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I. Sucandy et al.
to its anticipated need. Although some data suggests that uorescent identication can occur as early as 20min after injection, we
have found identication of biliary anatomy during hepatectomy
to occur much later than 20min, particularly in patients with liver
cirrhosis. This is caused by the delay in uptake and secretion by
the hepatocytes. Correct timing and dosage is critical in patients
with liver cirrhosis, as they are less tolerant of perioperative complications such as bile leak and intra-abdominal infection; therefore, they benet the most from an accurate anatomical delineation
during hepatobiliary resections.
The ICG is mixed so that one ampule (25 mg) dissolves in
20mL of 0.9% normal saline. In our experience, a higher concentration or dose results in difculty discriminating biliary and nonbiliary structures. This is particularly true when the patient has an
obstructive malignancy or stricture, which dilates smaller bile
ducts, resulting in ICG accumulation and an increase in background uorescent “noise.” It is possible to attenuate the intensity
of the uorescent image on the robotic console at the expense of
sensitivity, should this problem arise.
When performing an anatomical left or right hepatectomy, we
do not routinely dissect the common hepatic duct bifurcation at
the porta hepatis prior to liver parenchymal transection, except
for extrahepatic cholangiocarcinoma or tumor located near the
hilum, in order to preserve the collateral blood supply to the remnant hepatic duct. Instead, after committing to hemihepatic vascular inow (portal venous, hepatic arterial) ligation, we initiate
the parenchymal transection. The corresponding right or left
hepatic duct is identied intraparenchymal at the level of the
hilar place, isolated, and ligated. By utilizing a combination of
preoperative imaging and ICG uorescence and appreciating the
relationship between the glissonean pedicles, we are able to complete an anatomical hepatectomy while avoiding encroachment
and injury to the fragile blood supply of the remnant hepatic
duct. Our technique is demonstrated here in Figs.5.1, 5.2 and
5.3, in Video 5.1, and has been previously reported in the litera-
ture [17–19]. This technique can also be used to identify the biliary anatomy on the hepatic hilum during minimally invasive
donor hepatectomy [20].
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Fig. 5.1 Left hepatic duct identied within the parenchyma during left hepatectomy prior to transection under white light
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Fig. 5.2 Left hepatic duct identied within the parenchyma during left hepatectomy prior to transection under ICG uorescence
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Fig. 5.3 Left hepatic duct transected within the parenchyma during left hepatectomy with spillage of bile conrming anatomy under white light
I. Sucandy et al.
Identication ofPrimary andMetastatic Liver
Tumors
The second application of ICG uorescence imaging is localization of liver cancers in real time during hepatectomy. This
technique is based on the fact that ICG injected IV before surgery is acquired and retained by HCC and other cancerous tissues with signicant differentiation and retention vs. normal
hepatocytes, due to washout from surrounding noncancerous
hepatic parenchyma (Fig.5.4a, b) [21–23]. In poorly differentiated HCC and metastatic liver cancers, portal uptake of ICG
into cancerous tissues is difcult to observe. However, biliary
stasis surrounding these cancers results in a rim of ICG retention and uorescence in the noncancerous hepatic parenchyma
surrounding the tumor, possibly due to compression [23, 24] or
immature hepatocyte function, resulting in decreased biliary
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a
b
c
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Fig. 5.4 Fluorescence images of hepatic malignancies on cut surfaces of
resected specimen after preoperative intravenous injection of ICG (Fig. X).
(a) Well-differentiated HCC. (b) Moderately differentiated HCC. (c) Poorly
differentiated HCC (upper) and colorectal liver metastasis (below)
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Fig. 5.5 Tumor localization during laparoscopic hepatectomy for colorectal
liver metastasis (Fig. Y). (a) A subcapsular tumor is identied by uorescence
imaging on the surface of hepatic segment 4 prior to hepatic transection. (b)
Fluorescence imaging during hepatic transection identied uorescence signals emitted from noncancerous hepatic parenchyma surrounding the tumor,
suggesting the optimal transection plane (dotted line)
I. Sucandy et al.
excretion [25] and rim- enhancing uorescence (Fig. 5.4c).
Regardless of the uorescence patterns, surgeons can utilize the
above mechanism of ICG accumulation for intraoperative identication of subcapsular liver cancers by near-infrared uorescence imaging [21, 26] (Level IV), especially in the setting of
minimally invasive hepatectomy [27, 28] (Level IV) where surgeons cannot palpate hepatic surfaces directly for intraoperative diagnosis (Fig.5.5a).
The utility of ICG in hepatic retention as a measure of liver
function (described in more detail below) led to its use for intraoperative cancer localization [28, 29]. As a consequence, the most
commonly administered dose and timing of ICG is similar for
both modalities, notably at 0.5mg/kg, usually 1–14days prior to
surgery [21]. Alternatively, intravenous ICG injection at a dose of
10mg 24h before surgery [30] or 0.05–0.1mg/kg 24–72h before
surgery [31] works for intraoperative uorescence imaging of
hepatic malignancies. Administration of ICG on the day before
surgery should be avoided to achieve sufcient tumor-tobackground contrast at the time of surgery [23] (Level IV), particularly in instances of decreased liver function due to cirrhosis
or preoperative chemotherapy.
This strategy may not be practical in many countries, where
patient transportation to and from the hospital is sociogeographically challenging. Additionally, HCC even when well-
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differentiated will vary in tumor biology not only from patient to
patient but also among multiple tumors in the same given patient
[32]. Cirrhotic but noncancerous liver parenchyma will vary in
ICG excretion from patient to patient, depending on the level of
parenchymal brosis and other factors (evidence: Level IV) [33].
As a consequence of all these variabilities, the timing between
preoperative administration and operative resection is not exact,
and it is difcult to standardize between patients. The ICG administration must be long enough to allow the often dysfunctional
liver parenchyma to completely excrete the ICG while not permitting too much time to pass for the malignancy to excrete it as well.
The advantages of tumor localization by ICG uorescence
imaging lie in its feasibility and high sensitivity (around 90% or
higher [23, 27, 30], Level IV) for subcapsular tumors. On the
other hand, this technique has limitations in tissue permeability
(5–8 mm from hepatic surfaces) and a relatively high falsepositive rate [23] (Level IV). Surgeons still need intraoperative
ultrasonography for identication of deeply located tumors and
its spatial relationships with intrahepatic vasculature. Any additional resection for newly detected lesions by ICG uorescence
imaging, and not part of the preoperative plan, should only be
considered when malignancy is suggested by other modalities
such as palpation, ultrasonography, or re-evaluation of preoperative imaging studies.
In experienced hands, the high sensitivity and specicity of
liver tumor detection associated with IOUS approaches 95% [34]
(Level IV). Many high-volume liver surgery centers therefore do
not feel that a 1–2-week delay for ICGF tumor identication is
warranted.
Oftentimes, before proceeding to liver resection, a tissue diagnosis is required via percutaneous liver biopsy to conrm the type
of liver cancer. While this can worsen oncologic outcomes via
tumor cell seeding, the biopsy can also alter the dynamic of ICG
absorption and excretion at the local level [35] (Level III). As a
result, the surgeon cannot always be sure as to whether they are
looking for a uorescent HCC or a rim-enhancing non-HCC
malignancy at the time of diagnostic laparoscopy prior to the
intended liver resection.
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Despite these limitations and pitfalls, however, liver cancer
imaging by ICG uorescence retains a critical role in detecting
tiny tumors after effective neoadjuvant therapy or residual tumors
from prior resection [23, 27] (Level IV) and improves acquisition
of appropriate surgical margins (Fig. 5.5b) [27, 36, 37] (Level
IV). Some authors have demonstrated a reduction in operative
duration and recurrence risk with ICG [38, 39] (Level III).
Prospective trials demonstrating clinical efcacy of ICG in generating superior outcomes for liver cancer localization are required
to justify further development and dissemination of this modality,
particularly for hepatobiliary centers that do not routinely evaluate preoperative liver function with ICG.
I. Sucandy et al.
Identication ofVascular Structures andHepatic
Segmentation by Fluorescence Angiography
The third application of ICG is based on its albumin-bound status,
where it can freely circulate in the blood before being taken up by
hepatocytes for biliary excretion. This permits generation of a
rapid uorescent angiogram while performing hepatobiliary
resections. Dissipation of ICG and the angiogram is fairly rapid,
although the biliary excretion requires some time; therefore, multiple uorescent angiograms can be obtained in the same operation. This permits test clamping of multiple candidate pedicles
prior to transection followed by ICGF angiography to ensure correct anatomical identication of inow vessels to ultimately preserve the perfusion of the future liver remnant. A ner dissection
of segmental pedicle anatomy can permit highly accurate
segmentectomy and subsegmentectomy, which has been described
extensively in the literature to be associated with signicantly less
blood loss and blood transfusions—relevant factors in achieving
superior oncological outcomes [40, 41] (Level III).
Since the 2008 landmark paper on the use of ICG uorescence
imaging in the eld of hepatobiliary surgery [42] (Level IV), this
modality has been used for hepatic segmental boundary visualization (hepatic segmentation). In 2012, Ishizawa and Gayet [43] rst
ab
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Fig. 5.6 Hepatic segmentation with positive staining technique (Fig. X/Z).
(a) ICG solution (0.25mg/5mg) is injected into the tumor (HCC)-bearing
hepatic segment (segment 6) following intracorporal puncture of the root of
corresponding portal branch. (b) Fluorescence imaging clearly visualizes
boundaries between hepatic segments 6 and 7
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applied uorescence-guided hepatic segmentation to laparoscopic
hepatectomy utilizing a “positive staining technique” (injection of
ICG solution directly into the corresponding portal branch under
ultrasound guidance, following conventional dye- staining technique [44]) and “negative staining technique” (intravenous ICG
injection following closure of the corresponding portal pedicle at
its root, not unlike a conventional Glissonian approach [45]). The
positive staining technique (Fig.5.6) has the advantage in omitting
unnecessary dissection at the hepatic hilum; however, puncture of
the portal pedicle from the skin surface of the abdominal wall is
technically demanding, despite some described technical tricks
[46, 47], especially in the setting of minimally invasive surgery.
Robotic-assisted surgery may facilitate needle manipulation to
puncture the portal venous branch in the patient’s abdominal cavity [48] (Level III). In contrast, a negative staining technique is
suitable when the root of the target Glissonian sheath is easy to
access (e.c. Couinaud’s segment 2 to 6), as suggested by the current consensus guidelines [49] (Level VII).
Hepatic segmentation by ICG uorescence imaging enables
clear identication of intersegmental planes not only from the
hepatic surface but also on raw surfaces during parenchymal dissection throughout the hepatectomy procedure [27], enhancing
the accuracy of anatomical hepatectomy [50] (Level IV) and
improving operative outcomes. Liver remnant ischemia, prevented by ICG uorescence-guided hepatectomy, is known to
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I. Sucandy et al.
result in higher postoperative bile leaks, bilomas, and abscesses
[51] (Level IV). This is also associated with inferior long-term
oncological survival, especially in the case of hepatectomy for
primary liver cancer [52] (Level III).
In the growing eld of partial liver donation in hepatic transplantation, graft viability can be accurately assessed by ICG
uorescence angiography. The caveat to ICG uorescence angiography is that repeat application will be hindered 20–40min
later following the initial injection when biliary uptake and
excretion occurs so that any functional liver will uoresce and
will continue to do so for a few hours regardless of ischemic
clamping. Therefore, if the surgeon wishes to perform repeated
angiograms, they must do so before signicant biliary uptake
renders background noise too great to differentiate ischemic and
perfused tissue.
At our tertiary hepatobiliary institution, we isolate and visually test clamp the candidate specimen portal and hepatic arterial pedicle during minimally invasive robotic hepatectomy to
compensate for the absence of palpation. A bedside assistant,
usually a board-certied general surgeon who participates as a
hepatobiliary surgery fellow, laparoscopically inserts a bulldog
clamp through a right lower quadrant GelPort®. The console surgeon will then apply the clamp at the candidate pedicle. The
anesthesia team will then administer 0.5mL of our aforementioned ICG mixture (25mg in 20 mL of 0.9% normal saline)
through a venous access. After 1–2 min, the console surgeon
activates the Firey ™ camera system and can switch back and
forth between white light and ICG uorescence camera visualization. The surgeon can also continue the operation in ICG
uorescence mode, allowing a robotic monopolar cautery to be
used to mark the transection plane along the visualized uorescent demarcation. Upon conrmation of devascularization of the
specimen side and perfusion of the future liver remnant side, the
bulldog clamp is released under white light, the pedicle is
ligated, and the hepatectomy proceeds. Our technique is demonstrated in Figs.5.7, 5.8, 5.9 and 5.10 and Video 5.2. Very littleto-no ischemic-appearing tissue should remain on the transected
liver edge (Fig.5.11).
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Fig. 5.7 Right hepatic artery identied at the hepatic hilum prior to clamping
during a right hepatectomy under white light
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Fig. 5.8 Right hepatic artery identied at the hepatic hilum with bulldog
clamp applied during a right hepatectomy under white light
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