SECTION VI
I Diaphragm
CHAPTER 56
i The Diaphragm
ANATOMY, EMBRYOLOGY,
PATHOPHYSIOLOGY, AND SURGERY OF
THE PHRENIC NERVE AND DIAPHRAGM
Konstadinos A. Plestis
Stanley C. Fell
The diaphragm is the major muscle of ventilation. It is a
dome-shaped, musculofibrous sheet that separates the
thoracic cavity from the abdominal cavity. Its periphery
consists of three groups of muscular fibers that converge
into a central tendon. These muscular fibers originate
from the lower six ribs bilaterally, from small slips arising
from the posterior aspect of the xiphoid process, from
the medial and lateral arcuate ligaments, and from the
lumbar vertebrae by two pillars or crura. The medial and
lateral arcuate ligaments are tendinous bands that extend
the vertebral attachments of the diaphragm across the
upper portion of the psoas major and quadratus lum-
borum muscles. The right crus, broader and longer than
the left, arises from the upper three lumbar vertebrae,
while the left crus arises from the corresponding upper
two lumbar vertebrae. The medial margins of the two
crura meet in the midline to form a poorly defined arch
above the aorta, the median arcuate ligament. The right
crus forms the esophageal hiatus in 64% of individuals;
however, it is not uncommon (34% of individuals) that
fibers of the left crus take part in the formation of the
right side of the esophageal orifice. Also, in 2% of individ-
uals the left crus makes up the major part of the esopha-
geal hiatus (Collis, 1968). The central tendon is a roughly
trifoliate aponeurosis. Its two lateral leaves relate to the
parietal pleura superiorlyand the peritoneum inferiorly
while the middle leaf is fused to the pericardium superi-
orly and relates to the triangular ligament of the liver in
the abdomen.
Embryologically, the diaphragm arises from five mor-
phologic elements: the central tendon, two ventrolateral
parts, and two dorsal parts. The central tendon is formed
*Supported by the Feldesman Fund for Thoracic Surgery at Mon-
tefiore Medical Center.
from the transverse septum, the ventrolateral portions
arise from the ventrolongitudinal muscle layer of the
body, and the dorsal portions are derived from the para-
vertebral musculature. These five segments fuse and leave
a pleuroperitoneal foramen posteriorly in each side of the
thoracic cavity. These two foramina close early in fetal
life. The openings through which congenital and acquired
diaphragmatic hernias occur are the pleuroperitoneal
openings posteriorly; two small passages anteriorly, just
behind the sternum; and the esophageal hiatus between
the two dorsal divisions of the diaphragm.
Contraction of the costal portion of the diaphragm
causes the lower ribs to elevate with concomitant flat-
tening of the diaphragmatic convexity, thus enlarging the
thoracic cavity. Similarly, contraction of the crural portion
adds downward displacement of the diaphragm with a
lesser effect on overall ventilation. Diaphragmatic con-
traction occurs during the early phases of expiration
during quiet breathing.
During expiration, the anterior and inferior margins
of the lung do not extend as far forward and inferiorly
as the corresponding portions of the pleural space. These
portions of the pleural cavity that are entered by the
lung only during inspiration are termed pleural recesses;
therefore, penetrating wounds or inaccurately placed tho-
racic drainage tubes do not enter the pleural space (Rob-
inson and Brodman, 1981).
The arterial supply to the diaphragm is largely via the
right and left inferior phrenic arteries, the intercostal
arteries, and the musculophrenic branches of the internal
thoracic artery. There are minor contributions from the
pericardiophrenic arteries that run with the phrenic
nerves, entering the diaphragm where the nerve pene-
trates. Venous drainage of the diaphragm is via the infe-
rior phrenic veins, which drain into the inferior vena
1499
1500 CHAPTER 56 • Anatomy, Embryology, Pathophysiology, and Surgery of the Phrenic Nerve and Diaphragm

cava. In the thorax venous drainage is via the azygos

and hemiazygos vein system. Necrosis of the diaphragm
because of vascular insufficiency has not been reported.
Motor and sensory innervation of the diaphragm is via
the phrenic nerves. The lower six or seven intercostal
nerves distribute some sensory fibers to the peripheral
portion of the diaphragm.
The diaphragm has three major apertures: the aortic,
the esophageal, and the inferior vena cava. It also has a
number of smaller ones. The esophageal hiatus, elliptical
in shape, is located at the level of T10, just left of the
midline and anterior to the aortic hiatus. It transmits the
esophagus, the vagi and sympathetic trunks, esophageal
branches of the left gastric vessels, and lymphatic vessels.
The fascia on the inferior surface of the diaphragm ex-
tends upward into the opening in a conical fashion to
attach to the wall of the esophagus about 2 cm above the
gastroesophageal junction. This fascial expansion limiting
the upward displacement of the esophagus is known as
the phrenoesophageal ligament. The vena cava traverses
the right leaf of the central tendon of the diaphragm at
the level of the T8-T9 intervertebral disk. The inferior
vena cava orifice is stretched during diaphragmatic con-
traction, thus facilitating the flow of venous blood into
the thorax during inspiration. Small branches of the right
phrenic nerve and a few lymphatics also traverse the vena
cava orifice. The aortic aperture, strictly speaking, is an FIGURE 56-1 • Lateral chest film demonstrating intrathoracic
osseoaponeurotic opening, located anterior to the lower tumor in an asymptomatic patient.
border of T12, between the crura and behind the median
arcuate ligament. The aortic aperture also transmits the
azygos vein, the thoracic duct, and lymphatic vessels that
common finding on a chest radiograph is a well-defined,
ascend from the cisterna chyli to the thorax.
usually rounded, homogeneous mass in the lower right
There are also two lesser apertures in each crus, one lung field, occupying the cardiophrenic angle on the
transmitting the greater splanchnic nerve and the other, posteroanterior view. The frequent use of computed to-
the lesser splanchnic nerve. Other structures that pass mography (CT) scans has led to an increase in the diag-
between the abdomen and the thorax through the dia- nosis of congenital diaphragmatic hernia in asymptomatic
phragm or posterior to it are the superior epigastric adults (Figs. 56-1 and 56-2).
vessels between the sternal and costal origins of the Morgagni's hernia is rare; a cumulative 3.6% incidence
diaphragm, the musculophrenic vessels between the dia- of Morgagni's hernia has been found among all patients
phragmatic origins' at the level of the T7-T8 cartilages, with congenital diaphragmatic hernias (Berandi et al,
the lower five intercostal nerves at the level of the T7 1997). It is more common in adults than in children. It
cartilage inferiorly the sympathetic trunk deep to the
medial arcuate ligament, and the inferior hemiazygos
vein.
There may be a triangular gap between the sternal and
costal origins of the diaphragm bilaterally, where the
pleura and the peritoneum are separated merely by loose
areolar tissue. Similarly, the muscular fibers of the dia-
phragm may be deficient between the costal portion of
the diaphragm and the portion arising from the lateral
arcuate ligament bilaterally. These potential spaces are
not as common as the parasternal spaces, and when they
exist the superior surface of the kidney is separated from
the pleura only by areolar tissue. It is through these
potential spaces that congenital diaphragmatic hernia
may occur in the adult. In contrast to the acute, often
life-threatening symptoms of congenital diaphragmatic
hernia in the neonate, this entity is almost always asymp-
tomatic in the adult population (MacDougal et al, 1963).
On routine chest radiographs, congenital diaphragmatic
FIGURE 56-2 • A computed tomography (CT) scan
hernia may easily be misinterpreted as mediastinal or demonstrates a Bochdaiek hernia containing retroperitoneal
pulmonary tumors (Raymond et al, 1996). The most fat. Surgical repair was not performed.
 CHAPTER 56 • Anatomy, Embryology, Pathophysiology, and Surgery of the Phrenic Nerve and Diaphragm
FIGURE 56-3 • A chest film of elderly female, interpreted as
demonstrating a juxtapericardial fat pad.
occurs parasternally through a defect between the costal
and sternal origins of the diaphragm, as previously de-
scribed. Morgagni's hernia is almost always asymptomatic
(Figs. 56-3 and 56-4). When present, symptoms are
usually gastrointestinal, such as epigastric discomfort or
FIGURE 56-4 • A barium enema, in the same patient as that
in Figure 56-3, performed to investigate sigmoid colon,
demonstrates a Morgagni hernia. Surgery was not indicated in
this case.
1501
bloating. Rarely, intestinal obstruction may occur. These
hernias are more common on the right hemidiaphragm
because the pericardium protects the left side of the
diaphragm; occasionally they occur bilaterally. Obese, el-
derly females are most usually affected. A sac is almost
always present, and omentum and colon are the usual
contents. Surgical repair, when indicated, is best per-
formed via a subcostal transperitoneal approach. The
contents are reduced, the sac is excised, and the diaphrag-
matic defect is closed by suturing the edge of the defect
to the posterior rectus sheath, and to the lower ribs, if
required. Laparoscopic repair and repair via video-as-
sisted thoracoscopic surgery (VATS) have been described
in symptomatic patients, the former being technically
easier than the latter (Hussong et al, 1997; Newman
et al, 1995). The hernia sac should not be removed
during laparoscopic repair, as this may result in massive
pneumomediastinum with potential cardiorespiratory
complications.
Bochdalek's hernia has been reported in up to 6% of
the adult population (Gale, 1985). These hernias may
contain retroperitoneal fat, omentum, colon, and stomach
(Kirkland, 1959). Right hemidiaphragm occurrence has
been reported (Campbell and Lilly, 1982). Symptoms
caused by intestinal obstruction or respiratory compro-
mise may be episodic due to spontaneous reduction of
herniated viscera. The diagnosis of a Bochdaleck hernia
in a patient with intermittent symptoms may prove a
challenge despite the most sophisticated diagnostic test-
ing. Repair in the adult is best performed via the trans-
thoracic approach. Large defects may require a prosthetic
patch or advancement of the diaphragm to a higher rib
for adequate repair. VATS has also been employed in the
management of this condition with promising results
(Silen et al, 1995).
POROUS DIAPHRAGM SYNDROMES
Porous diaphragm syndrome is defined as the phenome-
non of peritoneopleural transphrenic passage of fluids,
blood, gases, tissue, and exudates by way of a common
pathophysiologic feature, a hole in the diaphragm.
Kirschner (1998) was the first to clearly define the vari-
ous porous diaphragm syndromes (Table 56-1). The de-
fects are usually located in the tendinous portions of the
diaphragm between the interlacing tendinous or muscle
fibers, and less commonly in the muscular portions of
the diaphragm. They may be single, multiple, or even
cribriform. Ranging in size from a tiny pinhole to a
centimeter or more in diameter, they definitely favor the
right hemidiaphragm. Some defects may be congenital;
however, the majority are acquired. Kirschner noted that
acquired defects occur as a result of challenges to the
integrity of the diaphragm by various space-occupying
intraperitoneal substances that increase intra-abdominal
pressure or produce necrosis of the diaphragm. Clinically,
patients usually present with thoracic findings such as
pleural effusion, pneumothorax, hemothorax, and empy-
ema secondary to abdominal pathology.
THE PHRENIC NERVE
The phrenic nerve arises chiefly from the C4 nerve root
with contributions from the C3 and C5 nerve roots. It
1502 CHAPTER 56 • Anatomy, Embryology, Pathophysiology, and Surgery of the Phrenic Nerve and Diaphragm
TABLE 5 6 - 1 • Porous Diaphragm Syndromes
FLUIDS
Spontaneous ascites
Cirrhosis of t h e liver
Meigs' syndrome
Pancreatic ascites
Chylous ascites
Iatrogenic ascites
Peritoneal dialysis
Hemoperitoneum
Abdominal/tubal pregnancy
R u p t u r e d spleen
R u p t u r e d aortic aneurysm
Operative hemorrhage
Endometriosis
GASES
Pneumoperitoneun
Catamenial pneumothorax
Therapeutic pneumoperitoneum
Spontaneous p n e u m o p e r i t o n e u m
Laparoscopic p n e u m o p e r i t o n e u m
Diagnostic p n e u m o p e r i t o n e u m
TISSUE
Endometriosis
Catamenial p n e u m o t h o r a x
Pleural e n d o m e t r i o s i s
EXUDATES/SECRETIONS
Subphrenic abscess
Liver abscess
Pancreatic pseudocyst
Bilothorax
INTESTINAL CONTENTS
P e r f o r a t e d peptic ulcer disease
From Kirschner PA: Porous diaphragm syndromes. Chest Surg Clin
North Am 8:449-472, 1998; with permission.
originates on the scalenus medius, at the lateral border
of the scalenus anterior under the sternomastoid muscle,
at the level of the upper border of the thyroid cartilage.
It descends on this muscle beneath a tough fascial invest-
ment, crossing the muscle from its lateral to its medial
border on the way to the thoracic outlet. At the root of
the neck, the phrenic nerve is crossed by the transverse
cervical and suprascapular arteries; the left phrenic nerve
is crossed also by the thoracic duct. At the apex of the
thorax the right phrenic nerve lies behind the innominate
vein and crosses the internal mammary artery laterally to
medially, usually in front of the artery. The left phrenic
nerve descends on the front of the first portion of the
subclavian artery to enter the thorax. The C5 nerve root
usually joins the phrenic nerve trunk on the surface of
the scalenus anterior. However, it may descend into the
thorax before it joins the main nerve. This is an im-
portant consideration in diaphragmatic pacing. In the
thorax the right phrenic nerve descends along the right
side of the innominate vein and the superior vena cava,
and then along the side of the pericardium anterior to
the hilum of the lung. It then passes along the upper
border of the inferior vena cava to just above the dia-
phragm where it branches. The left phrenic nerve de-
scends between the left common carotid and subclavian
arteries crossing in front of the left vagus nerve, then
passing lateral to the arch of the aorta continuing down
the side of the pericardium where it branches.
Merendino and associates (1956) clearly established
the anatomic and physiologic distribution of the phrenic
nerves at the diaphragm, and they also developed the
strategy for diaphragmatic incisions. Their findings are
freely quoted or paraphrased. The right phrenic nerve
reaches the diaphragm just lateral to the inferior vena
cava, while the left phrenic nerve enters the diaphragm
lateral to the left border of the heart, in a slightly more
anterior plane than the right phrenic nerve. Both nerves
divide at the level of the diaphragm or just above it into
several terminal branches, the right phrenic nerve being
the mirror image of the left. Two or three of these termi-
nal branches are usually very fine and are distributed to
the serosal surfaces of the diaphragm. Three muscular
branches arise directly from the phrenic nerve; one is
directed anteromedially toward the sternum, another is
directed laterally anterior to the lateral leaf of the central
tendon, and the third one is directed posteriorly. The
last-mentioned ramus divides into a branch that runs
posterior to the lateral leaf of the tendon, and a branch
that runs posteriorly and medially to the region of the
crus. These four branches are named the sternal or ante-
rior branch, the anterolateral branch, the posterolateral
branch, and the crural or posterior branch (Fig. 56-5).
They are usually located deep within the muscle rather
than lying exposed on the undersurface of the diaphragm
as it is described in anatomic texts. Because of the rapid
diminution in the size of the phrenic nerve rami, it is
impractical to delineate areas in the diaphragm where
incisions can be made safely. However, circumferential
incisions anywhere in the periphery of the diaphragm
result in little, if any, loss of diaphragmatic function
(Fig. 56-6). Similarly, incisions in the central tendon and
lateral or transverse incisions from the midaxillary line
medially do not result in diaphragmatic paralysis (Sicular,
1992). Prior to Merendino's seminal work, radial inci-
sions in the diaphragm were customarily employed. The
radial incision in the diaphragm from the costal margin
to the esophageal hiatus results in almost total diaphrag-
matic paralysis, and it should be condemned (Fig. 56-7).
The radial incision was a major cause of postoperative
morbidity and mortality in patients subjected to thoraco-
laparotomy; it resulted in ineffective cough, lower lobe
atelectasis, and associated pneumonia. Nevertheless, it is
still described in the literature (Heitmiller, 1992).
Technique for Diaphragmatic Incision
A circumferential incision is made with electrocautery 3
cm from the costal margin. The cut edges of the dia-
phragm are grasped with Allis clamps and elevated, facili-
tating further incision. Bleeders are managed with electro-
cautery, but large branches of the phrenic artery are best
controlled with suture ligatures. When a diaphragmatic
incision is made in association with antireflux proce-
dures, it is best to use only the anterolateral two thirds
of the diaphragm. Stay sutures are placed in the diaphrag-
matic flap and elevated over the rib spreader, as described
FIGURE 5 6 - 5 • Branches of t h e phrenic nerve at
the d i a p h r a g m . ( A d a p t e d f r o m M e r e d i n o KA,
Johnson RS, Skinner HH et al: The
i n t r a d i a p h r a g m a t i c d i s t r i b u t i o n o f t h e phrenic
nerve w i t h particular reference t o t h e p l a c e m e n t
of d i a p h r a g m a t i c incisions a n d c o n t r o l l e d
segmental paralysis. Surgery 39:189, 1956.)

FIGURE 5 6 - 6 • D i a p h r a g m incisions. (A radial incision;

B, circumferential incision; C a n d D, incisions in safe
areas.) ( A d a p t e d f r o m M e r e d i n o KA, Johnson RS,
Skinner HH et al: The i n t r a d i a p h r a g m a t i c d i s t r i b u t i o n
o f t h e phrenic nerve w i t h particular reference t o t h e
placement of d i a p h r a g m a t i c incisions and c o n t r o l l e d
segmental paralysis. Surgery 39:189, 1956.)

FIGURE 5 6 - 7 • A radial incision t h a t can cause

paralysis of a m a j o r p o r t i o n of phrenic nerve. ( A d a p t e d
f r o m M e r e d i n o KA, Johnson RS, Skinner HH et al: The
i n t r a d i a p h r a g m a t i c d i s t r i b u t i o n o f t h e phrenic nerve
w i t h particular reference t o t h e p l a c e m e n t o f
diaphragmatic incisions a n d c o n t r o l l e d segmental
paralysis. Surgery 39:189, 1956.)

1503
1504 CHAPTER 56 • Anatomy, Embryology, Pathophysiology, and Surgery of the Phrenic Nerve and Diaphragm
Outline of base
Esophagus of pericardium
Incision
by Collis (1968). This maneuver gives ample exposure
to the "attic of the abdomen" and simplifies management
of the vasa brevia and the gastrohepatic ligament. By
retracting the stay sutures caudally, the operator can dis-
sect the intrathoracic aspect of the diaphragmatic attach-
ment to the esophagogastric junction with two fingers
inserted in the abdomen while dissecting the chest,
allowing for repair of the crura in the abdomen and
performance of a fundoplication before closure of the
diaphragmatic incision. For left transthoracic esophago-
gastric resections, the circumferential incision may be
carried down to the esophageal hiatus. If the tumor is
adherent to the diaphragm, wide resection of the dia-
phragm can be easily performed using this technique.
The diaphragmatic incision through the central tendon
FIGURE 56-8 • Septum transversum incision for
transdiaphragmatic exposure of the cardia. A, Cross-
section view; 8, side view. (Adapted from Meredino
KA, Johnson RS, Skinner HH et al: The
intradiaphragmatic distribution of the phrenic nerve
with particular reference to the placement of
diaphragmatic incisions and controlled segmental
paralysis. Surgery 39:189, 1956; and Sicular A: Direct
septum transversum incision to replace
circumferential diaphragmatic incision in operations
of the cardia. Am J Surg 164:167, 1992.)
described by Sicular (1992) is shorter compared with the
circumferential incision and has the advantage of rapid
performance (Fig. 56-8). However, it does impose some
risk of trauma to the left phrenic nerve. Incisions in the
diaphragm should be closed with two layers of nonab-
sorbable sutures. A first layer of interrupted mattress
sutures is followed by a layer of continuous polypropyl-
ene sutures. This technique obviates the risk of diaphrag-
matic disruption, which is a known complication of dia-
phragmatic closure with absorbable sutures.
Phrenic Nerve Injury
Causes of phrenic nerve injury are listed in Table 56-2.
Cardiac procedures in both the pediatric and adult popu-
 CHAPTER 56 • Anatomy, Embryology, Pathophysiology, and Surgery oj the Phrenic Nerve and Diaphragm 1505

TABLE 5 6 - 2 • Causes of Phrenic Nerve Injury procedure, diaphragmatic function usually returned in 6
months; however, it was permanent in 20% of cases
Cervical (Iverson et al, 1966). Notably, in 50% of these patients
Birth injury there was delayed evidence of diminished diaphragmatic
Blunt-penetrating trauma: spine or soft tissue function resulting in ventilatory loss. Currently, tempo-
Operative injury rary paralysis of the phrenic nerve can be instituted
Neck surgery: thyroid, neck dissection, splenectomy
Jugular vein cannulation
during thoracotomy by local anesthetic injection. This
Deliberate: crush, exeresis for tuberculosis technique is used occasionally to diminish the pleural
Thoracic space following p u l m o n a r y resections. Pneumoperito-
neum is instituted concomitantly to facilitate elevation of
Trauma
Operative injury the diaphragm.
Thymectomy/mediastinal tumor In the postoperative patient who is supine and on
Pulmonary resection ventilatory support, diaphragmatic paralysis may not be
Deliberate: pneumonectomy, hiatal hernia repair
suspected because positive-pressure ventilation tends to
Blalock-Taussig shunt
Pericardiectomy mask abnormal findings. In the spontaneously breathing
Aortic arch aneurysms patient, left pleural effusion, lower lobe atelectasis, and
CABG: pericardial traction, topical hypothermia, ITA harvest elevation of the left hemidiaphragm are, unfortunately,
Neoplastic common sequelae of cardiac surgery and may mask phre-
Lung cancer nic nerve injury. Similarly, diaphragmatic paralysis is dif-
Malignant mediastinal tumor ficult to diagnose by either chest radiography or fluoros-
Lymphoma copy. In cases with a high index of suspicion, phrenic
Infectious n e r v e c o n d u c t i o n s t u d i e s are required (Russel et al,
Typhoid, pneumonias 1991). Measurement of phrenic nerve conduction time
Viral: polio, herpes zoster, rubella allows direct evaluation of phrenic nerve function and
Idiopathic integrity. An electrical stimulus is applied over the phre-
(Probable undiagnosed viral infection) nic nerve in the neck and a diaphragmatic electromyo-
gram from T7 and T8 intercostal spaces is displayed on
CABG, coronary artery bypass graft; ITA, internal thoracic artery. a storage oscilloscope. Prolongation of the phrenic la-
tency by more than 2 msec is considered indicative of
phrenic nerve paralysis. This test can establish the diag-
lations are the most common cause of phrenic nerve nosis at the bedside, and if it is serially performed, may
injury with resultant paralysis of the hemidiaphragm. prognosticate recovery. In cases in which recovery of
Phrenic nerve injury during cardiac procedures may re- phrenic nerve function is expected, prolonged ventilatory
sult from transection, contusion, and stretch or thermal support is indicated.
injury. Thermal injury may be due to heat caused by the In the nonacute situation, elevation of the hemidi-
injudicious application of electrocautery or due to cold aphragm on chest radiograph may suggest paralysis. Flu-
following topical cardiac hypothermia. In a series of 831
closed cardiac surgical procedures in infants and children,
Zhao and co-workers (1985) noted an incidence of phre-
nic nerve injury in 2 . 1 % of cases. This injury is most
commonly noted following systemic-pulmonary artery
anastomosis, atrial septectomy, or combined pulmonary
artery banding and ligation of a patent ductus arteriosus.
The most frequent cause of phrenic nerve injury during
operations for acquired heart disease is from the intraper-
icardial application of saline slush as a means of myocar-
dial preservation. The incidence of this complication has
been reported to be as high as 73%. However, it was
reduced to 17% with the use of an insulating pad to
protect the phrenic nerves (Esposito and Spencer, 1987).
Typically the left hemidiaphragm is most commonly af-
fected, although bilateral injuries are occasionally noted.
The proximity of the phrenic nerves to the internal mam-
mary artery puts them at risk during harvest of the artery
for coronary artery bypass procedures. Nerve injury in
these cases is usually caused by thermal injury from
cautery dissection or due to stretch injury (Markland et
al, 1985). Phrenic nerve paralysis was formerly employed
as an adjunct to collapse therapy for tuberculosis. Resec-
tion of the phrenic nerve was performed to ensure total
and permanent paralysis (Fig. 5 6 - 9 ) , while in other in- FIGURE 56-9 • Chest film of 70-year-old female who had
phrenicectomy for treatment of pulmonary tuberculosis 40
stances phrenic nerve crush was used. After the latter years prior to her coronary artery bypass.
1506 CHAPTER 56 • Anatomy, Embryology, Pathophysiology, and Surgery of the Phrenic Nerve and Diaphragm
oroscopy is considered the most reliable method to docu-
ment diaphragmatic paralysis. The diagnosis is
established by the "sniff test," which demonstrates para-
doxical motion of the diaphragm on fluoroscopy. The
paradoxical excursion should involve the entire hemidi-
aphragm and should exceed 2 cm for establishment of the
diagnosis of diaphragmatic paralysis (Alexander, 1996).
However, paradoxical movement of the diaphragm has
been noted in 6% of normal subjects during the sniff test
(Shim, 1980).
Pathophysiology of Diaphragmatic Paralysis
Infants are more likely to have respiratory difficulties
from diaphragmatic paralysis than older children and
adults. The intercostal and accessory muscles of respira-
tion in infants do not contribute significantly to respira-
tory mechanics; thus unilateral diaphragmatic paralysis
may produce a 50% loss in pulmonary function (Mickell
et al, 1978). Because infants are customarily maintained
in the recumbent position, there is further reduction in
vital capacity. Also, the mobile mediastinum of the infant
is shifted to the nonaffected side, further diminishing
pulmonary function. Further, the narrow airway in in-
fants predisposes to bronchial obstruction from retained
secretions that cannot be readily evacuated by crying
or cough.
In normal adults, diaphragmatic excursion may con-
tribute 30% to 60% of total tidal volume. With unilateral
diaphragmatic paralysis, there is a decrease of 20% to
30% of vital capacity and maximum voluntary ventila-
tion, and a 20% decrease in oxygen uptake on the in-
volved side, as well as decreased residual volume and
total lung capacity (Zhao et al, 1985). Hypoxemia and
hypercapnia result. These numbers increase when pa-
tients are supine. Disabling gastroesophageal reflux may
occur in left-sided paresis. These findings are increased
with the patient supine. Disabling gastroesophageal reflux
may occur in left-sided paresis. Nevertheless, in patients
with sufficient respiratory reserve, unilateral diaphrag-
matic paralysis may not be symptomatic despite the ven-
tilatory losses previously noted.
Treatment of Diaphragmatic Paralysis
A few cases of repair of a transected phrenic nerve have
been reported, without documentation of success by elec-
trophysiologic testing (Merav et al, 1983; Shoemaker et
al, 1981). The management of phrenic nerve injury and
diaphragmatic paralysis in infants following cardiac sur-
gery is still controversial. Some authors have used venti-
latory support in excess of 1 month for managing this
problem and rarely do they employ diaphragmatic plica-
tion (Zhao et al, 1985). In Mickell and co-workers's
series (1978) 19 of 32 patients demonstrated complete
resolution of diaphragmatic paralysis, 9 were asympto-
matic with persistent defect, and 1 patient was treated
with surgical plication. Shoemaker and co-workers
(1981) demonstrated reduction in the duration of ventila-
tory support, extubating his patients within 6 days fol-
lowing diaphragmatic plication. It is clear that intraopera-
tive recognition of phrenic nerve injury in the neonate
is an indication for immediate diaphragmatic plication;
however, when this injury is noted in a child older than
3 months, it can usually be managed successfully with
continuous positive airway pressure through a nasotra-
cheal tube. In 34 cases of diaphragmatic paralysis follow-
ing pediatric cardiac surgery, it was noted that no patient
older than 3 years of age required intubation for longer
than 2 weeks (Lynn et al, 1982). Patients younger than 3
years of age who still required intubation and continuous
positive airway pressure 3 to 4 weeks following surgery
were candidates for diaphragmatic plication because of
the potential complications of long-term intubation (pul-
monary and systemic infection) and difficulties in main-
taining adequate caloric intake. Shoemaker and associates
report (1981) confirmed the need for diaphragm plication
in infants less than 5 months old.
Most adults with unilateral diaphragmatic paralysis
are asymptomatic; those having troublesome dyspnea on
exertion or orthopnea may benefit from diaphragmatic
plication. Graham and associates (1990) reported 10-
year follow-up of 17 patients treated with diaphragmatic
plication. All patients were less dyspneic with objective
improvement in spirometry and oxygenation. Diaphrag-
matic plication has also been successfully employed in
adults following phrenic nerve injury associated with
cardiac surgery and after pneumonectomy with deliberate
sacrifice of the phrenic nerve (Glassman et al, 1994;
Takeda et al, 1994).
• REFERENCES
Alexander C: Diaphragm movements and a diagnosis of diaphragmatic
paralysis. Clin Radiol 17:79-83, 1966.
Berandi RS, Tenquist J, Sauter D et al: An update on the surgical aspects
of Morgagni's hernia. Surg Rounds 370-376, 1997.
Campbell DN, Lilly JR: The clinical spectrum of right Bochdalek's
hernia. Arch Surg 117:341-344, 1982.
CollisJL: Surgical control of reflux in hiatus hernia. AmJ Surg 115:465-
471, 1968.
Collis JL, Kelly TD, Wiley AM: Anatomy of the crura of the diaphragm
and the surgery of hiatus hernia. Thorax 9:175-189, 1954.
Eposito JA, Spencer FC: The effect of pericardial insulation on hypo-
thermic phrenic nerve injury during open heart surgery. Ann
Thorac Surg 43:303-308, 1987.
Gale ME: Bochdaleck hernias: Prevalence and CT characteristics. Radi-
ology 156:449-452, 1985.
Glassman LR, Spencer FC, Bauman G et al: Successful plication for
postoperative diaphragmatic paralysis in an adult. Ann Thorac
Surg 58:1754-1755, 1994.
Graham ER, Kaplan D, Evans CC et al: Diaphragmatic plication for
unilateral diaphragmatic paralysis: A ten-year experience. Ann
Thorac Surg 49:248-252, 1990.
Heitmiller R: Results of standard left thoracoabdominal esophagogas-
trectomy Semin Thorac Cardiovasc Surg 4:314-319, 1992.
Hussong R, Landreneau R, Cole F: Diagnosis and repair of Morgagni
hernia with video assisted thoracic surgery. Ann Thorac Surg
63:1474-1475, 1997.
Iverson LI, Mittal A, Dugan D et al: Injuries to the phrenic nerve
resulting in diaphragmatic paralysis with special reference to
stretch trauma. Am J Surg 132:263-266, 1966.
Kirkland JA: Congenital posterolateral diaphragmatic hernia in the
adult. Br J Surg 47:16-22, 1959.
Kirschner PA: Porous diaphragm syndromes. Chest Surg Clin North
Am 8:449-472, 1998.
Lynn A, Jenkins J, Edmonds J: Diaphragmatic paralysis after pediatric
cardiac surgery: A retrospective analysis of 34 cases. Crit Care
Med 11:280-282, 1982.
MacDougal J, Abbott A, Goodhand T: Herniation through congenital
diaphragmatic defects in adults. Can J Surg 6:301-316, 1963.
Markand O, Moorthy S, Mahomed Y: Postoperative phrenic nerve palsy
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in patients with open heart surgery. Ann Thorac Surg 39:68-73,
1985.
Merav A, Attai L, Condit D: Successful repair of a transected phrenic
nerve with restoration of diaphragmatic function. Chest 84:642-
644, 1983.
Merendino KA, Johnson RJ, Skinner HH et al: The intradiaphragmatic
distribution of the phrenic nerve with particular reference to the
placement of diaphragmatic incisions and controlled segmental
paralysis. Surgery 39:189-198, 1956.
Mickell J, Oh K, Siewers R et al: Clinical implications of postoperative
unilateral phrenic nerve paralysis. J Thorac Cardiovasc Surg
76:297-304, 1978.
Newman L, Eubanks S, Bridges WM et al: Laparoscopic diagnosis and
treatment of Morgagni hernia. Surg Laparosc Endosc 5:27-31,
1995.
Raymond GS, Miller RM, Muller NL, Logan PM: Congenital thoracic
lesions that mimic neoplastic disease on chest radiographs of
adults. AJR Am J Roentgenol 168:763-769, 1996
Robinson G, Brodman R: Going down the tube. Ann Thorac Surg
31:400-401, 1981.
I IMAGING OF THE DIAPHRAGM
David S. Gierada
Richard M. Slone
Matthew J. Fleishman
Diagnostic imaging of the diaphragm is challenging due
to its thin structure and complex shape. Abnormalities
that affect the diaphragm are often first detected on chest
radiographs as an alteration in position or shape. Cross-
sectional imaging studies, primarily computed tomogra-
phy (CT) and occasionally magnetic resonance imaging
(MRI), can depict structural defects and intrinsic and
adjacent pathology in greater detail. Fluoroscopy is the
primary radiologic means of evaluating diaphragm mo-
tion, although MRI and ultrasound can also image this
function. This chapter illustrates the normal appearance
of the diaphragm; the evaluation of abnormalities in
shape, position, and structure; and the role of imaging in
specific conditions, including congenital and acquired
hernias, diaphragm paralysis, and diaphragm masses.
THE NORMAL DIAPHRAGM
Radiography
On chest radiographs, the superior margin of each hemi-
diaphragm with overlying parietal pleura forms a dome-
shaped interface separating aerated lung from the opaque
soft tissues of the abdomen. The heart with subjacent
pericardium and fat forms a relative depression between
the two hemidiaphragms, obscuring the central and ante-
romedial portions of the diaphragm. Intraperitoneal free
air outlining the inferior surface of the diaphragm reveals
• The Diaphragm/Imaging of the Diaphragm 1507
Russel R, Molvey D, LaRoche C et al: Bedside assessment of phrenic
nerve function in infants and children. J Thorac Cardiovasc Surg
101:143-147, 1991.
Shim C: Motor disturbances of the diaphragm. Clin Chest Med 1:125-
129, 1980.
Shoemaker R, Palmer G, Brown J et al: Aggressive treatment of acquired
phrenic nerve paralysis in infants and small children. Ann Thorac
Surg 32:252-259, 1981.
Sicular A: Direct septum transversum incision to replace circumferential
diaphragmatic incision in operations on the cardia. Am J Surg
164:167-170, 1992.
Silen ML, Canvasser DA, Kurkchubasce AG et al: Video-assisted tho-
racic surgical repair of a foramen of Bochdalek hernia. Ann Thorac
Surg 60:448-450, 1995.
Takeda S, Nakahara K, Fujii Y et al: Plication of paralyzed hemidi-
aphragm after right sleeve pneumonectomy. Ann Thorac Surg
58:1755-1778, 1994.
Zhao H, DAgostino R, Pitlick P et al: Phrenic nerve injury complicating
closed cardiovascular surgical procedures for congenital heart dis-
ease. Ann Thorac Surg 39:445-449, 1985.
its thinness (Fig. 56-10). A smooth scalloped or polyar-
cuate contour of the diaphragm is a normal variation,
and most frequently involves the right hemidiaphragm.
The lumbar portions of the diaphragm occasionally may
be seen on the frontal view and the sternocostal inser-
tions are visible on the lateral view when there is ade-
quate x-ray penetration and adjacent fat on both sides.
Several signs help distinguish the right from left hemi-
diaphragm on the lateral radiograph (Fig. 56-11). The
entire anteroposterior (AP) extent of the right hemidi-
aphragm is usually visible because of its interface with
the lung, while a variable segment of the anterior left
hemidiaphragm is usually obscured by the adjacent heart
and mediastinal fat. Gas in the stomach or splenic flexure
of the colon beneath the left hemidiaphragm can be used
to identify this side on the lateral projection; interposi-
tion of the colon between the liver and right hemidi-
aphragm is seen in less than 1% of patients (Prassopoulos
et al, 1996). Finally, in a left lateral radiograph (left side
of the patient is in contact with the film cassette), the
right ribs are more magnified than the left ribs. Therefore,
the hemidiaphragm that inserts along the margin of the
larger ribs can be identified as the right, and vice versa.
Cross-Sectional Imaging
The muscular diaphragm can be seen on cross-sectional
imaging studies; however, due to its shape, thinness, and
1508 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm

FIGURE 56-10 • Normal diaphragm thickness.

Erect radiograph reveals the shape and
thickness of the diaphragm (arrows) in a
patient with a large amount of intraperitoneal
free air secondary to a bowel perforation. The
superior margins of the central, anterior aspect
of the diaphragm are obscured by the heart
and mediastinal fat. (From Gierada DS, Slone
RM, Fleishman MJ: Imaging evaluation of the
diaphragm. Chest Surg Clin North Am 8:237,
1998.)

close contact with the liver and spleen, portions are often
obscured. On CT, the diaphragm has the attenuation of
skeletal muscle, and is best seen where it is surrounded
by lower attenuation fat (Fig. 56-12A). However, some
segments of the diaphragm in contact with the liver or
spleen may be visible because the diaphragm enhances to
a lesser degree with intravenous contrast (Fig. 56-12B).
Nodular infoldings of the diaphragm near costal inser-
tions are often seen (Fig. 56-13), particularly in elderly
individuals, and these may indent the liver or spleen to
simulate focal lesions (Fig. 56-14) or simulate peritoneal
implants. The domes of the diaphragm are best depicted
using volumetric (helical) CT and coronal or sagittal
reformations (Brink et al, 1994).
The direct multiplanar imaging capability of MRI can
improve depiction of the diaphragm, which is clinically
useful in selected cases. On MRI, the muscular diaphragm
has signal intensity similar to skeletal muscle, liver, and
spleen on all pulse sequences, and similar to CT, it is
best depicted where it is separated from these structures
by high signal intensity abdominal or mediastinal fat
(Gierada et al, 1996). As on CT studies, the greater
enhancement of the liver after intravenous gadolinium
administration can improve depiction of the diaphragm
with MRI (Kanematsu et al, 1995). Occasionally, short
segments are sufficiently thick to allow distinction from
the adjacent liver without contrast (Gierada et al, 1996).
The diaphragmatic crura arise from the anterior as-
pects of the L1-L3 vertebral bodies on the right and the
LI and L2 vertebral bodies on the left (Williams et al,
1989). The right crus is larger, and its medial fibers
decussate around the esophagus to form the esophageal
hiatus, which may be seen on CT or MRI scans when
appropriately oriented in the axial plane (Fig. 56-14A).
The crura form the boundary of the retrocrural space
(Fig. 56-14B and C). The aortic hiatus, which lies poste-
rior to the esophageal hiatus, and the inferior vena caval
hiatus, which passes through the central tendon, are not
well depicted in the axial plane, but they may be seen in
coronal or sagittal planes.
Lymph nodes along the anterior aspect of the central
diaphragm drain the diaphragm, anterior mediastinum,
and adjacent liver (Rouviere, 1938). These anterior dia-
phragmatic (also referred to as pericardial and cardi-
ophrenic angle) lymph nodes are located anterior to the
diaphragm and posterior to the xiphoid and adjacent
costal cartilages in the cardiophrenic angles (Fig. 56-15).
One or two lymph nodes, usually smaller than 5 mm in
diameter, are normally visible on CT scans (Aronberg et
al, 1986). The inferior pulmonary ligaments (Cooper et
al, 1983; Godwin et al, 1983; Rost and Proto, 1983) and
phrenic nerves and vessels (Berkmen et al, 1989; Ujita et
al, 1993) are sometimes visible along the domes of the
diaphragm on CT

FIGURE 56-11 • Distinguishing the hemidiaphragms on the

lateral chest radiograph. The right hemidiaphragm (black arrows)
is visible to the anterior chest wall and extends posteriorly to the
margin of the more magnified right ribs (R) on this standard
lateral film obtained with the left side of the chest in contact
with the film cassette. The left hemidiaphragm (white arrows) is
obscured anteriorly by the subjacent heart, extends posteriorly to
the less magnified left ribs (L), and lies above air-filled colon (C).
(From Gierada DS, Slone RM, Fleishman MJ: Imaging evaluation
of the diaphragm. Chest Surg Clin North Am 8:237, 1998.)
 CHAPTER 56 • The Diaphragm/Imaging oj the Diaphragm 1509

FIGURE 56-12 • Normal diaphragm on a contrast enhanced computed tomography scan. A, A scan through the upper abdomen
in a 30-year-old man reveals portions of the diaphragm (open arrows) that have adjacent low attenuation fat (f) or aerated lung.
Segments of the diaphragm in contact with structures having similar attenuation such as the liver (L), spleen (Sp), or skeletal
muscle (M) are not separately visible. St, stomach. B, In this 78-year-old man, the diaphragm (arrowheads) enhances less than the
liver (L), but the same as skeletal muscle (m) and can be distinguished. Note the normal nodular appearance of the right crus
(black arrow). (From Gierada DS, Slone RM, Fleishman MJ: Imaging evaluation of the diaphragm. Chest Surg Clin North Am
8:237, 1998.)

The diaphragm can also be seen using ultrasound.

Although of similar echogenicity to the liver, the dia-
phragm can be distinguished because the acoustic imped-
ance of these structures differs, resulting in specular re-
flections that delineate the interface between them.
However, the field of view with ultrasound is limited,
and the diaphragm is more difficult to see in obese
patients, in whom liver is positioned higher up under the
rib cage, and in areas where the sound waves are blocked
by air in the stomach or intestines. Hence, ultrasound is
used infrequently in clinical evaluation.
Abnormalities Affecting the
Diaphragm
ABNORMALITIES OF DIAPHRAGM
POSITION
Alterations in diaphragm position or contour seen on
chest radiographs may be due to intrathoracic or intra-
abdominal processes, or they may be intrinsically related
to the diaphragm. Normally, the dome of the right hemi-
diaphragm projects at about the level of the anterior 6th

FIGURE 56-13 • Nodular diaphragm folds. Image in a 76-year-

old man demonstrates multiple normal nodular infoldings of the
right and left hemidiaphragm (arrows). (A, aorta; C, colon; E,
esophagus; L, liver; Sp, spleen; St, stomach.) (From Gierada DS,
Slone RM, Fleishman MJ: Imaging evaluation of the diaphragm.
Chest Surg Clin North Am 8:237, 1998.)
 FIGURE 56-14 • Normal variation of costal diaphragm slips
and normal retrocrural space. A, A computed tomography scan
through the upper abdomen reveals a nodular, low
attenuation focus surrounded by hepatic parenchyma {black
arrow). B and C, On successive caudal images, the nodular
focus is seen to be contiguous with a thickened portion of the
diaphragm near its costal attachment. Also note the
esophageal hiatus {curved arrow) bordered by the right (re)
and left (Ic) crura. The crura outline the retrocrural space,
which contains the aorta (A), lower posterior mediastinal fat
(f), azygos {white arrow) and hemiazygos {arrowhead) veins.
Smaller structures adjacent to the azygos vein likely represent
the thoracic duct and tiny lymph nodes. (A, aorta; j,
gastroesohageal junction; L, liver; Sp, spleen; St, stomach.)
(From Gierada DS, Slone RM, Fleishman MJ: Imaging
evaluation of the diaphragm. Chest Surg Clin North Am 8:237,
1998.)

FIGURE 56-15 • Anterior diaphragmatic lymphadenopathy in a patient with lymphoma. A and B, A computed tomography scan
shows enlarged lymph nodes {white arrows) in the pericardial fat, anterior to the diaphragm {arrowheads). Note the thin
enhancing caudal tip of atelectatic lung {black arrows), not to be mistaken for the diaphragm. (A, aorta; E, pleural effusion; H,
heart; L, liver; Sp, spleen; St, stomach; V, inferior vena cava.)

1510
 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm
rib and posterior 10th rib on erect PA chest radiographs
obtained in full inspiration (J u m \ 1987; Lennon and
Simon, 1965). It may be slightly higher (one-half rib
level) in obese individuals and lower in thin persons.
The left hemidiaphragm is usually positioned up to one
rib interspace, or several centimeters, below the right
hemidiaphragm (Armstrong et al, 1995; Juhl, 1987;
Tarver et al, 1989), although in about 10% of normal
subjects it is at the same level or slightly higher (Fel-
son, 1973).
CT usually helps in further assessment of diaphragm
position or contour abnormalities, and sometimes it re-
veals unsuspected abnormalities when it is performed for
other indications. The primary indication for MRI of the
diaphragm is assessment of congenital or acquired her-
nias. Suspected diaphragm paralysis is assessed using
fluoroscopy.
Unilateral Elevation
Lung volume loss is one of the most common causes of
unilateral hemidiaphragm elevation (Table 56-3); it can
be due to atelectasis, partial lung resection, radiation
or post-inflammatory fibrosis, or congenital hypoplasia.
Additional signs of volume loss that may be present
include ipsilateral shifting of mediastinal structures and
narrowing of the intercostal spaces. Malignant mesotheli-
oma can encase the lung and cause restrictive disease
with resultant ipsilateral volume loss and hemidiaphragm
TABLE 5 6 - 3 • Hemidiaphragm Elevation
UNILATERAL
Lung volume loss (atelectasis, lobar collapse, partial lung
resection, radiation fibrosis, congenital pulmonary
hypoplasia, encasement by tumor)
Eventration
Abdominal disease (dilated stomach or colon, hepatomegaly,
splenomegaly, subphremic abscess)
Phrenic nerve paralysis
Splinting (rib fracture, pneumonia, infarction, abscess,
peritonitis)
Mimics (subpulmonic pleural effusion, large pleural mass,
diaphragmatic hernia)
After single lung transplant for pulmonary fibrosis
Phrenoplasty
BILATERAL
Lung volume loss (suboptimal inspiration, supine positioning,
atelectasis, lung resection, pulmonary fibrosis)
Abdominal mass effect (obesity, pregnancy, marked bowel
dilation, ascites, hepatosplenomegaly, large abdominal
tumors)
Eventration
Subpulmonic pleural effusions
Neuromuscular disease (quadriplegia, multiple sclerosis,
amyotrophic lateral sclerosis, Guillain-Barre syndrome,
myasthenia gravis, Eaton-Lambert syndrome, muscular
dystrophy, steroid or alcohol myopathy, rhabdomyolysis)
Connective tissue disease (fibrosis in rheumatoid arthritis,
sclerodema, and ankylosing spondylitis; weakness in systemic
lupus erythematosus, polymyositis)
Endocrine and metabolic disorders (hypothyroidism,
hyperthyroidism, Cushing's disease, hypokalemia,
hypophosphatemia, hypomagnesemia, metabolic alkalosis)
Phrenic nerve paralysis
1511
elevation (Fraser et al, 1994; Kawashima and Libshitz,
1990; Rabinowitz et al, 1982).
Eventration is a frequently encountered cause of hemi-
diaphragm elevation. The abnormally thin portions of the
diaphragm are more easily stretched and displaced up-
ward by the liver and abdominal viscera (Hesselink et al,
1978; Vogl and Small, 1955). This may be of congenital
etiology due to incomplete muscularization of the peri-
cardioperitoneal membrane (Tarver et al, 1989), but the
increased incidence with age suggests that eventration of
the right hemidiaphragm is often acquired (Okuda et al,
1979). Eventration is usually unilateral and incomplete,
but it may involve the entire hemidiaphragm. The ante-
romedial right hemidiaphragm is most commonly af-
fected by partial eventration (Armstrong et al, 1995; Vogl
and Small, 1955), while complete eventration usually
occurs on the left hemidiaphragm and in males (Tarver
et al, 1989). Partial eventration is seen as a focal, broad-
based, mass-like, upward bulge of the hemidiaphragm
(Fig. 56-16). Complete eventration results in smooth
elevation of the hemidiaphragm on radiographs, with
slight paradoxical, little, or no movement during inspira-
tion on fluoroscopy, which may be indistinguishable from
phrenic nerve paralysis (Armstrong et al, 1995; Tarver et
al, 1989). CT, MR, ultrasound, and liver scintigraphy can
be used to determine the contents of the eventration. If
small, distinction from a localized herniation may be
difficult (Fig. 56-17).
Unilateral hemidiaphragm elevation may be related to
abdominal disease. Large abdominal tumors (Fig. 56-18)
or fluid collections, such as subphrenic abscesses (Fig.
56-19) are potential causes. Hemidiaphragm elevation
may also be associated with dilatation of the stomach
or colon.
Phrenic nerve paralysis, discussed subsequently in
greater detail, is often first suspected when hemidi-
aphragm elevation is noted on a chest radiograph (Fig.
56-20). Impaired inspiratory excursion of the diaphragm
and rib cage due to pain from a rib fracture or pleurisy
("splinting") can also produce hemidiaphragm elevation.
Additional causes of splinting include acute lower lobe
pneumonia or infarction, and acute intra-abdominal in-
flammatory processes such as subphrenic abscess, chole-
cystitis, and peritonitis (Fraser et al, 1994).
Subpulmonic accumulation of pleural fluid can mimic
hemidiaphragm elevation. This is suspected primarily
when the dome of the apparent hemidiaphragm margin
is positioned more laterally than usual (Fig. 56-21)
(Fleischner, 1963; Hessen, 1951; Peterson, 1960). On the
left, the distance .between the gastric air bubble and
the apparent hemidiaphragm margin may be increased
(Armstrong et al, 1995; Fleischner, 1963; Fraser et al,
1994; Hessen, 1951; Peterson, 1960), but this can be
seen in the absence of subpulmonic fluid if the gastric
air bubble is positioned anterior and inferior to the hemi-
diaphragm dome (Felson, 1973). Subpulmonic fluid, if
not loculated, can be confirmed by lateral decubitus ra-
diographs (see Fig. 56-21). A large basilar pleural mass
may also mimic hemidiaphragm elevation.
Phrenoplasty to minimize the pleural dead space fol-
lowing pulmonary resection by dissecting the ipsilateral
hemidiaphragm away from the pericardium and increas-
ing the hemidiaphragm surface area allows the hemidi-
1512 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm

FIGURE 56-16 • Partial eventration. Posteroanterior (A) and lateral (6) radiographs in a 42-year-old man reveal a broad,
upwardly bulging segment {arrows) of the anteromedial right hemidiaphragm.

aphragm to rise higher, resulting in unilateral elevation
(Brewer and Gazzaniga, 1968). This technique minimizes
the size of fluid collections accumulating in the lobec-
tomy space when the remaining lung is too small to fill
the thoracic cavity.
Bilateral Elevation
The most frequently encountered cause of bilateral hemi-
diaphragm elevation (see Table 56-3) is obesity. The
hemidiaphragms of pregnant women are also typically
positioned higher than usual. A large amount of ascites,
diffuse bowel dilatation due to ileus or mechanical ob-
struction, marked hepatosplenomegaly, and intra-abdom-
inal tumors are additional causes of bilateral elevation
(Felson, 1973).
Lung volume loss is the most common intrathoracic
cause of bilateral elevation. Etiologies include bilateral
atelectasis, diseases causing bilateral pulmonary fibrosis,
and bilateral partial lung resection. Lung volume may

FIGURE 56-17 • Multiplanar magnetic resonance image (MRI) of focal diaphragm defect. A, Radiograph in a
patient with breast cancer reveals a rounded "mass" (arrows) in the right lung base, suspicious for a lung nodule. B,
Postcontrast sagittal MRI that the "mass" {arrow) represents a focal bulge of the liver (L). The enhancement and
signal characteristics on this and other pulse sequences were identical to the liver, consistent with a small, focal
eventration or herniation. (From Slone RM, Gierada DS: Pleura, Chest Wall, and Diaphragm. In Lee JKT, Sagel SS,
Stanley RJ, Heiken JP (eds): Computed Body Tomography with MRI Correlation, Vol 1, 3rd ed. Philadelphia,
Lippincott-Raven, 1998.)
 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm 1513

FIGURE 56-18 • Abdominal liposarcoma. Posteroanterior (A) and lateral (fi) radiographs show left hemidiaphragm elevation
and retrocardiac mass. C and D, Computed tomography images reveal that radiographic findings are due to a large tumor (T)
of mixed fat and soft tissue attenuation, which extends through the esophageal hiatus (curved arrow in D). (A, aorta; E,
esophagus; la, left atrium; Ic, left crus of diaphragm; re, right crus of diaphragm.)

also be diminished in the absence of pulmonary disease
due to suboptimal patient inspiratory effort, as it may be
on supine portable radiographs since supine positioning
lowers functional residual capacity (Blair and Hickam,
1955).
Bilateral phrenic nerve paralysis results in bilateral
hemidiaphragm elevation. Bilateral subpulmonic pleural
effusions can simulate bilateral hemidiaphragm elevation.
Numerous neuromuscular, endocrine, and metabolic dis-
eases are rare etiologies of bilateral hemidiaphragm eleva-
tion due to diaphragm weakness or paralysis (Reid, 1995;
Wilcox and Pardy, 1989). Connective tissue diseases such
as polymyositis and systemic lupus erythematosus may
cause diaphragm elevation on the basis of weakness,
while other diseases such as rheumatoid arthritis, sclero-
derma, and ankylosing spondylitis may cause diaphragm
elevation when they result in pulmonary fibrosis (Reid,
1995; Wilcox and Pardy, 1989).
Unilateral Depression
Unilateral hemidiaphragm depression (Table 56-4) is a
relatively infrequent finding. One cause is a tension pneu-
mothorax, in which there may be ipsilateral hemidi-
aphragm depression accompanying contralateral medias-
tinal shift. In supine patients, a pneumothorax of
substantial size may collect anteriorly (preferentially in
the base of the hemithorax, the least dependent position)
 FIGURE 56-19 • Subphrenic abscess. A, A radiograph in a febrile 29-year-
old man demonstrates elevation of the right hemidiaphragm with atelectasis
and focal consolidation in the right lung base. B, A chest radiograph
obtained 3 weeks later reveals an air-fluid level (arrows) in the right
subphrenic space, consistent with an abscess. C, A computed tomography
scan confirms that the abscess (A) is within the abdomen, internal to the
hemidiaphragm (arrows) and adjacent to the liver (L). Consolidation (C) is
present in the medial right lung base. The patient had sustained a liver
laceration in a motor vehicle accident 9 months previously and developed a
biloma that required percutaneous catheter drainage; the drains had been
removed 4 months previously. (From Gierada DS, Slone RM, Fleishman MJ:
Imaging evaluation of the diaphragm. Chest Surg Clin North Am 8:237,
1998.)

FIGURE 56-20 • Paralyzed hemidiaphragm. A, Postoperative chest radiograph obtained after left carotid endarterectomy
demonstrates an elevated left hemidiaphragm. Note the skin staples in left lower neck. S, A radiograph obtained 1 month later
shows no change. Fluoroscopy revealed left hemidiaphragm paralysis.

1514
 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm 1515

FIGURE 56-21 • Subpulmonic pleural effusion. A, Apparent elevation of the right hemidiaphragm with a laterally positioned
dome (arrow) suggests the presence of a subpulmonic pleural effusion. S, Right lateral decubitus view (right side down)
confirms a mobile pleural effusion (e) of moderate size. (Courtesy of Harvey S. Glazer, MD, St. Louis, MO.) (From Gierada DS,
Slone RM, Fleishman MJ: Imaging evaluation of the diaphragm. Chest Surg Clin North Am 8:237, 1998.)

without significant separation of the lateral and apical
visceral p l e u r a l m a r g i n s . H e m i d i a p h r a g m d e p r e s s i o n
therefore can be an indirect sign of a pneumothorax in
the supine patient. Erect or lateral decubitus views with
the abnormal side up can resolve difficult cases.
Asymmetric bullous emphysema can be associated with
relatively greater hemidiaphragm depression on the more
severely affected side (Fig. 56-22). After single lung trans-
plantation for emphysema, the hemidiaphragm on the
transplanted side assumes a more normal position, and
unilateral depression is seen on the side of the native lung.
A large pleural effusion may invert a hemidiaphragm
(Mulvey, 1965; Swingle et al, 1969); in such cases, drain-
age of pleural fluid by thoracentesis may result in little
TABLE 5 6 - 4 • Hemidiaphragm Depression
UNILATERAL
Large pneumothorax
Asymmetric bullous emphysema
Large pleural effusion
Foreign body aspiration
Congenital lobar emphysema
Single lung transplant for emphysema
apparent change in the position of the pleural fluid mar-
gin on radiographs (Felson, 1973). However, detection of
hemidiaphragm inversion on radiography may be difficult
because the normal diaphragm-lung interface is obscured
by the fluid. Hemidiaphragm inversion is more readily
recognized on the left, since depression of the stomach
or colon may be seen (Armstrong et al, 1995). On axial
CT images, p l e u r a l fluid inverting the right hemidi-
aphragm may resemble a cystic intrahepatic mass (Hert-
zanu and Solomon, 1986).
In c h i l d r e n , u n i l a t e r a l h e m i d i a p h r a g m depression
raises the suspicion of congenital lobar emphysema or an
aspirated foreign body. In congenital lobar emphysema,
there is marked hyperinflation of the affected lobe with
depression of the ipsilateral hemidiaphragm and contra-
lateral shift of the mediastinum, and often compressive
atelectasis of the other lobes. Uncommonly, the enlarged
lobe may be completely opacified due to impairment of
fluid drainage by bronchial obstruction. Aspiration of
foreign bodies, particularly in children, is a reported
etiology of obstructive overinflation. However, this effect
may simply be related to air trapping, since full inspira-
tory radiographs can be difficult to obtain in children
(Fraser et al, 1994).

BILATERAL
Bilateral Depression
Chronic obstructive pulmonary disease (emphysema, asthma)
Deep inspiration (young, thin person) Bilateral hemidiaphragm depression (see Table 56-4) is
Bilateral large pneumothorax seen m o s t often w i t h hyperinflation in p a t i e n t s with
Mechanical ventilation at high pressures chronic obstructive pulmonary disease (Fig. 56-23). In
Cystic fibrosis emphysema, the hemidiaphragms are often flat and may
Pulmonary histiocytosis X be inverted; in asthma, they may be slightly less curved
Lymphangioleiomyomatosis
Tuberous sclerosis but are rarely flat (Armstrong et al, 1995). With the
marked hyperinflation sometimes seen in advanced em-
1516 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm

FIGURE 56-22 • Asymmetric bullous emphysema. Severe bullous

emphysema in a 36-year-old man is more severe on the right,
resulting in right hemidiaphragm depression and contralateral
mediastinal shift.

physema, the costal insertions of the diaphragm may be occasionally have a relatively low diaphragm. Mechanical
visible on radiographs (see Fig. 56-23) (Fras'er et al, ventilation at high pressure and bilateral tension pneu-
1994; Slone and Gierada, 1996). Healthy normal individ- mothorax can produce bilateral hemidiaphragm depres-
uals, particularly those who are young and thin, may sion. Finally, cystic fibrosis typically results in hyperin-

FIGURE 56-23 • Severe emphysema. A, A radiograph in a 65-year-old woman with severe emphysema demonstrates
hyperinflation with depression of the hemidiaphragm to below the 11th posterior ribs (11) and flattening of the diaphragm
contour. 6, Close-up view of the right hemidiaphragm reveals its costal insertions {arrows). (From Gierada DS, Slone RM,
Fleishman MJ: Imaging evaluation of the diaphragm. Chest Surg Clin North Am 8:237, 1998.)
 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm 1517

flation, and interstitial lung disease in association with
normal or increased lung volumes can be seen in histio-
cytosis X, lymphangioleiomyomatosis, and tuberous scle-
rosis.
CONGENITAL HERNIAS OF THE
DIAPHRAGM
Bochdalek's Hernia
Bochdalek's hernia results from incomplete closure of
the embryonic pleuroperitoneal membrane. Despite the
name, it typically occurs through posterolateral defects
in the diaphragm separate from the foramen of Bochdalek
(White and Suzuki, 1972). The defect is usually located
laterally, but it also occurs medially and may be small or
large (Fraser et al, 1994). This hernia is seen far more
commonly on the left than right diaphragm, an observa-
tion that has been attributed to earlier closure of the
right pleuroperitoneal membrane (Tarver et al, 1989) and
the protection of right-sided defects by the liver (Fraser
et al, 1994). A small defect may contain only retroperito-
neal fat, while larger defects can contain abdominal vis-
cera such as the stomach, intestine, spleen or kidney on
the left, and the liver on the right (Panicek et al, 1988;
Tarver et al, 1989).
In the neonatal period, a large Bochdalek hernia (con-
genital diaphragmatic hernia) is a surgical emergency
(Kirks and Caron, 1991). Newborns present-with severe
respiratory distress and a scaphoid abdomen. The initial
chest radiograph usually reveals opacification of the he-
mithorax and contralateral shift of the mediastinum due
to herniation of the abdominal contents into the chest
(Fig. 56-24). As air is swallowed, bowel loops in the
chest become filled with gas and produce multiple lucen-
cies. Morbidity and mortality are related to the degree of
underlying pulmonary hypoplasia. Prenatal diagnosis is
possible using fetal ultrasound (Bencerraf and Greene,
1986).
In the adult, a Bochdalek hernia is seen on the chest
radiograph as a soft tissue mass of variable size bulging
upward through the posterior aspect of a hemidiaphragm.
The hernia contents usually can be defined without diffi-
culty on CT, which can also demonstrate the diaphrag-
matic defect (Fig. 56-25). Other radiologic studies can
be used to demonstrate the hernia contents; barium stud-
ies may reveal herniated bowel loops, intravenous urogra-
phy may reveal a herniated kidney, and 99mTc sulfur col-
loid scintigraphy may demonstrate herniation of the liver
or spleen. Small, focal diaphragmatic defects or disconti-
nuity, with or without herniated fat or viscera, are seen
in more than 10% of adults on CT (Fig. 56-26) (Caskey
et al, 1989; Gale, 1985). Their increasing incidence with
age, obesity, and emphysema strongly suggests that the
majority of such abnormalities are acquired, and are not
true Bochdalek hernias (Caskey et al, 1989).
Morgagni's Hernia
Foramen of Morgagni hernias are related to maldevelop-
ment of the embryologic septum transversum with failure
of fusion of the sternal and costal fibrotendinous ele-
ments of the diaphragm (Panicek et al, 1988; Tarver et
al, 1989). In contrast to the true Bochdalek hernia, a
hernia sac of peritoneum and pleura surrounds the con-
tents of a Morgagni hernia (Fraser et al, 1994). Morgagni's
hernia is most often right sided, probably because left-
sided defects are covered by the heart and pericardium,
and it is often associated with obesity. The hernia sac
usually contains omentum, but it may contain transverse
colon or rarely stomach, small bowel, or liver (Tarver
et al, 1989). Most Morgagni's hernias are asymptomatic

FIGURE 56-24 • Congenital diaphragmatic hernia. A, a radiograph obtained in an infant shortly after birth reveals partial
opacification of the left hemithorax; a dilated, air-filled stomach (St); and upper abdominal bowel gas (B). B, Hours later, air has
passed into bowel loops (B) in the left hemithorax, confirming a large congenital hernia. (Courtesy of Marilyn J. Siegel, MD, St.
Louis, MO.) (From Gierada DS, Slone RM, Fleishman MJ: Imaging evaluation of the diaphragm. Chest Surg Clin North Am 8:237,
1998.)
1518 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm

FIGURE 56-25 • Bochdalek and hiatal hernias.

Posteroanterior (A) and lateral (B) radiographs in a 71-
year-old man show a large, left, posterolateral opacity
(long arrows) and a large opacity above the central
portion of the diaphragm (short arrows). Note the
preserved interface of the left lower lobe with the
anterior left hemidiaphragm (open arrows in A). C,
Tomographic image from intravenous urogram reveals
elevation of the enhancing left kidney (LK) into the lower
left hemithorax. The right kidney (RK) is in its normal
location. D and £, Computed tomography images through
the lower chest reveal herniation of the left kidney (LK)
and surrounding fat (f) through the margins (arrows in E)
of a large defect in the left hemidiaphragm, characteristic
of a Bochdalek hernia. A portion of the stomach (St) in
the posterior mediastinum represents the central
supradiahragmatic opacity seen on radiograph, consistent
with a concomitant large hiatal hernia. (A, aorta; H,
heart; L, liver.)
 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm 1519

FIGURE 56-26 • Posterior diaphragm defects. A and B, Computed tomography images in two different patients reveal
herniation of abdominal fat (f) through the margins (arrows) of posterior diaphragm defects, which could be either congenital or
acquired with aging. (A, aorta; L, liver; Sp, spleen; St, stomach.) (B, from Slone RM, Gierada DS: Pleura, Chest Wall, and
Diaphragm. In Lee JKT, Sagel SS, Stanley RJ, Heiken JP [eds]: Computed Body Tomography with MRI Correlation, Vol 1, 3rd ed.
Philadelphia, Lippincott-Raven, 1998.)

although some produce epigastric pressure or discomfort,
and rarely strangulation of contained portions of the
gastrointestinal tract (Fraser et al, 1994).
Morgagni's hernias usually come to clinical attention
as asymptomatic right cardiophrenic angle masses de-
tected on chest radiographs (Fig. 56-27). Gas-filled intes-
tinal loops may be present, facilitating radiographic diag-
nosis. CT permits distinction from other causes of
cardiophrenic angle masses such as pericardial cysts, peri-
cardial fat pads, and pleural or parenchymal masses by
revealing omental fat, omental vessels, and abdominal
viscera peripheral to the diaphragm in the lower anterior
chest (see Fig. 56-27). The actual diaphragmatic defect
may be difficult to identify owing to its typically small
size. As with the Bochdalek hernia, liver scintigraphy or
multiplanar MRI are occasionally useful.
ACQUIRED HERNIAS OF THE DIAPHRAGM
Hiatal Hernia
Hiatal hernia is the most frequently encountered type of
diaphragmatic hernia in adults. Acquired enlargement of
the esophageal hiatus and laxity of the phrenoesophageal
ligament are etiologic factors, often associated with con-
ditions resulting in increased intra-abdominal pressure,

FIGURE 56-27 • Morgagni hernia. A, Posteroanterior radiograph in a 50-year-old man demonstrates a right cardiophrenic
angle mass (M). B, A computed tomography scan through the lower chest reveals transverse colon (C) surrounded by
omental and mesenteric fat in the right lower chest. Mesenteric vessels (arrows) are seen coursing from the right
parasternal region. The diaphragm defect was not depicted. (A, aorta; H, heart.) (B, from Slone RM, Gierada DS: Pleura,
Chest Wall, and Diaphragm. In Lee JKT, Sagel SS Stanley RJ, Heiken JP [eds]: Computed Body Tomography with MRI
Correlation, Vol 1, 3rd ed. Philadelphia, Lippincott-Raven, 1998.)
1520 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm

FIGURE 56-28 • Hiatal hernia. Posteroanterior (A) and lateral (B) radiographs in an 83-year-old man reveal a large,
retrocardiac mass containing an air-fluid level (arrowheads) representing the herniated intrathoracic portion of the
stomach (arrows).

such as obesity and pregnancy (Fraser et al, 1994; Tarver
et al, 1989). Sliding hiatal hernias (Fig. 56-28) are much
more common than the periesophageal variety, in which
the stomach herniates up alongside the lower esophagus.
On chest radiography, hiatal hernias are depicted as
lower posterior mediastinal, retrocardiac soft tissue
masses, often containing air and fluid (see Fig. 56-28).
The diagnosis is easily confirmed by a barium esophago-
gram, although this is rarely necessary. Very large hernias
can become incarcerated or undergo volvulus (Pearson et
al, 1983). Hiatal hernias are frequent incidental findings
on CT scans. Extension of a portion of the proximal
stomach into the lower mediastinum is seen, and an
abnormally wide esophageal hiatus may be identified if it
is appropriately oriented in the transverse plane (Fig.
56-29). When marked ascites is present in a patient with
a hiatal hernia, CT may show fluid extending into the
lower posterior mediastinum mimicing a mediastinal ab-
scess, necrotic tumor, or foregut cyst (Godwin and Mac-
Gregor, 1987).

FIGURE 56-29 • Hiatal hernia. A, A computed tomography scan through the lower chest demonstrates herniation of a portion
of the stomach (St) into the lower mediastinum. B, Image obtained several centimeters caudad demonstrates widening of the
esophageal hiatus (arrows) and herniation of the stomach (St). (A, aorta; H, heart; I, inferior vena cava; L, liver; Sp, spleen.) (A,
from Gierada DS, Slone RM, Fleishman MJ: Imaging evaluation of the diaphragm. Chest Surg Clin North Am 8:237, 1998.)
 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm 1521

Traumatic Hernia omentum, liver, or spleen (Rodriguez-Morales et al, 1986;

Traumatic diaphragmatic hernia can result from either
penetrating or blunt injury. Diaphragmatic rupture is
recognized in 0.5% to 6% of blunt trauma survivors in
various series (Guth et al, 1995; Rodriguez-Morales et al,
1986; Voeller et al, 1990; Ward et al, 1981). It more often
affects the left hemidiaphragm, possibly because of the
protection of the right hemidiaphragm by the liver or
because of the inherently greater weakness of the left
hemidiaphragm; infrequently, bilateral rupture occurs
(Chen and Wilson, 1991; Gelman et al, 1991; Guth et al,
1995; Kearney et al, 1989; Rodriguez-Morales et al, 1986;
Voeller et al, 1990; Ward et al, 1981). Penetrating trauma
due to stab wounds most often affects the left hemidi-
aphragm, since most people are right-handed, while gun-
shot wounds affect both sides with equal frequency
(Chen and Wilson, 1991). Blunt traumatic tears can in-
volve any portion of the diaphragm (Boulanger et al,
1993), although they usually involve the posterior central
aspect of a hemidiaphragm and extend radially, or they
result in disruption of the posterolateral attachments
(Hood, 1971; Ward et al, 1981). Blunt traumatic defects
are usually large, often more than 10 cm in length (Chen
and Wilson, 1991; Panicek et al, 1988; Voeller et al,
1990; Wise et al, 1973). Penetrating wounds are usually
less than 2 cm in length (Wise et al, 1973).
Herniation through a traumatic defect most frequently
involves the stomach on the left and the diver on the
right, but it can also involve the large or small bowel,
Voeller et al, 1990; Ward et al, 1981). In virtually all
cases, traumatic rupture of the diaphragm is associated
with multisystem injuries that more directly determine
survival in the acute setting (Boulanger et al, 1993; Chen
and Wilson, 1991; Guth et al, 1995; Voeller et al, 1990;
Ward et al, 1981), and there are no reliable clinical
signs or symptoms (Rodriguez-Morales et al, 1986). In
addition, conservative management of patients whose ab-
dominal injures can now be followed by CT or ultra-
sound precludes the identification of diaphragmatic tears
that would have been detected during exploratory lapa-
rotomy. The diagnosis of diaphragm rupture therefore
may be overlooked and requires a high degree of suspi-
cion (Desforges et al, 1957; Guth et al, 1995). Early
diagnosis is important since the pleuroperitoneal pressure
gradient can cause defects to enlarge over time (Chen
and Wilson, 1991; Marchand, 1957) with eventual bowel
incarceration, strangulation, and obstruction (Andrus and
Morton, 1970; Boulanger et al, 1993; Desforges et al,
1957; Gourin and Garzon, 1974; Probert and Havard,
1961).
Numerous studies have found the chest radiograph to
be the most valuable test in the preoperative diagnosis of
diaphragmatic rupture. However, the range of reported
sensitivities is wide, from 20% to 71% (Chen and Wilson,
1991; Gelman et al, 1991; Guth et al, 1995; Rodriguez-
Morales et al, 1986; Voeller et al, 1990; Ward et al, 1981).
Herniation of hollow viscera into the chest (Fig. 56-30)
or identification of a nasogastric tube in the intrathoracic

FIGURE 56-30 • Diaphragmatic hernia caused by surgical trauma. A, Portable radiograph obtained immediately following
surgical repair of an abdominal aortic aneurysm reveals a normal position of the diaphragm and a nasogastric tube tip (arrow)
positioned in the proximal stomach (St). B, Portable radiograph 2 days later, after injection of an oral contrast agent through the
nasogastric tube, demonstrates marked upward displacement of a dilated stomach (St). The position of the nasogastric tube tip
(arrowhead) is unchanged, but there is focal narrowing (arrowhead) of the body of the stomach where the stomach has
herniated through the diaphragm into the chest, resulting in gastric obstruction and dilatation of the fundus, (a, gastric antrum.)
(A from Gierada DS, Slone RM, Fleishman MJ: Imaging evaluation of the diaphragm. Chest Surg Clin North Am 8:237, 1998.)
 1522 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm

FIGURE 56-31 • Traumatic diaphragm rupture. A, A radiograph

showing apparent elevation of the right hemidiaphragm in a 28-
year-old man complaining of increasing shortness of breath. B, A
computed tomography scan (CT) at the level of the main
pulmonary artery (PA) reveals the cause—herniation of the liver
(L) into the thorax. C, CT through the upper abdomen
demonstrates the free edge of the torn right hemidiaphragm
(arrow), with herniation of omental fat (f) and colon (C); the
caudal tip of the herniated liver (L) is also seen. The patient
reported involvement in an automobile accident 9 years
previously. (A, aorta; I, inferior vena cava; P, pancreas; PA,
pulmonary artery; Sp, spleen; St, stomach.) (From Slone RM,
Gierada DS: Pleura, Chest Wall, and Diaphragm. In Lee JKT, Sagel
SS, Stanley RJ, Heiken JP [eds]: Computed Body Tomography
with MRI Correlation, Vol -1, 3rd ed. Philadelphia, Lippincott-
Raven, 1998.)

stomach are the most specific radiographic signs. Dia-
phragm rupture should be suspected whenever radio-
graphs reveal apparent elevation of a hemidiaphragm,
although this can be due to atelectasis, eventration, post-
traumatic paralysis, or subpulmonic pleural effusion. Be-
cause nonspecific apparent elevation of the hemidi-
aphragm is usually the only sign of right hemidiaphragm
rupture (Fig. 56-31), right-sided rupture is more difficult
to detect. Evidence of rupture may not be present on the
initial film, but it may develop on subsequent films;
therefore, serial radiographs can be helpful in diagnosis
(Desforges et al, 1957; Rodriguez-Morales et al, 1986;
Voeller et al, 1990). Other plain radiographic findings of
diaphragm injury include hemothorax, basal lung opacity,
or abnormal contour of a hemidiaphragm. Rarely, herni-
ated omental fat can simulate pleural fluid on chest radio-
graphs (Gurney et al, 1985). Radiographic findings are
absent or nonspecific in most penetrating injuries, and
early diagnosis typically requires direct inspection
(Shackleton et al, 1998).
 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm
Diaphragm tears are often documented on CT, with
several findings indicative of traumatic disruption (De-
mos et al, 1989; Heiberg et al, 1980; Holland and Quint,
1991; Worthy et al, 1995). Abrupt discontinuity of the
diaphragm may be visible with or without visceral hernia-
tion (see Fig. 56-31). Inability to identify the diaphragm
(absent diaphragm sign) in an area where it does not
contact another organ and should normally be seen may
be noted. Identification of abdominal structures external
to the diaphragm indicates intrathoracic herniation. Fi-
nally, as on barium studies, focal constriction of the
stomach (collar or hourglass sign) at the site of hernia-
tion occasionally is demonstrated on CT.
Retrospective analyses indicate that most diaphrag-
matic tears are detectable by CT (Murray et al, 1996;
Worthy et al, 1995), but several studies have found CT to
be of limited value in prospectively making the diagnosis
(Chen and Wilson, 1991; Gelman et al, 1991; Voeller et
al, 1990). If hemidiaphragm elevation is only mild and a
defect is not seen on CT, further imaging may be indi-
cated. In problematic cases, direct coronal or sagittal
imaging with MR (Carter et al, 1996; Dosios et al, 1993;
Gelman et al, 1991; Mirvis et al, 1988; Shanmuganathan
et al, 1996), or spiral CT with coronal and sagittal re-
formatting (Fig. 56-32) (Israel et al, 1996), can be defin-
itive. These imaging planes can be of particular value in
depicting the secondary sign of a focal bulge or mush-
rooming in the diaphragmatic contour, particularly on
the right hemidiaphragm where diagnosis can" be difficult.
Other imaging studies are sometimes useful when ra-
1523
diographic or CT examinations are equivocal. Ultrasound
may be of particular value in assessing the right hemidi-
aphragm by depicting the free edge of the hemidiaphragm
as a flap within pleural fluid or demonstrating liver herni-
ated into the chest (Somers et al, 1990). Scintigraphy can
also demonstrate traumatic herniation of the liver or
spleen. Contrast studies of the upper or lower gastroin-
testinal tract may be useful, particularly in delayed pre-
sentation.
PARALYSIS OF THE DIAPHRAGM
Paralysis of the diaphragm can be due to an abnormality
at any point along its neuromuscular axis. It may be
unilateral or bilateral and has numerous potential causes
(Fraser et al, 1994; Ingram, 1987; Reid, 1995; Tarver et
al, 1989). Phrenic nerve trauma related to surgery
(stretch, crush, or transection) (see Fig. 56-20) and inva-
sion by a malignant neoplasm (Fig. 56-33) are the most
common causes, although many cases are idiopathic.
Central nervous system etiologies such as multiple sclero-
sis, Arnold-Chiari malformation, syringomyelia, and high
cervical quadriplegia are associated with bilateral hemidi-
aphragm paralysis. Hypothermic injury of the phenic
nerve related to the use of cold topical cardioplegia dur-
ing coronary artery bypass surgery can lead to unilateral
(usually left) or bilateral hemidiaphragm paralysis. Nu-
merous other causes have been implicated, including
mediastinal masses such as lymphadenopathy aortic an-
eurysm, and substernal goiter, and diabetes, vasculitis,
FIGURE 56-32 • Traumatic diaphragm rupture. A, A
radiograph in a 53-year-old man obtained following a
motor vehicle accident reveals a soft tissue bulge
(arrows) along the left hemidiaphragm. Transaxial
computed tomography (CT) image (B) and sagittal image
reconstructed from the transaxial CT images (Q reveal
herniation of abdominal fat (f) into the chest. The
sagittal image demonstrates a defect (arrows) in the left
hemidiaphragm (small arrows). There was no visceral
herniation. (A, aorta; ant, anterior; H, heart; Sp, spleen.)
(From Gierada DS, Slone RM, Fleishman MJ: Imaging
evaluation of the diaphragm. Chest Surg Clin North Am
8:237, 1998.)
1524 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm

FIGURE 56-33 • Paralyzed hemidiaphragm. Radiograph demonstrates an elevated left hemidiaphragm and a large
left paramediastinal mass (M) representing bronchogenic carcinoma involving the expected location of the phrenic
nerve. Fluoroscopic examination confirmed hemidiaphragm paralysis, consistent with phrenic nerve invasion. (From
Gierada DS, Slone RM, Fleishman MJ: Imaging evaluation of the diaphragm. Chest Surg Clin North Am 8:237, 1998.)

herpes zoster, and birth injury. As noted previously, dia-
phragm weakness without paralysis can be found in nu-
merous conditions, including myopathies, connective tis-
sue diseases, and various endocrine and metabolic
disorders (see Table 56-3).
Fluoroscopy is the simplest, quickest, and most practi-
cal method of assessing diaphragm movement. Dia-
phragm movement can also be assessed by ultrasound,
MRI, and by comparing radiographs obtained in full
inspiration and expiration. In most studies, the average
maximal excursion of the domes of the diaphragm is 3
to 5 cm (range, 2 to 10 cm) (Alexander, 1966; Gierada
et al, 1995; Harris et al, 1983; Simon et al, 1969). Normal
excursion is usually greater than 2.5 cm, but excursion
of less than 3 cm is fairly frequent (Armstrong et al,
1995; Fraser et al, 1994; Simon et al, 1969; Young and
Simon, 1972) and can be seen in healthy persons with a
normal vital capacity (Young and Simon, 1972). Unequal
excursion of the hemidiaphragms is common, generally
differing by less than 1.5 cm, and it may be greater on
either side (Gierada et al, 1995; Young and Simon, 1972).
Asynchronous motion of the hemidiaphragms is not un-
usual (Felson, 1973; Gierada et al, 1995; Juhl, 1987).
Depicting motion by MRI requires scanner hardware
that can produce strong magnetic field gradients to ac-
quire repeated images every 1 second or less in a single
plane during breathing. Relative advantages of MRI in-
clude a large field of view, easily obtained measurements
due to the inherent digital spatial calibration and lack of
image magnification, and the ability to view motion of
segments of the diaphragm in multiple planes rather
than just the highest points of the diaphragm as with
fluoroscopy, which provides a projection view only. Rela-
tive disadvantages include limited temporal resolution
(currently 3 to 5 images per second), restriction to hori-
zontal patient positioning, and greater time and expense.
We have used dynamic MRI to assess diaphragm motion
in patients undergoing lung volume reduction surgery
and have observed improved diaphragm excursion and
better coordination of chest wall and diaphragm move-
ment postoperatively (Fig. 56-34) (Slone and Gierada,
1996). Ultrasound has the advantage of portability so
that it can be performed at the bedside if necessary, but
it has the disadvantages of a limited field of view and
potential difficulty in imaging the left hemidiaphragm
due to gas in the stomach or intestine. These modalities
may be of value in assessing motion when the diaphragm
margin is obscured on fluoroscopy by a pleural effusion
or consolidation.
Fluoroscopy is the most efficient and reliable radiologic
means of assessing for diaphragm paralysis. The examina-
tion is typically performed with the patient erect; however,
supine positioning stresses the diaphragm by removing
the aid of gravity during inspiration and may increase the
sensitivity of the test. In most adults, the fluoroscopic
field of view in the frontal projection is large enough to
view only an entire hemidiaphragm or the medial aspects
of both hemidiaphragms. With oblique or lateral position-
ing, both hemidiaphragms are completely included in the
field of view and can be assessed simultaneously.
In unilateral paralysis, a paralyzed hemidiaphragm
paradoxically moves upward on inspiration and down-
ward on expiration (Fig. 56-35), passively following
changes in intrapleural and intra-abdominal pressure
(Juhl, 1987; Tarver et al, 1989). In bilateral paralysis,
both hemidiaphragms move upward on inspiration, con-
 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm 1525

FIGURE 56-34 • Dynamic magnetic resonance image of diaphragm motion. These sequential right midsagittal images were
obtained during slow, deep breathing in a 56-year-old woman with severe emphysema before (7-5, top row) and 6 months
after (6-70, bottom row) lung volume reduction surgery. Five of the 30 images obtained in each sequence are shown.
Comparison of the end-expiratory images (7 with 6, 5 with 10) and end-inspiratory images (3 with 8) reveals improved
curvature of the diaphragm and increased diaphragm excursion postoperatively. (From Gierada DS, Slone RM, Fleishman MJ:
Imaging evaluation of the diaphragm. Chest Surg Clin North Am 8:237, 1998.)

FIGURE 56-35 • Left hemidiaphragm paralysis following lung volume reduction surgery. Sequence of coronal
magnetic resonance images obtained during slow, deep inspiration (1-4) and expiration (4-6), with stars marking the
end expiratory position of the hemidiaphragm domes, reveals normal, full excursion of the right hemidiaphragm but
slight paradoxical motion of the left hemidiaphragm. Paradoxical movement during a subsequent fluoroscopic sniff
test was also consistent with left hemidiaphragm paralysis. (From Gierada DS, Slone RM, Fleishman MJ: Imaging
evaluation of the diaphragm. Chest Surg Clin North Am 8:237, 1998.)
1526 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm

comitant with inward rather than normal outward move-

ment of the abdominal wall (Higgenbottam et al, 1977).
However, a paralyzed hemidiaphragm may show a slight
descent on slow, deep inspiration due to passive stretch-
ing as the rib cage expands.
The sniff test is therefore necessary to confirm that
abnormal hemidiaphragm excursion is due to paralysis
rather than unilateral weakness. For the stiff test, the
patient inhales rapidly and forcefully through the nose
with the mouth closed. This normally produces a sharp,
brief descent of both hemidiaphragms. Paradoxical up-
ward motion greater than 2 cm of an entire hemidi-
aphragm, as seen in oblique or lateral projection, is con-
sistent with hemidiaphragm paralysis (Alexander, 1966).
Several potential difficulties may limit the fluoroscopic
assessment of diaphragm paralysis. Diaphragm motion
may be diminished due to inflammatory processes such
as pneumonia, pleuritis, pleural effusion, peritonitis, and
subphrenic abscess, so fluoroscopic assessment is best
delayed until such reversible conditions that may affect
the diaphragm have resolved. Complete eventration may
be difficult or impossible to distinguish from diaphragm
paralysis (Fraser et al, 1994), and severe weakness or
fatigue may appear identical to bilateral paralysis on flu-
oroscopy (Tarver et al, 1989). Although some patients
with bilateral paralysis show the typical paradoxical up-
ward motion of both hemidiaphragms during a deep
inspiration or sniff maneuver, normal inspiratory descent
of the diaphragm can be mimicked in those patients who
perform the compensatory maneuver of actively exhaling
below functional residual capacity using their abdominal
muscles, then inhaling by relaxation of the abdominal
muscles, which causes passive descent of the diaphragm
(Kreitzer et al, 1978). This effect can be detected by
carefully observing abdominal motion during breathing
(Malagari and Fraser, 1995), and it is minimized by
performing the examination with the patient in the re-
FIGURE 56-36 • Accessory hemidiaphragm. A, A radiograph
cumbent position, which eliminates the assistance of obtained in a 7-year-old girl demonstrates a small right
gravity and allows the paradoxical or absent motion to hemithorax, a hazy increase in opacity obscuring the right
be detected (Ch'en and Armstrong, 1993). heart border, and a curvilinear band of tissue (arrows)
extending laterally from the right hemidiaphragm. B, A
In some patients with phrenic nerve injury, even computed tomography scan reveals a thin band of tissue {open
though fluoroscopy demonstrates paralysis, the paralysis arrows) coursing through the right lower lobe parenchyma to
may not be permanent. Regeneration of phrenic nerve a posterior rib. Partial anomalous pulmonary venous return to
fibers may lead to partial or complete recovery of dia- the right atrium was evident on other images. The thin tissue
band with these associated finding's is characteristic of a rare
phragm function over time, usually within 1 year based accessory hemidiaphragm; no pathologic proof was obtained.
on the normal rate of peripheral nerve regeneration (Wil- (Courtesy of Marilyn J. Siegel, MD, St. Louis, MO.) (From
cox et al, 1990). The diagnosis of diaphragm paralysis Gierada DS, Slone RM, Fleishman MJ: Imaging evaluation of
can also be difficult in patients with severe hyperinflation the diaphragm. Chest Surg Clin North Am 8:237, 1998.)
due to chronic obstructive pulmonary disease, in whom
the normal hemidiaphragm moves very little; or in weak,
debilitated patients who cannot produce a strong inspira- lent to fluoroscopy in making the diagnosis of diaphragm
tory effort or forceful sniff. Care must be taken not to dysfunction (Diament et al, 1985; Gottesman and
mistake the jerking upward motion of the entire thorax McCool, 1997; Houston et al, 1995). Dynamic MRI of
produced by some patients in their attempt to sniff force- diaphragm movement can reveal abnormal motion due
fully for paradoxical upward diaphragm motion. Defini- to hemidiaphragm paralysis (see Fig. 56-35), but the
tive diagnosis of phrenic nerve paralysis can be obtained accuracy of this technique has not been studied.
using cervical phrenic nerve stimulation with electromyo-
graphic measurement of phrenic nerve latency (Gandevia,
1987; Shochina et al, 1983) or with concomitant fluoro- ACCESSORY DIAPHRAGM
scopic or ultrasound monitoring of the diaphragm to look An accessory, or duplicated, diaphragm is a rare congeni-
for diaphragm contraction (McGauley and Labib, 1984). tal anomaly in which a thin, fibromuscular membrane is
Several studies have reported that the sonographic attached to the diaphragm anteriorly and courses posteri-
assessment of diaphragm motion or thickness is equiva- orly and cephalad to attach to the posterior rib cage
 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm 1527

(Davis and Allen, 1968; Hopkins and Davis, 1988; Wille
et al, 1975). Most reported cases occur on the right side.
The accessory diaphragm may follow a fissure or divide
the lower lobe. There is a frequent association with other
congenital anomalies, particularly pulmonary hypoplasia,
partial anomalous arterial supply or venous drainage,
congenital heart disease (Davis and Allen, 1968; Kena-
noglu and Tuncbilek, 1978), and congenital pulmonary
venolobar ("scimitar") syndrome (Woodring et al, 1994).
The diagnosis is most frequently made during childhood
due to repeated respiratory infections or respiratory dis-
tress, but it may occur incidentally in an asymptomatic
patient.
On frontal radiographs, the affected hemithorax is
usually small due to the accompanying pulmonary hypo-
plasia, and the mediastinal border is indistinct and
blurred by a hazy increase in opacity (Fig. 56-36). The
lateral radiograph reveals a retrosternal band of increased
opacity produced by loose areolar connective tissue filling
the space between the anterior chest wall and the small
lung (Davis and Allen, 1968). The findings closely resem-
ble those of right upper and middle lobe atelectasis or
left upper lobe atelectasis or, alternatively, primary pul-
monary hypoplasia (Currarino and Williams, 1985; Davis
and Allen, 1968; Kenanoglu and Tuncbilek, 1978; Wille
et al, 1975). A thickened, oblique septum may be seen
extending posteriorly and cephalad from the diaphragm
to the posterior chest wall. CT (see Fig. 56-36) or MRI
may be helpful in suggesting the diagnosis -(Becmeur et
al, 1995).
TUMORS OF THE DIAPHRAGM
Primary tumors of the diaphragm are very rare. Benign
tumors are most common, with lipomas (Castillo and
Shirkhoda, 1985) and cystic masses such as bronchogenic
(Gourlay and Aspinall, 1966), mesothelial, and teratoid
(Muller, 1986) cysts reported most frequently (Olaffson
et al, 1971). Most malignant tumors are sarcomas of
fibrous or muscular origin (Olaffson et al, 1971). Numer-
ous other tumors have been reported, including
schwannoma (Koyama et al, 1996), chondroma (Itakura
et al, 1990), pheochromocytoma (Buckley et al, 1995),
and endometriosis (Posniak et al, 1990).
Tumors of the diaphragm large enough for radio-
graphic detection produce a focal bulge or contour abnor-
mality and can resemble a diaphragmatic hernia, eventra-
tion, or a pleural lesion. Since the diaphragm is a thin
structure, the diaphragmatic origin of a mass may be
difficult to confirm as separate from the lung, pleura, or
abdominal viscera, even on CT, MRI, or ultrasound. Small
masses of fat density are occasionally seen on CT within
the diaphragm muscle, which may represent lipomas that
are too small for clinical or radiographic detection, or the
density may be age-associated fat containing diaphrag-
matic defects (Caskey et al, 1989). The CT appearance
of nonlipomatous soft tissue tumors generally is not spe-
cific.
Pleural plaques related to prior asbestos exposure or
prior pleural inflammatory disease may produce calcified
(Fig. 56-37) or noncalcified diaphragmatic masses.
Calcified plaques can be detected on chest radiography,
but CT is more sensitive for detection of both calcified
and noncalcified pleural plaques. Features helpful in dis-
tinguishing asbestos-related diaphragmatic plaques from
pleural metastases, mesothelioma, or the rare primary
diaphragmatic tumor include bilateral occurrence, calci-
fication, sharp margins, and flattened contour.
Thoracic and abdominal tumors may secondarily in-
volve the diaphragm by direct extension. Such tumors
include bronchogenic carcinoma; mesothelioma and
other primary or secondary pleural or chest wall malig-

FIGURE 56-37 • Calcified pleural plaques. Computed tomography scans at (A) and just below (8) the left hemidiaphragm
dome demonstrate irregular calcified plaques (arrows) along the diaphragmatic pleura bilaterally in a 74-year-old man,
characteristic of prior asbestos exposure. Note the small hiatal hernia containing proximal stomach (St). (A, aorta; C, colon;
L, liver; Sp, spleen.) (From Gierada DS, Slone RM, Fleishman MJ: Imaging evaluation of the diaphragm. Chest Surg Clin
North Am 8:237, 1998.)
1528 CHAPTER 56 • The Diaphragm/Imaging of the Diaphragm
nancies; tumors of the stomach, kidney, adrenal gland,
colon, or retroperitoneum; lymphoma; and peritoneal
carcinomatosis (Tarver et al, 1989). However, when tho-
racic or abdominal masses abut the diaphragm without
traversing it on imaging studies, definitive diagnosis of
invasion cannot be made.
CONCLUSION
The diaphragm performs most of the physiologic work
of inspiration and forms an anatomic barrier between
the thoracic and abdominal cavities. Disorders of the
diaphragm can be related to impairment in either of these
functions, with most having radiologic manifestations.
Both intrathoracic and intra-abdominal disease processes
can alter the normal radiologic appearance of the dia-
phragm. Abnormalities are usually first detected on chest
radiographs, often incidentally in asymptomatic patients,
and many require further characterization by other im-
aging studies for definitive diagnosis. CT, MRI, and fluo-
roscopy are the most frequently useful additional studies,
while ultrasound, barium contrast studies, and liver-
spleen scintigraphy are occasionally helpful. Selection of
the most appropriate radiologic examination in a given
clinical situation can facilitate the diagnosis of diaphragm
abnormalities.
COMMENTS AND CONTROVERSIES
Diaphragmatic imaging is a subject that is not frequently
considered in the practice of general thoracic surgery.
Nonetheless, in recent years standard imaging techniques
have been augmented considerably to provide superb im-
aging by CT and MRI. In addition, dynamic MRI enables
real-time imaging of diaphragmatic function and pathol-
ogy. Drs. Gierada and Slone have written a clear and
extremely detailed chapter discussing the issues of dia-
phragmatic imaging. The illustrations clearly depict the
points under discussion.
G.A.P.
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1530 CHAPTER 56 • The Diaphragm/Congenital Diaphragmatic Hernias
I CONGENITAL DIAPHRAGMATIC HERNIAS
Geoffrey M. Graeber
Jacob Davtyan
Joseph I. Miller, Jr.
Congenital diaphragmatic hernias are classified as (1)
posterolateral (Bochdalek), (2) retrosternal anterior
(Morgagni), (3) septum transversum (central), or (4)
esophageal hiatal. The first three are discussed in this
chapter. Hiatal hernias are discussed in Esophageal Sur-
gery, Section IV.
Posterolateral Hiatal Hernia of
Bochdalek
HISTORICAL NOTE
Although Vincent Bochdalek's 1848 description was that
of bowel herniation through a dorsal diaphragmatic split
the lumbocostal triangle, the coagenital posterolateral di-
aphragmatic hernia (CPLDH) carries his name. In 1946,
Cross performed the first successful repair of CPLDH
in a newborn. Bartlett and co-workers (1976) reported
successful application of extracorporeal membrane oxy-
genation (ECMO) in infancy. German and co-workers
(1977) reported the first survivor of ECMO in the treat-
ment of CPLDH.
CPLDH occurs in 1:2000 to 1:5000 live births (Har-
rison and de Lorimier, 1981) and is a result of failure of
the pleuroperitoneal canal to close at the eighth week of
gestation (Gray and Skandalakis, 1972). Of these hernias,
80% occur on the left side. Bilateral hernias are extremely
rare (Levy et al, 1969), and very few of these newborns
survive (Sokal et al, 1990). In only 10% of cases is there
a true hernia sac. The abdominal organs herniate into the
chest through the diaphragmatic defect, compressing and
retarding the growth and development of the ipsilateral
lung. The mediastinum may be shifted to the opposite
side, affecting the contralateral lung as well. The mor-
phology of the diaphragmatic muscle is normal (Dietz
and Pongratz, 1991). The morphologic and biochemical
development of the lungs is retarded in most cases, par-
ticularly on the ipsilateral side (Nakamura et al, 1991).
The susceptibility of these babies to bronchopulmonary
dysplasia during artificial ventilation is probably related
to a defective antioxidant system and defective surfactant
production (Molenaar et al, 1991). Pulmonary hypoplasia
is also evident in pulmonary function studies. Nakayama
and associates (1991) showed restrictive lung defects in
infants who survived neonatal repair of CPLDH, and
Geggel and colleagues (1985) reported decrease of the
cross-sectional area of the pulmonary arterial bed in in-
fants dying after repair of CPLDH. Associated major
anomalies occur in up to 40% of live births (Cunniff
et al, 1990). Thorpe-Beeston (1989) reported prenatal
diagnosis of major abnormalities in 48% of fetuses, in-
cluding chromosomal defects in 31% and major malfor-
mations in 17% Trisomy 18 and trisomy 13 are the most
common chromosomal abnormalities. Cardiac, neural,
and genitourinary anomalies are frequent (Adzick et al,
1989). Malrotation of the bowel is always present.
• HISTORICAL READINGS
Bartlett RH, Gazzaniga AB, Jeffries MR et al: Extracorporeal membrane
oxygenation (ECMO): Cardiopulmonary support in infancy. Trans
Am Soc Artif Intern Organs 22:80, 1976.
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Dietz HG, Pongratz D: Morphology of the diaphragmatic muscle in
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Geggel RL, Murphy JD, Langleben D et al: Congenital diaphragmatic
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German JC, Gazzaniga AB, Amlie R et al: Management of pulmonary
insufficiency in diaphragmatic hernia using extracorporeal circula-
tion with a membrane oxygenator (ECMO). J Pediatr Surg
12:905, 1977.
Gray SW, Skandalakis JE: The diaphragm. In Embryology for Surgeons:
The Embryological Basis for the Treatment of Congenital Defects.
Philadelphia, WB Saunders, 1972 p 359.
Gross RE: Congenital hernia of the diaphragm. Am J Dis Child
71:580, 1946.
Harrison MR, de Lorimier AA: Congenital diaphragmatic hernia. Surg
Clin North Am 61:1023, 1981.
Levy JL Jr, Guyner WA, Louis JE et al: Bilateral congenital diaphrag-
matic hernias through the foramina of Bochdalek. J Pediatr Surg
4:557, 1969.
Molenaar JC, Bos AP, Hazelbrock FWJ, et al: Congenital diaphragmatic
hernia, what defect? J Pediatr Surg 26:248, 1991.
Nakamura Y, Yamamoto 1, Fukuda S et al: Pulmonary acinar develop-
ment in diaphragmatic hernia. Arch Pathol Lab Med 115:372,
1991.
Nakayama DK, Motoyama EK, Mutich RL et al: Pulmonary function in
newborns after repair of congenital diaphragmatic hernia. Pediatr
Pulmonol 11:49, 1991-.
Sokal MM, Yellin PB, Mestel AL et al: Survival after bilateral congenital
diaphragmatic hernia. Clin Pediatr (Phila) 29:677, 1990.
Thorpe-Beeston JG, Gosden CM, Nicolaides KH: Prenatal diagnosis of
congenital diaphragmatic hernia: Associated malformations and
chromosomal defects. Fetal Ther 4:21, 1989.
BASIC SCIENCE
Pathophysiology
The pathophysiology of CPLDH depends on the interplay
of pulmonary hypoplasia and pulmonary hypertension.
 CHAPTER 56
Hypoplastic lungs result in various degrees of hypoxia.
In addition, such lungs have increased sensitivity to the
stimuli increasing pulmonary vascular resistance, namely
hypoxia, acidosis, hypercarbia, and hypothermia (Sho-
chat, 1987). The resulting pulmonary hypertension re-
verses the flow through the patent ductus arteriosus and
opens the f o r a m e n ovale w i t h right-to-left s h u n t i n g .
Thus, the syndrome of persistent fetal circulation (Ger-
sony et al, 1969) is established, resulting in the vicious
circle of hypoxia, acidosis, even higher pulmonary resis-
tance, and increasing right-to-left shunting, which ulti-
mately culminates in the death of these babies.
DIAGNOSIS
The clinical presentation depends on the degree of respi-
ratory compromise, which may vary from severe distress
at birth to delayed presentation in infancy or early child-
hood. The age of the patient at presentation is one of the
determining factors of morbidity and mortality (Reynolds
et al, 1984). The newborn with CPLDH is usually dysp-
neic, tachycardic, and frequently cyanotic with a striking
scaphoid abdomen. The trachea and the heart are shifted
to the contralateral side. Breath sounds are decreased or
absent on the ipsilateral side. Chest radiography may be
diagnostic, with bowel loops in the affected hemithorax
and contralateral mediastinal shift. The gastric tube may
be seen in the chest, and paucity of gas is noted in the
abdomen. On the right the defect may be blocked by the
liver, with less extensive herniation and milder respira-
tory compromise.
The clinical presentation of the infant suffering from
foramen of Bochdalek hernia is dependent on the size of
the defect and the amount of visceral migration that
occurs from the peritoneal cavity to the ipsilateral pleural
space. In small hernias the amount of migration of ab-
dominal viscera into the thoracic cavity is minimal. These
patients do not present until later in infancy or even
childhood. Symptoms range from discomfort to feeding
abnormalities and colicky symptoms with poor progres-
sion of growth. Radiographs of the chest generally define
these hernias because air is located in one of the viscera
that has herniated through the foramen.
Correction of small hernias presenting after the perina-
tal period is generally conducted through an ipsilateral
thoracotomy. The hernia sac, if present, is generally iden-
tified, the abdominal viscera are reduced into the perito-
neal cavity, the sac is excised, and the defect is closed.
Closure is usually performed by horizontal mattress su-
tures placed over pledgets. Occasionally the repair is
reinforced with a running suture line placed superficial
to the horizontal mattress sutures. Prosthetic patch recon-
struction is seldom necessary. In infants and children
presenting in this manner, morbidity and mortality from
the condition and its operative correction are minimal.
The condition can be severe, however, because severe
respiratory distress and even death have been reported
with rapid expansion of abdominal viscera into the chest.
Infants who present with large congenital defects of
the diaphragm usually have respiratory distress very early
in the immediate perinatal period. Auscultation of the
chest at that time reveals bowel sounds in the chest on
• The Diaphragm/Congenital Diaphragmatic Hernias 1531
the side of the hernia. In the usual presentation of an
infant with this type of hernia, the bowel sounds are in
the left chest, and the heart sounds are displaced toward
the right side of the chest. The abdomen is scaphoid
because the viscera are in the chest. Compression of the
ipsilateral lung also causes a severe decrease in or absence
of breath sounds on the ipsilateral side. The mediastinum
is shifted to the contralateral side, and in severe cases the
contralateral lung is also compressed by the shift of
the thoracic viscera secondary to the migration of the
abdominal viscera into the pleural space. Auscultation of
the abdomen demonstrates a relative absence of bowel
sounds, which is consistent with the migration of the
bowels into the left chest. Confirmation of the diagnosis
is usually obtained radiographically If a nasogastric or
orogastric tube has been placed prior to radiography, the
tip of the tube is seen above the diaphragm, particularly
with left-sided hernias. This defines the stomach as being
in the left pleural space. The radiograph also demon-
strates bowels in the affected pleural space (Fig. 56-38).
The infant should not have mask ventilation at this time,
since mask ventilation promotes deposition of air in the
gastrointestinal tract, which causes further distention of
the stomach. The infant should be intubated, an umbili-
cal line should be established, and he or she should be
prepared for immediate surgical correction.
MANAGEMENT
Preoperative Management
The clinical suspicion of CPLDH in a newborn with
respiratory distress mandates endotracheal intubation, as-
sisted ventilation, and orogastric tube decompression of
the gastrointestinal tract to prevent further bowel disten-
tion and worsening of respiratory compromise. These
babies are maintained with an inspired oxygen fraction
(Fio 2 ) of 1.0, peak inspiratory pressure below 30 cmH 2 0,
positive end-expiratory pressure (PEEP) of less than 5
c m H 2 0 , and hyperventilation. High-frequency ventilation
may be used. Preductal and postductal arterial blood
gases are monitored by right radial and umbilical arterial
catheters, respectively. Ideally, postductal arterial oxygen
tension (Pao 2 ) is maintained above 100 mm Hg, arterial
carbon dioxide tension (Paco 2 ) below 30 mm Hg, and
pH above 7.50 to prevent and alleviate pulmonary vaso-
spasm. Sodium bicarbonate and tromethamine (THAM)
may be used to treat acidosis. Venous access and mainte-
nance of systolic blood pressure higher than 50 mm Hg
are basic. Fluids are kept to a minimum. Babies should
be paralyzed with pancuronium and anesthetized with
fentanyl. Fentanyl use is thought to be associated with
decreased frequency and severity of episodes of pulmo-
nary hypertension (Vacanti, 1989; Vacanti et al, 1984) as
well as decreased incidence of pneumothorax, a cata-
strophic complication (Hansen et al, 1984).
Multiple attempts have been made to define the pre-
dictive factors of mortality of patients with CPLDH (Ra-
phaely and Downes 1973; Boix-Ochoa et al, 1974; Boix-
Ochoa et al 1977; Manthei et al, 1983; Mishalany et al,
1979; Ruff et al 1980; Wilson et al, 1991). 1983; Wilson
et al, 1991; Ruff et al, 1980). Admission or preoperative
1532 CHAPTER 56 • The Diaphragm/Congenital Diaphragmatic Hernias

FIGURE 56-38 • A, This radiograph demonstrates typical findings in a newborn infant who has a foramen of
Bochdalek hernia. Note that the abdominal viscera have migrated through the diaphragm and are occupying the left
pleural space. The mediastinal contents, great vessels, and tracheobronchial tree are all shifted to the right. Note that
the cardiac silhouette blends with the compressed pulmonary parenchyma on the right side and that the stomach,
colon, and small bowel are all in the left chest. The child has been intubated and is being prepared for emergency
surgical correction. 6, This postoperative chest radiograph shows that the hernia has been corrected and that a chest
tube is in place in the left pleural space. Note that the left lung does not totally fill the left pleural space. This is
consistent with severe hypoplasia in the lung; the chest tube has been properly placed but does not establish
complete expansion of the lung. The tracheal air column, the cardiac silhouette, the great vessels, and the rest of the
mediastinal structures have returned to their normal position. Note also that the right lung is fully expanded and is
no longer compressed by the displacement of the mediastinal structures.

blood gas values, specifically, a pH higher than 7.2, a Operative Repair

Paco2 below 35 mm Hg, and a Pao2 above 100 mm Hg
are associated with an excellent prognosis. Patients with
a pH below 7.0, Paco2 above 50 mm Hg, and Pao2 below
80 mm Hg fare poorly. Vacanti and co-workers (1984)
termed the infants achieving a postductal Pao2 above 100
mm Hg with standard therapy responders and those who
were unable to achieve a postductal Pao2 of 100 mm Hg
with maximum therapy nonresponders The responders
most often survived without ECMO. Nonresponders had
more severe pulmonary hyperplasia and pulmonary hy-
pertension not responsive to medical and ventilatory in-
terventions; in the past all these babies died without
ECMO (Vacanti, 1989). Bohn (1987) compared preductal
Paco2 levels with ventilatory index (VI). Among those
with a Paco2 of 40 mm Hg and a VI over 1000 there
was 100% survival. Preoperative alveolar-arterial oxygen
difference (PA2 — Pao2) calculated from preductal (right
radial) arterial blood gas is another predictor of out-
come. Survivors have PA2 — PaQ2 below 200 mm Hg;
those with PA2 — PaQ2 above 200 mm Hg rarely survive
(Bohn, 1987).
Traditionally, newborns with CPLDH are taken to the
operating room emergently after expeditious resuscita-
tion. Neck lines should be avoided, preserving the vessels
for possible ECMO. A transabdominal subcostal approach
is preferred by most for left-sided lesions, whereas a
transthoracic approach may be more useful for right-
sided hernias. Herniated organs are returned to the peri-
toneal cavity, and the seldom-present hernia sac is ex-
cised. The lung is inspected, but no attempt should be
made to expand the hypoplastic lung. Extralobar pulmo-
nary sequestration, occasionally present, should be ex-
cised. The edges of the defect are defined. Frequently, a
significant span of the posterior diaphragm can be un-
rolled after incision of the posterior peritoneum.
Most of the defects can be closed primarily with inter-
rupted nonabsorbable sutures. In rare cases of absent
posterior rim, the sutures can be passed around the ribs.
Large defects can be closed with a prosthetic patch. The
left pleural space is drained with a 12 French chest tube,
which should be placed to an underwater seal but never
 CHAPTER 56 • The Diaphragm/Congenital Diaphragmatic Hernias
to suction. A contralateral chest tube is also placed. If
the patient's condition permits, the malrotation should
be corrected. The abdomen is closed by using techniques
developed for closure of abdominal wall defects, and
digital stretching of the anterior wall is performed. If
primary fascial closure is impossible, only the skin can
be closed, leaving ventral hernia to be closed later. Occa-
sionally the "silo" technique has to be used.
Surgical correction of a severe foramen of Bochdalek
hernia presenting in the perinatal period is conducted
through an upper abdominal approach. After the perito-
neal cavity has been opened, the abdominal viscera are
reduced from the pleural cavity. If a peritoneal sac is
present, it is resected following the removal of the ab-
dominal viscera from the defect. A 10 French chest tube
is placed in the pleural cavity to evacuate fluids, to aid
in the re-expansion, and to ensure that no pressure oc-
curs in the affected pleural space. Although the chest
tube in many cases may not completely re-expand the
ipsilateral lung, the equalization of pressure allows return
of the mediastinum to the midline and removes any
pressure on the contralateral lung. Before the defect is
repaired, any extralobar pulmonary sequestration that
may be present should be surgically removed. If the
defect is relatively small, it may be closed by the direct
suture technique as outlined previously. If the defect is
substantial and can only be closed with tension, synthetic
patch reconstruction should be performed. The patch
should be sewn to the margin of the defect" with perma-
nent horizontal mattress sutures. Some surgeons believe
that this suture line should be reinforced with a running,
fine Prolene suture superficial to the original layer of
horizontal mattress sutures. The peritoneal cavity should
then be inspected for obstructing duodenal bands and
malrotation of the midgut, which are often present. These
conditions should be corrected before closure is started.
Closure of the abdomen can sometimes be difficult,
since the abdominal viscera have not matured in the
peritoneal cavity. With return of the abdominal viscera
into the peritoneal cavity, compression of the diaphragm
can occur with a tight abdominal wall closure. Such
compression would impede good excursion of the dia-
phragm and ventilation of the patient. In order to avoid
this serious complication, a ventral epigastric hernia may
be created. In such cases the fascia and musculature are
left open, and only the skin is closed. If sufficient relaxing
incisions cannot be made by mobilizing only the skin
and subcutaneous tissues to close the defect, a surgical
gastroschisis is created. In such cases the peritoneal cav-
ity is not large enough to hold the viscera without caus-
ing serious encroachment on the diaphragm. The surgical
gastroschisis repair is made by using synthetic material
to fashion a pouch along the anterior abdominal wall
that contains a portion of the viscera. The abdominal
viscera are gradually returned to the enlarging peritoneal
cavity by gentle, progressive compression of the pouch
without causing undue embarrassment of respiratory
function.
The management of the chest tube during the opera-
tion and in the immediate postoperative period has been
a source of some controversy. Some surgeons prefer to
leave the chest tube to water seal, whereas others advo-
1533
cate placing a one-way valve in the tube and allowing for
manual pressure equalization. Still others advocate gentle
negative pressure generated through a water seal system
to promote expansion of the lung and relief of pressure
in the chest. In general, the majority feel that water seal
drainage or gentle suction across a water seal drainage is
most beneficial.
Timing of the Operation
As stated earlier, most newborns with CPLDH are oper-
ated on emergently Recently, however, there have been
several reports of comparable or even better results with
delayed repair after various periods of medical stabiliza-
tion (Breaux et al, 1991; Cartlidge et al, 1986; Charlton
et al, 1991; Haugen et al, 1991; Hazelbrock et al, 1988;
Langer et al, 1988). To answer these and many other
questions regarding the proper management of newborns
with CPLDH, a large, multicenter, prospective random-
ized study is necessary.
A recent development in the treatment of CPLDH is
antenatal surgical therapy (Harrison and deLorimier,
1981; Harrison et al, 1990a,b). There is an ongoing de-
bate over the feasibility of this experimental therapy (Sto-
lar, 1990). It imposes a risk to the mother as well as to the
fetus with potentially fatal results for both. The proper
indications for this procedure are yet to be defined (Wen-
strom et al, 1991).
Long-Term Results
Although some respiratory abnormalities can be found in
survivors of CPLDH, they generally have a normal life
and carry on normal physical activity (Frenckner and
Freyschuss, 1988). Most of these studies were performed
in the follow-up of patients operated on in the pre-ECMO
era. As more severely affected babies survive the modern
therapy, their prognosis may be different (Falconer et
al, 1990).
Retrosternal Anterior Diaphragmatic
Hernia (Morgagni)
BASIC SCIENCE
Retrosternal anterior diaphragmatic hernia was described
by Morgagni in 1769. It is much less frequent than
posterolateral hernia, accounting for only 1% to 6% of all
congenital defects of the diaphragm (Cullen et al, 1985).
The herniation occurs between the xiphoid and costo-
chondral attachments of the diaphragm, more frequently
on the right side (Gray and Skandalakis, 1972).
In rare cases, foramen of Morgagni hernias arise in
the potential spaces between the sternum and the costal
muscular portions of the diaphragm. These spaces,
through which the internal thoracic vessels exit the
thorax to become the superior epigastric vessels as they
enter the rectus sheath, exist just lateral to the posterior
table of the sternum. On the left side this potential
space is partially protected by the pericardium. For
this reason herniation through this foramen is more
common on the right side. The visceral peritoneum is
1534 CHAPTER 56 • The Diaphragm/Congenital Diaphragmatic Hernias
FIGURE 56-39 • A and B, These radiographs demonstrate a
loop of colon filled with air that protrudes into a foramen of
Morgagni hernia. The bowel was not strangulated or ob-
structed when the examination was performed. The patient
suffered from fullness and cramping abdominal pain. An ab-
dominal approach was used in correcting the hernia. The child
had an uneventful postoperative course.
usually completely adjacent to both potential spaces.
Hence, a foramen of Morgagni hernia usually has a true
hernia sac when the abdominal viscera protrude into
this space. Any one of the abdominal viscera that has a
mesentery may protrude into either one of these poten-
tial spaces.
The most frequent organs to protrude into a foramen
of Morgagni hernia are the colon, omentum, stomach,
and small bowel. Such hernias infrequently present in
childhood; more commonly this rare entity presents in
the adult with varying symptoms. Obese individuals are
more commonly affected than slender patients, and
women are more commonly affected than men. Many
foramen of Morgagni hernias may be missed because the
radiographic indication of a fat pad to the right of the
pericardium is mistaken for a pericardial fat pad or a
pleuropericardial cyst. Colicky pain is a relatively infre-
quent finding, as is vascular compromise of the organs
herniated into the space. Colonic, gastric, and intestinal
volvulus has been reported, although the volvulus is
seldom total; rather, the volvulus is relenting in nature,
causing the patient to have intermittent symptoms of
partial gastric, colonic, or intestinal obstruction. Com-
plete obstruction of any one of these viscera can occur
but is extremely rare.
DIAGNOSIS
A strong suspicion of the foramen of Morgagni hernia
may be generated by plain posterior, anterior, and lateral
radiographs. An excessively large density in the region of
the fat pad on the pericardium should suggest the diagno-
sis, which can occasionally be confirmed by plain films
alone. Computed tomography (CT), magnetic resonance
imaging (MRI), and ultrasound may confirm the diagno-
sis, depending on what abdominal viscera are in the sac.
Occasionally, upper gastrointestinal or colonic contrast
radiography are necessary to confirm the diagnosis by
identification of the stomach, small bowel, or colon above
the diaphragm in the peristernal position (Fig. 56-39).
Often CT scans or MRI make this diagnosis without
contrast since loops of bowel are found in a demonstrable
hernia sac. If the patient has only omentum in the hernial
sac or the diagnosis is equivocal for any reason, a diag-
nostic pneumoperitoneum may be conducted to outline
the hernia sac. In such cases the hernia sac is outlined
by the air entering the hernia and defining the omentum
or other structures.
MANAGEMENT
Surgical Repair
An abdominal approach for repair of this hernia is indi-
cated in most instances. An upper abdominal incision
based on the patient's body habitus, the size of the hernial
contents, and the extent of the hernia sac allows excellent
visualization. Foramen of Morgagni hernias have been
repaired through subcostal, paramedian, and midline in-
cisions. Once the peritoneal cavity is entered, the abdom-
inal viscera are withdrawn from the hernia sac and re-
duced to their normal anatomic positions. All adhesions
are taken down. The hernia sac is then defined, intro-
duced into the peritoneal cavity, and resected. The repair
of the defect may be effected by several means.
 CHAPTER 56
When the defect is small and the edges are relatively
mobile, horizontal mattress sutures of 0-gauge braided
permanent material may be placed to close the defect.
Some surgeons prefer using polypropylene. In some in-
stances the edges may be oversewn with a running suture
superficial to the horizontal mattress suture to further
secure closure. Under no circumstances should the edges
of the defect be closed under tension because the hernia
has a distinct tendency to recur. Many surgeons prefer to
close the defect with synthetic patch material if the defect
is too large for the edges to come together without ten-
sion. In such cases the prosthetic material is joined to
the edges of the diaphragmatic defect or the chest wall
by permanent synthetic horizontal mattress sutures,
which are tied individually. Some surgeons prefer to over-
sew the suture line with a running polypropylene suture
after the horizontal mattress suture layer has been placed.
Prosthetic materials that have found favor include poly-
tetrafluoroethylene (Teflon) sheeting, woven Dacron, and
various synthetic meshes. Most surgeons now prefer
Teflon sheeting since it has a relatively low adhesion
rate, is pliable, and sutures well to both muscle and the
chest wall.
When the foramen of Morgagni hernia is identified
through a thoracic incision, the principles of repair are
much the same. The hernial sac is entered, the visceral
contents are dissected and reduced into the abdomen,
the sac is resected, and repair is performed. Under no
circumstances should closure be completed under ten-
sion. If horizontal mattress sutures cannot close the de-
fect appropriately, a soft tissue patch, such as Teflon
sheeting, may be used for this purpose. In such instances
horizontal mattress sutures of permanent material are
placed around the edges. Some practitioners prefer using
pledgets on the diaphragmatic surface. Along the chest
wall, the sutures may be placed around a rib or costal
cartilage to secure the closure. Occasionally sutures have
to be placed through the periosteum of the sternum to
effect an adequate repair. The primary suture line may
then be reinforced, if necessary, with a continuous run-
ning suture.
Postoperative Management
Postoperative care is the same as with any other patient
who has had major abdominal surgery. The patient is
kept NPO until bowel sounds return and flatus is passed
per rectum. Judicious intravenous fluid replacement ther-
apy is maintained. Antibiotics are used appropriately if
any one of the abdominal viscera has been opened. If the
hernia has been repaired through a thoracic incision,
chest tubes are placed to maintain the expansion of the
lung. In most cases the patient enjoys a benign postopera-
tive course and should be discharged within 6 to 10 days
after the repair.
Septum Transversum (Central)
Diaphragmatic hernia
BASIC SCIENCE
Septum transversum diaphragmatic hernias are extremely
rare. They are among the midline congenital defects that
• The Diaphragm/Congenital Diaphragmatic Hernias 1535
may also include omphalocele, sternal defect, and pental-
ogy of Cantrell (Cantrell et al, 1958; Milne et al, 1990).
A high incidence of gastrointestinal anomalies, absent
pericardium, and herniation of the heart through the
defect occurs (Lee et al, 1991; Wesselhoeft and DeLuca,
1984).
DIAGNOSIS AND MANAGEMENT
Diagnostic workup may include plain radiographs of the
chest and abdomen, ultrasound, contrast studies of the
gastrointestinal tract, and nuclear scan. A cardiac workup
may be required to delineate the congenital heart defects.
Surgical repair is best done through the abdomen to
enable correction of intra-abdominal pathology. The first
priority is to reduce the herniated organs into their re-
spective cavities and to close the diaphragmatic defect
(Touloukian, 1984). Only then is the omphalocele, if
present, dealt with. Congenital heart defects may require
repair as well.
• KEY REFERENCES
Connors RH, Weber TR, Randolph JG: The diaphragm: Developmental,
traumatic, and neoplastic disorders. In Baue AE, Geha AS, Ham-
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risk infants with congenital diaphragmatic hernia. J Pediatr Surg
19:672, 1984.
Wenstrom KD, Weiner CP, Hanson JW: A five year statewide experience
with congenital diaphragmatic hernia. Am J Obstet Gynecol
165:838, 1991.
Wesselhoeft CW, DeLuca FG: Neonatal septum transversum diaphrag-
matic defects. Am J Surg 147:481, 1984
Wilson JM, Lund DP, Lillehei CW et al: Congenital diaphragmatic
hernia: predictors of severity in the ECMO era. J Pediatr Surg
26:1028, 1991.
 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm
I CONGENITAL EVENTRATION AND
ACQUIRED ELEVATION OF THE
DIAPHRAGM
Eric Frechette
Raymond Cloutier
Jean Deslauriers
Eventration ("e," out of; "venter," the belly) is a condition
in which all or a portion of one hemidiaphragm is perma-
nently elevated yet retains its continuity and normal
attachments to the costal margins. This congenital anom-
aly has a left-sided predominance with a marked decrease
in muscular fibers (Wright et al, 1985). Eventration is
differentiated from a hernia by the unbroken continuity
of the diaphragm in the former. By contrast, diaphrag-
matic paralysis is an acquired condition in which the
diaphragm, even if somewhat atrophic, is still muscular.
Diaphragmatic paralysis is generally related to pathologic
involvement of the phrenic nerve. Although different,
eventration and diaphragmatic paralysis often produce
the same radiographic appearance and lead to the same
physiologic disturbances.
In this chapter, we discuss the etiology, diagnosis,
indications for surgery, techniques of repair, and results
for both of these conditions. We also describe the meth-
ods used for distinguishing eventration from diaphrag-
matic paralysis.
HISTORICAL NOTE
Eventration of the diaphragm was first recognized in
1774 by Jean-Louis Petit in his Oeuvres medicates post-
humes (Petit, 1760) It was in 1829, however, that Beclard
first introduced the term "eventration of the diaphragm"
(cited in Cruveilhier, 1829). About one century later,
Wood (1916) (cited in Thomas, 1970) "expanded further
on eventration and made a plea that one should not
confuse this with diaphragmatic herniation. He further
suggested that surgical plication could be done if symp-
toms were sufficiently disabling and distressing (cited in
Laxdal et al, 1954). The term eventration is still currently
used, although numerous other definitions such as idio-
pathic high-lying diaphragm, relaxatio diaphragmatica,
relaxed diaphragm, insufficiency of the diaphragm, and
neurogenic muscular aplasia (Bovornkitti et al, 1960)
have been mentioned over the years. Clopton (1923) and
Beck (1950) speculated that eventration is a congenital
anomaly that is likely the result of a failure of musculari-
zation of the diaphragm.
Before the use of radiography, the diagnosis of eventra-
tion of the diaphragm was difficult to make, and Korns
in 1921 was able to collect only 65 cases in the world
literature. In 1935, only 183 cases had been published
(Reed and Borden, 1935). In 1951, a report by Nylander
1537
and Elfving identified localized eventration that was
sometimes encountered on mass chest surveys. Bilateral
eventration in infants and children has since been re-
ported by Avnet (1962) and Lindstrom and Allen (1966).
In 1923, Morrison performed the first successful repair
of an eventration, and he described the surgical principles
that are still used today. He plicated the diaphragm of
a 10-year-old girl with immediate relief of symptoms
(Morrison, 1923a). In infants, there were only 11 cases
of eventration described prior to the first successful repair
made by Bisgard (1947) in a 6-week-old male. In addition
to giving a good description of the technique, he provided
the presently accepted definition of eventration as an
abnormally high or elevated position of one leaf of the
intact diaphragm (cited in Thomas, 1970).
Eventration of the diaphragm still remains a rare con-
dition for which surgery is seldom indicated. In a 1954
review article by Arnheim, 300 surgical cases had been
reported, but only a few patients were operated on (Lax-
dal et al, 1954). The value of plication was even ques-
tioned by Svanberg (1956), who doubted whether any
functional benefit would result from fixing the diaphragm
in a lower position.
• HISTORICAL READINGS
Arnheim EE: Congenital eventration of the diaphragm in infancy. Sur-
gery 35:809, 1954.
Avnet NL: Roentgenologic features of congenital bilateral anterior dia-
phragmatic eventration. Am J Roentgenol 88:743, 1962.
Beck WC: Etiologic significance of eventration of the diaphragm. Arch
Surg 60:1154, 1950.
Bisgard JD: Congenital eventration of the diaphragm. J Thorac Surg
16:484, 1947.
Bovornkitti S, Kangsadal P, Sangvichien S, Chatikavanij K: Neurogenic
muscular aplasia (eventration) of the diaphragm. Am Rev Respir
Dis 82:876, 1960.
Clopton MB: Eventration of the diaphragm. Ann Surg 78:154, 1923.
Cruveilhier J: Atlas d'anatomiepathologique, Vol 1, Book 17, Plate V
Paris, Bailliere, 1829, p 2.
Korns HM: The diagnosis of eventration of the diaphragm. Arch Intern
Med 28:192, 1921.
Laxdal OE, McDougall H, Mellin GW: Congenital eventration of the
diaphragm. New Engl J Med 250:401, 1954.
Lindstrom CH, Allen RP: Bilateral congenital eventration of the dia-
phragm. Am J Roentgenol 97:216, 1966.
Morrison JMW: Elevation of one diaphragm, unilateral phrenic paraly-
sis: A radiological study with special reference to differential diag-
nosis. Arch Radiol Electrother 27:353, 1923a.
Nylander PEA, Elfving G: Partial eventration of the diaphragm. Ann
Chir et Gynec Fenniae 40:1, 1951.
1538 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm
Petit JL: Traite des maladies chirurgicales et des operations qui leur
conviennent: Ouvrage posthume de J. L. Petit Vol 2 (revised ed).
Paris, Meguignon, 1760, p. 233.
Reed JA, Borden DL: Eventration of the diaphragm. Arch Surg 31:30,
1935.
Svanberg L: Clinical value of analysis lung function in some intratho-
racic diseases: Spirometric, bronchospirometric and angiopneumo-
graphic investigation. Acta Chir Scand 111:1196, 1956.
Thomas TV: Congenital eventration of the diaphragm. Ann Thorac Surg
10:180, 1970.
Wood HG: Eventration of the diaphragm. Surg Gynecol Obstet
23:344, 1916.
BASIC SCIENCE
Terminology: Eventration and Paralysis
of the Diaphragm
According to most authors (Chin and Lynn, 1956; Simo-
neau et al, 1983; Wright et al, 1985), true eventrations
are always derived from a congenital defect in the muscu-
lature of one portion or the entire central part of the
diaphragm. It results from an incomplete migration of
myoblasts from the cervical somites into the pleuroperi-
toneal membrane during the fourth week of embryologic
development (Moore, 1988). McNamara and colleagues
(1968a) even suggested that the anomaly involved a de-
fect similar to that observed in a Bochdalek hernia, but
it occurred at a slightly later stage. According to Thomas
(1970), a premature return of the viscera to the abdomi-
nal cavity after their rotation and the absence of ingrowth
striated muscles to the pleuroperitoneal membrane from
the septum transversum may be factors involved in the
development of eventration. Based on this theory, the
premature return of the viscera to the peritoneal cavity
might prevent complete development of the diaphragm
FIGURE 56-40 • A, Standard posteroanterior chest radiograph showing an asymptomatic congenital eventration of
the right hemidiaphragm diagnosed in an adult moderate right diaphragm eventration. B, Lateral view showing the
incomplete anterior nature of the eventration.
TABLE 5 6 - 5 • Anatomic Classification of Eventration
Total Bilateral
Partial (localized) Partial
Anterior Complete
Posterolateral
Medial
From Thomas TV: Non-paralytic eventration of the diaphragm. J
Thorac Cardiovasc Surg 55:586, 1968.
by stretching it out. This concept is further supported by
the observation that both eventration and Bochdalek's
hernia occur more frequently on the left side, most often
in males, and generally have an intact anterior muscular
rim (Kirklin and Hodgson, 1947; McNamara et al, 1968a,
b; Reed and Borden, 1935).
Macroscopically the eventrated diaphragm is thin with
a membranous appearance, whereas the more peripheral
portion is still muscular with normal attachments of the
muscle to the sternum, lower ribs, and dorsolumbar
spine. Indeed, Wright and associates (1985) pointed out
that there is little difficulty at thoracotomoy in distin-
guishing eventration with its membranous appearance
from diaphragmatic paralysis, in which the diaphragm,
even if somewhat atrophic, is still partly muscular.
Histologically, the attenuated portion of the eventrated
diaphragm is composed of fibroelastic tissue (Shah-Mir-
any et al, 1968) with muscle fibers and nerve bundles
seldom seen and no evidence of degeneration of the
phrenic nerve. Based on their location, eventrations can
be further divided into three types (Thomas, 1968, 1970)
Table 56-5): (1) anterior (Fig. 56-40), (2) posterolateral,
and (3) medial. Bilateral eventrations are mostly seen
 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm 1539

TABLE 5 6 - 6 • Acquired Elevation of the Diaphragm

Intact phrenic nerve

Mechanical factors or blunt trauma
Idiopathic
Abnormal phrenic nerve
Post-traumatic or postoperative
Sequelae of neuromuscular or infectious disorders
Malignancies of lung or mediastinum
Idiopathic

within the context of polymalformations (Elberg et al,

1989).
In a carefully analyzed review, Revillon and Fekete
(1982) showed that cases of true eventrations could oc-
cur in any location over the dome of the diaphragm, such
as underneath the heart (6 patients), partially central (15
patients), partially peripheral (13 patients), and complete
(6 patients). These authors also showed that microscopi-
cally the abnormal area always contained some muscular
fibers, although these were fewer in number and dis-
persed in every direction. Often, muscular fibers were
replaced by fibrous tissue rich in collagen and leucocytic
infiltrate.
Occasionally, eventrations have been reported to be
associated with other developmental defects such as hy-
poplastic aorta, cleft palate, transposition of the abdomi-
nal organs, or undecended testicle. In Smith and co-
workers' series (1986) of 10 infants with congenital
eventrations, 7 had significant associated problems, in-
cluding congenital heart disease in 4. Eventration of the
diaphragm can also be associated with prenatal cytomega-
lovirus infections and maternal exposure to drugs such as
thiopental (Becroft, 1979; Elberg et al, 1989). In complete
eventration, the ipsilateral lung is nearly always hypo-
plastic, similar to what is seen with diaphragmatic hernias
(Fig. 56-41).
At birth, breech deliveries or difficult and prolonged
forceps deliveries can result in phrenic nerve injuries,
often associated with vocal cord paralysis or brachial
plexus injuries (Cavrot and Richard, 1956). These inju-
ries are usually the result of a pull on the C3-C5 nerve
root, but in severe cases, they may be produced by an
actual tearing off of these nerve roots (Stauffer and Rick-
ham, 1972). If there are no associated injuries, these
lesions can be difficult to differentiate from congenital
eventration.
Acquired elevation of the diaphragm (often inappro-
priately termed eventration) can be associated with an
FIGURE 56-41 • Standard posteroanterior chest radiograph
of a 10-month-old child with complete eventration of the right
hemidiaphragm.
intact or an abnormal phrenic nerve (Fig. 56-42, Table
56-6). In both cases, loss of contractility progressively
leads to muscular atrophy and distention of the dome.
Ultimately, the physiologic disturbances associated with
eventration and acquired elevation of the diaphragm are
similar. Table 56-7 outlines the main differences between
the two conditions.
Physiologic Consequences of an Elevated
Diaphragm
The most significant physiologic derangements associated
with a high hemidiaphragm relate to the respiratory sys-
tem because the diaphragm contributes to a large propor-
tion of the tidal volume in normal individuals (Agostini
and Sant'Ambrogio, 1970; Clague and Hall, 1979). Con-
sequently, several authors have been able to document a
restrictive pattern characterized by a reduction in lung
volumes and mild hypoxemia, all changes made worse
when measurements are obtained with the patient in a
supine position (Graham et al, 1990). In the group of
patients reported by Wright and colleagues (1985), there
was moderate hypoxia, and the total lung capacity (TLC),
vital capacity (VC), and expiratory reserve volume were

TABLE 5 6 - 7 • Differences Between True Congenital Eventration and Acquired Elevation of the Diaphragm

Feature Eventration Paralysis

Incidence Rare Common

Etiology Congenital anomaly in formation of the diaphragm Acquired lesion
Associated congenital anomalies Yes No
Phrenic nerve Intact Often abnormal
Appearance of the diaphragm Marked decrease in muscular fibers Atrophic but still muscular
Membranous appearance
Sniff test Decreased motion but not paradoxical Paradoxical motion
1540 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm

FIGURE 56-42 • A, Standard posteroanterior chest radiograph of a 55-year-old woman with an idiopathic elevation
(often called eventration) of the left diaphragm. At fluoroscopy, the diagram moves very little but there was no
paradoxical motion. No cause could be found to explain the anomaly. Spirometric studies showed a restrictive
pattern with a vital capacity of 72% of predicted. 6, Standard chest radiograph taken 4 years before A and
considered normal.

lower than predicted with the patients seated, falling
further away from predicted values with the patients in
the supine position. Obviously, this restrictive pattern is
more severe in cases of paralysis and complete eventra-
tion, while it can be nonexistent in cases of partial or
mild eventrations. Thus some patients with diaphrag-
matic elevation have few or no respiratory symptoms,
whereas others may present with shortness of breath,
poor exercise tolerance, orthopnea, or even frank respira-
tory failure if the patient has an underlying lung disease.
In addition to this restrictive defect, many authors (Eas-
ton et al, 1983; McCredie et al, 1962; Ridyard and Stew-
art, 1976) have shown various degrees of compressive
atelectasis with decreased ventilation and perfusion in
the involved lung base.
In 1979, Clague and Hall studied the effect of posture
on lung volume, airway closure, and gas exchange in
eight patients with diaphragmatic paralysis. They showed
that the mean VC in the sitting position was 81% of the
predicted normal value; in the supine position it fell by
a further 19% in right-sided paralysis and 10% in left-
sided paralysis. The mean Po2 was also less than pre-
dicted in the sitting position and fell significantly on
lying. All of these findings were attributed to the inability
of the paralyzed hemidiaphragm to resist movements of
the abdominal contents into the chest on lying down,
when gravitational forces must be overcome.
One other important respiratory consequence com-
monly seen in newborns with an abnormal diaphragm is
the phenomenon of paradoxical respiration, in which the
normal lung is compressed by the mediastinum during
forceful or even quiet inspiration. Thus, there is paradoxi-
cal deflation of the lung on the involved side during
inspiration and paradoxical inflation during expiration
resulting in rebreathing of dead space air (Rodgers and
McGahren, 1989). This paradoxical respiration is ex-
plained by the negative intrapleural pressure created by
the normal diaphragm that is not counterbalanced by the
paralyzed diaphragm on the affected side. Because of
weak intercostals, soft thoracic cage, and very mobile
mediastinum, this phenomenon is often worse in new-
borns than in children or adults. Indeed, paradoxical
respiration is often aggravated by the increased abdomi-
nal pressure associated with the supine position of new-
borns and by the small caliber of their bronchial tree
(Arnheim, 1954; Ribet and Linder, 1992; Stone et al,
1987), which results in higher airway resistance and
greater tendency toward airway obstruction caused by
secretions. Coexisting cardiac or pulmonary malforma-
tions may further aggravate the situation. In a series of
nine patients with eventration seen during the first 19
months of life reported by Paris and associates (1973),
severe respiratory symptoms were present in five of nine
patients. In Jarry et al's series (1982), four of seven
patients required assisted ventilation prior to correc-
tional surgery.
Elevation of the diaphragm can also be the cause of
digestive symptoms related to the rotation of the gastric
fundus underneath the diaphragm, or even to complete
volvulus of the stomach with outlet obstruction. Ac-
cording to Laxdal and others (1954), the stomach may
lie in any one of the following positions, all of which are
 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm
the result of its being drawn up into the chest: (1) normal
position, except that the fundus rises unusually high
under the diaphragm (Buckstein, 1948); (2) inversion
with the greater curvature lying adjacent to the undersur-
faces of the diaphragm (Fichardt, 1946; Malenchini and
Roca, 1946); and (3) inversion with partial or complete
volvulus (Ferriere, 1948).
CONGENITAL EVENTRATION OF THE
DIAPHRAGM
The true incidence of eventration of the diaphragm is
unknown, but Chin and Lynn (1956) reported that the
Southampton and Portsmouth mass radiography units
had diagnosed only 32 cases of elevation of the dia-
phragm in 412,000 subjects during a 5-year period
(1949-1954) for an incidence of approximately 1:1400.
In that series, it occurred nine times more often on the
left side than on the right side. In another series reported
by Christensen (1959), 38 cases out of 107,778 persons
examined were found, for a frequency four times greater
than in the Chin and Lynn report. In neonates and young
children, the true incidence of eventration is even harder
to pinpoint. In a review of 2500 chest radiographs of
neonates, Beck and Motsay (1952) found some diaphrag-
matic weakness in 4% of 2500 chest radiographs in new-
borns, but only 3 patients had severe symptoms, indicat-
ing that the incidence may have been overestimated. In
another study, Kinser and Cook (1944) 'identified an
abnormally elevated diaphragm in 31 of 412,149 radio-
graphs.
Overall, males are affected more often than females,
and the left hemidiaphragm is involved more frequently
than the right (Chin and Lynn, 1956; Wayne et al, 1974).
Clinical Presentation and Diagnosis
As many infants with unilateral eventration have few or
no symptoms, especially if the defect is focal, congenital
eventration is often undiagnosed until later in life when
weight gain and reduction of cardiopulmonary reserve
may generate pulmonary symptoms.
When eventration is symptomatic, the spectrum of
clinical presentation ranges from mild respiratory insuf-
ficiency to cyanosis, or even respiratory failure necessitat-
ing intubation (Kizilcan et al, 1993; Mclntyre et al, 1994;
Sarihan et al, 1996). Most often, however, difficulty in
feeding, repeated attacks of pneumonitis, and dyspnea are
the prominent symptoms. The symptoms of congenital
eventration can also develop very insidiously with inter-
mittent vomiting, necessitating small feedings given in
an upright position. Interestingly, the clinical course of
eventration in children does not always correlate with
the severity of involvement, as sometimes patients are
asymptomatic with large or complete eventrations.
According to Michelson (1961), one of the most valu-
able signs of eventration is the Hoover sign (Hoover,
1920), or accentuated outward excursion of the costal
margin from the midline on inspiration owing to failure
of the diaphragmatic action to oppose that of the inter-
costals. Diminished breath sounds, contralateral tracheal
shift, and depression of the abdomen of the involved side
1541
are other clinical signs that may be found on physical
examination (Huault et al, 1982; Rodgers and McGabren,
1989). In such cases, it is also important to look for
signs of birth trauma that could indicate diaphragmatic
paralysis rather than eventration.
The diagnosis of congenital eventration is usually sug-
gested on chest radiographs (see Fig. 56-41), and the
classic appearance is that of an elevated hemidiaphragm
often associated with loss of volume of the ipsilateral
lung and displacement of the mediastinum toward the
contralateral side. The lateral film is useful to determine
the degree of involvement as well as the type of eventra-
tion. On fluoroscopy, complete eventration results in
smooth elevation of the hemidiaphragm with little or
slightly paradoxical movement during inspiration, often
indistinguishable from phrenic nerve paralysis (Gierada
et al, 1998). In an attempt to clearly outline diaphrag-
matic contours and rule out possible diaphragmatic her-
nia, some authors (Avnet, 1962; Buchwald, 1965; Zeitlin,
1930) have described the use of peritoneography and
pneumoperitoneography, but these have now been re-
placed by the less invasive techniques of ultrasound and
computed tomography (CT) scanning. Ultrasound is par-
ticularly useful because it can be carried out at bedside
in neonatal units and can be used to assess diaphragmatic
motion and thickness as well as detect cysts or masses
that may on occasion mimic diaphragmatic elevation
(Othersen and Lorenzo, 1977). Prenatal ultrasound has
also been described as an aid to the diagnosis of eventra-
tion (Rodgers and McGahren, 1989). Occasionally, CT,
magnetic resonance imaging (MRI), liver isotope scan,
and gastrointestinal studies are useful to determine the
contents of the eventration.
Management
In all cases of newborns or infants with severe respiratory
difficulties, initial treatment must aim at supporting oxy-
genation and achieving gastric decompression. In severe
cases, the child may have to be intubated and placed on
a mechanical ventilator. Once the patient is stabilized,
the diagnosis is confirmed and surgical plication, often a
life-saving procedure, is carried out in a timely fashion.
Before proceeding with operation, it is particularly im-
portant to ensure that the respiratory symptoms are due
to the eventration and not to associated cardiac malfor-
mations or pulmonary anomalies.
If the eventration is only partial, if the child is asymp-
tomatic, or if he or she responds well to conservative
management, most surgeons agree that operation can be
delayed or even totally avoided. This approach is some-
what controversial in the pediatric literature because
some investigators recommend to proceed with early sur-
gery even in mildly symptomatic patients in order to
maximize development of the underlying lung (Gaultier,
1976; Revillon and Fekete, 1982) (Fig. 56-43). This is
especially true if the eventration limits expansion of the
thoracic cage or is the cause of repeated pulmonary
infections.
The operation is usually carried out through a postero-
lateral thoracotomy, and simple plication is recommended
because it is faster, can be done with minimal blood loss,
1542 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm
FIGURE 56-43 • Preoperative (A) and postoperative (S) chest radiograph of a child with incomplete
eventration of the right hemidiaphragm. Surgical plication was carried out to maximize development of the
underlying lung.
and involves no entry into the peritoneal cavity where
the spleen, liver, or other digestive organs can be injured
(Table 56-8) (Jewett and Thomson, 1964; Paris et al,
1973; Schwartz and Filler, 1978; Stone et al, 1987). To
plicate the diaphragm, most surgeons use the technique
(or modifications of the technique) described by
Schwartz and Filler (1978) in which the slack of the
diaphragm is pulled in a radial direction, and pleats
are created by the placement of full-thickness horizontal
mattress nonabsorbable sutures or staples (Maxson et al,
1993) in the anteromedial to posteromedial direction,
while avoiding injury to branches of the phrenic nerve.
This type of plication gives the diaphragm an "accordion"
appearance. In this manner, the diaphragm can be pli-
cated with as many rows of sutures as necessary for it to
become taut. During this type of plication, one should
aim at replacing the diaphragm one or two intercostal
spaces below where it should ultimately be located. Gra-
ham (1990) and co-workers also suggested buttressing
the final layers of suture with polytetra fluroethylene
(Leflon) pledgets in order to prevent tearing out of su-
TABLE 5 6 - 8 • Surgical Techniques for Repair of
Congenital Eventration
Advantages
Plication
Easier and faster operation
Minimal blood loss
No entry in peritoneal cavity
Excision and plication
Possible reapproximation of normal muscle with
recovery of functions
Avoids inadvertent injury to abdominal organs
tures. Central diaphragmatic pleating with two circular
purse-string sutures, and circumferential pleating directly
on the thoracic wall, have also been described, but they
are used less frequently (Affatato et al, 1988; Shoemaker
et al, 1981).
The alternative technique of plication (Bishop and
Koop, 1958; Thomas, 1970) is to open and resect the
excess aponeurotic portion of the diaphragm, followed
by a two-layer overlapping approximation of normal pe-
ripheral muscle while avoiding inadvertent injury to un-
derlying abdominal viscera. With this technique, it is
possible to anticipate a better functional recovery of the
diaphragm, although it is associated with increased blood
loss, phrenic nerve injury, and diaphragmatic dehiscence
(Revillon and Fekete, 1982).
As part of the plication procedure, the diaphragm can
be sutured anteriorly to the ribs (State, 1949; Stauffer
and Rickham, 1972) and posteriorly to the crurae. If the
medial component of the diaphragm is lacking, it is
recommended to use the diaphragmatic portion of the
pericardium or other autologous tissue or meshes for
reinforcement (Thomas, 1968, 1970). If the abdominal
cavity is not large enough to accommodate the return of
intrathoracic organs, the creation of a temporary ventral
hernia may be necessary (Thomas, 1970).
Patients who have bilateral eventration or those with
infracardiac involvement are best managed through an
abdominal approach. In such cases, an upper transverse
incision with liver mobilization allows the surgeon access
to both right and left hemidiaphragms. The abdominal
approach also allows for the creation of a transverse
abdominal muscle flap that can be used to reinforce the
repair (Rogers and McGahren, 1989). If a gastric volvulus
is present, a gastrostomy with gastropexy may be neces-
sary.
 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm
TAB LE 5 6 - 9 • Results of Plication for Congenital Eventration of the Diaphragm in the Pediatric Population
No. of Operative
Author Patients Mortality
Stauffer and Rickham, 1972 8 0%
Revillon and Fekete, 1982 28 4%
Stone et al, 1987 11 36% (4/11)
Kizilcan et al, 1993 25 0%
Total 83 6% (5/83)
Results
The results of surgical plication for congenital eventration
of the diaphragm are shown in Table 5 6 - 9 . In one series
(Kizilcan et al, 1993), assessment of long-term function
of plicated diaphragms was done by fluoroscopic, ultra-
sound, and spirometric studies. The absence of paradoxi-
cal motion with normal localization of the diaphragm
was documented in all patients, while satisfactory motion
of the diaphragm was also documented by fluoroscopy in
9 of 12 patients. Additionally, normal pulmonary function
test values were obtained in five of six patients of suitable
age for spirometric assessment. In another study (Revil-
lon and Fekete, 1982), good anatomic results as seen on
chest radiographs were obtained in 25 of 27 children
who had plication of the diaphragm while not in respira-
tory failure.
Several authors have noted that most ventilator-depen-
dent patients can be extubated within 1 week of plication
Revillon and Fekete, 1982; Smith et al, 1986; Symbas et
al, 1977).
In general, the surgical correction of bilateral eventra-
tion is associated with a higher operative mortality be-
cause of associated malformations and more severe hypo-
plasia of the lung (Watanabe et al, 1987).
ACQUIRED ELEVATION OF THE
DIAPHRAGM
Etiology
In the adult, diaphragmatic elevation is often found on
r o u t i n e chest r a d i o g r a p h s d o n e in a s y m p t o m a t i c or
mildly symptomatic patients. In some of these patients,
the diagnosis is clearly that of a congenital eventration
(true eventration) that had gone unnoticed during child-
hood only to become symptomatic with decreased pul-
monary function caused by obesity, chronic obstructive
lung disease, or any other pulmonary disorder. In most
other adult patients with an elevated diaphragm, the
disorder is acquired and it can be associated with an
intact or an abnormal phrenic nerve (see Table 5 6 - 6 ) .
Often the cause of diaphragmatic elevation is difficult to
determine and in Donzeau-Gouge and associates series
(1982) of 20 patients, no clear etiology for the elevation
of the diaphragm could be found even after full surgical
exploration. In those cases, diaphragmatic elevation may
be the early manifestation of a malignant disease or a
disabling neuromuscular disorder. In 1982, Piehler and
others reported an interesting study of 247 patients who
1543
Improvement
Length of
Follow-up Clinical Radiographic Functional
Up to 11 yr 100% 100%
Unknown — 95% —
1-7 yr — 100% —
1.5-11 yr 92% 75% 5/6
97% 91% 83%
were seen at the Mayo Clinic between 1960 and 1980. In
142 of 247 patients, initial evaluation failed to suggest a
cause for the elevated hemidiaphragm. In this cohort, a
cause for diaphragmatic paralysis was found in only six
patients (five tumors, one neurogenic) during follow-up
ranging from 5 months to 20 years. The authors con-
cluded that patients with unexplained diaphragmatic ele-
vation are unlikely to have an underlying occult malig-
nant process, but that recovery of diaphragmatic function
is also unlikely.
Most cases of diaphragmatic elevation with an intact
phrenic nerve are related to mechanical factors, such as
seen with loss of volume of the thoracic cage and in-
creased intrapleural negative pressure. Indeed, most of
these situations are associated with normal diaphragmatic
function or temporary paralysis with full recovery ex-
pected. W h e n pneumonectomy has been carried out, the
diaphragm is always elevated, but it seldom produces
symptoms requiring specific therapy (Fig. 56-44). An
abnormally thin and elevated diaphragm with a macro-
scopic aspect of eventration has been described following
blunt trauma (Holgersen and Schnaufer, 1973).
Diaphragmatic elevation related to involvement of the
phrenic nerve can be classified as post-traumatic, second-
ary to neuromuscular or infectious diseases, neoplastic,
or idiopathic (Table 56-10). Injuries to the phrenic nerve
can occur after any type of operation in the thorax or in
the neck, but they are more commonly reported after the
correction of congenital cardiovascular anomalies (Mok
et al, 1991) resulting from the use of electrocautery
(Allen et al, 1979) or following dissection (Affatato et al,
1988) near the zone where the phrenic nerve runs. In a
large series of children undergoing operation for congeni-
tal heart disease, Mickell and collaborators (1978) found
the incidence of postoperative symptomatic diaphrag-
matic paralysis to be 1.7%. In the adult patient undergo-
ing open heart surgery, the use of ice or slush topical
hypothermia is associated with a higher rate of diaphrag-
TABLE 5 6 - 1 0 • Causes of Phrenic Nerve Paralysis
Traumatic Surgical, obstetric, chest tube
Infectious diseases Poliomyelitis, herpes zoster, diphtheria,
influenza, syphilis, tuberculosis,
echinococcus infections
Neoplastic diseases Mediastinal tumors, N2 diseases
Others Dystrophia myotoxica, pericarditis,
subphrenic abscess, lead poisoning
Idiopathic
1544 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm

FIGURE 56-44 • A, Standard posteroanterior chest film. 8, Barium swallow showing a severe degree of elevation of
the diaphragm after pneumonectomy with volvulus of the stomach and outlet obstruction. Note that the gastric
fundus is above the level of the carina.

matic paralysis (Efthimiou et al, 1991), but many patients
with these injuries are expected to fully recover. Phrenic
nerve palsy after insertion of a chest tube has also been
reported (Arya et al, 1991; Ayalon et al, 1979; Marinelli
et al, 1981). A number of neuromuscular or infectious
disorders affecting the phrenic nerve or diaphragm have
been reported to be associated with an elevated dia-
phragm; these include poliomyelitis, herpes zoster (An-
derson, 1970; Brostoff, 1966), dystrophia myotoxica
(Chin and Lynn, 1956), diphtheria, influenza, syphilis,
lead poisoning (Wynn-Williams, 1954), pericarditis,
subphrenic abscesses (Hoover, 1913), and echinococcus
infection of the liver (Meyler and Huizinga, 1950). Per-
haps the most publicized cases have been those associ-
ated with the epidemic of polymyelitis in the early 1950s.
In 52 surviving adults submitted to follow-up examina-
tion by Sotrup (cited in Christensen, 1959), seven cases
of permanent eventration were found: four right-sided,
two left-sided, and one bilateral.
or metabolic disorders must be suspected although the
most common causes are obesity and pregnancy (Gierada
et al, 1998).
Clinical Presentation and Diagnosis
In the adult population, symptoms associated with ac-
quired elevation of the diaphragm are predominantly res-
piratory. Most patients complain of dyspnea and some-
times cough and retrosternal or epigastric pain. Other
complaints include a variety of digestive symptoms, rang-
ing from gas bloat, nausea; vomiting, heartburn, frequent
and uncontrollable belching to loud, abnormal noises
originating from air moving along the gastrointestinal
tract.
TABLE 5 6 - 1 1 Common Causes of Acquired
Diaphragmatic Elevation

Neoplastic involvement of the phrenic nerve is often Supradiaphragmatic Atelectasis

the cause of diaphragmatic elevation, and in patients Pulmonary resection
with bronchogenic carcinomas, phrenic nerve paralysis is Radiation fibrosis
usually secondary to mediastinal node disease. Phrenic Restrictive pleural disease
(diffuse mesothelioma)
nerve paralysis can also be associated with malignant Phrenic nerve paralysis
mediastinal masses such as thymomas, lymphomas, and Diaphragmatic Idiopathic elevation
germ cell tumors. Post-traumatic
Acquired diaphragmatic elevation can also be classified Infradiaphragmatic Hepatomegaly, splenomegaly
according to the location of the disorder that is responsi- Subphrenic abscess
Abdominal mass
ble for the anomaly (Table 56-11). When both hemidi- Colon or stomach distention
aphragms are elevated, neuromuscular, connective tissue,
 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm
The diagnosis of acquired elevation of the diaphragm
can usually be made on standard PA and lateral chest
films. The diaphragm is clearly elevated and forms a
round, unbroken line arching from the mediastinum to
the costal arch (Laxdal et al, 1954). The stomach is drawn
up into the chest, and it may be normally positioned with
a high fundus or it may be inverted with a partial or
complete volvulus. If there is involvement of the phrenic
nerve, true paradoxical motion of the diaphragm is seen
on fluoroscopy. Fluoroscopic examination may also be
useful in ruling out pericardial cysts or excess mediastinal
fat located at the cardiophrenic angle that may simulate
eventration. Diagnostic pneumoperitoneum might be
useful to distinguish between an elevated diaphragm and
frank herniation, although in chronic hernias adhesions
would prevent air from reaching the pleural space. The
original technique described by Zeitlin (1930) involved
the introduction of air, nitrous oxide, or carbon dioxide
into the peritoneal cavity, followed by an upright chest
radiograph to outline the diaphragmatic continuity. Un-
fortunately, CT scanning and ultrasound are not very
helpful in differentiating between elevated diaphragm and
true herniation (Yamashita et al, 1993). Michelson (1961)
has also shown that faradic stimulation of the phrenic
nerve at the time of thoracotomy may be helpful to
document the integrity of the phrenic nerve. Electromyo-
graphic studies can also be used preoperatively to docu-
ment the integrity of the phrenic nerve (Witz et al, 1982).
Two other issues in the investigation of-an elevated
hemidiaphragm in adults must be addressed during the
workup of these patients. The first involves the ruling
out of a malignancy by CT scanning and if necessary
by bronchoscopy and the second is to document the
consequences of the disorder on pulmonary function
through spirometric and exercise studies.
Management
Most cases of eventration occurring in adult life should
be treated conservatively unless severe dyspnea interfer-
ing with normal activities, orthopnea, or gastrointestinal
symptoms are clearly related to the high position of
the diaphragm. In infants with phrenic nerve paralysis
secondary to open heart surgery, aggressive treatment by
plication of the diaphragm is recommended by many
authors if the child is symptomatic or cannot be weaned
off the respirator. In the report of Shoemaker et al (1981),
six of seven patients treated by plication of the diaphragm
survived, the one death occurring in a premature infant
with multiple congenital cardiac defects. Children older
than 2 years of age are usually asymptomatic or have
only minor respiratory problems and as a rule they do
not require surgery (Tonz et al, 1996).
Although Wood (1916) was the first to suggest plica-
tion if symptoms were sufficiently distressing, Morrison
(1923b) is credited with being the first surgeon who
actually performed a successful plication of the dia-
phragm. The operation is usually carried out through a
posterolateral approach, and the repair can be done with
a simple plication without opening the diaphragm, or
through the excision of a central ellipse of aponeurotic
diaphragm followed by double breast suturing. In all
1545
cases, the objectives of surgery are to immobilize the
diaphragm in a lower flat position, to reduce its paradoxi-
cal movement and compression of the ipsilateral lung
and mediastinum, and possibily to recover function if
there is adequate residual muscle under the costal arch.
An abdominal approach is recommended for the repair of
bilateral eventrations, if there is infracardiac involvement
(Othersen and Lorenzo, 1977) or if there is a gastric
volvulus that requires repositioning.
More recently, plication done through a video-assisted
thoracic surgery approach was described by Mouroux
and co-workers (1996) (Fig. 56-45). With this technique,
the eventrated diaphragm is pushed down by endoscopic
long clamps and then plicated by the use of two superim-
posed transverse continuous sutures. The first line of
sutures holds the diaphragm down and keeps the excess
tissue within the abdomen, while the second suture line
completes the repair by placing the desired tension over
the dome. One obvious advantage of the technique is the
minimal access type of surgery, which facilitates postoper-
ative recovery and respiratory re-education.
Surgical repair of a transected phrenic nerve with res-
toration of diaphragmatic function has been reported in
patients with operative trauma to the phrenic nerve, even
4 months after the injury (Brouillette et al, 1986; Merav
et al, 1983). In such cases, sural or intercostal nerve
grafts can be used to bridge the gap between the severed
segments. Nerve regenerates at a rate of 1 mm per day,
so several months of observation are required before
restoration of motor function to the diaphragm. Good
results can be expected in approximately 75% of cases
(Fig. 56-46) (Millesi, 1981).
Results
Indications for surgery in adults are uncommon, and
the clinician must be very careful before recommending
plication for respiratory or digestive symptoms thought
to be related to elevation of the diaphragm. Table 56-12
summarizes the results obtained after surgical correction
of an elevated diaphragm. In Graham and co-workers'
series (1990) of 17 patients with a mean age of 53.7
years who underwent plication of the diaphragm, all
patients showed both subjective and objective improve-
ment (Table 56-13). Six patients were reassessed 5 or
more years after plication (range, 5 to 7 years) and the
improvement was maintained. In that series, the main
considerations before surgery were that the patient had
dyspnea interfering with normal activities and orthopnea
as well as respiratory function tests typical of diaphrag-
matic paralysis. In a very interesting paper reported by
Wright and colleagues (1985), seven adult patients un-
derwent plication of the diaphragm for dyspnea resulting
from unilateral diaphragmatic paralysis. There were no
postoperative complications and all patients' symptoms
were improved after surgery. After plication, significant
increases were noted in Pao2 and all lung volumes except
residual volume. The authors concluded that diaphrag-
matic plication is a safe and effective procedure for adult
patients with dyspnea resulting from unilateral diaphrag-
matic paralysis. Similarly, Ribet and Linder (1992) re-
ported good results in 11 adults followed up for a mean
1546 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm

Port 1

FIGURE 56-45 • A, Position of the two thoracoscopic ports. A minithoracotomy is made over the ninth intercostal space for
the suturing of the diaphragm. B, With the use of Duval forceps, the apex of the eventration is pushed down toward the
abdomen. C, The newly created transverse fold of diaphragm is sutured with nonabsorbable material. D, Completed operation.
ICS, intercostal space. (From Mouroux J, Padovani B, Poirier NC et al: Technique for the repair of diaphragmatic eventration.
Ann Thorac Surg 62:905, 1996.)
 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm 1547

TABLE 5 6 - 1 2 • Results of Plication for Diaphragmatic Elevation in the Adult Population

Operative Length of Improvement

No. of Mortality Follow-up
Author Patients (%) (yr) Clinical Radiographic Functional

Graham et al, 1990 17 0 5-7 6/6 SIS SIS

Wright et al, 1985 7 0 0.3-4 7/7 in in
Ribet and Linder, 1992 11 0 8.5 (mean) 10/11 — —
Pastor et a I, 1982 15 0 1-15 13/15 15/15 —
Donzeau-Gouge et al, 1982 9 10 0.4-10 7/8 — —
McNamara et al, 1968a 13 0 1-5 12/13 — —
Total 72 1.3% 92% 100% 100%

FIGURE 5 6 - 4 6 • A, Preoperative chest r a d i o g r a p h of a n e o n a t e w i t h acquired elevation of t h e r i g h t h e m i d i a p h r a g m secondary

to transection of t h e phrenic nerve, w h i c h occurred d u r i n g chest t u b e insertion f o r p n e u m o t h o r a x . 6, Chest r a d i o g r a p h done 12
m o n t h s a f t e r p l i c a t i o n a n d p r i m a r y repair o f t h e phrenic nerve.

TABLE 56-13 Dyspnea Scores and Physiologic Measurements Before and After Unilateral
Diaphragmatic Plication

Before Operation After Operation P value

D y s p n e a Score 7.4 + 0.8 3.3 0.9 <0.001

FVC
Sitting 2.7 + 0.7 3.2 ± • 0.5 <0.001
Lying 1.9 + 0.5 2.7 ± 0.6 <0.001
TLC
Sitting 4.1 + 1.6 4.5 ± 1.7 <0.002
Lying 3.4 + 0.8 4.2 ± 1.7 <0.002
FRC 2.5 + 0.2 2.9 ± 0.2 <0.01
ERV 0.6 + 0.2 0.9 ± 0.2 <0.01
RV 1.9 ± 0.2 2.0 ± 0.7 NS
DLCO (% predicted) 85 ± 4.5 100 ± 6.9 <0.05
Pao 2 73.1 ± 10.9 85.6 ± 13.2 <0.001
Paco 2 39.8 ± 6.7 38.4 ± 6.1 <0.001

DLCO, diffusion coefficient; ERV, expiratory reserve volume; FRC, Functional residual capacity; FVC, forced vital capacity; N5, not significant; RV,
residual volume; TLC, total lung capacity.
From Graham DR, Kaplan D, Evans CC, et al; Diaphragmatic plication for unilateral diaphragmatic paralysis: A 10-year experience. Ann Thorac Surg
49:249, 1990.
1548 CHAPTER 56 • The Diaphragm/Congenital Eventration and Acquired Elevation of the Diaphragm
period of 8.5 years after plication of the diaphragm. In
that series, the authors recommended surgery when there
were symptoms that could not be related to another cause
after complete thoracic and abdominal examinations.
CONCLUSION
Although there are few papers reporting the results of
surgical plication of the diaphragm for congenital
eventration, the operation can be life-saving in newborns
and infants. In these cases, the indication for surgery is
nearly always respiratory failure, and the results show
that operative treatment should be undertaken promptly.
In adults, great caution is recommended before plicating
the diaphragm for acquired elevation. In these cases, it is
important to rule out other possible causes of dyspnea
and sometimes small measures such as rehabilitation,
conditioning, proper respiratory hygiene, and weight loss
lessen dyspnea and orthopnea and help to avoid unneces-
sary surgery. If the patient has predominantly digestive
symptoms, one has to be even more careful in recom-
mending surgery before an appropriate period of observa-
tion and medical treatment.
COMMENTS AND CONTROVERSIES
The subject of diaphragmatic paralysis and eventration is
a puzzling one. This is a problem not frequently encoun-
tered by the adult thoracic surgeon. In their subchapter,
Dr. Deslauriers and his colleagues have made a significant
contribution in clarifying the circumstances of diaphrag-
matic paralysis and eventration. They point out the severe
physiologic and often life-threatening impairment in the
pediatric population and the need for early diaphragmatic
plication. Of greater interest to the adult thoracic surgeon
is the significant improvement that can be obtained by
diaphragmatic plication in symptomatic adult patients.
There is a growing literature clearly documenting im-
proved lung function after diaphragmatic plication.
G.A.P.
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Wayne ER, Campbell JB, Burrington JD, Davis WS: Eventration of the
diaphragm. J Pediatr Surg 9:643, 1974.
Witz JP, Jesel M, Roeslin N et al: Les eventrations diaphragmatiques de
l'adulte. Apport de Telectromyographie. Ann Chir Thorac Cardio-
vasc Surg 36:91, 1982.
Wood HG: Eventration of the diaphragm. Surg Gynecol Obstet
23:344, 1916.
Wright CD, Williams JG, Ogilvie CM, Donnelly RJ: Results of diaphrag-
matic plication for unilateral diaphragmatic paralysis. J Thorac
Cardiovasc Surg 90:195, 1985.
Wynn-Williams N: Hemidiaphragmatic paralysis and paresis of un-
known aetiology without any marked rise in level. Thorax 9:299,
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Yamashita K, Minemori K, Matsuda H et al: MR imaging in the diagnosis
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Zeitlin NS: Diagnostic pneumoperitoneum in diaphragmatic pathology.
Radiology 14:152, 1930.
1550 CHAPTER 56 • The Diaphragm/Phrenic Nerve Pacing
I PHRENIC NERVE PACING
Jacquelyn A. Quin
John A. Elefteriades
The process of breathing, though seemingly simple, re-
quires several components, all of which must function
and appropriately interact in order to achieve adequate
ventilation. Included are upper and lower motor neurons,
the diaphragm and other muscles of ventilation, and the
lungs themselves. Injury or involvement of any singular
component with disease may completely or permanently
interfere with the process of ventilation. Selected individ-
uals with respiratory failure, who would otherwise have
been dependent on mechanical ventilation, have regained
independence through diaphragm pacing. The purpose of
this chapter is to review diaphragmatic pacing including
diseases that respond to pacing, the process itself, and
results of pacing.
DIAPHRAGMATIC STRUCTURE AND
FUNCTION
As elucidated by West (1995), respiration is controlled
via respiratory centers, which are collections of upper
motor neurons located within the pons and medulla.
Three respiratory centers exist: (1) The medullary respi-
ratory center, located in the reticular formation of the
medulla, consists of inspiratory and expiratory areas,
which together influence the rhythm of breathing; (2) the
apneustic center, located in the lower pons, is believed to
prolong the inspiratory phase of breathing, while (3) the
pneumotaxic center, located in the upper pons, inhibits
inspiration and participates in the "fine tuning" of respira-
tion. Although it is considered an involuntary function,
voluntary control of breathing may supersede the brain-
stem reflex.
Input for regulation is provided by central and periph-
erally located chemoreceptors. Central chemoreceptors,
located near the medullary respiratory control center,
respond to changes in surrounding cerebral spinal fluid
(CSF) pH. During states of decreased ventilation, higher
partial pressures of carbon dioxide (Pco2) result in in-
creased co 2 diffusion across the blood-brain barrier. The
subsequent decrease in CSF pH and corresponding in-
crease in free [H + ] ions stimulate increased respiration
(Fig. 56-47). Peripheral chemoreceptors, located in the
carotid bodies, respond to decreased arterial partial pres-
sures of oxygen (Pao2); less of a response is seen with
changes in pH and Pco 2 (Fig. 56-47B).
Of the muscles that effect ventilation, the diaphragm is
the most important. This muscular sheet has two distinct
components: The thinner, costal muscle inserts on the
ribs and sternum and causes the diaphragm to flatten
and displace caudally. A thicker, crural component inserts
FIGURE 56-47 • A,
Ventilatory response to
increasing C0 2 at different
curve concentrations of
alveolar Po2. B, Ventilatory
response to hypoxia at
different concentrations of
alveolar Pco2. (BTPS, body
temperature, ambient pressure,
saturated with water vapor.)
(From West JB: Respiratory
Physiology: The essentials.
Baltimore, Williams & Wilkins,
1995.)
 CHAPTER 56 • The Diaphragm/Phrenic Nerve Pacing
on the lumbar vertebrae. In addition to diaphragm con-
traction, crural fibers increase thoracic diameter during
inspiration by elevating the lower ribs (DeTrover, 1982).
Three types of muscle fibers comprise the diaphragm.
Approximately 55% of diaphragm fibers are type 1, slow-
twitch, highly oxidative fibers that resist fatigue. Type IIA
fibers (21%) are fast-twitch, highly oxidative fibers that
resist fatigue to an intermediate degree. Type IIB fibers
(24%), by contrast, are fast-twitch, glycolytic fibers that
are prone to fatigue (Lieberman et al, 1973). This ratio
of different fiber types allows the diaphragm versatility in
meeting the metabolic demands of routine and strenuous
activity. During normal respiration, only a fraction of the
total number of fibers are stimulated during any given
respiration; this allows a proportion of fibers to recover
metabolically even as the diaphragm performs continu-
ous work.
The phrenic nerve, arising from the C3-C5 nerve
roots, carries lower motor innervation to the diaphragm.
In as many as 76% of patients, contribution of the C5
nerve root does not occur until the nerve trunk is in the
thorax, several centimeters below the level of the clavicle
(Kelley, 1950). This anatomic variant is important when
considering placement of the nerve electrode; a cervically
placed electrode may not capture all of the phrenic nerve
fibers. Although the nerve is comprised mostly of motor
fibers, a small number of sensory fibers innervates both
the thoracic and peritoneal surfaces of the muscle.
INJURY AND DISEASE
Injury may occur to any of the components of respiration:
diaphragm, phrenic nerve, or the central respiratory up-
per motor neuron; however, the change in respiration
may be imperceptible if the insult is slight. Symptomatic
injury is managed according to the affected ventilatory
component. In this regard, accurate assessment of the
level of injury is paramount, as this knowledge influences
the likelihood of successful phrenic nerve pacing.
Diaphragm
The diaphragm may be involved in a number of patho-
logic states, systemic diseases, and drug toxicities, as
outlined extensively by Syabbalo (1998). In general,
phrenic pacing is ineffective in these circumstances. Med-
ical or surgical management of the underlying disease
is appropriate. A different situation is encountered in
quadriplegic patients with diaphragm atrophy resulting
from chronic disuse. Provided it is otherwise normal with
an intact phrenic nerve, the diaphragm is expected to
respond favorably to diaphragmatic pacing.
Lower Motor Neuron and Phrenic Nerve
Iatrogenic phrenic nerve injury as a result of topical
cardiac hypothermia during cardiac surgery is well de-
scribed; the overall incidence ranges from less than 10%
to over 70%, depending on the method of diagnosis
(Dajee et al, 1983; Chroni et al, 1995; DeVita, 1993).
Injury more commonly occurs to the left phrenic nerve
1551
secondary to an increased risk of hypothermia exposure
(Dimopoulou et al, 1998). In this regard, placement of
an insulation pad within the pericardial well has been
shown to offer significant protection to the phrenic nerve.
In Wheeler and co-workers' (1985) study of 120 patients,
the incidence of injury was reduced from 60% to 8%.
Laub and associates (1991) demonstrated a reduction in
phrenic injury from 18% in the control group to 0% in
the protected group.
Injury to the phrenic nerve may occur during the
harvest of the left internal mammary artery owing to the
close proximity of the nerve to the origin of the artery
(Fig. 56-48) (Setina et al, 1993). Direct or thermal injury
may occur during dissection of the artery; injury may
also result from reduced perfusion of the nerve as the
proximal branches of the corresponding mammary artery
are divided (O'Brien et al, 1991). Iatrogenic injury to the
phrenic nerve during various congenital heart procedures
has been reported (Watanabe et al, 1997). Anecdotal
causes of phrenic nerve injury may occur as a result of
trauma (Merev et al, 1983) or during noncardiac proce-
dures (Sheridan et al, 1995). The phrenic nerve may
be directly involved in malignancy, infection, or other
metabolic disorders.
As with diaphragm injury, lower motor neuron injury
essentially precludes diaphragmatic pacing. Most cases of
FIGURE 56-48 • Interrelationships between the internal
mammary nerve and phrenic nerve. A, Right side. B, Left side.
Anatomic structures: 1, scalenus anticus muscle; 2, internal
mammary artery; 3, phrenic nerve; 4, subclavian artery; 5,
accessory phrenic nerve. (From Setina M, Carry S, Grim M, Pirk
J: Anatomical interrelation between the phrenic nerve and the
internal mammary artery as seen by the surgeon. J Cardiovasc
Surg (Torino) 34:449, 1993.)
1552 CHAPTER 56 • The Diaphragm/Phrenic Nerve Pacing
lower motor injury are well tolerated and temporary;
conservative management usually suffices. However, pro-
longed or bilateral paralysis may occur with significant
mortality and morbidity due to repeated pneumonia, ven-
tilatory failure with repeated incubation, and prolonged
mechanical ventilation (Diehl et al, 1994; Tonz et al,
1996).
Upper Motor Neuron Disease
Upper motor neuron injury may occur secondary to tu-
mor involvement, infection, trauma, or stroke. Idiopathic
nerve dysfunction may occur. Upper motor neuron injur-
ies are amenable to phrenic nerve pacing provided the
phrenic nerve is intact. The majority of phrenic nerve
patients fall into one of two categories of upper motor
neuron disease: central alveolar hypoventilation or quad-
riplegic.
Central alveolar hypoventilation (CAH) or central
sleep apnea falls under the category of sleep apnea disor-
ders. In general, sleep apnea represents a spectrum of
disturbed sleep patterns characterized by episodes of
failed respiration lasting greater than 10 seconds. The
number of apnea episodes varies: from 5 to greater than
20 episodes per hour may be seen in afflicted patients.
The exact prevalence is unknown; however, the reported
incidence varies from 0.3% to 15% of the population
(Davies and Stradling, 1995).
Central alveolar hypoventilation is also commonly
known as Ondine's curse. The history of this term is
outlined both by Goldblatt (1995) and Fodstad (1995).
The term originates from the Latin word for wave, unda.
Swiss philosopher von Hohenheim used the appellation
"undine" in his 1807 rendition of nature in which the
earth is represented by four types of spirits. In this
scheme, gnomes symbolize the earth and sylphs represent
the air. Salamanders depict fire and undines, or female
nymphs, epitomize water. In 1811, German playwright
de la Motte Fouque published Undine, a fictional story of
a mortal, Knight Huldbrand, who marries Undine, an
underwater spirit with an evil uncle, Kuhleborn. Follow-
ing a disagreement with Huldbrand, Undine is forced to
return to water, to the service of her uncle. She returns on
the wedding night of Huldbrand's remarriage to another
mortal to claim his life on behalf of Kuhleborn. Several
variations of the original story followed, including the
French play Ondine, by Jean Giraudoux, translated into
English by Valency in 1954. In this variation, Ondine's
husband Hans is fatally cursed for unfaithfulness by for-
getting to breathe. The term Ondine's curse was subse-
quently borrowed by Severinghaus and Mitchell (1962)
to describe three patients with failure of nocturnal hypo-
ventilation.
CAH is caused by a diminished response of the recep-
tors in the medulla to increased Pco 2 (Mellins et al,
1970). The normal increase in ventilation that occurs in
response to increasing arterial Pco 2 is diminished or ab-
sent in individuals with CAH; the ventilatory response to
decreases in Po2 is also blunted. Although the respiratory
impairment is continuous, affected individuals may con-
sciously augment ventilation while awake. At night, with
the loss of this voluntary contribution, episodic apnea
may ensue. However, because the condition is not truly
nocturnal, the term "central alveolar hypoventilation" is
preferred over sleep apnea. Adults may present with CAH
secondary to medullary involvement with tumor or infec-
tion. In the pediatric population, congenital CAH is often
diagnosed in association with other congenital diseases
including Hirshsprung's disease, metabolic disorders, and
other neuropathic conditions and tumors (Del Carmen
Sanchez et al, 1996).
Patients with central alveolar hypoventilation, or cen-
tral sleep apnea, must be distinguished from those with
obstructive sleep apnea. Patients with either affliction may
present with nocturnal episodes of apnea and complaints
of daytime somnolence (Mendelson, 1997); however, pa-
tients with obstructive sleep apnea have a normal ventila-
tory response to hypoxia and hypercarbia. Sleep apnea is
caused by mechanical airway obstruction secondary to
obesity, abnormal pharyngeal anatomy, exaggerated relax-
ation of the pharyngeal musculature with sleep, or by
space-occupying pharyngeal tumors.
The diagnosis of sleep apnea and the distinction be-
tween the two entities is usually performed using poly-
somnography in an overnight sleep laboratory. The pro-
cess is an involved one in which several parameters
including sleep, oxygenation, breathing airflow patterns,
and body movement are studied (Douglas, 1995). The
diagnosis is made in children similarly (Guilleminault et
al, 1996). Yen and colleagues (1997) have suggested a
simpler method of distinguishing between the two enti-
ties using measurements of airway impedance. Though
obstructive and central sleep apneas are considered two
distinct diseases, individuals may demonstrate character-
istics of both components. In such cases, if the obstruc-
tive component is present less than 50% of the time, the
apnea is considered central in origin (Mendelson, 1997).
Distinction between the two entities is necessary for
proper patient management. Patients with CAH are con-
sidered for phrenic nerve pacing; patients with obstruc-
tive sleep apnea are encouraged to undergo weight loss
if necessary, and they are supported at night with the use
of continuous positive airway pressure (CPAP). In more
advanced cases, patients with obstructive sleep apnea
may undergo uvulopalatopharyngoplasty, the removal of
redundant upper airway soft tissue to reduce upper air-
way impedance. In extreme cases, tracheostomy may be
necessary to secure an airway during sleep (Yen et al,
1997).
The other common condition that is treatable by phre-
nic nerve pacing is cervical spinal cord injury. The world-
wide incidence of spinal cord injury varies from less than
20 per million to over 40 per million population; the
incidence in industrialized countries appears slightly
higher (Karamenhetoglu, 1995; Lan et al, 1993; Otom et
al, 1997). In the United States, the estimated incidence
is 45 per million population (Johnson et al, 1997). Most
injuries are related to motor vehicle crashes (Burney et
al, 1993; Shingu et al, 1994; Thurman et al, 1995) with
a high degree of cervical injury and associated quadriple-
gia or quadriparesis (Price et al, 1994). Among the ado-
lescent population, preventable sport-related causes of
cervical injury are seen with a disturbingly high fre-
quency (Scher 1998; Tator et al, 1997; Tyroch et al,
 CHAPTER 56 • The Diaphragm/Phrenic Nerve Pacing
FIGURE 56-49 • Sensory and motor findings that distinguish "high" quadriplegia. Quadriplegia at C2-3 is amenable
to diaphragm pacing. (From Shields TW: General Thoracic Surgery, 4th ed. Baltimore, Williams & Wilkins, 1994.)
1997). In the elderly, cervical injuries from falls predomi-
nate (Alander et al, 1994; Spivak et al, 1994).
In general, patients with high cervical injury, that is,
above the C3 level, are most likely to benefit from pacing
since the nerve roots of C3-C5 and the integrity of the
phrenic nerve are maintained. The necrologic examina-
tion in these patients demonstrates intact sensation to
the clavicles, and motor function of the trapezius and
sternocleidomastoid muscles only (Fig. 56-49). Patients
whose cord injury involves any part of the C3-C5 nerve
roots have a compromised phrenic nerve, which may
interfere with pacing. Patients with cord injury below the
C5 level have an intact and functional phrenic nerve, and
they should be able to breathe independently although it
may not be apparent at the immediate time of injury. In
order to make this determination, a waiting period of
approximately 3 months is advised.
Diaphragmatic pacing has been attempted in two addi-
tional clinical situations: chronic obstructive pulmonary
disease (COPD) (Glenn, 1978) and intractable hiccups.
As patients with COPD become accustomed to chronic
hypercarbia, they become dependent on "hypoxic drive"
instead. If supplemental oxygen is required, episodic res-
piratory failure may occur, which may be treated using
phrenic nerve pacing. Fortunately, in practice, few pa-
tients have such advanced COPD. Similarly, intractable
hiccups have been treated with diaphragm pacing; how-
ever, the discomfort of pacing has often led to voluntary
cessation. Reports of phrenic nerve pacing in various
other diseases are not considered standard practice.
1553
HISTORICAL BACKGROUND OF PACING
Although full-time, simultaneous bilaterally diaphrag-
matic pacing has been in practice only for the last 2 to 3
decades, the concept of diaphragmatic contraction and
artificial respiration through electrical stimulation of the
phrenic nerve can be traced back to the late 1700s,
beginning with Cavallo in 1777 (Beard and Rockwell,
1875). In 1818, phrenic nerve stimulation was carried
out by Ure, who described his experimentation in a
criminal who had just recently been hanged: "The chest
heaved and fell; the belly was protruded and again col-
lapsed, with the relaxing and retiring diaphragm" (Ure,
1819).
Clinical applications of phrenic nerve stimulation fol-
lowed thereafter. Guillaume Duchenne de Boulogne used
phrenic nerve pacing to treat cholera patients who devel-
oped secondary asphyxia during a cholera epidemic in
1849 (Erdmann, 1858). Israel (1927) reported on the
successful use of phrenic nerve stimulation to support
ventilation in six asphyxiated newborns. In 1950, Sarnoff
and co-workers reported the use of phrenic nerve stimu-
lation in the management of patients with bulbar polio-
myelitis.
Long-term, continuous pacing of the conditioned dia-
phragm as it exists today was largely pioneered by Glenn
and his associates at Yale. Applying their background
knowledge of cardiac pacemakers, they first reported on
continuous phrenic nerve stimulation in an animal model
(Glenn et al, 1964), followed by its clinical application
in a patient with primary hypoventilation (Judson and
1554 CHAPTER 56 • The Diaphragm/Phrenic Nerve Pacing
Glenn, 1968). The next step in the development of phre-
nic nerve pacing systems should logically focus on the
refinement of a commercially available, totally im-
plantable pacing system with automatic rate adjustment,
based on the patient's end-tidal Paco2. While such ad-
vances have been realized experimentally Hogan et al,
1989; Lanmuller et al, 1997; the clinical application and
availability of such devices continue to be hindered by
the relatively small patient population who use such
devices and subsequent lack of interest in their commer-
cial development.
However, experimentation continues in the develop-
ment of artificial and assisted ventilation. Investigations
include the use of intercostal nerve stimulation as a sole
or supplementary source of artificial respiration (DiMarco
et al, 1989, 1994) and in combination with phrenic nerve
pacing (Supinski et al, 1991). Attempts to restore dis-
rupted phrenic nerve function have been reported, in-
cluding phrenic nerve grafting (Baldissera et al, 1993;
Krieger et al, 1994) and intradiaphragmatic phrenic nerve
stimulation (Peterson et al, 1994a, b). Other avenues
of research involve the study of diaphragm mechanics
(Coirault et al, 1995), strength and fatigue (Golgeli,
1995; Mador, 1996; Rochester, 1985), histology (Bisschop
et al, 1997), and gene expression (Gosselin et al, 1995).
The diaphragmatic response to pharmacologic agents
(Fujii et al, 1995; Van Lunteren and Moyer, 1996; Van
Lunteren et al, 1995), free radical scavengers (Supinski
et al, 1997; Travaline et al, 1997), and steroids (Dekhuij-
zen et al, 1995) are under study.
PREREQUISITES FOR PACING
It must be emphasized that phrenic nerve pacing is re-
served for patients with an intact phrenic nerve and
functional diaphragm. Accurate assessment of both is
imperative. New and modified techniques for assessment
of diaphragm strength and contraction have been de-
scribed (Maclean, 1981; Markland, 1984; McCauley,
1984; Syabbalo, 1998); however, established screening
tests for phrenic nerve function often suffice. These in-
clude observational assessment of the diaphragm during
transcutaneous phrenic nerve stimulation, fluoroscopy,
and phrenic nerve conduction studies.
Initial testing of the nerve is carried out by percutane-
ous stimulation in the neck, using a technique similar to
electromyography (Sarnoff et al, 1950; Shaw et al, 1975).
The lateral edge of the clavicular head of the sternoclei-
domastoid muscle is displaced medially. A thimble elec-
trode is placed at this level and a current is directed
posteriorly toward the presumed location of the nerve
(Fig. 56-50). Simple observation often suffices in assess-
FIGURE 56-50 • Access of the phrenic nerve for
stimulation studies. A, The phrenic nerve "trigger
point" is identified at the lateral border of the
sternocleidomastoid muscle where the nerve crosses
the scalene muscles. 6, Application of the thimble
electrode. (From Sarnoff SJ et al: Electrophrenic
respiration. VII. The motor point of the phrenic
nerve in relation to external stimulation. Surg
Gynecol Obstet 93:190, 1975.)
 CHAPTER 56 • The Diaphragm/Phrenic Nerve Pacing
ment of diaphragm function; significant and obvious con-
traction of the diaphragm should ensue if the nerve
is intact. Failure to elicit this response implies nerve
compromise, as the accuracy of the test approximates
100% (Mier et al, 1987; Shaw et al, 1980). Phrenic nerve
conduction time is also assessed, using two surface elec-
trodes (placed over the anterior and posterior axillary
line at the T8-T9 intercostal level) and an oscilloscope.
The interval time from cervical stimulation of the phrenic
nerve until a diaphragm action potential is recorded. The
average value in normal volunteers is 8.4 + 0.78 msec.
A prolonged latency (10 to 14 msec) is abnormal; how-
ever, this does not necessarily preclude successful pacing
(Glenn and Sairenji, 1985).
Quantitative diaphragm function is evaluated fluoro-
scopically A ruler with radiographically opaque numbers
is placed behind the pacing candidate such that the dome
of the unstimulated diaphragm lies over the numeral 1.
Maximal diaphragmatic descent on inspiration or phrenic
nerve stimulation is measured. In normal individuals, the
diaphragm descends approximately 8 to 10 cm; excursion
of at least 5 cm is desired for pacing (Glenn, 1985).
Phrenic nerve paralysis is suspected by elevation of the
affected hemidiaphragm on chest radiography or fluo-
roscopy. This is confirmed with a positive sniff test in
which a paradoxical, rapid upward movement of the
diaphragm is seen when the supine patient sniffs briskly
through the nose with the mouth closed. A functional
phrenic nerve should provide a brisk downward deflec-
tion of the diaphragm on nerve stimulation. The current
required to p r o d u c e m i n i m a l c o n t r a c t i o n of the dia-
phragm is defined as the threshold current; the maximal
current is defined as the least amount of current that
produces maximal excursion of the diaphragm.
Cervical magnetic stimulation (CMS) offers an alterna-
tive method to assess phrenic nerve conduction and dia-
phragm function. A magnetic coil, placed over the C3-
C5 nerve roots, causes depolarization of these roots. The
test is relatively painless and well tolerated. Because de-
polarization is applied to the roots comprising the phre-
nic nerve rather than the nerve per se, cross-stimulation
of the other muscles of respiration that are supplied by
the same nerve roots may occur; therefore, the test is not
specific for the phrenic nerve itself. The nerve roots may
be tested unilaterally (Mills et al, 1995) or bilaterally
(Similowski et al, 1998). Clinical applications using CMS
have included detection of diaphram fatigue (Laghi et al,
1996; Similowski et al, 1998), and the selection of phre-
nic nerve pacing candidates (Similowski et al, 1996);
however, experience with this mode of phrenic nerve
assessment is limited.
T r a n s d i a p h r a g m a t i c p r e s s u r e may also be u s e d for
p h r e n i c nerve a n d d i a p h r a g m assessment. Indwelling
midesophageal and stomach balloon catheters indirectly
measure pleural and abdominal pressures, respectively.
The transdiaphragmatic pressure (Pdi) is calculated as
the difference in pressure between the two catheters. A
value of approximately 10 cm H 2 0 is seen with phrenic
nerve stimulation in normal individuals (Moxham and
Shneerson, 1993). Diaphragm atrophy as well as phrenic
nerve dysfunction may cause lower values; thus, careful
interpretation of results is required.
1555
In addition to a functional phrenic nerve and dia-
phragm, phrenic pacing patients should have adequate
pulmonary function parameters and normal chest mor-
phology. Patients with CAH should demonstrate arterial
blood gas improvement with hyperventilation. All pa-
tients must be knowledgeable and cooperative and have
adequate medical and psychological support, including a
team of health care providers who can be made well
versed in phrenic nerve pacing, and a supportive network
of family members and friends. Patients with underlying
pulmonary disease, chest wall deformities, and neuro-
muscular disorders involving the diaphragm are poor
candidates for diaphragm pacing. Similarly, patients who
lack adequate nursing and emotional support often fail
pacing.
PACING PHYSIOLOGY
Unlike the heart, which is an electrical syncytium and
contracts with a single stimulus, the diaphragm requires
a series of stimuli to effect contraction. This form of
pacing, termed "pulse train stimulation," has several asso-
ciated definitions (Fig. 56-51). The pulse width defines
the duration of an individual stimulus within a pulse
train. The pulse interval, which defines the duration of
time between individual stimuli, may be alternatively
expressed as its reciprocal, frequency (frequency = 1000
per pulse interval). The pulse train duration defines the
total duration of a given series of pulse currents; this
corresponds to the actual duration of diaphragm con-
tractions. The amplitude of the pulse current measures
the voltage of the pulse train stimuli; this determines the
strength of diaphragmatic contraction as reflected by the
resulting tidal volume.
Unlike normal physiologic excitation, stimulation of
the phrenic nerve with a unipolar electrode causes simul-
Pulse width Pulse interval
FIGURE 56-51 • Pulse-train stimulation, associated
parameters, and units of measurements: amplitude (volts),
voltage of each stimulus within the pulse train; pulse width
(msec), duration of an individual pulse; pulse interval (msec),
duration between pulses within a train; pulse train duration
(msec), overall duration of one train of pulses. Frequency
refers to the timing of stimuli within a pulse train (i.e.,
frequency [Hz] = 1000/pulse interval). Rate is defined as the
number of pulse trains delivered in one minute. (From Shields
TW: General Thoracic Surgery, 4th ed. Baltimore, Williams &
Wilkins, 1994.)
1556 CHAPTER 56 • The Diaphragm/Phrenic Nerve Pacing
taneous depolarization of the entire nerve including all
associated motor units. Because the composition of the
native diaphragm includes fibers that are relatively prone
to fatigue, continuous, full-time pacing requires condi-
tioning of the diaphragm to electrical stimulation over a
period of weeks. As this occurs, the histology of the
diaphragm evolves from the existing composition of fast
(glycolytic) and slow (oxidative) fibers to one exclusively
of slow fibers. The vascular supply increases, enzyme
patterns change, and mitochrondria are increased (Man-
nion and Stephenson, 1985; Salmons and Hendriksson,
1981). These changes reflect the diaphragm's "plasticity"
and its inherent ability to sustain continuous mechani-
cal work.
PACING EQUIPMENT AND COMMERCIAL
DEVICES
Currently, three phrenic pacing systems are in clinical
use: the Avery model (Avery, Glen Cove, NY, USA), the
Jukka Astrostim (Atrotech OY, Tampere, Finland) and
the "Vienna phrenic pacemaker" (Medlmplant, Vienna,
Austria). Although each model varies slightly in design,
all subscribe to the same concept of phrenic nerve pacing
(Fig. 56-52): an extracorporeal generator and antenna
are used to encode pulse trains into radiofrequency sig-
nals which are transmitted across intact skin to a subcuta-
FIGURE 56-52 • Components of the diaphragm pacer. A, The
external generator and antenna (shown overlying the receiver)
and the implanted receiver and electrode. B, Electrode and
receiver as placed in patient. The phrenic nerve is placed at the
level of the upper thorax. The receiver is positioned over a flat
portion of the lower chest wall. (From Shields TW: General
Thoracic Surgery, 4th ed. Baltimore, Williams & Wilkins, 1994.)
FIGURE 56-53 • The two nerve-cuff electrode configurations
for phrenic nerve stimulation. A, 180-degree or "half cuff"
electrode configuration; S, 360-degree or "full cuff"
configuration. (From Letsou GV, Hogan JF, Lee P et al:
Comparison of 180-degree and 360 degree skeletal muscle
nerve cuff electrodes. Ann Thorac Surg 54:925, 1992.)
neously implanted radio receiver. The receiver translates
the radiofrequency signal into direct current, which is
delivered through an electrode to the phrenic nerve. All
three systems use increasing amplitude within each pulse
train to generate a smooth, gradual contraction of the
diaphragm. At present, there is no totally implanted phre-
nic nerve pacing system available for clinical use.
The Avery model uses the prototypic design of Glenn
and associates at Yale. The stationary extracorporeal gen-
erator is approximately the size of a clock radio. A hand-
held, portable generator is also available. The antenna
coil is taped securely to the patient's skin, directly over
the subcutaneously implanted receiver. The receiver,
about the size of a pocket watch, is placed subcutane-
ously over the lower, anterolateral aspect of the rib cage.
The unipolar electrode stimulates the entire phrenic
nerve with every impulse. A bipolar electrode is available
for patients in whom a competing device, such as a
cardiac pacemaker, is a consideration. The electrode is
preferentially placed beneath the nerve as a half-cuff or
180-degree configuration, as opposed to the cirumferen-
tial full-cuff or 360-degree configuration (Fig. 56-53), to
avoid the potential complication of circumferential scar
tissue that may occur with the latter (Letsou et al, 1992).
The Jukka Astrostim unit has a quadripolar electrode
made of two strips of polytetrafluoroethylene (Teflon)
with two electrode contacts on each strip. One strip is
placed in front of the nerve and the other behind it. In
theory, at any given time only partial recruitment of
motor units occurs, using one of the four electrode con-
tacts as a cathode, while the opposite side serves as the
anode (see Fig. 56-53A). Unstimulated motor units are
allowed time for metabolic recovery. This pattern of nerve
stimulation, which is designed to mimic the pattern of
metabolic recovery during natural ventilation, is believed
to alleviate diaphragm fatigue. At regular intervals, the
stimulation threshold may be increased to achieve a larger
tidal volume. These "sighs" condition additional dia-
phragm muscle mass in the event that recruitment of
these "reserve" muscle fibers are needed to meet increased
 CHAPTER 56 • The Diaphragm/Phrenic Nerve Pacing
FIGURE 56-54 • Quadrapolar electrodes. A, Atrotech
electrode. S, Single prong of the Vienna Pacemaker electrode,
enlarged to show sewing ring. Matchstick placed for
comparison. C, Full, 4-pronged Vienna Pacemaker electrode.
(From Creasey G, Elefteriades J, Dimarco A et al: Electrical
stimulation to restore respiration. J Rehab Res Dev 33:123,
1996.)
metabolic demands (Talonen et al, 1990). Similarly, the
Medlmplant model stimulates the nerve in a partial, stag-
gered fashion using multiple electrode contacts. After
each breath, the cathode-anode combination is alternated
bilaterally to avoid diaphragm fatigue. Each electrode has
four contact prongs that are sutured to the phrenic nerve
epineurium using 8-0 suture (Fig. 56-54).
SURGICAL PLACEMENT
In placing the phrenic nerve electrode, the operator must
use extreme caution in handling the nerve because injury
essentially precludes pacing or spontaneous breathing.
Muscle relaxants are avoided intraoperatively as they can
obfuscate pacing assessment. The prophylactic use of
antibiotics and careful aseptic surgical technique are of
paramount importance to avoid the disastrous complica-
tion of infection.
Electrode placement for the Avery of Atrotech model
1557
is carried out through a limited anterior thoracotomy in
the T2 or T3 intercostal space (Fig. 56-55). The internal
mammary artery and vein are divided to avoid injury or
disruption. The phrenic nerve is identified as it courses
anterior to the hilum, and a location is chosen to allow
flat, tension-free placement of the electrode. Two parallel
incisions are made in the mediastinal pleura on either
side of the phrenic neurovascular bundle. The electrode
is gently slipped behind the nerve and vessels such that
the phrenic nerve bundle is in contact with the electrode
without tension or distortion. Minor bleeding encoun-
tered during the dissection is anticipated to stop sponta-
neously; cautery, with potential injury to the phrenic
nerve, is best avoided.
Extra electrode length is left in the thorax to safeguard
against tension on the phrenic nerve by the electrode
with lung re-expansion. An intercostal segment of chest
tube is used to facilitate passage of the electrode wire
through the chest wall. After the electrode wire is con-
nected to the receiver unit, excess wire is placed into a
Teflon bag for easy, safe access later. The receiver and bag
are placed in a subcutaneous pocket with the receiver
closer to the skin surface to optimize signal transmission.
The subcutaneous tissues are closed tightly to avoid re-
ceiver migration within the pocket, with the skin incision
well away from the underlying receiver. Chest closure is
standard. Before undraping the patient, the system is
tested under sterile conditions. A stimulation threshold
of 1.0 to 2.9 mA indicates a functional unit. Failure to
achieve this necessitates re-evaluation of electrode place-
ment and component parts. If indicated, the contralateral
unit is placed approximately 2 weeks after the first im-
plantation. It is anticipated that thoracosopic electrode
placement may eventually supersede the open technique.
However, one must always adhere to the principle of
minimal nerve trauma, regardless of the method of place-
ment.
Cervical electrode placement remains somewhat con-
troversial. Advantages of this approach include the avoid-
ance of bilateral thoracotomy, which may be advanta-
geous in patients with pulmonary parenchymal disease
or chest wall deformity. Bilateral concurrent implantation
may be performed in the neck. The major disadvantage
of cervical electrode placement is failure to provide com-
plete phrenic nerve stimulation in individuals with an
accessory or bifurcated phrenic nerve; these compo-
nents often do not consolidate until the phrenic nerve is
in the thorax. Other anatomic variations of the nerve in
the neck, including an intramuscular segment within the
scalenus amicus, or proximity to the brachial plexus
(Fodstad 1987), may preclude effective pacing. The elec-
trode may also migrate with excessive neck movement.
In the event that cervical electrode placement is per-
formed, temporary endotracheal intubation, removal of
the tracheostomy, and occlusion of the tracheostomy site
may be used to decrease the risk of electrode contamina-
tion during placement. Exposure is obtained using a
supraclavicular incision. The lateral border of the sterno-
cleidomastoid muscle is identified and retracted medially.
The nerve is almost always found overlying the scalenus
amicus muscle at this level, crossing from the lateral to
medial aspect of the muscle, just deep to the scalene
1558 CHAPTER 56 • The Diaphragm/Phrenic Nerve Pacing
fascia. A stimulation probe is placed in this area, and 2
to 10 mA of current is applied. Diaphragm contraction
confirms correct identification of the nerve. Placement of
the nerve electrode and radio receiver is similar to that
in the chest. The subcutaneous pocket is placed inferior
to the clavicle, using the existing supraclavicular incision.
The Medlmplant system is placed through a median
sternotomy with bilateral simultaneous electrode place-
ment. The electrode prongs are sutured to the phrenic
nerve epineurium using fine polypropylene suture and
the surgical microscope. The receiver is placed under-
neath the rectus abdominis fascia.
A permanent tracheostomy is present in most, if not
all, patients in whom phrenic nerve pacing is undertaken.
This provides a secure airway in the event of pacemaker
malfunction, and it should be maintained, even after full-
time continuous pacing is achieved. The conventional
FIGURE 56-55 • Transthoracic
approach for phrenic nerve electrode
placement. Top frame: separate
incisions for the second to third
intercostal spaces and for receiver
placement shown (R, receiver; A,
anode plate; C, connectors.) Middle
and bottom frames: sequential steps
in placement of the electrode
behind the phrenic neurovascular
bundle. (From Elefteriades JA et al:
The Diaphragm: Dysfunction and
induced pacing. In Baue CL (ed):
Glenn's Thoracic and Cardiovascular
Srugery, 6th ed. Stamford, CT,
Appleton & Lange, 1996.)
tracheostomy may be replaced by a Teflon tracheal button
to maintain the airway with improved cosmesis and less
tracheal irritation.
CONDUCT OF PACING
Approximately 2 weeks of recovery are allowed after
device implantation before pacing is initiated, as attempts
to pace earlier may cause bloody pleural effusion, thought
secondary to disruption of immature pleural adhesions.
Low-frequency continuous, bilateral simultaneous pacing
is preferred in individuals totally dependent on diaphrag-
matic pacing; in adults with central alveolar hypoventila-
tion, unilateral pacing may suffice. Pacemaker settings
preset from the manufacturer (Avery) include inspiratory
duration (1.3 seconds for adults, 0.6 second for children)
and pulse width (150 msec). Settings for current are
 CHAPTER 56 • The Diaphragm/Phrenic Nerve Pacing
placed just above the maximum threshold level. The
respiratory rate is individualized for each patient. Rates
of 6 to 10 breaths/min usually suffice for patients who
pace bilaterally; higher rates are required for children and
for patients who pace unilaterally (Weese-Mayer, 1989).
Quadriplegia patients with diaphragm atrophy require
conditioning of the diaphragm prior to continuous, bilat-
eral stimulation. The usual conditioning regimen starts
with 15 minutes of pacing during each waking hour. The
number of minutes of eacb hour and the number of hours
paced each day are gradually increased until continuous
pacing is achieved. Patients are monitored during pacing
sessions using measurements of tidal volume, minute
ventilation, end-tidal C 0 2 , oxygen saturation, and occa-
sionally, blood gas measurements. A fall in tidal volume
with a corresponding rise in end-tidal C 0 2 is an indica-
tion that the diaphragm may be beginning to fatigue. The
patient is rested on mechanical ventilation overnight or
longer if necessary, and on resuming the pacing schedule,
a shorter pacing period is set. Advances in the pacing
schedule are made every 7 to 14 days (or less) as tolerated
by the patient. The conditioning phase usually lasts 3
to 6 months; however, this process may be longer in
quadriplegic p a t i e n t s w i t h severe d i a p h r a g m atrophy.
Once continuous pacing is achieved, the frequency of
stimuli within each pulse train and the number of breaths
per minute are decreased to minimize diaphragm fatigue.
Patients who require only intermittent pacing may initi-
ate the full pacing schedule without conditioning, as
diaphragm fatigue is unlikely. In children, bilateral pacing
should be performed to avoid mediastinal shifts, which
may occur with unilateral pacing. A faster respiratory
rate and shorter inspiratory duration (0.6 second) are
preferred in the pediatric population. Children over the
age of 8 to 10 may essentially pace as adults.
Unlike cardiac p a c e m a k e r s , w h i c h are essentially
maintenance free, phrenic pacemakers require constant
vigilance and a thorough understanding of the pacing
device, its limitations, and associated caveats to avert
potential complications including infection, respiratory
insufficiency, nerve injury, a n d diaphragmatic fatigue.
Pacemaker failure may occur from receiver or electrode
malfunction or from interference by another pacing de-
vice such as a cardiac pacemaker.
RESULTS
Given the relatively low numbers of phrenic nerve pace-
makers implanted worldwide, the number of institutions
with reported series of patients are few. The largest series
of patients with follow-up was that reported by Glenn
and associates, in 1988, of 165 patients who underwent
device implantation at one of six centers: Yale-New Ha-
ven Medical Center, Children's Memorial Hospital (Chi-
cago), Toronto Western Hospital, Umea University Hospi-
tal (Sweden), Mayo Clinic, and Children's Hospital of Los
Angeles. Sixty-five patients underwent unilateral elec-
trode placement; the remaining 100 patients underwent
bilateral p l a c e m e n t . Twenty-seven p e r c e n t of p a t i e n t s
paced full time; 6 1 % paced part time. Pacing successfully
met the ventilatory requirements of 47%, and was par-
tially successful in an additional 36%. The majority of
1559
patients in the study had paced for less than 5 years (108
patients, 68%). Thirty-one patients (20%) paced for 5 to
10 years, 16 patients (10%) paced for 10 to 15 years, and
4 patients (16%) paced for 15 to 20 years.
More recently, Weese-Mayer and associates (1996)
reported results with the quadripolar electrode, using
both physician questionnaire and the Atrotech registry.
Sixty-four individuals (35 children, 29 adults) from 13
countries underwent device implantation. Thirty-three
children and 27 adults paced bilaterally. At a mean fol-
low-up of 2.0 ± 1.0 years, 94% of 35 children paced
successfully. Of the 29 adults, 86% adults paced success-
fully at a mean follow-up of 2.2 ± 1.1 years. Thirteen
(45%) of the adults paced full time. Twelve (41%) adults
paced part time; two of these patients paced less than 5
hours daily. Nine (26%) of the children paced full time;
66% of the children paced part time (at least 5 hours
daily). Complication-free pacing rates were lower (60%
of pediatric and 52% of adult patients, at follow-up peri-
ods of 2.0 ± 1.0 and 2.2 ± 1.1 years, respectively).
Complications included electrode dysfunction (19%),
electrode failure requiring replacement (3.1%), receiver
failure (5.9%), infection (2.9%), and iatrogenic nerve
injury (3.8%).
Several series provide data on long-term follow-up
after pacemaker implantation. Fodstad (1995) reports
experience with device implantation in 42 patients (33
bilateral, 9 u n i l a t e r a l ) w i t h a m e a n follow-up of 62
months. Nineteen patients continued to pace full time, 5
patients paced intermittently, and 8 patients did not pace.
Seven patients had died after pacing for periods ranging
from 4 months to 11 years. Three patients died before
achieving pacing. Of the 8 patients who did not pace at
the time of follow-up, six patients with partial phrenic
nerve damage (C3-C5 injury) stopped pacing after peri-
ods ranging from 1 month to 3 years. The two remaining
patients, both of w h o m underwent pacemaker implanta-
tion for hiccups, stopped pacing voluntarily, shortly after
device implantation. Mayr and associates (1993) reported
on experience using the Vienna pacemaker in 15 patients
with high cervical quadriplegia and complete ventilatory
insufficiency. Three patients were undergoing condition-
ing. Eleven patients who achieved conditioned diaphragm
pacing, at time of follow-up, had paced a mean of 43.3
months (range, 5 to 83 months); included were 4 patients
who died after pacing 7, 3 1 , 58 and 60 months. One
patient was able to pace intermittently for 2 to 3 hours
at a time. Experience with the Vienna pacemaker in eight
pediatric patients, with ages ranging from 2 to 13 years
(mean age, 9 ± 3-), was reported by Girsch (1996). At
the time of follow-up, one patient continued to undergo
diaphragm conditioning. Continuous phrenic nerve pac-
ing was achieved in four patients after a mean condition-
ing period of 13 months; these four patients had paced
for periods of 10, 28, 38, and 48 months. Two of these
patients subsequently died of complications of pneumo-
nia. Two patients paced intermittently for 24 and 36
months, respectively; at the time of follow up, both had
died from complications of pneumonia. One patient re-
fused to pace after device implantation and was ventilated
mechanically.
Of 14 quadriplegia patients conditioned at Yale for
1560 CHAPTER 56 • The Diaphragm/Phrenic Nerve Pacing
bilateral full-time pacing, seven paced full time at a mean
follow-up of 7.6 years, when first reported by the senior
author (Elefteriades et al, 1992). Five patients continue
to pace full time and have all done so for over 10
years; the longest paced patient has done so for 17 years
(Elefteriades, unpublished data, 1997). Three patients are
deceased, two of whom previously paced for 10.5 years
and 6 months, respectively. Six patients did not achieve or
maintain pacing for multiple reasons, including medical
complications of quadriplegia, insufficient nursing care,
patient preference, and insufficient finances to support
pacing.
DIAPHRAGM PACING: ADVANTAGES AND
CAVEATS
When applied to carefully selected patients, the success
of long-term phrenic nerve pacing has been shown un-
equivocally by patients who pace for several years with-
out interruption. For quadriplegia patients this dia-
phragm pacing represents their only source of ventilation.
Patients who may otherwise face institutionalization and
mechanical ventilation have greater autonomy with phre-
nic pacing, often with great psychological benefit. With
proper supportive care, patients live independently and
carry out productive lives including full-time employ-
ment, travel, and leisure. Children who are paced have
greater ventilatory capacity and are able to participate in
sports and other strenuous activities. Diaphragm pacing
more closely mimics physiologic negative pressure venti-
lation and may pose less lung barotrauma, may decrease
pulmonary vascular resistance and may increase systemic
blood flow (Ishii et al, 1990). No randomized studies
directly compare phrenic nerve pacing with mechanical
ventilation; however, Esclarin and co-workers' (1994)
retrospective study comparing the two modalities suggest
that patients managed with phrenic nerve-pacing phonate
optimally, are more mobile, achieve a higher rate of hos-
pital discharge, and are managed at lower cost.
However, emphasis must be placed on the importance
of proper selection for pacing candidates. Patients with
equivocal indications, who fail to meet the prerequisites
for pacing, often fail during pacing, after having invested
considerable emotional, physical, and financial effort and
resources. Conversely, patients with the proper indica-
tions and with adequate medical and social support may
enjoy the benefits of successful pacing both in terms of
quality of life, medical condition, and financial costs and
may do so for extended periods.
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