Ventricular fibrillation: are swine a sensitive species?

  • Gregory P. Walcott
  • Mark W. Kroll
  • Raymond E. Ideker
Article

Abstract

Purpose

Legislation and sentiment have pushed large-animal electrophysiological research from the canine to the swine model. Anecdotal experience suggests that the swine is particularly sensitive to ventricular fibrillation (VF) induction, and radiofrequency ablation studies are consistent with this. Currently, no data exist directly comparing the VF threshold (VFT) in humans to swine. Because of the perceived difference in vulnerability to VF induction, we hypothesized that the VFT would be lower in swine compared to humans.

Methods

Six anesthetized open-chested swine, 31 ± 2 kg, were studied that were part of an ongoing study with up to 6 h of previous closed-chest percutaneous pacing with repeated VF cycles. Similar to the human study of Horowitz et al., 24 pulses of 4 ms each were applied at a rate of 100 Hz during the ST segment to the epicardium via a pair of 7-mm diameter platinum electrodes whose centers were 15 mm apart. Current was increased until VF was induced.

Results

The swine right ventricle (RV) VFT was 9.7 ± 2.1 mA [median = 9.0, interquartile range (IQR) = 7.8–12.0], and the left ventricle (LV) VFT was 10.7 ± 2.2 mA [median = 10.5, IQR = 8.8–12.5] (p = NS). Horowitz reported the RV VFT in six patients as 24.3 ± 5.2 mA [median = 24.5, IQR = 19.0–29.3] and the LV VFT in ten patients as 33.6 ± 9.5 mA [median = 36.5, IQR = 27.3–42.3] (p = .11). Both the RV and LV VFTs were lower for swine (p < 0.003), and each of the mean and median VFTs for the ventricles together was one third that of the humans.

Conclusions

Swine are about three times as sensitive to the electrical induction of VF as are humans.

Keywords

Purkinje Ablation Swine Animal model Ventricular fibrillation Threshold 

Abbreviations

DFT

Defibrillation threshold

ECG

Electrocardiograph

IQR

Interquartile range

LV

Left ventricle

RV

Right ventricle

UAB

University of Alabama

USDA

US Department of Agriculture

VF

Ventricular fibrillation

VFT

Ventricular fibrillation threshold

Notes

Conflict of interest

Authors have full control of all primary data and agree to allow the journal to review their data if requested. This work was funded by a grant from TASER International, Inc., and Dr. Kroll is a member of their corporate and scientific advisory board and holds their equity. Drs. Walcott and Ideker report no conflicts.

References

  1. 1.
    (1991) Final rules: animal welfare; 9 CFR Part 3, USDA 0579-AA20.Google Scholar
  2. 2.
    European Commission (1986) Directive 86/609/EEC on the protection of animals used for experimental and other scientific purposes.Google Scholar
  3. 3.
    Pak, H. N., Kim, Y. H., Lim, H. E., Chou, C. C., Miyauchi, Y., Fang, Y. H., et al. (2006). Role of the posterior papillary muscle and Purkinje potentials in the mechanism of ventricular fibrillation in open chest dogs and Swine: effects of catheter ablation. Journal of Cardiovascular Electrophysiology, 17, 777–783.CrossRefPubMedGoogle Scholar
  4. 4.
    Van Herendael, H., Zado, E. S., Haqqani, H., Tschabrunn, C. M., Callans, D. J., Frankel, D. S., et al. (2014). Catheter ablation of ventricular fibrillation: importance of left ventricular outflow tract and papillary muscle triggers. Heart Rhythm, 11, 566–573.CrossRefPubMedGoogle Scholar
  5. 5.
    Nishida, K., Michael, G., Dobrev, D., & Nattel, S. (2010). Animal models for atrial fibrillation: clinical insights and scientific opportunities. Europace, 12, 160–172.CrossRefPubMedGoogle Scholar
  6. 6.
    Holland, R. P., & Brooks, H. (1976). The QRS complex during myocardial ischemia. An experimental analysis in the porcine heart. Journal of Clinical Investigation, 57, 541–550.CrossRefPubMedCentralPubMedGoogle Scholar
  7. 7.
    Janse, M. J. (1998). Vulnerability to ventricular fibrillation. Chaos, 8, 149–156.CrossRefPubMedGoogle Scholar
  8. 8.
    Gaum, W. E., Elharrar, V., Walker, P. D., & Zipes, D. P. (1977). Influence of excitability on the ventricular fibrillation threshold in dogs. American Journal of Cardiology, 40, 929–935.CrossRefPubMedGoogle Scholar
  9. 9.
    Nimunkar, A. J., & Webster, J. G. (2009). Safety of pulsed electric devices. Physiological Measurement, 30, 101.CrossRefPubMedGoogle Scholar
  10. 10.
    Cunningham, B. (2011). Draft guidance for industry and FDA staff: class II special controls guidance document: transcutaneous electrical nerve stimulator with limited output for pain relief. http://www.fda.gov/MedicalDevices/DeviceRegulationandGuidance/GuidanceDocuments/ucm198585.htm
  11. 11.
    (2006) Household and similar electrical appliances—safety—IEC 60335-2-76: particular requirements for electric fence energizers.Google Scholar
  12. 12.
    (2005) Effects of current on human beings and livestock, IEC/TS60479-1: effects of currents passing through the human body.Google Scholar
  13. 13.
    Walcott, G. P., Kroll, M. W., & Ideker, R. E. (2011). Ventricular fibrillation threshold of rapid short pulses. Conference of the IEEE Engineering in Medicine and Biology Society, 33, 255–258.Google Scholar
  14. 14.
    Ferris, L. P., King, B. G., Spence, P. W., & Williams, H. B. (1936). Effect of electric shock on the heart. Electrical Engineering, 55, 498–515.CrossRefGoogle Scholar
  15. 15.
    Jacobsen, J., Buntenkotter, S., & Reinhard, H. J. (1975). Experimental studies in pigs on mortality due to sinusoidal and phase-controlled alternating and rectified currents (author’s transl). Biomedizinische Technik (Berl), 20, 99–107.CrossRefGoogle Scholar
  16. 16.
    Chilbert, M. (1998). High-voltage and high current injuries. In J. Reilly (Ed.), Applied bioelectricity: from electrical stimulation to electrical pathology (pp. 412–453). New York: Springer.CrossRefGoogle Scholar
  17. 17.
    Richardson, E. (2009) Intrapericardial delivery of anti-arrhythmic agents, PhD Thesis, University of Minnesota.Google Scholar
  18. 18.
    Stratbucker, R. A., Kroll, M. W., McDaniel, W., & Panescu, D. (2006). Cardiac current density distribution by electrical pulses from TASER devices. Conference of the IEEE Engineering in Medicine and Biology Society, 28, 6305–6307.Google Scholar
  19. 19.
    Wolf, P. D., Tang, A. S., Ideker, R. E., & Pilkington, T. C. (1992). Calculating endocardial potentials from epicardial potentials measured during external stimulation. IEEE Transactions on Biomedical Engineering, 39, 913–920.CrossRefPubMedGoogle Scholar
  20. 20.
    Swerdlow, C. D., Olson, W. H., O’Connor, M. E., Gallik, D. M., Malkin, R. A., & Laks, M. (1999). Cardiovascular collapse caused by electrocardiographically silent 60-Hz intracardiac leakage current. Implications for electrical safety. Circulation, 99, 2559–2564.CrossRefPubMedGoogle Scholar
  21. 21.
    Horowitz, L. N., Spear, J. F., Josephson, M. E., Kastor, J. A., & Moore, E. N. (1979). The effects of coronary artery disease on the ventricular fibrillation threshold in man. Circulation, 60, 792–797.CrossRefPubMedGoogle Scholar
  22. 22.
    (1985) Position of the American Heart Association on research animal use, Circulation, 71(4), 849A–50A.Google Scholar
  23. 23.
    Darragh, K. M., Manoharan, G., Navarro, C., Walsh, S. J., Allen, J. D., Anderson, J. M., et al. (2012). Synchronized defibrillation for ventricular fibrillation. European Heart Journal Acute Cardiovascular Care, 1, 285–290.CrossRefPubMedCentralPubMedGoogle Scholar
  24. 24.
    Huang, J., Walcott, G. P., Ruse, R. B., Bohanan, S. J., Killingsworth, C. R., & Ideker, R. E. (2012). Ascending-ramp biphasic waveform has a lower defibrillation threshold and releases less troponin I than a truncated exponential biphasic waveform. Circulation, 126, 1328–1333.CrossRefPubMedCentralPubMedGoogle Scholar
  25. 25.
    Rollins, D. L., Wolf, P. D., Ideker, R. E., & Smith, W. M. (1990). A Macintosh based programmable cardiac stimulator. Journal of the American College of Cardiology, 15, A261.CrossRefGoogle Scholar
  26. 26.
    Antoni, H. (1979). What is measured by the so-called threshold for fibrillation. Progress in Pharmacology, 2/4, 5–12.Google Scholar
  27. 27.
    Cha, Y.-M., Peters, B. B., Birgersdotter-Green, U., & Chen, P.-S. (1993). A reappraisal of ventricular fibrillation threshold testing. American Journal of Physiology, 264, H1005–H1010.PubMedGoogle Scholar
  28. 28.
    Dixon, M. E., Trank, J. W., & Dobell, R. C. (1964). Ventricular fibrillation threshold: variation with coronary flow and its value in assessing experimental myocardial revascularization. Journal of Thoracic and Cardiovascular Surgery, 47, 620–627.PubMedGoogle Scholar
  29. 29.
    Green, H. L., Raftery, E. B., & Gregory, I. C. (1972). Ventricular fibrillation threshold of healthy dogs to 50 Hz current in relation of earth leakage currents of electromedical equipment. Biomedical Engineering, 7, 408–414.PubMedGoogle Scholar
  30. 30.
    Swerdlow, C. D., Shehata, M., & Chen, P. S. (2007). Using the upper limit of vulnerability to assess defibrillation efficacy at implantation of ICDs. Pacing and Clinical Electrophysiology, 30, 258–270.CrossRefPubMedGoogle Scholar
  31. 31.
    Dalziel, C. F., & Lee, W. R. (1968). Reevaluation of lethal electric currents. IEEE Transactions on Industry and General Applications, IGA-4, 467–476.CrossRefGoogle Scholar
  32. 32.
    Geddes, L. A., Cabler, P., Moore, A. G., Rosborough, J., & Tacker, W. A. (1973). Threshold 60-Hz current required for ventricular fibrillation in subjects of various body weights. IEEE Transactions on Biomedical Engineering, 20, 465–468.CrossRefPubMedGoogle Scholar
  33. 33.
    Cooper, D., Ye, Y, Rolf L Jr, & Zuhdi, N. (1991) The pig as potential organ donor for man, In: Xenotransplantation (pp. 481–500). Berlin Heidelberg: Springer.Google Scholar
  34. 34.
    Douglas, W. R. (1972). Of pigs and men and research. Space Life Sciences, 3, 226–234.PubMedGoogle Scholar
  35. 35.
    Hughes, H. (1986). Swine in cardiovascular research. Laboratory Animal Science, 36, 348.PubMedGoogle Scholar
  36. 36.
    Lumb, G. (1966). Experimentally induced cardiac failure in swine: pathological changes. In L. K. Bustad & R. O. McClellan (Eds.), Swine in biomedical research (pp. 389–403). Richland: Pacific Northwest Laboratory.Google Scholar
  37. 37.
    White, D., & Wallwork, J. (1993). Xenografting: probability, possibility, or pipe dream? Lancet, 342, 879–880.CrossRefPubMedGoogle Scholar
  38. 38.
    Hamlin, R. L. (2007). Animal models of ventricular arrhythmias. Pharmacology and Therapeutics, 113, 276–295.CrossRefPubMedGoogle Scholar
  39. 39.
    Crick, S. J., Sheppard, M. N., Ho, S. Y., Gebstein, L., & Anderson, R. H. (1998). Anatomy of the pig heart: comparisons with normal human cardiac structure. Journal of Anatomy, 193(Pt 1), 105–119.CrossRefPubMedCentralPubMedGoogle Scholar
  40. 40.
    Glomset, D. J., & Glomset, A. T. (1940). A morphologic study of the cardiac conduction system in ungulates, dog, and man: Part II: the purkinje system. American Heart Journal, 20, 677–701.CrossRefGoogle Scholar
  41. 41.
    Sedmera, D., & Gourdie, R. G. (2014). Why do we have Purkinje fibers deep in our heart. Physiological Research, 63(Suppl 1), S9–S18.PubMedGoogle Scholar
  42. 42.
    Hamlin, R. L. (1960). The QRS electrocardiogram, epicardiogram, vectorcardiogram and ventricular excitation of swine. American Journal of Physiology, 198, 537–542.PubMedGoogle Scholar
  43. 43.
    Hamlin, R. L., Burton, R. R., Leverett, S. D., & Burns, J. W. (1975). Ventricular activation process in minipigs. Journal of Electrocardiology, 8, 113–116.CrossRefPubMedGoogle Scholar
  44. 44.
    Huang, J., Dosdall, D. J., Cheng, K. A., Li, L., Rogers, J. M., & Ideker, R. E. (2014). The importance of Purkinje activation in long duration ventricular fibrillation. Journal of the American Heart Association, 3, e000495.CrossRefPubMedCentralPubMedGoogle Scholar
  45. 45.
    Cheng, K. A., Dosdall, D. J., Li, L., Rogers, J. M., Ideker, R. E., & Huang, J. (2012). Evolution of activation patterns during long-duration ventricular fibrillation in pigs. American Journal of Physiology—Heart and Circulatory Physiology, 302, H992–H1002.CrossRefPubMedCentralPubMedGoogle Scholar
  46. 46.
    Horowitz, L. N., Spear, J. F., & Moore, E. N. (1981). Relation of the endocardial and epicardial ventricular fibrillation thresholds of the right and left ventricles. American Journal of Cardiology, 48, 698–701.CrossRefPubMedGoogle Scholar
  47. 47.
    Damiano, R., Smith, P. K., Tripp, H., Asano, T., Small, K., Lowe, J., et al. (1986). The effect of chemical ablation of the endocardium on ventricular fibrillation threshold. Circulation, 74, 645–652.CrossRefPubMedGoogle Scholar
  48. 48.
    Spear, J., Horowitz, L., Moore, E. (1977) Relationship of endocardial and epicardial ventricular-fibrillation thresholds of right and left-ventricles. American Journal of Cardiology, 39, 274–274.Google Scholar
  49. 49.
    Wong, M. C., Edwards, G., Spence, S. J., Kalman, J. M., Kumar, S., Joseph, S. A., et al. (2013). Characterization of catheter–tissue contact force during epicardial radiofrequency ablation in an ovine model. Circulation. Arrhythmia and Electrophysiology, 6, 1222–1228.CrossRefPubMedGoogle Scholar
  50. 50.
    Sacher, F., Wright, M., Derval, N., Denis, A., Ramoul, K., Roten, L., et al. (2013). Endocardial versus epicardial ventricular radiofrequency ablation: utility of in vivo contact force assessment. Circulation. Arrhythmia and Electrophysiology, 6, 144–150.Google Scholar
  51. 51.
    Li, G. R., Du, X. L., Siow, Y. L., Karmin, O., Tse, H. F., & Lau, C. P. (2003). Calcium-activated transient outward chloride current and phase 1 repolarization of swine ventricular action potential. Cardiovascular Research, 58, 89–98.CrossRefPubMedGoogle Scholar
  52. 52.
    Li, G. R., Feng, J., Yue, L., & Carrier, M. (1998). Transmural heterogeneity of action potentials and Ito1 in myocytes isolated from the human right ventricle. American Journal of Physiology, 275, H369–H377.PubMedGoogle Scholar
  53. 53.
    Zygmunt, A. C. (1994). Intracellular calcium activates a chloride current in canine ventricular myocytes. American Journal of Physiology, 267, H1984–H1995.PubMedGoogle Scholar
  54. 54.
    Dudel, J., Peper, K., Rüdel, R., & Trautwein, W. (1967). The dynamic chloride component of membrane current in Purkinje fibers. Pflüger’s Archiv für die gesamte Physiologie des Menschen und der Tiere, 295, 197–212.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Gregory P. Walcott
    • 1
    • 2
  • Mark W. Kroll
    • 4
  • Raymond E. Ideker
    • 1
    • 2
    • 3
  1. 1.Division of Cardiovascular Diseases, Department of MedicineUniversity of Alabama at BirminghamBirminghamUSA
  2. 2.Department of Biomedical EngineeringUniversity of Alabama at BirminghamBirminghamUSA
  3. 3.Department of PhysiologyUniversity of Alabama at BirminghamBirminghamUSA
  4. 4.Department of Biomedical EngineeringUniversity of MinnesotaMinneapolisUSA

Personalised recommendations