Low-Temperature Performance of Isolated Working Hearts from a Hibernator and a Nonhibernator

Burlington, Roy F.; Darvish, Ahmad

doi:10.1086/physzool.61.5.30161260

Cited by 31 publications

(18 citation statements)

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“…The windkessel effect promotes blood flow along vessels but with the prolonged diastole of slow heart rates, diastolic flow movement down the system does not proceed rapidly. Therefore, despite the fall in systolic pressure and prolongation of diastolic phase, the diastolic pressure, and thus mean pressure, remains relatively high (Lyman and O'Brien, 1963;Burlington and Darvish, 1998). Prolonged duration of systolic strain during hibernation as identified by strain echocardiography (discussed below) could also play a role in the hypertrophic response (Ritter and Neyses, 2003).…”

Section: Echocardiography In Ground Squirrelsmentioning

confidence: 99%

“…Individuals transition from an active, euthermic state (37°C) to a hibernating state where torpid body temperature falls to 3-5°C but is punctuated repeatedly by arousals to euthermy. During bouts of torpor over a 6 month hibernation, these animals may be completely inactive for 2 weeks at a time at near-freezing temperatures, while arousals may last 24 h. Cardiovascular adaptations must occur for the myocardium to remain healthy and efficient during a period of extremely low temperatures, and low heart rate and cardiac output (Folk et al, 1970;Caprette and Senturia, 1984;Milsom et al, 1993;Milsom et al, 1999;Burlington and Darvish, 1998;Brauch et al, 2005). Non-hibernators that suffer from low heart rate conditions alone will develop cardiac chamber remodeling and congestive heart failure over time (Kertesz et al, 1997;Verduyn et al, 2001;Schoenmakers et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

“…Low heart rates and cardiac output generally lead to chamber dilation due to volume overload (Verduyn et al, 2001;Schoenmakers et al, 2003). These conditions in hibernators may have led to a noted variety of cardiac adaptations (Folk et al, 1970;Caprette and Senturia, 1984;Milsom et al, 1993;Milsom et al, 1999;Burlington and Darvish, 1998;Brauch et al, 2005). In humans, cardiovascular function ceases with a cessation of pacemaker conduction at about 20°C, and this acute failure masks more chronic failure of the heart where pumping function can be maintained at a lower temperature in rats and mice.…”

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confidence: 99%

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Increase in cardiac myosin heavy-chain (MyHC) alpha protein isoform in hibernating ground squirrels, with echocardiographic visualization of ventricular wall hypertrophy and prolonged contraction.

Nelson

Rourke

2013

Journal of Experimental Biology

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SUMMARYDeep hibernators such as golden-mantled ground squirrels (Callospermophilus lateralis) have multiple challenges to cardiac function during low temperature torpor and subsequent arousals. As heart rates fall from over 300 beats min -1 to less than 10, chamber dilation and reduced cardiac output could lead to congestive myopathy. We performed echocardiography on a cohort of individuals prior to and after several months of hibernation. The left ventricular chamber exhibited eccentric and concentric hypertrophy during hibernation and thus calculated ventricular mass was ~30% greater. Ventricular ejection fraction was mildly reduced during hibernation but stroke volumes were greater due to the eccentric hypertrophy and dramatically increased diastolic filling volumes. Globally, the systolic phase in hibernation was ~9.5 times longer, and the diastolic phase was 28× longer. Left atrial ejection generally was not observed during hibernation. Atrial ejection returned weakly during early arousal. Strain echocardiography assessed the velocity and total movement distance of contraction and relaxation for regional ventricular segments in active and early arousal states. Myocardial systolic strain during early arousal was significantly greater than the active state, indicating greater total contractile movement. This mirrored the increased ventricular ejection fraction noted with early arousal. However, strain rates were slower during early arousal than during the active period, particularly systolic strain, which was 33% of active, compared with the rate of diastolic strain, which was 67% of active. As heart rate rose during the arousal period, myocardial velocities and strain rates also increased; this was matched closely by cardiac output. Curiously, though heart rates were only 26% of active heart rates during early arousal, the cardiac output was nearly 40% of the active state, suggesting an efficient pumping system. We further analyzed proportions of cardiac myosin heavy-chain (MyHC) isoforms in a separate cohort of squirrels over 5 months, including time points before hibernation, during hibernation and just prior to emergence. Hibernating individuals were maintained in both a 4°C cold room and a 20°C warm room. Measured by SDS-PAGE, relative percentages of cardiac MyHC alpha were increased during hibernation, at both hibernacula temperatures. A potential increase in contractile speed, and power, from more abundant MyHC alpha may aid force generation at low temperature and at low heart rates. Unlike many models of cardiomyopathies where the alpha isoform is replaced by the beta isoform in order to reduce oxygen consumption, ground squirrels demonstrate a potential cardioprotective mechanism to maintain cardiac output during torpor. Received 25 March 2013; Accepted 4 September 2013Key words: hibernation, MyHC, echocardiogram, atrial contraction, cardiac function. Echocardiogram and myosin of hibernatorsThe myosin heavy-chain isoforms (MyHC) are crucial determinants of contractile performance in cardiac muscle t...

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Section: Echocardiography In Ground Squirrelsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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Increase in cardiac myosin heavy-chain (MyHC) alpha protein isoform in hibernating ground squirrels, with echocardiographic visualization of ventricular wall hypertrophy and prolonged contraction.

Nelson

Rourke

2013

Journal of Experimental Biology

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“…Grizzly bears (Ursus arctos horribilis) do not eat, drink, or urinate and demonstrate minimal activity during their annual 4 -6 mo hibernation period. Cardiovascular adaptations must occur for the myocardium to remain healthy and efficient during a period of extremely low heart rates and cardiac output (6,7,8,12,26). Nonhibernators that suffer from bradycardic conditions will develop cardiac chamber dilation due to volume overload during the excessively long diastolic pauses (23,35,42).…”

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confidence: 99%

Titin isoform switching is a major cardiac adaptive response in hibernating grizzly bears

Nelson

Robbins

et al. 2008

American Journal of Physiology-Heart and Circulatory Physiology

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The hibernation phenomenon captures biological as well as clinical interests to understand how organs adapt. Here we studied how hibernating grizzly bears (Ursus arctos horribilis) tolerate extremely low heart rates without developing cardiac chamber dilation. We evaluated cardiac filling function in unanesthetized grizzly bears by echocardiography during the active and hibernating period. Because both collagen and titin are involved in altering diastolic function, we investigated both in the myocardium of active and hibernating grizzly bears. Heart rates were reduced from 84 beats/min in active bears to 19 beats/min in hibernating bears. Diastolic volume, stroke volume, and left ventricular ejection fraction were not different. However, left ventricular muscle mass was significantly lower (300 Ϯ 12 compared with 402 Ϯ 14 g; P ϭ 0.003) in the hibernating bears, and as a result the diastolic volume-to-left ventricular muscle mass ratio was significantly greater. Early ventricular filling deceleration times (106.4 Ϯ 14 compared with 143.2 Ϯ 20 ms; P ϭ 0.002) were shorter during hibernation, suggesting increased ventricular stiffness. Restrictive pulmonary venous flow patterns supported this conclusion. Collagen type I and III comparisons did not reveal differences between the two groups of bears. In contrast, the expression of titin was altered by a significant upregulation of the stiffer N2B isoform at the expense of the more compliant N2BA isoform. The mean ratio of N2BA to N2B titin was 0.73 Ϯ 0.07 in the active bears and decreased to 0.42 Ϯ 0.03 (P ϭ 0.006) in the hibernating bears. The upregulation of stiff N2B cardiac titin is a likely explanation for the increased ventricular stiffness that was revealed by echocardiography, and we propose that it plays a role in preventing chamber dilation in hibernating grizzly bears. Thus our work identified changes in the alternative splicing of cardiac titin as a major adaptive response in hibernating grizzly bears.collagen; bradycardia; diastolic function; echocardiography MANY MAMMALS UNDERGO A UNIQUE state of energy conservation in response to harsh climatic conditions. Grizzly bears (Ursus arctos horribilis) do not eat, drink, or urinate and demonstrate minimal activity during their annual 4 -6 mo hibernation period. Cardiovascular adaptations must occur for the myocardium to remain healthy and efficient during a period of extremely low heart rates and cardiac output (6,7,8,12,26). Nonhibernators that suffer from bradycardic conditions will develop cardiac chamber dilation due to volume overload during the excessively long diastolic pauses (23,35,42). Over time, chamber dilation and elevated end-diastolic pressures lead to congestive heart failure if no intervention is sought (23, 35). However, hibernating grizzly bears tolerate extremely low heart rates without ventricular chamber dilation (30). The mechanisms that circumvent chamber dilation are not well understood, but they might involve increased ventricular stiffness (30).Molecular changes in sarcomeric and ext...

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“…Profound metabolic suppression, hypothermia, and bradycardia observed at the organismal level during the hibernation period have no harmful effects (Geiser, 1988;Barnes, 1989;Buck and Barnes, 2000;Drew et al, 2001;Zhou et al, 2001;Carey et al, 2003a;Heldmaier et al, 2004;Tamura et al, 2005;Ross et al, 2006;Drew et al, 2007). The hearts of hibernating mammals remain functional even at 0°C while the hearts of non-hibernating mammals becomes arrhythmic and stop functioning between 10°C and 15°C (Lyman, 1982;Caprette and Senturia, 1984;Burlington and Darvish, 1988). This implies that an intrinsic difference in functional mechanism may exist between the hearts of a hibernator and a non-hibernator enabling the hibernator to survive despite low body temperatures.…”

Section: Resultsmentioning

confidence: 99%

Natural Protection Against Cardiac Arrhythmias During Hibernation: Significance of Adenosine

Jinka¹

2012

Cardiac Arrhythmias - New Considerations

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Low-Temperature Performance of Isolated Working Hearts from a Hibernator and a Nonhibernator

Cited by 31 publications

References 18 publications

Increase in cardiac myosin heavy-chain (MyHC) alpha protein isoform in hibernating ground squirrels, with echocardiographic visualization of ventricular wall hypertrophy and prolonged contraction.

Increase in cardiac myosin heavy-chain (MyHC) alpha protein isoform in hibernating ground squirrels, with echocardiographic visualization of ventricular wall hypertrophy and prolonged contraction.

Titin isoform switching is a major cardiac adaptive response in hibernating grizzly bears

Natural Protection Against Cardiac Arrhythmias During Hibernation: Significance of Adenosine

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