Typical and atypical rib articulations
Ribs 2-9: are typical ribs. They articulate via inferior and superior costal facets connecting to the bodies of two adjacent vertebrae; the vertebra of the same number and the vertebra above.
Ribs 1, 10, 11 and 12: are atypical ribs. Each rib articulates with only one vertebra. Ribs 11 and 12 (floating ribs) don’t have a costotransverse joint due to their absence of an articulation with the sternum.
Costovertebral joint capsule and ligaments
The fibrous capsule connects the rib head with the articular cavities formed from the intervertebral discs and adjacent vertebrae. Some of the upper fibers of the capsule pass through the intervertebral foramen to the back of the disc. The posterior fibers are continuous with the costotransverse ligament.
Connects the anterior rib head with the bodies of the two adjacent vertebrae and disc. Although rib 1, 10, 11 and 12 attach to a single vertebrae the radiate ligament still attaches to the corresponding vertebrae and the one above, but not the vertebrae below.
Attaches to the crest of the rib extending to the intervertebral disc. These ligaments are absent in rib 1, 10, 11 and 12.
The atypical ribs fail to provide as much intersegmental stability as the typical ribs. This is because the costovertebral joints are not located at the level of the intervertebral disc and have a diminished ligamentous structure (Liebsch et al 2016).
Costotransverse joint capsule and ligaments
The articular part of the tubercle of the rib artriculates with a reciprocal facet on the transverse process to which it corresponds numerically.
Ribs 1-5 (or 6): the joint surfaces are reciprocally curved. This allows a pump handle movement of the ribs during respiration.
Ribs 7 (or 6) to 10: the joint surfaces are more flattened. This allows a bucket handle movement at the ribs during respiration.
Ribs 11 and 12: the costotransverse joints are absent.
The fibrous capsule is a thin membrane that is attached to the circumference of the articular surfaces and lined with a synovial membrane.
Lateral costotransverse ligament
The lateral costotransverse ligament connects the posterior surface of the transverse process to the nonarticular part of the tubercle of the rib. These fibers run horizontally.
The costotransverse ligament connects the anterior surface of the transverse process to the posterior neck of the neighbouring rib. These fibers run more horizontally.
Superior costotransverse ligaments
The superior costotransverse ligament connects the anterior surface of the transverse process of the vertebra above to the posterior neck of the rib below. These fibers run vertically.
This ligament is frequently absent on rib 1.
The superior costotransverse ligament is composed of anterior and posterior fibers.
- Anterior fibers of the superior costotransverse ligament extends from the anterior surface of the superior transverse process to the rib neck below.
- Posterior fibers of the superior costotransverse ligament extends from the inferior border of the superior transverse process to the rib crest below.
Jiang et al (1994) found the superior costotransverse ligament to be involved in active lateral balancing of the spine. Saker at al (2016) found the costotransverse ligaments allow sidebending and rotation.
The lumbocostal ligament attaches rib 12 to the L1-2 transverse processes.
The transforamonal ligaments traverse the intervertebral foramen diminishing the space available for, and protecting, the nerves and blood vessels.
Gkasaris et al (2016) listed these ligaments as
- Superior corporopedicular ligament: extends from the superior pedicle to the posterolateral vertebral body and related annulus fibrosus.
- Inferior corporopedicular ligament: extends from the inferior pedicle to the posterolateral vertebral body and related annulus fibrosus.
- Superior transforaminal ligament: extends from the arches of the superior and inferior vertebral notches to the articular capsule of the superior pedicle.
- Mid transforaminal ligament: extends from the annulus fibrosus and superior and inferior corpopedicular ligaments to the articular capsule.
- Inferior transforaminal ligament: extends from the junction of the annulus fibrosus and the posterior vertebral body to the superior articular facet.
Kraan et al (2009) named the extraforaminal ligaments as the superior costotransverse ligament and the inferior transforaminal ligament. These ligaments anchor the nerve as it exits the intervertebral foramina.
From T2–T10 these authors describe these ligaments as being important for craniocaudal positioning of the thoracic spinal nerve.
Superior costotransverse ligaments
Kraan et al (2009) gave a different description of this ligament to Saker et al (2016) and described it as extending from the superior costovertebral joint capsule and transverse process to the inferior transverse process. This ligament attaches to the spinal nerves anteriorly.
Therefore this ligament attaches the spinal nerves to the neighbouring, superior and inferior, transverse processes and to the costovertebral joint capsule.
Inferior extraforminal ligament
Gkasdaris et al (2016) described this ligament as extending from the superior transverse process to the inferior transverse process. This ligament attaches to the spinal nerve posteriorly.
Therefore this ligament attaches the spinal nerve to the superior and inferior transverse processes.
Variations in the extraforaminal ligaments
Kraan et al (2009) described the variations of the extraforminal ligaments at different levels.
T10 & T11
At T10 and T11 the nerve is posteriorly attached to the internal intercostal membrane. At T11 the spinal nerve is attached caudally to the capsule of the costovertebral joint and the intervertebral foramen.
Zhang et al (2016) found the internal intercostal muscles rotated the lower ribs more than the upper ribs during expiration. Therefore could 'expiratory lesions' of the ribs at this level predispose to greater nerve pain?
T12 & L1
At T12 and L1 the superior costotransveres ligament and inferior transforaminal ligament cross the spinal nerves anteriorly connecting them to the intervertebral foramen and disc.
Biomechanics of the thoracic spine
The thoracic cage plays an important role in load-bearing, providing between 30-40% of thoracic spine stiffness. Rib joint stiffness is greatest at T2 and weakest at T10 (Saker et al 2016).
Rotation occurs inversely to flexion-extension.
Liebsch et al (2017) found the costovertebral joints provide stability to the thoracic spine primarily in rotation.
T1 rotates 9 degs incrementally decreasing to 2 degs at T12.
Ribs 2-10: in rotation there is a slight contralateral transverse plane translation that occurs between the ribs and their relative transverse processes (Lee 2015). Liebsch et al (2016) found sidebending in one direction induced a considerable amount of rotation in the opposite direction.
Ribs 1, 11, 12: do not appear to translate in the transverse plane during axial rotation (Lee 2015).
As these joints possess a diminished ligamentous structure (refer 'costovertebral joint capsule and ligaments') and rib 11 and 12 also lack a costotransverse and sternocostal joint they fail to provide as much intersegmental stability (Liebsch et al 2016). Could this lack of stability be the reason why these joints can freely rotate within their range of motion without producing a coupled sidebending?
T1 flexes-extends to 4 degs and increases incrementally to 12 degs at T12.
During side-bending, the ribs approximate on the concave side and separate on the convex side. This is accompanied by an ipsilateral>contralateral rotation (Lee 2015). Saker at al (2016) found the costotransverse ligaments allow sidebending and rotation.
The bucket and pump handle movements of the ribs are primarily produced by the intercostal muscles (Zhang et al 2016)
Pump handle movement: rib 1 to 5 (or 6)
Ribs 1-5 (or 6): the costotransverse joint surfaces are reciprocally curved. This allows a pump handle movement of the ribs.
The pump handle motion increases the anterior-posterior dimensions of the thorax. Because the ribs are sloped downward, any elevation during deep inspiration will result in a cephalic and anterior movement of the sternum. This increases the anterior-posterior diameter of the thorax.
The external intercostal muscles are the most important muscles for elevating the rib cage. However the cervical accessory muscles, i.e. sternocleidomastoid and scalene muscles, facilitate the pump handle movement not only in the upper ribs but play a role in elevating the entire rib cage (Zhang et al 2016).
Bucket handle movement: rib 7 (or 6) to 12
Ribs 7 (or 6) to 10: the costotransverse joint surfaces are more flat. This allows a bucket handle movement at the ribs. Ribs 11 and 12 don’t possess a costotransverse joint.
The bucket handle movement results in a lateral motion of the ribs when they are elevated. This increases the transverse diameter of the thorax.
At ribs 11 ands 12 there is a lack of articular stability. This is from the rib articulating with a sole vertebrae, an absent intraarticular ligament, partial radiate ligament attachment and no sternocostal attachment.
This articular instability could serve a functional role to help absorb force from the diaphragm.
Wallden (2017) found most of the contractile force of the diaphragm is transmitted peripherally to the lower ribs around a fulcrum formed from the phrenopericardial ligament (Bordoni & Zanier 2013); not downward to the viscera. This acts to dampens down the vertical pressure directed down to the pelvic floor.
Muscles of respiration
The muscles of deep inspiration involved in raising the rib cage are the:
- External intercostals.
- Serratus anterior.
- Levatores costarum.
- Serratus posterior superior.
- Additionally: pectoral muscles and serratus anterior.
Zhang et al (2016) found the cervical accessory muscles, i.e. sternocleidomastoid and scalene muscles, facilitate the pump handle movement not only in the upper ribs but play a role in elevating the entire rib cage.
In a forced inspiration the scapula is raised and fixed using the:
- Levator scapulae.
- Rhomboids. to raise and fix the scapula.
The muscles of forced expiration that pull the rib cage downward are the:
- Internal intercostals
- Abdominal muscles.
- Minor contributions from the quadratus lumborum, subcostals, transverse thoracic and serratus posterior inferior.
Innervation of the costovertebral ligaments is from the lateral branch of the thoracic dorsal rami of C8 to T11
The costovertebral joints receive this innervation in a segmental fashion with each joint receiving fibers from the level above and directly below it.
Due to the segmental innervation of the joints their pain pattern is well-localized and level specific but can radiate to the scapula or chest wall. However in cases of central sensitisation pain patterns are less predictable.
Relations of the costovertebral and costotransverse joints and brachial plexus
Whilst the costovertebral ligaments are innervated by C8 and T1 they are innervated by the dorsal rami and not the ventral rami that make up the brachial plexus.
In approximately 60% of individuals, there is a linkage of the brachial plexus to the first and/or second intercostal nerve and stellate ganglion, known as Kuntz’s nerve. This nerve carries sympathetic fibers to the brachial plexus without passing through the sympathetic trunk (Zaidi & Ashraf 2010).
Therefore, disorders affecting the first or second costovertebral joints can result in arm pain referred via this pathway.
The diaphragm is divided into three functional groups:
- Sternal part: attaches to the xiphoid.
- Costal part: these vertical fibers attach to the internal surfaces of rib 7-12 and blends with the transversus abdominis. Most of the contractile force of the diaphragm is transmtted to its costal attachments.
- Lumbar group: attaches to the L1-3 bodies (right) and L1-2 bodies (left) via the crus; L1 TP via the arcuate ligaments. The lateral arucate ligament (rib 12 to L1 TP) is a thckening of the quadratus lumborum fascia. The medial arcuate ligament (L1 body to L1 TP) is a thickening of the psoas fascia. The crural fibers have a minor role in respiration being more orientated to gastrointestinal function (Wallden 2017).
Innervation of the diaphragm
The innervation of the diaphragm is from:
- Phrenic nerve (C3,4,5 and sometimes C6): motor and sensory innervation to the diaphragm. The phrenic nerve does not innervate the crural fibers.
- Intercostal nerves 6-12: sensory innervation
Wallden (2017) attributed the clinical relevance of the diaphragms innervation as being:
- Phrenic nerve courses within the fascia associated with the anterior scalene. Could trauma to this muscle possibly affect sensory and motor drives in the phrenic nerve accounting for trophic changes to the diaphragm?
- The phrenic nerve spans both the cervical plexus and brachial plexus. Could aberrant afferent impulses from the diaphragm alter motor control at neck or into the shoulder and arm?
Verlinden et al (2018) investigated the phrenic nerve's autonomic fibers and connections describing it not only as a motor nerve for the diaphragm but also a conduit for the peripheral autonomic nervous system. These autonomic functions include regulating blood flow to the diaphragm and providing pressure recpetors for central venous pressure.
These authors noted an asymmetry in distribution of the autonomic fibres in the two phrenic nerves. The right side exhibited a predominance of catecholaminergic fibres in the intradiaphragmatic part; there was a complete absence of these fibers in the left phrenic nerve.
This right side predominance of autonomic fibers is possibly due to the presence of paraganglia in the wall of the (right-sided) inferior cava vein.
These authors identified paraganglia in the wall of the inferior cava where it passed through the diaphragm. These ganglia may have a role in regulating plasma volume. Just as the vagus nerve monitors central venous pressure as stretch of the atrial wall, the phrenic or autonomic nerve endings in the wall of the inferior cava could act as low-pressure receptors for the central venous pressure.
Interestingly these authors also found longitudinal cardiac muscle strands in the wall of the inferior cava. A caval sphincter supplied by the right phrenic nerve is a well-known feature of diving mammals. Myocardial ‘sleeves’ with such properties have also been described in pulmonary veins and at the base of the pulmonary trunk, where their presence can establish extranodal pacemaker activity.
Autonomic connections to the phrenic nerve are:
- Celiac plexus: the phrenicoabdominal branch is a separate catecholaminergic nerve branch from the right phrenic nerve. As it arises from the celiac ganglia it is therefore more appropriately termed the ‘phrenic branch of the celiac plexus’.
- Ansa cervicalis.
- Subclavian ansa (contributes to the inferior cervical sympathetic cardiac nerve), the cervical sympathetic trunk (including the middle and stellate ganglion) and the splanchnic nerves. These nerves are potential vasoregulators of the diaphragmatic vessels.
- CN: X, XI, XII
Biomechanics of respiration
Hudson et al (2010) found the external intercostals < posterior portion of the cephalic interspaces contract during inspiration and the internal intercostals < caudal interspaces contract during expiration. However the parasternal (intercartilagenous) intercostals function as an inspiratory muscle (Hudson et al 2011).
Intercostal intimi contract during expiration.
However when contraction of the neck muscles fixes the first two ribs, the lateral parts of the intercostals increase rib cage volume. If, however, the abdominal muscles fix the most caudal rib, contraction of the same muscles would have the opposite effect (Wallden 2017).
Therefore could hypertonic abdominal muscles or reduced abdominal breathing play a role in compromising the ability of the lateral intercostals to increase rib cage volume?
The intercostals may be more involved in postural control and locomotion than in respiratory movements (Wallden 2017) although Zhang et al (2016) described the intercostal muscles as being the primary movers in producing bucket-handle and pump-handle motions of the ribs not the diaphragm.
Liebsch et al (2017) found the intercostal stretched in sidebending and rotation. Whitelaw et al (1992) found the lateral portion of the external intercostals induces contralateral rotation whereas the lateral portion of the internal intercostals induces ipsilateral rotaion. Hudson et al (2010) found the parasternal intercostals (the intercartilagenous portion of the internal intercostals) induce an ipsilateral rotation and sidebending.
The fibers of the transversus thoracis contract during expiration and contralateral rotation. Therefore through reciprocal inhibition contraction of the transversus thoracis diminishes or prevents activation of the parasternal intercostals during contralateral rotation and expiration (Hudson et al 2010).
Diaphragm and the thorax
When it contracts the diaphragm shifts in a caudad-anterior direction. This is because the muscle fibres are shorter anteriorly (between the sternum and central tendon) and longer posteriorly on both sides of the diaphragm. This results in the posterior portion of the diaphragm descending caudally more than the anterior portion (Zhang et al 2016).
The anterior fibers, on isolated contraction of the diaphragm, although don't descend as much as the posterior fibers show a more complex pattern of movement.
Using a FEM Zhang et al (2016) found an isolated contraction of the diaphragm paradoxically folded the anterior ribs/sternum posteriorly-caudally into an "expiratory position". This occurred as the anterior fibers of the diaphragm contracted in an antero-posterior and lateral-medial direction back towards the central tendon of the diaphragm whilst the whole diaphragm was descending.
This “expiratory” position of the rib cage stretches the parasternal intercostals which function as inspiratory muscles.
This resultant stretch of the parasternal intercostal muscles acts as a stimulus for their contraction (Zhang et al 2016). The contraction of the parasternal intercostals, conversely to that of the diaphragm, moves the ribs cephalic and anteriorly to an "inspiratory" position and therefore stretches the diaphragm muscle fibres. Hudson et al (2011) found the inspiratory activity in the parasternal intercostals increases when individuals attempt to breath with the diaphragm alone.
This could be why the inspiratory position of the ribs manually recreated in techniques such as “doming the diaphragm” have been shown to improve diaphragmatic function by stretching its muscle fibers (Nair et al 2019).
This recpirocal action does not just exist between the diaphragm and the parasternal intercostals but also the parasternal intercostals and the triangularis sterni (Hudson et al 2010). Just as the parasternal intercostals are used for inspiration the triangularis sterni is used for expiration; and just as the parasternal intercostals are used for ipsilateral rotation of the rib above relative to the rib below the triangularis sterni is used for contralateral rotation.
The diaphragm does not stay stretched in inspiration. By extending and stretching the diaphragm muscle fibres they approach their optimal length to provide more muscle contraction force to resist the abdominal and pleural pressures during breathing (Zhang et al 2016).
Diaphragm and the abdomen and pelvis
Most of the contractile force of the diaphragm is transmitted peripherally to the lower ribs around a fulcrum formed from the phrenopericardial ligament (Bordoni & Zanier 2013); not downward to the viscera. This dampens down the vertical pressure directed down to the pelvic floor (Wallden 2017).
This lateral pressure on the lower ribs may account for the relative instability of rib 11 and 12 to accomodate this pressure. This instability is from these ribs articulating with a sole vertebrae, an absent intraarticular ligament, partial radiate ligament attachment and no sternocostal attachment.
Therefore it is the mechanics of the lower ribs that mitigates risk to pelvic floor integrity; and so, any restriction in these ribs as a result of injury, postural dysfunction or emotional bracing, may be a causative pathway to drive pelvic floor issues, such as stress incontinence or hernia (Wallden 2017).
The diaphragm functions as part of the abdominal cylinder along with the transversus abdominis, pelvic floor and deep intrinsic muscles of the spine. The abdominal cylinder helps to create stability of the spine.
The abdominal wall and pelvic floor may play a larger role than merely “pushing back” against the visceral pressure created by the diaphragm contracting.
The diaphragm has a very low level of spindle cells and therefore may not itself be able to regulate pressure effectively. Instead, it is likely to rely on information from the spindle cells in the abdominal wall and pelvic floor to regulate its level of activation in a neural feedback loop (Wallden 2017).
Diaphragm and gastrointestinal disturbances
Due to the crural diaphragm's mechanical influences Wallden (2017) attributed diaphragmatic dysfunction to:
In order for a food bolus to pass easily into the stomach, the crural diaphragm must briefly relax, while the rest of the diaphragm may be contracting during inspiration. This allows the bolus to transit across the diaphragm.
During vomiting the costal and crural diaphragm dissociate their activities. The costal diaphragm contracts to increase intra-abdominal pressure forcing up the gastric contents while the crural diaphragm relaxes to allow it to pass up the oesophagus.
Walldren (2017) proposed the dual respiratory-gastrointestinal function as having an evolutionary origin.
He hypothesised aquatic ancestors developed the diaphragm as a mechanism to prevent aerophagia (swallowing air) that would have left them vulnerable on the water's surface and unable to dive.
A different hypothesis is that the crural diaphragm may have played a role in preventing live prey, swallowed whole, from exiting the stomach.
Verlinden et al (2018) found a catecholaminergic nerve branch from the right phrenic nerve to the celiac plexus. As it arises from the celiac ganglia it is therefore more appropriately termed the ‘phrenic branch of the celiac plexus’.
Could this association of the phrenic nerve to the celiac plexus have a reflex effect in regulating digestion?
Ligaments of the Costovertebral Joints including Biomechanics, Innervations, and Clinical Applications: A Comprehensive Review with Application to Approaches to the Thoracic Spine (2016). Erfanul Saker, Rachel A Graham, Renee Nicholas, Anthony V D’Antoni, Marios Loukas, Rod J Oskouian, and R. Shane Tubbs
Extraforaminal ligament attachments of the thoracic spinal nerves in humans (2009). G. A. Kraan, P. V. J. M. Hoogland, and P. I. J. M. Wuisman
The Nerve of Kuntz: Incidence, Location and Variations (2010) Zeenat F. Zaidi & Arifa Ashraf
The diaphragm – more than an inspired design (2017). Matt Wallden
Biomechanics of the thorax – research evidence and clinical expertise (2015). Diane Gail Lee
Clinical anatomy and significance of the thoracic intervertebral foramen: A cadaveric study and review of the literature (2016). Grigorios Gkasdaris, Grigorios Tripsianis, Konstantinos Kotopoulos, Stylianos Kapetanakis
Quantitative morphology of the lateral ligaments of the spine. Assessment of their importance in maintaining lateral stability (1994). H Jiang, J V Raso, M J Moreau, G Russell, D L Hill, K M Bagnall
Comparison of Diaphragmatic Stretch Technique and Manual Diaphragm Release Technique on Diaphragmatic Excursion in Chronic Obstructive Pulmonary Disease: A Randomized Crossover Trial (2019). Aishwarya Nair, Gopala Krishna Alaparthi, Shyam Krishnan, Santhosh Rai, R Anand, Vishak Acharya, Preetam Acharya
Biomechanical simulation of thorax deformation using finite element approach (2016). Guangzhi Zhang, Xian Chen, Junji Ohgi, Toshiro Miura, Akira Nakamoto, Chikanori Matsumura, Seiryo Sugiura, and Toshiaki Hisada
The rib cage stabilizes the human thoracic spine: An in vitro study using stepwise reduction of rib cage structures (2017). Christian Liebsch, Nicolas Graf, Konrad Appelt and Hans-Joachim Wilke
Anatomic connections of the diaphragm: influence of respiration on the body system (2013). Bruno Bordoni and Emiliano Zanier
The human phrenic nerve serves as a morphological conduit for autonomic nerves and innervates the caval body of the diaphragm (2018). Thomas J. M. Verlinden, Paul van Dijk, Andreas Herrler, Corrie de Gier - de Vries, Wouter H. Lamers & S. Eleonore Köhler
Whitelaw W, Ford G, Rimmer K, De Troyer A (1992). Intercostal muscles are used during rotation of the thorax in humans
Hudson A, Butler J, Gandevia S, De Troyer A (2010). Interplay between the inspiratory and postural functions of the human parasternal intercostal muscles
Hudson A, Butler J, Gandevia S, De Troyer A (2011). Role of the diaphragm in trunk rotation in humans