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7 Application ofIndocyanine Green Fluorescent Imaging inBiliary Surgery
165
7.3 ICG Fluorescence Imaging
intheDiagnosis andManagement
ofBiliary Diseases
7.3.1 ICG Fluorescence Imaging inLocating
Bile Duct During Reoperation
oftheBiliary Tract
Every hepatobiliary surgeon must locate the bile duct, identify bile duct lesions correctly, and avoid bile duct injury in
biliary surgery. Current preoperative imaging techniques for
assessing the biliary tract include MRCP, CT, and
B-ultrasound. Through these imaging modalities, surgeons
can understand the anatomy and pathology of the biliary
tract preliminarily and determine operation approaches. In
recent years, near-infrared uorescence imaging technology
has gradually seized people’s attention. Through intraoperative real-time uorescence imaging, surgeons can grasp the
intraoperative situation while performing the procedure and
Fig. 7.6 For patients
undergoing biliary tract
reoperation, intraoperative
ICG uorescent imaging was
used to display the
extrahepatic biliary tract to
avoid biliary tract injury
provide substantial guidance and assistance for the operation. For patients with a history of multiple biliary tract surgery, it is recommended that ICG uorescence imaging
technology should be used to help locate the biliary tract and
identify the hilar tissue intraoperatively, if the hospital has
the necessary equipment; choledocholithotomy should be
performed after accurate identication of the bile duct and
duodenum from the rst porta hepatis with tissue contracture
and unclear structure, which is conducive to avoid iatrogenic
injury (Fig.7.6).
7.3.2 ICG Fluorescent Imaging inDiagnosis
andManagement ofBiliary Stricture
ICG uorescent imaging technology can detect the location
and extent of hilar biliary stricture and guide the selection of
appropriate repair and reconstruction surgery methods
(Fig.7.7).
Fig. 7.7 No uorescence
development was observed in
the bile duct when the rst
porta hepatis was viewed
under uorescence state,
according to which, the
location and degree of bile
duct stricture in hilar of the
liver could be determined and
appropriate repair and
reconstruction surgical
methods could be selected
166
C. Fang and W. Zhu
7.3.3 ICG Fluorescence Imaging inFinding
Biliary Anastomosis After Reoperation
oftheBiliary Tract
For biliary tract surgery, full exposure of the surgical eld
is helpful to identify variations of the bile duct and avoid
iatrogenic bile duct injury. After repeated operations,
extensive adhesion brosis or scar formation in the right
upper abdominal cavity may develop. Postoperative adhesions lead to signicant changes in the normal anatomy
and increase the difculty in identifying the common bile
duct. Reoperation following multiple biliary operations is
a complex procedure; dissociating and searching for the
bile duct is an important step, and sometimes challenging.
For the patient who has a history of biliary tract surgery,
especially Roux-en-Y anastomosis, the extrahepatic biliary tract is buried deep in an envelope of severe scar adhe-
Fig. 7.8 For patients with a
history of previous Roux-Y
choledochojejunostomy, the
hilar tissues could be clearly
identied by ICG uorescent
imaging because bile
containing indocyanine green
was present in the ascending
jejunal loops. The
uorescence in this gure
shows the ascending jejunal
loops
sion. At reoperation, imprecise incision can easily injure
the colon were adhered to the porta hepatis, stomach, and
duodenal bulb, and mesentery, and even severely damage
the hepatic hilus structure. The more conservative approach
is to mobilize the encapsulated lower right hepatic margin.
From the right approach, dissociate along the visceral surface against the liver capsule to the left, mainly with sharp
dissection. Dissociate from shallow to deep, until the hepatoduodenal ligament is exposed. Identify the ascending
jejunal loop by ICG uorescent imaging and locate the
anastomotic site. From the original anastomotic site,
search for the common bile duct, and puncture to conrm.
Alternatively, accurate bile duct incision or anastomotic
removal can be performed after administration of ICG
through which ascending jejunal loops and extrahepatic
bile ducts can be fully displayed under uorescence
(Figs.7.8 and 7.9).
Fig. 7.9 Intraoperative use of
ICG uorescent imaging
required to locate ascending
jejunal loops for
choledochojejunostomy
7 Application ofIndocyanine Green Fluorescent Imaging inBiliary Surgery
167
7.3.4 ICG Fluorescence Imaging inSearching
forDilated Intrahepatic Bile Duct
Patients with complicated hepatolithiasis usually have a long
course, recurrent cholangitis, and formation of hepatic
atrophy/hyperplasia. In some patients with hepatolithiasis,
dilated bile ducts and stones are located in the segments VII
and VIII and the bare area of the liver; patients are also
intolerant of hepatectomy. In order to avoid blind exploration
and inadvertent injury, ICG-mediated near-infrared
uorescence imaging of bile ducts can be used to navigate
the biliary surgery (Fig.7.10). It helps surgeons accurately
locate distal dilated bile ducts, reducing time spent blindly
cutting liver parenchyma in search of the bile duct,
signicantly shortening the duration of the operation.
7.3.5 ICG Fluorescence Imaging inDening
Cholangiocarcinoma Tumor Boundaries
Cholangiocarcinoma is an uncommon malignancy with
poor prognosis, and surgery remains the only curative treatment option. Patients with intrahepatic cholangiocarcinoma
and hilar cholangiocarcinoma often require extensive hepatectomy, or even extended left/right liver lobectomy combined caudate lobectomy. Obtaining R0 resection and
ensuring the safety of surgery is the goal of hilar cholangiocarcinoma surgery and the primary condition for preventing
postoperative recurrence. For patients with impaired cholestasis, how to preserve the volume and function of the
remaining liver to the maximum extent has become one of
the focuses of liver surgery. The critical step of liver tumor
operation is to locate the tumor accurately and dene the
tumor boundary and range of resection. If the resection
range is too small, it will lead to residual tumor; and if the
resection scope is too large, it will increase the risk of vascular injury and liver failure. At present, it is mainly based
on preoperative imaging, intraoperative naked eye ndings,
and exploration results, combined with clinical experience
to make a comprehensive judgment. Compared with traditional imaging methods such as B-ultrasound CT, and MRI,
ICG uorescent imaging has the advantages of high contrast
uorescence imaging between healthy liver tissue and tumor
tissue. Moreover, ICG uorescent imaging reects the pathological changes of cells and molecules in vivo, and the
boundary of the cell functional level is preliminarily realized. Therefore, ICG uorescent imaging can locate liver
tumors in real time during operation and help to dene the
tumor boundary and the scope of hepatectomy through this
unique imaging method.
7.3.6 ICG Fluorescent Imaging inDetermining
theBoundary ofLiver Resection
In patients with hilar cholangiocarcinoma and some patients
with hepatolithiasis, when resection of a hepatic segment/
region is required, intraoperative ICG uorescent imaging
can help to clearly display and conrm the cross section of
liver resection; and guide the accurate hepatic parenchymal
disconnection in real time. At present, Glisson pedicle occlusion and ultrasound-guided portal vein puncture staining are
commonly used to distinguish the lobe/segmental boundary
in anatomical hepatectomy. Both methods have certain limitations. Firstly, indigo solution, as a common staining agent
of portal vein puncture, cannot guide the whole process
because of its short residence time in the liver. Secondly, it is
difcult to obtain a clear hepatic lobe/segment boundary
Fig. 7.10 Intraoperative ICG
uorescent imaging of the
biliary tract plays a role of
“navigation” in biliary tract
surgery, accurately locating
guiding the accurate incision
of liver parenchyma for stone
extraction
168
C. Fang and W. Zhu
when the Glisson pedicle occlusion is used on the uneven
surface of the cirrhotic liver and the surface of the liver with
a history of abdominal surgery and covering brous tissue;
also, the ischemic boundary of the liver parenchyma is not as
evident as the liver surface during the process of liver dissection, and it does not play a good guiding role. In 2008, Aoki
etal. rst applied ICG uorescent imaging to the differentiation of the intrahepatic hepatic lobe/segment (Aoki et al.
2008). The technique was then further developed by using a
diluted ICG solution as a uorescent agent and a more
advanced uorescent image fusion system. At present, the
use of ICG uorescent imaging to display the liver lobe/segment can be performed by two methods.
Positive Display Method In the positive display method,
the portal vein of the hepatic segment to be resected is identied by intraoperative B ultrasound and 3D visualization
models. A small amount of diluted ICG solution is extracted
using a ne puncture needle and injected into the target portal venous branches for uorescence detection, showing the
hepatic lobe/segment to be resected. The uorescence signal
of the positive display method is reliable, but this method is
more complicated than the negative display method.
Negative Display Method
In the negative display method,
the portal vein of the liver segment to be resected is separated
and ligated with the help of the 3D reconstructed model. A
small amount of diluted ICG solution is injected intravenously
for uorescence detection, revealing the hepatic lobe/
segment to be preserved. The negative display method is
usually suitable for hepatic segment where portal venous
branches are easily exposed. The disadvantage of this method
lies in its low concentration of ICG accumulation, and hence
weak uorescence signal.
The positive display method is generally suitable for the
development of liver segments or subhepatic segments
supplied by fewer liver pedicles (1–2) because this method
requires injection of ICG after ne-needle aspiration in the
target liver lobe/segment. While, the negative display method
is suitable for hepatic segment where portal venous branches
are easily exposed, usually for development of liver segments supplied by more hepatic pedicles (≥ 3 branches) or
development of semi-liver.
In clinical application, it is found that both positive and
negative display methods present a specic failure rate, which
often occurs in patients with vascular anatomic variations in
porta hepatis. For the patients whose target hepatic segment/
pedicle are challenging to dissect and lead to puncture failure,
a negative display method should be used. When there is
more pedicle supply in the target liver segment, if the hepatic
pedicle is only partially blocked, the negative display method
is more prone to a failure to stain, so the positive display
method should be used. At present, a 3D portal vein display
can be realized both preoperatively and intraoperatively.
Therefore, intraoperative ultrasound and 3D visualization
systems can be combined to accurately understand the portal
venous variations, which is helpful for portal venous puncture
and hepatic pedicle anatomy. Appropriate display methods
can be selected according to actual conditions to further
improve the success rate of ICG uorescence development.
In the course of clinical application, we used a negative display method and a positive display method to divide the
hemi-hepatic boundary, respectively, and achieved good
results. We realized a strong visual segmentation effect of the
liver surface and the 3D staining of liver parenchyma.
Moreover, using the positive and negative methods provides
consistent results when there is hepatic ischemia after blocking the corresponding portal vein and hepatic artery. The
dynamic situation was observed concurrently with the operation, and the direction of hepatectomy was adjusted and corrected according to the uorescence boundary of liver
parenchyma, which conrmed that the method has good surgical guidance value (Figs.7.11, 7.12, 7.13, and 7.14).
Fig. 7.11 Left intrahepatic
cholangiocarcinoma. Left
hepatic ICG excretion
obstruction due to tumor
invasion of the left hepatic
duct, showing the left hepatic
boundary clearly
7 Application ofIndocyanine Green Fluorescent Imaging inBiliary Surgery
Fig. 7.12 Fluorescence of
the specimen after left
hemi-hepatectomy showed a
clear tumor boundary
Fig. 7.13 For one patient
who requires right hemihepatectomy for hilar
cholangiocarcinoma, the
target liver segment was
clearly displayed by the
negative display method, and
the boundary between left and
right liver was clearly
observed
169
Fig. 7.14 The left half of the
liver was clearly displayed by
negative display method, and
the boundary between the left
and right liver was clearly
observed
170
C. Fang and W. Zhu
7.3.7 ICG Fluorescent Imaging inDetection
andManagement ofBiliary Leakage
In recent years, due to the improvement of surgical techniques and perioperative work, the safety of biliary tract
surgery has been improved, and mortality has been reduced.
Although the overall postoperative complications are
declining, bile leakage after liver surgery continues to be
reported with unchanged incidences, ranging from 3.6% to
33% (Capussotti et al. 2006; Tanaka et al. 2002).
Postoperative bile leakage is a serious surgical complication, often occurring in the hepatic duct stump and liver
section. Bile leakage increases the perioperative risk of
abdominal infection, sepsis, liver failure, and even multiple
organ failure, prolongs hospital stay, and even increases
perioperative mortality. It is especially important to reduce
the occurrence of bile leakage. The management of bile
leakage should highlight the importance of prevention,
early detection, and timely treatment. It is imperative to
detect potential leakage before closure. The current intraoperative leak testing method mainly is injection of normal
saline or methylene blue solution through the cystic duct or
the open bile duct on the liver section after blocking the
common bile duct, and then to observe whether biliary
leakage or staining is present. Injection of normal saline is
a low-cost, non-toxic, and reproducible approach; however,
the clarity of aqueous solution makes it difcult to detect
small leaks. Injection of dyes such as methylene blue can
detect biliary leakage more clearly because of their high
contrast with liver parenchyma, however, these dyes can
often stain the surrounding liver tissue at the same time, so
it is difcult to locate the leakage accurately. Intraoperative
cholangiography is an effective method for leak detection,
but it is not the rst choice because of its complicated radiation exposure risks and attendant safety procedures during
the operation. With the application of ICG uorescent technique in hepatobiliary surgery, the effectiveness of intraoperative ICG uorescent imaging in detecting small bile duct
leakage in liver transection has been conrmed. The detection of bile leakage after hepatectomy by ICG uorescent
imaging is mainly based on the biological characteristics of
the bile duct excretion through the bile duct system. Bile
duct excretion begins 15min after the intravenous injection
of ICG.Therefore, the method is to temporarily block the
distal common bile duct after hepatectomy, then inject ICG,
through the gallbladder duct or cross-section bile duct to
carry out uorescence imaging to detect bile leakage in the
transect of the liver, and then to detect and deal with the
bile leakage promptly during the operation. As shown
below in one patient with hilar cholangiocarcinoma who
underwent right hemi-hepatectomy, the bile duct was temporarily blocked after ICG injection through the bile duct,
and the extrahepatic bile duct was developed. There was no
uorescence residue in the right hepatic section (Figs.7.15
and 7.16).
7.3.8 ICG Fluorescent Imaging inDetection
andManagement ofAnastomotic
Leakage
Choledochojejunostomy is often used in the repair of bile
duct injuries, excision of extrahepatic bile duct lesions, and
biliary reconstruction in the treatment of biliary calculi. It
mainly involves, those who had extrahepatic or hilar bile
duct lesions, including tumors, congenital cholangiectasis,
inammatory stenosis; and the reconstruction of biliary
drainage is necessary after pathological bile ducts are
resected. The following cannot undergo this procedure:
Those who experienced iatrogenic bile duct injury and the
Fig. 7.15 After right
hemi-hepatectomy for hilar
cholangiocarcinoma, there
was no bile leakage at the
broken end of the right
hepatic duct
7 Application ofIndocyanine Green Fluorescent Imaging inBiliary Surgery
Fig. 7.16 After right
hemi-hepatectomy, no
uorescent residue was found
in the residual liver section,
indicating no bile leakage in
the hepatic section
171
Fig. 7.17 The indwelling
supporting tube of the right
hepatic duct. No uorescence
development was observed at
the choledochojejunostomy,
while bile and uorescence
were observed in the
supporting tube of the right
hepatic duct, indicating no
leakage at the
choledochojejunostomy and
unobtrusive right bile duct
drainage
local repair of the bile duct; those with advanced periampullary cancer whose tumor cannot be removed and palliative
treatment of obstructive jaundice are needed; those who have
intrahepatic bile duct stones associated with hilar bile duct
stricture and need the resection of the strictured bile duct or
open plastic surgery. The surgeon must ensure there is no
stricture above the anastomosed bile duct. It is necessary to
detect the presence of bile leakage in the biliary anastomosis
during surgery. Since ICG near-infrared molecular uorescence can be excreted from bile, it is possible to effectively
observe the presence of bile leakage in the biliary anastomosis by uorescence imaging (Figs.7.17 and 7.18).
172
Fig. 7.18 After
choledochojejunostomy, no
obvious uorescence
development was observed at
the anastomosis, suggesting
no bile leakage at the
choledochostomy
C. Fang and W. Zhu
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Application ofEndoscopic Techniques
inBiliary Tract Surgery
ZhaohuiTang andChihuaFang
8
8.1 Introduction
In 1806, German physician Philip Bozzini invented an optical device that used a candle as a light source to inspect the
interior of the bladder and rectum (Bozzini 1806), which was
historically recorded as the earliest endoscopic instrument.
Dr. Bozzini set the stage for over 200years of innovations in
endoscope development. Endoscopy has experienced the
development stage of rigid endoscopy, semiexible lens
endoscopy, ber-optic endoscopy, and electronic endoscopy.
Because of the critical status of the human digestive system,
the progress of endoscopy has often played an essential role
in the overall advancement of digestive tract disease diagnosis and treatment. Gastrointestinal endoscopy has undergone the stages of rigid-wire endoscopy, ber-optic
endoscopy, electronic endoscopy, radio-electronic endoscopy-capsule endoscopy. The continuous development of
gastrointestinal endoscopy provides clinicians with an accurate diagnostic basis. Currently, the commonly used endoscopes are beroptic endoscopy and tubular electronic
endoscopy, both of which have relatively stable and accurate clinical applications. However, the pain caused by the
two types of endoscopy is obvious. This problem has been
solved by capsule endoscopy. Although capsule endoscopy
has seen tremendous advances in a short period of time,
there are still some technical problems to be solved. With
the continuous integration of digital science information
technology, articial intelligence technology, and minimally
invasive surgery in the new era, it is believed that endoscopic robot technology will become an inevitable trend of
digestive tract endoscopy.
Z. Tang
Xinhua Hospital, School of Medicine, Shanghai Jiaotong
University, Shanghai, China
C. Fang (
Zhujiang Hospital, Southern Medical University,
Guangzhou, China
*)
8.2 Duodenoscopy
Fiberoptic duodenoscopy, one of the most rapidly developing digestive endoscopes, has opened new vistas in the diagnostic of duodenal, biliary, and pancreatic diseases.
Specialized beroptic duodenoscopy is a side-viewing
instrument (JF- B2, Olympus), which is convenient for
inspection of duodenal bulb and the major duodenal papilla,
rendering cannulation easier; moreover, when the pyloric
region and the duodenal bulb is markedly distorted, it can be
changed into a straight or strabismus lens by replacing the
contact lens. The endoscopy is usually thinner than the gastroscope, and has a long working length (1300–1600mm);
so, it can be inserted into the deep part of the duodenum.
Since endoscopy has an extremely small diameter, especially
in the front end, it facilitates reversal observation in the duodenal bulb. The hardness of the proximal portion and distal
end of the duodenoscope varies; the soft distal portion and
the strengthened proximal part satises the requirements of
the duodenoscopy to be soft and exible but also improves
the performance of the front-end follower. The following
surgical procedures are feasible with duodenoscopy: diagnostic endoscopic retrograde cholangiopancreatography
(ERCP) and therapeutic ERCP; therapeutic ERCP includes
endoscopic sphincterotomy (EST), endoscopic biliary drainage (EBD), endoscopic nose biliary drainage (ENBD), endoscopic retrograde pancreatodrainage (ERPD), and
corresponding endoscopic stula.
Indications
• Patient with suspected duodenal diseases that cannot be
diagnosed by other examinations.
• Differential diagnosis of benign and malignant duodenal
ulcer.
• Patient with suspected pancreatic and biliary diseases
who is recommended to undergo ERCP.
© The Author(s), under exclusive license to Springer Nature Singapore Pte Ltd. 2021
C. Fang, W. Y. Lau (eds.), Biliary Tract Surgery, https://doi.org/10.1007/978-981-33-6769-2_8
173
174
Z. Tang and C. Fang
Contraindications
• Patients unwilling to cooperate, such as mental disorder
or psychosis.
• Severe cardiopulmonary disease and spinal deformity.
• Severe esophageal, cardiac, and pyloric obstruction.
• Patients who are not suitable for ERCP due to acute pancreatitis, biliary tract infection, and iodine allergy.
ERCP with duodenoscopy is the most technically
demanding and risky digestive endoscopic operation. Based
on the actual situation in China, the ERCP Group of
Digestive Medicine branch of the Chinese Medical
Association has formulated the “Chinese guidelines for
ERCP 2018” (2018). Indications for ERCP include obstructive jaundice, pancreatic or biliary ductal system diseases,
suspicion for pancreatic cancer, pancreatitis of unknown
cause, preoperative evaluation of chronic pancreatitis or
pancreatic pseudocyst, manometry for sphincter of Oddi,
and biliary stenting for leakage. Sphincterotomy is indicated in cases of the sphincter of Oddi dysfunction or stenosis, difculty with biliary stenting or accessing the
pancreatic duct, biliary strictures, bile duct stones, bile
sump syndrome following choledochoduodenostomy, choledochocele, and in poor surgical candidates with ampullary carcinoma.
Where laboratory or noninvasive imaging studies do not
suggest that abdominal pain is due to pancreaticobiliary
disease, the probability of meaningful discovery is low, and
the risk of complications is high, ERCP is not advised. ERCP
should only be performed when Oddi sphincter manometry
is considered for this group of patients. For routine
examination before cholecystectomy, preoperative ERCP
should be considered only in patients with cholangitis or
biliary obstruction, or with clinical and imaging ndings
suggesting cholelithiasis. ERCP is routinely performed for
malignant obstruction of distal bile duct with the opportunity
of surgical resection, but there is no evidence that preoperative
biliary decompression can improve the prognosis of the
operation. However, it can cause both preoperative and
postoperative complications. In patients with acute
cholangitis or severe pruritus for which the surgery may be
delayed, preoperative ERCP can resolve the obstruction.
Complications attributed to ERCP include (a) pancreati-
tis, hemorrhage after duodenal papillary sphincterotomy,
infectious complications; (b) cholangitis, including
cholecystitis and infection of peripancreatic effusion; (c)
cardiopulmonary adverse reactions, usually caused by
sedative drugs; (d) perforation. Patients should be informed
that they may be hospitalized in the event of a complication.
If perforation occurs, a surgical repair may be required.
Post-ERCP pancreatitis (PEP) occurs in 3–15% of all
ERCP procedures, and in high-risk patients, the risk of PEP
can increase to more than 25% (Talukdar 2016; Fogel etal.
2002; Elmunzer 2017). Endoscopists should inform the
patient that PEP may lead to a prolonged hospital stay, and
surgical treatment will be required; or even worse, it is very
likely to lead to death. Possible factors (patients and
operations) affecting the incidence of PEP should be
considered when designing surgical protocols and signing
informed consent. The incidences post-ERCP acute
cholangitis and cholecystitis are 0.5–1.7% and 0.2% to 0.5%,
respectively (Vandervoort etal. 2002; Freeman etal. 1996a,
b; Lenriot etal. 1993). Bleeding is the most common compli-
cation of endoscopic biliary and/or pancreatic sphincterotomy. The incidence of post sphincterotomy bleeding after
ERCP is reported to be 0.3% to 2% (Freeman etal. 1996a, b;
Cotton etal. 2009; Rustagi and Jamidar 2015). The patients
who underwent simple diagnostic ERCP without sphincterotomy and transmucosal puncture (such as simple stent
indwelling) have minimal risk of massive postoperative
bleeding. Factors that increase the incidence of bleeding
include coagulopathy, preoperative acute cholangitis, anticoagulant therapy within postoperative 3days, and unskillful
operation. This condition can be treated by local injection of
epinephrine, washing, and clamping of titanium clips. The
incidence of perforation after ERCP ranges from 0.3% to
0.6%. Perforation can be mechanical perforation of the
esophagus, stomach, duodenum caused by endoscopy, or
caused by therapeutic procedures such as sphincter incision
and guidewire placement. Anatomical changes caused by
surgery can increase the risk of perforation (such as in
patients undergoing previous Billmth II surgery via an injectable loop insertion). Perforation often requires surgery.
8.3 Choledochoscopy
In 1923, Bakes invented a laryngoscopic “choledochoscope”
(Bakes 1923), and used it in an operation to inspect the lower
end of the common bile duct, which was then ofcially
published at the Berlin Institute of Surgery. It was later
recognized as the earliest form. In 1930, Barlet successfully
inspected the gallbladder by inserting the cystoscope through
the stula of the gallbladder. In 1941, McIver announced a
rigid choledochoscope (produced by ACMI) co-designed
with Reinhold Wappler. The choledochoscope was L-shaped,
with a long arm of 45cm, a short arm of 7cm, and a diameter
of 0.5 cm. It is equipped with a perfusion system and a
photographic system. However, this mirror can only be used
for observation but not for treatment, so it was not taken
seriously. In 1965, the American doctor Shore cooperated
with ACMI to develop optical ber choledochoscope, also
known as soft choledochoscope. The length of the
choledochoscope was 50 cm, with a exible end, freely
adjustable focal length, and clear imaging. The endoscopy is
very convenient; it can not only be used intraoperatively, but