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The prenatal development of the pancreatic and extra-hepatic ducts in the Canadian porcupine (Erethizon dorsatum).

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Department o f Zoology, Syraovse University, New Yorlc
The form and arrangement of the extrahepatic and pancreatic ducts in adult mammals have been widely investigated.
IJsually the common bile duct joins the duodenum a short distance from the pylorus, into which it pours bile collected from
the tributary hepatic ducts. I n most mammals a gall bladder
and cystic duct form a part of the hepatic system, but a surprising number of mature birds and mammals possess no gall
bladder (Gorhani and Ivy, ’38). The pancreatic ducts commonly consist of the main pancreatic duct (Wirsung’s duct)
and the accessory duct (Duct of Santorini). The latter is
absent in some mammals. Wirsung’s duct may empty directly
into the duodenum, or at various levels into the common bile
duct, or may be absent, as in the adult guinea pig.
The ontogenetic development of these structures has been
studied in many vertebrates, including several primates, herbivorous mammals, carnivores, and among the rodents, the
mouse, rat, ground squirrel, and guinea pig. These investigations disclose the major developmental processes, but there
still remain obscure questions relating to the underlying agencies which cause some of the structural conditions found in
adult animals.
An ontogenetic study of the pancreatic and bile ducts in the
Canadian porcupine (Erethizon dorsatum) adds additional
information on the prenatal development of these structures.
THE A N A T O M I C A b RECORD, VOL. 81. NO. 2
This mammals belongs to the Hystricomorpha, rodents of
which little is known beyond the fact that they have a defensive
covering of quills, and thrive on a diet consisting mainly of
tree bark and wood. The intestinal tract of the porcupine
shows striking adaptations for assimulating this type of food.
I n addition to the caecum, which has a capacity of about 1 quart
of food material, the tract of an adult also includes 25 feet
of intestine, of which considerably over one-half consists of
small intestine. The pancreas is an elongated slender gland,
its single duct (Santorini) inserting on the duodenum about
16 inches (40em.) from the pylorus. A gall bladder is absent
and the common bile duct inserts close t o the pylorus, usually
less than 1inch distant.
The absence of both a gall bladder and a ventral pancreatic
duct in the adult porcupine presents a structural arrangement
not previously reported. This condition, plus the uniformly
ribbon-like shape of the pancreas, its distally inserted duct
and the specialized intestinal canal, offer an incentive for the
investigation of the developmental anatomy which precedes
this post-natal plan.
Fifty-seven adult porcupines were used in this study. I n
ten specimens the hepatic ducts were injected with starch
solution and the pancreatic duct with India ink. The embryological material consisted of the following histological series.
28-12- 4
38-12- 1
28-12- 7
25-12- 7
27-12- 7
27-12- 5
27-12- 9
2.5-12- 2
28-12- 6
38-12- 6
LENGTH ( C . R.)
2.4 mm.
Graphic reconstructions of the enteric canal, including the
pancreatic and extra-hepatic ducts, were prepared for several
stages, Micro-dissections were made of a 35 mm. (37-12-19),
a 50 mm. (27-12-4) and an 85 mm. (38-1-1) embryo to expose
the ducts. Models were made of the region in question for the
4 mm., 6.5 mm., 9 mm., 13.5 mm., 14.5 mm., 16.5 mm., 19 mm.,
and the 25 mm. stages. Many photomicrographs were taken
to facilitate tlie studies.
To gain a first hand knowledge of the relationship of these
structures in other mammals the writer examined histological
series and post-natal specimens of the cat, guinea pig, field
mouse, deer mouse, cottontail rabbit and human.
2.4-mm. embryo. I n this initial stage the liver diverticulum
appears as a shallow groove on the ventral surface of the foregut in the region of the stomach. This groove lies between the
paired vitelline veins, and from its thick side walls short
trabecular sprouts may be seen. No rudiment of the pancreas
can be identified in this stage. The fore-gut has become tubular
for a considerable distance caudal to the groove.
4-mm. embryo (fig. 1 ) . The hepatic outgrowth appears as a
low knob-like structure, arising from the floor of the fore-gut
in the region of the stomach enlargement. The posterior wall
of the diverticulum, identified as the pars cystica (P.c.),has
a smooth unbroken outer surface, while the walls of the remainder, or pars hepatica (P.h.) are continuous with developing trabeculae ( The dorsal pancreas appears at a
slightly more caudal position on the dorsal surface of the foregut as a laterally compressed elevation (P.d.). At this stage
the primordium of the lung (Lg.d.) can be recognized, the
enteric canal is nearly straight and the yolk sac is constricted
to a narrow stalk joining the gut.
6.5-mm. embryo (fig.2). I n this stage the liver outgrowth
and the dorsal pancreas lie in nearly the same dorso-ventral
plane, caudal to the stomach. The two structures differ greatly
in shape. The dorsal pancreas (P.d.) is a thick straight column
directed dorsally and it is solid in the distal three-quarters of
Fig. 1 Side view of the fore-gut in a 4-mm. embryo.
Fig. 2 Side view of the pyloric region in a 6.5 mm. embryo.
its length. At its extremity rudiments of pancreatic cords iriay
be seen ( The dorsal pancreas lies just anterior to the
annulus venosus caudalis and is to a large extent surrounded
by the vein (fig. 7). The liver anlagen is directed anteroventrally as a narrow stalk which expands into a bulbous extremity. The stalk, or ductus choledochus (D.c.), has a very
small lumen, while the bulbous portion is hollow, forming a
sizable cavity. The pars cystica reaches its greatest development at this stage, forming a pronounced bulge in the posterior
wall (P.c.). From the thick-walled pars hepatica (P.h.) a
profusion of hepatic trabeculae are developing ( There
are no outgrowths on the liver diverticulum or on the duodenum, indicating the presence of a ventral pancreas. Midway
between the ductus choledochus and the cloaca, the yolk stalk
appears to draw the intestine toward the abdominal wall, thus
giving the gut a low V-shaped curve (fig.5A).
8-nznz. embryo. The stomach has now rotated 60 degrees to
the left, causing the hepatic diverticulum and the dorsal pancreas to be directed somewhat to the right and the left respectively. The dorsal pancreas inserts on the duodenum at a
distinctly more caudal level than the ductus choledochus. Its
distal half is still solid. The pars hepatica of the liver outgrowth has become elongated, and its terminal portion divides
into two slight protuberances from which the trabeculae
sprout. The pars cystica bulges less than in the 6.5-mm. stage.
9-mrn. cmbryo (fig. 3). This embryonic series shows a
marked lengthening of the gut (fig. 5B). The apex of the
intestinal loop, noted in the 6.5-mm. stage, has now reached
the abdominal wall. The stomach has rotated furthcr to the
left and the ductus choledochus is directed forward and to the
right from its insertion on the duodenum, distal to the pplorus
( D.c.). I n this stage the liver diverticulum is Y-shaped (fig. 8).
The two limbs of the forked extremity are directed laterally
and each possesses a well developed lumen (P.h.). The endothelium covering the end of each limb is thickened and is
continuous with the trabeculae of the gland. A slight outpocketing on the right limb is identified as the much reduced
pars cystica (PA.).The dorsal pancreas now joins the duodenum nearly midway between the insertion of the bile duct
and the duodenal flexure (fig. 5B),although, due t o a lengthening of the diverticulum, its terminal portion (P.d.) retains its
same primitive relation to the liver outgrowth. The pancreatic
outgrowth inserts on the dorso-lateral surface of the duodenum
and bends forward, lying between the intestine and the portal
vein. There is no indication of a ventral pancreas.
Fig. 3 Ventral view of the pylorie region in a 9-mm. embryo.
10-mm. and 12-nzm. embryos. In these two series no new
structural developments occur. A pars cystica can no longer
be identified. The trabeculae of the liver multiply rapidly,
while those of the pancreas develop at the extremity of the
diverticulum and near its insertion on the duodenum.
13.5-mm. embryo (fig. 4). The intestinal loop has begun to
rotate on the superior mesenteric artery and its terminal portion protrules outside the abdomen. The liver occupies a large
part of the visceral cavity, the stomach lies well to the left,
while the duodenum crosses the abdomen in a transverse plane
and then arches caudally in a U-shaped bend to the base of the
anterior limb of the intestinal loop. No appreciable change of
position has altered the insertion of the bile duct (D.c.), but
the pancreatic duct (D.p.) inserts on the duodenum close to
Pig. 4 Ventral view of the biliary and pancreatic insertions on the duodenum
in a 13.5-mm. embryo.
the base of the anterior limb of the intestinal loop, and is
directed cranially. This change of direction is not due to any
tortion of the duodenum, but it is caused by the U-shaped
bending of the gut. A short distance from its insertion the
primordiuni of the pancreas gives rise to a small cluster of
pancreatic cords. As the duct skirts through the restricted
space between the portal vein and duodenum no cords sprout
off, but beyond the vein, and bordering the stomach, the duct
joins another mass of pancreatic cords (P,tr.). The ductus
choledochus divides distally into a left limb having three
branches and a slightly larger right limb which bears two
branches (D.c.). The cells forming the wall of the bile duct,
facing the pancreas, are irregularly placed and the surface is
marked by tiny elevations (fig. 9).
14.5-mrn. embryo. This stage resembles closely the preceding. One structural condition, observed only in this embryo,
is a pair of buds arising from the duodenum, one dorsal and
the other ventral to the insertion of the bile duct. The ventral
outgrowth is much the longer, it has a lumen, and runs parallel
with the bile duct. Neither have any associated trabeculae nor
are they connected with either the hepatic or pancreatic ducts.
The dorsal pancreas now inserts on the duodenum at the sharp
flexure marking the base of the anterior limb of the intestinal
loop (fig. 5C). This flexure lies adjacent to the primitive
urinary bladder.
15.5-mm. embryo. The close relationship between the ductus
choledochus (D.c.) and the portion of the dorsal pancreas
(P.d.) lying craniad to the portal vein (P.v.) is shown in the
accompanying photomicrograph (fig. 10). I n most mammals
a ventral pancreas is also found in this region. The small
elevations on the bile duct, seen in the 13.5-mm. stage, arc
observed again in this embryo.
16.5-mm. embryo. Both limbs of the intestinal loop are
lengthening rapidly, resulting in numerous coils which crowd
against the proximal portion of the duodenum pushing it
forward and to the right. Using the primitive urinary bladder
as a landmark, it will be seen that the insertion of the dorsal
pancreas on the duodenum, at the base of the anterior limb
of the intestinal loop, now lies at a higher antero-posterior
level than in the 14.5-mm. stage. The pancreatic cords have
developed an extensive lumen and the portion of the duct,
bordering the portal vein, has given rise to a compact mass
of cords.
27-mm. embryo. This embryo shows the same structural
features observed in the previous stage.
19-mm. embryo. Due to the rapid growth of the intestinal
tract, the duodenum has been crowded anteriorly so that the
duodenal flexure, marking the insertion of the dorsal pancreas,
lies on the extreme right and nearly on the same antero-
Fig. 5 The enterie canal in side view: A, 6.5-mm. ; B, g-mm., and C, 14.5-mm.
posterior level as the pylorus. The intestinal loop now lies
entirely within the abdomen. The dorsal pancreas consists of
a large group of cords lying in the lesser omentum adjacent
to the stomach, another elongated mass of cords near the
insertion, and a thin ribbon of cords which occupies the restricted space between the portal vein and the duodenum. The
extrahepatic ducts show no pronounced change from the condition observed in the 13.5-mm. stage.
25-mm. embryo. Further growth of the enteric canal causes
the fundus of the stomach to occupy a position against the left
abdominal wall, with its long axis parallel with the primary
axis of the body. The pyloi-ic stomach passes cranially and to
the right, while the U-shaped proximal portion of the duodenum now tips caudally, with its outer rini lying against the
right abdominal wall. These readjudtments have not effected
the position of the extrahepatic ducts. As a result of changes
in the position of the intestinal coils the right half of the
pancreas and its insertion on the duodenum lie more caudally.
The pancreatic duct is now directed anteriorly and to the left
from its insertion. A tortion in the proximal U-shaped portion
of the duodenum, first noted in the 16.5-nim. stage is still
50-mm. embrgo (fig. 6). The liver and pancreas, including
their ducts, are similar in position and structure to the respective organs found in the adult porcupine. The pancreas extends anteriorly and to the left from its insertion, passes dorsal to the bile duct and terminates in the lesser omentum
(P.d.). The hepatic ducts converge into two main trunks which
unite to form the common bile duct (D.c.). The bile duct still
inserts on the duodenum close to the pylorus.
Adult porcupine. Although the definitive plan of structure
of the pancreatic and hepatic ducts is complete in the 50-mm.
stage, it is desirable to record certain measurements of the
adult structures and relationships. The average weight of
seventy-three adult breeding females was 5900 gm. (13 pounds),
while forty-two adult males had an average weight of 7121 gm.
(15.7 pounds). Measurements of the common bile duct gave
an average diameter of 3 mm. and an average length of 27 mm.
The distance between the pylorus and the insertion of the
common bile duct on the duodenum averaged 24 mm. The
distance between the insertions of the common bile duct and
the pancreatic duct averaged 4336 mm. (17 inches) in the
male, and 3697 mm. (14.5 inches) in the female.
Fig. G
Ventral view of the biliary and pancreatic insertions in a 50-mm. embryo.
At all stages in the ontogeny of the porcupine the insertion
of the ductus choledochus on the duodenum is at a higher level
than the insertion of the pancreatic duct. I n its initial position
the liver diverticulum lies partly in the ventral wall of the
stomach enlargement, while the diverticulum of the dorsal
pancreas forms somewhat caudal to the primitive stomach.
The insertion of the common bile duct relatively close t o the
pylorus is a relationship formed early in prenatal development and retained in the adult. A similar relationship has
been reported to occur in the rabbit, guinea pig and striped Mann, Brimwall and Foster ( '20). Boyden ( '32)
suggests two factors which may influence such a close relationship between the bile duct and the pylorus. If the liver diverticulum arises more cephalad than usual the ductus choledochus may remain with the gastric portion of the gut. Or
an anastomosis between the right and left vitelline veins may
cause the pars hepatica to remain with the gastric portion of
the gut, while the adjacent pancreatic field may move caudally
with the elongation of the duodenum. Both the high cephalic
position of the liver diverticulum and the presence of anastomosing veins (6.5-mm. stage) exist in the embryo of the porcupine, at the time when differential caudal migration of the
insertion of the extra-hepatic and pancreatic ducts take place.
Rudiments of a gall bladder make a very transitory appearance during the early embryonic stages of the porcupine. In
the 4-mm. stage the cup-shaped diverticulum opens into the
gut by a large circular orifice, the caudal portion of which gives
off no trabeculae and its wall is somewhat thicker than in other
parts of the outgrowth. This structural plan is similar to that
seen in the embryo rat by Helly ( '01) and Scammon ( '16),
and in the prenatal deer by Bremer ( '23). Johnson ( '17)
reports that in the American ground squirrel the pars cystica
arises later than the pars hepatica, as a caudal extension of
the hepatic portion. The similarity in structural pattern of the
primitive pars hepatica and pars cystica in the early stages of
the embryo porcupine, with that of other mariimals cited,
indicate that, as in the development of the rat, a trace of a
cystic anlage appears in the early prenatal stages of the porcupine, but later is lost.
Measurements of the diameter and length of the ductus
hepato-entericus in adult porcupines compared with coi-responding measurements taken from mammals with or without
a gall bladder are very similar. This observation adds confirmation to the statement made by Mann, Brimwall and Foster
( ' Z O ) , that they could find, in the investigations of several
domestic and laboratory mammals, no indication of an increase in the capacity of the extraliepatic ducts to compensate
for the absence of a gall bladder.
Although no ventral pancreas can be recognized at any stage
in the ontogeny of the porcupine, certain structural elements
do appear which might relate to such a structure. The irregular caudal surface of the common bile duct in the 13.5-mm.
stage resembles a similar roughened condition occurring in
other mammalian embryos as reported by Bremer ('23), who
considers these small elevations isolated accessory pancreatic
glandulae. If Bremer 's interpretation correctly explains the
elevations on the bile duct of the porcupine, it is interesting
to note, that there are rudimentary pancreatic elements in
the extrahepatic ducts, although no ventral pancreas occurs.
A second developmental structure, possibly relating to a
ventral pancreas, is the pair of diverticula arising from the
duodenum at the base of the bile duct in the 14.5-mm. stage.
Their relatively late appearance, unusual occurrcnce, and nonrelationship to structures appearing later in other embryos,
place them as anomalies. Somewhat similar outgrowths on
the hepatic anlagen of pig embryos are identified as intestinal
diverticula, by Lewis and Thyng ( '08).
Another important consideration relates to the unusually
long interval which exists between the insertion of the bile
duct near the pylorus and that of the dorsal pancreatic duct
f a r down the duodenum. I n the adult porcupine this represents a distance of over 14 inches. The cause of this great
distal migration of the insertion of the pancreas is due primarily to a great lengthening of the duodenum in this rodent.
While the pancreatic insertion is moving distally, it retains its
primitive dorso-ventral position on the duodenum with respect
to the insertion of the bile duct, thus indicating an absence of
tortion in the proximal portion of the gut during this early
developmental period. Moreover the initial position of the
pancreatic diverticulum is at a lower level than that of the
bile duct and it is situated on the dorsal surface of the duodenum, thus placing it in the region of the greatest linear
growth of the gut. During this embryonic period the pancreatic duct has an unobstructed pathway for its caudal migration. Structural relationships which prevent a similar caudal
movement of the insertion of the bile duct may be very transitory, for in the 13.5-mm. stage the respective insertions have
nearly reached their definitive levels on the duodenum.
During the ontogeny of the visceral organs, the insertion of
the pancreatic duct on the duodenum occupies several different
positions in the abdominal cavity. Following the initial formation of the dorsal pancreatic diverticulum, its primitive duct
inserts on the duodenum at an increasingly distal position,
until in the 13.5-mm. stage the insertion is at the base of the
anterior limb of the intestinal loop. Meanwhile, the rapidly
growing liver has crowded the proximal part of the duodenum
caudally, so that the primary flexure lies at the level of the
urinary bladder. Further developmental changes, particularly the increase in size of the abdominal cavity and the
enlarged mass of the lower intestine, cause the proximal part
of the duodenum to swing cranially, to lie in approximately
the same vertical plane as the pylorus, while the primary flexure lies against the right abdominal wall. This position is
attained a.t about the 19-mm. stage. I n the 50-mm. stage
embryo a third shift in the position of the primary flexure and
its pancreatic connection has been completed. This change is
brought about by readjustments in the position of the nurnerous intestinal coils. I n this definitive position, the duodenal
flexure, on which the duct of the pancreas inserts, lies against
the right kidney. Its former more cranial position is now
occupied by two loops of the large intestine.
The short interval between the insertion of the bile duct on
the duodenum and the pylorus of the porcupine may be due
to the high cephalic position of the primitive liver diverticulum and to a transitory anastomosis between the right and left
vitelline veins, which cause an obstruction to the caudal movement of the ductus choledochus.
Rudiments of a gall bladder are seen, during carly ontogeny,
in the form of a caudal portion of the hepatic diverticulum
identified as the pars cystica.
Evidence is given to contradict the suggestion that there is
an increase in the capacity of the extrahepatic ducts to compensate for the absence of a gall bladder.
Structures identified as possible pancreatic glandulae occurring on the caudal surface of the bile duct, indicate the presence of a pancreatic field, although no ventral pancreas is
present at any stage in the ontogeny of the porcupine.
The ribbon-shaped pancreas of the adult drains into the
duodenum approximately 14 inches distal to the pylorus.
This unusually remote insertion of the pancreatic duct is the
result of great linear growth of the gut*and the absence of
obstructions retarding caudal migration.
The hepatic insertion assumes a definitive position in the
abdominal cavity early in prenatal development, but the pancreatic insertion is shifted frequently, due to ontogenetic
changes in the liver, the intestine, and the position of the
intestinal coils.
E. A. 1932 The problem of the double ductus choledochus. Anat. Rec..
vol. 55, no. 1.
a. L. 1923 Pancreatic ducts and pancreatic bladders. Am. J. Anat.,
vol. 31.
HELLY,K. 1901 Zur Pankreasentwickelung der Saugethiere. Arch. f . mikr.
Anat., Bd. 57.
C. E. 1917 On the development of the liver in the genus Citellus.
Anat. Rec., vol. 13, no. 3.
LEWIS,F. T., AND F. W. THYNG 1908 The regular occurrence of intestinal
diverticula in embryos of the pig, rabbit, and man. Am. J. Anat.,
vol. 7.
AND FOSTER 1920 The extrahepatic biliary tract in common
domestic and laboratory animals. Anat. Ree., vol. 18, no. 1.
R. E. 1916 On the development of the biliary system in animals
lacking a gall-bladder in postnatal life. Anat. Rec., vol. 10, no. 8.
G O R H A ~ II?.
, W., AND A. C. IVY1938 General function of the gall bladder from
the evolutionary standpoint. Zool. Ser., Field Mus. Nat. IIist., rol. 22,
pp. 159-213.
7 Photomicrograph showing the dorsal pancreatic diverticulum and the annulus
venosus caudalis in a 6.5-mm. embryo.
8 Photomicrograph of a section through the liver diverticulum in a 9-mm.
9 Photomicrograph of a section through the ductus choledochus in a 13.5 mm.
10 Photomicrograph of a section through the pyloric region near the insertion
of the bile duct, in a 15.5-mm. embryo.
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development, porcupine, prenatal, extra, canadian, hepatica, pancreaticum, erethizon, dorsatum, duct
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