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Craniocervical junction

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Myofascial attachments to the dura mater in the craniocervical junction

The dura mater receives myofascial attachments in the craniocervical junction from: 

  • Myodural bridges (Scali et al 2013): bands of fascia crossing the epidural space link the suboccipital muscles and the dura mater. This suboccipital fascia is continuous with the galea aponeurotica (Dacey et all 2018). Myodural bridges reach the dura via the PAO membrane from the Rectus Capitis Posterior Minor (RCPMi) and via the atlantoaxial interspace from the Rectus Capitis Posterior Major (RCPMa), Obliquus Capitis Inferior (OCI) and the Nuchal Ligament (NL). Zheng et al (2019) described the vertebrodural ligaments (refer below) as the final common pathway for the myodural bridge (RCPMa, OCI & NL) in the posterior atlanto-axial interspace.

The myodural bridges may function in: (i) protect the spinal cord from dural enfolding (ii) transmission of proprioception from the spinal dura (iii) allows the suboccipital muscles to exert a reflexive myostatic response in placing the dura under tension (iv) myodural biofeedback might participate in maintaining the integrity of the subarachnoid space and posterior cerebellomedullary cistern (iv) these muscles exert a pumping effect by deforming the dura providing an important force required to move CSF in the spinal canal (Zheng et al 2014 & Xu et al 2016). Xu et al (2016) found CSF circulation at the craniocervical junction is significantly propelled in a cranial direction by head rotations attributed to the effects of these muscles on the dural sac (as well as changes in heart rate and respiratory rate).

  • Posterior atlanto-occipital membrane (PAO): The PAO membrane extends between the posterior arch of C1 and the occiput. Connective tissue fibres create a PAO membrane-spinal dura complex (Nash et al 2005). 

    The PAO membrane is mainly formed by the rectus capitis posterior minor tendinous fibers, the deep layer of the rectus capitis posterior minor fascia, and arterial and venous perivascular connective tissue sheathes. The rectus capitis posterior minor attaches to the dura indirectly via the PAO (Zheng et al 2019).

The PAO attachments are:

Laterally: the membrane extends between the rectus capitis posterior minor tendon (or aponeurosis) --> vertebral artery and vertebral cavernous sinus vascular sheath. Via the vascular sheath this membrane was continuous with the spinal dura.

Medially: can not be identified but was formed from the rectus capitis posterior minor fascia and the perivascular sheathes of vertebral venous vessels.

Inferiorly: fuses with the spinal dura and the perivascular sheath of the internal vertebral plexus.

Superiorly: continues with the deep layer of the rectus capitis posterior minor fascia fusing to the occiput.

  • First (intracranial) denticulate ligament: its attachments extend from (lateral): outer layer of the dura mater of the marginal sinus at the foramen magnum --> pierces the posterior atlantooccipital membrane and dura mater --> (medial): spinomedullary junction (Tubbs et al 2011).
  • Epidural ligaments (of Hoffman): dura mater (dural sac and dural extension of the nerve root sleeve) --> posterior longitudinal ligament, the vertebral canal and the ligamentum flavum (Tardieu et al 2016).
  • Dorsal meningodural ligaments (Shi et al 2014): connective tissue bands running mainly from the ligamentum nuchae but also the laminae to the posterior dural (thecal) sac. Most commonly from C5 up with the strongest attachments being at C1-C2. They only exist in the cervical spine.
  • Vertebrodural ligaments include the verterebrodural ligament (VDL), to be named ligament (TBNL) and the craniale durae matris spinalis (CDMS) (Zheng et al 2014). Even though they are described seprarately all the vertebrodural ligaments are anatomical and functional linked with each other and the myodural bridges. Zheng et al (2019) described the VDL as the final common pathway for the myodural bridge (RCPMa, OCI & NL) in the posterior atlanto-axial interspace:

i. Vertebrodural ligament: connects C1-2 ligamentum nuchae and posterior wall of the C1 & C2 vertebral canal to the cervical dura mater. The dura mater is distinctly thick at the VDL insertion. 

VDL subdivided into three parts: Superior portion: C1: posterior arch of the atlas. Middle portion (TBNL’s part): C1-2 interspace. It is continuous with the TBNL. Inferior portion (axial part): C2 lamina. It is continuous with the TBNL which adheres to the lamina. 

Suboccipital myodural bridge becomes part of the VDL as it passes through the atlantoaxial interspace.

ii. TBNL: local enhancement of the ligamentum nuchae that forms part of the myodural bridge. It enters the epidural space through the atlanto-axial interspace and terminates at the posterior cervical spinal dura mater.

Posterior border of ligamentum nuchae* --> atlantoaxial interspace --> C1-2 dura mater.

*: Ligament nuchae attachments of the TBNL are: main attachment is below C3 SP at the common origins of the splenius capitis, superior posterior serratus and rhomboid minor muscles. Also attaches to the C2 SP.

As well as its more indirect muscular attachments at C3 it receives direct attachments from the rectus capitis posterior minor, rectus capitis posterior major and obliquus capitis inferior (Yuan et al 2017). 

Zheng et al (2014) speculated that cervical flexion draws the cervical dura mater posteriorly creating a bulge via the TBNL and VDL passage through the atlantooccipital interspace.

iii. Ligamentum craniale durae matris spinalis (CDMS): continuous with the deep part of the ligamentum nuchae.

Edge of the foramen magnum, the posterior border of the O/A joints, nuchal ligament posterior arch of the atlas, and the arch of the axis --> cervical dura.

Superior attachments of the suboocipital fascia comes from the galea aponeurotica. Dacey et al (2018) found the galea aponeurotica transitions to the suboccipital fascia by dense fibrous attachments. Therefore we have myofascial continuity from Tenon's capsule running posteriorly via the occipitofrontalis to the galea aponeurotica/suboccipital fascia terminating in the upper cervical complex.

Venous return at the craniocervical junction

At the craniocervical junction the internal vertebral venous plexus communicates with:

  • Occipital-marginal sinus.
  • Condylar veins: posterior condylar emissary vein and anterior condylar (venous plexus of the hypoglossal canal), lateral condylar vein.
  • Other emissary vein: occipital and mastoid (Ruiz et al 2002).
  • Anterior condylar confluent external to the hypoglossal canal to the posterior cranial fossa and internal jugular vein. 

Cervical kyphosis causes the internal jugular vein to bend around the transverse process of atlas. This reverses its normal course, as well as potentially compressing the vein which increases the resistance to blood flow.

Therefore malformations and misalignments of the craniocervical junction may play a role in chronic ischemia and oedema, which may in turn lead to neurodegenerative processes and subsequent diseases (Flanagan 2015). Mandolesi et al (2015) found an anterolisthesis between the first two cervical vertebral bodies is greater than two-fold in patients with MS rather than in those without neurologic disease.

Haemodynamics of the vertebral venous plexus, marginal sinus and internal jugular vein

Venous outflow from the cranial cavity is mainly through the internal jugular veins (Urakov et al 2015). However there seems to be reciprocal relationship between the internal jugular venous flow from the head and the marginal sinus-verterbral venous flow.

The internal jugular vein has a valve just above the termination of the internal jugular vein. It is the only valve between the heart and the brain and prevents the cephalic flow of venous blood. This valve permits an increase in intrathoracic pressure from shooting blood up to the brain and therefore increasing intracranial pressure (Silva et al 2002).

Because of this valve drainage in the internal jugular vein isn’t as dependent on a pressure gradient. By contrast the dural sinuses, facial veins, and vertebral veins have no valves. This means the direction of venous blood flow is determined by hydrostatic pressure gradients.

The internal jugular veins are the major cerebral venous outflow pathway that is not reliant on a pressure gradient e.g. when supine. The vertebral venous plexus is the major cerebral venous outflow pathway that is reliant on a pressure gradient e.g. when standing. Both the vertebral and internal jugular vein show twice the outflow when supine than sitting (Ciuti et al 2013).

When supine, with head elevation, overall there is a a decreased venous pressure toward the head. This becomes zero above the heart or even negative where the veins do not collapse. Accordingly, there is a point or a level, where pressure remains independent of posture, referred to as the hydrostatic indifference point. This point is located a few centimetres below the diaphragm (Peterson et al 2014).

Even though there is an overall decrease in venous pressure with supine head elevation there is a relative decrease internal jugular venous flow (Urakov et al 2015) and corresponding increase in vertebral vein flow (Tobinick 2017). This is because with head elevation the internal jugular vein bends around the TP of C1, reversing its normal course, as well as potentially compressing the vein (Flanagan 2015).

When standing the pressure gradient produced means the major cerebral outflow pathway is from the dural sinuses into the vertebral venous plexus (Valdueza et al 2000 & Gisolf et al 2004). 

However when performing a standing valsalva manoeuvre the internal jugular veins are opened without increasing vertebral venous drainage. This is because the increases intraabdominal pressure redirects venous blood from the body cavities to vertebral venous plexus. By clogging up this drainage route with diverted venous blood from the thoracic and abdominal cavities the body opens up the internal jugular venous pathway (Gisolf et al 2004).

Fricke et al (2001) found receptors in the dural sinuses and internal jugular bulb that may measure volume changes in the cranial vascular system supporting autonomic reflexes to control intracranial blood flow and volume.

The jugular bulb is located at the jugular foramen. It is the connection between the sigmoid sinus and internal jugular vein. The myofascial connections of this area are discussed below. Could direct manipulation of myofascial tension andfblood flow through the internal jugular vein produce a therapeutic neurological reflex?

Venous pressure and CSF production and absorbtion

Passive production of CSF occurs during upright posture which decreases venous pressure in the vertebral veins and dural sinuses:

A decrease venous pressure in the superior sagittal sinus means the venous sinus has greater capacity to absorb CSF into it from the subarachnoid space. This increase flow of CSF out of the brain via the dural sinus decreases intracranial CSF volume. To address this reduced CSF volume additional blood gets drawn from the choroid plexus to produce more CSF to make up for that that has been lost. This is called passive production of CSF (Flanagan 2015).

Superior sagittal sinus venous pressure and flow is affected by posture, respiration, and movement. It is also affected by downstream pressure in the internal jugular and vertebral veins.

Therefore to maintain constant intracranial pressure there is a balance between the influx of fluid into and out of the cranium:

DECREASE INTRACRANIAL PRESSURE: increase venous outflow (decreases venous pressure) --> increase CSF absorbtion --> INCREASE INTRACRANIAL PRESSURE: increase arterial inflow --> increase CSF production.

INCREASE INTRACRANIAL PRESSURE: decrease venous outflow (increases venous pressure) --> decrease CSF absorbtion --> DECREASE INTRACRANIAL PRESSURE: decrease arterial inflow --> decrease CSF production.

Myofascial anatomy of the internal jugular vein, internal carotid artery, vertebral artery and the jugular foramen

Rectus capitis lateralis (Cohen et al 2016)

  • Origin and insertion.

C1 TP --> occiput: jugular process. 

Kulkarni et al (2001) found these muscles have a high proprioceptive content. These authors disputed their primary role as ipsilateral sidebenders of the head and instead allocated their function to primarily being proprioceptive.

  • Vascular relations

The rectus capitis lateralis covers the posterior aspect of the opening of the jugular foramen. Its anterior border fuses with the posterior wall of the carotid sheath at the midportion of this muscle.

The origin of the rectus capitis lateralis on the C1 TP overlays the C1 foramen transversarium, where the vertebral artery exits the TP to enter the dura.

Extracranial neurovascular compartment of the upper retrostyloid parapharyngeal space

The extracranial neurovascular compartment of the upper retrostyloid parapharyngeal space is a transitional space between the intracranial aspect of the jugular foramen and the cervical carotid sheath. It is traversed by the structures exiting the jugular foramen.

The compartment to be bounded by the:

  • Medially: occipital condyle.
  • Laterally: styloid process.
  • Posteriorly: rectus capitis lateralis.
  • Superiorly: jugular foramen.
  • Inferiorly: carotid sheath.

Condylar triangle

Condylar triangle:

  • Anterior: rectus capitis lateralis.
  • Posterior: superior oblique.
  • Superior: a line connecting these muscles along the occipital bone superiorly.

Contains the superior segment of the vertebral artery as it exits the C1 foramen transversarium and bends posteriorly toward the atlantooccipital membrane.

Fascial relations to the internal jugular vein and internal carotid artery

The relationship of the rectus capitis lateralis to the carotid sheath has already been described with its anterior border fusing with the posterior wall of the carotid sheath (Cohen et al 2016).

Komune et al (2019) identified the fascial attachments to the cranial base.

These authors found at the cranial base a complex fascial network around the internal jugular vein and the internal carotid artery.

This network is made up from:

  • Prevertebral fascia: fascia of the longus capitis and rectus capitis lateralis.
  • Middle layer of the deep cervical fascia: tensor-vascular styloid fascia.
  • Stylopharyngeal fascia.
  • Deep cervical fascia: carotid sheath. The carotid sheath attaches anteriorly and laterally to the vaginal process (temporal bone) and posteriorly to the fibrocartilaginous tissue around the jugular foramen (temporal bone) and carotid canal (occipital/temporal bone).

Bordoni (2020) found the fascial network of the internal carotid artery to merge with the:

  • Tensor-vascular styloid fascia: inferior border of the tensor veli palatini --> styloid process and muscles.
  • Fascia of the digastric muscle.
  • Interpterygoid fascia: extends between the pterygoid muscles sometimes reflecting onto the deep surface of the temporalis. It's pierced by the auriculotemporal nerve (Barker and Davies 1972) and merges with the main muscle of the tongue (styloglossus) and with the fascial system of the internal carotid artery (Bordoni 2020). Its attachments are (Barker and Davies 1972):

i. Superiorly: cranial base at the sphenoid and temporal bone (Bordoni 2020 & Komune et al 2019) and the suture between the palatine and sphenoid (Lang 2001). Maxilla (Lang 2001) 

ii. Posteriorly: extends between the lateral and medial pterygoid muscles.

iii. Inferiorly: mandible from above the upper border of medial ptcrygoid insertion extending backwards to the neck of the condyle. Here it blends with the stylomandibular fascia.

Forms the sphenomandibular ligament (spine of sphenoid --> mandible: lingula of the mandibular foramen).

iv. Anteriorly: the fascia is usually flimsy but it may be reflected to form a septum between the pterygoids and the fascia on the deep surface of the temporalis muscle. This is called temporopterygoid fascia.

In addition to the preverterbal fascia vascular relations in forming a fascial network around the internal jugular vein and internal carotid artery there are also relations to the vertebral artery.

The triangle of the vertebral artery is formed lower down where the prevertebral fascia splits between the longus colli and scalene anterior.

References

The Craniocervical Venous System in Relation to Cerebral Venous Drainage (2002). Diego San Millán Ruíz, Philippe GailloudDaniel A. RüfenachtJacqueline DelavelleFrank Henry and Jean H.D. Fasel

The Role of the Craniocervical Junction in Craniospinal Hydrodynamics and Neurodegenerative Conditions (2015). Michael F. Flanagan

C1-C2 X-Ray assessment of misalignment parameters in patients with Chronic Cerebra-spinal Venous Insufficiency and Multiple Sclerosis versus patients with other pathologies (2015). Mandolesi SMarceca Gd'Alessandro ADesogus ACiccone MMZito AManconi ENiglio TMandolesi Dd'Alessandro AFedele F.

The dynamics of changing internal jugular veins diameter based on increasing head elevation angle (2015). Aleksandr L. UrakovAnton A. Kasatkin, and Anna R. Nigmatullina

The internal jugular vein valve may have a significant role in the prevention of venous reflux: evidence from live and cadaveric human subjects (2002). Silva MADeen KIFernando DJSheriffdeen AH.

Differences between internal jugular vein and vertebral vein flow examined in real time with the use of multigate ultrasound color Doppler (2013). Ciuti G, Righi DForzoni LFabbri APignone AM.

The Hydrostatic Pressure Indifference Point Underestimates Orthostatic Redistribution of Blood in Humans (2014). L G PetersenJ F CarlsenM B NielsenM DamgaardN H Secher

The dynamics of changing internal jugular veins diameter based on increasing head elevation angle (2015). Aleksandr L. UrakovAnton A. Kasatkin, and Anna R. Nigmatullina

The Cerebrospinal Venous System: Anatomy, Physiology, and Clinical Implications (2017). Edward Tobinick

Postural dependency of the cerebral venous outflow (2000). Valdueza JMvon Münster THoffman OSchreiber SEinhäupl KM.

Human cerebral venous outflow pathway depends on posture and central venous pressure (2004). Gisolf J, van Lieshout JJvan Heusden KPott FStok WJKaremaker JM.

Nerve Fibers Innervating the Cranial and Spinal Meninges: Morphology of Nerve Fiber Terminals and Their Structural Integration (2001) BRITTA FRICKE, KARL HERMANN ANDRES, AND MONIKA VON DU¨ RING

The rectus capitis lateralis and the condylar triangle: important landmarks in posterior and lateral approaches to the jugular foramen (2016). Michael A. Cohen, Alexander I. Evins , Gennaro Lapadula , Leopold Arko , Philip E. Stieg and Antonio Bernardo

Quantitative study of muscle spindles in suboccipital muscles of human foetuses (2001). Kulkarni V, Chandy MJ, Babu KS

The Fascial Layers Attached to the Skull Base: A Cadaveric Study (2019). Komune N, Matsuo S, Nakagawa T.

The Five Diaphragms in Osteopathic Manipulative Medicine: Myofascial Relationships, Part 1 (2020). Bruno Bordoni

Investigation of meningomyovertebral structures within the upper cervical epidural space: A sheet plastination study with clinical implications (2015). Scali F, Pontell ME, Nash LG, Enix DE. 

Shunt scissors: technical note (2018). Dacey RG, Flouty OE, Grady MS, Howard MA, Mayberg MR. 

Configuration of the Connective Tissue in the Posterior Atlanto-Occipital Interspace: A Sheet Plastination and Confocal Microscopy Study (2005). Lance Nash, Helen Nicholson, Antonio S J Lee, Gillian M Johnson, Ming Zhang

The second terminations of the suboccipital muscles: An assistant pivot for the To Be Named Ligament (2017). Xiao-Ying Yuan, Chan Li, Jia-Ying Sui, Qi-Qi Zhao, Xiao Zhang, Na-Na Mou, Zhao Huang-Fu, Okoye Chukwuemeka Samuel, Nan Zheng, Seung-Ho Han, Sheng-Bo Yu, and Hong-Jin Sui

The Myodural Bridge Complex Defined as a New Functional Structure (2019). Nan Zheng, Beom Sun Chung, Yi-Lin Li, Tai-Yuan Liu, Lan-Xin Zhang, Yang-Yang Ge, Nan-Xing Wang, Zhi-Hong Zhang, Lin Cai, Yan-Yan Chi, Jian-Fei Zhang, Okoye Chukwuemeka Samuel, Sheng-Bo Yu, Hong-Jin Sui

The morphology and clinical significance of the dorsal meningovertebra ligaments in the cervical epidural space (2014). Shi B, Zheng X, Min S, Zhou Z, Ding Z, Jin A.

Head movement, an important contributor to human cerebrospinal fluid circulation (2016). Qiang XuSheng-Bo YuNan ZhengXiao-Ying YuanYan-Yan ChiCong LiuXue-Mei WangXiang-Tao Lin, and Hong-Jin Suib

The intracranial denticulate ligament: anatomical study with neurosurgical significance Laboratory investigation (2011) R. SHANE TUBBS, MARTIN M. MORTAZAVI, MARIOS LOUKAS, MOHAMMADALI M. SHOJA AND AARON A. COHEN-GADOL

The Epidural Ligaments (of Hofmann): A Comprehensive Review of the Literature (2016). Gabrielle G Tardieu, Christian Fisahn, Marios Loukas, Marc Moisi, Jens Chapman, Rod J Oskouian, and R. Shane Tubbs

The Five Diaphragms in Osteopathic Manipulative Medicine: Myofascial Relationships, Part 2 (2020). Bruno Bordoni 

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