Magnetic Resonance Imaging Volumetry for Noninvasive Measures of Phenotypic Flexibility during Digestion in Burmese Pythons

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Physiological cardiac hypertrophy is characterized by reversible enlargement of cardiomyocytes and changes in chamber architecture, which increase stroke volume and V · O2,max via augmented convective oxygen transport. Cardiac hypertrophy is known to occur in response to repeated elevations of O 2 demand and/or reduced O 2 supply in several species of vertebrate ectotherms, including postprandial Burmese pythons (Python bivittatus). Recent data suggest postprandial cardiac hypertrophy in P. bivittatus is a facultative rather than obligatory response to digestion, though the triggers of this response are unknown. Here, we hypothesized that an O 2 supply-demand mismatch stimulates postprandial cardiac enlargement in Burmese pythons. To test this hypothesis, we rendered animals anemic prior to feeding, essentially halving blood oxygen content during the postprandial period. Fed anemic animals had heart rates 126% higher than those of fasted controls, which, coupled with a 71% increase in mean arterial pressure, suggests fed anemic animals were experiencing significantly elevated cardiac work. We found significant cardiac hypertrophy in fed anemic animals, which exhibited ventricles 39% larger than those of fasted controls and 28% larger than in fed controls. These findings support our hypothesis that those animals with a greater magnitude of O 2 supply-demand mismatch exhibit the largest hearts. The 'low O 2 signal' stimulating postprandial cardiac hypertrophy is likely mediated by elevated ventricular wall stress associated with postprandial hemodynamics.

Section: Adrenergic and Cholinergic Cardiac Tone In Fasting And Possupporting

confidence: 75%

Section: Introductionmentioning

confidence: 99%

Reduction of blood oxygen levels enhances postprandial cardiac hypertrophy in Burmese python (Python molurus)

Slay

Enok

Hicks

et al. 2013

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“…In fasting reptiles, however, ejection fraction is already very high (Burggren et al, 2013), leaving little capacity for further reductions in end-diastolic volume. Enhanced cardiac filling during diastole is therefore a more likely contributor, a view that is supported by magnetic resonance imaging, demonstrating substantial increases of end-diastolic heart volume during digestion in pythons and anacondas (Hansen et al, 2013;Zerbe et al, 2011). The increased cardiac filling must occur despite the shortened filling time that results from the postprandial tachycardia, and must therefore stem from increased venous return.…”

Section: Introductionmentioning

confidence: 93%

“…While the tachycardia stems from a combination of NANC (non-adrenergicnon-cholinergic) factors and a withdrawal of cholinergic tone (Enok et al, 2012;Skovgaard et al, 2009), the rise in V S remains more enigmatic. The postprandial increase of V S in pythons was originally ascribed to a rapid and extensive growth of the heart allowing for an elevated end-diastolic volume (Andersen et al, 2005;Secor and White, 2010), but a number of recent studies clearly demonstrate that heart mass does not increase during digestion (Hansen et al, 2013;Henriksen et al, 2014;Jensen et al, 2011;Slay et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Improved cardiac filling facilitates the postprandial elevation of stroke volume inPython regius

Enok

Leite

et al. 2016

Self Cite

To accommodate the pronounced metabolic response to digestion, pythons increase heart rate and elevate stroke volume, where the latter has been ascribed to a massive and fast cardiac hypertrophy. However, numerous recent studies show that heart mass rarely increases, even upon ingestion of large meals, and we therefore explored the possibility that a rise in mean circulatory filling pressure (MCFP) serves to elevate venous pressure and cardiac filling during digestion. To this end, we measured blood flows and pressures in anaesthetized Python regius. The anaesthetized snakes exhibited the archetypal tachycardia as well as a rise in both venous pressure and MCFP that fully account for the approximate doubling of stroke volume. There was no rise in blood volume and the elevated MCFP must therefore stem from increased vascular tone, possibly by means of increased sympathetic tone on the veins. Furthermore, although both venous pressure and MCFP increased during volume loading, there was no evidence that postprandial hearts were endowed with an additional capacity to elevate stroke volume. In vitro measurements of force development of paced ventricular strips also failed to reveal signs of increased contractility, but the postprandial hearts had higher activities of cytochrome oxidase and pyruvate kinase, which probably serves to sustain the rise in cardiac work during digestion.

“…Within 24 h of ingestion of a meal, a python's small intestine doubles in mass (Secor, 1995;Secor and Diamond, 1995;Lignot et al, 2005) and volume (Hansen et al, 2013), and increases its mass-specific lipid content by 75% (Henriksen et al, 2015). A portion of this increase in lipid content is caused by the accumulation of lipid droplets in the apical side of the enterocytes during the first day of digestion (Starck and Beese, 2001;Lignot et al, 2005;Starck and Wimmer, 2005;Helmstetter et al, 2009).…”

Section: −1mentioning

confidence: 99%

Digesting pythons quickly oxidize the proteins in their meals and save the lipids for later

McCue

Guzman

Passement

2015

Pythons digesting rodent meals exhibit up to 10-fold increases in their resting metabolic rate (RMR); this increase in RMR is termed specific dynamic action (SDA). Studies have shown that SDA is partially fueled by oxidizing dietary nutrients, yet it remains unclear whether the proteins and the lipids in their meals contribute equally to this energy demand. We raised two populations of mice on diets labeled with either [ 13 C]leucine or [ 13 C]palmitic acid to intrinsically enrich the proteins and lipids in their bodies, respectively. Ball pythons (Python regius) were fed whole mice (and pureed mice 3 weeks later), after which we measured their metabolic rates and the δ 13 C in the breath. The δ 13C values in the whole bodies of the protein-and lipid-labeled mice were generally similar (i.e. 5.7±4.7‰ and 2.8±5.4‰, respectively) but the oxidative kinetics of these two macronutrient pools were quite different. We found that the snakes oxidized 5% of the protein and only 0.24% of the lipids in their meals within 14 days. Oxidation of the dietary proteins peaked 24 h after ingestion, at which point these proteins provided ∼90% of the metabolic requirement of the snakes, and by 14 days the oxidation of these proteins decreased to nearly zero. The oxidation of the dietary lipids peaked 1 day later, at which point these lipids supplied ∼25% of the energy demand. Fourteen days after ingestion, these lipids were still being oxidized and continued to account for ∼25% of the metabolic rate. Pureeing the mice reduced the cost of gastric digestion and decreased SDA by 24%. Pureeing also reduced the oxidation of dietary proteins by 43%, but it had no effect on the rates of dietary lipid oxidation. Collectively, these results demonstrate that pythons are able to effectively partition the two primary metabolic fuels in their meals. This approach of uniquely labeling the different components of the diet will allow researchers to examine new questions about how and when animals use the nutrients in their meals.