SURGICAL ANATOMY AND EMBRYOLOGY

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EMBRYOLOGIC AND ANATOMIC

BASIS OF DUODENAL SURGERY
John Androulakis, MD, Gene L. Colborn, PhD,
Panagiotis N. Skandalakis, MD, Lee J. Skandalakis, MD,
and John E. Skandalakis, MD, PhD

EMBRYOGENESIS

The caudal (distal or terminal) part of the foregut and the cranial (cephalic
or proximal) part of the midgut are responsible for the genesis of the duodenum.
The origin of the liver and pancreas is located just above the union of foregut
and midgut, so the foregut is responsible for the genesis of these two glands.
The midgut opens ventrally into the yolk sac. During the third and fourth weeks
of gestation, the embryo grows rapidly, whereas the yolk sac and open midgut
do not. The ventral boundary between foregut and midgut is the future duodenum. During this period and during these movements, the cells and structures
of the mature duodenum develop, including the smooth muscles, villi, argentaffin cells, goblet cells, Paneth cells, Brunner 's glands, and lymphoid tissue.
At approximately 24 days of gestation, the hepatic diverticulum of endoderm arises from the floor of the future duodenum and grows into the septum
transversum. At the end of the fourth week of gestation, the dorsal pancreatic
primordium arises from the dorsal side of the duodenum. By this time, the
ventral diverticulum has differentiated into primitive liver cords, the gallbladder
and cystic duct, and the ventral pancreatic duct (Fig. 1).
Several embryologic questions about duodenal rotation, mesenteric attachments, retroperitoneal position of the duodenum, and reduction of the duodenal

From the Centers for Surgical Anatomy and Technique (GLC, PNS, LJS, JES) and Department of Surgery (LJS, JES), Emory University School of Medicine, Atlanta; Piedmont
Hospital, Atlanta (JES); Center for Clinical Anatomy (GLC) and Department of Surgery (GLC, JES), The Medical College of Georgia, Augusta; and Mercer University
School of Medicine, Macon, Georgia (JES); the Department of Surgery, University of
Patras Medical School, Patras, Greece (JA); and the Department of Surgery, Medical
School, University of Athens, Athens, Greece (PNS)

SURGICAL CLINICS OF NORTH AMERICA

VOLUME 80 * NUMBER 1 * FEBRUARY 2000

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ANDROULAKIS et a1

lumen remain. M e y e r ~
finds
~ ~ a role for the ligament of Treitz in the embryologic
rotation of the bowel. ORahilly and Muller42believe that duodenal rotation is
unlikely. SadleF supports duodenal rotation to the right, reaching a retroperitoneal position (Figs. 1 and 2). Kluth et a129also question the rotation of the
intestine and cite the "puzzling embryology of the midgut."
The first part of the duodenum retains dorsal and ventral mesentery, but
during rotation, when the duodenal loop is fixed in the retroperitoneal space,
the dorsal mesentery of the rest of the duodenum "disappears." The disappearing dorsal duodenum mesentery remains as an avascular plane of loose
connective tissue (the fascia of Treitz) (Fig. 2C). It is not related to the ligament
of Treitz, which is perhaps a remnant of the dorsal mesentery bridging the
flexure to the right crus of the diaphragm or to the tissues around the celiac
artery (CA). A duodenal mesentery is rare. The authors have seen only two
cases in 40 years in the operating room and the anatomic laboratory. This plane

Stomach

Figure 1. Embryonic relations of pancreas and duodenum. A, Formation of dorsal and

ventral pancreatic primordia. B, Rotation of ventral pancreas. C, Fusion of primordia to
form adult pancreas. (From Gray SW, Colborn GL, Pemberton LB, et al: The duodenum.
Am Surg 55(part 1):258, 1989; with permission.)

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173

Dors
me

mesecery

, -----

J[

plone of

fusion (fascia
of Treitz)

Duodenum

C
Figure 2. Rotation of pancreas and duodenum. A, Primitive relation of dorsal and ventral
pancreatic primordia. B, Disappearance of ventral mesentery and rotation of ventral pancreas. C,Final retroperitoneal position of duodenum and pancreas. The plane of fusion of
the mesoduodenum is the avascular fascia of Treitz. IVC = inferior vena cava; A = aorta;
Inf = inferior. (From Gray SW, Colburn GL, Pemberton LB, et al: The duodenum. Am Surg
55(part 1):258,1989; with permission.)

is entered when the Kocher maneuver is performed to lift the second part of the
duodenum to the left, thereby exposing the retroduodenal and retropancreatic regions.
The midgut of embryology is incongruent with the midgut of surgery,
which is supplied by the superior mesenteric artery (SMA), but because of its
dual embryologic origin (i.e., the foregut and midgut), the duodenum has a dual
blood supply (CA and SMA).
CONGENITAL ANOMALIES
Stenosis and Atresia

Duodenal stenosis is often associated with annular pancreas or intramural,

ectopic pancreatic tissue. Stenosis may also result from a perforated diaphragmatic atresia. The aperture may be sufficiently large that functional atresia
develops only in adult life.
Duodenal atresia may be membranous (Fig. 3A) or segmental (Fig. 3B
and C), the former being the most common. Membranous atresia, complete or
perforated, has been called intraluminal duodenal diverticulum. Although this is

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ANDROULAKIS et a1

Figure 3.Types of intestinal atresia. A, Diaphragmatic. 6,Segmental with complete mesentery. C,Segmental with absence of mesentery and no connection between the blind ends.
In each case, the proximal loop is dilated and the distal loop is unexpanded. The diaphragmatic type may perforate under pressure of intestinal contents, becoming a stenosis rather
than an atresia. (From Skandalakis JE, Gray SW, Ricketts R, et al: The small intestines. In
Skandalakis JE, Gray SW (eds): Embryology for Surgeons, ed 2. Baltimore, Williams &
Wilkins, 1994, p 184; with permission.)

not incorrect, it does not reflect the origin of the lesion from an atresia. In all
forms of duodenal atresia, the proximal duodenum is dilated and the distal
duodenum is completely unexpanded; obstruction is complete.
Approximately 75% of all intestinal stenoses and 40% of intestinal atresias
are found in the duodenum. A congenital duodenal diaphragm in a woman was
associated with abnormal location of the ampulla of Vater in the third part of
the duodenum.31Multiple atresias may occur; in such cases, only the proximal
one will have a dilated proximal segment. Stenosis may cause intermittent
obstruction, which may be amenable to a liquid diet.

Annular Pancreas

In patients with an annular pancreas (Fig. 4), a thin, flat band of pancreatic
tissue completely surrounding the second part of the duodenum forms this
annular pancreas. It is usually associated with duodenal stenosis. The band may
be wholly or partially free from the duodenum, or the pancreatic tissue may be
intermingled with the duodenal muscular coat. The ring of pancreatic tissue
contains a large duct that usually drains into the main pancreatic duct.

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Portal v
\

SMV

SMA

Figure 4. Stenosed duodenum beneath annular pancreas. SMA = superior mesenteric

artery; SMV=superior mesenteric vein; v=vein; a=artery. (From Colborn GL, Gray SW,
Pemberton LB, et al: The duodenum. Am Surg 55(part 3):469,1989; with permission.)

Ectopic Duodenal Pancreatic Tissue

Pancreatic tissue may be found in several abdominal sites, the most common
of which is the duodenal wall. The pancreatic tissue may be sequestered in the
submucosa beneath the muscularis of the duodenum. A second source of intramural pancreatic tissue results from the pancreatization of Brunner's glands, a
phenomenon that is normally suppressed by the developing pancreas.
Duodenal pancreatic tissue has been reported in 14% of necropsies.22aIt is a
potential source of obstruction, disruption of normal peristalsis, and production
of peptic ulcer or neoplasm.
Megaduodenum

Megaduodenum is most likely secondary to neuromotor function at the

myenteric plexus of Auerbach, which produces a functional obstruction similar
to that of patients with congenital megacolon. Mishalany et a14" reported on a
case of a newborn infant with intestinal obstruction secondary to severe depletion of ganglion cells and nerve fibers at Auerbachs plexus; the submucous
plexus of Meissner was normal.
Duodenal Diverticula and Duplications

False diverticula of the duodenum (Fig. 5) are usually found on the concave
wall of the second and third parts of the duodenum, often close to the duodenal
papillae. According to Eggert et a1,2I more than two thirds of duodenal diverticula are located within 2 cm of the vicinity of the ampulla of Vater. Although

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Figure 5. Relative distribution of primary false diverticula of the duodenum. Greatest

incidence (dark area). Most common location is near the papilla of Vater. (From Colborn
GL, Gray SW, Pemberton LB, et al: The duodenum. Am Surg 55(part 3):469,1989; with

permission.)

they usually reveal themselves only in adult life, many such lesions originate
before birth. They are usually solitary and asymptomatic, and the authors agree
with Eiseman et alZ2to leave them alone. A diverticulum lying near the papilla
may present difficulties for endoscopists.
Cystic intramural duplications of the alimentary tract are uncommon, but
20% of all such lesions are found in the duodenum.
Preduodenal Portal Vein

Rarely, during the development of the portal vein, a channel passing anterior to the duodenum rather than posterior to it becomes the definitive portal
vein of adults (Fig. 6). Such an anomalous vein produces compression of the
first or second part of the duodenum. This anomaly is usually associated with
malrotation, situs inversus viscerum, duodenal atresia, annular pancreas, or
cardiac and biliary malformations.
Paraduodenal Fossae and Hernias

Paraduodenal fossae are pockets of peritoneum on the posterior abdominal

wall produced by areas of failure of fusion of the dorsal mesocolon with the
parietal peritoneum in the fifth fetal month. These fossae are inconstant; any, all,
or none may be present. An intestinal loop herniated into the fossa forms a
paraduodenal hernia. If the loop passes to the right, it is a right paraduodenal
hernia; If the loop passes to the left, it is a left paraduodenal hernia, without

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177

Figure 6. Embryonic origin of preduodenal portal vein. A, Embryonic extrahepatic communications between vitelline veins (V). 13,Normal development; persistent superior communicating vein forms a part of normal, postduodenal portal vein. C, Anomalous persistent
inferior communicating vein forms a part of an anomalous preduodenal portal vein.
(From Colborn GL, Gray SW, Pemberton LB, et al: The duodenum. Am Surg 55(part
3):469,1989; with permission.)

reference to the midline of the body or to the specific fossa concerned. In more
than 95% of these hernias, the loop passes to the right.
Early investigators believed that paraduodenal fossae were congenital and
that a paraduodenal hernia was acquired by gradual enlargement of the existing
fossa. Investigators now believe that the hernias and fossae are of congenital
origin. An empty paraduodenal fossa is not the site of a potential hernia in later
life; instead, it marks the location in which a congenital hernia might have
formed but failed to do so.
Vascular Compression of the Duodenum (Superior
Mesenteric Artery Syndrome or Wilkes Disease)
Vascular compression of the duodenum is the result of compression of the
third part of the duodenum against the aorta and vertebral column by the SMA
at the level of L2 or L3 (Fig. 7). The resulting obstruction may be acute or
chronic, partial or complete?
Although the mechanics of the obstruction are clear, the contributing
events are not. Several variations from the normal anatomy have been
suggested, including congenitally short mesentery, aberrant SMA, excessive
mobility of the right colon, malrotation, and short suspensory ligament.

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ANDROULAKIS et a1

Pancreas

Transverse colon

Superior MesentericArtery

Figure 7. A, Sagittal section showing position of duodenum in relation to aorta and superior
mesenteric artery. SMA = superior mesenteric artery; X = transverse mesocolon. (From Gray
SW, Akin JT Jr, Milsap JH Jr, et al: Vascular compression of the duodenum. Part I. Contemp
Surg 9:37, 1976; with permission). B, Relationship between superior mesenteric artery and
duodenum. Compression of duodenum between artery and aorta may produce obstruction
characteristic of superior mesenteric artery syndrome. (From Colborn GL, Gray SW, Pemberton LB, et al: The duodenum. Am Surg 55(part 3):469, 1989; with permission.)

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The first three are difficult to evaluate anatomically and impossible to prove
embryologically. The last two can be recognized easily; unfortunately, they are
absent in many affected patients.
Acquired factors, such as obesity, excessive weight loss, enforced bed rest
in the supine position, and the presence of a body cast, may alter unfavorably
the angle of mesenteric traction and increase the possibility of duodenal compre~sion.~

SURGICAL ANATOMY
Duodenal Wall
The wall of the duodenum is composed of the serosa or adventitia, muscularis externa, submucosa, and mucosa. Histologic and physiologic details about
the duodenal wall are not within the scope of this article. This presentation is
strictly from a surgical standpoint.

Gastroduodenal Junction
At the gastroduodenal junction, the continuity of the circular musculature
is interrupted by a ring-shaped septum of connective tissue derived from the
submucosa. Proximal to this ring, the circular muscle layer is thickened to form
the pyloric sphincter of the stomach; distal to the ring is an abrupt decrease in
the thickness of the circular muscle to form the relatively thin-walled duodenum.
This decrease results in a pyloric "0s pylorus" surrounded by a duodenal fornix.
This arrangement must be kept in mind when pyloromyotomy is performed.
The longitudinal muscle layer, without a change in thickness, is also interrupted at the gastroduodenal junction, except on the side of the lesser curvature,
where some peripheral muscle fibers are continuous with fibers of the duodenal
musculature. This arrangement may serve to carry peristaltic contractions across
the interruption at the connective tissue
Internally, the appearance of the submucosal glands of Brunner marks the
gastroduodenal junction. This may not agree with the muscular junction. The
submucosal glands may extend a few centimeters into the pylorus. Antral gastric
mucosa may prolapse through the pylorus, producing a radiologic finding but
not a true clinical syndrome.
L a ~ s o nreports
~ ~ three histologically distinct types of normal duodenal
mucosa at the gastroduodenal junction: (1)antral, (2) transitional, and (3) jejunal.
Acute and chronic duodenal ulcers occur in the jejunal m u c o ~ aChronic
. ~ ~ duodenitis most likely does not have the association with chronic duodenal ulceration
that chronic gastritis has with chronic gastric ulcer.
The musculature of the upper duodenum forms an extensive helicoidal
system of bundles.37 Some fiber bundles belong to the external and internal
muscular layers and penetrate the pancreatic stroma. Others are related to the
tunica adventitia of the duodenum, hepatoduodenal ligament, and gastroduodenal artery.
The duodenojejunal junction is marked internally by the disappearance of
Brunner's glands and externally by the attachment of the suspensory ligament
of Treitz. No line of demarcation is present at this junction.

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Suspensory Ligament of Treitz

The suspensory muscle or ligament is a fibromuscular band that arises
from the right crus of the diaphragm and inserts on the upper surface of the
duodenojejunal flexure. It passes posterior to the pancreas and the splenic vein
and anterior to the left renal vein. It may surround the celiac artery or course to
its left as the ligament passes toward the terminal region of the duodenum. At
its origin, the band contains striated muscle fibers continuous with those of the
crus. Near its insertion, the suspensory band contains smooth muscle fibers
continuous with those of the longitudinal duodenal muscularis.
In 1853, T r e i t ~described
~~
the suspensory muscle of the duodenum. It
originates from the duodenojejunal flexure and a part of the inferior transverse
portion of the duodenum. It travels upward to insert in the connective tissue
around the SMA and CA. Treitz also described the Hilfsmuskel, a bridge that
starts from the right border of the esophageal hiatus of the duodenum and
terminates at the suspensory ligament in a caudal way. From a surgical standpoint, the origin and insertion of the ligament are academic.
Jit and Grewa126reported the following:
The gross anatomy, microscopic structure and nerve supply of the
suspensory muscle of the duodenum and Hilfsmuskel have been
studied in cadavers of 88 adults, 5 children, 1 infant and 6
neonates. The suspensory muscle of the duodenum, consisting of
plain muscle fibres, arose from the connective tissue around the
stems of the coeliac and superior mesenteric arteries. It was
inserted into the third and fourth parts of the duodenum in 53%,
and into the duodeno-jejunal flexure in addition in 40%. It was
innervated by non-myelinated fibres arising from the coeliac and
superior mesenteric plexuses. Although both the longitudinal and
circular muscle coats of the duodenum extended into the
suspensory muscle, it was not supplied by Auerbachs plexus.
The Hilfsmuskel, which is a slip of the diaphragm, is attached above
to the margin of the oesophageal hiatus and below to the
connective tissue in the region of the stem of the coeliac artery,
sometimes extending to the stem of the superior mesenteric artery.
The Hilfsrnuskel and the suspensory muscle of the duodenum are
separate entities.
The suspensory ligament usually inserts on the duodenojejunal flexure and
the third and fourth portions of the duodenum (see Fig. 8B). It may insert on
the flexure only (Fig. 8A) or on the third and fourth portions only (Fig. 8C).
There also may be multiple attachments (Fig. 80). In almost one fifth of cadavers,
the ligament is absent, apparently without associated symptom~.'~
The proximal half of the first part of the duodenum is completely covered
by peritoneum, but all the other parts are located retroperitoneally. The second
and third parts are overlapped by the head of the pancreas, so that a pancreatic
bare area of the duodenum is not covered by peritoneum. A second bare area
exists on the anterior surface of the second part of the duodenum where the
transverse colon is attached (Fig. 9). In patients with pancreatic cancer or pancreatitis, the pancreas and mesocolon, with its middle colic artery, become firmly
fixed. The anatomic entities responsible for duodenal fixation are the pylorus,
superior mesenteric vessels, ligament of Treitz, and peritoneum.

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of Treitz

Treitz

Treitz

Treitz

D
Figure 8. Four configurations of suspensory ligament (lig) of Treitz. A, Attachment to
duodenojejunal flexure. B, Attachments to flexure and third and fourth portions of duodenum. C,Attachments to only third and fourth portions. D, Multiple separated attachments
of suspensory ligament. (From Skandalakis JE, Akin JT Jr, Milsap JH Jr, et al: Vascular
compression of the duodenum. Contemporary Surgery 1O(part 2):33,1977; with permission.)

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ANDROULAKIS et a1

.,;

Pancreatic bare area

Figure 9. Bare areas of duodenum. Pancreas in intimate contact with duodenum along
concave surface. Attachment of transverse mesocolon produces additional bare area.
(From Skandalakis JE, Skandalakis LJ, Colborn GL, et al: The duodenum. Am Surg 55(part
2):291,1989; with permission.)

Parts of the Duodenum

First Part

The first (or ascending) part of the duodenum is 5 cm in length. The

proximal half is mobile; the distal half is fixed. The duodenum passes upward
from the pylorus to the neck of the gallbladder (Fig. 10). It is related posteriorly
to the common bile duct, portal vein, inferior vena cava, and gastroduodenal
artery; anteriorly to the quadrate lobe of the liver; superiorly to the epiploic
foramen; and inferiorly to the head of the pancreas.
The initial 2.5 cm is freely movable and is covered by the same two layers
of peritoneum that invest the stomach. The hepatoduodenal portion of the lesser
omentum attaches to the superior border of the duodenum; the greater omentum, to its inferior border. The distal 2.5 cm is covered with peritoneum only on
the anterior surface of the organ, so that the posterior surface is in contact with
the bile duct, portal vein, and gastroduodenal artery. The duodenum is separated
from the inferior vena cava by a small amount of connective tissue.
Second Part

The second (or descending) part of the duodenum is 7.5 cm in length. It

extends from the neck of the gallbladder to the upper border of L4. It is crossed
by the transverse colon and mesocolon and consists of a supramesocolic portion
and an inframesocolic segment. The parts above and below the attachment of
the transverse colon are covered with visceral peritoneum. The first and second
parts of the duodenum join behind the costal margin above and medial to the
tip of the ninth costal cartilage and on the right side of L1.
The second part of the duodenum forms an acute angle with the first part
and descends from the neck of the gallbladder anterior to the right kidney, right
ureter, right renal vessels, psoas major, and edge of the inferior vena cava. It is
related anteriorly to the right lobe of the liver, transverse colon, and jejunum.
At approximately the midpoint of the second part of the duodenum, the pancre-

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183

Figure 10. Relationships of duodenum and pancreas. lig = ligament. (From Skandalakis
JE, Skandalakis LJ, Colborn GL, et al: The duodenum. Am Surg 55(part2):291, 1989; with

permission.)
aticobiliary tract opens into its concave posteromedial side. The right side is
related to the ascending colon and right colic flexure.
Third Parl

The third (or horizontal) part of the duodenum is 10 cm in length. It extends

from the right side of L3 or L4 to the left side of the aorta. It begins about 5 cm
from the midline to the right of the lower end of L3 at approximately the level
of the subcostal plane. The third, or transverse, part passes to the left anterior
to the ureter, right gonadal vessels, psoas muscle, inferior vena cava, lumbar
vertebral column, and aorta and ends to the left of L3.
This inframesocolic portion of the duodenum is covered anteriorly by the
peritoneum. It is crossed anteriorly by the superior mesenteric vessels and, near
its termination, by the root of the mesentery of the small intestine. The third
part is related superiorly to the head and uncinate process of the pancreas. The
inferior pancreaticoduodenal artery lies in a groove at the interface of the
pancreas and duodenum. Anteriorly and inferiorly, this part of the duodenum
is related to the small bowel, mostly jejunum.
Fourth Part

The fourth (or ascending) part of the duodenum is 2.5 cm in length. It

extends from the left side of the aorta to the left upper border of L2. It is directed

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ANDROULAKIS et a1

obliquely upward, ending at the duodenojejunal junction at the left side of L2

at the root of the transverse mesocolon. This junction occurs at approximately 4
cm below and medial to the tip of the ninth costal cartilage. The fourth part is
related posteriorly to the left sympathetic trunk, psoas muscle, and left renal
and gonadal vessels. Its termination is close to the terminal part of the inferior
mesenteric vein, left ureter, and left kidney. The upper end of the root of the
mesentery also attaches here. The duodenojejunal junction is suspended by the
ligament of Treitz, a remnant of the dorsal mesentery, which extends from the
duodenojejunal flexure to the right crus of the diaphragm.

Pancreaticobiliary Structures

The fourth part (intramural) of the common bile duct passes obliquely
through the wall of the second part of the duodenum with the main pancreatic
duct (Wirsung). Other associated structures are the major and minor papillae,
the ampulla of Vater (if present), and the sphincteric mechanism of Boyden.
Together they form the Vaterian system of Dowdy.20This term expresses the
anatomic and surgical unity of these structures but has no functional significance.
The terminal portion of the common bile duct passing through the duodenal
wall is approximately 1.5 cm in length and narrows from 1.0 cm extramurally
to 0.54 cm at the papilla. The main pancreatic duct enters the duodenum caudal
to the bile duct, also decreasing in diameter. The ducts usually lie side by side
with a common adventitia for several millimeters. The septum between them
becomes reduced to a mucosal membrane before confluence is reached.
Major Duodenal Papilla

The major papilla is on the posteromedial wall of the second (descending)

part of the duodenum to the right of L2 or L3. It may lie at a slightly lower
level with increased age. The distance from the pylorus varies from 7 cm to 10
cm (range, 1.5-12.0 cm). The distance is decreased in the presence of inflammation of the cap or the postbulbar region of the duodenum.
Viewed from the mucosal surface, the papilla may be difficult to locate
because of the mucosal folds, being sometimes completely overlaid by a transverse fold of duodenal mucosa. Its oval or slitlike orifice lies at its tip, the
posterior tip of which is prolonged downward, and the posterior tip raises a
longitudinal fold, the plica longitudinalis (Fig. 11). The orifice is commonly filled
by villouslike projections called valvules or valvulae. A diverticulum lying near
the papilla may cause difficulty for surgeons or endoscopists.
Ampulla of Vater

The ampulla is a dilatation of the common pancreaticobiliary channel within

the papilla and below the junction of the two ducts (Fig. 12). If a septum is
present as far as the duodenal orifice, the ampulla does not exist (see Fig. 12).
MicheW9 reviewed the findings of 25 investigators of 2500 specimens and
concluded that an ampulla was present in 63%. By definition, an ampulla was
said to be present if the edge of the septum between the two ducts fell short of
the tip of the papilla. Measurements of the distance between the septa1 edge
and papillary tip range from 1 mm to 14 mm, with 75% being 5 mm or less.45

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185

Figure 11. T-arrangement of duodenal mucosal folds indicates site of major duodenal
papilla (major papilla is rarely this obvious). In some cases, a mucosal fold may cover
orifice of papilla. No such arrangement marks site of minor papilla. (From Skandalakis JE,
Skandalakis LJ, Colborn GL, et al: The duodenum. Am Surg 55(part 2):291, 1989; with
permission.)

Figure 12. Variations in relation of common bile duct and main pancreatic duct at duodenal
papilla. A, Minimal absorption of ducts into duodenal wall during embryonic development
(ampulla present). 6, Partial absorption of common channel (no true ampulla). C, Maximum
absorption of ducts into duodenum. Separate orifices on papilla (no ampulla). (From
Skandalakis JE, Skandalakis LJ, Colborn GL, et al: The duodenum. Am Surg 55(part
2):291, 1989; with permission.)

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ANDROULAKIS et a1

Purists would require a dilatation of the common channel to apply the term
ampulla. Where the common channel is less than 5 mm long, little or no dilatation
is present.'* In such specimens, the presence of a true ampulla becomes a matter
~ ~ the following
of opinion (see Fig. 12). The authors agree with M i ~ h e l sthat
classification is the most useful.

Type 1-The pancreatic duct opens into the common bile duct at a variable
distance from the opening in the major duodenal papilla. The common
channel may or may not be dilated (85%).
Type 2-The pancreatic and bile ducts open close to one another but
separately on the major duodenal papilla (5%).
Type 3-The pancreatic and bile ducts open into the duodenum at separate points (9%).
A true dilated ampulla is present in approximately 75% of individuals with
type 1 and is absent in individuals with type 2 or 3.
This variation in the distance between the pancreaticobiliary junction and
the duodenal lumen is the result of developmental pr0cesses.4~In the embryo,
the main pancreatic duct arises as a branch of the common bile duct, which in
turn arises from the duodenum. Growth of the duodenum absorbs the proximal
bile duct up to its junction with the pancreatic duct. When the resorption is
minimal, a long ampulla is present and the junction of the ducts is high in the
duodenal wall (type 1)or extramural. With increased resorption of the terminal
bile duct, the junction lies closer to the duodenal orifice and the ampulla is
shortened. The maximum resorption results in separate orifices for the main
pancreatic duct and the common bile duct (type 3).
Sphincter of Boyden

Like the papilla of Vater, the sphincter of Oddi at the duodenal end of the
pancreatic and common bile ducts is misnamed. By priority of description, it
should have been named after Glisson (1654),24who described annular fibers
around the whole of the intramural portion of the bile duct and believed that
they guarded the opening against reflux of duodenal contents (Glisson's account
of his work is found in the article by BoydenI4).A complex of several sphincters
is composed of circular or spiral smooth muscle fibers around the intramural
part of the common bile duct, the main pancreatic duct, and the ampulla, if
present. This sphincteric complex has been named the sphincter of B0yden.2~
The muscle fibers have an embryonic origin separate from that of the duodenal
muscularis and are functionally separate from it (Fig. 13).
Minor Duodenal Papilla

The minor papilla, through which the accessory pancreatic duct of Santorini
opens, is approximately 2 cm cranial and slightly anterior to the major papilla.
It is smaller and less easily identified than is the major papilla. The most useful
landmark is the gastroduodenal artery, under which lies the accessory duct and
the minor papilla. Duodenal dissection for gastrectomy should end proximal to
the artery.
The minor papilla may contain no duct or only a microscopic, tortuous
channel. Valverde Barbato de Prates et a156report that the sphincter of the minor
papilla of the duodenum is not a typical anatomic sphincter because the muscular and elastic fibers have a peculiar contraction that causes the orifice to open

EMBRYOLOGIC AND ANATOMIC BASIS OF DUODENAL SURGERY

187

Figure 13. Four sphincters comprise the sphincter of Boyden: superior choledochal ( l ) ,
inferior choledochal (2),sphincter ampullae (papillae) (3), and pancreaticus (4).(From
Skandalakis JE, Skandalakis LJ, Colborn GL, et al: The duodenum. Am Surg 55(parl

T Surgical anatomy of the pancreas. In Carey LC

2):291, 1989; and data from White l
(ed):The Pancreas. St. Louis, Mosby, 1973, p 12; with permission.)

and permit pancreatic juice into the duodenum. A true sphincter of Helly is
rarely present.
In approximately 10% of individuals, the duct of Santorini is the only duct
draining most of the pancreas. Accidental ligation of this duct, together with the
gastroduodenal artery, results in catastrophic pancreatitis.
Duodenal Sphincters

The authors' knowledge about duodenal sphincters was obtained from

The 'Sphincters' of the
the excellent book by Didio and A n d e r s ~ n ' entitled
~
Digestive System.
If the well-known gastroduodenal pyloms is ignored, the duodenum has
the following sphincters, which are a matter of controversy.

The first duodenal sphincter is said to be located at the distal end of the
duodenal bulb and is perhaps related to, if not responsible for, segmental
achalasia and "megabulb."
The supra-Vaterian sphincter, described by Villemin,5*.59 is proximal to
the ampulla of Vater.
The so-called "Ochsner muscle" probably is located, if it exists, below
the ampulla of Vater. O c h ~ n e presented
r~~
his findings in 1906. As early as
1907, Boothby13 doubted the existence of this sphincter.

188

ANDROULAKIS et a1

A sphincter just proximal to the duodenojejunal flexure was also described by both O c h ~ n e and
r ~ ~Villemin.58,59

In the introduction to his book about Scarpa, M0nti41 stated that, like the
poet, and perhaps even more so, the scientist is the product of the period in
which he lives. Och~ner:~Boothby,13 and Villemin58,59 worked in a time that
stimulated them to perform their investigative work. The authors agree with
Didio and A n d e r s ~ n that
~ the descriptions of the sphincteric component are
vague, and their clinical significance, none.
Vascular Supply of the Duodenum

The blood supply of the duodenum is confusing because of origin, distribution, and individual variations (Figs. 14-16). This is especially true of the blood
supply of the first portion of the duodenum. In his excellent presentation
about the stomach and duodenum, GriffithZ5is cautious. Akkinis5 states that no
collateral circulation exists beyond the terminal arcades of the small boweL5
Does the same phenomenon exist in the first portion of the duodenum? Does
the anemic spot of Mayo that corresponds to the distribution of the supraduodenal artery exist? Do the variations of the above named arteries represent, as
GriffithZ5states, an underlying factor in necrosis and leakage? The authors do

Supraduodenal a.
roduodenal a.

Figure 14. Major arterial supply to duodenum. SMA= superior mesenteric artery. a = artery.
(From Skandalakis JE, Skandalakis LJ, Colborn GL, et al: The duodenum. Am Surg 55(parl
2):291, 1989; with permission.)

EMBRYOLOGIC AND ANATOMIC BASIS OF DUODENAL SURGERY

189

Ant
Post
i inf
pancreoticoduodenal o

Common hepatic a

Figure 15. Anterior (ant) (A) and posterior (post) (B)arterial supply of duodenum and
pancreas. Post = posterior; a = artery; inf = inferior; sup = superior; n = nerve. (From Skandalakis JE, Skandalakis LJ, Colborn GL, et al: The duodenum. Am Surg 55(part 2):291, 1989;
with permission.)

not want to take a position. Their only advice is to use good surgical technique
and not an overenthusiastic approach for benign disease.
The first part of the duodenum is supplied by the supraduodenal artery
and the posterosuperior pancreaticoduodenal (PSPD) branch of the gastroduodenal artery (retroduodenal artery of Edwards, Michel, and Wilkie), which is a
branch of the common hepatic artery. In many individuals, the upper part of
the first 1 cm is also supplied by branches of the right gastric artery. After giving
origin to the PSPD and supraduodenal branches, the gastroduodenal artery
descends between the first part of the duodenum and the head of the pancreas

190

ANDROULAKIS et a1

and terminates by dividing into the right gastroepiploic and anterosuperior

pancreaticoduodenal arteries, both supplying twigs to this part of the duodenum.
Bianchi and AlbaneseIz studied the supraduodenal artery in 30 specimens.
It was present in 28 specimens; the right gastric artery served as a substitute in
the two cases in which it was absent. The supraduodenal artery was distributed
to the distal two thirds of the proximal duodenum, extending to the supraduodenal and retroduodenal parts of the common bile duct. In 50% of cases, the artery
anastomosed with the right gastric and PSPD arteries.
The remaining three parts of the duodenum are supplied by an anterior
and a posterior arcade. From the arcades spring pancreatic and duodenal
branches. Those supplying the duodenum are called arteriae rectae; they may be
embedded in the substance of the pancreas.
Four arteries contribute to the pancreaticoduodenal vascular arcades: (1)
anterior superior pancreaticoduodenal arteries, commonly two, arising from
the gastroduodenal artery on the ventral surface of the pancreas; (2) PSPD
(retroduodenal) artery, usually passing in front of the common bile duct and
descending on the posterior surface of the pancreas, then crossing behind the
bile duct and joining the posterior branch of the inferior pancreaticoduodenal
artery; and ( 3 ) anteroinferior and (4) posteroinferior pancreaticoduodenal arteries, arising from the SMA or its first jejunal branch separately or from a common stem.
Blood reaches the concave surface of the duodenum by the vasae rectae
from the pancreaticoduodenal arcades. At first supplying the muscularis externa,
they form a large plexus in the submucosa, from which arteries pierce the
muscularis mucosae and form a second rich plexus just beneath the epithelium
of the villi. Surgeons should ligate only one of the two arcades, superior or
inferior only.

Vascular Drainage of the Duodenum

Veins of the lower first part of the duodenum and the pylorus usually open
into the right gastroepiploic veins (Fig. 16). They are the subpyloric veins. The
upper first part of the duodenum is drained by suprapyloric veins, which open
into the portal vein or the PSPD vein. Anastomoses between the subpyloric and
suprapyloric veins pass around the duodenum. One of these has been said to
mark the site of the pylorus (prepyloric vein of may^).^^ It is not a constant
indicator of the location of the pylorus.
The venous arcades draining the duodenum follow the arterial arcades and
tend to lie superficial to them. The anterosuperior vein drains into the right
gastroepiploic vein, whereas the posterosuperior vein usually passes behind the
common bile duct to enter the portal vein. Takamuro et a152report that the PSPD
vein runs posteroinferior to the common bile duct without the accompaniment
of the artery in 71.1% of specimens. Several tributaries of veins draining the
second and third parts of the duodenum formed the so-called dorsal pancreatic
vein in 28.9% of specimens. The inferior veins can enter the superior mesenteric,
inferior mesenteric, splenic, or first jejunal vein. The veins may terminate separately or by a common stem.

Lymphatic Drainage of the Duodenum

The duodenum is richly supplied with lymphatics (Fig. 17). They originate
as blind ending vessels (i.e., lacteals) in each villus of the mucosa. These vessels

EMBRYOLOGIC AND ANATOMIC BASIS OF DUODENAL SURGERY

Ant &Post
sup. pancreaticoduodenal v

Spleen

f mesenreric v

Ant
pancreatic0
venous

Sup rnesenterc v

R qastroepiploic

191

Ant 8 Post
inf pancreaticoduodenol v
a

Figure 16. A, Anterior (ant) view of venous drainage of duodenum and pancreas. 13,
Posterior (post) view of venous drainage. Formation of hepatic portal vein. (From Skandalakis JE, Skandalakis LJ, Colborn GL, et al: The duodenum. Am Surg 55(part 2):291, 1989;
with permission.)

form a plexus in the lamina propria and, piercing the muscularis mucosae, form
a second submucous plexus. Another lymphatic lies between the circular and
longitudinal layers of the muscularis. Collecting trunks pass over the anterior
and posterior duodenal walls toward the lesser curvature to enter the anterior
and posterior pancreaticoduodenal lymph nodes.
The anterior extramural collecting ducts drain to nodes anterior to the
pancreas and the posterior pass to nodes posterior to the head of the pancreas.
These follow the veins and arteries to nodes related to the SMA. In other words,
the duodenal lymphatics have two pathways: (1) one up to the hepatic nodes
and (2) another down to the nodes in the vicinity of the origin of the SMA.

192

ANDROULAKIS et a1

Hepatic

I 1I

I(

,)L-

// 4

::

''

Pancreaticoduodenal

?reaortic
nodes

Figure 17. Duodenal lymphatics. Direction of flow (arrows). A 0 = abdominal aorta; IVC = inferior vena cava. (From Skandalakis JE, Skandalakis LJ, Colborn GL, et al: The duodenum.
Am Surg 55(pari 2):291,1989; with permission.)

In 1907, Bartels7 presented evidence that valves of lymphatic vessels connecting the duodenal wall with the head of the pancreas are arranged so that
normal lymph flow is from pancreas to duodenum and not the reverse. This has
not been recently confirmed. Although the lymphatics of the pancreas have
received some attention, those of the duodenum have received little.

Nerve Supply of the Duodenum

Within the duodenal wall are two plexuses, each of which is composed of
groups of neurons connected by a network of fibers. The neuronal cell bodies in
the plexuses are assumed to be postganglionic parasympathetic. The plexus of
Meissner is in the submucosa, and the plexus of Auerbach is in the connective
tissue between circular and longitudinal layers of muscularis externa. These
plexuses contain preganglionic parasympathetic fibers carried initially by the
vagus nerves, and sympathetic postganglionic fibers from cell bodies located in
the celiac and superior mesenteric plexuses. Duodenal nerves may also arise
from the anterior hepatic plexus close to the origin of the right gastric artery. In
6 of 100 specimens examined by the authors, nerves from the hepatic division
of the anterior vagal trunk gave rise to one or more branches that innervated.
the first part of the duodenum.50In most specimens, such branches could be
traced only to or above the gastric incisura. The vagaries of the vagus are
well known.51

EMBRYOLOGIC AND ANATOMIC BASIS OF DUODENAL SURGERY

193

SURGICAL APPLICATIONS
First Part

The authors are skeptical about the blood supply to this area. Good technique, conservative skeletonization, and good anatomic knowledge produce
good results with surgical procedures in this area.

Second Part
The duodenum is one of the most difficult areas to approach during surgery
because of the fixation of the duodenum and pancreas, the common blood
supply for both organs (i.e., the superior and inferior pancreaticoduodenal
arcades), and the opening of the common bile and pancreatic ducts. In patients
with malignant disease, a pancreaticoduodenectomy should be performed, but in
patients with benign disease, a more conservative approach, such as segmental
resection, is the preferred treatment.
Kimura and Nagai**did not find the anterosuperior, anteroinferior, posterosuperior, posteroinferior, or pancreaticoduodenal arteries, or their branches to
the duodenal wall, common bile duct, or ampulla of Vater to be buried into the
pancreatic parenchyma, which suggests that the pancreas can be dissected from
the duodenum. They reported that dissection at the accessory papilla was difficult and that dissection of the pancreas from the common bile duct and identification of the main pancreatic duct were straightforward. Kimura and Nagaiz8
concluded that the blood supply of the duodenum may be protected and that
the head of the pancreas may be removed.
Third Part

The proximal one third is difficult to deal with because of its association
with the head of the pancreas and the uncinate process. Surgeons should remember the superior mesenteric vessels; transverse mesocolon, with its marginal
artery and the middle colic artery; and inferior mesenteric artery, which, in most
cases, is covered by the third portion of the duodenum. Surgeons should proceed
slowly with the uncinate process, which is closely related to the superior mesenteric vessels. Many small vessels originate from the inferior pancreaticoduodenal
arcades, and small twigs from the SMA are present.
Fourth Part

The fourth part of the duodenum is related to two anatomic entities of

importance: (1)the ligament of Treitz and (2) the inferior mesenteric vein, located
to the left of the paraduodenal fossae. Surgeons should use the fourth part to
begin the exploration of the distal duodenum (third and fourth parts) and
remember that mobilization of the right colon and transection of the ligament
of Treitz are necessary for good exposure of the distal duodenum. The blood
supply here originates from the divisions of the intestinal branches of the SMA
and is similar to that of the rest of the small bowel. The arteries are without
collateral circulation and with least efficient blood supply in the antimesenteric border (the duodenum does not have a mesentery; the middle of the

194

ANDROULAKIS et a1

anterior wall, which is covered by peritoneum, should be considered "antimesenteric").

EXPOSURE OF THE DUODENUM

Exposure of the duodenum may be necessary in a search for traumatic

injury, for pancreatic procedures, for exploration of the distal common bile duct,
for section of the suspensory ligament to relieve duodenal compression, or to
reduce a redundant proximal loop of a gastrojejunostomy above the transverse
mesoc01on.~~
The following maneuvers provide the needed exposures.

Mobilization of the second and proximal third parts of the duodenum

is obtained by incising the parietal peritoneum along the descending
duodenum (second part) and retracting it medially; this is the Kocher
maneuver (Madden34states that this procedure should bear the name of
Jourdain, who described it in 1895). This maneuver permits examination
of the posterior wall of the duodenum and exploration of the retroduodenal and pancreatic portions of the common bile duct.
Exposure of the third portion of the duodenum, proximal to the superior
mesenteric vessels, may be obtained by an incision through the transverse
mesocolon, an incision through the gastrocolic omentum, or reflection of
the right half of the
Exposure of the duodenum distal to the superior mesenteric vessels may
be accomplished by incision through the gastrocolic omentum and further
reflection of the right colon. In addition, division of the parietal fold just
inferior to the paraduodenal fossa permits the visualization of the distal
duodenum. Further mobilization of the duodenum can be obtained by
transection of the suspensory muscle.17Laparoscopic severance of the
ligament of Treitz is recommended for the treatment of SMA syndrome.35
Transection of the ligament of Treitz and complete evaluation of the distal
duodenum are advised for the location of blunt inj~ries.5~

SUMMARY

The following points should be remembered by surgeons (Table 1).

In writing about the head of the pancreas, the common bile duct, and the
duodenum in 1979, the authors49stated that
Embryologically, anatomically and surgically these three entities
form an inseparable unit. Their relations and blood supply make it
impossible for the surgeon to remove completely the head of the
pancreas without removing the duodenum and the distal part of
the common bile duct. Here embryology and anatomy conspire to
produce some of the most difficult surgery of the abdominal cavity.
The only alternative procedure, the so-called 95% pancreatect~my,~~
leaves a rim of pancreas along the medial border of the duodenum
to preserve the duodenal blood supply.
The authors had several conversations with Child, one of the pioneers of
this procedure, whose constant message was to always be careful with the

EMBRYOLOGIC AND ANATOMIC BASIS OF DUODENAL SURGERY

195

Table 1. ANATOMIC COMPLICATIONS OF DUODENAL, GASTRIC, AND PANCREATIC

PROCEDURES
Procedure

Gastrectomy
a. total
b. proximal
c. distal with or
without vagotomy

Vascular Injury

Organ Injury

Hemorrhage, ischemia,
or necrosis
a. distal esophagus
b. gastric remnant
c. duodenal cuff

Spleen, liver,
mediastinal pleurae,
pericardium, cisterna
chyli, esophagus,
gastric remnant
necrosis, omental
infarction, common
bile duct, pancreas,
colon
Pyloroplasty
Hemorrhage, leakage of Pancreas, common bile
suture line
duct
Pyloromyotomy
Hemorrhage
Duodenum
Vascular compression of Aorta, superior
Colon, duodenum,
duodenum
mesenteric artery and
jejunum
vein, inferior
mesenteric artery and
vein, middle colic
artery, small vessels in
suspensory muscle
Exploration of proximal Right gastric artery,
Common bile duct,
duodenum
gastroduodenal artery,
pancreas, colon, right
pancreaticokidney
duodenal arcades,
superior mesenteric
artery and vein,
inferior vena cava,
aorta
Exploration of distal
As above and inferior
As above and jejunum
duodenum
mesenteric vein
Paraduodenal herniae
Superior mesenteric
Pancreas, colon, jejunum
artery and vein,
inferior mesenteric
vein
Pancreaticoduodenostomy and
pancreaticojejunostomy

As above

As above

Inadequate Procedure

Incomplete vagotomy,
inadequate gastric
resection, small
stoma, antral
remnant, anastomotic
leakage, duodenal
blow-up secondary to
obstruction
Small stoma
Small stoma
Failure to sever
ligament of Treita

Failure of good
mobilization with
multiple sequelae

As above
Inadequate closure of
hernia ring,
overenthusiastic
closure of hernia ring
with mesenteric vessel
involvement
As above

From Skandalakis LJ, Pemberton LB, Gray SW, et al: The duodenum: Part 4. Surgery. Am Surg
55:492, 1989; with permission.

blood supply of the duodenum (personal communication, 1970). Beger et

als, popularized duodenum-preserving resection of the pancreatic head,
emphasizing preservation of endocrine pancreatic function.yThey reported
that ampullectomy (removal of the papilla and ampulla of Vater) carries
a mortality rate of less than 0.4% and a morbidity rate of less than 10.0%."
Surgeons should not ligate the superior and inferior pancreaticoduodenal
arteries because such ligation may cause necrosis of the head of the
pancreas and of much of the duodenum.
The accessory pancreatic duct of Santorini passes under the gastrointestinal artery. For safety, surgeons should ligate the artery away from the
anterior medial duodenal wall, where the papilla is located, thereby
avoiding injury to or ligation of the duct. "Water under the bridge"
applies not only to the relationship of the uterine artery and ureter but

196

ANDROULAKIS et a1

also to the gastroduodenal artery and the accessory pancreatic duct. In

10% of cases, the duct of Santorini is the only duct draining the pancreas,
so ligation of the gastroduodenal artery with accidental inclusion of the
duct is catastrophic.
With the Kocher maneuver, surgeons reconstruct the primitive mesoduodenum and achieve mobilization of the duodenum, which is useful for
some surgical procedures.
Surgeons should not skeletonize more than 2 cm of the first part of the
duodenum. If more than 2 cm of skeletonization is done, a duodenostomy
using a Foley catheter may be necessary to avoid blow-up of the stump
secondary to poor blood supply. Proximal duodenojejunostomy is advised
for the safe management of patients with difficult duodenal sturnps.l5
Roux-en-Y choledochojejunostomy and duodenojejunostomy divert bile
and food in the treatment of the complicated duodenal divertic~lum.~~
The suspensory ligament may be transected with impunity. It should be
ligated before being sectioned so that bleeding from small vessels contained within can be avoided. Failure to sever the suspensory muscle
completely, which is possible if the insertion is multiple, fails to relieve
the symptoms of vascular compression of the duodenum (Fig. 18).

Figure 18. Section of suspensory ligament usually lowers duodenum two finger-widths
below origin of superior mesenteric artery. (From Akin JT Jr, Milsap JH Jr, Gray SW, et al:
Vascular compression of the duodenum. Contemporary Surgery lO(part 3):52,1977; with
permission.)

EMBRYOLOGIC AND ANATOMIC BASIS OF DUODENAL SURGERY

197

Mobilization, resection, a n d end-to-end anastomosis of the duodenal flexu r e have been performed a s a uniform surgical procedure, avoiding the
conventional g a s t r o j e j u n o ~ t o m y . ~ ~
With a large, penetrating posterior duodenal o r pyloric ulcer, surgeons
should remember that
The proximal d u o d e n u m shortens because of the inflammatory process
(duodenal shortening)
The anatomic topography of the distal common bile d u c t and the
opening of the d u c t of Santorini a n d t h e ampulla of Vater is distorted
Leaving t h e ulcer i n situ is wise
Careful palpation for o r visualization of the location of the ampulla of
Vater or common bile d u c t exploration w i t h a catheter insertion into
the common bile d u c t and the d u o d e n u m are useful procedures
In most cases, the common bile d u c t is located t o the right of the gastroduodenal artery a t the posterior wall of the first p a r t of t h e d u o d e n u m . In
m a n y cases, the artery crosses the supraduodenal p a r t of the common bile
d u c t anteriorly or posteriorly, a phenomenon also observed with the PSPD
artery, which crosses the common bile d u c t ventrally a n d dorsally.
Duodenal hamartoma of Brunner s glands h a s been treated b y laparoscopic excision.2
The authors recommend the article by Rabenstein e t a144a n d the editorial
by. Baillie6 for a balanced view of the benefits and risks of needle-knife
papillotomy for diagnostic and therapeutic procedures.

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John E. Skandalakis, MD, PhD
Centers for Surgical Anatomy and Technique
Emory University School of Medicine
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