Effect of dietary omega-3 polyunsaturated fatty acids on heart rate and heart rate variability in animals susceptible or resistant to ventricular fibrillation

Frontiers in Physiology

Volumn 3 MAR, Issue , 2012, Pages

  Billman, George E ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Docosahexaenoic acid; Eicosapentaenoic acid; Exercise; Fish oil; Myocardial ischemia; Parasympathetic nervous system

Indexed keywords

EID: 84865152195     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00071     Document Type: Article

References (62)

1. Albert, C. M., Campos, H., Stamfer, M. J., Ridker, P. M., Mason, J. E., Willet, W. C., and Ma, J. (2002). Blood levels of long-chin n-3 fatty acids and the risk of sudden death. N. Engl. J. Med. 346, 1113-1118.
2. Berntson, G. G., Bigger, J. T., Eckberg, D. L., Grossman, P., Kaufmann, P. G., Malik, M., Nagaraja, H. K., Proges, S. W., Saul, J. P., Stone, P. H., and van der Molen, M. W. (1997). Heart rate variability: origins, methods, and interpretive caveats. Pyschophysiology 34, 623-648.
3. Billman, G. E. (2006). A comprehensive review and analysis of 25 years of data from an in vivo canine model of sudden cardiac death: implications for future anti-arrhythmic drug development. Pharmacol. Ther. 111, 808-835.
4. Billman, G. E. (2009). Cardiac autonomic neural "remodeling" and susceptibility to sudden cardiac death: effect of endurance exercise training. Am. J. Physiol. Heart Circ. Physiol. 297, H1171-H1193.
5. Billman, G. E. (2011). Heart variability - a historical perspective. Front. Physiol. 2:86. doi:10.3389/fphys.2011.00086
6. Billman, G. E., and Dujardin, J.-P. (1990). Dynamic changes in cardiac vagal tone as measured by time-series analysis. Am. J. Physiol. Heart Circ. Physiol. 258, H896-H902.
7. Billman, G. E., Hallaq, H., and Leaf, A. (1994). Prevention of ischemia-induced ventricular fibrillation by omega-3 fatty acids. Proc. Natl. Acad. Sci. U.S.A. 91, 4427-4430.
8. Billman, G. E., and Harris, W. S. (2011). Effect of dietary omega-3 fatty acids on heart rate and the heart rate variability responses to myocardial ischemia or exercise. Am. J. Phys-iol. Heart Circ. Physiol. 300, H2288- H2299.
9. Billman, G. E., Harris, W. S., Carnes, C. A., Adamson, P. B., Vanoli, E., and Schwartz, P. J. (2012). Dietary omega-3 fatty acids and susceptibility to ventirualr fibrillation: lack of protection and a proarrythmic effect. Circ. Arrhythm. Electrophysiol. doi:10.1161/CIRCEP.111.966739 (in press).
10. Billman, G. E., and Hoskins, R. S. (1989). Time-series analysis of heart rate variability during submaximal exercise. Evidence for reduced cardiac vagal tone in animals susceptible to ventricular fibrillation. Circulation 80, 146-157.
11. Billman, G. E., and Kukielka, M. (2006). Effects of endurance exercise training on heart rate variability and susceptibility to sudden cardiac death: protection is not due to enhanced cardiac vagal regulation. J. Appl. Physiol. 100, 896-906.
12. Billman, G. E., and Kukielka, M. (2007). Effect of endurance exercise training on the heart rate onset and heart rate recovery responses to submaximal exercise in animals susceptible to ventricular fibrillation. J. Appl. Physiol. 102, 231-240.
13. Billman, G. E., Nishijima, Y., Belevych, A. E., Terentyev, D., Xu,Y., Haizlip, K. M., Monasky, M. M., Hiranandani, N., Harris, W. S., Gyorke, S., Carnes, C. A., and Janssen, P. M. L. (2010). Effects of dietary omega-3 fatty acids on ventricular function in dogs with healed myocardial infarctions. Am. J. Physiol. Heart Circ. Physiol. 298, H1219-H1228.
14. Billman, G. E., Schwartz, P. J., Gagnol, J. P., and Stone, H. L. (1985). The cardiac response to submaximal exercise in dogs susceptible to sudden cardiac death. J. Appl. Physiol. 59, 890-897.
15. Billman, G. E., Schwartz, P. J., and Stone, H. L. (1982). Baroreceptor reflex control of heart rate: a predictor of sudden death. Circulation 66, 874-880.
16. Bligh, E. G., and Dyer, W. J. (1959). A rapid method for total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917.
17. Buckley, J. D., Burgess, S., Murphy, K. J., and Howe, P.R.C. (2009). DHA-rich fish oil lowers heart rate during submaximal exercise in elite Australian Rules footballers. J. Sci. Med. Sport. 12, 503-507.
18. Carney, R. M., Freedland, K. E., Stein, P. K., Steinmeyer, B. C., Harris, W. S., Rubin, E. H., Krone, R. J., and Rich, W. W. (2010). Effect of omega-3 fatty acids on heart rate variability in depressed patients with coronary heart disease. Psychosom. Med. 72, 748-754.
19. Casadei, B., Pipillis, A., Sessa, F., Conway, J., and Sleight, P. (1993). Low doses of scopolamine increase cardiac vagal tone in the acute phase of myocardial infarction. Circulation 88, 353-357.
20. Christensen, J. H. (2011). Omega-3 fatty acids and heart rate variability. Front. Physiol. 2:84. doi:10.3389/fphys.2011.00084
21. Christensen, J. H., Christensen, M. S., Dyerberg, J., and Schmidt, E. B. (1999). Heart rate variability and fatty acid content in blood cell membranes: a dose-response study with n-3 fatty acids. Am. J. Clin. Nutr. 70, 331-337.
22. Christensen, J. H., and Schmidt, E. B. (2007). Autonomic nervous system, heart rate variability and n-3 fatty acids. J. Cardiovasc. Med. 8(Suppl. 1), S19-S22.
23. Collins, M. N., and Billman, G. E. (1989). Autonomic response to coronary occlusion in animals susceptible to ventricular fibrillation. Am. J. Physiol. Heart Circ. Physiol. 257, H1886-H1894.
24. De Ferrari, G. M., Mantica, M., Vanoli, E., Hull, S. S. Jr., and Schwartz, P. J. (1993). Scopolamine increases vagal tone and vagal reflexes in patients after myocardial infarction. J. Am. Coll. Cardiol. 22, 1327-1334.
25. den Ruijter, H. M., Berecki, G., Verkerk, A. O., Bakker, D., Baartscheer, A., Schumacher, C. A., Belterman, C. N., de Jonge, N., Fiolet, J. W., Brower, I. A., and Coronel, R. (2008). Acute administration of fish oil inhibits triggered activity in isolated myocytes from rabbits and patients with heart failure. Circulation 117, 536-544.
26. den Ruijter, H. M., Verkerk, A. O., and Coronel, R. (2010). Incorporated fish oil fatty acids prevent action potential shortening induced by circulating fish oil fatty acids. Front. Physiol. 1:149. doi:10.3389/fphys.2010.00149
27. Di Stasi, D., Bernasconi, R., Marchioli, R., Marfisi, R. M., Rossi, G., Tognoni, G., and Tacconi, M. T. (2004). Early modifications of fatty acid composition in plasma phospholipids, platelets and mononucleates of healthy volunteers after low doses of n-3 polyunsaturated fatty acids. Eur. J. Clin. Pharmacol. 60, 183-190.
28. Geelen, A., Zock, P. L., Swenne, C. A., Brouwer, I. A., Schouten, E. G., and Katan, M. B. (2003). Effect of n-3 fatty acids on heart rate variability and baroreflex sensitivity in middle-aged subjects. Am. Heart J. 146, E4.
29. Halliwill, J. R., Billman, G. E., and Eckberg, D. L. (1998). Effect of a vagomimetic atropine dose on canine cardiac vagal tone and susceptibility to sudden cardiac death. Clin. Auton. Res. 8, 155-164.
30. Hamaad, A., Lee, W. K., Lip, G. Y. H., and MacFadyen, R. J. (2006). Oral omega-3 PUFA therapy (Omacor) has no impact on indices of heart rate variability in stable post myocardial infarction patients. Cardiovasc. Drugs Ther. 20, 359-364.
31. Harris, W. S., Gonzles, M., Laney, N., Sastre, A., and Borkon, A. M. (2006). Effects of omega-3 fatty acids on heart rate in cardiac transplant recipients. Am. J. Cardiol. 98, 1393-1395.
32. Harris, W. S., Sands, S. A., Windsor, S. L., Ali, H. A., Stevens, T. L., Magalski, A., Porter, C. B., and Borkon,A. M. (2004). Omega-3 fatty acids in cardiac biopsies from heart transplantation patients: correlation with erythrocytes and response to supplementation. Circulation 110, 1645-1649.
33. + channel blockers in acute myocardial infarction. Eur. Heart J. 14 (Suppl. F), 18-25.
34. 2-adreneric receptor stimulation in dogs susceptible to lethal arrhythmias. J. Appl. Physiol. 91, 1627-1637.
35. Houle, M. S., and Billman, G. E. (1999). Low-frequency component of the heart rate variability spectrum: a poor marker of sympathetic activity.Am. J. Physiol. Heart Circ. Physiol. 276, H215-H223.
36. Hull, S. S. Jr., Vanoli, E., Adamson, P. B., De Ferrari, G. M., Foreman, R. D., and Schwartz, P. J. (1995). Do increases in markers of vagal activity imply protection from sudden death? The case of scopolamine. Circulation 91, 2516-2519.
37. Jouven, X., Empana, J. P., Escolano, S., Buyck, J. F., Tafflet, M., Desnos, M., and Ducimetiere, P. (2009). Relation of heart rate at rest and long-term (>20 years) death rate in initially healthy middle-aged men. Am. J. Cardiol. 103, 279-283.
38. Kang, J. X., and Leaf, A. (1994). Effects of long-chain polyunsaturated fatty acids on the contraction of neonatal rat cardiac myocytes. Proc. Natl. Acad. Sci. U.S.A. 91, 9886-9890.
39. Kottmeier, C. A., and Gravenstein, J. S. (1968). The parasympathomimetic activity of atropine and atropine methylbromide. Anesthesiology 29, 1125-1133.
40. Laustiola, K., Salo, M. K., and Metsä-Ketelä, T. (1986). Altered physiological responses and decreased cyclic AMP levels in rat atria after dietary cod liver oil supplementation and its possible association with n3/n6 fatty acid ratio. Biochim. Biophys. Acta 889, 59-79.
41. Marchioli, R., Barzi, F., Bomba, E., Chieffo, C., Di Gregorio, D., Di Mascio, R., Franzosi, M. G., Geraci, E., Levantesi, G., Maggioni, A. P., Mantini, L., Marfisi, R. M., Mastrogiuseppi, G., Mininni, N., Nicolisi, G. L., Santini, M., Schweiger, C., Tavazzi, L., Tognoni, G., Tucci, C., and Valagussa, F. (2002). Early protection against sudden death by n-3 polyunsaturated fatty acids after myocardial infarction: time-course analysis of the results of the Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto Miocardico (GISSI)-Prevenzione. Circulation 105, 1897-1903.
42. Mayyas, F., Sakurai, S., Ram, R., Rennison, J. H., Hwang, E.-S., Castel, L., Lovano, B., Brennan, M.-L., Bibus, D., Lands, B., Barnard, J., Chung, M. K., and Van Wagoner, D. R. (2011). Dietary ω3 fatty acids modulate the substrate for post-operative atrial fibrillation in a canine cardiac surgery model. Cardiovasc. Res. 89, 852-861.
43. Morrison, W. R., and Smith, L. M. (1964). Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoride-methanol. J. Lipid Res. 5, 600-608.
44. Mozaffarian, D., Geelen, A., Brouwer, I. A., Geleijnse, J. M., Zock, P. L., and Katan, M. B. (2005). Effect of fish oil on heart rate in humans: meta-analysis of randomized controlled trials. Circulation 112, 1945-1952.
45. Mozaffarian, D., Prineas, R. J., Stein, P. K., and Siscovick, D. S. (2006). Dietary fish and n-3 fatty acid intake and cardiac electrocardiographic parameters in humans. J. Am. Coll. Cardiol. 48, 478-484.
46. Mozaffarian, D., Stein, P. K., Prineas, R. J., and Siscovick, D. S. (2008). Dietary Fish ω-3 fatty acid consumption and heart rate variability in US adults. Circulation 117, 1130-1137.
47. Ninio, D. M., Hill, A. M., Howe, P. R., Buckley, J. D., and Saint, D. A. (2008). Docosahexaenoic acid-rich fish oil improves heart variability and heart rate responses to exercise in overweight adults. Br. J. Nutr. 100, 1097-1103.
48. O'Keefe, J. H. Jr., Abuissa, H., Sastre, A., Steinhaus, D. M., and Harris, W. S. (2006). Effects of omega-3 fatty acids on resting heart rate, heart rate recovery after exercise, and heart rate variability in men with healed myocardial infarctions and depressed ejection fraction. Am. J. Cardiol. 97, 1127-1130.
49. Opthof, T., Coronel, R., Wilms-Schopman, F. J. G., Plotnikov, A. N, Shlapakova, I. N., Danilo, P. Jr., Rosen, M. R., and Janse, M. J. (2007). Dispersion of repolarization in canine ventricle and electrocardiographic T wav: Tp-e interval does not reflect transmural dispersion. Heart Rhythm 4, 341-348.
50. Parati, G., di Rienzo, M., Castiglioni, P., Mancia, G., Taylor, J. A., and Studinger, P. (2006). Point: counterpoint: cardiovascular variability is/is not an index of autonomic control of circulation. J. Appl. Physiol. 101, 676-682.
51. Peoples, G. E., McLennan, P. L., Howe, P. R. C., and Groeller, H. (2008). Fish oil reduces heart rate and oxygen consumption during exercise. J. Cardiovasc. Pharmacol. 52, 540-547.
52. Porges, S. W. (1986). "Respiratory sinus arrhythmia: physiological basis, quantitative methods and clinical implications," in Cardiac, Respiratory, and Cardiosomatic Psychophysiology, eds P. Grossman, K. H. L. Janssen, and D. Vaitl (New York: Plenum), 101-115.
53. Russo, C., Olivieri, O., Girelli, D., Azzini, M., Stanzial, A. M., Guarini, P., Friso, S., De Franceschi, L., and Corrocher, R. (1995). Omega-3 polyunsaturated fatty acid supplements and ambulatory blood pressure monitoring parameters in patients with mild hypertension. J. Hypertens. 13, 1823-1826.
54. Scher, A. M., Ohm, W. W., Bumgarner, K., Boynton, R., and Young, A. C. (1972). Sympathetic and parasympathetic control of heart rate in the dog, baboon and man. Fed. Proc. 31, 1219-1225.
55. Schwartz, P. J., Billman, G. E., and Stone, H. L. (1984). Autonomic mechanisms in ventricular fibrillation due to acute myocardial ischemia during exercise in dogs with healed myocardial infarction: an experimental model for sudden cardiac death. Circulation 69, 790-800.
56. Siscovick, D. S., Raghunathan, T. E., King, I., Weinmann, S., Wicklund, K. G., Albright, J., Bouberg, V., Arbogast, P., Smith, H., Kushi, L. H., Cobb, L. A., Copass, M. K., Psaty, B., Lemaitre, R., Retzlaff, B., Childs, M., and Knopp, R. H. (1995). Dietary intake and cell membrane levels of long-chain n-3 polyunsaturated fatty acids and the risk of primary cardiac arrest. JAMA 274, 1363-1367.
57. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. (1996). Heart rate variability: standards of measurement,physiological interpretation, and clinical use. Circulation 93, 1043-1065.
58. Van de Water, A., Verheyen, J., Xhonnex, R., and Reneman, R. S. (1989). An improved method to correct QT interval of the electrocardiogram fro changes in heart rate. J. Pharmacol. Methods 22, 207-217.
59. Verkerk, A. O., den Ruijter, H. M., Bourier, J., Boukens, B. J., Brouwer, I. A., Wilders, R., and Coronel, R. (2009). Dietary fish oil reduces pacemaker current and heart rate in rabbit. Heart Rhythm 6, 1485-1492.
60. Verkerk, A. O., van Ginneken, A. C., Berecki, G., den Ruijter, H. M., Schumacher, C. A., Veldkamp, M. W., Casini, S., Opthof, T., Hovenier, R., Fiolet, J. W., Zock, P. L., and Coronel, R. (2006). Incorporated sarcolemmal fish oil fatty acids shorten pig ventricular action potentials. Cardiovasc. Res. 70, 509-520.
61. Von Schacky, C. (2006). A review of omega-3 ethyl esters for the cardiovascular prevention and treatment of increased blood triglyceride levels. Vasc. Health Risk Manag.2,251-262.
62. Yan, G. X., and Antzelevitch, C. (1998). Cellular basis for the normal T wave and the electrocardiographic manifestations of the long-QT syndrome. Circulation 98, 1928-1936.