Anatomy & mechanics of the ribs & Diaphragm
True, false and floating ribs
True ribs: ribs 1-7 attach to the sternum which may contribute to the decreased movement in flexion-extension seen at T1-7 (<T1-2) during respiration (Burgos et al 2021).
False ribs: ribs 8-10 don’t attach to the sternum (ribs 8-10 attach to costal cartilage) which may contribute to the increased movement in flexion-extension seen at T7-10 during respiration. This allows an increase in lordosis at T7-10 in inspiration to allow ascent and expansion of the thorax, facilitate diaphragmatic function, relieve abdominal pressure and expand the elastic base of the thorax in order to facilitate muscle contraction (Burgos et al 2021).
Floating ribs: ribs 11-12 have no ventral attachment. T11-12 is more rigid in respiration, despite having ribs with less attachments, due to the high mechanical strain it is under being between the rigid thoracic and mobile lumbar spine, and, being in neither kyphosis nor lordosis (Burgos et al 2021).
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. The ‘upper rigid segment’ comprising rib 1, sternum and T1-2 ascends during inspiration being facilitated by the lordosis from the more mobile T7-10 segments (Burgos et al 2021). 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
Fibrous capsule
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.
Radiate 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.
Intraarticular ligament
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 articulates 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.
Fibrous capsule
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.
Costotransverse ligament
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.
Lumbocostal ligament
The lumbocostal ligament attaches rib 12 to the L1-2 transverse processes.
Innervation of the costovertebral joints
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.
Transforaminal ligaments
The transforaminal 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.
Extraforaminal ligaments
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 costotransvere 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.
Rotation
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 'costovertberal 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?
Flexion-extension
T1 flexes-extends to 4 degs and increases incrementally to 12 degs at T12. During forced respiration T1–T7 (=true ribs ribs 1-7) was more rigid in flexion-extension (<T1-2) than T7–T10 (= false ribs ribs 8-10). The increased mobility of T7–T10 during respiration could be the underlying cause of the cranial displacement of the apex of the thoracic kyphosis during forced exhalation and allows an increase in lordosis during forced inspiration. This lordosis: (i) allows ascent and expansion of the thorax; (ii) facilitates diaphragmatic function; (iii) relieves abdominal pressure; (iv) expands the elastic base of the thorax to facilitate muscle contraction (Burgos et al 2021).
T10–T12 was found to be more fixed in flexion and extension during respiration, despite their floating rib attachments due to the high mechanical strain at this area, being transitional between the rigid thoracic and mobile lumbar spine, and, these vertebrae being neither kyphotic nor lordotic (Burgos et al 2021).
Sidebending
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.
Respiratory mechanics
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. T11 and 12 is fairly fixed during respiration as it absorbs a lot of mechanical strain, being transitional between the rigid thoracic spine and mobile lumbar spine, and is neither in kyphosis or lordosis (Burgos et al 2021).
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.
Scalenes.
Sternocleidomastoid.
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. These muscles, along with the trapezius, not only contribute to respiration but stabilise the cervical spine, showing diminished strength, endurance, motor control, and proprioception as a result of pain (Tatsios et al 2022).
In a forced inspiration the scapula is raised and fixed using the:
Levator scapulae.
Trapezius.
Rhomboids: 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.
Diaphragm
Anatomy
The diaphragm is divided into three functional groups:
Sternal part. Attaches to the xiphoid. Also attaches to the adjacent aponeurosis of the transversus abdominis or to a tendinous arch extending from the xiphoid to the cartilages of the rib 5 and 6 (Rives & Barker 1942).
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 transmitted to its costal attachments. The rib 7-9 is inseparable from the transversus abdominis, and the more posterior portion (rib 10-12) attaches to the trasnversus abdominis via a common aponeurosis. This common aponeurosis can be traced backward to the lateral margin of the quadratus lumborum (blending with anterior layer of the thoracolumbar fascia) attaching to rib 10 and 11 and indirectly to rib 12 via a fascial attachment (refer below ‘lateral arcuate ligament’) (Rives & Barker 1942).
Lumbar group. Crura: (right) attaches to the L1-3 bodies and discs (left) L1-2 bodies and disc; L1 TP via the arcuate ligaments. The lateral arucate ligament (rib 12 to L1 TP) is a thickening of the quadratus lumborum fascia. The medial arcuate ligament (L1 body to L1 TP) is a thickening of the psoas fascia. Median arcuate ligament connects the two crura over the aortic hiatus (T12 level).
*: the transversalis fascia is a continuous structure that encircles the abdominal cavity covering the quadratus lumborum (quadrautus lumborum fascia) and is continuous with the psoas fascia and anterior layers of the thoracolumbar fascia
The structures passing through the diaphragm include:
Vena cava hiatus in the central portion (T8 level) for the inferior vena cava to pass through.
Oesophageal hiatus: near the right crus at the left part of the diaphragm (T10 level) for the oesophagus and vagus nerve plexus to pass through.
Aortic hiatus on the vertebral column between the left and right diaphragmatic crura (T12 level) for the descending aorta, thoracic duct, and azygous vein to pass through.
Whilst not passing through a hiatus the phrenic nerve pierces the diaphragm.
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
Vagus nerve. The vagus nerve innervates the crura (and phrenoesophageal ligament).
Phrenic nerve
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 by monitoring the 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
Therefore, the phrenic nerve contains somatic motor, sensory, and sympathetic fibers for the diaphragm. Its motor and sympathetic fibers control the diaphragmatic voluntary and autonomic movements respectively. The motor outputs of the phrenic nerve control breathing, but also regulating swallowing, voicing, spitting, emesis, and coordinating with pelvic floor muscles for defecation, urination, and even sexual activity (Liu et al 2023).
Sensory innervation (pain and proprioception) at the central tendinous part is innervated by the phrenic nerves, while the peripheral portions are innervated by the intercostal nerves 6-11 (Liu et al 2023). Phrenic afferents reach the cerebellum, the limbic area (thalamus, amygdala, pre-frontal cortex, periaqueductal grey area, hypothalamus, pituitary), reticular formation (Nair et al 2017) and the somatosensory cortex (Bordoni et al 2020) effecting propriospinal neurons and/or spinal motoneurons. For this reason activation of phrenic afferent neurons triggers a diverse range of physiological responses including increases in sympathetic neural outflow and arterial blood pressure, short-latency inhibition of phrenic motoneurons, increases in ventilation and decreases in intercostal motor output (Nair et al 2017).
Vagus nerve
Vagus nerve relays sensory information from the lungs, trachea, and larynx including threats to airway integrity, pathogens to evoke immune responses, airway hyperreactivity, sickness behaviors, and pain (sore throat), provide proprioceptive feedback from the vocal folds for speech control, and evoke the sensation of air hunger. The airways from larynx to lungs also receive afferent innervation by C1-T6 dorsal root ganglion neurons whose sensory functions remain poorly understood. From the nasopharynx to the distal lung (e.g. alveoli and pleura) vagal sensory neurons display a multitude of epithelial and subepithelial terminal types that detect, for instance, taste, irritants (when to cough), chemosensory and neuro-immune-endocrine milieu and also mechanoreceptors that report activity across the respiratory cycle (e.g. inflation and deflation) (Prescot & Liberles 2022).
Airway stretching activates the vagus nerve which is the afferent limb of the Hering-Breuer inspiratory reflex that characterises normal breathing: degree of airway stretch (<inspiration >expiration) —> vagus —> nucleus solitarius (along with baro- & chemoreceptor information) —> respiratory brainstem centres —> phrenic nerve. Relaying this sensation of airway volume contributes to normal breathing patterns, may protect the airways from hyperinflation-induced injury, and regulates heart rate and vascular tone, perhaps contributing to respiratory sinus arrhythmia in which pulmonary circulation increases during high airway volumes to optimize gas exchange(Prescot & Liberles 2022).
Diaphragmatic vagal afferents innervate the diaphragmatic crura and the phrenoesophageal ligament. The mechanoreceptors from the crura and the phrenoesophageal ligament induce a reflex that allows transient lower oesophageal sphincter relaxation independent of cardiac and respiratory activity (Bordoni et al 2020).
The vagal diaphragmatic information reaches the nucleus of the solitary trait and will eventually be brought to the vestibular and limbic area (Bordoni et al 2020).
The vagal efferences of the oesophageal breath are of the cholinergic and excitatory type and are independent of cardiac and respiratory activity (Bordoni et al 2020).
Biomechanics of respiration
Intercostals
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 rotation. 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
Diaphragm and the larynx
A coordination between the diaphragm, pelvic floor, abdominal muscles and larynx (< the rima glottiis between two true vocal folds) is significant for physical and physiological activities. For instance, when lifting a weight the intrabdominal pressure has to dissipate evenly and the glottal aperture closes up as the larynx elevates to close the airway. When coughing or sneezing intraabdominal pressure is pushed superiorly, the pelvic floor elevates and the and the glottal aperture opens up between the true vocal folds so the larynx keeps the airway open. When defecating or urinating the intrabdominal pressure is pushed inferiorly, the pelvic floor lowers and the glottal aperture closes up as the larynx elevates to close the airway (Liu et al 2023).
For example, weak coughing, low/short voicing, urinary or stool retention might be resulted from the weak diaphragm and/or abdominals. Urinary or bowl movement incontinence might be caused by the weak pelvic floor muscles that are not able to sustain the increased intraabdominal pressure. The push-down action during the bowel movement always occurs during exhalation with the glottal aperture closed so if a person has a weak or dysfunctional laryngeal muscles, this may cause decreased downward pressure to the pelvic floor, which may lead to constipation, an often-seen symptom in patients with Parkinson disease (Liu et al 2023).
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 (and scalenes), conversely to that of the diaphragm, moves the ribs cephalic and anteriorly to an "inspiratory" position preventing the thorax from being drawn inwards by the action of the diaphragm (Han et al 1993) and stretches the diaphragmatic fibers. Hudson et al (2011) found the inspiratory activity in the parasternal intercostals increases when individuals attempt to breath with the diaphragm alone. This elevation of the thorax in inspiration is permitted by the mobility in lordotic extension at T7-10 inferiorly, and the elevation of a rigid segment comprising the first rib, T1-2 and sternum superiorly (Burgos et al 2021). This could be why the inspiratory position of the ribs manually recreated in techniques such as “doming the diaphragm” has been shown to improve diaphragmatic function by stretching its muscle fibers (Nair et al 2019).
This reciprocal action does not just exist between the diaphragm and the parasternal intercostals but also the parasternal intercostals and the transversus thoracis (Hudson et al 2010). Just as the parasternal intercostals are used for inspiration the transversus thoracis 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 transversus thoracis is used for contralateral rotation.
The diaphragm does not stay stretched in inspiration. By extending and stretching the diaphragmatic 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
In the abdominal cavity there are many ligaments, primarily formed by peritoneal fold or thickening, that connect the internal digestive organs to the undersurface of the diaphragm, including oesophagus, stomach, duodenum, colons, liver, and spleen. It is likely that with deep breathing, these ligaments may assist the movement of the attached internal organs to prevent potential adhesion among these organs, and enhance the peristalsis of the GI tract. These peritoneal ligaments include (Liu et al 2023):
Phrenicocolic ligament: left lateral extension of the root of the transverse mesocolon. Diaphragm: opposite left r10 & r11 —> large intestine: left (splenic) colic flexure. Passes below the spleen acting as a suspensory ligament of the spleen.
Phrenoesophageal ligament: diaphragm —> lower end of the oesophagus. Comprised of an up-leaf arising from the endothoracic fascia and a low-leaf from the transversalis fascia.
Gastrophrenic ligament: diaphragm —> upper-left surface of the stomach.
Suspensory ligament of duodenum (ligament of Treitz): left diaphragm, connective tissue surrounding the coeliac artery and superior mesenteric artery —> D3 & D4 & duodenojejunal angle.
Left/right triangular ligaments: diaphragm —> upper-left and right surfaces of the liver.
Coronary ligament: diaphragm —> upper posterior surface of the liver.
Falciform ligament: anteroinferior surface of the diaphragm —> umbilical fissure of the liver.
Splenophrenic ligament: diaphragm —> upper medial surface of the spleen.
Since the abdominal contents are essentially incompressible, all diaphragmatic displacements must be met by equal displacements of the anterolateral abdominal wall and vice versa (Sembera et al 2022). This means 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 which 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 to create stability of the spine. During contraction, the central tendon of the diaphragm moves caudally and reduces intra-thoracic pressure while concurrently increasing intra-abdominal pressure. As lung volume increases above tidal volume, it increases intra-abdominal pressure and causes stiffening of the spine. Conversely, intra-abdominal pressure decreases during tidal expiration.
However, in situations requiring higher respiratory demands, intra-abdominal pressure may increase during expiration due to abdominal muscle activity (<transversus abdominis) assisting in the respiratory pump. With activity of the diaphragm and transversus abdominis preceding phasic movement of the limbs as a part of the anticipatory postural adjustments, and this contraction of the abdominal muscles doing nothing to reduce diaphragmatic excursions or its position during respiration, the abdominal wall and pelvic floor may play a larger role than merely having an antagonistic respiratory function to the diaphragm and “pushing back” against the visceral pressure created by diaphragm contraction. However, even though postural functions during inspiration further challenge the diaphragm as it engages to maintains intraabdominal pressure, and postural functions during expiration further challenge the the abdominal muscles as they engage to maintains intraabdominal pressure, when the abdominals do contract, and intra-abdominal pressure increases, the diaphragm has to contract harder to descend during inspiration (Sembera et al 2022).
In elderly people who have greater difficulty maintaining balance and have altered posture the hamstrings are weaker and thinner resulting in weaker control of the lumbar spine. This results in more frequent sustained contraction of the diaphragm to stabilise the lumbar spine, regardless of the breathing, so the diaphragm becomes thicker, more flatter, less elastic (stiffer) and with a lower shortening speed resulting in a decreased diaphragmatic force (Bordoni et al 2020).
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 cardiopulmonary organs
There are ligaments (phrenopericardial, sternopericardial, xiphopericardial and vertebropericardial ligaments) that connect the heart to the diaphragm and the lungs to the dipahragm (pulmonary ligament). The pulmonary ligament (aka inferior pulmonary ligament): diaphreagm —> base of lungs; phrenopericardial ligament: diaphragm —> pericardium (Liu et al 2023).
Diaphragmatic inspiration increases the intrathoracic capacity as the pulmonary ligament pulls down the base of the lung as the dipahragm descends to enhance ventilation efficiency. This maybe caused by increasing alveolar recruitment, expanding the lung tissue, activating the hypoglossal nerve to retract the tongue and/or widening the respiratory tract (Liu et al 2023).
Chest wall compliance and lung elastic recoil decreases with aging leading to a diminished respiratory system compliance, and increased residual volume and functional residual capacity with age. The accumulation of air in the lungs from reduced lung elastic recoil causes a flattening of the diaphragm that diminishes its force-generating capacity. Whilst in chronic heart failure the lung volumes and mechanics are the opposite of aging, i.e. there is a decreased residual volume and functional residual capacity (that minimises diapthragm flattening), it also increases lung stiffness which diminishes respiratory system compliance. Therefore, elderly patients with a flatter diaphragm from accumulation of air in the lungs who’s reduced respiratory system compliance from both age and chronic heart failure will have compounded respiratory dysfunction (Kelley & Ferreira 2017).
Diaphargamtic inspirations may also affect cardiovascular flow through the hiatuses on the diaphragm and the pericardial ligaments. During inspiration, the vena cava hiatus is stretched and enlarged to facilitate blood flow from the abdomen back to the heart (the aortic hiatus, being retrocrural, is unaffected by diaphragmatic contractions). Also during inspiration, as the diaphragm moves inferiorly, the xiphoid and sternum move superiorly and anteriorly, while the thoracic vertebral column extends slightly, the pull on the pericardial ligaments may expand the pericardial cavity to create a negative intra-pericardial pressure (Liu et al 2023).
Thus, the vacuum action due to both intrathoracic and intra-pericardial pressures could be the primary driving factor or the fundamental mechanism to facilitate blood flow to the heart; to increase coronary perfusion, ventricular filling, and stroke volume; and subsequently to enhance circulation to vital organs all over the body (Liu et al 2023)
Diaphragm and gastrointestinal disturbances
Due to the crural diaphragm's mechanical influences Wallden (2017) attributed diaphragmatic dysfunction to:
GORD.
Swallowing.
Vomiting.
At the gastro-oesphageal junction, a striated muscle structure, made by fibers contributed from either the right crus in 60% of individuals or from both the left and right crura in 40% of individuals, circles around the internal sphincter to act as an external oesophageal sphincter or diaphragmatic sphincter of the lower oesophagus (Liu et al 2023). The phrenoesphageal ligament (refer ‘Diaphragm; diaphragm and the abdomen and pelvis’), although doesn’t have a sphincter action, limits upward displacement of the oesophagus into the thorax, and draws the oesophagus back into position while minimising circumferential traction on the lower oesophageal ligament. 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.
However, during transient lower oesophageal sphincter relaxation resulting in reflux, there is a simultaneous relaxation of the lower oesophageal sphincter, inhibition of crura and oesophageal shortening. In the ferret model this pathway involves activation of vagal mechanoreceptors in the stomach, phrenoesophageal ligament and crura* —> medulla oblongata —> coordinate episodic activation of vagal pathways to inhibitory enteric neurons supplying smooth muscle of the lower oesphageal sphincter and crura (Young et al 2010). Therefore, 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.
*: crura also has afferent innervation from the phrenic nerve.
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 of air) that would have left them vulnerable on the waters 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?
Diaphragm and baroreceptors, balance, coordination and emotions
In animal studies alterations in cardiorespiratory outflow in preparation for a change in posture by relying on interactions between the somatic and autonomic nervous systems. For example, the somatosympathetic reflex: stimulation of neck muscle afferents (<proprioception) —> superficial laminae of the dorsal horn < deeper laminae of the dorsal horn & central cervical nucleus (CCN) (C1-4: lamina VII) & its superior continuation into the medulla the perihypoglossal nucleus (intermediate nucleus of the medulla) & the external cuneate nucleus (medulla). The perihypoglossal nucleus also receives and integrates information from the external cuneate nucleus (Edwards et al 2015) and vestibular system. CCN-perihypoglossal nucleus —> vestibular nuclei (Matsushita & Yaginuma 1995), cerebellum & reticular formation (providing integrated data about the head position relative to the trunk and space) (Li et al 2022), nucleus solitarius (a site for cardiorespiratory integration) and hypoglossal nuclei (Szelényi & Fava 2022). Whilst this is an animal model the perihypoglossal nuclei, nucleus of Roller and nucleus intercalatus might have the same connections in humans (Szelényi & Fava 2022).
This is the proposition how activation neck muscle afferents via neck flexion or respiration (<suboccipitals due to their high spindle content & sternocleidomastoid), either independent of the vestibular system (Edwards et al 2007), or by activating the vestibular system via the reticular formation and parabrachial nucleus (integrates behaviours, affective states, and autonomic responses) —> thoracic sympathetic preganglionic neurons (Li et al 2022) to increases heart rate, muscle sympathetic nerve activity, and arterial blood pressure, increases splanchnic, hypoglossal, and abdominal nerve activity (Edwards et al 2007) and effect respiratory and oromotor control (Edwards et al 2015). The parabrachial nucleus —> ventrolateral medulla (preBötzinger Complex) —> drives state-dependent breathing patterns (e.g.integrating breathing with pain and anxiety) and breathing patterns not gated by state (Arthurs et al 2023).
The perihypoglossal nucleus is also a major source of input to XII and on stimulation of the neck muscle afferents inhibits the phrenic nerve (and inspiration), increases sympathetic nerve activity (with no obvious heart rate response) and evokes a tonic discharge to XII. As such it appears to be in a prime position to integrate information from both the periphery and the CNS before influencing airway patency and tongue movements through XII (Edwards et al 2015).
A healthy diaphragm muscle should stimulate baroceptors (stretch receptors) in the aortic arch and carotid glomus, particularly during a deep inhalation. Aortic arch (X) and carotid baroreceptors (IX) —> nucleus of the solitary tract —> inhibits rostral ventrolateral medulla descending input to the preganglionic neurons in the spinal cord that control sympathetic nerve activity —> vascular smooth muscle, including that to the muscles, to improves overall muscle strength and coordination (Bordoni et al 2020). However, this baroreflex pathway is polysynaptic, poorly myelinated, has a relatively long latency and is solely reactive, modulating vasoconstriction and heart rate in response to whatever circumstances the cardiovascular system has just happened to find itself in, such as a drop in blood pressure (Holstein et al 2016).
A less lethargic and more direct and rapid modulation of blood pressure can be achieved in response to postural adjustments (e.g. head movement). This vestibulo-sympathetic reflex is again achieved through direct projections between the vestibular nuclei and the presympathetic brainstem (rostral ventrolateral medulla and caudal ventrolateral medulla). The vestibulo-sympathetic reflex functions to redistribute blood during changes in posture and movement, e.g. to increase blood pressure when going from supine to standing, as to ensure consistent cerebral perfusion irrespective of head position. Subsequently to the activation of sympathetic nerve activity by the vestibulo-sympathetic reflex, the baro- and cardiopulmonary reflexes re-establish and maintain homeostatic blood pressure control (Holstein et al 2016).
Therefore, by not only influencing postural control and stimulating baroreceptors in the aortic arch and carotid glomus, but also by vagal diaphragmatic information —> nucleus of the solitary trait —> vestibular and limbic areas, the diaphragm can effect vestibular function (Bordoni et al 2020). Overall strength and coordination of the skeletal muscles can be compromised from inspiratory muscle fatigue (St Croix et al 2000). This results in the respiratory muscles, when they need it, steeling blood and oxygen from the skeletal muscles by inducing a reflex vasoconstriction of larger vessels, whilst constriction in smaller vessels is blunted, thereby limiting total skeletal muscle blood flow but distributing it more optimally. This reflex is mediated by afferent phrenic nerve fibers that project to supraspinal centers in the brainstem involved in cardiorespiratory control and even higher to the cerebellum, hypothalamus, and somatosensory cortex. During heavy intensity exercise the skeletal muscles induce a reflex vasoconstriction on the diaphragm vasculature promoting respiratory muscle fatigue (Sheel et al 2018).
Shallow breathing can also cause vasoconstriction in the limb musculature by causing accumulation of metabolites —> stimulates group IV phrenic afferent nerve fibers —> reflex sympathetic activation (Kelley & Ferreira 2017). Increase sympathetic activity causes vasoconstriction in limb muscles limiting whole-body exercise tolerance (Kelley & Ferreira 2017).
Via the phrenic nerve’s projections to the somatosensory cortex diaphragm fatigue alters the ‘cortical integration’ of phrenic sensory afferent information. This negatively effects the conscious perceptions of breathing and diaphragm activation which contributes to diaphragm proprioception (i.e. its ‘body positon’) and somatosensation, which, in turn, helps determine respiratory motor output (inhibition of diaphragm mechanoreceptors —> disinhibition of the inspiratory intercostals). Changes in the phrenic nerves somatosensory representation may also account for diaphragmatic referred pain patterns in the neck or shoulder (Nair et al 2017).
Breathing also activates the primary cortex, premotor cortex and neighbouring motor areas to improve the response of muscle strength and performance by up to 10% (Bordoni et al 2020).
The diaphragm’s effect on brain function to improve emotional well being can be through:
Breathing from the nose (deep and rhythmic) produces rhythmical oscillations that propagate in different areas of the brain, to allow improved function and a temporary improvement in synaptogenesis in the limbic system (emotions), hippocampus (memory), insular cortex (planning, speech articulation and gesture) and somatosensory (Bordoni et al 2020).
Cognitive, emotional and pain control can also be regulated throught the phrenic nerve. Cortex —> limbic system, amygdala and thalamus —> hypothalamus and periaqueduct gray —> medulla: ventral respiratory column including the ventral respiratory group (rostral <inspiration & caudal <expiration) and pre-Botzinger group —> (i) bulbophrenic pathway —> phrenic nucleus (diaphragm) & (ii) nucleus ambiguus (intrinsic laryngeal muscles), spinal motor neurons (abdominal muscles), onuf’s nucleus (pelvic floor). Therefore the caudal respiratory group (retroambiguus nucleus) acts like a pianist’s hand striking on the piano keys (analogue to different motor nuclei for different muscles) for different tones (analogue to different muscle actions on targeted organs) (Liu et al 2023).
The diaphragm affects neural oscillations or brainwaves (the rhythmic or repetitive pattern of neural activity) that include increased alpha activity (improves alertness in quiet status, abstract thinking, and self-control); decreases theta activity (improves concentration, reduces anxiety, and decreases distraction); increases gamma activity in the frontal, parietal, and temporal lobes (activation of cognitive functions such as fear, despair, memory, attention, and motivation) (Liu et al 2023).
Diaphragmatic breathing moves the brain mass in a cephalic direction during deep inspiration and caudally during expiration which may facilitate the circulation of cerebrospinal fluid. Also by decreasing intracranial pressure and increasing blood flow to the brain diaphragmatic breathing provides nutritional support of cognition-processing (Liu et al 2023).
In patients with stress and depression sympathetic activity is continuously activated without the normal counteraction of the parasympathetic nervous system. Diaphragmatic breathing increases parasympathetic activity and decreases sympathetic activity assisting in stress control, attention focus, and cortisol reduction (Liu et al 2023). In contrast to diaphragmatic breathing, shallow breathing, accumulates metabolites —> stimulates group IV phrenic afferent nerve fibers —> reflex sympathetic activation (Kelley & Ferreira 2017).
Neurocognitive and neuro-regenerative functions can be associated with inflammation and oxidative stress and diaphragmatic breathing is able to increase the antioxidant activity and reduce oxidative stress (Liu et al 2023). Reduced antioxidant activity that fails to suppress reactive oxygen species (ROS) causing a redox imbalance leading to protein oxidation that triggers diaphragm atrophy and impairs contractile function (Kelley & Ferreira 2017).
Consequences of poor respiratory mechanics
Inspiratory muscle dysfunction is highly prevalent in the elderly and in cretain pathologies such as chronic heart failure (< older chronic heart failure patients or those in advanced stages of the disease). This decrease in maximal inspiratory muscle function means ventilatory behaviours occur at a higher percentage of the maximal value. This results in increases in motor unit firing frequency and recruitment and a mismatch between input (phrenic nerve activity) and output (diaphragm force). This process is complicated in the aging (and in chronic heart failuire) as there is a remodeling (enlargement and fragmentation) and loss of synaptic contact in individual neuromuscular junctions leading to a decrease in neurotrophic factors and efficiency of muscle firing. This results in sensations of dyspnea, a compromised ability to sustain elevated ventilation during physical activity and exercise intolerance, and a compromised ability to clear airways through coughing or sneezing (Kelley & Ferreira 2017). Consequences of poor respiratory mechanics include (Tatsios et al 2022):
Increased or decreased pH blood levels.
Altered respiratory pattern causing smooth respiratory muscle constriction in the vessels and bronchi constriction.
Altered electrolyte balance.
Decreased tissue oxygenation.
Increased excitability of the muscular system including, hypertonia and shortening of the accessory muscles, with associated reduced activation of the longus colli and longus capitis contributing to a forward head posture and neck pain.
Increased excitability of the sympathetic nervous system (NA) and decreased activation of the vagus nerve from reduced diaphragmatic breathing. Shallow breathing accumulates metabolites —> stimulates group IV phrenic afferent nerve fibers —> reflex sympathetic activation (Kelley & Ferreira 2017). Increase sympathetic and decrease vagal activation stimulates activation of proinflammatory cytokines (which self sustains activation of the HPA axis and promotes neurotoxic pathways and decreases 5-HT), promotes hyperalgesia (Tatsios et al 2022), vasoconstriction in limb muscles limiting whole-body exercise tolerance and in chronic heart failure patients with poor inspiratory muscle strength cardiac arrhythmias and a high risk of death (Kelley & Ferreira 2017).
Proinflammatorey cytokines IL-8 and TNF cause atrophy of the diaphragm. Cytokines (and angiotensin II) activate sphingomyelinase disrupts the contractile function of the diaphragm (Kelley & Ferreira 2017).
Hypomobility of the thoracic cage with reduced descent of the diaphragm and chest wall expansion and increase activation of the external oblique.
Decreased respiratory muscle strength and associated respiratory outcomes, such as maximum expiratory pressure (MEP), maximum inspiratory pressure (MIP), end tidal CO2 (ETCO2), forced expiratory volume in the 1st second of expiration (FEV1), maximum voluntary ventilation (MVV), and forced vital capacity (FVC).
A consequence of this shallow breathing pattern is an increase in the ratio of dead space-to-tidal volume (VD/VT). Elevated VD/VT, which in chronic heart failure reflects an inefficient breathing pattern, compromises alveolar ventilation and gas exchange within the lungs. Markers of impaired gas exchange during exercise have greater prognostic value than VO2max in patients with chronic heart failure (Kelley & Ferreira 2017).
Associated anxiety, depression, kinesiophobia, catatsrophising, dysfunction breathing patient-subjective sensations.
An inability to generate normal inspiratory pressures can impair airway clearance (coughing) and predisposes individuals to pulmonary infections. Pneumonia is a common pulmonary complication with aging and in chronic heart failure patients that are prone to poor inspiratory muscle strength (Kelley & Ferreira 2017).
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