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Arterial wall thickening normalizes arterial wall tension with growth in American alligators, Alligator mississippiensis

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Abstract

Arterial wall tension increases with luminal radius and arterial pressure. Hence, as body mass (Mb) increases, associated increases in radius induces larger tension. Thus, it could be predicted that high tension would increase the potential for rupture of the arterial wall. Studies on mammals have focused on systemic arteries and have shown that arterial wall thickness increases with Mb and normalizes tension. Reptiles are good models to study scaling because some species exhibit large body size range associated with growth, thus, allowing for ontogenetic comparisons. We used post hatch American alligators, Alligator mississippiensis, ranging from 0.12 to 6.80 kg (~ 60-fold) to investigate how both the right aortic arch (RAo) and the left pulmonary artery (LPA) change with Mb. We tested two possibilities: (i) wall thickness increases with Mb and normalizes wall tension, such that stress (stress = tension/thickness) remains unchanged; (ii) collagen content scales with Mb and increases arterial strength. We measured heart rate and systolic and mean pressures from both systemic and pulmonary circulations in anesthetized animals. Once stabilized alligators were injected with adrenaline to induce a physiologically relevant increase in pressure. Heart rate decreased and systemic pressures increased with Mb; pulmonary pressures remained unchanged. Both the RAo and LPA were fixed under physiological hydrostatic pressures and displayed larger radius, wall tension and thickness as Mb increased, thus, stress was independent from Mb; relative collagen content was unchanged. We conclude that increased wall thickness normalizes tension and reduces the chances of arterial walls rupturing in large alligators.

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Abbreviations

f H :

Heart rate

LPA:

Left pulmonary artery

M b :

Body mass

Pmpul :

Pulmonary mean arterial pressure

Pmsys :

Systemic mean arterial pressure

Pspul :

Pulmonary peak systolic pressure

Pssys :

Systemic peak systolic pressure

RAo:

Right aortic arch

r i :

Internal radius

T :

Arterial wall tension

W :

Arterial wall thickness

σ :

Arterial wall stress

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Acknowledgements

We thank Janna Crossley, Kevin Stewart, Amanda Reynolds, and Brandt Smith for caring of the alligators. Janna Crossley and Brandt Smith also helped during the experiments, and Andrea Bernardino-Schaefer provided microscopy and imaging support.

Funding

RF received a postdoctoral grant from São Paulo Research Foundation (FAPESP, process #2016/20158-6); BDD was financed by World Precision Instruments, LLC. and the UNT College of Science Seed Grant; BHD was financed by Tarleton State University Office of Research and Innovation; CACL had financial support from FAPESP (process #2018/05035-0); TW was supported by the Danish Council for Independent Research, Natural Sciences (Det Frie Forskningsråd | Natur og Univers, FNU). DAC II had financial support from National Science Foundation (NSF) and a Career Award IBN IOS-0845741.

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Authors

Contributions

RF, TW, CACL, and DAC conceived the study. RME provided resources and specimens. RF, BDD and BHD collected and analyzed the data. RF wrote the manuscript, and all the authors approved the final version of the manuscript.

Corresponding author

Correspondence to Renato Filogonio.

Additional information

Communicated by G. Heldmaier.

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Filogonio, R., Dubansky, B.D., Dubansky, B.H. et al. Arterial wall thickening normalizes arterial wall tension with growth in American alligators, Alligator mississippiensis. J Comp Physiol B 191, 553–562 (2021). https://doi.org/10.1007/s00360-021-01353-1

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  • DOI: https://doi.org/10.1007/s00360-021-01353-1

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