Surgical Science, 2011, 2, 102-108
doi:10.4236/ss.2011.22021 Published Online April 2011 (
Copyright © 2011 SciRes. SS
Partial IVC Clamping Improves Intraoperative
Hemodynamic Parameters in the Rodent Portacaval
Anastomosis Model
Merhdad Asgeri1, Nash Waghray1, Kevin Mullen1, N. Nade3, Henri Brunengraber4, Juan Sanabria2,4
1Departments of Medicine MetroHealth Medical Center and University Hospitals–Case Medical Center,
Case Western Reserve University School of Medicine, Cleveland, OH
2Departments of Surgery, University Hospitals–Case Medical Center and
Case Western Reserve School of Medicine, Cleveland, OH
3Departments of Anest hesi ol o gy an d Surgery, VA Western New York Healthcare System,
State University of New York at Buffalo, Buffalo, NY
4Department of Nutrition, Case Western Reserve University School of Medicine, Cleveland, OH
E-mail:, juan.sanabria@ca
Received January 23, 2011; revised February 28, 2011; accepted Ma rch 25, 2011
The mechanisms involved in the development of hepatic encephalopathy still remain uncertain. The rodent
portacaval shunt is a model that reproduces many of the pathological features observed in humans (1), but is
a technically demanding exercise. While the traditional technique involves complete occlusion of the IVC, a
c-clamp was fashioned to partially clamp the IVC thereby sustaining venous return and cardiac output. The
aim of this study is to determine if the c-clamp technique provides greater hemodynamic stability and en-
hances the success rate of the portacaval shunt procedure. To answer this question, two experimental groups,
c-clamp (N = 7) and cross-clamp (N = 7), and a sham group (N = 3) were included. Intraoperative hemody-
namic parameters were recorded at specific times during the procedure. The c-clamp group showed greater
hemodynamic stability when compared to the cross-clamp group. It was manifested by 1) significantly
higher mean arterial blood pressure [63 (range, 8) vs 47 (range, 10) mmHg, p < 0.05], 2) faster capillary re-
fill [4 (range, 2) vs 6 (range, 2) seconds, p < 0.05], 3) higher urinary output [0.18 (range, 0.02) vs 0.14 (range,
0.02) ml, p < 0.05], and 4) lower bowel wet-to-dry ratio [4.168 (range, 0.258) vs 4.731 (range, 0.271), p <
0.05]. We conclude partial IVC clamping improves hemodynamic stability during the construction of the rat
portacaval shunt model.
Keywords: Portacaval Anastomosis, Portosystemic Shunt, Microvascular Surgery, Ivc Clamping, Surgical
Technique, Encephalopathy-Like Rodent Model
1. Introduction
Hepatic encephalopathy (HE) is a complex neuropsy-
chiatric syndrome characterized by global depression of
CNS function, progression to impaired consciousness,
and coma. The varying severity typically seen in patien ts
is associated with evidence of liver failure and portosys-
temic shunt formation. Surgical construction of a porta-
caval shunt in rats reproduces many of the pathological
features of portosystemic hepatic encephalopathy in hu-
mans [1]. Developed by Lee and Fisher in 1961, the ro-
dent portacaval shunt model has been well validated but
remains a technically demanding procedure [2-4]. Hemo-
dynamic instability associated with complete occlusion
of both the portal vein and the inferior vena cava remains
the underlying factor in mortality rates related to shunt
construction [5,6]. The instability is manifested in the rat
as hypotension, bowel edema, reduction of urine output,
and hypovolemic cardiac arrest [5,7-10].
Since the interpretation of experimental work in the
rodent portacaval shunt model could be significantly
influenced by the performance of the operation and its
complications, several technical modifications have been
suggested to improv e animal survival and shun t patency.
Changes have focused on reducing the procedural time
of portal vein ligation, IVC occlusion, and completion of
portacaval anastomosis [8,11,12]. We hypothesized that
complete occlusion of the IVC substantially reduced ve-
nous return and was a major factor in the technical diffi-
culties associated with the traditional cross-clamp
method. The concept of partial IVC occlusion is not new;
Welch et al. first reported its use for portacaval shunt
construction in dogs [13]. Later, Jacob et al. applied this
technique to the rodent model [14]. Partially clamping
the IVC provides the operator with greater time to con-
struct the anastomosis while limiting the severity of
hemodynamic compromise. This is especially important
for the surgeon during the learning phase of the proce-
dure. Therefore, we fashioned a micro-serrifine clamp to
create a c-clamp that would only partially occlude the
IVC. Partial clamping would be verified by direct visu-
alization of the IVC and indirectly by measuring the
mean arterial pressure. By sustaining venous return, in-
traoperative hemodynamic stability would improve and
preserve renal function. The current study was designed
to evaluate the c-clamp vs the traditional cross-clamp
technique in the construction of the portacaval shunt in
rats. Refining this animal model of encephalopathy may
enhance the interpretation of fu ture research and it trans-
lation to the human.
2. Materials and Methods
2.1. Animals
Male Sprague-Dawley rats weighing 275-325 grams
were used for purpose of the present study. After arrival,
animals were in quarantine for five days. Healthy rodents
were kept in fixed daynight cycles (12h) at standard
room temperature and humidity, fed with rat chow and
provided with water ad libitum until scheduled for sur-
gery. After completion of the shunt, rats were sacrificed
using a high flow of CO2 into the anesthetic chamber. All
surgical procedures were approved and performed ac-
cording to the regulations of the IAIRB at Case Western
Reserve University.
2.2. Hemodynamic Parameters
In order to evaluate two different techniques in the con-
struction of the portacaval shunt, several intra-operative
variables were recorded 1) at the time of skin incision, 2)
two minutes after IVC clamp placement, and 3) two
minutes after shunt clamp release. They included: mean
arterial pressure (MAP), heart and respiratory rates, rec-
tal temperature, capillary refill, bowel color, urine output
and intestinal wet-to-dry ratio. Th e ventral tail artery was
cannulated with MRE-33 tubing (0.014 in ID, 0.033 in
OD, BrainTree Scientific) and connected via transducer
to Digimed BP analyzer machine (Micromed Inc. Model:
BPA-400a) to record the heart rate and the blood pres-
sure in mmHg. After lubrication, a rectal thermometer
was placed and the temperature was maintained between
37-38˚C via a heating lamp [15,16]. Once the abdominal
cavity was entered, the bladder was emptied of urine by
manual compression. A non-traumatic clamp was then
placed occluding the urethra. Upon shunt clamp release,
urine output was measured by suctioning the urine from
the bladder with a 1mL syringe connected to a 25G nee-
dle. Baseline bowel color and capillary perfusion were
evaluated by an observer who had no knowledge as to
the type of procedure being performed. Bowel color was
identified as pink, pink/purple, or purple. Capillary per-
fusion was noted by blanching a segment of proximal
small bowel, releasing, and recording the refill time in
seconds. In order to obtain information regarding intes-
tinal edema, a 6 cm length of proximal small bowel (be-
ginning two centimeters from the pylorus) was removed
immediately after euthanasia. The section of bowel was
examined, gently milked dry, and weighed (Sargent-
Welch scale, TL 400-DR). Subsequently, the proximal
small bowel segment was placed in a 60˚C dessicator
oven (Quincy Lab Inc., Model: 10-210) and allowed to
dry until dry weights were equal. The intestinal wet to
dry ratio was determined to provide a measure of intes-
tinal edema [16].
3. Porto-Systemic Shunt Procedure
Animals were weighed (Model: Scout Pro SP2001) and
placed in a chamber for induction of anesthesia by a gas
mixture of Isoflurane: O2 (2:98% at 3L/min). Uncon-
scious rodents were positioned in sup ine position , affixed
to a metal board and maintained with a similar gas mix-
ture through a nose cone (2 L/min). Time from induction
of anesthesia to laparotomy incision, and shunt clamp
release (completion of portacaval anastomosis) were
recorded (Table 1).
3.1. Shunt Dissection
The abdominal wall was shaved and the surgical site was
cleaned with alcohol and allowed to dry. A midline inci-
sion was made from the bladder to the xyphoid process.
Warm moist gauzes in saline solution (NS 0.9%) were
used to cover and position the abdominal contents to
provide a wider surgical field. The area of abdominal
contents were irrigated with saline solution (NS 0.9%)
every 10 minutes. An operative scope was positioned
(Olympus, 10X). The portal vein was dissected along its
Copyright © 2011 SciRes. SS
Copyright © 2011 SciRes. SS
Table 1. Parameters reco r de d during construction of portacaval shunt.
Rodent Portacaval Shunt Data [Median (Range)]
Variables Sham (N = 3) C-Clamp (N = 7) Cross Clamp (N = 7) P-value§
Weight (grams) 294.4 (7.4) 302.7 (22) 296.3 (20.1) 0.38
Anesthesia Time (minutes) 77 (2) 77 (9) 78 (6) 0.29
Laparotomy to SCR(minutes)* 52 (1) 55 (5) 56 (6) 0.22
Mean Arterial Pressure
Baseline 114 (4) 114 (10) 115 (8) 0.45
IVC clamp 63 (8) 47 (10) < 0.05
SCR 110 (4)** 86 (12) 71 (9) < 0.05
Heart Rate
Baseline 358 (3) 356 (16) 358 (13) 0.32
Respiratory Rate
Baseline 72 (4) 72 (8) 72 (6) 0.37
IVC clamp 63 (8) 63 (9) 0.23
SCR 71 (4)** 66 (11) 67 (7) 0.34
Rectal Temp (˚C)
Baseline 37.9 (0.6) 38.1 (1.6) 37.2 (1.6) 0.29
IVC clamp 37.3 (1.1) 37.4 (0.8) 0.26
SCR 37.1 (0.6)** 36.9 (0.4) 36.9 (0.4) 0.29
Capillary Perfusion (seconds)
Baseline 1 (0) 1 (0) 1 (0)
IVC clamp 2 (1) 2 (0)
SCR 1 (0)** 4 (2) 6 (2) < 0.05
Bowel Color #
Baseline 1 (0) 1 (0) 1 (0)
IVC clamp 2 (0) 2 (0)
SCR 1 (0)** 2 (1) 3 (1) 0.05
Urine Output (mL) 0.20 (0.02) 0.18 (0.02) 0.14 (0.02) < 0.05
Intestinal W/D Ratio 3.820 (0.115) 4.168 (0.258) 4.731 (0.271) < 0.05
*SCR denotes s hunt clamp release: all clamps from portal vein and IVC are rel eased at completion of shunt; **Sham rat values at completion
of procedure; # Bowel Color: 1-pink, 2-pink/purple, 3-pur ple; § Denotes compar ison between c-clamp an d cross clamp groups.
tract and isolated to about 1.5 cm in length, with gastro-
duodenal vein sectioned between ligatures (6:0’s). Fur-
ther isolation of the hepatic artery was completed by
dissecting the fibrous tract along the hilar end of the por-
tal vein (2-4). Subsequently, the inferior vena cava was
dissected from the hepatic parenchyma to the right renal
vein to an approximate length of 1.5 cm.
3.2. Shunt Creation
The type of procedure was randomly identified by an
assistant prior to time of clamp placement. A micro-ser-
rifine vascular clamp (Fine Science Tools, jaw width 1
mm) was modified to create a clamp that would only
partially occlude the IVC. A c-clamp or regular clamp
was brought to the field. The IVC was cross clamped
above and below the v enotomy site or partially clamped
using a c-clamp, above the renal veins. Partial clamping
was verified by direct intraoperative examination of the
IVC. A 4mm incision was made along the medial aspect
of the occluded wall of th e IVC using a Phaco blade. The
portal vein was subsequently ligated at the bifurcation
and a clamp was placed on the distal end of the isolated
portal vein. A partial venotomy was performed on the
lateral aspect of the hepatic end of the portal vein. This
approach increased the size of the portal vein aperture so
as to match the corresponding IVC opening (12). A por-
tal vein clamp was used to approximate the apertures of
the IVC and portal vein to facilitate the anastomosis. Th e
upper pole of the portal vein was stitched to the corre-
sponding upper pole of the IVC with 9:0 Prolene (Ethi-
con, NJ). The posterior walls of the veins were secured
in continuous running suture to the inferior pole at which
point the needle was exteriorized from the inferior pole
of the IVC. The anterior walls were secured in a con-
tinuous running suture up to the superior pole. The portal
vein clamp was temporarily released to remove air from
the anastomosis line. The upper pole was secured com-
pleting the anastomosis.
4. Statistical Analysis
Results are expressed as median and ranges. The data
was analyzed by parametric (two sided ttest) and non-
parametric tests (Wilcoxon Rank Sum Test) where ap-
propriate. Associations between variables were deter-
mined by linear regression analysis and Pearson’s corre-
lation coefficient using SPSS17 (Chicago, IL, licensed to
CWRU). Statistical significance was considered to be
achieved at a p < 0.05.
5. Results
Animal weights, procedure OR time and anesthesia time
as well as baseline hemodynamic parameters were com-
parable among groups (Table 1). In contrast, there were
significant differences in the hemodynamic parameters
after IVC clamp placement and shunt clamp release
when groups were compared. The c-clamp technique had
statistically significant greater mean arterial pressures
after IVC clamp placement and shunt clamp release
(Figure 1), higher urine output (Figure 2) and faster
capillary refill at the completion of the shunt procedure.
The median MAP after IVC clamping was 63 (range, 8)
mmHg in the c-clamp group and 47 (range, 10) mmHg in
the cross clamp group (p < 0.05, Wilcoxon rank sum
Figure 1. Mean arterial pressure at baseline, Two minutes
after IVC clamp placement and Two minutes after shunt
clamp release. (*,**p < 0.05 – Denotes statistical signifi-
cance betw ee n groups).
Figure 2. Urinary output at completion of portacaval shunt.
(*,**p < 0.05 – Denotes statistical significance between
After shunt clamp release, MAP demonstrated a simi-
lar pattern (c-clamp group 86 (range, 12) mmHg vs cross
clamp group 71 (range, 9) mmHg, p < 0.05, Wilcoxon
rank sum test). Urine production was significantly greater
in the sham group [0.20 (range, 0.02) mL, p < 0.05]
when compared to the c-clamp group [0.18 (r ange, 0.02)
mL, p < 0.05] and the cross-clamp group [0.14 (range,
0.02) mL, p < 0.05, Wilcoxon rank sum test]. Further
analysis was performed to evaluate for correlation be-
tween the mean arterial pressure and the rate of urine
output. The results demonstrated a significant positive
linear relationship between mean arterial pressure after
IVC clamp placement for both c-clamp and cross clamp
groups (Pearson’s correlation coefficient, cclamp: r =
0.95, cross clamp: r = 0.96). Sustained mean arterial
pressure after IVC clamp placement correlates with in-
creased urine output, suggesting improved renal perfu-
sion and GFR. In addition, the evaluation of capillary
Copyright © 2011 SciRes. SS
Figure 3. Small bowel wet-to-dry ratio, a surrogate for in-
testinal edema. (*p < 0.05).
perfusion was used as a surrogate of not only intestinal
perfusion but of peripheral perfusion. After shunt clamp
release, there was a statistically significant difference in
capillary refill time between the c-clamp group and the
cross clamp group [4 (range, 2) vs 6 (range, 2) seconds,
p < 0.05, Wilcoxon rank sum test].
To examine bowel edema, intestinal wet-to-dry ratios
were measured at the proximal small intestine in each
animal. The data reveals a statistically significant higher
ratio of tissue water content in the cross clamp group
[4.731 (range, 0.271)] when compared to the c-clamp
group [4.168 (range, 0.258)] and sham group [3.820
(range, 0.115), p < 0.05, Wilcoxon rank sum test] (Fig-
ure 3). A significant difference was also noted in the
tissue water content between the cclamp and sham rat
groups. Further analysis demonstrated a significant nega-
tive linear relationship between mean arterial pressure
(MAP) after IVC clamp placement and intestinal wet-to-
dry ratio (Pearson’s correlation coefficient, c-clamp: r =
–0.95, cross clamp: r = –0.95). The degree of reduction
in mean arterial pressure is associated with increased
intestinal wet-todry ratio, thus, greater intestinal edema.
6. Discussion
The rat portacaval shunt is a reliable model of portosys-
temic hepatic encephalopathy (1-4), but remains a tech-
nically demanding exercise. To the best of our knowl-
edge, the present study is the first one to use objective
intraoperative hemodynamic parameters to evaluate a
modified portacaval shunt procedure. Our results showed
significantly greater hemodynamic stability in the ani-
mals that underwent the portacaval shunt using the
c-clamp compared to the cross clamp technique. While
surgical and anesthesia time can impact hemodynamic
stability, their effects were comparable among the groups.
The use of this technique may enhance th e interpretation
of future research in encephalopathy by decreasing sur-
gical bays.
Consistent with previous animal studies [17, 18], we
demonstrated a significant linear correlation between
MAP and tissue perfusion. The severity of hypotension
after IVC clamp placement predicts the degree of intes-
tinal edema and the reductio n in renal perfusion resulting
in decreased urine output. Studies in dogs and rodents
have demonstrated that rapid changes in arterial pressure
result in changes in urine production [17,18]. Steele and
colleagues demonstrated significant changes in urine
flow in an average of 6 seconds following changes in
arterial pressure [18]. Consistent with these findings, the
transient reduction in mean arterial pressure after IVC
clamp placement resulted in significantly diminished
urine production in both groups (c-clamp and cross
clamp) versus sham operated controls. Human studies
further corroborate this finding, demonstrating that renal
perfusion is significantly reduced in sh ock and th e reduc-
tion of urin e production is proportional to the severity of
hypotension [19,20].
By sustaining venous return, the specially designed
c-clamp maintains greater hemodynamic support.
Analogous to rat shock models, the intraoperative pa-
rameters in the cross clamp group revealed significant
hypotension resulting in greater intestinal ischemia and
edema [21-23]. Intestinal hypoxia and ischemia result in
bowel edema and increased microvascular permeability
[21-24]. This leads to increases in gut derived LPS in the
circulation resulting in the release of oxygen free radicals
and TNF [21,22]. In animal models, LPS concentrations
are significantly elevated as early as 25 minutes after
induction of shoc k [24]. Therefore, greater hemodynamic
stability seen in the c-clamp group places the animals
under less stress and reduces the likelihood of ischemic
damage to the bowel.
The reduction in cardiac output associated with the
cross clamp technique establishes factors that may com-
plicate the study of hepatic encephalopathy in this animal
model. Tissue hypoperfusion secondary to portal vein
and IVC occlusion in humans results in multiple meta-
bolic abnormalities including hypocalcemia, hyper-
kalemia, hypoxia, and subsequent metabolic acidosis
[21-26]. In rodent studies, electrolyte abnormalities such
as hypocalcemia can lead to activation of specific cal-
cium channels (csNSC) resulting in altered neuronal in-
hibition [27]. Furthermore, transient periods of cerebral
ischemia have been implicated in the elevation of pe-
ripheral type benzodiazepine receptor (PTBR) densities
[28-31]. Expressed on normal astrocytes, the upregula-
tion of PTBR’s leads to the production of specific neu-
rosteroids that activate the GABA receptor enhancing
further neural inhibition. In addition, the systemic in-
Copyright © 2011 SciRes. SS
flammatory response observed with hypotension, i.e.
TNF and IL-1 production, also upregulates PTBR ex-
pression [28,29,32]. These mechanisms of neurological
dysfunction have been implicated in traumatic brain in-
jury, focal cerebral ischemia, global cerebral ischemia
and hepatic encephalopathy [31,33,34]. Thus, the sever-
ity of hypotension associated with the cross clamp tech-
nique may result in the upregulation of PTBR densities
thereby potentiating any neural inhibition and confound-
ing investigations in the rat model of hepatic encephalo-
Limitations of the study include the subjective nature
of accounting for respiratory rate and assessment of
bowel capillary perfusion. Data for heart rate was limited
to the baseline line measurement as the Digimed BP ana-
lyzer machine could not accurately assess heart rates
below a blood pressure of 90 mmHg. Further, the rela-
tively small sample size in each group is a limitation in
defining the statistical power of the results and a larger
scale study is needed to confirm these findings.
Based on the results of the present study, we con clude
that partial clamping of the IVC results in greater hemo-
dynamic stability compared to the traditional cross clamp
technique in the construction of the portacaval shunt.
Therefore, the technique offers the potential for in-
creased animal survival and a model with fewer con-
founding factors affecting the study of portosystemic
hepatic encephalopathy.
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