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Resection of noncolorectal liver metastases 229
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230 Chapter 14
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Videos 1–20 will be of interest to readers of this chapter.
Visit the companion website at:
www.wiley.com\go\conrad\liver-pancreas-biliary-laparoscopic-surgery
CHAPTER 15
Intraoperative laparoscopic ultrasound for
laparoscopic hepatopancreatobiliary surgery
Kenichiro Araki1and Claudius Conrad
1
Department of General Surgical Science, Gunma University Graduate School of Medicine, Gunma, Japan
2
Department of Surgical Oncology, University of Texas MD Anderson Cancer Center, Houston, USA
EDITOR COMMENT
In this chapter, we describe the critical importance of intraoperative ultrasound. A probe with at least four degrees of freedom is needed
to overcome the limitations imposed by the trocar-to-target axis and to obtain optimal apposition of the probe against the target lesion.
Nevertheless, trocar placement must anticipate the intraoperative use of ultrasound. Additionally, because of the limitation of the trocarto-target axis, the laparoscopic ultrasound image might be more challenging to interpret and therefore requires practice. Frequent use of
intraoperative ultrasound during laparoscopic liver surgery increases its safety through the identification of landmark structures and
assessment of the relationship of lesions to critical anatomical structures. Ultrasound of the future liver remnant with and without
Doppler mode excludes other lesions and ensures perfusion. Intraoperative laparoscopic ultrasound also has an important role during
pancreatic surgery in nodal staging and in the identification of pancreatic neuroendocrine tumors. This chapter can help the reader to
improve their ultrasound technique, while further practice is needed to optimize the skill.
Keywords: anatomical laparoscopic liver resection, contrast-enhanced laparoscopic ultrasound, intraoperative laparoscopic ultrasound
2
15.1 Introduction 15.2 Technical requirements for
laparoscopic intraoperative
Intraoperative ultrasonography (IOUS) is a critical tool for
laparoscopic hepatopancreatobiliary (HPB) surgery. This
techniqueisvaluablebothforthe intraoperative diagnosis
of liver or pancreas lesions but also for guidance of the actual
resection. Especially in open and laparoscopic liver resection, laparoscopic IOUS technique is important for planning
and guiding liver parenchymal transection. In our experience, the systematic use of IOUS is indispensable for both
laparoscopic anatomical and nonanatomical liver resections [1]. In pancreas surgery, reports show that laparoscopic IOUS is useful for detecting tumors (especially
neuroendocrine tumors) and screening for metastatic
lesions. In this chapter, we describe our IOUS technique
for laparoscopic HPB surgery, with a focus on laparoscopic
IOUS techniques for laparoscopic liver resection.
ultrasonography
The patient is usually placed in a low lithotomy position,
and the operating surgeon stands in the middle between
the patient’s legs; the ultrasound probe should be handled
from this position. Five or six trocars are used in the right
upper quadrant of the abdomen and maintained in position with a focus on optimal triangulation. While most
trocars are 5 mm in size, we usually insert two 12 mm (or
10 mm) trocars in an axis that allows for using the ultrasound probe while maintaining an optimal view with the
camera on the liver. The observed liver anatomy and
target lesions should complement the mental image
obtained preoperatively using multidetector computed
tomography (CT) or magnetic resonance imaging (MRI).
Laparoscopic Liver, Pancreas, and Biliary Surgery: Textbook and Illustrated Video Atlas, First Edition.
Edited by Claudius Conrad and Brice Gayet.
© 2017 John Wiley & Sons, Ltd. Published 2017 by John Wiley & Sons, Ltd.
231
232 Chapter 15
Figure 15.1 Pro Focus ultrasound system and flexible laparoscopic probe (BK Medical).
The laparoscopic ultrasound probe should have a flexi-
ble tip to allow for optimal apposition with the liver. This
probe can be adjusted through an angle of up to 90° in four
planes by two levers. Keeping the handle as a reference in
an upright position, possible movements are up, down,
left, and right as well as twisting the probe (Figure 15.1).
Thus, it can be placed into the optimal relationship to the
target structure to obtain a high-quality ultrasound
image, despite the limitations in movements defined by
the trocar–target axis.
The ultrasound monitor is optimally placed next to the
laparoscopic monitor to allow for in-line working. Preferred over this approach is the “picture-in-picture” mode
on the laparoscopic monitor, which allows the surgeon to
see both laparoscopic and ultrasound images on one
monitor, which further optimizes ergonomics. Using a
remote control function of the ultrasound system optimizes team dynamics and facilitates making changes to
the ultrasound settings such as changing parameters of
the echo mode, measuring tumor margin, and switching
Doppler blood flow mode (Figure 15.2).
15.2.1 Intraoperative ultrasonography
with contrast enhancement
in liver
Recent studies of intraoperative contrast-enhanced ultrasound (CEUS) with different contrast agents have shown
that it is more sensitive, specific, and accurate than normal IOUS, CT, or MRI in defining resectability of liver
metastases or hepatocellular carcinoma. It is now recognized that the more aggressive the adopted surgical
approach, the higher the impact of intraoperative
CEUS. Also, in laparoscopic procedures, intraoperative
CEUS can be helpful to exclude new liver lesions not
previously discovered on preoperative imaging. The new
guideline for the use of CEUS was published in 2013 [2].
Contrast agents for ultrasonography are now licensed
in many parts of the world. There are two vascular
contrast agents: SonoVue (sulfur hexafluoride with a
phospholipid shell; Bracco SpA, Milan, Italy) and Definity/Luminity (octafluoropropane [perflutren] with a
lipid shell; Lantheus Medical, Billerica, MA, USA). Injections may be repeated for global assessment or to assess
the arterial phase enhancement of identified lesions for
their characterization. After it has disappeared from the
Figure 15.2 Handling the laparoscopic IOUS with a remote
controller.
Laparoscopic ultrasound for hepatopancreatobiliary surgery 233
vascular pool, Sonazoid (perfluorobutane with a phospholipid shell: hydrogenated egg phosphatidyl serine;
Daiichi-Sankyo, Tokyo, Japan) persists for several hours
in liver and spleen. Sonazoid is phagocytosed by Kupffer
cells, which contributes to its persistent uptake in the
liver. However, this agent is licensed only in Japan and
South Korea (November 2013). Using Sonazoid
enhanced intraoperative ultrasound, detection of malignant focal liver lesions begins 10 minutes after injection.
15.3 Laparoscopic ultrasonography
for liver resection
Laparoscopic hepatectomy is a safe procedure and has
potential advantages over open surgery with respect to
blood loss and postoperative hospital stay [3,4]. However,
significant bleeding is more difficult to control during
laparoscopic hepatectomy than during an open approach
and therefore the prevention of vascular injury is crucial.
This should be achieved not only through an excellent
preoperative understanding of the vascular anatomy
derived from preoperative imaging but also through
real-time image guidance during surgery. Some procedures, such as posterosuperior segmentectomy (Sg7 or
Sg8) and limited resection for deeply located liver tumors,
require expert laparoscopic hepatectomy techniques. For
these procedures, accurate real-time imaging of liver
anatomy and a thought-out operative resection plan
are necessary. In order to accomplish this, the use of
intraoperative ultrasound imaging is of the utmost
importance.
The procedural steps for IOUS of hepatectomy are as
follows. After screening the entire liver, we focus our
attention on the future liver remnant in case of cancer
surgery. It is more important to rule out any undetected
lesions in the future liver remnant than to identify liver
lesions in the liver to be resected. The tumor characteristics of known tumors are important as known isodense
liver lesions predict a higher likelihood of missing lesions
not identified on preoperative imaging. The hepatic veins
and their branches and their relationship to the resection
line are determined and the portal structures at the
transection plane visualized. After this information has
been gathered, we determine the vertical (longitudinal)
and horizontal (latitudinal) lines of the parenchymal
transection plane. Doppler mode is used to identify the
portal pedicles, hepatic veins, and hepatic arteries if
necessary.
Table 15.1 summarizes technical differences between
laparoscopic and open IOUS techniques. The laparoscopic
ultrasound probe position and angulation are restricted
by the trocar’s position, abdominal cavity, and target area
of the liver. The laparoscopic liver surgeon is frequently
required to place the probe at an angle different from that
of an open procedure because of the laparoscopic restrictions imposed by the trocar–target axis. Thus, laparoscopic surgeons must consider the relationship between
the trocar positions and liver in order to place the ultrasonic probe in such a way that the resulting image is easily
Table 15.1 Technical differences between laparoscopic and open IOUS in liver surgery.
Laparoscopic IOUS Open IOUS
Visualization of ultrasound view On the monitor Direct view
(PiP mode)
Width of scan area Good Good
Depth of scan area Good Good
Freedom of ultrasound probe Limited Good
(need flexible probe)
Direction tendency of probe Vertical Horizontal
Application for PS segments Transdiaphragmatic access Mobilization of right lobe
Additional tactile information Poor Good
Ultrasound-guided puncture Difficult Easy
(biopsy attachment)
Contrast enhancement Possible Possible
IOUS, intraoperative ultrasonography; PiP, picture in picture; PS, posterosuperior.
234 Chapter 15
interpretable. Achieving an optimal and easily interpretable ultrasound image is facilitated with a laparoscopic
probe that is flexible.
An important goal of IOUS is to identify portal and
hepatic vessels and their positional relationship. In major
hepatectomy procedures, IOUS allows for the identification of the middle (right and left hepatectomy) or the right
(central hepatectomy and extended left hepatectomy)
hepatic veins as a landmark of the parenchymal transection plane and the drainage branches of the hepatic vein.
The flexibility of the IOUS probe allows placement of the
probe in the necessary direction. We discourage the use of
fixed probes as the probe orientation is determined by the
relationship of trocar to target and the most effective
orientation of the probe might not be achievable. In
segmentectomies, it is important to identify the vertical
(longitudinal) demarcation line and IOUS allows for
visualization of the hepatic vein as a vertical landmark;
for example, the middle hepatic vein is between segments
IV and V/VIII, and the right hepatic vein is between
segments V/VIII and VI/VII. To identify the horizontal
(latitudinal) demarcation line of the segment, such as that
between segments V and VIII, or segments VI and VII,
IOUS allows for visualization of the bifurcation of the
portal pedicle as a horizontal landmark.
Below, we describe six applications of IOUS, which
highlight the importance of it. The cases demonstrated in
the accompanying video (Video 1) are left lateral sectionectomy, right hepatectomy, and segmentectomy VIII.
We aimed to describe general principles of our IOUS
technique in this video, so it can be adapted for other
procedures, such as limited (wedge or partial) resection,
left hepatectomy, and so on.
15.3.1 Identification of hepatic and
portal vessels in left lateral
sectionectomy
In left lateral sectionectomy, it is important to understand
the distance between the portal pedicle and left hepatic
vein along the transectionplane using IOUS (Figure 15.3).
The video shows identification of the portal pedicle (P2,
P3) and left hepatic vein, and their subsequent safe resection. In this procedure, the middle hepatic vein also needs
to be identified, because its drainage runs close to the
transection plane in the upper part of the parenchymal
transection plane (see Figure 15.3).
15.3.2 Visualization and dissection of
branches of the hepatic vein
during major hepatectomy
In major hepatectomies (e.g. right and left hepatectomy),
we identify with IOUS the middle hepatic vein as the
landmark vein as well as its branches (V4, V5, and V8
and the fissure veins) before commencing with the parenchymal transection. The video shows that the branches of
V4, V5, and V8 are exposed during right hepatectomy
(Figure 15.4) and can be safely dissected (V5 and V8)
or preserved (V4). These steps described in the video
for a right hepatectomy are analogous for a left
hepatectomy.
Figure 15.3 Laparoscopic IOUS in left lateral sectionectomy.
Figure 15.4 Laparoscopic IOUS in major hepatectomy.
Laparoscopic ultrasound for hepatopancreatobiliary surgery 235
15.3.3 Determination of the parenchymal
transection plane in
segmentectomy
For segmentectomies, we visualized the landmark
hepatic vein as the vertical (longitudinal) demarcation
line using IOUS and bifurcation of the portal pedicle as the
horizontal (latitudinal) demarcation line in each procedure (Figure 15.5). In the video we demonstrate a resection of Sg8: we visualize the middle and right hepatic
veins as the landmarks of the vertical line and the P8
portal pedicle as the landmark of the horizontal line (see
Figure 15.5). In limited resection, accurate recognition of
the hepatic vein and portal pedicle near the resected liver
tumor is also important, so these steps are also important
for limited (wedge or partial) resection.
15.3.4 Identification the tumor-bearing
portal pedicles for
segmentectomies
The tumor-bearing portal pedicle was determined with
IOUS, which allowed for visualization of the portal flow
and calculation of the margin. We sometimes inject dye or
indocyanine green into the vein in order to visualize the
true limits of the segment [5]. The video shows the Sg8
portal pedicle and measurement of the resection margin
(see Figure 15.5). We used regenerated oxidized cellulose
(Surgicel Fibrillar, Ethicon Inc., Somerville, NJ, USA) for
hemostasis during parenchymal dissection. In addition,
the echogenicity of the material is useful for visualization
of the transecting line as the echo artifact can be clearly
visualized in the parenchymal transection plane.
15.3.5 Ensuring intact vascularization in
the remnant parenchyma
Doppler mode is useful for detecting intact vascularization
in the remnant liver parenchyma. The video shows a case
of segmentectomy VIII after left lateral sectionectomy and
visualization of the preserved hepatic vein vascularization
(V4a, V4b) in the remnant segment IV after the dissection
between segments IV and VIII.
15.3.6 Visualization of the drainage of
the right hepatic vein for
posterosuperior segmentectomy
Posterosuperior segmentectomy (Sg7 or Sg8) is one of the
most difficult procedures of laparoscopic hepatectomy. In
this procedure, we used a right intercostal and transdiaphragmatic access. Transdiaphragmatic trocar placement allows for a direct approach to the drainage of the
right hepatic vein. Such transdiaphragmatic trocars might
facilitate accurate location of the position of the right
hepatic vein and venous branches for parenchymal dissection with IOUS. In the video, using IOUS, we expose
the V8 branch of the right hepatic vein (Figure 15.6),
safely perform the dissection, and finally expose the roots
of the middle and right hepatic veins.
15.4 Laparoscopic ultrasonography
for pancreas surgery
In pancreatic surgery, laparoscopic ultrasonography provides the surgeon with an additional sensitive means of
236 Chapter 15
Figure 15.5 Laparoscopic IOUS in segmentectomy.
Figure 15.6 Laparoscopic IOUS in posterosuperior
segmentectomy.
detecting small metastases during staging and allows for the
assessment of local tumor invasion, regional nodal involvement, and distant metastatic spread to the liver [6]. Several
articles have reported encouraging preliminary results with
laparoscopy and laparoscopic ultrasonography in the assessment of patients with pancreatic tumors and liver metastases. We usually perform laparoscopic staging with IOUS for
presumably resectable pancreatic cancer. This frequently
demonstrates metastastic disease or local unresectability,
which precludes curable resection. This approach reduces
the rate of nontherapeutic laparotomy.
Resection for pancreatic neuroendocrine tumor requires
accurate localization. However, pancreatic neuroendocrine tumors are frequently difficult to detect with
the laparoscopic view only.Theirlocalization can be greatly
facilitated through the use of intraoperative ultrasound.
Several articles have described the utility of laparoscopic
ultrasonography for the intraoperative localization of
Laparoscopic ultrasound for hepatopancreatobiliary surgery 237
neuroendocrine tumors [7]. Because of their hypervascularity, IOUS with contrast enhancement can be performed
for selected, difficult-to-detect pancreatic neuroendocrine
tumors.
also in evaluating the biliary anatomy [8]. We routinely
use laparoscopic IOUS during laparoscopic cholecystectomy to rule out the existence of common bile duct stones.
Some reports suggest that routine use of IOUS reduces the
need for intraoperative cholangiography during laparo-
15.5 Laparoscopic ultrasonography
for biliary surgery
scopic cholecystectomy with high sensitivity and without
increased overall cost [9].
In biliary surgery, IOUS has been reported to be an
effective tool not only in detecting bile duct stones but
KEY POINTS
• Intraoperative laparoscopic ultrasound is crucial for operative planning, lesion detection, and ensuring perfusion of the future
liver remnant.
• Contrast-enhanced laparoscopic ultrasound can facilitate lesion detection and characterization.
• Laparoscopic ultrasound can facilitate the identification of pancreatic neuroendocrine tumors.
• Advanced laparoscopic anatomical resections can only be performed if the surgeon is well versed in the use of laparoscopic
ultrasound.
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CHAPTER 16
Minimally invasive liver surgery: indications
and contraindications
Thomas A. Aloia
Department of Surgical Oncology, University of Texas MD Anderson Cancer Center, Houston, USA
EDITOR COMMENT
This chapter describes a conceptual framework for the indications and contraindications for liver resection for achieving the healthcare
goals set forth by the Institute of Medicine’s publication Safe, Effective, Patient-Centered, Timely, Efficient, and Equitable Care. This
review of the available literature indicates that the majority of minimally invasive liver resections have been minor procedures. Only a
limited number of highly specialized centers have reported major minimally invasive liver resections. To us, these data indicated that there
is a need for greater diffusion of surgical concepts and techniques that would allow for the safe and oncologically sound expansion of
more advanced laparoscopic liver surgery – a prime impetus for creating this work. Further, the author calls for introspective
professionalism, oversight, and monitoring of exact indications on a case-by-case basis to safely expand the experience to more
extensive laparoscopic liver resection. These are concepts that certainly are not limited to minimally invasive liver resections, but the
complex nature of advanced minimally invasive liver resection demands apprehension of a significant number of oncological, patient
management, and technical concepts that have been presented to the reader throughout this work.
Keywords: indications for laparoscopic liver surgery, indications for minimally invasive liver surgery, oncological outcomes
of laparoscopic liver surgery, professionalism in laparoscopic liver surgery, quality control in laparoscopic liver surgery, safety in
laparoscopic liver surgery
16.1 Introduction
The past 20 years have seen a rapid expansion of the
indications for minimally invasive approaches to liver
surgery. The increased utilization of minimally invasive
approaches to liver resection has paralleled improvements in open surgical technique, anesthetic management, and multidisciplinary care that have combined to
greatly improve the safety of liver surgery. Given our
current ability to rapidly introduce and communicate
new techniques and technologies, there is no doubt
that the indications for liver surgery and minimally invasive approaches will continue to evolve. As experience
builds, new techniques are disseminated and new equipment is introduced, the indications for minimally invasive
liver resection will undoubtedly expand, potentially mak-
Laparoscopic Liver, Pancreas, and Biliary Surgery: Textbook and Illustrated Video Atlas, First Edition.
Edited by Claudius Conrad and Brice Gayet.
© 2017 John Wiley & Sons, Ltd. Published 2017 by John Wiley & Sons, Ltd.
238
ing the specific content of this chapter obsolete. To reduce
the chance of this occurring, this chapter intentionally
avoids drawing concrete “lines in the sand” regarding the
indications and contraindications to minimally invasive
liver resection. Instead, it proposes a more flexible conceptual framework for evaluating resectability issues that
may accommodate both predictable and unpredictable
future advances in the field.
From a quality of medicine perspective, the discussion
of indications and contraindications for minimally invasive liver surgery can be framed by the Institute of
Medicine (IOM) healthcare goals of Safe, Effective,
Patient-Centered, Timely, Efficient, and Equitable Care [1]
(Table 16.1). Independent of advances in instrumentation, when these criteria are met, there is and will
continue to be a clear indication for this approach to liver
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