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Journal of Comparative Physiology B

, Volume 180, Issue 3, pp 465–473 | Cite as

Cardiac function adaptations in hibernating grizzly bears (Ursus arctos horribilis)

  • O. Lynne Nelson
  • Charles T. Robbins
Original Paper

Abstract

Research on the cardiovascular physiology of hibernating mammals may provide insight into evolutionary adaptations; however, anesthesia used to handle wild animals may affect the cardiovascular parameters of interest. To overcome these potential biases, we investigated the functional cardiac phenotype of the hibernating grizzly bear (Ursus arctos horribilis) during the active, transitional and hibernating phases over a 4 year period in conscious rather than anesthetized bears. The bears were captive born and serially studied from the age of 5 months to 4 years. Heart rate was significantly different from active (82.6 ± 7.7 beats/min) to hibernating states (17.8 ± 2.8 beats/min). There was no difference from the active to the hibernating state in diastolic and stroke volume parameters or in left atrial area. Left ventricular volume:mass was significantly increased during hibernation indicating decreased ventricular mass. Ejection fraction of the left ventricle was not different between active and hibernating states. In contrast, total left atrial emptying fraction was significantly reduced during hibernation (17.8 ± 2.8%) as compared to the active state (40.8 ± 1.9%). Reduced atrial chamber function was also supported by reduced atrial contraction blood flow velocities and atrial contraction ejection fraction during hibernation; 7.1 ± 2.8% as compared to 20.7 ± 3% during the active state. Changes in the diastolic cardiac filling cycle, especially atrial chamber contribution to ventricular filling, appear to be the most prominent macroscopic functional change during hibernation. Thus, we propose that these changes in atrial chamber function constitute a major adaptation during hibernation which allows the myocardium to conserve energy, avoid chamber dilation and remain healthy during a period of extremely low heart rates. These findings will aid in rational approaches to identifying underlying molecular mechanisms.

Keywords

Atrial chamber Bradycardia Cardiac function Diastolic function Ursus arctos horribilis 

Notes

Acknowledgments

This work was supported by the Autzen Foundation and the Washington State University Bear Research Education and Conservation Center. We thank the graduate students Jennifer Fortin and Justin Teisburg, and technologists, Gary Radamaker, and Pam Thompson at Washington State University for excellent technical assistance and management of bear care.

Supplementary material

Supplementary material (MPG 502 kb)

Supplementary material (MPG 1936 kb)

References

  1. Appleton CP, Firstenberg MS, Garcia MJ, Thomas JD (2000) The echo-Doppler evaluation of left ventricular diastolic function. A current perspective. Cardiol Clin 18:513–546 ixCrossRefPubMedGoogle Scholar
  2. Brauch KM, Dhruv ND, Hanse EA, Andrews MT (2005) Digital transcriptome analysis indicates adaptive mechanisms in the heart of a hibernating mammal. Physiol Genomics 23:227–234CrossRefPubMedGoogle Scholar
  3. Burlington RF, Darvish A (1998) Low temperature performance of isolated working hearts from a hibernator and a nonhibernator. Physiol Zool 161:387–395Google Scholar
  4. Caprette DR, Senturia JB (1984) Isovolumetric performance of isolated ground squirrel and rat hearts at low temperature. Am J Physiol 247:R722–R727PubMedGoogle Scholar
  5. Dernellis JM, Stefanadis CI, Zacharoulis AA, Toutouzas PK (1998) Left atrial mechanical adaptation to long-standing hemodynamic loads based on pressure-volume relations. Am J Cardiol 81:1138–1143CrossRefPubMedGoogle Scholar
  6. Folk GE Jr, Hunt JM, Folk MA (1974) Further evidence for hibernation in bears. In: Pelton MR, Lentfer JW, Folk GE Jr (eds) Third international conference on bears-their biology and management, pp 43–47Google Scholar
  7. Folk GE Jr, Brewer MC, Sanders D (1970) Cardiac physiology of polar bears in winter dens. Arctic 23:130–131Google Scholar
  8. Garcia MJ, Firstenberg MS, Greenberg NL, Smedira N, Rodriguez L, Prior D, Thomas JD (2001) Estimation of left ventricular operating stiffness from Doppler early filling deceleration time in humans. Am J Physiol Heart Circ Physiol 280:H554–H561PubMedGoogle Scholar
  9. Hellyer P, Muir WW 3rd, Hubbell JA, Sally J (1988) Cardiorespiratory effects of the intravenous administration of tiletamine-zolazepam to cats. Vet Surg 17:105–110CrossRefPubMedGoogle Scholar
  10. Hissa R, Siekkinen J, Hohtola E, Saarela S, Hakala A, Pudas J (1994) Seasonal patterns in the physiology of the European brown bear (Ursus arctos arctos) in Finland. Comp Biochem Physiol A Physiol 109:781–791CrossRefPubMedGoogle Scholar
  11. Kertesz NJ, Friedman RA, Colan SD, Walsh EP, Gajarski RJ, Gray PS, Shirley R, Geva T (1997) Left ventricular mechanics and geometry in patients with congenital complete atrioventricular block. Circulation 96:3430–3435PubMedGoogle Scholar
  12. Kirkebo A (1968) Cardiovascular investigations on hedgehogs during arousal from the hibernating state. Acta Physiol Scand 73:394–406PubMedGoogle Scholar
  13. Kuecherer HF, Kee LL, Modin G, Cheitlin MD, Schiller NB (1991a) Echocardiography in serial evaluation of left ventricular systolic and diastolic function: importance of image acquisition, quantitation, and physiologic variability in clinical and investigational applications. J Am Soc Echocardiogr 4:203–214PubMedGoogle Scholar
  14. Kuecherer HF, Kusumoto F, Muhiudeen IA, Cahalan MK, Schiller NB (1991b) Pulmonary venous flow patterns by transesophageal pulsed Doppler echocardiography: relation to parameters of left ventricular systolic and diastolic function. Am Heart J 122:1683–1693CrossRefPubMedGoogle Scholar
  15. Lyman CP (1982) The hibernating state. In: Lyman TA, Willis JS, Malan A, Wang LCH (eds) Hibernation and torpor in mammals and birds. Academic press, New York, pp 12–53Google Scholar
  16. Milsom WK, Burlington RF, Burleson ML (1993) Vagal influence of heart rate in hibernating ground squirrels. J Exp Biol 185:25–32Google Scholar
  17. Milsom WK, Zimmer MB, Harris MB (1999) Regulation of cardiac rhythm in hibernating mammals. Comp Biochem Physiol A Mol Integr Physiol 124:383–391CrossRefPubMedGoogle Scholar
  18. Narahashi T, Tsunoo A, Yoshii M (1987) Characterization of two types of calcium channels in mouse neuroblastoma cells. J Physiol 383:231–249PubMedGoogle Scholar
  19. Nelson OL, McEwen MM, Robbins CT, Felicetti L, Christensen WF (2003) Evaluation of cardiac function in active and hibernating grizzly bears. J Am Vet Med Assoc 223:1170–1175CrossRefPubMedGoogle Scholar
  20. Nelson OL, Robbins CT, Wu Y, Granzier H (2008) Titin isoform switching is a major cardiac adaptive response in hibernating grizzly bears. Am J Physiol Heart Circ Physiol 295:H366–H371CrossRefPubMedGoogle Scholar
  21. Ntalianis A, Nanas JN (2006) Immediate relief of congestive heart failure by ventricular pacing in chronic bradycardia. Cardiol Rev 14:e14–e15CrossRefPubMedGoogle Scholar
  22. Propovic V (1964) Cardiac output in hibernating ground squirrels. Am J Physiol 207:1345–1348Google Scholar
  23. Roth DM, Swaney JS, Dalton ND, Gilpin EA, Ross J Jr (2002) Impact of anesthesia on cardiac function during echocardiography in mice. Am J Physiol Heart Circ Physiol 282:H2134–H2140PubMedGoogle Scholar
  24. Schiller NB, Shah PM, Crawford M, DeMaria A, Devereux R, Feigenbaum H, Gutgesell H, Reichek N, Sahn D, Schnittger I et al (1989) Recommendations for quantitation of the left ventricle by two-dimensional echocardiography. American Society of Echocardiography Committee on Standards, Subcommittee on Quantitation of Two-Dimensional Echocardiograms. J Am Soc Echocardiogr 2:358–367PubMedGoogle Scholar
  25. Schoenmakers M, Ramakers C, van Opstal JM, Leunissen JD, Londono C, Vos MA (2003) Asynchronous development of electrical remodeling and cardiac hypertrophy in the complete AV block dog. Cardiovasc Res 59:351–359CrossRefPubMedGoogle Scholar
  26. Sitsapesan R, Montgomery RA, MacLeod KT, Williams AJ (1991) Sheep cardiac sarcoplasmic reticulum calcium-release channels: modification of conductance and gating by temperature. J Physiol 434:469–488PubMedGoogle Scholar
  27. Stefanadis C, Dernellis J, Lambrou S, Toutouzas P (1998) Left atrial energy in normal subjects, in patients with symptomatic mitral stenosis, and in patients with advanced heart failure. Am J Cardiol 82:1220–1223CrossRefPubMedGoogle Scholar
  28. Stein AB, Tiwari S, Thomas P, Hunt G, Levent C, Stoddard MF, Tang XL, Bolli R, Dawn B (2007) Effects of anesthesia on echocardiographic assessment of left ventricular structure and function in rats. Basic Res Cardiol 102:28–41CrossRefPubMedGoogle Scholar
  29. Thomas WP, Gaber CE, Jacobs GJ, Kaplan PM, Lombard CW, Moise NS, Moses BL (1993) Recommendations for standards in transthoracic two-dimensional echocardiography in the dog and cat. Echocardiography Committee of the Specialty of Cardiology, American College of Veterinary Internal Medicine. J Vet Intern Med 7:247–252PubMedCrossRefGoogle Scholar
  30. Thomas L, Levett K, Boyd A, Leung DY, Schiller NB, Ross DL (2003) Changes in regional left atrial function with aging: evaluation by Doppler tissue imaging. Eur J Echocardiogr 4:92–100CrossRefPubMedGoogle Scholar
  31. Tsang TS, Abhayaratna WP, Barnes ME, Miyasaka Y, Gersh BJ, Bailey KR, Cha SS, Seward JB (2006) Prediction of cardiovascular outcomes with left atrial size: is volume superior to area or diameter? J Am Coll Cardiol 47:1018–1023CrossRefPubMedGoogle Scholar
  32. Verduyn SC, Ramakers C, Snoep G, Leunissen JD, Wellens HJ, Vos MA (2001) Time course of structural adaptations in chronic AV block dogs: evidence for differential ventricular remodeling. Am J Physiol Heart Circ Physiol 280:H2882–H2890PubMedGoogle Scholar
  33. Volders PG, Sipido KR, Vos MA, Kulcsar A, Verduyn SC, Wellens HJ (1998) Cellular basis of biventricular hypertrophy and arrhythmogenesis in dogs with chronic complete atrioventricular block and acquired torsade de pointes. Circulation 98:1136–1147PubMedGoogle Scholar
  34. Walsh KB, Begenisich TB, Kass RS (1989) Beta-adrenergic modulation of cardiac ion channels. Differential temperature sensitivity of potassium and calcium currents. J Gen Physiol 93:841–854CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  1. 1.Department of Veterinary Clinical SciencesWashington State UniversityPullmanUSA
  2. 2.Department of Natural Resource Sciences, School of Biological SciencesWashington State UniversityPullmanUSA

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