AJR 2004; 182:1187-1193
© American Roentgen Ray Society
Collateral Venous Pathways in the Transverse Mesocolon and Greater Omentum in Patients with Pancreatic Disease
Kenji Ibukuro1,
Rei Ishii,
Hozumi Fukuda,
Shoko Abe and
Toshitaka Tsukiyama
1 All authors: Department of Radiology, Mitsui Memorial Hospital, 1-Kanda
Izumicho, Chiyoda-ku, Tokyo 101-8643, Japan.
Received June 25, 2003;
accepted after revision October 31, 2003.
Address correspondence to K. Ibukuro
(kj-ibkr{at}qd6.so-net.ne.jp).
Abstract
OBJECTIVE. The purpose of this study was to describe the radiologic
findings of the collateral venous pathways in the transverse mesocolon and the
greater omentum associated with pancreatic diseases and to correlate these
venous pathways and the accompanying arterial anatomy.
CONCLUSION. The collateral pathway in the transverse mesocolon
consists of the inferior mesenteric vein, left transverse colic vein, marginal
vein of the transverse colon, and middle colic vein. The pathway in the
greater omentum consists of anastomosis of the left and right epiploic veins
deriving from the gastroepiploic vein. The former pathway is the vena comitans
of Riolan's arch and the latter is the vena comitans of the arch of
Barkow.
Introduction
The gastric varices develop as a collateral venous pathway because of
isolated splenic vein occlusion in various pancreatic diseases
[1–3].
The dilated gastroepiploic vein along the great curvature of the stomach is
also shown in this condition
[4–8].
However, detailed description of the radiographic findings of the collateral
pathways in the transverse mesocolon and the greater omentum is rare.
The dilatation of these veins is a clue to the venous involvement by the
pancreatic diseases. The location and the direction of the blood flow of these
pathways are significant to prevent accidental bleeding during surgery for
pancreatic disease (either pancreatectomy or bypass surgery).
The purpose of this study is to describe the specific imaging features and
flow dynamics of these two venous pathways with correlation to the
accompanying arterial anatomy.
Materials and Methods
We performed both thin-section helical CT of the pancreas and subsequent
angiography in 54 patients (35 men, 19 women) with various pancreatic diseases
(pancreatic head carcinoma in 31, pancreatic body carcinoma in 12, pancreatic
tail carcinoma in two, mucin-producing tumor in four, large pancreatic cyst
with chronic pancreatitis in five) between 1998 and 2002. Three radiologists
experienced in abdominal imaging retrospectively reviewed both the
thin-section helical CT scans of the pancreas and the angiograms, paying
particular attention to the collateral venous pathways in all 54 patients. The
collateral vessels were seen in 21 of the 54 patients. The well-known
collateral vessels—the dilated short gastric vein with gastric varices,
the dilated gastroepiploic vein, or both—were found in 11, 10, and seven
of the 54 patients, respectively. We also identified two unknown collateral
venous pathways: one in the transverse mesocolon in five patients and the
other in the greater omentum in three patients. Our review included these
eight patients with two unknown collateral pathways. The patients were three
men and five women with a mean age of 62 years (age range, 40–78
years).
Thin-section helical CT scans of the pancreas were obtained at 3-mm
collimation in 30 sec scanning time using 120 kV and 270 mAs. Scanning was
started 60 sec after injection of the IV contrast material ([iopamidol]
Iopamiron 300, Schering) at a rate of 2 mL/sec, up to 100 mL. The patients
were instructed to hold their breath during the 30-sec helical scanning time.
Axial images of the helical CT scan were reconstructed at 1.5-mm intervals. We
used Xvigor (Toshiba) as the helical CT scanner.
All patients underwent both celiac artery and superior mesenteric artery
angiography using the digital subtraction angiography system (Advantx LC+,
General Electric Medical Systems). Angiography was performed within a week
after thin-section helical CT in each patient. Superior mesenteric artery
angiography was performed using a vasodilator (alprostadil, Mitsubishi Pharma:
5 µg). When some part of the collateral venous pathway was outside the
field of view on the celiac artery angiogram, we resized and repositioned the
field of view for the entire venous pathway and performed additional selective
splenic artery angiography. Because only the venous phase was significant to
see the collateral venous pathway, we began angiography after the contrast
material injection in the splenic artery. Therefore, it was not necessary for
the patients to hold their breath from the beginning of the contrast material
injection.
Because the two venous pathways we describe here have not been reported in
the radiology literature, to our knowledge, we should confirm a possibility
for the existence of these venous pathways. Therefore, we dissected one
cadaver without any abdominal disease. We dissected the greater omentum and
the transverse mesocolon to show the epiploic branches of the gastroepiploic
vein and the marginal vein of the transverse colon, respectively.
Results
Collateral Pathway in the Transverse Mesocolon
Patient details are summarized in Table
1. The diameter of the vein in the transverse mesocolon ranged
from 6 to 10 mm (mean, 8 mm). Collateral pathways in the transverse mesocolon
are classified into two types on the basis of the direction of the blood
flow.
Because the proximal portion of the splenic vein was occluded and the
distal portion was patent (occlusion between the portal–splenic vein
confluence and the level of the inferior mesenteric vein entry), the splenic
venous flow consequently emptied into the inferior mesenteric vein in two
patients with pancreatic body carcinoma (Fig.
1A,
1B,
1C,
1D). The blood flow of the
inferior mesenteric vein drained into the left transverse colic vein and the
marginal vein along the transverse colon, then finally toward the superior
mesenteric vein via the middle colic vein. The flow in the marginal vein along
the transverse colon was from left to right in these patients. The short
gastric vein and the gastroepiploic vein were dilated in one and both
patients, respectively.
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Fig. 1A. —78-year-old woman with pancreas body carcinoma. Selective
splenic artery digital subtraction angiography (venous phase) shows that
splenic venous flow runs through distal portion of splenic vein, inferior
mesenteric vein (arrowheads), left transverse colic vein (large
black arrow), marginal vein (small black arrows) extending along
transverse colon, and middle colic vein (M), then ends at superior mesenteric
vein (star). Note gastroepiploic vein (white arrows) is also
shown and mimics marginal vein along transverse colon.
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Fig. 1B. —78-year-old woman with pancreas body carcinoma.
Contrast-enhanced axial CT scan shows low-density mass (long arrow)
where splenic vein (arrowhead) is occluded. Note dilated
gastroepiploic vein (short arrows) along great curvature of
stomach.
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Fig. 1C. —78-year-old woman with pancreas body carcinoma.
Contrast-enhanced axial CT scan shows dilated middle colic vein (thin
arrow) ending at anterior aspect of superior mesenteric vein. Note
dilated inferior mesenteric vein (arrowhead) and left transverse
colic vein (thick arrow).
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Fig. 1D. —78-year-old woman with pancreas body carcinoma. Drawing shows
left-to-right direction of blood flow. When proximal splenic vein is
obstructed, splenic venous flow runs into inferior mesenteric vein, left
transverse colic vein, marginal vein along transverse colon, then middle colic
vein (M), ending at superior mesenteric vein. X indicates location of venous
obstruction and arrows indicate direction of blood flow. RGV = right gastric
vein, LGV = left gastric vein, SGV = short gastric vein, IMV = inferior
mesenteric vein, GEV = gastroepiploic vein, EV = epiploic vein, MV = marginal
vein along transverse colon, GCT = gastrocolic trunk, LTCV = left transverse
colic vein, SP = spleen, ST = stomach.
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The same pathway was also shown in three patients with localized superior
mesenteric vein occlusion (between the portal–superior mesenteric venous
confluence and the level of the middle colic vein entry) due to pancreatic
head carcinoma (n = 2) and postoperative changes in a patient with
pancreatic head carcinoma (n = 1) (Fig.
2A,
2B). Because the direction of
blood flow was opposite from the proximal splenic vein occlusion, the blood
from the superior mesenteric vein drained into the portal vein via the patent
splenic vein through this pathway. The short gastric vein and the
gastroepiploic vein were not dilated in these three patients.
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Fig. 2A. —57-year-old woman with postoperative change to pancreatic
head. Selective superior mesenteric artery angiography (venous phase) shows
venous flow of superior mesenteric vein empties into middle colic vein
(star), left transverse colic vein (arrowheads), inferior
mesenteric vein, and splenic vein (arrow), then flows toward portal
vein.
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Fig. 2B. —57-year-old woman with postoperative change to pancreatic
head. Drawing shows right-to-left direction of blood flow. Because confluence
of superior mesenteric vein with portal vein is obstructed, blood flow of
superior mesenteric vein runs into middle colic vein (M), marginal vein along
transverse colon, left transverse colic vein, inferior mesenteric vein, then
splenic vein. X indicates location of venous obstruction and arrows indicate
direction of blood flow. IMV = inferior mesenteric vein, LTCV = left
transverse colic vein, MV = marginal vein along transverse colon.
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Axial CT showed the dilated inferior mesenteric vein and the marginal vein
along the transverse colon were both located deep in the abdomen.
Collateral Pathways in the Greater Omentum
Patient details are summarized in Table
1. The diameter of the vein in the greater omentum ranged from 6
to 8 mm (mean, 7 mm).
The venous anastomosis between the left and right epiploic veins was shown
in three patients with total splenic vein occlusion (Fig.
3A,
3B). The epiploic vein was
shown inferior to the gastroepiploic vein and the anastomosis between the left
and right epiploic veins was shown as an arch toward the lower abdomen on
angiography. Because the epiploic veins are located in the greater omentum,
they are situated just behind the anterior abdominal wall on the axial CT
scan. The short gastric vein and the gastroepiploic vein were dilated in two
and three of the three patients, respectively.
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Fig. 3A. —48-year-old woman with giant pancreatic cyst. Celiac artery
digital subtraction angiography (venous phase) shows arch of dilated epiploic
vein (arrowheads) running from splenic hilum toward pelvis, then
right and upward. C = giant pancreatic cyst.
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Fig. 3B. —48-year-old woman with giant pancreatic cyst. Drawing shows
direction of blood flow in omental vein. When splenic vein is occluded,
splenic venous flow can empty into epiploic branch of left gastroepiploic
vein. Because anastomosis exists between left and right epiploic veins, which
makes a venous arch, splenic venous blood flow runs into gastrocolic trunk,
then portal vein. X indicates location of venous obstruction and arrows
indicate direction of blood flow. GCT = gastrocolic trunk, GEV =
gastroepiploic vein, EV = epiploic vein, SP = spleen.
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Cadaver Dissection
Inferior to the gastroepiploic vessel, an arch was located in the greater
omentum (Fig. 4A). This arch
consisted of the epiploic artery and vein deriving from the gastroepiploic
artery and vein. The arch as well as small branches of the epiploic vessels
were also shown in the greater omentum.
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Fig. 4A. —Dissected abdomen from cadaver of 67-year-old woman with no
evidence of abdominal disease. Photograph shows anterior aspect of stomach and
greater omentum. Anastomosis of right and left epiploic veins in greater
omentum, arch of epiploic vein (arrowheads), is located inferior to
gastroepiploic vein (arrows) extending along greater curvature of
stomach. ST = stomach, OM = greater omentum.
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Two branches of the inferior mesenteric vein ran toward the splenic flexure
of the colon: the left transverse colic vein and the left superior colic vein
(Fig. 4B). Both veins joined
the marginal vein extending along the transverse colon in the transverse
mesocolon. The left transverse colic vein ran with the accessory middle colic
artery and the superior left colic vein accompanying the superior left colic
artery.
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Fig. 4B. —Dissected abdomen from cadaver of 67-year-old woman with no
evidence of abdominal disease. Photograph shows posterior aspect of transverse
mesocolon and left mesocolon. Small intestine was removed. Transverse colon
(TC) was flipped upward to show transverse mesocolon. Two venous branches
extend from inferior mesenteric vein toward marginal vein (arrows)
along transverse colon, left transverse colic vein (black
arrowheads), and left superior colic vein (white arrowheads).
Note left transverse colic vein accompanying accessory middle colic artery.
IMA = inferior mesenteric artery, IMV = inferior mesenteric vein, D = fourth
portion of duodenum.
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Discussion
Collateral Pathway in the Transverse Mesocolon
The collateral pathway along the great curvature of the stomach, the
gastroepiploic vein, develops in patients with isolated splenic vein occlusion
[4–8].
However, the pathway along the transverse colon in the transverse mesocolon
has not been reported, to our knowledge. Because both pathways are located
below the stomach, one might not differentiate this marginal vein extending
along the transverse colon from the gastroepiploic vein, especially on
angiography. However, when we carefully observed the sequential films of the
celiac or splenic artery angiography, we noticed the pathway along the
transverse colon appeared slightly after the gastroepiploic vein. Once one
recognizes the existence of the pathway along the transverse colon, it is easy
to notice this pathway on both CT scans and angiograms.
This pathway is classified into two types on the basis of the direction of
the blood flow: the left-to-right type (Fig.
1A,
1B,
1C,
1D) and the right-to-left type
(Fig. 2A,
2B). In the former, the
proximal part of the splenic vein is occluded; however, the inferior
mesenteric vein and the superior mesenteric vein are patent. In the latter,
the proximal part of the superior mesenteric vein is occluded; however, the
splenic vein is patent. Therefore, the visualization of these pathways
indicates either the splenic vein or the superior mesenteric vein is
patent.
Cadaver dissection showed two possible venous pathways from the inferior
mesenteric vein to the marginal vein of the transverse colon: the left
transverse colic vein and the superior left colic vein
[9]. In our patients, the
branch of the inferior mesenteric vein running toward the splenic flexure was
located above the location of the left superior colic vein, thus this branch
was thought to be the left transverse colic vein. The location of the left
transverse colic vein is the same as that of the accessory middle colic artery
that was known as the artery of Riolan
[10]. The accessory middle
colic artery sometimes arises from the celiac trunk via the dorsal pancreatic
artery. Thus, the venous collateral pathway described here is morphologically
the same as the accessory middle colic artery arising from the celiac trunk
and the marginal artery along the transverse colon, which is sometimes called
Riolan's arch [11].
Mori et al. [7] reported
that the middle colic vein and the gastrocolic trunk were dilated in patients
with occlusion of portal–superior mesenteric venous confluence above the
level of gastrocolic trunk entry. Although they evaluated the gastrocolic
trunk and its tributaries on CT scans in terms of the diameter of those veins
in the various venous occlusions, those authors did not determine a detailed
description of the pathway. We anatomically reviewed both the CT scans and the
angiograms for the pathway and found that it was possible to differentiate the
marginal vein of the transverse colon ending in the middle colic vein from the
gastroepiploic vein ending in the gastrocolic trunk. MDCT scans may show these
venous structures clearly and in 3D; however, we believe angiography can show
the flow dynamics of the venous collaterals as well as the pathways better
than CT.
Pathway in the Greater Omentum
Cho and Martel [8] stated
that existing collateral channels include the omental vein in splenic venous
occlusion, but radiologic features of the omental vein were not described.
Sompayrac et al. [12] reviewed
the various pathologic processes of the greater omentum and showed multiple
collateral veins in the greater omentum in a patient with portal hypertension;
however, these veins are not the epiploic venous arch that we report here.
The collateral vein we show here is the omental venous arch that consists
of anastomosis between the left and right epiploic veins deriving from the
gastroepiploic vein. According to Michels
[10], Barkow described the
anastomosis between the right and left epiploic branches of the gastroepiploic
artery in the greater omentum 2–4 cm below the transverse colon as the
arcus epiploicus magnus. Therefore, the venous pathway we report here can be
called the venous arch of Barkow.
The lower end of this venous arch was located in the lower abdomen;
therefore, it was necessary to perform angiography using a large field of view
and additional angiography for the lower abdomen to show the whole arch.
Because the dilated left epiploic vein was noticed on celiac angiography, we
performed additional angiography to trace the left epiploic vein in each
patient. Thus, we could show the whole venous arch between the left and right
epiploic veins.
Because the venous arch of Barkow is located in the greater omentum, it was
shown below the transverse colon and just behind the abdominal wall on axial
CT scans. Therefore, it is possible to differentiate the three similar
collateral venous arches: the gastroepiploic vein located along the great
curvature of the stomach, the marginal vein along the transverse colon located
deep in the abdomen, and the anastomosis of the right and left epiploic veins
in the greater omentum located superficially compared with the other two
pathways on CT.
Embryologically, the primitive omental bursa bulged downward in front of
the transverse mesocolon and the transverse colon, then adhered to them,
thereby forming the greater omentum
[13]. Therefore, three
mesenteric reflections exist around the pancreas known as the transverse
mesocolon, the gastrocolic ligament, and the greater omentum
(Fig. 5). Meyers
[14] described the importance
of these mesenteric reflections in terms of the extension of primary neoplasms
to the other sites. The anatomic continuity of these mesenteric reflections
toward the left and the right are the splenic hilum and the head of the
pancreas, respectively, so we assumed that collateral vessels we report here
develop in these mesenteric reflections when the splenic vein is occluded.
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Fig. 5. —Drawing of sagittal section of transverse mesocolon and
greater omentum shows spatial relationship between splenic vein (SpV), short
gastric vein (SGV), gastroepiploic vein (GEV), marginal vein along transverse
colon (MV), and epiploic vein (EV). When splenic vein is occluded, four
anatomically possible pathways exist that splenic venous flow drains: short
gastric vein, gastroepiploic vein in gastrocolic ligament, epiploic vein in
greater omentum, and marginal vein of transverse colon in transverse
mesocolon. P = pancreas.
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Because the dilated veins are easily torn and might be the cause of massive
bleeding during surgery, it is useful for surgeons to know which veins are
dilated and the direction of the blood flow before ligation of the vessels.
Because the dilated omental venous arch is located superficially, one should
avoid damage to the vessels when opening the abdominal wall at surgery. The
pathway via the marginal vein of the transverse colon is located deep in the
abdomen and could be overlooked; however, the dilatation of this pathway is an
important clue to venous involvement by pancreatic disease.
Conclusion
We described the two collateral pathways, one in the transverse mesocolon
and the other in the greater omentum, in patients with pancreatic disease with
correlation to the accompanying arterial anatomy.
Acknowledgments
We thank Tatsuo Sato, Department of Functional Anatomy, Tokyo Medical and
Dental University, for cooperation in the cadaver dissection. We also thank
Jan E. Oda-Biro for manuscript preparation.
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Abstract
Introduction
