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Research Articles
Laparoscopic Cholecystostomy in Pigs: Technique and Comparison
with Traditional Open Cholecystostomy for Surgical Stress
Zhang, H.,1, 2 Tong, J.,1 Zhang, S.,1 Zhang, J.1 and Wang, H.1*
1
2
College of Veterinary Medicine, Northeast Agricultural University, Harbin, China.
Animal Science and Technology College, Beijing University of Agriculture, Beijing, China.
* Corresponding author: College of Veterinary Medicine, Northeast Agricultural University, No.59 Mucai Street, Harbin 150030, China.
Email: hbwang1940@126.com
AB ST RAC T
This article describes a simple technique of laparoscopic cholecystostomy (LC) and compares the LC
technique with open cholecystostomy (OC) for clinical outcome and surgical stress response. LC was
performed under general anesthesia using three portals. The gallbladder was fixed to the anterior abdominal
wall using two sets of simple interrupted sutures placed between the anterior abdominal wall and gallbladder,
rather than the traditional single set. A cauterized incision was made at the gallbladder fundus such that
it lay at the center of a purse-string suture; an 18-F Malecot catheter was introduced into the gallbladder
lumen through this incision. The mean duration required for completing LC was 38±12 min, which was
decreased by 16 min with increasing experience. In a matched group of pigs, OC was performed using the
conventional approach. All animals underwent tube cholecystocholangiography and follow-up laparoscopy
at 15 days and 1 month after the surgery, respectively. The investigations showed that the gallbladder was
viable with no bile leakage or abscess formation and that it remained adherent to the abdominal wall. In
addition, the serum concentrations of cortisol, interleukin-6, and C-reactive protein showed that the surgical
stress response was lower for LC than OC. Thus, in terms of surgical stress, and possibly operative time,
laparoscopic placement of the Malecot catheter using a three-portal approach and two suture anchors may
be more beneficial than OC for the creation of a short-term access route into the gallbladder and bile ducts
in pigs, under both interventional and experimental settings.
Keywords: Laparoscopy; Tube Cholecystostomy; Technique; Response Stress; Miniature Pig.
INTRODUCTION
Percutaneous cholecystostomy (PC) is a safe alternative to
cholecystectomy and surgical exploration of the bile ducts
in the management of acute cholecystitis (1-5) and inspissated bile syndrome (6) in humans. PC is also performed to
facilitate diagnostic T-tube cholangiography in humans (7).
In veterinary medicine, experiments related to procedural
development and in vivo evaluation of techniques and/or
devices, as well as professional training protocols for biliary
interventional procedures, require the establishment of a
safe and easy access route into the gallbladder and the bile
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Zhang, H.
JUNE 2016.indb 10
ducts (8-10) and such purposes a porcine model is frequently
sought. Previous studies on large animal models involved
either open surgery with anchoring of the gallbladder and
subsequent placement of large-bore external tubes or placement of a permanent catheter that was inserted percutaneously under radiological or ultrasonic guidance and retained
until the formation of a mature tract (11-16).
In our experience, the laparoscopic approach enables good
visualization of the abdominal cavity while maintaining good
hemostatic control, enabling fast recovery, and affording an
efficacy level that was comparable to that afforded by open
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surgery. However, a previous study has not shown differences
between the two surgical approaches in regard to surgical
stress response (17). To achieve minimally invasive treatment
of benign and malignant diseases of the biliary tract and to
facilitate interventional procedures and experimental studies
related to the biliary system, it is necessary to establish an
easy and reliable route to access the gallbladder and the bile
ducts.
In this study, we employed a simple method for performing LC in pigs using two suture anchors and inserting
the Malecot catheter into the gallbladder. In addition, we
compared LC and OC in terms of the clinical outcome and
surgical stress response.
(Harbin Pharma, China), tiletamine/zolazepam (Huaen
Pharma, China), xylazine (Libang Pharma, China), and
tramadol ( Jiupai Pharma, China)at doses of 0.02 mg/kg,
3.0 mg/kg, 1.2 mg/kg and 1.6 mg/kg, respectively (18). The
core body temperature (measured using a rectal probe) was
maintained between 36°C and 38°C by warming the operating table and using an infrared heating lamp. Throughout the
procedure, physiologic saline (0.9% NaCl, Kelun Pharma,
China) solution was continuously infused at a rate of 3 ml/
kg/h via the marginal ear vein of the pig and the vital signs,
blood gas levels, and respiratory parameters of the animal
were monitored.
MATERIALS AND METHODS
The 7 animals in the LC group were placed in the supine
position, and the ventral aspect of the abdomen (from the
xiphoid to the pubis and the inguinal folds) was shaved, aseptically prepared, and draped for laparoscopy. A Veress needle
(Olympus Corporation, Tokyo, Japan) was then inserted into
the peritoneal cavity to establish a carbon dioxide pneumoperitoneum of pressure 12 mm Hg. A 3-portal approach was
adopted for LC (Figure 1).
The laparoscope provided good visualization of the peritoneal cavity. The gallbladder was located adjacent to the
right medial liver lobe and showed a grayish discoloration in
several cases. The site of the planned cholecystostomy on the
anterior abdominal wall was identified and digitally palpated
under laparoscopic visualization. To decompress the gallbladder, a 22-gauge, 6-inch spinal needle was inserted into the
gallbladder through the abdominal wall, after which the stylet
was removed and the gallbladder contents aspirated as much
as possible. A single traction suture was placed with an intracorporeal laparoscopic suture at a distance of approximately
1 cm from the gallbladder fundus (19). A purse-string suture
(2-0 polyglycolic acid; Pudong Jinhuan Medical Products
Co., Ltd., Shanghai, China) was then placed in the wall of
the gallbladder fundus approximately 1 cm caudal to the
first fixation point of the gallbladder. A cauterized incision
extending up to the gallbladder lumen was made at the center
of the purse-string suture by using a laparoscopic monopolar hook electrode (Tonglu Medical Instruments Co., Ltd.,
Hangzhou, China) introduced through portal B (Figure 2).
A sterilized, modified 18-F Malecot catheter (Zhanjiang
Star Enterprise Co., Ltd., Zhanjiang, China) was advanced
through the cannula at portal A. The gallbladder was then
Study design
The study was carried out on Chinese experimental miniature
pigs that were equally divided into 2 groups: the LC group, in
which LC was performed and the OC group, in which open
surgery was performed using the conventional approach. The
experimental protocol was approved by the ethics committee
of Northeast Agricultural University (NAUEC2014-0205).
Animals
The animals used in this study were 14 Chinese experimental miniature pigs (3 males and 4 females in each group) of
ages 3–6 months and weight 15.5–25.8 kg. Seven animals
each were enrolled in the 2 treatment groups. The pigs were
housed individually and fed a standard piglet diet with tap
water ad libitum. The animals were allowed a 14-day period
to acclimatize to the laboratory conditions before the start
of the study. Care and handling of the animals were in accordance with regulations for the administration of affairs
concerning experimental animals (Approved by the State
Council on October 31, 1988 and promulgated by Decree
No. 2 of the State Science and Technology Commission on
November 14, 1988).
Preoperative protocol
Before commencement of the experiments, food and water
were withheld for 12 and 6 hours, respectively, to reduce
the gastrointestinal content and minimize the risk of regurgitation during surgery. To induce anesthesia, each pig
was administered intramuscular (IM) injections of atropine
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Technique of the cholecystostomy
Laparoscopic cholecystostomy in pigs
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Figure 1: The locations of the portals A, B, and C. Portal A
(laparoscope) was located 5–8 cm below the umbilicus along the
ventral midline (in male pigs, portal A was shifted 2–3 cm to the
left). Portals B and C were 3–5 cm cranial to portal A and 8–10 cm to
the left and right of the ventral midline, respectively; they were used
for introducing laparoscopic surgical instruments.
secured with an atraumatic grasping forceps (Tonglu
Medical Instruments Co., Ltd., Hangzhou, China). Under
direct laparoscopic visualization, the Malecot catheter was
advanced into the gallbladder lumen through the cauterized
incision mentioned above, by using a laparoscopic left-curved
preparation forceps (Tonglu Medical Instruments Co., Ltd.,
Hangzhou, China). The catheter was then withdrawn slightly
to allow the winged end of the catheter to expand and anchor
itself in the gallbladder tissue; the purse-string suture was
then pulled tightly. The catheter was subjected to mild tension and infused with 10 mL of sterile saline (0.9% NaCl)
solution to check for leakage around the site of entry into
the gallbladder. Another set of simple interrupted sutures was
placed opposite to the first fixation point in a manner similar
to that described above for the first set of sutures (Figure 3).
The two sets of sutures were used to attach the gallbladder to
the anterior abdominal wall at the point where the catheter
exited the peritoneal cavity.
The intra-abdominal pressure was then reduced from
12 mm Hg to 6 mm Hg, and the gallbladder fundus was
approximated to the parietal peritoneum by retracting the
catheter, to prevent biliary leakage. A hemostatic forceps
was then advanced into the peritoneal cavity through a stab
incision made in the ventral body wall parallel to and approximately 1–2 cm from the ventral midline. The forceps
was used to clamp the catheter outside the abdominal cavity.
The abdomen was then completely deflated; the sutures were
Figure 2: Intraoperative view showing a cauterized incision made by
the laparoscopic monopolar hook electrode (white arrow) in the middle
of the purse-string suture (black arrow).
Figure 3: Intraoperative view showing the second set of simple
interrupted sutures (black arrow) placed opposite to the first fixation
point (white arrow).
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JUNE 2016.indb 12
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tightened and knotted extracorporeally; and the knots were
buried in the subcutaneous tissues (20, 21). Immediately
afterwards, a tube cholecystocholangiogram was obtained
using 60% diatrizoate sodium (Hansen Pharma Co., Ltd.,
Changsha, China).
The external portion of the Malecot catheter was sutured
to the skin using the finger-trap method (20) and clipped at
about 4–5 cm from the point of its exit from the peritoneal
cavity to prevent its dislodgement. Sutures of 2-0 polyglycolic
acid (Shanghai Medical Instruments Co., Ltd., China) were
used to close portal A in 2 layers and portals B and C, in a
single layer. All the skin wounds were closed with a simple
interrupted 3-0 nylon suture (Shanghai Medical Instruments
Co., Ltd., China).
The 7 pigs in the OC group underwent OC performed
with the conventional technique (14). All the procedures
were performed by the same team comprising a surgeon and
2 assistants.
Postoperative care
After the surgery, the temperature, heart rate, respiratory rate,
and arterial blood pressure of the pigs were monitored until
the values returned to the preoperative levels and the animals
regained consciousness; additionally, clinical examination and
blood tests for the complete blood count were conducted
daily. For analgesia, fentanyl patches (5 mg; Durogesic,
Janssen Pharma, Xian, China) were applied on the median
line of the back after shaving every 3 days for 6 days, and
for antibiotic coverage, ampicillin (20 mg/kg IM; Lukang
Pharma, Jining, China) was administered every 8 hours for
3 days. The pigs were housed individually in dry and clean
barns to avoid damage to the catheters and contamination by
feces. The extracorporeal portion of the catheter was washed
every day. In both groups, the Malecot catheter was removed
15 days after the surgery and laparoscopic examination was
conducted one month after the surgery to assess the status
of the abdominal cavity and its viscera.
Measurements of serum cortisol, interleukin-6, and
C-reactive protein concentrations and white
blood cell count
For all pigs in both groups, blood samples (2.5 mL) from the
precaval vein were collected at the following time points: 1 h
before surgery; immediately (0 h) after the surgery; and 4 h
and 1, 2, 3, 5, and 7 days after the surgery. The samples were
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used to measure the serum concentrations of cortisol (COR),
interleukin-6 (IL-6), and C-reactive protein (CRP) and the
white blood cell (WBC) count. The serum IL-6, CRP and
COR concentrations were measured using enzyme-linked
immunosorbent assay kits (Yapu Biological Technology Co.,
Ltd., Shanghai, China) for the measurement of the porcine
parameters (sensitivity, 0.1 ρg/mL, 0.1 mg/L, and 1.0 ηg/mL,
respectively. The WBC count was determined using an automatic blood cell analyzer (Mindray Bio-medical Electronics
Co., Ltd., Shenzhen, China).
Statistical analysis
For the LC group, the operating time was defined as the
duration from the initial stab incision to the closure of the
last portal. For the OC group, this value was defined as the
time from the start of the skin incision to its closure. The
data were expressed as mean±standard error of the mean.
Inter- and intragroup differences in values were determined
by one-way analysis of variance, which was performed using
the SPSS software (version, 17.0; SPSS Institute, Cary,
NC, USA). The significance of differences was set at a P
value of <0.05.
RESULTS
Surgical procedure
LC was successfully performed for all the pigs, without any
major intraoperative, surgery-related complications. Minimal
hemorrhage and biliary leakage were noted in a few cases
during the puncturing of the gallbladder with the needle and
the monopolar hook electrode; nevertheless, intraoperative
bleeding was negligible for LC. The total length of the skin
incisions, including those for all the 3 portals, was 2 cm
for the LC procedure; this value was significantly less than
that required for the OC procedure (10 ± 2 cm) (P < 0.01).
The mean operating time was 38±12 min and 33±10 min in
the LC group and OC group, respectively. Further, the LC
operative time was reduced by 16 minutes with increasing
experience.
Clinical outcome
The catheter was left in place for 15 days and washed
once a day under sterile conditions, before feeding; the clamp
was released once a day to drain the gallbladder under sterile
conditions. Intraperitoneal bile leakage or dislodgement of or
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Figure 5: Repeat laparoscopy performed 1 month after the surgery
shows close attachment and adherence of the gallbladder (G) to the
anterolateral abdominal wall.
Figure 4: Follow-up cholecystocholangiogram performed 15 d
after surgery shows absence of bile extravasation and catheter
occlusion.
damage to the catheter did not occur in any of the pigs while
the catheter was left in situ. In the case of one pig, the stoma
continued to leak small amounts of bile even after the drain
was removed; however, this was resolved within 5 days after
the formation of healthy granulation tissue. Furthermore,
two pigs developed irritation at the site of the stoma. Since
bacterial culture of the bile samples was not performed, we
are unable to comment on the status of postoperative infections of the gallbladder or bile tract. However, it appears that
there may have been no clinical infection since the total blood
counts were within the reference range for all the pigs at 5
postoperative days and none of the pigs showed any evidence
of digestive complications during the 1-month postoperative
follow-up period.
Follow-up cholecystocholangiography was successfully performed 15 days after the surgery confirming
the absence of bile extravasation and catheter occlusion
in the LC group (Figure 4). The drainage tube allowed
easy access to the gallbladder for performing repeat
cholangiography. Repeat laparoscopy was performed 1
month after the surgery in both groups. The findings of
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JUNE 2016.indb 14
repeated laparoscopy in the animals of the LC group were
as follows: a viable gallbladder; the absence of bile leakage
and abscess formation; close attachment and adherence
of the gallbladder to the anterolateral abdominal wall
(Figure 5); absence of omental attachment to the suture
anchors; and presence of white or reddish, oval, and raised
structures at the trocar sites, indicating advanced peritoneal healing. On the other hand, the OC group showed
omental attachment to the site of the suture anchor in
two pigs and to the abdominal incision in one pig. No
other complications were observed in either group within
3 months of the surgery until the animals were euthanized
with administration of pentothal sodium (4–8 mg/kg) and
potassium chloride injection (2 g, 20 ml) via the marginal
ear vein successively.
White blood cell count
At 24 hours after the surgery, the mean WBC count increased
significantly from preoperative levels of 8.34±0.61×109/L and
9.43±2.19×109/L to 15.21±0.30×109/L and 21.22±4.60×109/L
in the LC and OC groups, respectively (P < 0.01, for all
comparisons). However, in both groups, the values did not
exceed the upper limit of the reference interval (11–22 ×
109/L) in this study. The increased WBC levels in the LC
and OC groups returned to the preoperative levels on days 3
and 5, respectively (8.56±1.52×109/L and 10.39±0.78×109/L,
respectively) (Table 1).
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Table 1: White blood counts and serum concentrations of C-reactive protein, interleukin-6, and cortisol
Pre-Op
POD-0h
WBC (× 109/L)
LC
OC
8.34±0.61
9.43±2.19
8.68±1.79
14.43±1.88**▲▲
POD-1d
15.21±0.30**
21.22±4.60**▲
POD-3d
8.56±1.52
13.57±0.34*▲▲
9.86±0.19
11.44±0.53
POD-4h
POD-2d
POD-5d
POD-7d
11.34±1.81*
11.18±1.56*
8.81±2.41
CRP (mg/L)
LC
1.19±0.06
1.98±0.55**
2.49±0.03**▲
40.22±1.82**
2.53±0.06**
2.69±0.26**
50.13±1.58**
17.24±2.58**
2.50±0.04**
14.39±2.51**▲
1.55±0.03*
10.39±0.78
OC
1.29±0.22
IL-6 (ρg/mL)
LC
OC
34.39±1.86
33.49±1.99
2.63±0.02**
33.22±1.78**
40.59±1.90**▲
53.60±0.53**
68.69±4.68**▲
37.12±0.91**
43.66±3.38**▲
1.99±0.07**▲
48.03±2.83**
60.68±.32**▲▲
32.74±0.67**
39.50±3.22**▲
1.18±0.09
35.67±3.79
36.89±5.73
1.09±0.11
1.56±0.04*▲▲
1.20±0.04
1.29±0.11
1.10±0.08
45.98±2.53**
COR (ηg/mL)
LC
OC
20.57±2.79
21.11±1.01
37.12±5.30
33.90±1.48
67.28±2.24**▲
51.99±2.79**▲
35.03±3.82
31.30±2.30**
38.75±1.20**▲
25.94±4.04
35.41±3.91**▲
23.10±3.77
19.19±2.77
25.01±5.56
22.44±7.13
Note: Pre-Op = pre-operation; POD = postoperative day; WBC = white blood cell; CRP = C-reactive protein; IL-6 = interleukin-6;
COR = cortisol; LC = laparoscopic cholecystostomy; OC = open cholecystostomy;
Compared with preoperative values: * 0.01 < P < 0.05; ** P < 0.01;
Compared with the OC group: ▲0.01 < P < 0.05; ▲▲P < 0.01; one-way ANOVA.
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Serum concentrations of C-reactive protein,
interleukin-6, and cortisol
In the LC group, the postoperative serum CRP concentrations were significantly higher than the preoperative values
(1.19±0.06 mg/L) at the following time points: immediately
after surgery (1.98±0.55 mg/L), at 4 hours after surgery
(2.50± 0.04 mg/L, and 1 day after surgery (2.53±0.06 mg/L)
(P < 0.01, in all cases). The postoperative levels were the highest (2.53 mg/L) at 24 hours after the surgery. Compared to
the OC group, the LC group showed a slower rise in the
postoperative levels of serum CRP, but a more rapid decrease
to the preoperative levels (Table 1).
The serum IL-6 concentration in the LC group showed
an immediate increase after surgery compared to the preoperative level (34.39 ± 1.86 ρg/mL) and was the highest
(53.60±0.53 ρg/mL; P < 0.01) at 4 h after the surgery. As was
the case with the serum CRP concentrations, the serum IL-6
levels showed a more rapid restoration to preoperative levels
in the LC group than in the OC group. The postoperative rise
in the serum IL-6 levels in the OC group was significantly
higher than that in the LC group (Table 1).
The mean serum COR concentrations in both groups
increased immediately after surgery, but the levels were lower
in the LC group than in the OC group (33.22±1.78 ηg/
mL and 40.59±1.90 ηg/mL, respectively). The serum COR
concentrations did not show any statistically significant
intergroup differences at any time point but they remained
lower in the LC group than in the OC group at all time
points (Table 1).
DISCUSSION
Several techniques have been proposed for performing PC in
humans (2, 22). In this study, we performed cholecystostomy
using a laparoscopic approach in swine models. We tested this
method in the miniature pig since this is a useful model for
research on laparoscopic techniques by virtue of their similarity with humans with respect to the hepatobiliary anatomic
and functional aspects (19).
We successfully completed LC in all the 7 healthy pigs
without any intraoperative or immediate postoperative complications. Further, the operative time was reduced by 16 min
(74 min to 58 min) with increasing experience and further
improvement may be expected with additional practice.
The serum concentrations of CRP, IL-6, and COR are
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JUNE 2016.indb 16
considered useful in evaluating the extent of surgical trauma
(21). In our study, the postoperative increase in serum levels
of CRP and IL-6 were significantly greater for OC than for
LC. Moreover, the serum cortisol concentrations were lower
for the LC group than the OC group at all time points.
This implies that the surgical stress and postoperative pain
associated with LC are less than those associated with OC.
Unlike the case with surgery requiring celiotomy, LC
precludes the need for the exposure of the abdominal
viscera to air; allows for the completion of all surgical procedures within the abdomen; enables direct visualization
of the gallbladder through the laparoscope; and entails
minimal invasion, reduced bleeding, and a quick recovery.
Moreover, direct laparoscopic visualization allows proper
positioning of the aspiration needle; this avoids entry into
the gallbladder through a liver lobe, which is sometimes
unavoidable when cholecystostomy is performed under
ultrasonographic, computed tomographic, or fluoroscopic
guidance (22).
In the present study, a 3-portal approach was used to perform LC. The laparoscope was introduced through a portal
located below the umbilicus and on the ventral midline; this
position allowed for excellent visualization of the gallbladder and its associated structures. The two instrument portals
were located 3–5 cm cranial to the laparoscope portal, one on
each side of the midline (8–10 cm away). The 3 portals were
positioned in a triangular formation that facilitated optimal
manipulation of the gallbladder. This triangular positioning of
the 3 portals, along with the infra-umbilical placement of the
laparoscope portal, appears to be suitable for the manipulation of the gallbladder and catheter placement. Additionally,
in our technique, we used 2 sets of sutures to attach the gallbladder to the abdominal wall. This was intended to prevent
the malpositioning and damage to the Malecot catheter.
In the presence of excessive fullness or internal pressure
in the gallbladder, penetration of the gallbladder wall with
the needle may be challenging. A quick, forceful jabbing
action, however, usually enables penetration with minimal
leakage of the remaining contents. Bile leakage may also be
controlled by placing a double purse-string suture; suture
anchoring of the gallbladder with the parietal peritoneum is
also useful in preventing cholecystic hemorrhage, inadvertent
peritoneal migration of the catheter, and peritoneal leakage
of the gallbladder contents (16, 23). Further, we suggest that
the intra-abdominal pressure be decreased to 6 mm Hg beIsrael Journal of Veterinary Medicine  Vol. 71 (2)  June 2016
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fore tying the fixed sutures since this will reduce the tension
between the ventral body wall and the gallbladder.
Repeat laparoscopy performed 1 month after the respective surgeries in both groups showed the presence of
focal fibrous adhesions between the gallbladder and the
ventral body wall. These adhesions are useful in that they
reduce the risk of bile leakage into the abdomen. Further,
the adhesions should be strong so as to avoid kinking of
the catheter.
The findings of this study should be considered in
the light of a couple of limitations. Since cultures of bile
samples were not performed, we could not conclusively assess the status of postoperative infection. However, since
relevant clinical and laboratory signs were not observed,
infection may be presumed to be absent. Postoperative infections of the gallbladder and biliary tract can be avoided
by the employment of appropriate sterilization techniques
and proper administration of intensive postoperative care.
Another limitation of our study is the short follow-up duration. This may be overcome by further investigations on the
long-term advantages of LC. Silicone-coated tubes may be
useful only for short-term biliary drainage, i.e., for a period
less than 2 weeks. Further investigations are necessary to
determine whether tubes manufactured using other types of
material, such as teflon, polyurethane, or polyvinyl chloride,
are superior to silicone-coated ones for cholecystostomy
(24).
In conclusion, our results indicate that LC using a threeportal approach with placement of 2 sets of sutures for the
insertion of the Malecot catheter is better than OC for the
establishment of a short-term access route to the gallbladder and bile ducts of swine, with a lower level of surgical
stress response. LC appears to be a simpler and safer method
compared to the conventional approach involving the surgical
insertion of the percutaneous catheter in swine; our findings
also show that with an increase in the surgeon’s experience,
it may be possible to further reduce the operative time for
LC. Further studies are necessary to evaluate the efficacy of
the laparoscopic approach for cholecystostomy in clinically
affected pigs as well as over the long term.
ACKNOWLED GEMENTS
This work was financially supported by grants from the National
Natural Science Foundation of China (Grant no. 31472245), and
the Da Bei Nong Foundation for Young Teachers (15ZK006).
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ET H ICAL STANDARD
The experiments comply with the current laws of the People’s
Republic of China and Institutional Animal Care and Use
Committee (Northeast Agricultural University, China).
CONFLICT OF I NT EREST
The authors have no conflict of interest to declare.
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