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Selective hepatic vascular exclusion and Pringle maneuver:

A comparative study in liver resection
W. Zhou*, A. Li, Z. Pan, S. Fu, Y. Yang, L. Tang, Z. Hou, M. Wu
The Third Department of Hepatic Surgery, Eastern Hepatobiliary Surgery Hospital, 225 Changhai Road, Shanghai 200438, P.R. China
Accepted 4 July 2007

Abstract
Objective: Most liver resections require champing of the hepatic pedicle (Pringle maneuver) to avoid excessive blood loss. But Pringle
maneuver cannot control backflow bleeding of the hepatic vein. Resection of liver tumors involving hepatic veins may cause massive hemorrhage or air embolism from injuries of the hepatic vein. Although total hepatic vascular exclusion (THVE) can prevent bleeding of the
hepatic vein effectively, it also may result in systemic hemodynamic disturbance because of the clamped inferior vena cava (IVC). SHVE,
a new technique, can control the inflow and outflow of the liver without clamping the vena cava. We compared the effects of selective
hepatic vascular exclusion (SHVE) and Pringle maneuver in resection of liver tumors involving the junction of the hepatic vein.
Methods: From January 2000 to October 2005, 2100 patients with liver tumors had undergone liver resections in our department. Among
them, tumors of 235 cases adhered to or were close to the junction of one or more hepatic veins. Both SHVE and Pringle maneuver were
used to control blood loss during hepatectomy. These 235 cases were divided into two groups: Pringle maneuver group (110) from January
2000 to December 2002 and SHVE group (125) from January 2003 to October 2005. Data were analyzed regarding the intraoperative and
postoperative courses of the patients. In the SHVE group, total SHVE (clamping the porta hepatis and all major hepatic veins) was used in
69 cases and partial SHVE (clamping the porta hepatic and one or two hepatic veins) in 56 cases. There were three methods in hepatic veins
occlusion: ligating with suture, encircling and occluding with tourniquets and clamping with Satinsky clamps.
Results: There was no difference between the two groups regarding the age, gender, tumor size, cirrhosis and HBsAg rate, ischemia time
and operating time. Intraoperative blood loss and transfusion requirements were significantly decreased in the SHVE group. Hepatic veins
rupture with massive blood loss occurred in 14 and air embolism in three during the tumor resection, but there was no massive blood loss
and air embolism in the SHVE group due to hepatic vein occlusion. Postoperative bleeding, reoperation, liver failure and mortality rate were
higher, and ICU stay and hospital stay were longer in the Pringle group than those in the SHVE group.
Conclusion: SHVE is much more effective than Pringle maneuver in controlling intraoperative bleeding. It can prevent massive blood loss
and air embolism from hepatic veins rupture and can reduce the postoperative complication rate and mortality rate. Clamping the hepatic
veins with Satinsky clamps is much safer and easier than ligating with suture and occluding with tourniquets.
2007 Elsevier Ltd. All rights reserved.
Keywords: Liver neoplasm; Hepatic vein exclusion; Hepatectomy

Introduction
Although some hepatic resections can be safely performed without any kind of liver vascular control, vascular
occlusion is required in most hepatectomies, especially
when liver tumors are very large or close to the major vessels.1e6 In most cases, inflow occlusion is used by means of
portal tried clamping (Pringle maneuver).7 Pringle maneuver, however, can only stop bleeding from the port vein and
* Corresponding author. Tel.: 86 21 25070792; fax: 86 21 65341828.
E-mail address: ehphwp@126.com (W. Zhou).

hepatic artery, but cannot prevent backflow bleeding from

hepatic veins. If the liver tumor adheres to or is very close
to the junction of the hepatic vein, fatal hemorrhage and air
embolism may develop. These complications can be prevented simply by total hepatic vascular exclusion
(THVE),8,9 which involves clamping both inflow and outflow of hepatic vascular occlusion, with clamping the intrahepatic and suprahepatic vena cava (IVC) being included.10
THVE causes major hemodynamic changes,11 which are
not always well tolerated and even require anesthetic
management.12 Another technical way is employed to
clamp the hepatic vein without clamping the IVC,13 which

0748-7983/$ - see front matter 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.ejso.2007.07.001
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Surg Oncol (2007), doi:10.1016/j.ejso.2007.07.001

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W. Zhou et al. / EJSO xx (2007) 1e6

can preserve caval flow and avoid hemodynamic disturbance. This technique is called selective hepatic vascular
exclusion (SHVE)14 or hepatic vascular exclusion with
preservation of the caval flow (HVEPC).15
Patients and methods
From January 2000 to October 2005, 235 patients with
tumors adhering to the junction of the hepatic veins underwent hepatic resections. According to different ways of
hepatic vascular exclusion, these patients were divided
into two groups: Pringle maneuver group (110) from January
2000 to December 2002 and SHVE group (125) from
January 2003 to October 2005. The preoperative data and
operative indications of two groups are shown in Tables 1
and 2, respectively. In the Pringle group, tumors adhered
to one, two and three major hepatic veins and IVC, respectively, developed in 37, 47, 26 and 38 cases; and in 44, 46,
35 and 43 cases in SHVE group.
Routine preoperative assessment and a series of imaging
including ultrasonography (US), computed tomography
(CT) or/and magnetic resonance imaging (MRI) were undertaken in all patients; preoperative chemoembolization
was carried out in 17 patients (eight in Pringle group and
nine in SHVE group). Various types of hepatectomy
performed in two groups are shown in Table 3.
Surgical technique
We entered the abdomen via a bilateral subcostal incision. The ligaments were dissociated around the liver after
the tumor was assessed resectable by intraoperative US. In
the Pringle group, the hepatoduodenal ligament was
clamped with a tourniquet; the aberrant arteries originating
from the left gastric artery were occluded; and the hilar
structures were transected and ligated intrahepatically.
The hemostases of raw surface were sutured with 3e0 or
4e0 polypropylene. If the liver was normal, the porta
hepatis was continuously clamped for 30e40 min; if the
liver developed cirrhosis, the porta hepatis was

intermittently clamped for 15e20 min with a 5-min interval. IVC clamp bands were pre-placed in 20 patients in
the Pringle group and 24 patients in the SHVE group,
and no occlusion was used in the SHVE group, but used
in 10 patients in the Pringle group because of the massive
bleeding and/or air embolism of the ruptured hepatic vein.
In the SHVE group, the IVC was disconnected from the
liver by dissecting and ligating the short hepatic veins. On
the right side, the hepatocaval ligament was dissected and
ligated, and the right hepatic vein was exposed and
encircled.16,17 On the left side, the ligament venosum was
transected, exposing the junction of the left hepatic vein
and IVC, and the common trunks of the left and middle
hepatic vein were dissected free from surrounding tissues
and encircled together.18,19 In four cases of this group,
the left and middle hepatic veins joined the IVC separately,
so they were occluded individually. When the right inferior
hepatic vein was present, it was either encircled or ligated
according to its size and the side of the resection. No
hepatic vein was injured during dissecting.
Three occlusion methods were selected: (1) ligating the
hepatic veins of the resected lobe with polypropylene 1e0
sutures (ligating the right hepatic when the right live resection was performed); (2) encircling the hepatic veins with
vessel loops and clamping them by a tourniquet; and (3)
clamping the hepatic veins with bulldog clamps or Satinsky
clamps. Liver blood inflow was occluded as done in the
Pringle group.
Liver resection was carried out by a clamp-crushing
manner in all patients. Cholecystectomy was performed
in 120 patients.
Anesthetic management was accomplished by general
anesthesia. A SwaneGanz catheter and a radial arterial
line were inserted. The central venous pressure (CVP)
was maintained during the liver resection.

Data and statistical analysis

The data of two groups were collected and compared,
including intraoperative blood loss and transfusion, warm

Table 1
Preoperative data for undergoing hepatectomy using the Pringle maneuver or SHVE
Parameter
a

Age (years)
Sex (male/female)
Tumor size
(cm)a
Hemoglobin (g/l)a
Platelet count
(109/l)a
Child-type (A/B)
With cirrhosis
HBsAg ()

Pringle group (n 110)

SHVE (n 125)

P-value

52.3 (4e76)
77/33
11.8 (4e41)

51.6 (0.5e71)
86/39
12.4 (3e48)

NS
NS
NS

130.4 (104.4e170.6)
174.3 (65.0e310.2)

131.2 (90.5e167.3)
180.2 (56.6e296.7)

NS
NS

102/8
65
71

113/12
74
90

NS
NS
NS

HVEPC: selective vascular exclusion with preservation of the caval flow.

a
Values were expressed as the median (range).
Please cite this article in press as: Zhou W et al., Selective hepatic vascular exclusion and Pringle maneuver: A comparative study in liver resection, Eur J
Surg Oncol (2007), doi:10.1016/j.ejso.2007.07.001

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W. Zhou et al. / EJSO xx (2007) 1e6
Table 2
Indications for liver resection using Pringle maneuver or SHVE
Indication

Pringle group
(n 110)

SHVE group
(n 125)

Hepatocellular carcinoma
With cirrhosis
Without cirrhosis
Cholangio carcinoma
Metastatic carcinoma
Hepatoblastoma
Hepatosarcoma
Giant hemangioma
FNH
Angiomyolipoma
Adenoma

74
63
11
5
4
1
1
20
2
2
1

86
70
16
4
5
2
2
24
1
1
0

ischemia time of the liver, operative time, morbidity and

mortality rate, reoperative rate, liver function failure, ICU
stay and hospital stay. The results were expressed as medians and ranges. The ManneWhitney U-test was used to
compare continuous variables, and the c2 test was used to
deal with discrete variables. P < 0.05 was considered statistically significant.
Results
During operative procedures
In both groups, there were no significant differences in
the age, sex ratio, preoperative status, tumor size, ratio of
malignant to benign lesions, resection type, volume of the
resected liver, CVP, warm ischemia time and operation
time (Tables 1e4). The intraoperative data showed that
the amount of blood loss and blood transfusion (packed
red blood cell) in the Pringle group was significantly
greater than that in the SHVE group (P < 0.01); patients
without blood transfusion in the Pringle group (21 patients)
were fewer than those in the SHVE group (85 patients); and
Table 3
Types of hepatectomy performed
Procedure

Pringle group
(n 110)

SHVE group
(n 125)

Right hepatectomy
Right extended
hepatectomy
To segment IV
To segment I
Left hepatectomy
Left extended hepatectomy
To segment V VIII
To segment I
Segment hepatectomy
IV V VIII
VII VIII
VI VII
VIII
IV I

24
13

26
16

9
4
19
16
11
5
38
15
6
7
8
2

11
5
21
17
13
4
45
17
6
10
10
2

there was no difference in the ratio of intraoperative hepatic

vein injury between the two groups (17/110 and 18/125). In
the Pringle group, massive blood loss developed in 14
patients (>2700 ml) and air embolism in three because of
the hepatic vein rupture, while there was no massive blood
loss and air embolism occurred in the SHVE group because
hepatic veins were occluded before hepatic resection.
Bleeding of the raw surface could not be controlled by
suture and compressed with gauze packing in four patients
of the Pringle group and in one patient of the SHVE group
for no coagulation.
In the SHVE group, total SHVE was used in 69 patients
with tumors adhering to the three major hepatic veins or the
right and middle hepatic veins; left partial SHVE was used
in 37 patients with tumors adhering to the left and middle
hepatic veins; right partial SHVE was used in 16 patients
with tumors adhering to the right or/and the right inferior
hepatic veins; and alternate SHVE was used in three
patients with tumors adhering to the three hepatic veins
(Table 5).
Complications and death
The postoperative complication rate was 51.8% in the
Pringle group and 39.2% in the SHVE group (Table 6).
In the Pringle group the amount of postoperative bleeding
(five patients) was higher than that in the SHVE group
(no patient) and reoperation at 3e12 h after the first operation was performed in five patients who developed postoperative bleeding. According to 50e50criteria
(prothrombin time (PT) <50% and serum bilirubin (SB)
>50 mmol/l on day 5 after operation) initially described
by Belghiti,20 liver failure developed in three patients,
which was caused by lower blood pressure during the operation from massive bleeding (5000e16,000 ml) in two and
by complication of cirrhosis and warm ischemia time of the
liver for 36 min in one.
Both ICU stay and hospital stay in the Pringle group
were longer than those in the SHVE group (P < 0.05).
Among two deaths occurred in the Pringle group, one
patient died of DIC and liver failure (blood loss
16,000 ml) and the other patient died of renal function
failure, resulting from massive bleeding and IVC obstruction. Five patients gauzes were removed at 6e8 days after
operation, and no rebleeding occurred. In our series, we
ligated one or two major hepatic veins in 16 cases, clamped
with bulldog or Satinsky clamps in 34, with tourniquet in
26, ligating tourniquet in 18, ligating clamping in 17,
and tourniquet clamping in 14.
Discussion
During liver resection, bleeding control should be
considered as one of the main priorities since it markedly
reduces postoperative morbidity and mortality.5,6,9,19,21
With more cases of liver resection in the area of the hepatic

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W. Zhou et al. / EJSO xx (2007) 1e6

Table 4
Intraoperative data for patients operated on the Pringle maneuver or SHVE
Intraoperative
dataa
Warm ischemia
time (min)
Operating time
(min)
CVP (mmHg)
Blood loss (ml)
Blood transfusion
(units)
(packed RBCs)
Notransfused
patients
Hepatic vein
rupture
Massive blood
loss
Air embolism
Gauze packing
of the resected
surface

Pringle group
(n 110)

P-value

SHVE group
(n 125)

Complication

22.5 (12e42)

21.7 (14e45)

NS

137.4 (90e240)

135.6 (80e200)

NS

4.6 (1e8)
1160
(200e16,000)
4.3 (0e72)

4.4 (1e10)
680
(100e6000)
2.2 (0e24)

NS
0.001*

21/110

85/125

0.001*

17/110

18/125

NS

14

0.001*

3
4

0
1

0.05*
0.05*

0.001*

*P < 0.05.
RBCs: red blood cells.
a
Values were expressed as the median (range).

cava junction, the morbidity associated with injury to

hepatic veins has also increased.17,22,23 Among the complications, massive bleeding and venous air embolism are the
most serious ones. Of the 2100 patients having liver resection, nearly 60% developed intraoperative massive bleeding, caused by injury to the hepatic veins. The Pringle
maneuver can only control inflow into the liver, but not
prevent backflow bleeding from the hepatic veins.
Table 5
Type of SHVE performed
Type of
hepatectomyb

Total SHVE Left SHVE Right SHVE Alternate

(n 69)
(n 37)
(n 16)
SHVEa
(n 3)

Right
hepatectomy
Right extended
hepatectomy
To segment IV
To segment I
Left hepatectomy
Left extended
hepatectomy
To V VIII
To I
Segment
hepatectomy
IV V VIII
VII VIII
VI VII
VIII
IV I

20

a
b

15
11
4
3
3
31

21
14
10
4
2

10

17
6

3
1

10
8

Table 6
Mortality, morbidity, ICU and hospital stay for Pringle maneuver or SHVE
group

2
2

Right partial SHVE and left partial SHVE were excluded alternately.
Hepatic resections were named according to Couinaud.

Bleeding
(early postoperative
period)
Reoperation
Bile leak
Subphrenic collection
Liver disfunction
after operation
Wound infection
Pleural effusion
Death
ICU stay
(days)a
Hospital stay
(days)a
Overall complication rate

Pringle group
(n 110)

SHVE group
(n 125)

5
7
11
3

0
9
15
0

2
21
2
3 (0e11)

2
23
0
1 (0e3)*

22 (12e66)

16 (11e30)*

51.80%

39.2%*

*P < 0.05 vs the other cohort.

ICU: intensive care unit.
a
Values were expressed as the median (range).

THVE, consisting of both liver blood inflow and outflow

occlusion, provides a field of blood loss surgery and can
prevent bleeding of the hepatic veins,8e10 but it also hinders
IVC flow, which gives rise to systemic hemodynamic
disturbance and even intolerance in 20e30% of patients.9e12,24 SHVE is as effective as THVE in controlling
both inflow and outflow without disturbing IVC patency,
since it combines the Pringle maneuver with extrahepatic
selective occlusion of hepatic veins13e15,19,21 so as to overcome the drawbacks of the two methods mentioned above.
In 2100 cases, the tumor adhered to IVC in 181 cases, and
THVE was used in 65 cases, among which, the tumor grew
into the hepatic vein or/and IVC or involved the IVC wall
in only 10 cases. Therefore, it is unnecessary to occlude the
IVC except the 10 cases.
In this study, the volume of intraoperation blood loss and
blood transfusion in the Pringle group was significantly
higher than that in the SHVE group. The reason is that
the Pringle maneuver cannot prevent backflow from the
hepatic veins during the liver resection. In the Pringle
group, rupture of the hepatic veins occurred in 17 cases
during liver resection, and led to massive bleeding in 14
(>2700 ml) and air embolism in three. In the SHVE group,
the hepatic vein rupture developed in 18 cases during transecting the liver parenchyma, but did not result in massive
bleed and air embolism because the hepatic veins were
clamped before liver resection.
The postoperative complication rate in the Pringle group
(51.8%) was higher than that in the SHVE group (39.2%)
(P < 0.05). In the Pringle group, postoperative bleeding
developed in five patients, who then underwent reoperation.
The cause of two deaths was associated with injury of the
hepatic veins. Due to the higher complication rate, ICU

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stay and hospital stay in the Pringle group were longer than
those in the SHVE group. The results showed that less intraoperative blood loss and the lower transfusion requirement played a crucial role in reducing complications
rate.2,7,14,15,25,26
SHVE has not been used extensively, because dissection
of the hepatic vein has been considered hazardous.6,13e16 In
our experience, we have a good command in the following
important anatomical sites: (1) the fossa venae cavae,27
which is a depressed space located at the anterior wall of
the IVC, between the right hepatic vein and the common
trunk of left and middle hepatic vein. After downward
dissection along this fossa, the short hepatic vein will not
be encountered in the anterior wall of the IVC; (2) the hepatocaval ligament,16 which is a layer of connective tissue
located on the right lateral and upper aspect of retrohepatic
IVC. After division along this space, the right lateral wall
and the interior border of the right hepatic vein can be
visualized and the right hepatic vein can be encircled;
and (3) the space between the posterior wall of the common
trunk of the left-middle hepatic vein and the anterior wall
of the IVC,28 which can be exposed by division of the
peritoneum reflection. After division along this space, the
common trunk can be encircled.
If the tumor is very close to the roots of hepatic veins
and may be dangerous to be divided, it is unnecessary to
isolate the hepatic vein reluctantly. Depending on the resection range and on whether the hepatic veins can be isolated
or not, three methods of occlusion can be used as follows:
(1) ligating the hepatic veins when the hepatic vein will be
cut with the resected lobe; (2) occluding with a tourniquet;
with both of the occlusion, the posterior wall of the hepatic
veins should be divided and encircled with loops. When the
tumors involve the roots of the hepatic veins, the division of
the posterior wall may result in the posterior wall injury;
and (3) occlude with bulldog or Satinsky clamps. With
our experience, clamping with Satinsky clamps is a safer
and easier occlusion method, by which, the posterior wall
of the hepatic veins do not need to be divided and encircled
especially when the tumors involve the cavohepatic junction and the hepatic vein cannot be divided. It is effective
to occlude outflow from the hepatic veins by clamping at
the origin from IVC with Satinsky clamps, and it is unnecessary to dissect the hepatocaval ligament or/and short
hepatic vein, which can shorten the dissection time.
In the SHVE group, two injuries developed during the
hepatic veins dissection, which were occluded with Satinsky
clamps successfully, and no massive blood loss occurred and
no death occurred during and after the operation. The
massive bleeding caused by the hepatic vein rupture was
prevented successfully.
Because of the higher incidence of tumor invading hepatic vein than that invading IVC (Only 10 patients with tumor invaded the wall of IVC or with IVC tumor embolism
in our 2100 series), SHVE can play a more important role
in hepatic resection.29

Conclusions
Compared with Pringle maneuver, SHVE is a safer and
more effective method employed when liver tumors invade
the hepatic veins. It can control both liver blood inflow and
outflow, prevent massive bleeding caused by the hepatic
vein injury, reduce the intraoperative and postoperative
complication rate and stabilize hemodynamics. It will
play a definite role and be widespread in liver surgery.
Conflicts of interest
I have been briefed about my responsibilities relating to
conflict of interest in my article.
I do not have any conflict of interest, personal or organizational, financial or familial, real or apparent, in participating in this procurement.
I further represent that my spouse/domestic partner has no
conflict of interest as defined in the Conflict of Interest Code.

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Surg Oncol (2007), doi:10.1016/j.ejso.2007.07.001