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Extreme Respiratory Sinus Arrhythmia Enables Overwintering Black Bear Survival—Physiological Insights and Applications to Human Medicine

  • Timothy G. Laske
  • Henry J. Harlow
  • David L. Garshelis
  • Paul A. Iaizzo
Article

Abstract

American black bears survive winter months without food and water while in a mildly hypothermic, hypometabolic, and inactive state, yet they appear to be able to return to near-normal systemic function within minutes of arousal. This study’s goal was to characterize the cardiovascular performance of overwintering black bears and elicit the underlying mechanisms enabling survival. Mid-winter cardiac electrophysiology was assessed in four wild black bears using implanted data recorders. Paired data from early and late winter were collected from 37 wild bears, which were anesthetized and temporarily removed from their dens to record cardiac electrophysiological parameters (12-lead electrocardiograms) and cardiac dimensional changes (echocardiography). Left ventricular thickness, primary cardiac electrophysiological parameters, and cardiovascular response to threats (“fight or flight” response) were preserved throughout winter. Dramatic respiratory sinus arrhythmias were recorded (cardiac cycle length variations up to 865%) with long sinus pauses between breaths (up to 13 s). The accelerated heart rate during breathing efficiently transports oxygen, with the heart “resting” between breaths to minimize energy usage. This adaptive cardiac physiology may have broad implications for human medicine.

Keywords

Black Bear Hibernation Cardiac Physiology Echocardiography Electrophysiology Implanted Data Recorders 

Notes

Acknowledgments

This work was supported by the National Science Foundation, Minnesota Department of Natural Resources, University of Minnesota Institute for Engineering in Medicine, Colorado Wildlife Management, Wyoming Department of Natural Resources, and Medtronic, Inc.

We thank Pamela L. Coy, Karen V. Noyce, Brian Dirks, Barb Olson, Lixue Yin, Elizabeth Bohn, and Jin Back Hong for technical assistance and Monica Mahre for assistance with manuscript preparation.

References

  1. 1.
    Austen, M. L., & Wilson, G. V. (2001). Increased vagal tone during winter in subsyndromal seasonal affective disorder. Biological Psychiatry, 50(1), 28–34.CrossRefPubMedGoogle Scholar
  2. 2.
    Berntson, C. G., Cacioppo, J. T., & Quigley, K. S. (1993). Respiratory sinus arrhythmia: Autonomic origins, physiological mechanisms, and psychophysiological implications. Psychophysiology, 30(2), 183–196.CrossRefPubMedGoogle Scholar
  3. 3.
    Bolling, S. F., Benedict, M. B., Tramontini, N. L., Kilgore, K. S., Harlow, H. H., Su, T. P., et al. (1998). Hibernation triggers and myocardial protection. Circulation, 98(19 Suppl), II220–II223.PubMedGoogle Scholar
  4. 4.
    Chien, S., Diana, J. N., Oeltgen, P. R., Todd, E. P., O’Connor, W. N., & Chitwood, W. R., Jr. (1989). Eighteen to 37 hours preservation of major organs using a new autoperfusion multiorgan preparation. Annals of Thoracic Surgery, 47(6), 860–867.CrossRefPubMedGoogle Scholar
  5. 5.
    Dausmann, K. H., Glos, J., Ganzhorn, J. U., & Heldmaier, G. (2004). Hibernation in a tropical primate. Nature, 429(6994), 825–826.CrossRefPubMedGoogle Scholar
  6. 6.
    Folk, G. E., Jr., Folk, M. A., & Minor, J. J. (1972). Physiological condition of three species of bears in winter dens. In S. Herrero (Ed.), Bears: Their biology and management (New Series Publication No. 23) (pp. 107–124). Morges: IUCN.Google Scholar
  7. 7.
    Fedorov, V. V., Li, L., Glukhov, A., Shischkina, I., Aliev, R. R., Mikheeva, T., et al. (2005). Hibernator Citellus undulates maintains safe cardiac conduction and is protected against tachyarrhythmias during extreme hypothermia: possible role of Cx43 and Cx45 up-regulation. Heart Rhythm, 2(9), 966–975.CrossRefPubMedGoogle Scholar
  8. 8.
    Geiser, F., & Ruf, T. (1995). Hibernation versus daily torpor in mammals and birds: Physiological variables and classification of torpor patterns. Physiological Zoology, 68(6), 935–966.Google Scholar
  9. 9.
    Giles, J. (2004). Could astronauts sleep their way to the stars? News@Nature.com.Google Scholar
  10. 10.
    Harding, J. D., Piacentino, V., III, Gaughan, J. P., Houser, S. R., & Margulies, K. B. (2001). Electrophysiological alterations after mechanical circulatory support in patients with advanced cardiac failure. Circulation, 104(11), 1241–1247.CrossRefPubMedGoogle Scholar
  11. 11.
    Harlow, H. J., Lohuis, T., Anderson-Sprecher, R. C., & Beck, T. D. (2004). Body surface temperature of hibernating black bears may be related to periodic muscle activity. Journal of Mammalogy, 85(3), 414–419.CrossRefGoogle Scholar
  12. 12.
    Harlow, H. J., Lohuis, T., Beck, T. D. I., & Iaizzo, P. A. (2001). Muscle strength in overwintering bears. Nature, 409(6823), 997.CrossRefPubMedGoogle Scholar
  13. 13.
    Harris, M. B., & Milsom, W. K. (1995). Parasympathetic influence on heart rate in euthermic and hibernating ground squirrels. Journal of Experimental Biology, 198(Pt 4), 931–937.PubMedGoogle Scholar
  14. 14.
    Hellgren, E. C. (1998). Physiology of hibernation in bears. Ursus, 10, 467–477.Google Scholar
  15. 15.
    Hirsch, J. A., & Bishop, B. (1981). Respiratory sinus arrhythmia in humans: How breathing pattern modulates heart rate. American Journal of Physiology: Heart and Circulatory Physiology, 241(4), H620–H629.Google Scholar
  16. 16.
    Hong, J., Sigg, D. C., Coles, J. A., Jr., Oeltgen, P. R., Harlow, H. J., Soule, C. L., et al. (2005). Hibernation induction trigger reduces hypoxic damage of swine skeletal muscle. Muscle and Nerve, 32(2), 200–207.CrossRefPubMedGoogle Scholar
  17. 17.
    Khositseth, A., Hejlik, J., Shen, W. K., & Ackerman, J. M. (2005). Epinephrine-induced T-wave notching in congenital long QT syndrome. Heart Rhythm, 2(2), 141–146.CrossRefPubMedGoogle Scholar
  18. 18.
    Kondo, N., Sekijima, T., Kondo, J., Takamatsu, N., Tohya, K., & Ohtsu, T. (2006). Circannual control of hibernation by HP complex in the brain. Cell, 125(1), 161–172.CrossRefPubMedGoogle Scholar
  19. 19.
    Laske, T. G., Harlow, H. J., Werder, J. C., Marshall, M. T., & Iaizzo, P. A. (2005). High capacity implantable data recorders: System design and experience in canines and denning black bears. Journal of Biomechanical Engineering, 127(6), 964–971.CrossRefPubMedGoogle Scholar
  20. 20.
    Levine, B. D., Zuckerman, J. H., & Pawelczyk, J. A. (1997). Cardiac atrophy after bed-rest deconditioning. Circulation, 96(2), 517–525.PubMedGoogle Scholar
  21. 21.
    Linnell, J. D. C., Swenson, J. E., & Andersen, R. (2000). How vulnerable are denning bears to disturbance? Wildlife Society Bulletin, 28, 400–413.Google Scholar
  22. 22.
    Lohuis, T., Beck, T. D. I., & Harlow, H. J. (2005). Hibernating black bears have blood chemistry and plasma amino acid profiles that are indicative of long-term adaptive fasting. Canadian Journal of Zoology, 83(9), 1257–1263.CrossRefGoogle Scholar
  23. 23.
    Lohuis, T. D., Harlow, H. J., Beck, T. D. I., & Iaizzo, P. A. (2007). Hibernating bears conserve muscle strength and maintain fatigue resistance. Physiological and Biochemical Zoology, 80(3), 257–269.CrossRefPubMedGoogle Scholar
  24. 24.
    Milsom, W. K., Zimmer, M. B., & Harris, M. B. (1999). Regulation of cardiac rhythm in hibernating mammals. Comparative Biochemistry and Physiology, 124(4), 383–391.CrossRefPubMedGoogle Scholar
  25. 25.
    Moody, G. B., Mark, R. G., Zoccola, A., & Mantero, S. (1985). Derivation of respiratory signals from multi-lead ECGs. Computers in Cardiology, 12, 113–116.Google Scholar
  26. 26.
    Nelson, O. L., McEwen, M. M., Robbins, C. T., Felicetti, L., & Christensen, W. F. (2003). Evaluation of cardiac function in active and hibernating grizzly bears. Journal of the American Veterinary Medical Association, 223(8), 1170–1175.CrossRefPubMedGoogle Scholar
  27. 27.
    Nelson, O. L., Robbins, C. T., Wu, Y., & Granzier, H. (2008). Titon isoform switching is a major adaptive response in hibernating grizzly bears. American Journal of Physiology. Heart and Circulatory Physiology, 295(1), 366–371.CrossRefGoogle Scholar
  28. 28.
    Novotny, T., Sisakova, M., Kadlecova, J., Florianova, A., Semrad, B., Gaillyova, R., et al. (2004). Occurrence of notched T wave in healthy family members with the long QT interval syndrome. American Journal of Cardiology, 94(6), 808–811.CrossRefPubMedGoogle Scholar
  29. 29.
    Perhonen, M. A., Franco, F., Lane, L. D., Buckey, J. C., Blomqvist, C. G., Zerwekh, J. E., et al. (2001). Cardiac atrophy after bed rest and space flight. Journal of Applied Physiology, 91(2), 645–653.PubMedGoogle Scholar
  30. 30.
    Perhonen, M. A., Zuckerman, J. H., & Levine, B. D. (2001). Deterioration of left ventricular chamber performance after bed rest: “cardiovascular deconditioning” or hypovolemia? Circulation, 103(14), 1851–1857.PubMedGoogle Scholar
  31. 31.
    Porges, S. W., & Byrne, E. (1992). Research methods for measurement of heart rate and respiration. Biological Psychology, 34(2–3), 93–130.CrossRefPubMedGoogle Scholar
  32. 32.
    Razeghi, P., & Taegtmeyer, H. (2006). Hypertrophy and atrophy of the heart: The other side of remodeling. Annals of the New York Academy of Sciences, 1080, 110–119.CrossRefPubMedGoogle Scholar
  33. 33.
    Rogers, L. L., & Durst, S. C. (1987). Evidence that black bears reduce peripheral blood flow during hibernation. Journal of Mammalogy, 68(4), 876–878.CrossRefGoogle Scholar
  34. 34.
    Sigg, D. C., Coles, Jr., J. A., Gallagher, W. J., Oeltgen, P. R., & Iaizzo, P. A. (2001). Opioid preconditioning: myocardial function and energy metabolism. Annals of Thoracic Surgery, 72, 1576–1582.Google Scholar
  35. 35.
    Spaak, J., Montmerle, S., Sundblad, P., & Linnarsson, D. (2005). Long-term bed rest-induced reductions in stroke volume during rest and exercise: Cardiac dysfunction vs. volume depletion. Journal of Applied Physiology, 98(2), 648–654.CrossRefPubMedGoogle Scholar
  36. 36.
    Summers, R. L., Martin, D. S., Meck, J. V., & Coleman, T. G. (2005). Mechanism of spaceflight-induced changes in left ventricular mass. American Journal of Cardiology, 95(9), 1128–1130.CrossRefPubMedGoogle Scholar
  37. 37.
    Tinker, D. B., Harlow, H. J., & Beck, T. D. I. (1998). Protein use and muscle-fiber changes in free-ranging, hibernating black bears. Physiological Zoology, 71(4), 414–424.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Timothy G. Laske
    • 1
    • 2
  • Henry J. Harlow
    • 3
  • David L. Garshelis
    • 4
  • Paul A. Iaizzo
    • 1
  1. 1.University of MinnesotaMinneapolisUSA
  2. 2.Medtronic, Inc.Mounds ViewUSA
  3. 3.University of WyomingLaramieUSA
  4. 4.Minnesota Department of Natural ResourcesGrand RapidsUSA

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