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The spinal canal
The vertebrae, the IVD, and the ligaments delineate spinal canals in which the central nervous system (the cord, the nerves and nerve roots) and the arteries are inserted (Fig. 3) These channels include :
the central canal (also called vertebral foramen) that surrounds and protects the cord and the cauda equina. It is continuous, through the foramen magnum (cranial base), with the cranial cavity of the head and ends in the sacrum.
The root canals that surround and protect the roots, called the intervertebral foramina. They are formed on each side of the central canal, by the zygapophysial joint posteriorly and the intervertebral disc anteriorly, and by the vertebral notch on the pedicle above and below the foramen. It is a space surrounded by bone, ligaments ad cartilage. Pathology in the intervertebral foramina can affect the structures within these structures.
The description arteries and venous is briefly addressed in the manuscript. However, further details could be found in [Bosmia et al. 2015]. The spinal canal opens into the cranial cavity through the occipital foramen, or foramen magnum, and ends caudally, in a flute-like beak at the distal end of the sacral canal.
The spinal canal has a strategic role both from an anatomical point of view but also from a biomechanical point of view. The latter was developed in section 3.4.2 in this chapter.
Figure 3. Vertebral canal and central nervous system [from Gray’s Anatomy for Students, 4th Edition (2020)].
The spinal central nervous system
The spinal cord, which is located in the vertebral canal, is cranially continuous until the medulla oblongata of the brain stem and terminates caudally with a tapered inferior end of lumbosacral roots called the cauda equina (Fig. 5). In addition to the protection of the bony-ligamentous structure, the cord is well protected by the CSF and a group of membranes, collectively called the meninges. The spinal cord does not lie immediately adjacent to the bone and ligaments but it is separated from them by fluid, meninges, fat, subarachnoid trabeculae, denticulate ligaments and a venous plexus.
The spinal cord and brain develop from the same embryologic structure (the neural tube) and together they form the central nervous system (CNS). One end, the neural tube is encased in the skull, whereas the remainder of the neural tube is encased in the vertebral column, occupying about the upper two thirds of the vertebral spinal canal [Darby 2014]. The cord segments, delimited by the nerve roots, are not necessarily located at the same level as their corresponding vertebrae. The relationship between cord segments and vertebral levels is still unclear [Cadotte et al. 2014].
A transverse section of the spinal cord reveals regions of white matter that surround an inner core of gray matter (Fig. 4). The white matter of the spinal cord consists primarily of bundles of myelinated axons of neurons. Two grooves penetrate the white matter of the spinal cord and divide it into right and left sides. The gray matter of the spinal cord is shaped like a butterfly or the letter H; it consists of dendrites and cell bodies of neurons, unmyelinated axons, and neuroglia (Appendix – Fig. 20). The gray commissure forms the crossbar of the H. In the center of the gray commissure, there is a small space called the central canal [Tortora, 14th edition] ; it extends in the entire length of the spinal cord and encompasses an internal system of CSF cavities that include the cerebral ventricles, aqueduct of Sylvius, and fourth ventricle [Saker et al. 2016].
Figure 4. Functional and descriptive anatomy of the spinal cord (transverse antero- lateral view) [from Tortora, 14th edition].
The spinal cord has two principal functions: nerve impulse propagation and integration of information. The white matter tracts in the spinal cord are highways for nerve impulse propagation through axons of nervous fibres. Sensory inputs travels along these tracts toward the brain, and motor outputs travels from the brain along these tracts toward skeletal muscles and other effector tissues such as vital organs. The gray matter of the spinal cord receives and integrates incoming and outgoing information through the dendrite of the nervous fiber. Information are electrically propagated along a nervous fiber and transmitted to another nervous fiber by chemical exchanges of neurotransmitters at the synapse levels [Tortora, 14th edition].
For the CNS to respond to the environment it requires inputs from structures peripheral to the CNS and, in turn, a way to send output to structures called effectors. The sensory inputs begins in peripheral receptors found throughout the entire body in skin, muscles, tendons, joints, and viscera. These receptors send electrical currents (action potentials) toward the spinal cord of the CNS via the nerves that compose the peripheral nervous system (PNS). The sensory receptors respond to general sensory information such as pain, temperature, touch (pressure, vibrations), or proprioception (the perception of body position and movement). The PNS is also used when the CNS sends outputs to the body’s effectors, which are the smooth muscles, cardiac muscles, skeletal muscles, glands of the body and the vital organs. Thus, the PNS consists of the body’s peripheral nerves and is the way by which the CNS communicates with its surrounding environment [Darby 2014].
The white matter is organized within the SC into the following three parts: posterior, lateral, and anterior. Those fibers form tracts that eventually represent the components of sensory, motor, propriospinal, and autonomic pathways.
The blood supply to the SC is provided craniocaudally by one anterior and two posterior spinal arteries and horizontally by several radicular arteries originating at various levels, whereas the radicular arteries vascularize the ventral and dorsal roots. Originating from the fusion of the vertebral arteries, the anterior spinal artery, irrigated notably by the Adamkiewicz artery, is located within the pia mater in the median sulcus [Ganau et al. 2019]. Surrounding the arteries and veins, fluid channels called perivascular spaces provide a conduit between the cerebrospinal fluid (CSF) in the subarachnoid space and parenchymal interstitial fluid, facilitating solute transport and waste clearance [Thomas JH. 2019].
The mechanical role of the spinal cord was firstly addressed with its pathological involvement in the section 3.4.2. of this chapter 1. Its kinematics description was secondly developed in the chapter 2 from the literature review, and studied in the chapter 3. Finally, the mechanical properties of the spinal cord and the other structures described below composing the spinal central nervous system were described in the chapter 2 section 2.
The nerves and nerve roots
Spinal nerve roots provide functional and structural neural continuity between peripheral nervous system (PNS) and spinal cord. Also, these tissues differ in cellular composition, organization and function, and in amount of connective material. Due to the organization of the nerve roots as well as the nerves along the cord, they may be susceptible to be inflamed and damaged because of tensile or compressive forces from surrounding structural modifications such as disk herniation, foraminal stenosis and avulsion injuries. That could lead to demyelination and then cause pain, paresthesia (alteration of sensorial functions) and loss of motor control [Beel et al. 1986, Singh et al. 2006].
31 pairs of nerves roots called the spinal nerves attach to the spinal cord and communicate with structures primarily located in the neck, trunk, and extremities. These cord segments are numbered similarly to the numbering of the spinal nerves: 8 cervical, 12 thoracic, 5 lumbar, 5 sacral, and 1 coccygeal cord segment (the first seven cervical nerves exit the intervertebral foramen (IVF) above their corresponding vertebra, and the remaining nerves exit below their corresponding vertebra. This allows one more cervical spinal nerve than cervical vertebrae (Fig. 5).
A spinal nerve is composed by the unification of two roots within the IVF (Fig 4). On one hand, the dorsal roots contain fibers of various diameters and conduction velocities that convey all types of sensory information. On the other hand, the ventral roots contain axons of motor neurons which conduct nerve signals from the CNS to muscles or glands. As the roots approaches the spinal cord within the vertebral canal, it divides into approximately six to eight dorsal rootlets, or filaments. These rootlets attach in a vertical row to the cord’s dorsolateral sulcus (i.e. a groove in Latin) [Tortora, 14th edition].
The meninges
This section was inspired by [Reina et al. 2020, Gassner et al. 2017, Sakka et al. 2016].
The meninges are concentric connective tissue layers wrapping the central nervous system from the caudal side with the filum terminale to the cranial side with the brain. They have morphologies and physiologies which are involved in immunologic, trophic, metabolic, thermal and biomechanical protection of the spinal cord. They begin into the radially inner direction after the osteofibrous wall of the vertebral canal and the epidural space, filled by a loose connective tissue (extracellular matrix) and epidural fat. Their locations protect the spinal cord from the potential injuries related to the movements of the vertebral column. The epidural fat, the internal vertebral venous plexus and the cerebrospinal fluid (CSF) between meninges behave as the mechanical cushion probably acting as a damping element between the spinal cord and the bone enclosure. Then, the mechanical properties of the spinal meninges were more deeply studied by mechanical testing approaches in the chapter 4.
The meninges are categorized in four main tissues organized from the outermost layer to the innermost layer : the dura mater, the arachnoid mater forming the dural sac, the pia mater and the denticulate ligaments which are the bridges between the pia and the arachnoid maters.
The dura mater
It is a sheath described as a white, thick, and resistant membrane formed by a dense connective tissue poorly vascularized. Cranially, the spinal dura mater begins and is fixed at the foramen magnum.
Caudally, the dural sheath wrapped the spinal cord, the spinal nerve roots and contracts into the filum terminale.
The dura mater forms 90 % of the outer layer of the dural sac. This fibrous structure, although permeable, forms a mechanical barrier. The dura mater thickness varies along the spinal cord. Dura mater is comprised of concentric dural laminas containing a ratio collagen fibers (collagen do not seem to have been clearly identify) on elastin fibers which varies radially [Chauvet et al. 2010]. No consensus about the fibers’ organization was highlighted by the literature in an histological point of view. On one side, papers showed a distribution of fibers at randomly distributed in all spatial directions (Fig. 6) [Reina et al. 2020, 1997] and on other side, papers showed a predominantly longitudinally orientation [Patin et al. 1993, Chauvet et al. 2010] (all human specimen). The biomechanical literature tends to confirm the longitudinal fiber orientation as mechanical characterization experiments showed a greater longitudinal tensile stiffness compared to transverse stiffness.
The arachnoid mater
The arachnoid mater can be described as an outer layer attached to the dura mater by thin fibers of collagen so that there is no subdural space (Fig. 7). The remaining internal 10% of the dural sac is formed by the arachnoid layer and consists in a thin transparent membrane forms of several cell layers and mainly composed of collagen and elastin fibers. The arachnoid is semi-permeable and regulates the passage of substances through the dural sac [Reina et al. 2008].
The arachnoid mater is attached to the pia via a framework of fine connective trabeculae and is connected to an inner layer by the septum posticum of Schwalbe to bridge the subarachnoid space (in the dorsal direction of the median sulcus of the SC). The trabecular arachnoid surrounds the structures inside the subarachnoid space, including spinal cord, nerve roots, and blood vessels that are scattered within the space. These easily cuttable attachments are called arachnoid trabeculae [Sakka et al. 2016, Mortazavi et al. 2017], sheet-like trabeculae [Adeeb et al. 2013] or leptomeningeal layer[Gassner et al. 2017].
The pia mater
The spinal pia mater is described as a thin tissue closely adhering to the spinal cord glia limitans or subpial layer, which covers the outer surface of the spinal cord and is situated immediately subjacent to the pia mater. The glia limitans is a dynamic structure of exchange between the CSF and the cord (Fig 8). Cranially, the spinal pia mater continues the cranial pia mater at the foramen magnum. Below the conus terminalis, it forms a thin tubular ligament, the filum terminale. The spinal pia mater is composed of mainly longitudinally orientated collagen fibers, in which is embedded carry larger branches of the spinal vasculature. The morphology of the pia mater differs between spinal and cranial location; the spinal pia mater is thicker, more compact, and less vascular.
The subpial compartment has large amounts of collagen fibers, a few elastin fibers and, fibroblasts, and a small number of macrophages as well as blood vessels. The subpial compartment is enclosed between the pial cellular layer and a basal membrane that is in contact with neuroglial cells on the spinal cord side and separates the CSF from the spinal cord. The orientation of fibers was not clearly proved and no study showed a preferential uni-axial direction from a mechanical point of view for human subjects. Moreover, most of the above considerations were observed at the lumbar spinal level.
Figure 8. A – Pia mater. Human spinal pia mater at spinal cord level. Scanning electron Microscopy, magnification: x300. B – Natural fenestration within human spinal pia mater at spinal cord level. Scanning electron microscopy, magnification: x2000. [From Reina et al. 2020]. C – Fraction of the pial cellular layer, presumably detached during dissection. Subpial tissue with collagen fibers is placed between the pial layer and spinal cord. The space seen between the pial layer and the subpial tissue is an artifact. The “D” arrow marks the area that has been magnified in D. Scanning electron microscopy, magnification: x70. D – Pial cellular layer. The arrows delimit the pia mater thickness. Scanning electron microscopy, magnification x 500. [From Reina et al. 2002].
The subarachnoid space, also named perimedullar space at the level of the spinal cord, occupies the space between the arachnoid and pia maters. It fills around a third of the vertebral canal. The subarachnoid space contains cerebrospinal fluid and extracellular collagen and fibroblasts.
The denticulate ligaments
The denticulate ligaments (DL) or subarachnoid ligaments have a similar composition to arachnoid trabeculae, although they are composed of more collagen fibers and are therefore more resistant to mechanical forces. The denticulate ligaments have been shown histologically to consist of thick collagenous bundles that merge medially with subpial collagen and laterally are attached to the spinal dura mater (Fig. 9). The narrow fibrous strip portion of the DL consisted of longitudinal collagen fibers whereas the triangular extensions featured transverse and oblique collagen fibers. Collagen fibers were thicker and more abundant in the cervical DL than in the thoracic DL.
The DL have a biomechanical role of stabilization of the spinal cord in the dural sac due to their mechanical properties in tension [Polak et al. 2019, 2014, Ceylan et al. 2012, Tubbs et al. 2001]. Indeed, DL were more resistant when stress was applied to the cord in the caudal as opposed to cranial direction. The DL in the cervical region were strongest, and their strength decreased with respect to the lower spinal levels. They are less able to resist anteriorly directed forces as the cord descends and overall, inferior to T8, the cord was shown to come into contact with the anterior spinal canal before the denticulate ligaments tie [Ceylan et al. 2012, Tubbs et al. 2001].
The number of DL range from 18 to 21 dentate ligaments at each side of the spinal cord [Ceylan et al.2012, Reina et al. 2020]. They are mainly located in the cervical and thoracic regions (ending around T12) of the spine.
The apex (i.e. the tip of a pyramidal/triangular structure) attached craniomedially to the dura mater to the intervertebral foramen of the vertebrae at the spinal level below. Each DL is laterally attatched to the pia mater between the ventral and dorsal roots of the spinal nerves. Each ligament had lateral triangular extensions oriented perpendicular to the long axis of the vertebral column.
The amount of space between them differed according to spinal level and the distance from the dural attachment site to the intervertebral foramen increased according to such level from upper to lower levels of the spine. The dural attachments of the ligament were not always bilaterally symmetrical.
The anatomy and histology of DL correspond with the motion capacity of each different region of the vertebral column. Indeed, due to a high mobility of the cervical segment, the DL in that region have to allow the necessary motion of the cervical portion of the spinal cord within the canal. The direct apical attachments at the thoracic levels may reflect the lower mobility of vertebrae in that region of the spine. No presence of DL was reported was reported in the lumbar region [Ceylan et al. 2012].
Finally, the DL are clinically significant reference markers as they divide the spinal canal into anterior and posterior compartments[Ceylan et al. 2012].
Figure 9.The denticulate ligaments. A – The spinal attachments of the DL. The DLs are attached to the spinal cord by loose connective tissue throughout the length of the spine. At cervical levels (*), there were also collagen fibers penetrating the substance of the spinal cord at various intervals, creating a firmer attachment. Magnification ×10 (DL: denticulate ligament, SC: spinal cord, CT: connective tissue). B – a and b Histological structure of the DL. The DLs were composed of collagen fiber bundles. The narrow fibrous strip portion (*) of the DL consisted of longitudinal collagen fibers, whereas the triangular extensions (**) featured transverse and oblique collagen fibers. a) Magnification ×10, b) magnification ×20. (D L: denticulate ligament, CT:connective tissue) [From Ceylan et al. 2012].
The porcine model
The porcine model (Fig. 10) becomes a preferential model for spine research [Kim et al.2019, Brummund et al. 2017, Fradet et al. 2016b, Swnindel et al. 2013] due to a high similarity with the human species. Indeed, the genetic, anatomical [Fig. 1.7], physiological, pathophysiological [Schomberg et al. 2017], histological [Kinaci et al. 2020], biomechanical (in particular in term of ROM of the upper cervical, upper and middle thoracic sections) [Wilke et al. 2011] of this quadruped makes the best transversal models for human research, next to non-human primates[Schomberg et al. 2017].
Biomechanical characteristics, physiology, motion and pulsation of the CSF system
The dynamics and physiology of the cerebrospinal fluid need to be deeply understood to investigate many traumatic or degenerative axonal diseases such as spinal cord injuries [Kwon et al. 2016], Alzheimer’s disease [Hansson et al. 2019], cerebral malaria [Datta et al. 2019] or migraine [Van Dogen et al. 2017], and also to develop potential high impact solution as intrathecal drug delivery [Fowler et al. 2020].
Characteristics and physiology of CSF
Cerebrospinal fluid has an estimated total volume ranging from 250 to 400 mL in adult humans, with a ratio of ¾ in the intracranial part. It renews itself 3 to 4 times a day. The CSF motion is mainly located within the intracranial space (cortical subarachnoid space, cisterns and ventricles) and the spine (spinal subarachnoid space).
This fluid serves several physiological functions such as :
– structural protection [Fradet et al. 2016a, Persson et al. 2011], acting as a damping element.
– mechanical regulation (intracranial pressure/compliance) to adapt to sudden fluctuations caused by obstruction of venous outflow and/or expanding mass lesion [Garnotel et al. 2017, Marmarou et al. 1975].
– metabolic homeostasis of the CNS, by providing nutrients to neural and glial cells, to eliminate metabolic wastes (neurotoxic wastes products, neurotransmitters, hormones, etc …) due to the activities of these cells [Sakka et al. 2011]
– immunological support of the CNS [Villar et al. 2014].
Circulation of the cerebrospinal fluid
There is no consensus in the literature regarding the circulation of CSF. Two hypothesis emerges from the literature : a classical one developed for more than one hundred years and a more recent hypothesis dating from ten years.
According the first hypothesis, CSF is produced by the epithelial cells of the choroid plexus of the brain ventricles and flows from the lateral ventricles through the foramina of Monro to the third ventricle. From there, the CSF flows through the aqueduct of Sylvius into the fourth ventricle. CSF exits the ventricular system through the median aperture (also called foramen of Magendie) and the two lateral apertures of Luschka, and enters the cisterns surrounding the cerebellum in the inferior cranial SAS. The CSF bulk flow continues to move superiorly and inferiorly to the cranial and spinal SAS, respectively (Fig. 11). The bulk flow is driven by a dynamic combination between CSF secretion, absorption and resistance to flow [Sakka et al. 2011]. Thus, CSF pressure is maintained by equalization of the rates of CSF secretion and reabsorption. Changes in CSF pressure can occur rapidly when the rates of CSF secretion and reabsorption are not balanced, leading to cranial SAS volume gain such as hydrocephalus [Simon and Iliff 2016].
Table of contents :
Chapter 1 – Anatomy
1.The spine and the spinal canal
2.Biomechanical characteristics, physiology, motion and pulsation of the CSF system
3.Clinical and biomechanical contexts
Chapter 2 – Literature Review
1.Studying cervical spinal canal morphometry
2.Studying mechanical properties of the mechanical properties of the CNS and the CSF
3.Studying the CSF flow and the central nervous system modelling
Chapter 3 – Morphometry of the human cervical canal
1.Cervical canal morphology : effects of neck flexion in normal conditions – New elements for Biomechanical simulations and surgical management
2. Degenerative cervical myelopathy morphology : effects of decompressive surgery by laminectomy -New elements for patient follow-up
3. References
Chapter 4 Mechanical properties of spinal porcine meninges
1. Tensile Mechanical Properties of the Cervical, Thoracic and Lumbar Porcine Spinal Meninges
2. Experimental Bi-axial Tensile Tests of Meningeal Tissues and Constitutive Models Comparison
3. References
Chapter 5 – Towards fluid-structure modelling
1. Mathematical background
2. Monolithics FSI modelling investigation in RADIOSS
General conclusions and perspectives
1. Main results and limitations
2. Perspectives
3. References – Chapter 5 and General conclusions and perspectives
