Anatomia y Fisiologia Del Diafragma

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Surgical Conditions

of the Diaphragm :
Anatomy and Physiology
Masaki Anraku, MDa,Yaron Shargall, MDb,*

KEYWORDS
 Diaphragm  Anatomy  Physiology  Surgery
 Surgical incisions

The diaphragm (Greek: dia 5 in-between, phragma mesentery of esophagus, and (4) the body wall
5 fence) is a musculoaponeurotic structure that muscles.3
serves as the most important respiratory muscle The septum transversum is derived from meso-
and the separating structure between the abdom- derm and this structure forms the central tendon
inal and thoracic cavities. This article reviews the of the diaphragm, a process that starts during the
anatomic components of the diaphragm, its pivotal third embryonic week. Between this week and the
role in respiration and in the gastroesophageal eighth week, the developing diaphragm descends
mechanism, and the surgical implications of the from the level of C3 to the final position at the level
anatomic structuring. of L1, carrying with it the phrenic nerves, which
originate from the third to fifth cervical levels. Right
ANATOMY and left sides of pleuroperitoneal membranes
attach to the septum transversum laterally and
In adults, the diaphragm represents less than caudally and to the dorsal mesentery medially.
0.5% of body weight,1 but it is the most important The right and left pleuroperitoneal membranes ulti-
muscle in the human body after the heart (Box 1). It mately close at approximately the eighth week of
is composed of a central noncontractile tendon gestation and separate the thoracic and abdominal
and two major muscular portions: the costal and cavities. The dorsal mesentery of the esophagus
crural diaphragm. An additional minor muscular attaches the foregut to the dorsal body wall and
portion is the sternal part of the diaphragm. The eventually becomes the crura of the diaphragm.
diaphragm is an elliptical cylindroid structure, cap- The pleural cavities and their costodiaphragmatic
ped by a dome2; it arches over the abdomen, with recesses split the inner and outer layers of the
the right hemidiaphragm higher than the left. The body wall between the 9th and 12th weeks of
concave, dome-shaped part allows the liver and gestations; the inner layer of the body wall muscle
the spleen, situated underneath the diaphragm, composes the posterolateral portion of the dia-
to be protected by the lower ribs and the chest phragm, and the outer layer of the body wall
wall. The caudal and cranial views of the dia- becomes the thoracic wall.
phragm with the various anatomic structures are The costal part of the diaphragm develops from
shown in Figs. 1 and 2. the lateral body walls whereas the crural part of the
diaphragm originates from the dorsal mesentery of
Embryology
the esophagus, which explains why the diaphragm
The diaphragm is formed by four embryologic enti- is characterized by two separate functional
ties, including (1) the septum transversum, (2) the components, the costal diaphragm and the crural
pleuroperitoneal membranes, (3) the dorsal diaphragm.4,5
thoracic.theclinics.com

a
Division of Thoracic Surgery, Toronto General Hospital, University of Toronto, 200 Elizabeth Street, Toronto,
Ontario M5G2C4, Canada
b
Division of Thoracic Surgery, St Joseph Health Centre, University of Toronto, 30 The Queensway, SSW W221,
Toronto, Ontario M6R 1B5, Canada
* Corresponding author.
E-mail address: [email protected] (Y. Shargall).

Thorac Surg Clin 19 (2009) 419–429


doi:10.1016/j.thorsurg.2009.08.002
1547-4127/09/$ – see front matter ª 2009 Elsevier Inc. All rights reserved.
420 Anraku & Shargall

Box 1 diaphragm has three components, which originate


Anatomy from the lumbar spine dorsally, ribs laterally, and
sternum ventrally. The three muscular compo-
, The diaphragm is composed of a central non- nents are separated from each other by muscle-
contractile tendon and two major muscular free gaps and are named (1) the lumbar (pars
portions: the costal and crural diaphragm. lumbaris), (2) costal (pars costalis), and (3) sternal
, The costal and crural parts of diaphragm have (pars sternalis) parts. The muscle fibers of the
different embryologic origins, different lumber (crural) diaphragm project onto the antero-
segmental innervation, and different func- lateral aspect of L1 to L3 whereas those of the
tional properties. costal diaphragm project from the central tendon
, Major blood supply is from the pericardio- to the upper margins of the lower 6 ribs and the
phrenic, musculophrenic (from the internal xiphoid process of the sternum.
thoracic artery), superior phrenic (from the
thoracic aorta), and inferior phrenic (from Lumbar (crural) part (pars lumbalis)
the abdominal aorta) arteries. The lumbar (crural) part of the diaphragm forms the
, From the surgical perspective, understanding right and left crura along the lumbar spine. It is the
the phrenic nerve distribution on the dia- most powerful part of the diaphragm. The right
phragm is of crucial importance to avoid crus arises from the anterior surface of lumbar
injury to the nerve during diaphragmatic inci- vertebrae (L1-4 on the right and L1-2 on the left),
sions. the intervertebral disks, and the anterior longitu-
dinal ligament. The right crus is larger than the
left crus, and it directs to the middle part of the
central tendon on both sides of the medial plane
The Muscular Parts of the Diaphragm
superiorly. The right crus splits to form the esoph-
The diaphragm is a striated skeletal muscle ageal hiatus in more than 60% of individuals
consisting of two major parts: the muscular part (whereas in the rest, the esophageal crura is
radiating outward and the central, noncontractile derived by contribution of both crurae), functioning
tendinous part. The muscular part of the as a sphincter-like opening of the diaphragm (the

Fig. 1. The diaphragm as seen from the chest.


Diaphragm: Anatomy and Physiology 421

Fig. 2. The diaphragm as seen from the abdomen.

esophageal hiatus), and the split muscle fibers triangular gaps between the sternal and costal
meet again to form the anterior margin of the aortic parts of the diaphragm (discussed later).
opening. Although the esophageal crura consists
of muscular and tendinous tissues, only the tendi- Sternal part
nous part is strong enough to hold sutures during The sternal part of the diaphragm originates with
surgery. In 90% of patients, however, the medial small dentations from the posterior layer of the
edge of the crura is tendinous, allowing for a safe rectus sheath and from the back of the xiphoid
suturing.6 Inferiorly, the right crus forms the liga- process, inserting at the central tendon (see
ment of Treitz, a portion of the suspensory muscle Fig. 2). Lateral to it (on both sides), there is
of the duodenum, which runs downward to the left a narrow gap between the sternal and costal parts,
of the celiac artery. The left crus, alternatively, which is usually composed of connective tissue
directs upward to the left of the esophageal hiatus. only. These gaps (named after Morgagni and Lar-
It is much smaller than the right crus. A separate rey, or the sternocostal triangles) pass the internal
part of the left crus reaches to the central tendon, thoracic/superior epigastric vessels and are
running behind the muscle fibers of the right crus. potential sources for herniation, more commonly
seen in adults (Fig. 3).

Tendinous Part of the Diaphragm


Costal part (pars costalis)
(Central Tendon)
The costal part of the diaphragm originates from
the inner surface and upper margins of the six Essentially, all the musculature of the diaphragm
lower (caudal) ribs and radiates into the central inserts on the thickened central tendon, which is
tendon. The lumbocostal triangles/trigones (Boch- the highest part of the diaphragm. The tendinous
dalek’s gap) exist between the lumbar and costal part is a fascial aponeurosis that has a clover-
parts of the diaphragm, more commonly on the leaf-like shape consisting of three leaflets (one
left side than on the right side. In these areas, anterior and two lateral leaves) separated from
the gaps are usually closed only by fascia, perito- each other by slight indentations. In contrast to
neum, and pleura. Anteriorly, there are bilateral its name, the central tendon is not located
422 Anraku & Shargall

Fig. 3. Structures passing through the diaphragm, as seen from the abdomen.

centrally, and it is not symmetric. It lies more ante- the xiphoid process of the sternum, and other
riorly than posteriorly (with the posterior crural portions radiate posterolaterally, the left leaflet
muscular fibers longer than the anterior ones), a little narrower than the right one. The central
and the right leaf of the tendon is the largest of portion of the tendon is located underneath the
all three. A midanterior portion extends toward pericardium, thus the superior surface of the

Fig. 4. Surgical incisions on the diaphragm. (A) An incision with a risk of total paralysis of the diaphragm. (B) A
preferred incision with minimal risk of nerve injury. (C, D) Incisions in safe areas, but with small risk of nerve injury.
Diaphragm: Anatomy and Physiology 423

tendinous part is attached firmly to the pericar- The diaphragmatic blood flow is respiratory-
dium. Lateral to the heart, the right and left phase dependent: it increases during the dia-
diaphragmatic dome parts are mobile, and their phragmatic relaxation (resting) phase, decreases
position is dependent on the extent of ventilation. during inspiration phase, and can be completely
At resting position, the right dome is at the level diminished during forceful inspiration.7 Resistive
of the fourth intercostal space, whereas the left loading ventilation increases blood flow to the dia-
dome is at the fifth intercostal space. In deep inspi- phragm much more than unobstructed ventilation.
rium, both domes descend approximately two Animal studies showed that during resistance
intercostal levels lower than their resting position. breathing, diaphragmatic blood flow increased
The foramen of the inferior vena cava is located 26-fold, whereas the blood flow to the rest of the
in the tendinous part of the diaphragm to the right inspiratory and expiratory muscles increased to
of the midline. a lesser extent.8 Increased intramuscular pressure
during muscle contraction attributes to blood flow
restriction.9 Because the diaphragmatic contrac-
Blood Supply of the Diaphragm
tility is dependent on the blood circulation with
The diaphragm has an enormously rich blood an appropriate oxygen supply, it is important that
supply. As a result, necrosis of the diaphragm is the diaphragm returns to its constant resting posi-
extremely rare. The arterial blood supply to the tion with optimal relaxation, which allows for
diaphragm is derived from (1) the pericardio- diaphragmatic blood flow to occur. Another
phrenic arteries, (2) the musculophrenic arteries, mechanical factor influencing the diaphragmatic
(3) the superior and inferior phrenic arteries, and blood flow is the change in the intrathoracic
(4) the intercostal arteries. The pericardiophrenic and intra-abdominal pressures. Increased intra-
arteries run through the chest along with the abdominal pressure produced by diaphragmatic
phrenic nerves, then distribute on the thoracic contraction leads to blood flow limitation.10
side of the diaphragm. The musculophrenic Hypoxemia increases blood flow to the dia-
arteries (branched from the internal thoracic phragm, an adapative mechanism in patients
arteries) and the superior phrenic arteries with chronic obstructive pulmonary disease
(branched from the thoracic aorta) also provide (COPD), in whom faster respiratory rate and
blood supply to the thoracic side of the diaphragm. smaller tidal volumes might help to preserve dia-
The right and left internal thoracic arteries pass phragmatic performance.11
through the Morgagni’s (right) and Larrey’s (left)
gaps after giving rise to the musculophrenic Lymphatic System of the Diaphragm
arteries, and then become the superior epigastric
The thoracic and abdominal surfaces of the
arteries.
diaphragm have a rich lymphatic system accom-
The right and left inferior phrenic arteries, direct
panying the blood vessels. The lymphatic vessels
branches from the abdominal aorta or from the
from the abdominal side of the diaphragm are
celiac trunk, supply the abdominal side of the
distributed parallel to the blood vessels. The
diaphragm. They are much larger than the other
anterior (ventral) lymphatic system drains to the
arterial branches and are the main source for arte-
parasternal nodes. Right and left lateral lymphatic
rial blood supply to the diaphragm. On rare occa-
systems run along with the phrenic nerves. Their
sions, the right renal artery gives rise to the right
efferent lymphatics drain into the lymph nodes of
inferior phrenic artery. The peripheral parts of the
the posterior mediastinum (brachiocephalic and
costal diaphragm have an additional blood supply
parasternal nodes). The posterior (dorsal)
from the intercostal arteries. These arteries form
lymphatic vessels drain to the lateral aortic and
anastomoses with the surperior and inferior
posterior mediastinal lymph nodes. The diaphrag-
phrenic arteries to maintain blood flow to the
matic lymphatic drainage system plays a major
diaphragm.7
role in the absorption of material from the perito-
The veins of the diaphragm follow the arteries.
neal cavity.
The venous drainage from the thoracic side of
the diaphragm is via the azygos and hemiazygos
Innervation of the Diaphragm
systems, whereas that of the abdominal side is
mainly via the inferior phrenic veins to the inferior Motor and sensory innervations are supplied by
vena cava. Venous drainage of the peripheral the phrenic nerve and the sixth or seventh inter-
costal and sternal portions of the diaphragm is costal nerves, the latter distributed to the costal
via the intercostal and the internal thoracic veins, part of the diaphragm. The muscular part of the
respectively. These vessels are accompanied by diaphragm receives its main motor innervation
lymphatic vessels. via the phrenic nerve. The right and left phrenic
424 Anraku & Shargall

nerves originate in the cervical plexus (mainly the


fourth cervical nerve roots, with lesser contribu-
tions from the third and fifth roots) and run
craniocaudally toward the diaphragm, passing
anterior to the hilum of the lungs, attaching to the
pericardium along with the pericardiophrenic
artery and veins where they provide pericardial
branches. The right phrenic nerve descends along
the superior vena cava, subsequently along the
side of the pericardium anterior to the right pulmo-
nary hilum, then enters into the central tendon
anterolaterally to the vena caval opening. The left
phrenic nerve descends laterally to the side of
the aortic arch and runs downward along the
side of the pericardium, anterior to the left pulmo-
nary hilum. Thereafter, it enters into the diaphragm
lateral to the left border of the heart and anterior to Fig. 5. Potential diaphragmatic defects/hernias. 1.
the central tendon. The phrenic nerves give Morgagni’s. 2. Larrey’s. 3. Peritoneopericardial
branches on the thoracic side of the diaphragm. communication (defect of the septum transversum).
Once the right and left phenic nerves pass through 4. Paracaval hernia. 5. Hiatal hernia. 6. Pleuroperito-
neal (see Fig. 6). 7. Bochdalek’s (lumbocostal triangle/
the diaphragm, they branch off anteromedially to
trigone). Both short and long arrows indicate direc-
the sternum, anterolaterally to the costal dia-
tion of potential extension.
phragm, and posteromedially to the crural dia-
phragm. The left phrenic nerve also passes
through the esophageal hiatus to the peritoneum vertebral body, laterally by the crural diaphragm,
and several upper abdominal organs. These and ventrally by the median arcuate ligaments.
diaphragmatic branches are not always visible This hiatus transmits the aorta, the aortic plexus,
directly even after removal of the diaphragmatic the thoracic duct, lymphatic vessels that descend
pleura because the branches extend into the from the thorax to the cisterna chili,2 and (usually)
muscle of the diaphragm. the azygos vein. The median arcuate ligament
Understanding the distribution of the phrenic forms a tendinous arch in front of the aortic hiatus
nerves on the diaphragm is of significant impor- at the level of the celiac trunk and connects the
tance if diaphragmatic incision is considered two cruras of the diaphragm. It may be used for
during surgery (eg, left thoracoabdominal incision) surgical narrowing and reconstruction of the
because phrenic nerve injury could cause signifi- esophageal hiatus.3 Incidental injury to the
cant loss of diaphragmatic function. Surgical inci- thoracic duct during manipulations of the aorta
sions can generally be safely made without injury along the hiatus might result in chylous ascites
to the phrenic nerves because the anatomic and occasionally result in chylothorax due to injury
arrangement of the nerve branches is constant in higher into the chest or chyle leakage from the
most cases. The diaphragmatic branches of the abdominal side of the hiatus into the pleural cavity.
phrenic nerves, however, are commonly The esophageal hiatus is an oval aperture
embedded deep in the muscle and are not located at the level of T10 on the left of the midline
exposed on the undersurface of the diaphragm. and ventrally to the aortic hiatus behind the central
Therefore, one cannot rely on visualization of those tendon. It is formed by the diaphragmatic crura an-
branches before incising the diaphragm (Fig. 4). terolaterally by splitting of the medial fibers of the
right crus and posteriorly by the median arcuate
ligament. Ventrally, this hiatus is framed by muscle
Openings in the Diaphragm
fibers. As a result of this anatomic structuring, dia-
The diaphragm has three anatomic openings: the phragmatic contraction can contribute to the
aortic, the esophageal, and the inferior vena cava closure of the caudal end of the esophagus.
orifices. Other small openings include a triangular The esophageal hiatus transmits the esophagus,
gap between the sternal and costal parts of the the anterior and posterior vagal nerve trunks,
diaphragm bilaterally and between the costal and and the phrenicoabdominal (sensory) branch of
lateral arcuate ligaments bilaterally, respectively the left phrenic nerve (eventually supplying the
(see Fig. 3). pancreas and peritoneum). The phrenoesopha-
The aortic hiatus is located anterior to the lower geal ligament, the fascia on the inferior surface of
border of T12 or L1 and is bordered dorsally by the the diaphragm extending to the esophageal wall
Diaphragm: Anatomy and Physiology 425

approximately 2 cm above the gastroesophageal


junction, limits the upward displacement of the
esophagus. Other structures passing through this
hiatus include esophageal branches and
tributaries of the left gastric artery and vein.
The foramen vena cava is located at the right
portion of the central tendon at the level of T8
and T9, thus its margins are tendinous. The right
phrenic nerve also passes through this foramen
and few lymphatics.12 Although a source for
controversy for years, it is believed that the vena
caval blood flow to the heart is facilitated by venti-
lation as the foramen vena cava is stretched by the
diaphragmatic contraction during inspiration.6
The internal thoracic artery and veins extend
down through the Larrey’s and Morgagni’s gaps
(left and right, respectively [see Fig. 3]) and from
then on are termed the superior epigastric artery
and veins, respectively. Few lymphatics usually
accompany those vessels through the gaps. Mor-
gagni’s hernia (see ‘Congenital Hernia in Adults’)
are more common on the right gap because the Fig. 6. Delayed traumatic diaphragmatic hernia
left is protected by the pericardium. Given the rela- through a potential pleuroperitoneal defect in a 25
tionship with the peritoneum, most hernias contain year old, presenting with bowel obstruction 2 years
a sac, and the most commonly herniating struc- after blunt trauma. Notice the stretched venous
tures are the colon and the omentum. branch of the superior mesenteric vein passing
Posteriorly, the lumbocostal triangle between through the defect (arrow), suggesting chronic
process.
the costal portion of the diaphragm and the portion
arising from the lateral arcuate ligament (bilaterally
but mostly on the left side) might contain only few size from a tiny pinhole to up to a centimeter, and
muscle fibers, and only pleura and peritoneum are usually located in the tendinous part of the
divide the abdominal and thoracic cavities. This diaphragm, most commonly on the right side. The
defect, the foramen of Bochdalek, might extend majority of defects are believed acquired.
further anteriorly and medially and is the site of Although the precise mechanism is unknown,
congenital diaphragmatic hernia or, rarely, similar the transdiaphragmatic pressure gradient between
hernia in adults. Additional potential openings/ the peritoneal and pleural cavities premotes transfer
defects in the diaphragm, such as peritoneoperi- from the abdomen to the thorax. The acquired pores
cardial hernia, paracaval, and pleuroperitoneal are a result of a challenge to the diaphragmatic integ-
hernias (see Fig. 5), are extremely rare. They rity by various space-occupying materials that
have been described in newborns and are rarely increase the intra-abdominal pressure. Although
seen in adults in association with trauma (Fig. 6); the so-called porous diaphragm syndrome13 has
in late presentation of diaphragmatic tear through many causes, the common clinical presentation is
a potential pleuroperitoneal defect; and in asymp- that of thoracic symptoms and signs (pleural
tomatic patients with an incidental finding of left effusion, hemothorax, empyema, pneumothorax)
pleuroperitoneal hernia (Fig. 7). Other structures secondary to the abdominal pathology. The most
passing between the thorax and the abdomen, common manifestations are cirrhotic hydrothorax,
through the diaphragm or posterior to it, are shown secondary to ascites, and iatrogenic ascites with
in Fig. 3. Those include the splanchnic nerves and hydrothorax secondary to peritoneal dialysis.
occasionally the azygos or hemiazygos veins. Another clinically significant scenario is tension
pneumothorax during laparoscopic surgery. The
role of diaphragmatic pores in catamenial
Diaphragmatic Pores
pneumothorax is not completely defined, although
Passage of fluids, gases, or tissues transdiaphrag- diaphragmatic pores are found in large proportions
matically through pores in the diaphragm was recog- of cases.
nized but not well defined until comprehensively When found, (thoracoscopic) closure of pores is
reviewed by Kirchner in 1998.13 Diaphragmatic curative in patients with ascitic or peritoneal dial-
pores/holes might be single or multiple, ranging in ysis induced hydrothorax. In many patients, the
426 Anraku & Shargall

Fig. 7. Diaphragmatic 3-D reconstruction of an asymptomatic 72-year-old woman investigated for ‘‘lung mass’’ on
a yearly chest readiograph. There was no previous history of trauma. (A, B) A posterior defect of the left hemi-
diaphragm is clearly seen (arrow). (C) The defect can be defined as peluroperitoneal type hernia (arrow A), con-
taining omental fat (arrow B).

diaphragm might be found intact during thoraco- allow for a safe reduction of abdominal contents
scopy. Pleurodesis should always be considered. back into the peritoneal cavity. Transdiaphrag-
matic exposure of the cardia can be achieved
using a septum transversum incision from the
Anatomical Consideration in Surgery
anterior portion of the esophageal hiatus antero-
Diaphragmatic incisions are necessary for various laterally but it risks injury to the left phrenic nerve
thoracic or abdominal procedures. They should and is not commonly used. The most commonly
be carefully made to avoid significant injury to used incision is the circumferential incision at
major branches of the phrenic nerve and impor- the periphery of the diaphragm. It allows for an
tant vascular structures (in particular, the right excellent exposure of the abdominal contents
and left inferior phrenic arteries). Due to the rapid from the chest and vice versa, with minimal risk
decrease in size of the phrenic nerve branches for nerve injury (see Fig. 4B). Using a cautery,
and their positioning embedded in the muscle, a diaphragmatic rim of 2 to 3 cm parallel to the
it is not practical to try and follow them. The chest wall should be maintained, as a smaller
radial incision (see Fig. 4A) from the costal rim makes closure technically demanding, and
margin to the esophageal hiatus was used in marking sutures should be placed to ensure
the past, but resulted in complete paralysis of correct orientation of the edges upon closure. It
the hemidiaphragm and is now abandoned. is generally easier to start the incision anteriorly,
Incisions in various safe areas can be carried lateral to the pericardium, and carry it circumfer-
with little risk for phrenic nerve damage entially as far posteriorly as needed, using the
(see Fig. 4C, D) but are not optimal due to anterolateral two thirds for procedures associ-
a limited surgical exposure. Although incisions ated with antireflux repairs, and more posterior
made into the central tendon rarely cause extension (when needed) for esophageal resec-
diaphragmatic paralysis (phrenic nerve distribu- tions. Used on the left side, this incision usually
tion [see Fig. 4]), they also provide only minimal encounters the main branch of the inferior
exposure of the abdomen. The safety of cutting phrenic artery, requiring division and ligation of
through the central tendon can be useful during the vessel. When thoracoabdominal approach is
repair of traumatic diaphragmatic tears and selected, this incision can be extended and
various acquired diaphragmatic hernias, where started medially between the pericardial attach-
the opening in the diaphragm is often small, ment to the diaphragm and the entrance of the
and an enlargement is frequently required to phrenic nerve into the diaphragm.
Diaphragm: Anatomy and Physiology 427

PHYSIOLOGY Finally, the relationship of the contracting,


descending diaphragm to the opposing effect of
The diaphragm has two major physiologic func- the abdominal contents serves as a fulcrum. The
tions: (1) to support respiration and (2) to support net effect is force exerted on the lower ribs crani-
gastroesophageal functions, including esophageal ally, resulting in their upward and outward
emptying, antireflux barrier, and emesis. The movement.14
costal part of the diaphragm supports mainly The costal part of the diaphragm is the main mu-
respiration (especially during inspiration), whereas sclature for the act of respiration, specifically the
the crural part of the diaphragm has an important inspiratory phase. Breathing is endurance work,
role in gastrointestinal function. The diaphragm like that of the heart, as the diaphragm must
gives additional powers to any expulsive acts; contract in repetitive fashion for life. The muscle
a deep inspiration is taken place before sneezing, fibers of the diaphragm are well suited for this
coughing, laughing, crying, and before the expul- task; up to 55% of the fibers in adult human dia-
sion of urine or feces. The diaphragm also phragm are type I, slow-twitch, which are highly
provides anatomic stability to thoracic and resistant to fatigue.15 The remaining muscle fibers
abdominal organs. are type II, fast-twitch that are susceptible to
The Role of the Diaphragm in Respiration fatigue. Type II fibers are 21% IIA, rapid oxydative
fibers and 24% IIB, rapid glycolytic fibers.16 In
The diaphragm is the most important respiratory normal breathing, type I muscle fibers are mainly
muscle, responsible for the majority of the work used. Fast-twitch type II muscle fibers are re-
of breathing in normal individuals and those with cruited when the breathing rate increases because
lung diseases (Box 2). Paralysis of all nondiaph- the fundamental contractile unit in muscle is more
ragmatic respiratory muscles usually does not in type II than in type I fibers.17
result in respiratory failure, whereas bilateral dia- The shape of the diaphragm is an elliptical
phragmatic paralysis usually causes carbon cylinder capped by a dome.14 This unique shape
dioxide retention and respiratory failure.2 The gives the ability to increase the dimensions of the
inspiratory mechanism of the diaphragm is chest cavity to inflate the lungs. In resting position,
a combination of three pathways, all of which are the diaphragm forms a dome concave toward the
significantly influenced by the cranial-caudal abdomen in right and left sides. The diaphragmatic
orientation of the muscle fibers and the existence muscle is active during inspiration; its contraction
of the zone of opposition (the area of contact causes descent of the diaphragm that results in
between the diaphragm and the rib cage) First, outward movement of the abdominal wall.2 The
as the muscle fibers shorten, they pull the central dome of the diaphragm in each side moves down-
tendon in a caudal direction, thus expanding chest ward nearly parallel to its original position during
volumes with a piston-like action. At the same time deep inspiration. This increased diaphragmatic
of inspiration, the dome of the diaphragm tension produces a caudally oriented force onto
descends, thus pushing the abdominal organs the central tendon and a cephalically oriented
down and increasing the intra-abdominal pres- force onto ribs 7 to 12 (costal part) and the verte-
sure. This elevated pressure is transmitted across bral column (crural part). The caudally and cephal-
the apposition zone, pushing the lower ribs ically oriented forces increase the cephalocaudal
outward, resulting in expansion of the rib cage. dimensions of the chest wall thus assisting inspira-
tion. The effectiveness of these actions is reduced
by physiologic (hyperinflation with increased lung
Box 2 volumes) and pathologic (emphysematous lungs)
The diaphragm in respiratory function conditions.18–20
, The costal part of the diaphragm is the major The diaphragmatic muscles are controlled by
muscle for inspiration and is composed of voluntary and autonomic neural pathways via the
type I, slow-twitch, fatigue-resistant muscle phrenic nerves and can respond to neural drive
fibers and type II, fast-twitch, fatiguing and workload. It has been shown that the dia-
muscle fibers. phragm contracts against elastic resistive forces
, A fiber-type shift from type II to type I occurs and returns to a constant resting position with
to adapt to a chronic changes in obstructive each relaxation, with balance between the lung
pulmonary disease. and chest wall recoil forces. Thus, expiration is
, Diffuse atrophy of the costal diaphragm is partly effected by the elastic recoil of the thoracic
seen in patients who undergo prolonged walls and partly by the action of the abdominal
ventilation with diaphragmatic inactivity. muscles that push back the displaced abdominal
viscera.
428 Anraku & Shargall

Although the diaphragm is known to be resistant Box 3


to fatigue, diaphragmatic fatigue (defined by the The diaphragm in gastroesophageal function
loss of contractility and decreased duration of dia-
phragmatic contraction) can occur and is associ- , The crural part of the diaphragm is a major
ated with unsuccessful weaning from mechanical contributor for gastroesophageal functions.
ventilation.21,22 A recent study by Levine and , The relaxation of the crural diaphragm along
colleagues21 demonstrated that prolonged with the extension of the esophagus with
mechanical ventilation with diaphragmatic inac- food bolus is necessary for smooth
tivity caused diffuse atrophy of diaphragmatic swallowing.
muscle fibers. The diaphragms of brain-dead , Emesis requires a complex orchestration of
donors before organ harvest, who underwent the abdominal muscles, gastrointestional
mechanical ventilation for more than 18 hours, tract, respiratory muscles, and diaphragm.
demonstrated marked decrease in slow-twitch , The crural diaphragm acts as an external
type I and fast-twitch type II fibers when compared sphincter of the esophagus to prevent acid re-
with diaphragms of control subjects who under- flux from the stomach.
went elective thoracic surgery. It is also established
that COPD patients have increased proportion of
type I, fatigue-resistant fibers and a decreased strongly along with the abdominal muscles to
proportion of type II, fatiguing fibers.22 This fiber- increase the abdominal pressure while the gastro-
type shift is thought to be a beneficial adaptive esophageal junction is tightly closed because of
response to increased diaphragmatic loading.23 the contraction of the crural part of the diaphragm.
The shift increases fatigue resistance but During emesis (the expulsive phase), dissociation
decreases force-generating capacity.24 In of the costal and crural muscles occurs. The costal
summary, whereas several adaptation mecha- diaphragm keeps contracting to produce
nisms might allow the diaphragm to continue to increased abdominal pressure, whereas the crural
function adequately, inactivity of the diaphragm diaphragm relaxes to allow the gastric contents to
(as seen in ventilated patients or in various clinical be ejected upwards. The coordination between
conditions of diaphragmatic dysfunction or paral- the increased intra-abdominal pressure caused
ysis) can be rapidly associated with marked muscle by rapid diaphragmatic descent, costal diaphrag-
atrophy and increased proteolysis. matic contraction, and relaxation of the esopha-
geal sphincters enables expulsive vomitting.4
The diaphragm functions as an antireflux barrier;
The Role of the Diaphragm the crural diaphragm serves as an external
in Gastroesophageal Function sphincter whereas the smooth muscle of the
A detailed description of the gastroesophageal esophagus acts as an internal sphincter.26 The
junction anatomy and mechanism is beyond the crural diaphragm, an external sphincter producing
scope of this article (Box 3); a short description an esophagogastric junction pressure, seems to
of the relationship between the diaphragmatic grip the esophagus consistently and prevents
physiology and the functioning of the gastro- acid reflux from the stomach.3
esophageal area is warranted. Although the crural
part of the diaphragm has a relatively smaller role ACKNOWLEDGMENTS
in respiratory function when compared with the We are indebted to Dennis Wei for his examplary
costal part, it plays an important part in gastro- artwork, to Roger Harris for his assistance in
esophageal functions, including swallowing, vom- designing the figures, and to Basil Jardine for the
iting, and preventing gastroesophageal reflux. The radiologic images.
crural part relaxes for easy passage of a food
bolus from the esophagus to the stomach in coor- REFERENCES
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