. Comparison of time- and frequency domain-based measures of cardiac parasympathetic activity in Holter recordings after myocardial infarction. Am J Cardiol 1989; 64: 536–538.Google Scholar
23. Ewing, DJ, Neilson, JMM, Shapiro, CM, Stewart, JA, Reid, W. Twenty-four hour heart rate variability: effects of posture, sleep, and time of day in healthy controls and comparison with bedside tests of autonomic function in diabetic patients. Br Heart J 1991; 65: 239–244.CrossRefGoogle Scholar
24. Hayano, J, Sakakibara, Y, Yamada, A, Yamada, M, Mukai, S, Fujinami, T, Yokoyama, K, Watanabe, Y, Takata, K. Accuracy of assessment of cardiac vagal tone by heart rate variability in normal subjects. Am J Cardiol 1991; 67: 199–204.Google Scholar
25. Rottman, JN, Steinman, RC, Albrecht, P, Bigger, JT, Rolnitzky, LM, Fleiss, JL. Efficient estimation of the heart period power spectrum suitable for physiologic or pharmacologic studies. Am J Cardiol 1990; 66: 1522–1524.Google Scholar
26. Koizumi, K, Terui, N, Kollai, M. Effect of cardiac vagal and sympathetic nerve activity on heart rate in rhythmic regulations. J Auton Nerv Syst 1985; 12: 251–259.Google Scholar
27. Fouad, FM, Tarazzi, RC, Ferrario, CM, Fighaly, S, Alicandri, C. Assessment of parasympathetic control of heart rate by a non-invasive method. Am J Physiol 1984; 246: H838–H842.Google Scholar
28. Molgaard, H, Sorensen, KE, Bjerregaard, P. Circadian variation and influence of risk factors on heart rate variability in healthy subjects. Am J Cardiol 1991; 68: 777–784.Google Scholar
29. Bigger, JT, Hoover, CA, Steinman, RC, Rolnitzky, LM, Fleiss, JL. Autonomic nervous system activity during myocardial ischemia in man estimated by power spectral analysis of heart period variability. Am J Cardiol 1990; 66: 497–498.CrossRefGoogle ScholarPubMed
30. Korkushko, OV, Shatilo, VB, Plachida, YI, Shatilo, TV. Autonomic control of cardiac chronotropic function in man as a function of age: assessment by power spectral analysis of heart rate variability. J Auton Nerv Syst 1991; 32: 191–198.Google Scholar
31. Strauss, HC, Saroff, AL, Bigger, JT, Giardina, EGV. Premature atrial stimulation as a key to the understanding of sinoatrial conduction in man. Circulation 1973; 47: 86–93.CrossRefGoogle Scholar
32. Narula, OS, Shanth, N, Vasquez, M, Towne, WD, Linhart, JW. A new method for measurement of sinoatrial conduction time. Circulation 1978; 58: 706–714.Google Scholar
33. Rudas, L, Pflugfelder, PW, Menkis, AH, Novick, RJ, McKenzie, FN, Kostuk, WJ. Evolution of heart rate responsiveness after orthotopic cardiac transplantation. Am J Cardiol 1991; 68: 232–236.Google Scholar
34. Pickering, TG, Gribbin, B, Sleight, P. Comparison of the reflex heart rate response to rising and falling arterial pressure in man. Cardiovasc Res 1972; 6: 277–283.Google Scholar
35. Saul, JP, Berger, RD, Chen, MH, Cohen, RJ. Transfer function analysis of autonomic regulation. II. Respiratory sinus arrhythmia. Am J Physiol 1989; 256: H153–H161.Google ScholarPubMed
36. Zbilut, JP, Murdock, DK, Lawson, L, Lawless, CE, Von Dreele, MM, Porges, SW. Use of spectral analysis of respiratory sinus arrhythmia to detect graft rejection. J Heart Transplant 1988; 7: 280–288.Google ScholarPubMed
37. Sands, KEF, Appel, ML, Lilly, LS, Schoen, FJ, Mudge, GH, Cohen, RJ. Power spectrum analysis of heart rate variability in human cardiac transplant recipients. Circulation 1989; 79: 76–82.Google Scholar
38. Bernardi, L, Keller, F, Sanders, M, Reddy, PS, Griffith, B, Meno, F, Pinsky, MR. Respiratory sinus arrhythmia in the denervated human heart. J Appl Physiol 1989; 67: 1447–1455.Google Scholar
39. Folino, AF, Buja, G, Miorelli, M, Livi, U, Nava, A, Thiene, G, Volta, SD. Heart rate variability in patients with orthotopic heart transplantation: long-term follow-up. Clin Cardiol 1993; 16: 539–542.Google Scholar
40. Myers, GA, Martin, NM, Magid, NM, Barnett, PS, Schaad, JW, Weiss, JS, Lesch, M, Singer, DH. Power spectral analysis of heart rate variability in sudden cardiac death: comparison to other methods. IEEE Trans Biomed Eng 1986; 33: 1149–1156.CrossRefGoogle ScholarPubMed
41. Anselme, F, Saoudi, N, Redonnet, M, Letac, B. Atrioatrial conduction after orthotopic heart transplantation. J Am Coll Cardiol 1994; 24: 185–189.CrossRefGoogle ScholarPubMed
42. Grossman, P, Wientjes, K. Respiratory sinus arrhythmia and parasympathetic cardiac control: some basic issues concerning quantification, applications and implications. In: Grossman, P, Janssen, KHL, Vaitl, D (eds). Cardiorespiratory and Cardiosomatic Psychophysiology. Plenum Press, New York, 1986, pp 117–138.CrossRefGoogle Scholar
43. Kleiger, RE, Bigger, JT, Boner, MS, Chung, MK, Cook, JR, Rolnitzky, LM, Steinman, R, Fleiss, JL. Stability over time of variables measuring heart rate variability in normal subjects. Am J Cardiol 1991; 68: 626–630.Google Scholar
44. Ahmed, MW, Suleiman, M, Zhang, F, Weiss, JW, Van Hoogenhuyze, D, Parker, M, Singer, DH, Rosenthal, JE. Heart rate variability: is it really reproducible? J Am Coll Cardiol 1993;21: 286A.Google Scholar