DOI:10.2214/AJR.07.2990
AJR 2008; 191:W8-W16
© American Roentgen Ray Society
Changes of Portosystemic Collaterals and Splenic Volume on CT After Liver Transplantation and Factors Influencing Those Changes
Se Hyung Kim1,
Jeong Min Lee1,2,
Jin Young Choi3,
Kyung-Suk Suh4,
Nam-Joon Yi4,
Joon Koo Han1,2 and
Byung Ihn Choi1,2
1 Department of Radiology, Seoul National University Hospital, 28, Yeongon-dong,
Jongno-gu, Seoul 110-744, Korea.
2 Institute of Radiation Medicine, Seoul National University Hospital, Seoul,
Korea.
3 Department of Radiology, Yonsei University Hospital, Seoul, Korea.
4 Department of Surgery, Seoul National University Hospital, Seoul, Korea.
Received August 7, 2007;
accepted after revision January 27, 2008.
WEB
This is a Web exclusive article.
Address correspondence to J. M. Lee
(leejm{at}radcom.snu.ac.kr).
Abstract
OBJECTIVE. The objective of our study was to investigate the changes
of portosystemic collaterals and splenic volume after liver transplantation
and to determine the factors influencing those changes.
MATERIALS AND METHODS. Ninety-nine patients underwent liver CT
before; immediately after (< 2 weeks); and 2, 6, and 12 months after liver
transplantation. Two radiologists retrospectively reviewed the CT images to
determine the grade of the portosystemic collaterals and the volume of the
spleen. Portosystemic collaterals were categorized as esophageal,
paraesophageal, gastric submucosal, gastric adventitial, splenic, mesenteric,
or retroperitoneal varices. First, the largest diameter of each varix was
determined. Each varix was graded using a 5-point scale according to the
number of dilated vessels and the largest diameter. Splenic volume was
calculated using a previously reported formula. To determine how varices and
splenomegaly develop over time, the grade of varices on each postoperative CT
scan was compared with those on the preoperative and immediately prior CT
scans. The degree of change of the portosystemic collaterals and change in the
splenic volume on CT were correlated with the type of transplantation
(deceased-donor-related liver transplantation [DDLT] vs living-donor-related
liver transplantation [LDLT]), the transplanted liver weight, and the presence
of postoperative adverse events such as rejection and portal or hepatic vein
stenosis.
RESULTS. All varices except splenic and retroperitoneal varices and
splenic volume were significantly decreased on CT performed within 2 weeks
after liver transplantation (p < 0.05). Approximately 2 months
after liver transplantation, all varices except the esophageal varices and
splenic volume became stable. The type of transplantation and the presence of
postoperative adverse events did not affect the degree of change of varices or
change in splenic volume. However, the rate of volume reduction of the spleen
in LDLT was weakly but significantly correlated with the weight of the
transplanted liver (Pearson's correlation coefficient, r = 0.401;
p < 0.0001).
CONCLUSION. Most varices and splenomegaly significantly decrease
during the early postoperative period (< 2 months) after liver
transplantation. Patients with large liver transplants undergo a greater
decrease in spleen volume than patients with small liver transplants.
Keywords: hemodynamics • liver transplantation • portal hypertension • splenomegaly • varices
Introduction
Portal hypertension is one of the major complications of end-stage liver
disease that may cause complications such as variceal bleeding, ascites, and
hepatorenal syndrome. Indeed, gastroesophageal varices, the most clinically
important portosystemic collaterals because of their propensity to rupture
[1], are present in
approximately 50% of patients with cirrhosis, and their presence often
correlates with the severity of liver disease
[2,
3].
There are several treatment options for varices: drug therapy, endoscopic
variceal ligation, transjugular intrahepatic portosystemic shunt (TIPS)
placement, and various surgical procedures
[4–7].
Among them, liver transplantation is notably the only causal treatment
[8]. Indeed, after liver
transplantation, the risk of variceal bleeding dramatically decreases to 9%
from 10–30% without liver transplantation
[9,
10]. Given that the risk of
bleeding is associated with variceal size and Child-Pugh class but not with
portal venous pressure itself
[2], monitoring the evolution
of portosystemic collaterals after treatment can be important in predicting
the risk of variceal bleeding after varix treatment.
Considering the dramatic decrease in the incidence of variceal bleeding
after liver transplantation, we could easily expect that the size of varices
should also decrease after liver transplantation. However, contrary to our
expectation, Chezmar et al.
[11] found that portosystemic
collaterals and splenomegaly may persist for up to 2–4 years after liver
transplantation and that the persistence of portosystemic collaterals and
splenomegaly does not indicate recurrence of hepatic disease or presence of
other posttransplantation complications.
Recently, endoscopy was considered as one of the techniques of choice for
the evaluation of gastroesophageal varices in patients with cirrhosis.
However, with the advances in CT technology, the role of CT has expanded as a
necessary examination for the routine surveillance of liver cirrhosis because
of its less invasive nature and lower cost compared with endoscopy
[12,
13]. CT can also assist in the
detection and grading of gastroesophageal varices and in the detection of
other major complication of liver cirrhosis such as hepatocellular carcinoma.
Although few CT reports regarding the changes of portosystemic collaterals and
splenomegaly after liver transplantation have been published in the
literature, most focused on patients who had undergone only
deceased-donor-related liver transplantation (DDLT) or focused on a small
number of patients, thus limiting the importance of the results
[11,
14,
15]. However,
living-donor-related liver transplantation (LDLT) is now being considered in
the treatment of patients with end-stage liver disease because of deceased
donor shortages.
The type of liver transplantation along with many other factors, such as
the volume or weight of the transplanted liver and the presence of
posttransplantation adverse effects (e.g., acute rejection, primary hepatic
dysfunction, vascular complications, and the presence of hepatic venous
congestion), may be factors that influence the evolution of varices.
Therefore, the purpose of our study was to investigate the serial changes of
portosystemic collaterals and splenic volume on CT after liver transplantation
and to determine the factors influencing their evolution.
Materials and Methods
Patient Population
For this retrospective study, we collected the records of 131 consecutive
patients who underwent liver transplantation at our hospital between January
2003 and April 2005. Of these 131 patients, 32 were excluded from the study
for one of the following reasons: CT was not performed within 3 months before
liver transplantation (n = 17); CT was not performed at more than two
of the four follow-up intervals (within 2 weeks after liver transplantation
and at intervals of approximately 2 months, 6 months, and 1 year after liver
transplantation) (n = 13); or the patient died within 1 month of
transplantation (n = 2). A total of 99 patients were ultimately
included in this study: 70 men and 29 women. The mean age of the study group
was 43 years (range, 1–77 years). Nine patients were children or
adolescents (age 
18 years) and 90 were adults (age > 18 years).
Seventy-nine patients received living donor liver grafts, and the remaining
20 received deceased donor liver grafts. The primary liver disease was viral
liver cirrhosis in 74 patients, biliary atresia in eight, alcoholic cirrhosis
in four, Wilson's disease in two, Alagille syndrome in two, and another liver
disease in nine. Of the 20 patients who underwent DDLT, 19 received a total
liver graft and the remaining patient received only the left lobe of the
deceased donor liver. The living donor grafts included 50 right lobe grafts
without the middle hepatic vein (MHV), nine left lateral segment grafts, seven
right lobe grafts with MHV, six left lobe grafts without MHV, and seven left
lobe grafts with MHV. This study was approved by the institutional review
board of our hospital and written informed consent was waived for this
retrospective study.
CT Acquisition
Because our surgeons had no strict strategy to determine the interval and
frequency of CT follow-up for liver transplant recipients before 2005, the
number of CT scans obtained at each follow-up period varied. The indications
for CT examinations during the early postoperative per iod (i.e., within 3
months) included abnormal laboratory results, clinical findings, or sonography
findings. Furthermore, most CT examinations dur ing that period were performed
to evaluate for the presence of biliary complications. During the late post
operative period (6 months–1 year after liver trans plantation), the
indication for most CT examinations was screening for hepatocellular
carcinoma. Both of these major indications are known to have little effect on
the evolution of varices.
A total of 394 CT scans were obtained of the 99 patients preoperatively
(n = 99); within 2 weeks of liver transplantation (n = 90);
and at intervals of approximately 2 months (n = 66), 6 months
(n = 62), and 1 year (n = 77) after transplantation. The
mean interval between transplantation and preoperative CT was 40 days. The
mean interval between transplantation and postoperative CT was 10 days for the
first CT scan, 71 days for the second scan, 206 days for the third scan, and
382 days for the fourth scan. In addition, because this study was performed
retrospectively, various types of CT scanners and acquisition parameters were
used.
Most of the CT scans were obtained on one of three MDCT scanners: Sensation
16 (Siemens Medical Solutions), n = 87; LightSpeed Ultra (GE
Healthcare), n = 168; or Mx8000 (Philips Medical Systems), n
= 101. For the other 38 CT scans, one of two single-detector CT
scanners—Somatom Plus 4 (Siemens Medical Solutions), n = 36, or
HiSpeed (GE Healthcare), n = 2—was used. Slice thickness and
reconstruction interval were 1–5 mm and 3–5 mm, respectively. A
pitch of 1–1.5 and rotation time of 0.5–1 second were used.
Effective tube current ranged from 150 to 250 mAs and kilo-voltage was 120 kVp
for all CT examinations.
With 8- and 16-MDCT scanners, quadruple-phase CT (unenhanced, early hepatic
arterial, late hepatic arterial, and portal venous phases) was performed.
First, a baseline unenhanced scan was obtained through the entire liver.
Patients received 120 mL of iopromide (Ultravist 370, Bayer HealthCare) IV
using a power injector at a rate of 2–4 mL/s. The scanning delay for the
early hepatic arterial phase was 5 seconds after reaching the enhancement of
the descending aorta up to 100 H as measured by a bolus-tracking technique.
For the late hepatic arterial and portal venous phases, the interscan delays
were 9 and 30 seconds for the 16-MDCT scanner and 7 and 20 seconds for the
8-MDCT scanner, respectively. For the 4-MDCT and single-detector CT scanners,
triple-phase CT (unenhanced, arterial, and portal venous phases) was
performed. The scanning delay was 25 and 60 seconds for the arterial and
portal venous phases, respectively, after IV contrast administration.
Image Interpretation and Statistical Analysis
Portal phase CT scans were analyzed retrospectively by two experienced
abdominal radiologists (10 years' experience) in consensus to
semiquantitatively determine the presence of varices and, if present, to grade
the severity of the varices. Portosystemic collaterals were categorized as
esophageal, paraesophageal, gastric submuc osal, gastric adventitial, splenic,
mesenteric, or retroperitoneal varices
[16]. The dilated veins
located within the wall of the lower esophagus and outside the wall of the
esophagus were designated as esophageal and paraesophageal varices,
respectively. Dilated veins located within the submucosal layer of the gastric
wall were defined as gastric submucosal varices, whereas veins within the
adventitial layer at the exterior border of the gastric wall were defined as
gastric adventitial varices. Splenic varices were seen as tortuous veins in
the region of the splenic hila. Dilated or tortuous branches of the superior
or inferior mesenteric vein within the mesenteric fat were classified as
mesenteric varices. Tortuous retro peritoneal tributa ries of the superior or
inferior mesenteric vein located in the retroperitoneum were defined as
retroperitoneal varices. A schematic drawing of the portosystemic collaterals
and corresponding CT images is presented in Figure
1A,
1B,
1C,
1D,
1E,
1F.
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Fig. 1A —Schematic drawing of portosystemic collaterals and
corresponding CT images. Schematic drawing illustrates portosystemic
collateral vessels in portal hypertension. 1 = esophageal varices; 2 =
paraesophageal varices; 3 = gastrorenal shunt; 4 = splenorenal shunt; 5 =
inferior mesenteric, hemorrhoidal, and internal iliac veins; 6 = mesocaval
shunt; 7 = intrahepatic portosystemic shunt; 8 = Sappey's veins.
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Fig. 1B —Schematic drawing of portosystemic collaterals and
corresponding CT images. On portal venous phase CT scan, esophageal
(asterisk) and paraesophageal (arrows) varices appear as
dilated veins located within and outside wall of lower esophagus,
respectively. Patient is 57-year-old man who received partial transplant.
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Fig. 1C —Schematic drawing of portosystemic collaterals and
corresponding CT images. Gastric submucosal (asterisks) and
adventitial (arrows) varices are seen as dilated veins located within
submucosal layer of gastric wall and in adventitial layer at exterior border
of gastric wall, respectively. Patient is 51-year-old man who received partial
transplant.
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Fig. 1D —Schematic drawing of portosystemic collaterals and
corresponding CT images. Splenic varices (arrows) are seen as
tortuous veins in region of splenic hila. Patient is 50-year-old woman who
received partial transplant.
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Fig. 1E —Schematic drawing of portosystemic collaterals and
corresponding CT images. Dilated or tortuous branches of superior or inferior
mesenteric vein within mesenteric fat are classified as mesenteric varices
(arrows). Patient is 47-yearold man who received total
transplant.
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Fig. 1F —Schematic drawing of portosystemic collaterals and
corresponding CT images. Retroperitoneal (arrows) varices appear as
tortuous retroperitoneal tributaries of superior or inferior mesenteric vein
located in retroperitoneum. Patient is 53-year-old woman who received partial
transplant.
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Varices excluding the esophageal, paraeso phageal, and submucosal gastric
types were defined as serpiginous vascular structures > 3 mm in diameter
and showing contrast enhancement during the portal venous phase. For
esophageal, paraesophageal, and submucosal gastric varices, the size criterion
was 2 mm [17]. When varices
were considered to be present, radiologists were asked to measure the diameter
of the largest visible varix. Then, according to the number of dilated vessels
and the diameter of the largest varix, radiologists graded the varices on a
5-point scale. The criteria for grading varices are presented in
Table 1. If there were more
than four dilated vessels on 2D cross-sectional images, the varices were
graded one step higher.
Radiologists were also asked to determine spleen size using width, length,
and thickness measurements. The length was obtained by multiplying the number
of sections in which the spleen was visualized by slice thickness. The width
was recorded at the point of maximum width of the spleen. The thickness was
obtained at the midpoint of the section where width was determined
(Fig. 2). Splenic volume was
then calculated using the following formula: 30 + 0.58 x (width x
length x thickness)
[18].
To determine the evolution of varices and splenomegaly over time, the grade
of varices and splenic volume on each postoperative CT scan were compared with
those on the preoperative and immediately prior CT scans. Statistical
significance of the difference was determined using the Wilcoxon's signed rank
test for categoric variables—that is, grade—and the paired Stu
dent's t test for continuous variables—that is, volume. To
evaluate the changes of varices and splenic volume 1 year after
transplantation, the grade of each varix and splenic volume were compared
between the preoperative CT scan and the fourth CT scan obtained approximately
1 year after liver transplantation. Statistical analysis was performed using
the Wilcoxon's signed rank test for categoric variables and a paired Student's
t test for continuous variables.
To determine the factors influencing the evolution of varices and
splenomegaly, the degree of changes in the varices and the changes in splenic
volume between the preoperative CT scan and fourth postoperative CT scan were
calculated and then were compared between the types of donor liver graft
(total vs partial) using the Mann-Whitney U test. A similar
comparison was made between the presence of postoperative adverse events such
as rejection and abnormalities of anastomotic vessels, such as thrombosis,
stenosis, or aneurysm of three hepatic vasculatures. In particular, to
evaluate the influence of the postoperative portal or hepatic venous status on
the evolution of portosystemic collaterals and spleen volume, the difference
in portal vein (PV) diameter between the anastomotic site and just proximal
recipient PV and the presence of hepatic venous congestion were determined
using CT scans only in patients with partial donor liver grafts. PV diameters
at both the anastomotic site and recipient main PV just proximal to that area
were measured by a radiologist using an electronic caliper.
Hepatic venous congestion was determined to be present at the first
postoperative CT scan when a hepatic attenuation difference in the anterior
seg ment of the right lobe transplant or the medial segment of the left lobe
transplant with hypo- or hyperattenuation in those segments was seen on portal
venous phase imaging [19]. The
degree of the changes in the varices and changes in splenic volume between the
two CT scans (preoperative and fourth postoperative) were correlated with the
difference between PV diameters using the Pear son's or Spearman's correlation
test. In addition, the degree of varices changes and splenic volume changes
were also compared between the presence and absence of hepatic venous
congestion using the Mann-Whitney U test.
To investigate whether the weight of the transplanted liver influenced the
evolution of each varix and of spleen volume, the degree of the changes in the
varices and changes in splenic volume between the two CT scans (preoperative
and fourth postoperative) were correlated with the transplanted liver weight
using Pearson's correlation test. For evaluation of spleen volume
(SV), the volume reduction rate was calculated using the following
formula:
where SVpreop CT and SVfourth CT
represent spleen volume calculated on preoperative CT and on the fourth
follow-up CT examination after liver transplantation, respectively. Clinical,
laboratory, and imaging findings were used to determine whether portal or
hepatic venous stenosis was present. Rejection was confirmed after percu t
aneous liver biopsy. The transplanted liver weight was measured just after
retrieving the donor liver graft in the operating room.
Statistical analysis was performed using SPSS software (version 11.0, SPSS)
for Windows (Microsoft). For the correlation tests, we considered a
correlation coefficient of more than 0.7 to represent strong correlation and a
coefficient of 0.3–0.7 to represent weak correlation. A correlation
coefficient of less than 0.3 was considered to indicate little or no
correlation.
Results
In 16 patients, acute rejection was confirmed on both clinical and
pathologic examinations. Four, two, and six patients were diagnosed as having
hepatic arterial, portal venous, and hepatic venous stenosis, respectively.
Five of the 16 patients diagnosed as having acute rejection also had vascular
complications. Therefore, 23 patients were classified as having postoperative
adverse events. In 80 patients who underwent liver transplantation with a
partial liver graft, the mean weight of the living donor liver grafts was 631
g (range, 130–1,005 g).
The mean grades and SDs of each varix and the mean spleen volumes and SDs
on each CT scan are listed in Table
2, along with details of the comparative statistical analysis
compared with those on the preoperative and just-prior CT scans. To
intuitively show the evolution of each varix and of spleen size over time,
graphs are presented in Figure
3. All varices except the splenic and retroperitoneal varices had
significantly decreased in both grade and size on CT performed within 2 weeks
after transplantation (p < 0.05). All varices except the
esophageal varices become stable approximately 2 months after transplantation.
On the contrary, esophageal varices continuously decreased even for more than
1 year after liver transplantation. Spleen volume also decreased significantly
within 2 weeks after transplantation and remained stable for 1 year.
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TABLE 2: Grades Assigned to Each Varix and Spleen Sizes on All CT Examinations
with Preoperative and Just-Prior CT Values for Statistical Comparison
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Fig. 3 —Graph shows evolution of varices and spleen volume over time
after liver transplantation (LT). First CT scan was obtained within 2 weeks
after transplantation, second CT at approximately 2 months, third CT at 6
months, and fourth CT at 1 year after transplantation. Numbers on main
y-axis indicate mean value of variceal grade and numbers on second
y-axis indicate spleen volume on each CT. Solid lines indicate that
difference of mean values of variceal grade or spleen volume between each CT
and just-prior CT are statistically significant, whereas dotted lines indicate
difference is not significant. All varices except splenic and retroperitoneal
varices significantly decreased in diameter on CT performed within 2 weeks
after transplantation (p < 0.05). All varices except esophageal
varices became stable approximately 2 months after transplantation. On the
contrary, esophageal varices continuously and significantly decreased in size
even more than 1 year after liver transplantation. Spleen volume decreased
significantly within 2 weeks after transplantation and became stable after
that time.
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When the grade of each varix and spleen volume were compared between the
preoperative and fourth postoperative CT examinations to evaluate the changes
of varices and spleen volume 1 year after transplantation, all varices except
retroperitoneal varices and splenic volume had decreased significantly on the
fourth CT examination compared with preoperative CT
(Table 2). Representative
examples are shown in Figures
4A,
4B,
5A,
5B,
5C,
6A,
6B,
7A,
7B.
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Fig. 4A —45-year-old woman with grade 4 esophageal and paraesophageal
varices before undergoing liver transplantation. Preoperative CT scan obtained
at level of lower esophagus during portal venous phase shows tortuous enhanced
esophageal (asterisk) and paraesophageal (arrows) varices.
Largest diameters of esophageal and paraesophageal varices are 8.9 and 8 mm,
respectively, and number of both varices on transverse image is more than
four. Therefore, final variceal grade recorded by two radiologists was 4 for
both varices.
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Fig. 4B —45-year-old woman with grade 4 esophageal and paraesophageal
varices before undergoing liver transplantation. Transverse CT image obtained
11 days after deceased donor liver transplantation shows no varices within or
around esophagus. CT scans obtained at 190 days and 400 days after
transplantation (not shown) revealed no varices.
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Fig. 5A —43-year-old man with grade 4 gastric submucosal and
adventitial varices before undergoing liver transplantation. Preoperative CT
scan obtained at level of gastroesophageal junction during portal venous phase
shows multiple tortuous enhanced gastric submucosal (arrows) and
adventitial (arrowheads) varices. Largest diameters of gastric
submucosal and adventitial varices are 8.5 and 10.6 mm, respectively, and
number of both varices on transverse image is more than four. Therefore, final
grade of both varices was recorded as 4.
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Fig. 5B —43-year-old man with grade 4 gastric submucosal and
adventitial varices before undergoing liver transplantation. CT image obtained
11 days after living donor liver transplantation shows decrease in size of
largest diameter of gastric submucosal (arrows) and adventitial
(arrowheads) varices to 4 and 2.9 mm, respectively, and number of
varices is not changed. Consequently, grades of varices decreased from 4 to 3
and 2, respectively.
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Fig. 5C —43-year-old man with grade 4 gastric submucosal and
adventitial varices before undergoing liver transplantation. On CT image
obtained 1 year after transplantation, gastric submucosal (arrows)
and adventitial (arrowheads) varices are still seen.
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Fig. 6A —52-year-old man with retroperitoneal varices shown even 1
year after living donor liver transplantation using left lateral segment.
Preoperative CT scan shows conglomerated and enhanced varices
(arrows) at left retroperitoneal space. These varices were recorded
as grade 4 by radiologists.
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Fig. 6B —52-year-old man with retroperitoneal varices shown even 1
year after living donor liver transplantation using left lateral segment. CT
image obtained 1 year after transplantation shows persistent grade 4
retroperitoneal varices (arrows).
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Fig. 7A —6-year-old boy who underwent living donor liver
transplantation due to fulminant hepatic failure. Preoperative CT image
obtained during portal venous phase shows splenomegaly. Spleen (S) volume was
measured as 139.6 cm3.
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Fig. 7B —6-year-old boy who underwent living donor liver
transplantation due to fulminant hepatic failure. CT image obtained 10 days
after transplantation shows marked decrease of splenomegaly. Spleen (S) volume
at that time was measured as 92 cm3. On CT image obtained 14 months
after transplantation (not shown), spleen size had not decreased further and
spleen volume was measured as 93.5 cm3.
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In Table 3, the mean
differences in grade of each varix and the spleen volume reduction rate
between the preoperative and fourth CT examinations are summarized according
to the type of donor liver graft (total vs partial), the presence of
postoperative adverse effects, and the presence of hepatic venous congestion.
Although the differences of variceal size and spleen volume reduction between
the two CT scans tended to be larger in the total liver graft group than in
the partial graft group in most varices and splenomegaly, there was no
significant difference between the two groups (p > 0.05). In
addition, even though the differences of variceal size and spleen volume
reduction between the two CT scans tended to be larger in the group without
postoperative adverse events than the group with those events, there was also
no significant difference (p > 0.05). Furthermore, the differences
of variceal size and spleen volume reduction between the two CT scans did not
significantly differ between the two groups with and without hepatic venous
congestion (p > 0.05). In other words, the type of liver graft,
the presence of postoperative adverse events, and the presence of hepatic
venous congestion did not affect the degree of change on the varices or spleen
volume reduction between preoperative CT examination and the fourth follow-up
CT examination performed approximately 1 year after transplantation
(Table 3).
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TABLE 3: Mean Difference of Grade of Each Varix and Spleen Volume Reduction
Between Preoperative CT and Fourth Postoperative CT
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The degree of the changes in the varices and the splenic volume reduction
between the two CT scans (preoperative and fourth postoperative) was not
significantly correlated with the difference of PV diameters between the
recipient and anastomotic sites (p > 0.05). In addition, the
degree of the changes in the varices between the two CT scans (preoperative
and fourth postoperative) was not significantly correlated with the weight of
the transplanted liver (p > 0.05). However, the rate of volume
reduction of the spleen was weakly but significantly correlated with the
transplanted liver weight (Pearson's correlation coefficient, r =
0.401; p < 0.0001).
Discussion
In our study, all varices except the splenic and retroperitoneal varices
and spleen volume dramatically decreased during the early postoperative period
(i.e., within 2 weeks) and became stable 2 months after transplantation.
Because liver regeneration and volume increase become most active 2 weeks
after liver transplantation and remain active for 2 months after liver
transplantation [20], the
evolution of most varices may also follow the trend of liver regeneration.
Indeed, such a hypothesis was partially proven in our study.
Like our results, the results of Chezmar et al.
[11] also have shown that
splenic and retroperitoneal varices among the various types of varices persist
for the longest period of time in the largest number of patients. From our and
previous studies, we conclude that splenic and retroperitoneal varices may
remain even 1 year after liver transplantation. Unlike esophageal and gastric
varices, splenic and retroperitoneal varices frequently have large systemic
draining routes, such as the splenorenal shunt and mesocaval or
retroperitoneocaval shunt, even before a portal decompression procedure such
as liver transplantation. Because the two varices can be easily bypassed and
decompressed by a large portosystemic shunt, the decompression effect of
portal hypertension after liver transplantation would be minimal compared with
other types of varices in which portal decompression by transplantation is
critical. Indeed, several reports about liver transplantation have shown that
portosystemic shunts, such as the splenorenal or mesocaval shunts through the
large left renal or retroperitoneal vein, may persist after liver
transplantation and may induce the portal steal phenomenon. Therefore, several
authors have insisted that ligating those large runoffs during surgery can
maintain the appropriate amount of flow through an anastomosed PV
[21–23].
We believe that the portal steal phenomenon after liver trans plant ation
might be indirect evidence of the slow and insignificant decrease and lack of
marked change in these two types of varices.
Esophageal varices evolved significantly for 1 year after liver
transplantation. Indeed, at the fourth postoperative CT examination, the grade
of esophageal varices was 0 in most patients (63/74, 85.1%) and only two
patients (2/74, 2.7%) had grade 2 varices. These results may be indirectly
responsible for the marked decrease in the incidence of esophageal variceal
bleeding after liver transplantation. Spleen volume also evolved rapidly and
significantly within 2 weeks after liver transplantation. After 2 weeks,
spleen volume continuously decreased; however, the differences in spleen
volumes between the two following successive CT scans were not significant.
Even 1 year after liver transplantation, on the fourth CT scan, the mean
postoperative spleen volume (456.05 cm3) was greater than the
normal range (219 ± 76 cm3)
[24], and most patients
(66/76, 86.8%) still had splenomegaly.
There was a discrepant result regarding the effect of the type of
transplanted liver (total vs partial) and of transplanted liver weight on the
rate of spleen volume reduction. Because there was a weak but significant
correlation between transplanted liver weight and spleen volume reduction rate
(correlation coefficient, r = 0.401), we expected that the volume
reduction rate would be significantly greater in patients receiving total
liver grafts than those with partial liver grafts, but this was not the case.
Usually DDLT provides larger liver grafts than LDLT, but the regeneration
power of the liver obtained from a deceased liver is known to be less than
that of the living donor liver graft. That may be one of the reasons for the
insignificant differences of variceal change and spleen volume reduction
between DDLT and LDLT. Another possible reason for such a discrepancy between
our expectation and our results is that there might be a threshold in weight
or volume of the transplanted liver to decompress the portal pressure to the
normal range. In other words, a partial donor liver, which is always used for
LDLT, would be large enough to normalize the portal pressure. Beyond a certain
amount of weight or volume of donor liver—usually in total liver
transplantation, there might be no further reduction of portal hypertension.
This theory is also one of the major rationales to use partial liver grafts
from living donors for liver transplantation.
Our results regarding hepatic congestion also support our threshold theory.
In our study, there were no significant differences in variceal changes and
spleen volume reduction between the presence and absence of hepatic venous
congestion. This finding may indirectly indicate that graft volume
corresponding to the right posterior segment or left lateral segment is enough
to decompress portal hypertension in the postoperative stage. However, our
hypothesis should be studied further using a larger number of transplantation
cases.
Contrary to our expectation, the presence of postoperative adverse events
also did not influence the evolution of variceal grade and splenomegaly.
Theoretically, vascular complications such as the narrowing of venous
anastomosis lead to persistent portal hypertension and consequently to no or
minimal change of portosystemic collaterals or splenomegaly. However, we
believe that because ethical concerns dictate the necessity of prompt and
adequate treatments such as angioplasty or reoperation in most patients who
had postoperative adverse events, these events were never allowed to become
influencing factors for the evolution of portosystemic collaterals or
splenomegaly. In addition, although the criteria we used for the determination
of posttransplantation rejection were based on results from pathology reports,
the real clinical impact of pathologic rejection is still under debate.
Indeed, the histopathologic diagnosis of acute rejection may not automatically
signal that treatment is indicated, particularly if rejection is low grade
[25]. This uncertainty about
the clinical impact of rejection may be one of the reasons the presence of
rejection did not affect the evolution of varices and spleen volume over
time.
Our study has several limitations. First, because we do not have long-term
follow-up data regarding whether the evaluated patients eventually had
variceal bleeding, we cannot conclude that such morphologic decreases of the
varices truly indicate a decreased incidence of variceal bleeding. However,
previous large prospective studies regarding the incidence of variceal
bleeding before and after liver transplantation have shown that bleeding
prevalence significantly decreases after transplantation.
Second, we only followed the patients for approximately 1 year after liver
transplantation. Therefore, we cannot know whether each varix evolved
continuously after the 1-year mark. On the basis of the results of both our
study and that of Chezmar and colleagues
[11], we think that varices
would continue to evolve slowly even after 1 year. However, to know the
long-term results regarding variceal evolution, further study is needed.
Third, with regard to spleen volume, we did not use manual tracing or
automatic measurement methods to calculate spleen volume. Rather, we
calculated spleen volume with a previously reported formula using three
parameters: width, thickness, and length
[18]. Such a simple method can
lead to errors in calculating organ volume; however, because change in volume,
not absolute volume, was the only factor in our study we focused on, we think
that such a method can be applied in our study.
Fourth, the number of CT scans at each follow-up examination varied because
our surgeons had no strict strategy to determine CT follow-up interval and
frequency for transplant recipients before 2005 and therefore may have
introduced a selection bias. Fifth, because of the retrospective study design,
various types of CT scanners and scanning parameters were used. However,
because portal phase CT images were obtained at 3- to 5-mm reconstruction
intervals in every CT examination, analyses of varices and spleen volume
should not have been influenced by these factors. Finally, because
radiologists did not determine the grade of varices and spleen volume
independently, interobserver variation may be problematic.
In conclusion, most varices and spleen volume significantly decrease in the
early postoperative period (2 weeks) and become stable approximately 2 months
after liver transplantation. Esophageal varices evolve continuously for 1 year
after transplantation, and there is more volume reduction of the spleen in
patients with large transplanted livers.
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Abstract
Introduction
