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

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.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

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

References

  1. Altimiras J, Franklin CE, Axelsson M (1998) Relationships between blood pressure and heart rate in the saltwater crocodile Crocodylus porosus. J Exp Biol 201:2235–2242

    CAS  PubMed  Google Scholar 

  2. Altimiras J, Lindgren I, Giraldo-Deck LM et al (2017) Aerobic performance in tinamous is limited by their small heart. A novel hypothesis in the evolution of avian flight. Sci Rep 7:15964. https://doi.org/10.1038/s41598-017-16297-2

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Alves AC, de Ribeiro CLDB, Cotrin JV et al (2016) Descrição morfológica do coração e dos vasos da base do jacaré-do-pantanal (Caiman yacare Daudin, 1802) proveniente de zoocriadouro. Pesqui Vet Bras 36:8–14. https://doi.org/10.1590/S0100-736X2016001300002

    Article  Google Scholar 

  4. Avery RA (1994) Growth in reptiles. Gerontology 40:193–199. https://doi.org/10.1159/000213587

    CAS  Article  PubMed  Google Scholar 

  5. Axelsson M, Franklin CE, Löfman CO et al (1996) Dynamic anatomical study of cardiac shunting in crocodiles using high-resolution angioscopy. J Exp Biol 199:359–365

    CAS  PubMed  Google Scholar 

  6. Azuma T, Oka S (1974) Circumferential tension in the wall of bent blood vessels. Microvasc Res 7:10–18. https://doi.org/10.1016/0026-2862(74)90033-8

    CAS  Article  PubMed  Google Scholar 

  7. Barnes PJ, Liu SF (1995) Regulation of pulmonary vascular tone. Pharmacol Rev 47:87–131

    CAS  PubMed  Google Scholar 

  8. Baudinette RV (1978) Scaling of heart rate during locomotion in mammals. J Comp Physiol B 127:337–342. https://doi.org/10.1007/BF00738418

    Article  Google Scholar 

  9. Bautista NM, Burggren WW (2019) Parental stressor exposure simultaneously conveys both adaptive and maladaptive larval phenotypes through epigenetic inheritance in the zebrafish (Danio rerio). J Exp Biol 222:jeb208918. https://doi.org/10.1242/jeb.208918

    Article  PubMed  Google Scholar 

  10. Campos R, Justo AFO, Jacintho FF et al (2019) Pharmacological and transcriptomic characterization of the nitric oxide pathway in aortic rings isolated from the tortoise Chelonoidis carbonaria. Comp Biochem Physiol Part C Toxicol Pharmacol 222:82–89. https://doi.org/10.1016/j.cbpc.2019.04.015

    CAS  Article  Google Scholar 

  11. Çeçen G, Topal A, Sacit O, Akgöz S (2009) The cardiopulmonary effects of sevoflurane, isoflurane and halothane anesthesia during spontaneous or controlled ventilation in dogs. Ank Üniv Vet Fak Derg 50:255–261. https://doi.org/10.1501/Vetfak_0000002291

    Article  Google Scholar 

  12. Cook AC, Tran V-H, Spicer DE et al (2017) Sequential segmental analysis of the crocodilian heart. J Anat 231:484–499. https://doi.org/10.1111/joa.12661

    Article  PubMed  PubMed Central  Google Scholar 

  13. Cox RH (1978) Comparison of carotid artery mechanics in the rat, rabbit, and dog. Am J Physiol Heart Circ Physiol 234:H280–H288. https://doi.org/10.1152/ajpheart.1978.234.3.H280

    CAS  Article  Google Scholar 

  14. Crossley DA, Hicks JW, Altimiras J (2003) Ontogeny of baroreflex control in the American alligator Alligator mississippiensis. J Exp Biol 206:2895–2902. https://doi.org/10.1242/jeb.00486

    Article  PubMed  Google Scholar 

  15. Dawson TH (2001) Similitude in the cardiovascular system of mammals. J Exp Biol 204:395–407

    CAS  PubMed  Google Scholar 

  16. Dingemans KP, Teeling P, Lagendijk JH, Becker AE (2000) Extracellular matrix of the human aortic media: an ultrastructural histochemical and immunohistochemical study of the adult aortic media. Anat Rec 258:1–14. https://doi.org/10.1002/(SICI)1097-0185(20000101)258:1%3c1::AID-AR1%3e3.0.CO;2-7

    CAS  Article  PubMed  Google Scholar 

  17. Dubansky BH, Dubansky BD (2018) Natural development of dermal ectopic bone in the American alligator (Alligator mississippiensis) resembles heterotopic ossification disorders in humans. Anat Rec 301:56–76. https://doi.org/10.1002/ar.23682

    Article  Google Scholar 

  18. Enok S, Slay C, Abe AS et al (2014) Intraspecific scaling of arterial blood pressure in the Burmese python. J Exp Biol 217:2232–2234. https://doi.org/10.1242/jeb.099226

    Article  PubMed  Google Scholar 

  19. Ferguson MWJ (1985) Reproductive biology and embryology of the crocodilians. Biology of the Reptilia, vol 14, Development A. Wiley, New York, pp 329–491

    Google Scholar 

  20. Filogonio R, Crossley DA II (2019) Long term effects of chronic prenatal exposure to hypercarbia on organ growth and cardiovascular responses to adrenaline and hypoxia in common snapping turtles. Comp Biochem Physiol A Mol Integr Physiol 234:10–17. https://doi.org/10.1016/j.cbpa.2019.04.009

    CAS  Article  PubMed  Google Scholar 

  21. Filogonio R, Taylor EW, Carreira LBT et al (2014) Systemic blood flow relations in conscious South American rattlesnakes. S Am J Herpetol 9:171–176. https://doi.org/10.2994/SAJH-D-14-00012.1

    Article  Google Scholar 

  22. Filogonio R, Wang T, Danielsen CC (2018) Analysis of vascular mechanical properties of the yellow anaconda reveals increased elasticity and distensibility of the pulmonary artery during digestion. J Exp Biol 221:jeb177766. https://doi.org/10.1242/jeb.177766

    Article  PubMed  Google Scholar 

  23. Filogonio R, Wang T, Abe AS, Leite CAC (2019) Cooling and warming rates are unaffected by autonomic vascular control in the South American rattlesnake (Crotalus durissus). S Am J Herpetol 14:242–249. https://doi.org/10.2994/SAJH-D-18-00013.1

    Article  Google Scholar 

  24. Filogonio R, Sartori MR, Mogensen S et al (2020) Cholinergic regulation along the pulmonary arterial tree of the South American rattlesnake: vascular reactivity, muscarinic receptors, and vagal innervation. Am J Physiol Regul Integr Comp Physiol 319:R156–R170. https://doi.org/10.1152/ajpregu.00310.2019

    CAS  Article  PubMed  Google Scholar 

  25. Galli GLJ, Skovgaard N, Abe AS et al (2007) The adrenergic regulation of the cardiovascular system in the South American rattlesnake, Crotalus durissus. Comp Biochem Physiol A Mol Integr Physiol 148:510–520. https://doi.org/10.1016/j.cbpa.2007.06.420

    CAS  Article  PubMed  Google Scholar 

  26. Greenfield JC, Griggs DM (1963) Relation between pressure and diameter in main pulmonary artery of man. J Appl Physiol 18:557–559. https://doi.org/10.1152/jappl.1963.18.3.557

    Article  PubMed  Google Scholar 

  27. Greenfield JC, Patel DJ (1962) Relation between pressure and diameter in the ascending aorta of man. Circ Res 10:778–781. https://doi.org/10.1161/01.RES.10.5.778

    Article  PubMed  Google Scholar 

  28. Hagensen MK, Abe AS, Wang T (2010) Baroreflex control of heart rate in the broad-nosed caiman Caiman latirostris is temperature dependent. Comp Biochem Physiol A Mol Integr Physiol 156:458–462. https://doi.org/10.1016/j.cbpa.2010.03.028

    CAS  Article  PubMed  Google Scholar 

  29. Holt JP, Rhode EA, Holt WW, Kines H (1981) Geometric similarity of aorta, venae cavae, and certain of their branches in mammals. Am J Physiol Regul Integr Comp Physiol 241:R100–R104. https://doi.org/10.1152/ajpregu.1981.241.1.R100

    CAS  Article  Google Scholar 

  30. Humphrey JD (2008) Mechanisms of arterial remodeling in hypertension: coupled roles of wall shear and intramural stress. Hypertension 52:195–200. https://doi.org/10.1161/HYPERTENSIONAHA.107.103440

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Joyce W, Miller TE, Elsey RM et al (2018) The effects of embryonic hypoxic programming on cardiovascular function and autonomic regulation in the American alligator (Alligator mississippiensis) at rest and during swimming. J Comp Physiol B 188:967–976. https://doi.org/10.1007/s00360-018-1181-2

    CAS  Article  PubMed  Google Scholar 

  32. Lima MO, Nóbrega YC, Santos MRD et al (2020) Notes on the gross anatomy of the heart of the broad-snouted caiman, Caiman latirostris (Daudin, 1802). Anat Histol Embryol. https://doi.org/10.1111/ahe.12636

    Article  PubMed  Google Scholar 

  33. MacDonald DJ, Finlay HM, Canham PB (2000) Directional wall strength in saccular brain aneurysms from polarized light microscopy. Ann Biomed Eng 28:533–542. https://doi.org/10.1114/1.292

    CAS  Article  PubMed  Google Scholar 

  34. Mulvany MJ, Aalkjaer C (1990) Structure and function of small arteries. Physiol Rev 70:921–961. https://doi.org/10.1152/physrev.1990.70.4.921

    CAS  Article  PubMed  Google Scholar 

  35. Nichols WW, O’Rourke MF, Vlachopoulos C (2011) McDonald’s blood flow in arteries: theoretical, experimental and clinical principles, 6th edn. CRC Press, Boca Raton

    Google Scholar 

  36. Poulsen CB, Wang T, Assersen K et al (2018) Does mean arterial blood pressure scale with body mass in mammals? Effects of measurement of blood pressure. Acta Physiol 222:e13010. https://doi.org/10.1111/apha.13010

    CAS  Article  Google Scholar 

  37. Prim DA, Mohamed MA, Lane BA et al (2018) Comparative mechanics of diverse mammalian carotid arteries. PLoS ONE 13:e0202123. https://doi.org/10.1371/journal.pone.0202123

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. Schmidt-Nielsen K (1984) Scaling: why is animal size so important? Cambridge University Press, Cambridge

    Google Scholar 

  39. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  40. Seldinger SI (1953) Catheter replacement of the needle in percutaneous arteriography: a new technique. Acta Radiol 39:368–376. https://doi.org/10.3109/00016925309136722

    CAS  Article  PubMed  Google Scholar 

  41. Seymour RS (1987) Scaling of cardiovascular physiology in snakes. Am Zool 27:97–109

    Article  Google Scholar 

  42. Seymour RS, Blaylock AJ (2000) The Principle of Laplace and scaling of ventricular wall stress and blood pressure in mammals and birds. Physiol Biochem Zool 73:389–405. https://doi.org/10.1086/317741

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. Seymour RS, Hu Q, Snelling EP, White CR (2019) Interspecific scaling of blood flow rates and arterial sizes in mammals. J Exp Biol 222:jeb199554. https://doi.org/10.1242/jeb.199554

    Article  PubMed  Google Scholar 

  44. Shadwick RE (1998) Elasticity in arteries: a similar combination of rubbery and stiff materials creates common mechanical properties in blood vessels of vertebrates and some invertebrates. Am Sci 86:535–541

    Article  Google Scholar 

  45. Smerup M, Damkjær M, Brøndum E et al (2016) The thick left ventricular wall of the giraffe heart normalises wall tension, but limits stroke volume and cardiac output. J Exp Biol 219:457–463. https://doi.org/10.1242/jeb.132753

    Article  PubMed  PubMed Central  Google Scholar 

  46. Smith B, Crossley JL, Elsey RM et al (2019) Embryonic developmental oxygen preconditions cardiovascular functional response to acute hypoxic exposure and maximal β-adrenergic stimulation of anesthetized juvenile American alligators (Alligator mississippiensis). J Exp Biol 222:jeb205419. https://doi.org/10.1242/jeb.205419

    Article  PubMed  Google Scholar 

  47. van Soldt BJ, Danielsen CC, Wang T (2015) The mechanical properties of the systemic and pulmonary arteries of Python regius correlate with blood pressures. J Morphol 276:1412–1421. https://doi.org/10.1002/jmor.20429

    CAS  Article  PubMed  Google Scholar 

  48. Vatner SF, Braunwald E (1975) Cardiovascular control mechanisms in the conscious state. N Engl J Med 293:970–976. https://doi.org/10.1056/NEJM197511062931906

    CAS  Article  PubMed  Google Scholar 

  49. Wagenseil JE, Mecham RP (2009) Vascular extracellular matrix and arterial mechanics. Physiol Rev 89:957–989. https://doi.org/10.1152/physrev.00041.2008

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  50. West GB, Brown JH, Enquist BJ (1997) A general model for the origin of allometric scaling laws in biology. Science 276:122–126. https://doi.org/10.1126/science.276.5309.122

    CAS  Article  PubMed  Google Scholar 

  51. Westerhof N, Elzinga G (1991) Normalized input impedance and arterial decay time over heart period are independent of animal size. Am J Physiol Regul Integr Comp Physiol 261:R126–R133. https://doi.org/10.1152/ajpregu.1991.261.1.R126

    CAS  Article  Google Scholar 

  52. White FN (1976) Circulation. Biology of the Reptilia 5, physiology A. Academic, New York, pp 275–334

    Google Scholar 

  53. White CR, Seymour RS (2014) The role of gravity in the evolution of mammalian blood pressure. Evolution 68:901–908. https://doi.org/10.1111/evo.12298

    Article  PubMed  Google Scholar 

  54. Wolinsky H, Glagov S (1967) A lamellar unit of aortic medial structure and function in mammals. Circ Res 20:99–111. https://doi.org/10.1161/01.RES.20.1.99

    CAS  Article  PubMed  Google Scholar 

Download references

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.

Author information

Affiliations

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

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by G. Heldmaier.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

Keywords

  • Arterial wall stress
  • Crocodilians
  • Law of Laplace
  • Scaling