Compressive Biomechanics of the Reptilian Intervertebral Joint

Authors

  • Kadi Fauble Department of Anatomy, Kirksville College of Osteopathic Medicine, A.T. Still University, Kirksville, MO, USA.
  • James Adams Department of Anatomy, Kirksville College of Osteopathic Medicine, A.T. Still University, Kirksville, MO, USA.
  • Maura Gerdes Department of Internal Medicine, Kirksville College of Osteopathic Medicine, A.T. Still University, Kirksville, MO, USA.
  • Caroline Vansickle Department of Anatomy, Kirksville College of Osteopathic Medicine, A.T. Still University, Kirksville, MO, USA.
  • Bruce A. Young Department of Anatomy, Kirksville College of Osteopathic Medicine, A.T. Still University, Kirksville, MO, USA.

DOI:

https://doi.org/10.30564/jzr.v2i4.2259

Abstract

This study compared the pre-sacral intervertebral joints of the American alligator (Alligator mississippiensis) with those from specimensof Varanus. These two taxa were chosen because they have similarnumber of pre-sacral vertebrae and similar body weights; however,Varanus can move bipedally and has diarthrotic intervertebral joints,whereas Alligator has intervertebral discs and cannot move bipedally.This study consisted of three objectives: (1) to document the anatomyof the intervertebral joint, (2) to quantify the compressive biomechanicsof the intervertebral joints and explore which features contributed tocompression resistance, and (3) to quantify the impact of compressionon the intervertebral foramen and spinal nerves in these two taxa. Theexperimental results revealed that the diarthrotic intervertebral jointsof Varanus were significantly (4x) stiffer than the intervertebral disc ofAlligator, and that a significant component of this increased stiffnessarose from the facet joints. Compressing the intervertebral joints of thetwo taxa caused a reduction in foraminal area, but the magnitude of thisreduction was not significantly different. We hypothesize that the mainfactor preventing spinal nerve impingement in Varanus during gravitational compression is the relatively small size of the spinal ganglion/nerve relative to the foraminal area.

Keywords:

Stress, Displacement, Intervertebral joint, Varanus, Alligator, Articular facet, Bipedalism

References

[1] Parrish JM. The Origin of Crocodilian Locomotion. Paleobiology, 1987, 13: 396-414.

[2] Bell G, Polcyn M. Dallasaurus Turneri, a New Primitive Mosasauroid from the Middle Turonian of Texas and Comments on the Phylogeny of Mosasauridae (Squamata). Neth J Geosci, 2005, 84: 177-194.

[3] Caldwell MW. From Fins to Limbs to Fins: Limb Evolution in Fossil Marine Reptiles. Amer J Med Genet. 2002, 112: 236-249.

[4] Motani R. The Evolution of Marine Reptiles. Evol Educ Out, 2009, 2: 224-235.

[5] Molnar J, Pierce S, Hutchinson J. An Experimental and Morphometric Test of the Relationship between Vertebral Morphology and Joint Stiffness in Nile Crocodiles (Crocodylus Niloticus). J Exp Biol, 2014, 217: 758-768.

[6] Molnar J, Pierce S, Bhullar B-A, Turner A, Hutchinson J. Morphological and Functional Changes in the Vertebral Column with Increasing Aquatic Adaptation in Crocodylomorphs. Roy Soc Open Sci, 2015, 2: 150439.

[7] Frey E. The Carrying System of Crocodilians - a Biomechanical and Phylogenetic Analysis. Stuttgart Beit Naturkund Biol, 1988, 426: 1-60.

[8] Hoffstetter R, Gasc J-P. Vertebrae and Ribs of Modern Reptiles. In - Biology of the Reptilia, Vol. 1, pp. 201-310. 1969, Academic Press, New York.

[9] Haines RW. The Development of Joints. J Anat, 1947, 81: 33-55.

[10] Werner YL. The Ontogenic Development of the Vertebrae in Some Gekkonoid Lizards. J Morphol, 1971, 133: 41-91.

[11] Taylor M, Wadel M. The Effect of Intervertebral Cartilage on Neutral Posture and Range of Motion in the Necks of Sauropod Dinosaurs. PLoS One, 2013. DOI: 10.1371/journal.pone.0078214

[12] Morinaga G, Bergmann PJ. Angles and Waves: Intervertebral Joint Angles and Axial Kinematics of Limbed Lizards, Limbless Lizards, and Snakes. Zoology, 2019, 134: 16-26.

[13] Persons WS, Currie PJ. The Functional Origin of Dinosaur Bipedalism: Cumulative Evidence from Bipedally Inclined Reptiles and Disinclined Mammals. J Theor Biol, 2017, 420: 1-7.

[14] Gauthier JA, Nesbitt SJ, Schachner ER, Bever GS, Joyce WG. The Bipedal Stem Crocodilian Poposaurus Gracilis: Inferring Function in Fossils and Innovation in Archosaur Locomotion. Bull Peabody Mus Nat Hist, 2011, 52: 107-126.

[15] Snyder RC. Adaptations For Bipedal Locomotion Of Lizards. Amer Zool, 1962, 2: 191-203.

[16] Schuett GW, Reiserer RS, Earley RL. The Evolution of Bipedal Postures in Varanoid Lizards. Biol J Linnean Soc, 2009, 97: 652-663.

[17] Currey J. Comparative Mechanical Properties and Histology of Bone. Amer Zool, 1984, 24: 5-12.

[18] Nicholson P, Cheng X, Lowet G, Boonen S, Davie M, et al., Structural and Material Mechanical Properties of Human Vertebral Cancellous Bone. Med Engin Physics, 1997, 19: 729-737.

[19] Blob RW, Snelgrove JM. Antler Stiffness in Moose (Alces alces): Correlated Evolution of Bone Function and Material Properties? J Morph, 2006, 267: 1075-1086.

[20] Leone A, Guglielmi G, Cassar-Pullicino VN, Bonomo L. Lumbar Intervertebral Instability: A Review. Radiology, 2007, 245: 62-77.

[21] Howarth SJ, Callaghan JP. Compressive Force Magnitude and Intervertebral Joint Flexion/Extension Angle Influence Shear Failure Force Magnitude in the Porcine Cervical Spine. J Biomech, 2012, 45: 484-490.

[22] Moon BR. Testing an Inference of Function from Structure: Snake Vertebrae Do the Twist. J Morph, 1999, 241: 217-225.

[23] Crock H. Normal and Pathological Anatomy of the Lumbar Spinal Nerve Root Canals. J Bone Joint Surg, 1981, 63B: 487-490.

[24] Jenis LG, An HS. Lumbar Foraminal Stenosis. Spine, 2000, 25: 389-394.

[25] Jensen K, Mosekilde L, Mosekilde L. A Model of Vertebral Trabecular Bone Architecture and Its Mechanical Properties. Bone, 1990, 11: 417-423.

[26] Goel VK, Ramirez SA, Kong W, Gilbertson LG. Cancellous Bone Young’s Modulus Variation Within the Vertebral Body of a Ligamentous Lumbar Spine-Application of Bone Adaptive Remodeling Concepts. J Biomech Engin, 1995, 117: 266-271.

[27] Haj-Ali R, Massarwa E, Aboudi J, Galbusera F, Wolfram U, et al., A New Multiscale Micromechanical Model of Vertebral Trabecular Bones. Biomech Model Mechanobiol, 2016, 16: 933-946.

[28] Hoffman B, Martin M, Brown BN, Bonassar LJ, Cheetham J. Biomechanical and Biochemical Characterization of Porcine Tracheal Cartilage. Laryngoscope, 2016, 126: E325-E331.

[29] Bae WC, Ruangchaijatuporn T, Chang EY, Biswas R, Du J, et al., Morphology of Triangular Fibrocartilage Complex: Correlation with Quantitative MR and Biomechanical Properties. Skel Radiol, 2015, 45: 447-454.

[30] Koike T, Wada H. Modeling of the Human Middle Ear Using Finite-Element Method. J Acoust Soc Amer, 2002, 111: DOI: 10.1121/1.1451073

[31] Barfuss D, Dantzler W. Glucose Transport in Isolated

[32] Perfused Proximal Tubules of Snake Kidney. Amer J Physiol, 1976, 231: 1716-1728.

[33] Han D, Young BA. The rhinoceros among serpents:

[34] Comparative anatomy and experimental biophysics of Calabar burrowing python (Calabaria reinhardtii) skin. J Morph, 2017, 279: 86-96.

[35] Luna, LG. Manual of Histological Staining Methods of the Armed Forces Institute of Pathology. 1968, McGraw-Hill, New York.

[36] Rho JY, Ashman RB, Turner CH. Young’s Modulus of Trabecular and Cortical Bone Material: Ultrasonic and Microtensile Measurements. J Biomech, 1998, 26: 111-119.

[37] Cortes DH, Jacobs NT, Delucca JF, Elliott DM. Elastic, Permeability and Swelling Properties of Human Intervertebral Disc Tissues: A Benchmark for Tissue Engineering. J Biomech, 2014, 47: 2088-2094.

[38] Zhang X, Gan RZ. Experimental Measurement and Modeling Analysis on Mechanical Properties of Incudostapedial Joint. Biomech Model Mechanobiol, 2010, 10: 713-726.

[39] Hashizume H, Akagi T, Watanabe H, Inoue H, Ogura T. Stress Analysis of PIP Joints Using the Three-Dimensional Finite Element Method. In - Advances in the Biomechanics of the Hand and Wrist. pp 237-244. 1994, Springer, New York.

[40] Fowler N, Nicol A. Interphalangeal Joint and Tendon Forces: Normal Model and Biomechanical Consequences of Surgical Reconstruction. J Biomech, 2000, 33: 1055-1062.

[41] Doube M, Klosowski MM, Wiktorowicz-Conroy AM, Hutchinson JR, Shefelbine SJ. Trabecular bone scales allometrically in mammals and birds. Proc Royal Soc B, 2011, 278: 3067-3073.

[42] Salisbury S, Frey E. A biomechanical transformation

[43] model for the evolution of semi-spheroidal articulations between adjoining vertebral bodies in crocodilians. In - Crocodilian Biology and Evolution. pp. 85-134. 2000, Surrey Beatty & Sons: Chipping Norton, UK.

[44] IiJima M, Kubo T. Comparative morphology of presacral vertebrae in extant crocodylians: taxonomic, functional and ecological implications. Zool J Linnean Soc, 2019, 186: 1006-1025.

[45] Fronimos JA, Wilson JA. Concavo-convex intercentral joints stabilize the vertebral column in sauropod dinosaurs and crocodylians. Ameghiniana, 2017, 54: 151-176.

[46] Sunderland S. Meningeal-Neural Relations in the Intervertebral Foramen. J Neurosurg, 1974, 40: 756-763.

[47] Stephens M, Evans JH, Oʼbrien JP. Lumbar Intervertebral Foramens. Spine, 1991, 16: 525-529.

[48] Wiltse LL, Fonseca AS, Amster J, Dimartino P, Ravessoud FA. Relationship of the Dura, Hofmannʼs Ligaments, Batsonʼs Plexus, and a Fibrovascular Membrane Lying on the Posterior Surface of the Vertebral Bodies and Attaching to the Deep Layer of the

[49] Posterior Longitudinal Ligament. Spine, 1998, 18: 1030-1043.

[50] Jagla G, Walocha J, Rajda K, Dobrogowski J, Wordliczek J. Anatomical Aspects of Epidural and Spinal Analgesia. Adv Pall Med, 2009, 8: 135-146.

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