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A
Fig. 6.2.4 Recovering femoral palsy from haematoma in the femoral
triangle in a 69-year-old farmer who was taking warfarin after aortic valve
replacement. Two months previously he had injured his thigh whilst
vaulting a gate. He experienced severe pain for 24 hours but this
recovered spontaneously. The area of sensory loss is outlined and the
site of the Tinel’s sign is also marked. Recovery was good but not
complete by 6 months. (Courtesy of Rolfe Birch, all rights reserved,
published in Birch R, Surgical Disorders of the Peripheral Nerve. 2nd
edition, 2011. Springer-Verlag, London.)
B
Fig. 6.2.5 A, ‘Closed’ intramedullary nailing of a fracture of a long
bone. The tibial nerve and the posterior tibial artery were involved in the
fracture. B, The muscles of the deep flexor compartment were fibrosed,
causing severe clawing of the toes. (Courtesy of Rolfe Birch, all rights
reserved, published in Birch R, Surgical Disorders of the Peripheral Nerve.
2nd edition, 2011. Springer-Verlag, London.)
REFERENCES
Birch R 2011 Surgical Disorders of the Peripheral Nerves, 2nd ed. London: Williams WW, Twyman RS, Donnell ST 1996 The posterior triangle and the
Springer UK, pp 171–2. painful shoulder: spinal accessory nerve injury. Ann R Coll Surg 78:
Camp SJ, Birch R 2011 Injuries to the spinal accessory nerve – a lesson to 521–5.
surgeons. J Bone Jt Surg Br 93B:62–7. Wynn Parry CB 1981 Rehabilitation of the Hand, 4th ed. Butterworths,
Narakas AO 1993 Paralytic disorders of the shoulder girdle. In: Tubiana R London.
(ed) The Hand, Vol. 4. Saunders, Philadelphia; Ch. 9, pp 112–25.
Seddon HJ 1975 Surgical Disorders of the Peripheral Nerves, 2nd ed. Edin-
burgh: Churchill Livingstone, p. 177.


COMMENTARY
6.3
Thoracic outlet syndromes
Rolfe Birch
Thoracic outlet syndromes (TOS) are amongst the most confusing and Seventh cervical rib
controversial of peripheral nerve disorders. Several different entities are
grouped under this one heading but they have little in common beyond
Estimates of incidence range from 0.004% to 1%. Cervical ribs are
the presumed site of the lesion. The lower part of the brachial plexus,
asymptomatic in most people. The extent of the rib, which is rarely
and the lower trunk in particular, joined at the first rib by the subclavian
symmetrical bilaterally, ranges from a prolongation and pointing of the
vessels, run a regular obstacle course on their way to the lower borders
seventh cervical transverse process to a complete rib in all respects like
of pectoralis minor. Some of the more important obstacles will be
a first thoracic rib. The classification proposed by Sargent (1921) is
described here.
illustrated in Figure 6.3.2, and is as follows: type 1, prolongation and
pointing of the seventh cervical transverse process; type 2, short articu-
Suprapleural membrane (Sibson’s fascia)
lating rib with fibrous prolongation; type 3, jointed rib long enough to
carry the eighth cervical nerve; type 4, jointed rib fused at its end with
In its pure form, the suprapleural membrane is a thin, fan-shaped
structure attached anteriorly to the internal border of the first rib, and
posteriorly to the anterior border of the transverse process of the
seventh cervical vertebra. It covers the apical pleura and intervenes
between it and the subclavian artery. The deep part of the membrane
may be quite tough and aponeurotic (Fig. 6.3.1). The extent of its
peripheral attachment varies. Scalenus minimus is the muscle that
sometimes replaces the deep or posterior part of the membrane; it may
be up to 10 mm in diameter in its widest part but is usually much
smaller than that. The posterior border of the membrane forms, with
the edge of the first rib, the foramen through which the first thoracic
nerve escapes.
First rib


The broad first rib (see Fig. 53.9A) has a surface that is more horizontal
than vertical. It extends over the apical pleura and curves round to the
costochondral junction and then to the manubrium (see Fig. 53.8). In
the healthy state, the apical pleura is easily separable from the head and
neck, and most of the underside of the first rib; anteriorly, it becomes
rather adherent to the underside of the rib, in relation to the costo- A
chondral junction. Scalenus medius is attached to the upper surface of
the rib posteriorly. The upper portion of the nerve to serratus anterior
is usually formed in scalenus medius by branches from the ventral
primary rami of C4, 5 and 6; it emerges from the lateral surface of the
muscle to be joined by a contribution from C7. Anterior to scalenus
medius, the surface of the rib is, in the adult, grooved by the passage
of the ventral primary ramus of T1 and the lower trunk of the brachial
plexus. There is a distinct tubercle at the attachment of scalenus an-
terior; the subclavian artery lies in a slight depression posterior to the
tubercle, and the subclavian vein runs over the upper surface of the rib
anterior to the tubercle. The intercostal muscles are attached to the edge
of the rib. The lower part of the cervicothoracic (stellate) ganglion lies
on the head of the first rib, deep to the proximal part of the vertebral
artery as it arises from the first part of the subclavian artery (see Fig.
29.18). The major part of the ventral primary ramus of T1 is at first
below the rib, then medial to its edge. The preganglionic (sympathetic)
ramus of T1 connects it to the stellate ganglion; the postganglionic
ramus is less noticeable. The size and disposition of scalenus anterior
vary: it may bifurcate to include the artery; it may be bulky and its
tendon may curve posteriorly round the artery to form a kind of snare. B
Deep to scalenus anterior, a very thin fascia covers the artery. The


phrenic nerve, chiefly derived from the ventral primary ramus of C4,
Fig. 6.3.1 Entrapment of the lower trunk through an anomaly of the
curves round the muscle to run down anterior to it into the thorax,
suprapleural membrane and scalenus medius. A, The right lower trunk is
lying, at first, posterior to the internal jugular vein and crossing behind
trapped between the aponeurotic edge of scalenus medius posteriorly
the subclavian vein. The thoracic duct and the right lymphatic duct and the suprapleural membrane anteriorly. B, A ‘scalenus sickle’ and an
enter the brachiocephalic (innominate) vein at the subclavian–jugular anomalous scalenus anterior. The left lower trunk passes over the edge of
(triradiate) junction on the left and right, respectively. All of the scalene the sickle and behind the part of scalenus anterior that passes posterior
muscles vary in formation and size. Bridges of muscle and fascia may to the subclavian artery. (Courtesy of Rolfe Birch, all rights reserved,
pass between them, altering and diminishing the space available for the published in Birch R, Surgical Disorders of the Peripheral Nerve. 2nd
neurovascular bundles. edition, 2011. Springer-Verlag, London.) e63


Thoracic ouTleT syndromes
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6
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TYPE I Fig. 6.3.2 Variations of the seventh cervical rib
(purple), ranging from elongation of the seventh
cervical transverse process to a virtually
complete additional rib (after Sargent 1921).
C7 (Courtesy of Rolfe Birch, all rights reserved,
published in Birch R, Surgical Disorders of the
T1 Peripheral Nerve. 2nd edition, 2011. Springer-
Verlag, London.)
TYPE II TYPE III
Omohyoid
C7 C7
T1 T1
TYPE IV
TYPE V
C7
C7
T1
T1
the first rib or articulating with it; and type 5, a complete seventh cervi- or synchondrosis or synostosis with, a boss on the first rib at about its
cal rib with cartilaginous union to the first costal cartilage or to the middle part. The vessel is distorted by the bone and constricted by a
manubrium. leash formed by the tendon of insertion of scalenus anterior. There is
commonly dilation of the artery distal to the point of constriction, and
the dilation may proceed to the formation of a true aneurysm (Wickham
Arterial thoracic outlet syndrome
and Martin 1962). Complete obstruction of the main vessel with distal
embolization may lead to critical ischaemia. The most dangerous com-
Arterial TOS was the first of the syndromes to be recognized and the plication is contralateral hemiplegia, doubtless from embolization
first to be treated surgically. Astley Cooper wrote, ‘I have seen an exos- from a thrombus extending proximally to the carotid vessel (Symonds
tosis arise from the 6th or 7th cervical vertebrae or perhaps from both’ 1927).
(Cooper and Travers 1817). He went on to describe the case of a woman The arterial form of this outlet syndrome is a condition predomi-
who came into Guy’s Hospital with no pulse at the wrist or elbow and nantly affecting young women; the occurrence of such symptoms in
with ‘venous redness’ of the upper limb, which was cold, ‘ennumbed’ older individuals must suggest a primary diagnosis of atherosclerosis


and painful; she also had a projection of the lower cervical vertebrae or other systemic disorder. The symptoms are initially those of a Ray-
towards the clavicle, with consequent pressure on the subclavian artery. naud’s phenomenon with episodic blanching and temperature change,
Coote (1861) reported the removal of a left seventh cervical rib causing episodic pain with muscular activity, and distal ulceration and necrosis.
aneurysm of the subclavian artery. Two physicians, Lewis and Pickering The extremity may be cooler than the unaffected limb and there is likely
(1934), pointed to the mechanism of production of the arterial lesion, to be a pulse difference, even the absence of a pulse. Even if the hands
namely: intimal breakage with local thrombosis and distal emboliza- are the same colour at rest and slightly dependent, there is likely to be
tion. Arterial affection occurs as the subclavian artery crosses a ‘normal’ blanching of the affected hand on elevation. The artery is prominent,
first rib or a seventh cervical rib, commonly one with bony union to, displaced upwards and anteriorly by the underlying rib; there is a loud


Thoracic outlet syndromes
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3.6
yraTnemmoc
bruit and there may be a thrill. Doppler ultrasound examination is likely, in time, to cause intimal breakage and thrombosis. Arterial TOS
likely to show an abnormality: principally, a clamped, monophasic is uncommon rather than rare and it is potentially dangerous. The bruit
velocity signal anywhere over the arterial tree of the upper limb (Parry from a prominent subclavian artery associated with an underlying
and Eastcott 1992). Radiographs will, of course, show a seventh cervical seventh cervical rib cannot be ignored and investigations need to be
rib if one is present. Magnetic resonance angiography and duplex ultra- pursued to define the extent of distortion of the artery.
sonography have generally superseded arteriography in this field, as in
others, and will confirm the site and extent of the obstruction, the extent Neurogenic thoracic outlet syndrome
of stenosis and aneurysm formation, and the degree of distal occlusion
(Fig. 6.3.3).
Neurogenic TOS is rare. As Gilliatt (1984) pointed out, a number of
Operation is required urgently in cases of critical ischaemia, and
cases were seen at the National Hospital for Nervous Diseases, Queen
soon in cases in which ischaemia is threatened. It may be indicated
Square, London, UK, in the early years of the last century, with wasting
when a cervical rib is present, causing no symptoms but producing
of the thenar muscles that were attributed to a cervical rib. In fact, these
deformity of the subclavian artery sufficient to cause a steady bruit over
patients probably had a carpal tunnel syndrome. The confusion was not
the vessel, which must surely indicate distortion of the vessel that is
resolved for more than 40 years until the application of nerve conduc-
tion studies defined the much more common disorder. Gilliatt put the
annual incidence of cervical rib syndrome with muscle wasting as low
as 1 in 1 million in the general population. The patients are usually
young to middle-aged women and the abnormalities are usually con-
fined to one upper limb. The symptoms are insidious and often mild;
presentation is delayed for some years, and is usually occasioned by the
sudden realization that the hand has become wasted. There is pain in


the medial aspect of the forearm and there may also be some blunting
of sensibility in that area and in the little finger. The latter is frequently
shorter than it is in a normal, age-matched hand, suggesting that the
affliction of the fibres in the lower trunk commenced before skeletal
maturity. There is wasting of the superficial thenar muscles, which
sometimes extends to all of the small muscles of the hands (Fig. 6.3.4)
A
A
B
B
Fig. 6.3.4 The classical neurogenic outlet syndrome; shortening of the
little finger is often evident. A, Severe wasting of the intrinsic muscles of
C the right hand in a 35-year-old woman. B, The right lower trunk is seen
angulated over a ‘scalenus sickle’ and there is extreme attenuation of the
Fig. 6.3.3 Arterial thoracic outlet syndrome: angiographic appearances. trunk, which, in the photograph, appears to be rather lateral to the sickle.
A, Complete occlusion over a cervical rib. B, Complete occlusion at the When the nerve was first exposed at operation, the zone of attenuation
thoracic outlet in a 40-year-old woman, a heavy smoker. C, Obstruction was, in fact, at the site of angulation. There was slow improvement after
of the artery at the thoracic outlet on elevation of the limb. (Courtesy of decompression. (Courtesy of Rolfe Birch, all rights reserved, published in
Rolfe Birch, all rights reserved, published in Birch R, Surgical Disorders of Birch R, Surgical Disorders of the Peripheral Nerve. 2nd edition, 2011.
the Peripheral Nerve. 2nd edition, 2011. Springer-Verlag, London.) Springer-Verlag, London.)


Thoracic ouTleT syndromes
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6
noiTces
and there may be weakness of the flexor muscles of the forearm, most Neural thoracic outlet syndrome without
evident in those innervated by the ulnar nerve. There may be a bruit plain motor signs
over the subclavian artery. Radiographs of the neck show rudimentary
cervical ribs or elongated transverse processes of the seventh cervical
Neural TOS without plain motor signs is more common and more dif-
vertebrae. The diagnostic electrophysiological findings were character-
ficult. Patients present with symptoms and signs consistent with a diag-
ized by Gilliatt, Le Quesne and Logue in 1970 and include a small or
nosis of TOS but studies of blood flow and nerve conduction are
absent sensory response in the ulnar nerve and the medial cutaneous
normal. It is important to seek causes of the symptoms beyond the
nerve of the forearm; a normal sensory response in the median nerve;
apparent diagnosis and to remember that the presence of a cervical rib
an attenuated compound motor action potential amplitude from
does not, of itself, permit a diagnosis of TOS. The urge to advise opera-
abductor pollicis brevis; and a low-amplitude ulnar motor response
tion should be tempered with knowledge of the possibility of complica-
(Smith and Knight 2011). Operation is indicated in these patients in
tions and the high rate of recurrence of symptoms as time passes (Birch
the expectation of alleviation of pain, improvement in sensation and
2011).
some improvement in strength; recovery of the wasted small muscles
of the hand is rare.
REFERENCES
Birch R 2011 Operating on peripheral nerves. In: Birch R (ed.) Surgical upon gangrene of the digits: observations relevant to so-called ‘Ray-
Disorders of the Peripheral Nerves. London: Springer; Ch. 7, naud’s disease’. Clin Sci 1:327–66.
pp 231–302. Parry EW, Eastcott HHG 1992 Cervical rib and thoracic outlet syndrome. In:
Cooper A, Travers B 1817 On exostosis. In: Cooper A, Travers B (eds) Surgical Eastcott HHG (ed) Arterial Surgery, 3rd ed. Edinburgh: Churchill Liv-


Essays, 2nd ed. London: Cox & Son, p. 171. ingstone, pp. 333–53.
Coote H 1861 Exostosis of the left transverse process of the seventh cervical Sargent P 1921 Lesions of the brachial plexus associated with rudimentary
vertebra, surrounded by blood vessels and nerves, successful removal. ribs. Brain 44:95–124.
Lancet 1:360–1. Smith S, Knight R 2011 Clinical neurophysiology in peripheral nerve inju-
Gilliatt RW 1984 Thoracic outlet syndrome. In: Dyck PJ, Thomas PK, ries. In: Birch R (ed.) Surgical Disorders of the Peripheral Nerves.
Lambert EH et al (eds) Peripheral Neuropathy, 2nd ed. Philadelphia: London: Springer; Ch. 6, pp. 191–230.
WB Saunders, pp. 1409–24. Symonds CP 1927 Cervical rib: thrombosis of subclavian artery, contra-
Gilliatt RW, Le Quesne PM, Logue V 1970 Wasting of the hand associated lateral hemiplegia of sudden onset, probably embolic. Proc Roy Soc
with a cervical rib or band. J Neurol Neurosurg Psychiatry 33:615–24. Med 20:1244–5.
Lewis T, Pickering GW 1934 Observations upon maladies in which the Wickham JEA, Martin P 1962 Aneurysm of the subclavian artery in associa-
blood supply to the digits ceases intermittently or permanently and tion with cervical abnormality. Br J Surg 50:205–9.


CHAPTER
51
Thorax: overview and surface anatomy
The thorax is the upper part of the trunk. It consists of an external
MUSCULOSKELETAL FRAMEWORK
musculoskeletal cage, the thoracic wall, and an internal cavity that
contains the heart, lungs, oesophagus, trachea and principal bronchi,
thymus, vagus and phrenic nerves, right and left sympathetic trunks, BONES AND JOINTS
thoracic duct, lymph nodes, and major systemic and pulmonary blood
vessels. Inferiorly, the thorax is separated from the abdominal cavity by The thoracic skeleton consists of twelve thoracic vertebrae and their
the diaphragm; superiorly, it communicates with the neck and the intervening intervertebral discs (midline, posterior), twelve pairs of ribs
upper limbs. The thoracic wall offers protection to some of the abdomi and their costal cartilages (predominantly lateral), and the sternum
nal viscera: the greater part of the liver lies under the right dome of (midline, anterior). When articulated, they form an irregularly shaped
the diaphragm; the stomach and spleen lie under the left dome of osteocartilaginous cylinder, reniform in horizontal section, which is
the diaphragm; and the posterior aspects of the superior poles of the narrow above, broad below, flattened anteroposteriorly and longer
kidneys lie on the diaphragm and are anterior to the twelfth rib on the behind (see Fig. 53.8). Laterally, the thoracic cage is convex and is
right, and to the eleventh and twelfth ribs on the left (Fig. 51.1). formed by the ribs; anteriorly, it is slightly convex and is formed by the
Variations in thoracic dimensions and proportions are partly indi sternum and the distal parts of the ribs and their costal cartilages. The
vidual and also linked to age, sex and race. At birth, the transverse first seven pairs of ribs are connected to the sternum by costal cartilages,
diameter is relatively less than it is in the adult, but adult proportions the costal cartilages of the eighth to tenth ribs usually join the super
develop as walking begins. Thoracic capacity is less in females than jacent cartilage, and the eleventh and twelfth ribs are free (floating) at


it is in males, both absolutely and proportionately: the female sternum their anterior ends. The posterolateral curvature of the ribs, from their
is shorter, the thoracic inlet more oblique, and the suprasternal notch vertebral ends to their angles, produces a deep internal groove, the
is level with the third thoracic vertebra, whereas it is level with the paravertebral gutter, on either side of the vertebral column. The ribs and
second thoracic vertebra in males. In all individuals, the size of the costal cartilages are separated by intercostal spaces, which are deeper
thoracic cavity changes continuously according to the movements of anteriorly and between the upper ribs. Each space is occupied by three
the ribs and diaphragm during respiration (Ch. 55) and the degree of layers of flat muscles and their aponeuroses, neurovascular bundles and
abdominal visceral distension. lymphatic channels.
The narrow thoracic inlet (superior thoracic aperture) typically
measures 5 cm anteroposteriorly and 10 cm transversely. It is bounded
Vertebral column Superior thoracic aperture
by the first thoracic vertebral body posteriorly, the medial border of the
Right pleural
cavity Mediastinum first ribs on each side, and the superior border of the manubrium sterni
anteriorly. It slopes down and forwards, so that the apex of the lung
First rib extends upwards into the neck behind the anterior end of the first rib;
Left pleural cavity structures that pass between the thorax and the upper limb therefore
pass over the first rib and the apices of the lungs and the apical pleurae.
The broad thoracic outlet (inferior thoracic aperture) is limited pos
teriorly by the twelfth thoracic vertebral body, posterolaterally by the
Manubrium sterni twelfth rib and the distal end of the eleventh rib, anterolaterally by the
distal cartilaginous ends of the seventh to tenth ribs (which unite and
ascend to form the costal margin), and anteriorly by the xiphoid
Manubriosternal joint
process. It is wider in the transverse plane than in the sagittal plane and
slopes obliquely inferiorly and posteriorly, so that the thoracic cavity is
Cardiac notch deeper posteriorly than anteriorly.


of left lung The horizontal sternal plane is traditionally reported to pass through
the intervertebral disc between the fourth and fifth thoracic vertebrae
posteriorly and the manubriosternal joint (sternal angle or angle of
Body of sternum Louis) at the level of the second costal cartilage anteriorly. Recent data
place the sternal angle between the fourth thoracic vertebra and the
upper half of the fifth thoracic vertebra in the majority of adults (Mir
jalili et al 2012a). The sternal plane separates the superior mediastinum
from the inferior mediastinum and marks the positions of the superior
limits of the pericardium; the bifurcation of the pulmonary trunk; the
origin of the arch of the aorta; the level at which the trachea bifurcates
into right and left principal bronchi; and the site where the superior
vena cava penetrates the pericardium to enter the right atrium.
Diaphragm MUSCLES
Xiphoid process
Intrinsic and extrinsic muscles
The intrinsic muscles of the chest wall are the intercostal muscles, sub
costalis, transversus thoracis, levatores costarum and serratus posterior
Inferior thoracic aperture
superior and inferior.
The uncommon variants, sternalis and rectus thoracis bifurcalis, are
Fig . 51 .1 The thoracic wall and cavity . (With permission from Drake RL, important clinically as they may mimic a focal density in medial breast
Vogl AW, Mitchell A (eds), Gray’s Anatomy for Students, 2nd ed, Elsevier, craniocaudal mammograms and be encountered during reconstructive
898 Churchill Livingstone . Copyright 2010 .) surgery of the breast and chest wall (p. 942).


Vascular supply and lymphatic drainage
899
15
rETPahC
The intercostal muscles occupy each of the intercostal spaces and are recesses such as the costodiaphragmatic recess, which separates the
named according to their surface relations, i.e. external, internal and costal and diaphragmatic pleura, in deep breathing.
innermost. All except levatores costarum are innervated by the adjacent The left pleural cavity is the smaller of the two pleural cavities
intercostal nerves derived from the ventral rami of the thoracic spinal because the heart extends further to the left.
nerves; levatores costarum are innervated by the dorsal rami of the
thoracic spinal nerves. The intrinsic muscles can elevate or depress the
rib and are particularly active in forced respiration; their primary action MEDIASTINUM
is believed to be to stiffen the chest wall, preventing paradoxical move
ment during inspiration. The mediastinum lies between the right and left pleural sacs in and near
The skeletal framework of the thoracic wall provides extensive the median sagittal plane of the chest (Ch. 56). It extends from the
attachment sites for muscles associated functionally with the neck, sternum anteriorly to the vertebral column posteriorly. A horizontal
abdomen, back and upper limbs. Some of them (scalenes, infrahyoid plane passing through the manubriosternal joint, and the intervertebral
strap muscles, sternocleidomastoid, serratus anterior, pectoralis major disc between the fourth and fifth thoracic vertebrae separates the media
and minor, external and internal obliques, and rectus abdominis) func stinum into superior and inferior portions.
tion as accessory muscles of respiration and are usually active only
during forced respiration; scalenus medius is active in quiet inspiration. Superior mediastinum
Scalenus anterior, medius and posterior are described in Chapter 29.
Trapezius, latissimus dorsi, rhomboid major, rhomboid minor, levator
The superior mediastinum lies between the manubrium sterni anteri
scapulae, pectoralis major and minor, subclavius and serratus anterior
orly and the upper thoracic vertebrae posteriorly, and is limited laterally


are described in Chapter 48. Rectus abdominis, external oblique and
by the pleurae. Its inferior boundary is a slightly oblique plane that
internal oblique are described in Chapter 61.
passes backwards from the manubriosternal joint to the lower part of
the body of the fourth thoracic vertebra. It contains the lower ends of
Diaphragm sternohyoid, sternothyroid and longus colli on each side; the aortic
arch, brachiocephalic trunk and thoracic portions of the left common
The diaphragm, a curved musculotendinous sheet attached to the cir carotid and left subclavian arteries; the brachiocephalic veins and upper
cumference of the thoracic outlet and to the upper lumbar vertebrae, half of the superior vena cava; the left highest intercostal vein; the vagus,
forms the floor of the thoracic cavity, separating it from the abdominal cardiac, phrenic and left recurrent laryngeal nerves; and the trachea,
cavity (Ch. 55). The diaphragm is relatively flat centrally and domed oesophagus, thoracic duct, thymic remnants and lymph nodes.
peripherally, rising higher on the right side than on the left, an asym
metry that reflects the relative densities of the underlying liver and Inferior mediastinum
gastric fundus, respectively. From its most superior point on each side,
the diaphragm slopes inferiorly to its costovertebral attachments; this The inferior mediastinum is divided into three parts: anterior, in front
slope is most marked posteriorly, where the space between the dia of the pericardium; middle, containing the pericardium and its contents
phragm and the posterior wall of the thorax is very narrow. The domes (Ch. 57); and posterior, behind the pericardium.
are higher in the supine position. During quiet respiration in the erect
position, diaphragmatic excursion is about 2 cm in both sexes, increas Anterior mediastinum The anterior mediastinum exists only on the
ing to around 7 cm during deep breathing (Boussuges et al 2009); left side where the left pleura diverges from the midsternal line. It is


values are greater in men and possibly increase further in the supine bounded anteriorly by the sternum, laterally by the pleurae, and poste
position (Takazakura et al 2004). riorly by the pericardium. It is narrow above but widens a little below.
Its anterior wall is formed by the left transversus thoracis and the fifth
Diaphragmatic openings
to seventh left costal cartilages. It contains a quantity of loose areolar
The inferior vena cava passes through an opening in the central tendon tissue, lymphatic vessels that ascend from the convex surface of the liver,
of the diaphragm to enter the right side of the mediastinum at the two or three anterior mediastinal lymph nodes, and the small media
level of the eighth thoracic vertebra; the oesophagus passes through stinal branches of the internal thoracic artery.
the muscular part of the diaphragm and enters the abdomen just to
the left of the midline at the level of the tenth thoracic vertebra; and Middle mediastinum The middle mediastinum is the broadest part
the descending thoracic aorta passes posterior to the diaphragm in the of the interpleural space; it contains the heart enclosed in the pericar
midline at the level of the twelfth thoracic vertebra (see Fig. 55.1). dium; the ascending aorta; the lower half of the superior vena cava with
Other structures that pass between the thorax and abdomen include the azygos vein opening into it; the bifurcation of the trachea and the
the right and left vagi, phrenic and subcostal nerves, thoracic duct, right and left principal bronchi; the pulmonary artery dividing into its
sympathetic trunks, thoracic splanchnic nerves, right and left superior two branches; the right and left pulmonary veins and phrenic nerves;
epigastric arteries, and the hemiazygos and accessory hemiazygos and some bronchial lymph nodes.
veins.
According to a CT study, the inferior vena cava and the oesophagus Posterior mediastinum The posterior mediastinum is an irregular
traverse the diaphragm at the upper and lower borders, respectively, of triangular space, bounded anteriorly by the pericardium above and the


the eleventh thoracic vertebra; these levels are lower than those based posterior surface of the diaphragm below, posteriorly by the vertebral
on cadaveric/radiographic studies (eighth and tenth thoracic vertebrae, column from the lower border of the fourth to the twelfth thoracic
respectively) (Mirjalili 2012a). vertebrae, and laterally by the mediastinal pleura. It contains the tho
racic part of the descending aorta, the azygos and hemiazygos veins, the
vagus and splanchnic nerves, oesophagus, thoracic duct and lymph
THORACIC CAVITY nodes.
PLEURAL CAVITIES
VASCULAR SUPPLY AND LYMPHATIC DRAINAGE
The right and left pleural cavities are separate compartments on either
side of the mediastinum. Each encloses a lung and its associated bron ARTERIES
chial tree, and vessels, nerves and lymphatics (Ch. 54). The walls are
formed by a serous membrane, the pleura, arranged as a closed sac. The The skin of the thorax is supplied by direct cutaneous vessels and mus
outer layer of the sac, the parietal pleura, lines the corresponding half culocutaneous perforators, which reach the skin primarily via the inter
of the thoracic wall and covers much of the diaphragm and structures costal muscles, pectoralis major, latissimus dorsi and trapezius. Branches
occupying the middle region of the thorax. The inner or visceral layer from the thoracoacromial axis, lateral thoracic, internal thoracic, ante
is more delicate and adheres closely to the pulmonary surface, follow rior and posterior intercostal, thoracodorsal, transverse cervical, dorsal
ing the interlobar fissures. The two layers are continuous with each scapular and circumflex scapular arteries are the major contributing
other around the hilar structures, and remain in close, though sliding, vessels (see Figs 43.4, 53.1–53.2).
contact at all phases of respiration. The potential space between them Muscles of the thoracic wall receive their blood supply from the
is the pleural cavity, which is maintained at a negative pressure by the internal thoracic artery (either directly or via the musculophrenic


inward elastic recoil of the lung and the outward pull of the chest wall. artery), the superior intercostal artery (from the costocervical trunk),
The lungs do not fill this space in quiet respiration, but move into superior thoracic artery (from the axillary artery), descending thoracic


ThOrax: OVErVIEw aNd SurfaCE aNaTOmy
900
7
NOITCES
Superior thoracic artery Brachiocephalic vein
Posterior Superior intercostal vein
Superior intercostal vein
intercostal artery Costocervical trunk
Brachiocephalic vein
Collateral branch Posterior intercostal vein
of posterior
intercostal Subclavian artery
artery
Azygos vein
Accessory
Descending hemiazygos vein
thoracic aorta
Internal
Internal thoracic
thoracic artery
vein
Anterior perforating
branches Anterior
perforating
branches
Anterior
intercostal artery
Musculophrenic artery
Hemiazygos vein
Superior
epigastric artery
Anterior intercostal vein
Fig . 51 .2 Arteries of the thoracic wall and thoracic aorta . (With permission
Fig . 51 .3 Veins of the thoracic wall and azygos system . (With permission
from Drake RL, Vogl AW, Mitchell A, Tibbitts R, Richardson P (eds),
from Drake RL, Vogl AW, Mitchell A, Tibbitts R, Richardson P (eds),
Gray’s Atlas of Anatomy, Elsevier, Churchill Livingstone . Copyright 2008 .)
Gray’s Atlas of Anatomy, Elsevier, Churchill Livingstone . Copyright
2008 .)
aorta, and the subcostal artery (Fig. 51.2). Additional contributions
come from vessels that supply the proximal muscles of the upper limb,
namely: suprascapular, superficial cervical, thoracoacromial, lateral of the sympathetic trunk by pre and postganglionic branches (white
thoracic and subscapular arteries. and grey rami communicantes, respectively). Intercostal nerves are dis
The detailed arterial supply of the thoracic viscera is described with tributed primarily to the thoracic and abdominal walls. The greater part
the viscera. of the first thoracic ventral ramus passes into the brachial plexus,
together with a variable proportion of the second. The next four ventral
supply only the thoracic wall, and the lower five supply both thoracic
VEINS and abdominal walls. The subcostal nerve is distributed to the abdomi
nal wall and the gluteal skin. Communicating branches link the inter


The intercostal veins accompany the similarly named arteries in the costal nerves posteriorly in the intercostal spaces, and the lower five
intercostal spaces (Fig. 51.3). The small anterior intercostal veins are nerves communicate freely in the abdominal wall. Thoracic dorsal rami
tributaries of the internal thoracic and musculophrenic veins; the inter divide into medial and lateral branches that supply the intrinsic muscles
nal thoracic veins drain into the appropriate brachiocephalic vein. The of the back and the overlying postvertebral skin on a segmental basis
posterior intercostal veins drain backwards, and most drain directly or (see Fig. 43.3).
indirectly into the azygos vein on the right and the hemiazygos or The supraclavicular branches of C4 from the cervical plexus inner
hemiazygos veins on the left. The azygos veins exhibit great variation vate the skin over the clavicle and may communicate with the anterior
in their origin, course, tributaries, anastomoses and termination. cutaneous branches of the second thoracic ventral ramus (p. 443).
LYMPHATIC DRAINAGE
AUTONOMIC INNERVATION
Superficial lymphatic vessels of the thoracic wall ramify subcutaneously
The autonomic nervous system in the thorax consists of right and left
and converge on the axillary nodes (see Fig. 53.22). Lymph vessels from
sympathetic trunks and vagus nerves, and the cardiac, oesophageal and
deeper tissues of the thoracic walls drain mainly to the parasternal,
pulmonary plexuses.
intercostal and diaphragmatic lymphatic nodes.
Sympathetic trunks
INNERVATION
The ganglionated sympathetic trunks lie anterior to the heads of the
THORACIC SPINAL NERVES ribs; the ganglia are arranged segmentally (see Fig. 56.6). Preganglionic
sympathetic axons originate from neurones in the lateral grey column
There are twelve pairs of thoracic spinal nerves. The ventral rami, unlike of the spinal cord from T1 to L2, and leave the spinal cord with the
their cervical and lumbar counterparts, have retained a largely segmen corresponding ventral roots as white rami communicantes. Their targets


tal distribution to the body wall (see Figs 16.10, 53.3). The upper eleven vary. Some enter the sympathetic trunk, where they either synapse in
lie between the ribs (intercostal nerves), and the twelfth lies below the their segmental ganglion, or ascend or descend in the trunk to synapse
last rib (subcostal nerve). Each is connected with the adjoining ganglion in cervical or lumbar ganglia. Many of the preganglionic axons that


Surface anatomy
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originate in the lower thoracic spinal segments (T5–12) do not synapse the nipple is dependent on the size and shape of the breasts. In adult
locally but enter the abdominal cavity as the thoracic splanchnic nerves; males, the nipple is usually sited either in the fourth intercostal space
they synapse either in prevertebral ganglia, especially the coeliac gan or over the fifth rib in the midclavicular line, approximately 20 cm
glion (Ch. 59), or around the medullary chromaffin cells of the supra from the sternal notch and midclavicular point (Beckenstein et al
renal gland (Ch. 71). Axons destined for the cervical ganglia are derived 1996). The pigmented areola surrounding the nipple varies in size.
from preganglionic neurones in T1.
SKELETAL LANDMARKS
Vagus nerves in the thorax
Anteriorly, the clavicle, sternoclavicular and acromioclavicular joints are
Preganglionic parasympathetic fibres arise from neuronal cell bodies in
both palpable and visible in all but obese individuals (Fig. 51.4). The
the dorsal motor nucleus of the vagus in the medulla. Those destined
sternum may be felt throughout its length in the midline, although
for the thoracic viscera travel in the pulmonary, cardiac and oesopha
laterally it may be covered by pectoralis major. The jugular (supraster
geal branches of the vagus and synapse in minute ganglia in the visceral
nal) notch is palpable in the midline at the superior sternal border and
walls. Axons travelling in cardiac branches join the cardiac plexuses and
typically lies at the level of the junction between the second and third
synapse in ganglia distributed over both atria; when stimulated, they
thoracic vertebrae. The cartilaginous rings of the trachea are palpable
slow the cardiac cycle (Ch. 57). Pulmonary branches contain axons that
immediately superior to the notch, using a posteriorly directed finger.
relay in ganglia of the pulmonary plexuses; they are motor (broncho
The manubriosternal angle is more pronounced in the male than in the


constrictor) to the circular nonstriated muscle fibres of the bronchi and
female, and is palpable at the junction of the manubrium with the
bronchioles, and secretomotor to the mucous glands of the respiratory
sternal body. It serves as a useful landmark because it indicates the level
epithelium.
of the sternal plane and the medial ends of the second costal cartilages,
and so offers an accurate point at which to start counting ribs. In the
Autonomic plexuses in the thorax majority of adults, the sternal angle is located between the fourth tho
racic vertebra and the upper half of the fifth thoracic vertebra, with a
Cardiac plexus The cardiac plexus has a superficial component range from the lower half of the second thoracic vertebra to the lower
inferior to the aortic arch, lying between it and the pulmonary trunk, half of the sixth thoracic vertebra, a linear distance of about 8 cm; the
and a deep part between the aortic arch and tracheal bifurcation (Ch. plane lies at a slightly higher vertebral level in women. The xiphisternal
57). The superficial part is formed by the cardiac branch of the left joint and xiphoid process are palpable at the inferior end of the sternum;
superior cervical sympathetic ganglion and the lower of the two cervical the joint usually lies at the level of the ninth thoracic vertebra. The
cardiac branches of the left vagus. The deep part is formed by the cardiac costal margin is palpable passing inferolaterally from the xiphisternum.
branches of the cervical and upper thoracic sympathetic ganglia and of Posteriorly, the free ends of the eleventh and twelfth ribs may be
the vagus and recurrent laryngeal nerves. The only cardiac nerves that
do not join it are those that join the superficial part of the plexus.
Branches from the cardiac plexuses also form the left and right coronary
and atrial plexuses.
3
Pulmonary plexus The pulmonary plexuses are anterior and poste 2 4 2
5
rior to the other structures at the hila of the lungs (Ch. 54). They are 1
6 7
formed by cardiac branches from the second to fifth (or sixth) thoracic A
sympathetic ganglia and from the vagus and cervical sympathetic


B
cardiac nerves. The left plexus also receives branches from the left recur
8
rent laryngeal nerve.
9
B*
Oesophageal plexus The oesophageal plexus surrounds the 10 C D
oesophagus below the level of the lung roots (Ch. 56). Vagal fibres 12
either pass through the plexus or are given off directly by the vagus in 11 13
the thorax. All fibres relay in the oesophageal wall and are motor to the
smooth muscle in the lower oesophagus and secretomotor to mucous 14 14
glands in the oesophageal mucosa. Vasomotor sympathetic fibres arise
from the upper six thoracic spinal cord segments. Those from the upper
segments synapse in cervical ganglia; postganglionic axons innervate 15
the vessels of the cervical and upper thoracic oesophagus. Fibres from
the lower segments pass directly to the oesophageal plexus or to the
coeliac ganglion, where they synapse; postganglionic axons innervate
the vessels of the distal oesophagus.
Fig . 51 .4 Surface anatomy of the anterior thorax . Key: 1, right
SURFACE ANATOMY
acromioclavicular joint; 2, clavicle and mid-clavicular line (dashed black);
3, apex of right lung, located posterior to the medial third of the clavicle;
In clinical practice, an evidencebased knowledge of thoracic surface 4, sternal notch of manubrium sterni: the trachea may be located here by
anatomy underpins practical procedures such as placing drains or cath posterior palpation; 5, sternoclavicular joint: marks the junction of the
eters and siting surgical incisions. The accuracy of some older descrip internal jugular and subclavian veins to form the brachiocephalic vein; 6,
tions of clinically important surface landmarks, based on cadaveric or zone of formation of the superior vena cava: from first intercostal space
radiographic studies, has been questioned recently (Hale et al 2010). to second costal cartilage level (78% of subjects, white zone); 7, sternal
Crosssectional computed tomography (CT) imaging, undertaken with angle: marks the level of the sternal plane and the second costal


subjects supine, at end tidal inspiration, and with arms abducted, has cartilage; 8, pectoralis major and the anterior axillary fold; 9, horizontal
emphasized a greater interindividual variation in some thoracic surface fissure; 10, right oblique fissure; 11, lower anterior border of the right
lung: typically, either the sixth intercostal space or the seventh rib in the
anatomy landmarks than appears in the current anatomical literature
mid-clavicular line; 12, lower anterior border of the left lung: typically,
(Mirjalili et al 2012a).
either at the fifth rib or fifth intercostal space in the mid-clavicular line; 13,
xiphisternum; 14, costal margin; 15, tenth costal cartilage, forming the
lower part of the costal margin . A–D and blue line: conventional surface
BREAST
markings of the heart . A overlies the left second costal cartilage; B
overlies the right third costal cartilage; B*, zone of the superior vena cava
In females, the base of the breast is relatively constant in position; it meeting the right atrium from the fourth to fifth costal cartilage in 71% of
extends vertically from the second or third to the sixth rib, and from subjects at end tidal inspiration (from CT data); C, right sixth costal
the lateral sternal border medially almost to the midaxillary line later cartilage; D, zone of location of the cardiac apex: almost always from the
ally. The tail of the breast extends towards the axilla along the infero level of the fifth to the sixth rib, and a mean of 8 .7 ± 1 cm from the
lateral border of pectoralis major (Ch. 53). In adult females, the site of midline .


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1 1
1
2 2
3 3
T3
2
4 5
6
T9
7
8
3 T12 9
L1
4
Fig . 51 .5 Surface anatomy of the posterior thorax . The levels of the Fig . 51 .6 Surface anatomy of the great vessels and tracheobronchial tree
spinous processes of the third, ninth and twelfth thoracic vertebrae and relative to bony landmarks . Key: 1, internal jugular vein; 2, subclavian
the first lumbar vertebra are indicated in the midline . Key: 1, border of the vein; 3, formation of the brachiocephalic vein posterior to the
left lung; 2, oblique fissure: passes anteroinferiorly from the spinous sternoclavicular joints; 4, formation of the superior vena cava, posterior to
process of the third thoracic vertebra to cross the fifth rib in the mid- the right second costal cartilage or first intercostal space; 5,
axillary line . The upper lobe sits superiorly and the lower lobe inferiorly; manubriosternal joint, 6, concavity of the aortic arch, typically sitting
3, lower border of the lung: this is often located at level of the twelfth inferior to the sternal plane, level with the upper half of the fifth thoracic
thoracic vertebra but may be lower, at the level of the first lumbar vertebra; 7, azygos vein entering the superior vena cava: typically, it sits
vertebra, adjacent to the vertebral column at end tidal inspiration . Dashed inferior to the sternal plane, level with the lower half of the fifth thoracic
blue lines indicate the range of levels for the lower border of the lung vertebra; 8, tracheal bifurcation: typically, it sits inferior to the sternal
(ninth thoracic vertebra to first lumbar vertebra); 4, twelfth rib: can be plane, level with the upper half of the sixth thoracic vertebra; 9,


traced superomedially to aid identification of the spinous process of the bifurcation of the pulmonary trunk, level with the upper half of the sixth
twelfth thoracic vertebra . thoracic vertebra, approximately 3 cm inferior to the sternal angle .
(Redrawn with permission from Mirjalili S, Hale S, Buckenham T, Wilson
B, Stringer M . 2012 . A reappraisal of adult thoracic surface anatomy . Clin
palpable. Tracing the twelfth rib superomedially aids identification of Anat 25:827–34 .)
the spinous process of the twelfth thoracic vertebra (Fig. 51.5). In thin
individuals, it is possible to palpate all the ribs anteriorly, from the first
to the costal margin. Posteriorly, the spinous processes of the thoracic Table 51.1 The level of key thoracic viscera relative to the sternal plane
vertebrae are palpable; the spinous process of the first thoracic vertebra and vertebrae
sits below that of the seventh cervical vertebra (vertebra prominens)
Mean position Most common Sex differences
and is often more prominent. The angles of the ribs are palpable several
relative to sternal position/level (95% CI)
centimetres lateral to the spinous processes of the vertebrae. plane (Range, cm) (frequency % of 153
The surface anatomy of the back is described in Chapter 43. subjects studied)
Tracheal −3.1 cm T6 (46%) 1.3 cm higher in
bifurcation (0 to −7.5) (lower T4 to lower T7) females
MUSCULOTENDINOUS LANDMARKS
(0.8–1.8 cm: p < 0.001)
Aortic arch −1.1 cm T5 (55%) 0.6 cm higher in
In a lean, muscular subject, pectoralis major, the slips of serratus ante concavity (+2.8 to −4.8) (lower T3 to lower T6) females
rior, latissimus dorsi, trapezius, external oblique and rectus abdominis (0.1–1.1 cm: p = 0.01)


are all easily visible. In females, the breasts may significantly obscure Azygos vein −2 cm T5 (49%) 0.7 cm higher in
the anterior thoracic wall. joining the (+1.3 to −6.4) (upper T4 to upper T7) females
superior vena (0.3–1.2 cm: p = 0.001)
cava
INTRATHORACIC VISCERA Pulmonary trunk Not reported T6 upper (28%) No significant effect
bifurcation (T4/5 to T7/8)
The sternal plane represents the lower border of the superior mediasti
Measurements relative to the sternal plane are shown as + (superior to the plane) and − (inferior to the
num. At this point, the right and left pleurae are in contact with each
plane). Adapted from Mirjalili S, Hale S, Buckenham T, Wilson B, Stringer M. 2012. A reappraisal of adult
other; it is therefore a useful starting point when delineating the surface thoracic surface anatomy. Clin Anat. Oct;25(7):827–34.
markings of the parietal pleura (see Fig. 51.7). The sternal plane is
conventionally described as lying over the tracheal bifurcation, the
concavity of the aortic arch and the point where the azygos vein enters latter point, as represented by the junction between the superior vena
the superior vena cava. CT analysis places these three major surface cava and right atrium, most commonly between the fourth and fifth
landmarks typically a little lower, at the level of the fifth or sixth thoracic right costal cartilages. The right border is a gently curved line, convex
vertebra rather than in the plane of the sternal angle (between the to the right, running from the third to the sixth right costal cartilages,
fourth and fifth thoracic vertebrae) (Mirjalili et al 2012a) (Fig. 51.6; usually 1–2 cm lateral to the sternal edge. The inferior or acute border
Table 51.1). runs leftwards from the sixth right costal cartilage to the cardiac apex,
located approximately 9 cm lateral to the midline, often in the left fifth
Heart


intercostal space or level with the fifth or sixth rib. Clinicians vary when
locating the midclavicular line (Naylor et al 1987); a measurement
The cardiac surface projections described below apply to an average from the midline is preferable. The most inferolateral point at which a
adult. They may be modified by age, sex, stature, ventilation, the posi pulsation is visible and palpable is called the cardiac apex beat and is
tion of the diaphragm and posture (Macklin 1925). The projection of usually palpable near the cardiac apex.
the cardiac borders on to the anterior thoracic wall forms a trapezoid. The left (‘obtuse’) border is convex laterally and extends superome
The area of cardiac dullness may be mapped out via percussion. dially from the cardiac apex to meet the second left costal cartilage
The upper border slopes gently from the second left costal cartilage approximately 1 cm from the left sternal edge. An oblique line joining
to the third right costal cartilage (see Fig 51.4). CT analysis places the the sternal end of the third left and sixth right costal cartilages


Surface anatomy
903
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represents the anterior part of the coronary sulcus/atrioventricular reflection (the costodiaphragmatic recess) and may retreat from the
groove, which separates the right atrium from the right ventricle. The retrosternal costomediastinal recess.
projections of the cardiac valves, although in different planes, are also
Trachea and bronchi
sited along or close to this line (see Fig. 57.19). The orifice of the pul
monary valve is represented by a horizontal line approximately 2.5 cm The trachea starts at the level of the inferior border of the cricoid carti
long that lies over the superior border of the left third costal cartilage lage, which usually sits at the level of the seventh cervical vertebra
and behind the corresponding region of the sternum. The pulmonary (range C5 to T1) (Mirjalili et al 2012b). It runs inferiorly in the midline
trunk is delineated by two parallel lines drawn perpendicular to the and bifurcates level with the upper half of the sixth thoracic vertebra,
ends of the pulmonary valve line, up to the level of the left second i.e. inferior to the sternal angle, and lower than was previously believed
intercostal space. The orifice of the aortic valve is located below and to (see above). The trachea is palpable immediately superior to the
the right of the orifice of the pulmonary valve, and is represented by a suprasternal notch either by rolling one finger over its convex surface
line approximately 2.5 cm long running inferolaterally and to the right or by defining its lateral extents with two fingers. A shift to one side
from the medial end of the left third intercostal space. Two parallel indicates that the mediastinum has either been pulled over to that side
lines, drawn perpendicular to the ends of the valve line and slanting up by loss of lung volume, or pushed over by a pneumothorax or pleural
towards the right half of the manubriosternal joint, outline the location effusion. The level at which the trachea bifurcates moves down, on
of the ascending aorta. average, by a mean of 3 mm per decade.


The orifice of the tricuspid valve is represented by a line approxi
Pulmonary fissures
mately 4 cm long that starts near the midline just below the level of the
right fourth costal cartilage and passes down and slightly to the right. On either side, the upper and lower lobes of the lung are separated by
The centre of this line should be level with the middle of the right the oblique fissure. This can be marked by a line that runs anteroinfe
fourth intercostal space. The orifice of the mitral valve is level with the riorly from the posterior end of the fourth rib (spinous process of the
left half of the sternum opposite the left fourth costal cartilage and is third thoracic vertebra), crosses the fifth rib in the midaxillary line and
represented by a line approximately 3 cm long and descending to continues inferiorly, crossing either the sixth intercostal space/seventh
the right. rib on the right or the fifth rib/intercostal space on the left, on both
The direction of blood flow through a valve carries the valve sound sides at the midclavicular line (i.e. 7–8 cm lateral to the midline). As
with it and thus the sites of cardiac valve auscultation do not corre a convenient approximation, the oblique fissure follows the medial
spond to the surface anatomy of the valves. Convenient sites at which border of the scapula when the upper limb is in full abduction. The left
to auscultate using a stethoscope are: the sternal end of the left second oblique fissure may be slightly more vertical than the right.
intercostal space (pulmonary area); the sternal end of the right second The horizontal fissure lies between the upper and middle lobes
intercostal space (aortic area); near the cardiac apex (mitral area); and of the right lung (see Fig. 51.4; Fig. 51.7). It extends from the fourth
over the left lower sternal border, at the level of the fifth intercostal costal cartilage at the right sternal border to intersect the oblique fissure.
space (tricuspid area) (see Fig. 57.19). The right middle lobe may be projected on to the thoracic wall using


three points, namely: the fourth costal cartilage at the right parasternal
Great vessels edge, the fifth rib at the midaxillary line and the sixth intercostal
space/seventh rib at the midclavicular line. The upper and middle lobes
lie anterior to the oblique fissure and are best examined from in front
The aortic arch lies mainly posterior to the manubrium (see Fig. 51.6).
and to the side. The lower lobes lie posteriorly and should be examined
The concavity of the arch sits approximately 1 cm inferior to the sternal
from behind.
plane, level with the upper half of the fifth thoracic vertebra (range
2.8 cm superior to 4.8 cm inferior). Starting at the aortic valve (see Pleural reflections
above), the ascending aorta curves anteriorly, superiorly and to the Starting in the midline at the sternal angle, the anterior reflections of
right, and becomes the aortic arch posterior to the right half of the the parietal pleura may be traced superiorly along a curved line that
manubrium at the level of the right second costal cartilage. It continues diverges from the midline and extends up and outwards to the apex of
to ascend to the right side of the manubrium sterni, then arches to the the lung and pleural cavity (see Fig. 51.4). The line lies 3–4 cm above
left across or over the sternal plane and descends such that the aortic the anterior end of the first rib; the surface marking is posterior to the
knuckle protrudes just to the left of the manubrium sterni around the
first intercostal space. The brachiocephalic trunk arises approximately
posterior to the centre point of the manubrium sterni and ascends to
the right sternoclavicular joint. The left and right brachiocephalic veins
are formed posterior to the sternoclavicular joints; the right brachio
cephalic vein descends almost vertically, whereas the left brachio
cephalic vein passes posterior to the superior portion of the manubrium
sterni. According to conventional descriptions, the superior vena cava 1
forms posterior to the right first costal cartilage and descends vertically
to enter the right atrium at the level of the right third costal cartilage.


CT data show that it commonly forms posterior to the right second
2
costal cartilage or first intercostal space and the associated part of the
manubrium sterni, and joins the right atrium between the right fourth
and fifth costal cartilages; the level at which it forms is higher in females
and younger adults. The azygos vein enters the superior vena cava 3
approximately 2 cm inferior to the sternal plane at the level of the lower
part of the fifth thoracic vertebra. Horizontal
fissure 4 Cardiac notch
of left lung
Lungs and pleurae
Oblique
fissure 5
Anteriorly, the apex of the lung sits posterior to the medial third of the
clavicle; posteriorly, it lies level with the seventh cervical vertebra (see Costodiaphragmatic
Fig. 51.4). The surface markings of both the apex and costovertebral 6 line of reflection of
border of the lung correspond to those of the parietal pleura. Conven left pleura
tionally, the surface projection of the lower border of the lung is repre
7
sented by a curved line that crosses the midclavicular line at the sixth
rib, the midaxillary line at the eighth rib and the tenth rib just lateral Inferior border
to the vertebral column. CT data reveal considerable variation, redefin of right lung 8 Costodiaphragmatic
ing the lower lung border, at the end of tidal inspiration, as lying line of reflection of
mainly behind the fifth rib/fifth intercostal space on the left, or the 9 right pleura
sixth intercostal space/seventh rib on the right in the midclavicular 10
line, and adjacent to the twelfth thoracic vertebra posteriorly (ranging 12 11
from the ninth thoracic to the first lumbar vertebra). In full expiration, Fig . 51 .7 The relation of the pleura and lungs to the chest wall, right
the lower margin of the lung may rise 5 cm above the parietal pleural lateral aspect .


ThOrax: OVErVIEw aNd SurfaCE aNaTOmy
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medial third of the clavicle. The right and left pleurae are in contact (see Fig. 51.4). The position of the diaphragmatic pleura varies accord
retrosternally in the midline from the second to the fourth costal carti ing to the phase of ventilation.
lages, at which point they diverge. The pleura on the right descends
vertically to the xiphisternum, whereas the pleura on the left deviates
Diaphragm
laterally by 3–5 cm and then passes inferiorly to cross the anterior end
of the sixth rib. This deviation produces an area between the heart and
the sternum that is free of pleura; a needle puncture of the heart may The dome of the diaphragm is often located level with the fifth inter
be performed at this site without risk of damaging the pleura. costal space on the right and the sixth rib on the left; it ranges widely,
The costodiaphragmatic reflections of the pleurae may be followed from the fourth intercostal space to below the costal margin. Conven
around the chest wall from the sixth rib/costal cartilage anteriorly to tionally, the diaphragm is said to be traversed by the inferior vena cava
the eighth rib in the midclavicular line, tenth rib in the midaxillary at about the level of the disc between the eighth and ninth thoracic
line and twelfth rib, or just below, adjacent to the vertebral column. vertebrae, the oesophagus at the level of the tenth thoracic vertebra and
Viewed from behind, the medial edges of the pleurae may be followed the aorta at the level of the lower border of the twelfth thoracic vertebra
along a line joining the transverse processes of the second to the twelfth and the adjacent disc, slightly to the left of the midline. CT assessment
thoracic vertebrae on either side. reveals that the inferior vena cava and the oesophagus frequently pass
The parietal pleura is fused with the inner aspect of the thoracic through the diaphragm at levels slightly lower than those predicted
cavity and can be followed laterally and inferiorly down the inner aspect from chest radiographs, at the level of the eleventh thoracic vertebra


of the thoracic wall to the level of the tenth rib in the midaxillary line (Mirjalili et al 2012a).
KEY REFERENCES
Hale SJ, Mirjalili SA, Stringer MD 2010 Inconsistencies in surface anatomy: Mirjalili S, Hale S, Buckenham T et al 2012a A reappraisal of adult thoracic
the need for an evidencebased reappraisal. Clin Anat 23:922–93. surface anatomy. Clin Anat 25:827–34.
Analyses the consistency of modern clinical and surface anatomy texts in Examines key thoracic surface anatomical landmarks in vivo using
their reporting of common surface anatomy landmarks and calls for an computed tomographic (CT) imaging.
evidence-based reappraisal of clinically relevant surface projections that takes
account of the influence of age, sex, body mass, posture, respiration and
ethnicity.


Thorax: overview and surface anatomy
904.e1
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REFERENCES
Beckenstein MS, Windle BH, Stroup RT 1996 Anatomical parameters for Mirjalili S, Hale S, Buckenham T et al 2012a A reappraisal of adult thoracic
nipple position and areolar diameter in males. Ann Plast Surg 36: surface anatomy. Clin Anat 25:827–34.
33–6. Examines key thoracic surface anatomical landmarks in vivo using
Boussuges A, Gole Y, Blanc P 2009 Diaphragmatic motion studied by computed tomographic (CT) imaging.
Mmode ultrasonography: methods, reproducibility, and normal values. Mirjalili SA, McFadden SL, Buckenham T et al 2012b Vertebral levels of key
Chest 135:391–400. landmarks in the neck. Clin Anat 25:851–7.
Hale SJ, Mirjalili SA, Stringer MD 2010 Inconsistencies in surface anatomy: Naylor C, McCormack D, Sullivan S 1987 The midclavicular line: a wander
the need for an evidencebased reappraisal. Clin Anat 23:922–93. ing landmark. Can Med Assoc J 136:48–50.
Analyses the consistency of modern clinical and surface anatomy texts in
Takazakura R, Takahashi M, Nitta N et al 2004 Diaphragmatic motion in
their reporting of common surface anatomy landmarks and calls for an
the sitting and supine positions: healthy subject study using a vertically
evidence-based reappraisal of clinically relevant surface projections that takes
open magnetic resonance system. J Magn Reson Imaging 19:605–60.
account of the influence of age, sex, body mass, posture, respiration and
ethnicity.
Macklin CC 1925 Xray studies on bronchial movements. Am J Anat 35:
303–29.


CHAPTER
52
Development of the thorax
in line with the craniocaudal progression of development and the elon-
THORACIC WALL AND DIAPHRAGM
gation of the neck. The parietal pericardium remains attached to the
diaphragm as it descends.
The thorax as an entity is not apparent in embryos until the end of the For the lungs to inflate and deflate, they must be surrounded by a
embryonic stage of development (stage 23). It develops around the complete pleural cavity slightly larger than the capacity of the lungs.
early pericardial cavity and the associated pericardioperitoneal canals The synchronous development of the thoracic cage, diaphragm and
(Fig. 52.1A; see Fig. 52.3A). The pericardioperitoneal canals give rise to pleural cavities is, therefore, of vital importance for the normal develop-
the pleural cavities surrounding the lungs and that part of the peritoneal ment of the lungs and postnatal functioning of the respiratory system.
cavity surrounding the lower end of the foregut, which becomes the Before birth, fetal breathing movements may be observed using ultra-
distal oesophagus, stomach and proximal duodenum. Later, these por- sonography. These can have no respiratory function, but it is thought
tions of peritoneal cavity are sequestered into the abdominal cavity by that these phasic changes lead to the release of growth factors that
the development of the diaphragm. promote normal lung development. These movements require an intact
In stage 14 embryos, the heart is at the level of the upper cervical thoracic and abdominal cavity, so that the diaphragm can descend
somites and above the upper limb buds. The thoracic somites are oppo- towards the rigid pelvic bowl, pushing out the abdominal wall. In
site the midgut. The putative thoracic region contains the pericardial conditions where this is not the case, e.g. exomphalos, the lungs may
cavity ventrally and the pericardioperitoneal canals posteriorly, on each be smaller than normal. Other causes of interference with these move-
side of the foregut. The future pleural cavities are as yet undefined ments include neuromuscular disorders of antenatal onset, such as


regions of the pericardioperitoneal canals. Below the heart, septum severe spinal muscular atrophy and myotonic dystrophy inherited from
transversum mesenchyme is being invaginated by endodermal epithe- the mother, and reduced volume of amniotic fluid, e.g. in Potter’s syn-
lial cells from the foregut hepatic primordium. drome (bilateral renal agenesis, oligohydramnios sequence).
The heart and pericardial cavity are relatively large in the early The lung buds are invested by splanchnopleuric mesenchyme
embryo (Fig. 52.1B; see Fig. 52.3A). Throughout development, the derived from the medial walls of the pericardioperitoneal canals,
lungs remain unexpanded and do not achieve their full size within whereas the lateral walls produce somatopleuric mesenchyme, which
the thorax, reflecting the fact that the placenta, and not the lungs, is contributes to the body wall. This latter mesenchyme is penetrated by
the organ of fetal respiration. The lower partition of the thorax, the the developing ribs, which arise from the thoracic sclerotomes. In the
diaphragm, can be identified in stage 13 embryos; it migrates caudally midline, the somatopleuric mesenchyme gives rise to the sternum and
A B C
Pharynx
Pericardial cavity
Foregut
Pericardioperitoneal canals
Septum transversum
Midgut
Body wall,
somatopleuric mesenchyme
and coelomic epithelium
Epithelium of midgut,
splanchnopleuric mesenchyme
and coelomic epithelium Peritoneal cavity
Hindgut
Allantois
Fig. 52.1 A, The arrangement of the epithelial populations in an embryo at about stage 11. The future thoracic region lies caudal to the pharynx and
extends to the upper part of the septum transversum. B, The heart is shown in situ within the pericardial cavity. Venous tributaries return blood from the
body, yolk sac and placenta, and arterial trunks pass each side of the pharynx. C, The respiratory diverticulum arises in the midline from the lower


portion of the pharynx, and lung buds extend dorsally into the pericardioperitoneal canals. 905


Development of the thorax
906
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A Somites B
Oesophagus
Somite ‘Oesophageal mesentery’
Pleuropericardial
‘Oesophageal mesentery’
membrane
Pleuroperitoneal membrane Pleuroperitoneal Oesophagus
membrane
Septum transversum
Primary pleural cavity Septum transversum
Fig. 52.2 A, A dorsolateral view of the foregut between the pericardioperitoneal canals. The respiratory diverticulum arises from the ventral side of the
pharynx and grows caudally. Bilateral lung buds extend dorsally into the pericardioperitoneal canals dorsolaterally. Later changes in position of the
common cardinal veins contribute to the formation of the pericardiopleural membranes cranial to the developing lungs, whereas folds of coelomic
epithelium, pleuroperitoneal membranes, separate the pleural cavities from the peritoneal cavity. B, Components of the diaphragm.
costal cartilages. The bony and cartilaginous cage provides insertions (vertebral; anorectal; cardiac; tracheal; esophageal; renal; limb) associa-
for the intercostal muscles, which arise from the ventrolateral edge of tion, or with congenital syndromes such as Marfan’s and congenital
the epithelial plate of the somites. The somatopleuric coelomic epithe- neurofibromatosis. The diagnosis may be missed at birth. There are a
lium, after its proliferative phase, contributes to the mesothelium of the number of syndromes in which the chest wall does not develop prop-
parietal layer of pleura. erly, and the lungs are consequently hypoplastic. These include Jeune’s
As the lung buds project into the pericardioperitoneal canals (Figs syndrome (asphyxiating thoracic dystrophy – an autosomal recessive
52.1C, 52.2A), they subdivide them into primary pleural coeloms condition that may be associated with short-limb dwarfism and poly-
around the lung buds cranially, and paired peritoneal coeloms caudally, dactyly). Ribcage abnormalities also occur in thanatrophic dwarfism,


which are contiguous with the wider peritoneal coelom around the achondroplasia, chondroectodermal dysplasia and giant exomphalos.
mid- and hindguts. The communications with the pericardial and peri- Many of these conditions are fatal soon after birth; milder forms may
toneal coeloms become termed the pleuropericardial and pleuroperito- improve with time, but affected individuals may need prolonged respi-
neal canals, respectively. When separation between these fluid-filled ratory support.
major coelomic regions is advancing towards completion, they are
named the pericardial, pleural and peritoneal cavities. In early embryos,
the cavities retain substantial volumes of fluid and their walls are sepa- DIAPHRAGM
rate; they provide the route for a primitive type of circulation until
superseded by the blood vascular system. In later fetal and postnatal The separation of the pleural and peritoneal cavities is effected by
life, the cavity walls are coapted, so that a mere microscopic film of development of the diaphragm, which forms from a portion of the
serous fluid intervenes between them. septum transversum mesenchyme above the developing liver (see Fig.
A curved elevation of tissue, the pulmonary ridge, develops on the 52.2). The septum transversum is a population of mesenchymal cells
lateral wall of the pleural coelom and partly encircles the pleuroperi- that arises from the coelomic wall of the caudal part of the pericardial
cardial canal. The ridge is continuous with the dorsolateral edge of the cavity. As the population proliferates, it forms a condensation of mes-
septum transversum. The developing lung bud abuts on the ridge, enchyme, caudal to the pericardial cavity and extending from the ventral
which, as a result, divides into two diverging membranes meeting at and lateral regions of the body wall to the foregut. Dorsal to it, on each
the septum transversum. One is cranially placed and termed the pleuro- side, are the relatively narrow pleuroperitoneal canals. The endodermal


pericardial membrane (see Fig. 52.2A); embedded within it are the hepatic bud grows into the caudal part of the septum transversum,
common cardinal vein and phrenic nerve, which reach the septum whereas the cranial portion will form the diaphragm.
transversum by this route. The other membrane, caudally placed, is The oesophagus and stomach are medial to the pleuroperitoneal
termed the pleuroperitoneal membrane (see Fig. 52.2A). As the apical canals. As development proceeds, the lower portion of the oesophagus
part of the lung forms, it invades and splits the body wall, and extends inclines ventrally anterior to the descending thoracic aorta. Although
cranially on the lateral aspect of the common cardinal vein, preceded the oesophagus has no true ventral or dorsal mesentery, in descriptions
by an extension from the primary pleural coelom to form part of the of diaphragmatic development, the portion of mesenchyme between
secondary, definitive, pleural sac. In this way, the common cardinal vein the oesophagus and aorta at the level of the forming diaphragm is often
and the phrenic nerve come to lie medially in the mediastinum. The homologized with part of a dorsal meso-oesophagus. The pleuroperi-
pleuropericardial canal, which lies medial to the vein, is gradually nar- toneal membranes, which remain small, are dorsolateral to the canals,
rowed to a slit, which is soon obliterated by the apposition and fusion and the mesonephric ridges, suprarenal glands and gonads are dorsal.
of its margins. Closure occurs early and is mainly effected by the growth Just as the enlargement of the pleural cavity cranially and ventrally is
and expansion of the surrounding viscera (heart and great vessels, lungs, effected by a process of burrowing into the body wall, so is its caudo-
trachea and oesophagus), and not by active growth of the pleuroperi- dorsal enlargement. The expanding pleural cavities extend into the
cardial membrane across the opening to the root of the lung. mesenchyme dorsal to the suprarenal glands, the gonads and (degen-


In addition to its extension in a cranial direction, the lung and its erating) mesonephric ridges. Thus, somatopleuric mesenchyme is
associated visceral and parietal pleurae also enlarge ventromedially and peeled off the dorsal body wall to form a substantial portion of the
caudodorsally. With the ventromedial extension, the lungs and pleurae dorsolumbar part of the diaphragm (see Fig. 52.3C). The pleuroperito-
therefore excavate and split the somatopleuric mesenchyme over the neal canal is closed by the fusion of its edges, which are carried together
pericardium, separating the latter from the ventral and lateral thoracic from posterolaterally to anteromedially by growth of the organs sur-
walls (Fig. 52.3B–D). The ventrolateral fibrous pericardium, parietal rounding it: in particular, by growth of the suprarenal gland. The right
serous pericardium and mediastinal parietal pleura, although topo- pleuroperitoneal canal closes earlier than the left, which presumably
graphically deep, are, therefore, somatopleuric in origin. explains why an abnormal communication persisting between the
pleural and peritoneal cavities is more frequently encountered on the
Congenital anomalies of the chest wall
left.
The dorsal portion of the thorax is derived from somites, the sclero- While these changes are occurring, the septum transversum under-
tomal portions of which form the thoracic vertebrae and ribs (Ch. 44). goes a progressive alteration in relative position. The dorsal border of
Vertebral anomalies, including formation of hemivertebrae and block the septum transversum, which initially lies opposite the second cervi-
vertebrae (where cranial and caudal sclerotomal halves do not sepa- cal segment, migrates caudally as the embryo grows and the heart
rate), may contribute to scoliosis. Five per cent of scoliosis is congenital; enlarges. At first, the ventral border moves more rapidly than the dorsal,
it may be associated with multiple other anomalies, e.g. the VACTERL but after the embryo has attained a length of 5 mm, the dorsal border


thoracic wall and diaphragm
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A B Diaphragmatic hernias
Diaphragmatic hernias may result from failure of fusion of the compo-
Pericardial
cavity nent parts or from a primary defect. Posterolateral defects (Bochdalek’s
hernia) are the most common (85–90%) and may be bilateral (5%) or
Pericardio- unilateral. Of the unilateral defects, the left side is more commonly
peritoneal affected (80%). Although these hernias have been attributed to failure
canal
of fusion of the pleuroperitoneal membrane, there is increasing evi-
dence that the primary abnormality is lung hypoplasia, and the hernia-
tion of the abdominal contents is secondary, which has important
implications for treatment (Jesudason 2002). A non-muscular membra-
Pericardial cavity Early pleural nous sac, possibly derived from the pleuroperitoneal canal wall, is
cavity present in 10–15% of cases, signifying the early occurrence of this lesion
prior to closure of the pleuroperitoneal canal. Hernias between the
costal and sternal origins (Morgagni hernias) are rare (1–2%) (Fig.
52.4). Midline defects in the central tendon arise from septum trans-
C
versum defects. The incidence of congenital diaphragmatic hernias is
about 1 : 3000 to 1 : 5000 in neonates, with a prenatal incidence of
Neural arch Spinal cord
1 : 2000.
Centrum Diaphragmatic hernias can usually be diagnosed by antenatal ultra-
Postcardinal vein
sound examination. The presence of bowel in the thorax and media-
Costal element stinal shift may be seen sonographically and radiographically (Fig.
Oesophagus 52.5). The main causes of death in babies with diaphragmatic hernias
Sympathetic
are pulmonary hypoplasia and hypertension. Pulmonary hypoplasia is
ganglion
Right bronchus related to the abnormal branching of the airways both ipsilaterally and
Descending aorta contralaterally, resulting in the formation of reduced numbers of alveoli.
Pulmonary hypertension is related to pulmonary hypoplasia, and also
Right lung Left bronchus


to the increased muscularization and reactivity of the pulmonary circu-
Right pleural sac Left lung lation. There may be associated abnormalities, including trisomy 13
and 18, and diaphragmatic hernia may be part of a number of syn-
Left pleural sac dromes, many of which may lead to termination of the pregnancy or
Right atrium to death of the neonate. For a review summarizing the recurrent genetic
Rib causes of congenital diaphragmatic hernia, see Wynn et al (2014).
Ventricular septum Diaphragmatic eventration is a condition in which an abnormal
Pericardial cavity
diaphragmatic silhouette is seen on X-ray with an abnormal medial
Rib bulge into the thorax; it is associated with paradoxical motion of the
diaphragm during respiratory movements. This may be a benign condi-
tion, often a chance finding and requiring no treatment, or it may lead
to respiratory symptoms, requiring plication; it is occasionally associ-
D
ated with rib and cardiac abnormalities.
OESOPHAGUS
The development of the oesophagus is described in Chapter 36.
Oesophageal atresia, with or without tracheo-oesophageal fistula, may
present antenatally with polyhydramnios due to failure of movement
of amniotic fluid into the gut after fetal swallowing (Ch. 9), and choking
and inability to swallow saliva in the neonatal period.
Ultrasound antenatal imaging of the thorax
The overall shape of the fetal chest is best seen on coronal section. A
Region of
bell-shaped chest is present in pulmonary hypoplasia. In axial section,
costodiaphragmatic recess
the thorax is almost circular. Fetal chest size is estimated by measuring
Fig. 52.3 A, A ventral view of the intraembryonic coelom forming early the chest circumference on axial section at the level of the four-chamber-
body cavities. B, The parietal pericardium is shown surrounding the
heart view. Such measurement can confirm or exclude reduced chest
developing heart ventrally, with the parietal pleura of the lungs dorsal and
volume (Karl and Chaoui 2015). The relative circumference of the
lateral on each side. C, A transverse section through the thoracic region,


thorax and heart remains the same in the second and third trimesters.
showing the ventral extensions of the pleural sacs on each side of the
The diaphragm is best viewed in sagittal view. Diaphragmatic hernias
pericardium that split the body wall mesenchyme. D, An anterior view of
can be diagnosed from about 18 weeks onwards.
the pleural sacs. The position of the pericardium is shown by a dotted
A number of differences between the neonatal and adult thorax and
line. Dorsolateral growth of the pleural sacs also splits the body wall
dorsocaudally, defining the costodiaphragmatic recess. diaphragm are significant in early postnatal life, especially in the
preterm infant. The full-term neonatal thorax has a rounded circumfer-
ence, whereas the adult profile is dorsoventrally flattened. The compli-
ance of the adult chest wall and lung is approximately equal, but the
migrates more rapidly. When the dorsal border of the septum transver- neonatal chest wall is up to five times more compliant than the lungs
sum lies opposite the fourth cervical segment, the phrenic nerve (C3, 4 and so is easily deformable; indrawing of the chest wall is an important
and 5) and portions of the corresponding myotomes grow into it and sign of increased work of breathing in the neonate. The diaphragm is
accompany it in its later migrations. The dorsal border of the septum relatively flat at birth and gains its dome shape as the thorax and
transversum does not come to lie opposite the last thoracic and first abdominal viscera grow. The arrangement of the ribs and diaphragm in
lumbar segments, the final position occupied by some of the dorsal the neonate means that contraction of the diaphragm pulls the compli-
attachments of the diaphragm, until the end of the second month. The ant ribs inwards; this does not contribute to inspiration and leads to
main derivatives of the central part of the diaphragm lie at considerably chest distortion, and may be opposed by the stabilizing action of the
more cranial levels. expiratory muscles. The neonatal diaphragm exhibits an exaggerated
The diaphragm is, therefore, composed of the dorsal meso- asymmetric movement: the posterior portion shows a considerably
oesophagus and paired pleuroperitoneal membranes (posteriorly); greater excursion than the anterior portion.


septum transversum mesenchyme (ventrally); and excavated body wall A neonate undertakes relatively greater work in order to breathe, and
(posteriorly and laterally). is much more vulnerable to developing respiratory muscle fatigue and


Development of the thorax
907.e1
25
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Posterior Anterior
surface of diaphragmatic
sternum defect
Loops of
Mediastinal intestine in left
Thorax shift to the right hemithorax
Liver
Edge of hernial defect showing diaphragmatic muscle
Fig. 52.4 A Morgagni hernia in an 8-year-old boy, as displayed at
Paucity of gas
laparotomy. (Courtesy of Mr G Jawaheer, Great North Children’s Hospital,
in the abdomen
Newcastle upon Tyne.)
Fig. 52.5 A plain radiograph of the chest and abdomen in a 1-day-old
neonate with left posterolateral congenital diaphragmatic hernia. (Courtesy
of Mr G Jawaheer, Great North Children’s Hospital, Newcastle upon
Tyne.)


Development of the thorax
908
7
noItCeS
respiratory muscle failure than an adult. Experimental animal studies A Amnion B
suggest that neonates may be especially vulnerable to respiratory muscle
failure because of the initial immaturity of synapses. Moreover, myosin Buccopharyngeal membrane Bucco-
isoforms are developmentally regulated in the diaphragm; the reduced Primary heart-forming field pharyngeal
membrane
power output and work performance of the newborn diaphragm may Notochord
reflect these molecular differences. 2
In expiration, there may be active braking of airflow, caused by
1
inspiratory muscle activity and partial constriction of the larynx; this
2 2
produces grunting on expiration, especially if the lungs are stiff, e.g. in
3
neonatal respiratory distress. A very preterm neonate is difficult to study,
but respiration is likely to be even more compromised by the compliant 1 1
chest wall and lack of reserve than it is in the term newborn (van Von-
deren et al 2014).
At all ages, there is a reduction in, if not loss of, tonic intercostal 3 3
activity during rapid eye movement (REM) sleep. The mechanism is
believed to be related to a descending spinal inhibition of the muscle
spindle system. In addition, although, during REM sleep, the diaphragm 1 Primary heart-forming field
descends further, this inspiratory effort is dissipated in sucking in the 2 Septum transversum
ribs and enlarging the abdomen; thus, the ribcage and abdominal ven-
3 Secondary heart-forming field
tilatory movements become out of phase. The neonate is at particular
risk in this respect because the chest wall is flexible and much of the Border between primary and
Yolk sac Primitive streak secondary heart fields
infant sleep activity is of the REM type. Furthermore, the upper airway
musculature may lose tone during REM sleep, so that the soft tissues Fig. 52.6 A, The early embryonic disc viewed from a dorsolateral aspect,
of the pharynx are sucked in during inspiration, limiting the cross- showing the position of the primary heart-forming field relative to the


sectional area of the upper airway, and further increasing the work of surface ectoderm of the trilaminar disc. B, The rostral end of the unfolded
breathing. embryonic disc from a dorsal aspect, showing the position of the
mesenchymal populations that will give rise to the primary heart-forming
field, septum transversum mesenchyme and second heart-forming field.
HEART AND GREAT VESSELS
In the last few decades, understanding of the development of the heart endocardium, including its derived cardiac mesenchymal population,
and great vessels has been revolutionized by molecular lineage tracing which produces the valvular tissues of the heart. Splanchnopleuric coe-
and cell division studies. Cardiac development has traditionally been lomic epithelium is also the source of the epicardium, coronary arteries
taught from the standpoint of a formed heart tube, with venous and and interstitial fibroblasts.
arterial ends, which folds within an external pericardial cavity. It is now Primitive cardiac myocytes can first be seen in embryos at stage 8.
clear that this view is incorrect. The cells contributing to the heart arise During the onset of neurulation and somitogenesis, the intraembryonic
sequentially from a range of extracardiac cell populations, and local coelom forms across the midline, initially above the endoderm, in a
instructive interactions maintain the developmental progression; car- horseshoe-shaped area termed the primary heart-forming field (cardiac
diomyocyte identity is not fixed but dependent on spatial and temporal crescent) (Fig. 52.6). As the head fold emerges, the coelom undergoes
signals (Sylva et al 2013). As the changing orientation of the developing a reversal, so that the future pericardial cavity comes to lie ventral to
heart within three dimensions is particularly difficult to understand the endodermal foregut (see Fig. 52.1; Fig. 52.7). The splanchnopleuric
conceptually, and considering that the received view of organogenesis wall of the pericardial coelom, subjacent to the endoderm, provides a
is coloured by past explanations and specific pedagogic approaches, it germinal epithelium that produces early cardiac myocytes. It is charac-


is necessary to maintain some of the older terminology by which heart terized by the expression of myocardial-specific markers, such as cardiac
development was described, as well as considering the most recent myosin heavy chain and the cardiac transcription factor Nkx2-5. Later
findings. myocardial additions from mesenchyme localized central and periph-
Cardiac differentiation and morphogenesis are intimately related eral to the cardiac crescent on the embryonic disc are termed the second
processes, achieved by a highly complicated transcriptional network. heart-forming field (see Fig. 52.6). Whether these two myocardial fields
The cardiac transcription factor Nkx2–5, which has a homogeneous represent distinct myocardial lineages, or constitute a single field, which
distribution over the embryonic heart tube, is generally important for is gradually added to the heart, remains a matter of debate.
cardiac-specific gene expression. In the human, mutations in this factor The endocardium also develops during stage 8–9 from the coelomic
cause atrial septal defects and disturbances of atrioventricular conduc- splanchnopleuric epithelium. Cells arise singly close to the ventrolateral
tion; in Drosophila, the heart will not form in its absence. The recent edges of the cranial intestinal portal and form an endocardial plexus
discovery of the involvement of the role of T-box transcription factors, between the splanchnopleuric coelomic epithelium and the foregut
which are locally expressed, provides some evidence of the further endoderm. These groups of cells are now termed angioblastic mesen-
complexity of patterning the heart. Whereas Tbx5 confers caudocranial chyme; they are amongst the earliest intraembryonic vascular precursors
positional information over the heart tube, thereby determining the to appear and express markers for the endothelial cell lineage. The cells
regional development of the cardiac chambers along these axes, Tbx2 aggregate to form an epithelium, the endocardium, which encloses
and 3 prevent regional formation of the cardiac chambers, permitting small cavities that coalesce in the vicinity of the developing foregut to
the myocardium in these regions to differentiate into the conduction establish bilateral, hollow, endocardial tubes. The latter fuse across the


system. Tbx18 is involved in the development of the sinus venosus and midline progressively, commencing at the outflow tract, or arterial pole,
Tbx1 in the development of the outflow tract of the heart. and extending to the inflow tract, or venous pole (see Fig. 52.7). By
A number of terms must be specified before development of the stage 10, a single endocardial tube is present and is almost completely
heart and discussion of the cardiac chambers can be described. The surrounded by myocardial cells. This arrangement of an outer myocar-
inflow tract of the heart starts at the transition of the systemic tributaries dial sleeve containing an inner endocardial tube constitutes the primary
(sinus venosus) into the primary heart tube. Within the straight heart heart tube. The inner endocardial epithelium induces the myocardial
tube, forming atrial and ventricular chambers can be discerned, sepa- cells to synthesize specific extracellular matrix proteins, which form a
rated by an atrioventricular canal. The inflow tract thus connects the fine extracellular reticulum that holds the endocardial tube apart from
sinus venosus with the forming atrium, whereas the outflow tract con- the developing myocardium. Close to the foregut endoderm, the myo-
nects the ventricles with the aortic sac; a proximal portion (close to the cardial cells at the reflections of the pericardial splanchnopleuric epi-
ventricle) and a distal portion can be defined within the outflow tract. thelium form the dorsal mesocardium, which may stabilize the
developing endothelium and promote the fusion of the bilateral endo-
cardial tubes. The dorsal mesocardium encompasses a mesenchymal
CELLS THAT GIVE RISE TO THE HEART population specifically referred to as mediastinal mesenchyme, and is
contiguous with the splanchnopleuric mesenchyme surrounding the
The heart is formed from tissues derived from the midline splanchno- embryonic foregut.
pleuric coelomic epithelium with later contributions from neural crest Much later in heart development, neural crest cells, arising from the
mesenchyme. The splanchnopleuric coelomic epithelium gives rise to region between the otic vesicle and the caudal limit of somite three,


the myocardium, including the conduction system of the heart, and the grow into the outflow tract of the heart. They are believed to play a role


heart and great vessels
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A Intraembryonic mesoderm – coelomic wall B
Intraembryonic coelom – future pericardial cavity
Amnion wall Neural plate
Future
septum
transversum
Notochordal
plate
Yolk sac wall Buccopharyngeal membrane
Mesenchyme Buccopharyngeal Notochord Proliferating
membrane splanchnopleuric layer
Proliferating
somatopleuric layer
Endocardial plexus which
Pericardial cavity forms endocardium
C Foregut Dorsal mesocardium
Buccopharyngeal
membrane Floor of neural tube
Endoderm
Septum transversum
D
Notochord
Inflow tract of heart Neural tube
Dorsal aorta
Notochord
Foregut
Outflow
Endocardial
tract of
heart tube Cardiac
heart Dorsal mesocardium
extracellular
matrix
Cardiac
Myocardium
extracellular matrix
Endocardial
Pericardial cavity heart tube
Myocardium
Splanchnopleuric wall of the pericardial coelom (cavity)
Somatopleuric wall of the pericardial coelom (cavity)
Fig. 52.7 A, A median section through part of the embryonic disc to show the position of the future pericardial cavity before head folding. B, A median
section through the cranial end of a human embryo during early head folding, showing its reversal effect on the position of the pericardium. C, A median
section through the cranial end of a human embryo after head folding, showing the pericardial cavity and endothelial heart tube now ventral to the
foregut. D, A horizontal section through the pericardium and endothelial heart tube shown in C. The position of the dorsal mesocardium, a source of
secondary heart field mesenchyme, is indicated.
in the spatio-temporal regulation of the division of the outflow tract lining the atrioventricular canal and the proximal outflow tract to trans-
into the aortic and pulmonary pathways, and the development of the form into mesenchyme (cardiac mesenchyme); the endocardial cells in


muscular subpulmonary infundibulum. other regions of the heart tube, such as those in the ventricle, do not
The epicardium, sometimes included in descriptions of the myocar- undergo such a transition. When activated by myocardial inductive
dium as ‘epimyocardium’, is not present at the early stages of heart factors, the endocardial cells lose their cell-to-cell associations, and
development. show decreased expression of neural cell adhesion molecule, and
increased expression of substrate adhesion molecules such as chondroi-
tin sulphate and fibronectin. They undergo rearrangement of their
Endocardial cushions
cytoskeleton necessary for migration, and they express type I procolla-
gen. Uniquely, they retain their expression of endothelial markers. This
The extracellular matrix of the heart, historically termed cardiac jelly, epithelial to mesenchymal transition may, perhaps, be the only example
promotes occlusion of the endocardial tubular lumen during myocar- of a mesenchymal population that is derived from an endothelial
dial contraction, thus providing mechanical assistance for the genera- lineage.
tion of the flow of blood. It also acts as a site for the deposition of Formation of cardiac mesenchymal cells at the atrioventricular
inductive factors from the myocardial cells, which, in turn, modify the canal and the proximal myocardial outflow tract is followed by their
differentiation of specific endocardial cells. It has been called a gelatino- migration into the cardiac extracellular matrix. These cells proliferate
reticulum, a myoepicardial reticulum (see Fig. 52.7C–D) and, more between the endocardium and myocardium, and, with local accumula-
recently, the myocardial basement membrane. Here, the term cardiac tion of extracellular matrix molecules, produce protrusions, termed
extracellular matrix will be used. It is composed of hyaluronic acid, endocardial or cardiac cushions, which bulge into the primary heart
hyaluronidase and fibronectin, among other things. Inductive signals tube and initially provide the valvular mechanisms required in the
originating from the myocardial cells cause a subset of endocardial cells atrioventricular canal and outflow tract. Their position corresponds to


Development of the thorax
910
7
noItCeS
the future positions of the definitive cardiac valves. In the distal part of undergo restriction, differentiate and leave the cell cycle. After folding,
the outflow tract, which initially has myocardial walls, cells that are the second heart field contributes cells to the heart. It has been sug-
derived from the neural crest subsequently make significant contribu- gested that the secondary heart field may contribute cells only to those
tions to the mesenchyme of the endocardial cushions. Although proper cardiac components that are required for the pulmonary circulation:
migration of these cells from the neural crest is crucial for normal namely, the right ventricle and outflow tract at the arterial pole, and the
development of the outflow tract and formation of the leaflets and atrial septum and the dorsal atrial wall at the venous pole. To extend
sinuses of the arterial valves, their function is largely obscure. They are this suggestion, the original primary heart-forming field would give rise
no longer found in the leaflets of the arterial valves in the formed heart, to those components that are required for the systemic circulation:
or in the muscular subpulmonary infundibulum, which is also derived namely, the systemic venous sinus and its tributaries, the initial atrium,
from the outflow cushions. The endocardial cushions themselves ulti- the left ventricle and the arterial conus, as seen in the outflow tract of
mately fuse, forming a wedge of mesenchyme that serves to guide the primitive fishes, although this latter structure has no homologue in
union of the internal muscular septal structures. At their time of fusion, mammalian hearts.
the atrioventricular endocardial cushions are large, relative to the size During the process of folding, the pericardial cavity and, concomi-
of the atrioventricular orifices; they will provide the scaffold for forma- tantly, the myocardium gradually extend around the forming endocar-
tion of the leaflets of the tricuspid and mitral valves. dial tube, leaving the dorsal mesocardium, a transient connection that
is analogous to the mesentery of the intestines (see Fig. 52.7C–D). The
Cardiac myocytes – contraction, conduction persisting stalk of the dorsal mesocardium connects the venous pole of