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Fig. 3.6 To ensure long-standing visualization during surgery, the ureteral
stent can be occluded for approximately 30s to allow the indocyanine green
(ICG) to bind to the protein molecules in the urine
M. R. Freund et al.
der of the procedure, a fact of which nursing and anesthesia team
should be aware.
Literature Review ofUse ofFluorescence Guidance
inColorectal Surgery
In recent years, there have been an increasing number of publications regarding use of ICG uorescence perfusion assessment in
colorectal surgery and its effect on reducing anastomotic leak
complications [30]. We will succinctly review the most signicant
and relevant articles (Table3.2).
The earliest and one of the largest studies exploring the effect
of ICG uorescence perfusion assessment on anastomotic leak
came from Germany by Kudzos etal. [38]. The ICG perfusion
assessment study group, after matching, included 201 patients
undergoing surgery for colorectal cancer between 2003 and 2008.
The control group contained a similar number of patients operated
between 1998 and 2003. The study included laparoscopic as well
as open surgery and right colectomies, left colectomies, and low
anterior resection (LAR). The study looked at clinically apparent
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8% change in surgical
plan. Overall leak rate
1.4%. 0% leak rate in
patients with revised
anastomosis based on
inadequate
Primary:
Feasibility and
safety;
Left-sided colectomy
and anterior
resection
No. of
patients Operations Endpoint Conclusions
139
assessed
with ICG
intraoperative
decision- making
Secondary:
uorescence
Clinical outcomes
5.8% change in
surgical plan. No
including
anastomotic leak
Primary:
Intraoperative
Right
hemicolectomy, high
504
assessed
anastomotic leaks in
group with change in
surgical plan. Overall
leak rate for
decision- making
Secondary:
Anastomotic leak.
and low anterior
resection, reversal of
Hartmann’s, ileoanal
K pouch, and
with ICG
97
(continued)
colorectal procedures
2.6%. Overall leak
rate for low anterior
resection 3%.
ileorectal
anastomosis
POINPOINT—
Novadaq
PILLAR
II—Prospective
multicenter
clinical trial, 11
centers
Author/year Study type System used
Jafari
Table 3.2 Literature review of use of uorescence guidance in colorectal surgery
(2015) [31]
POINPOINT—
Novadaq
Prospective
phase II study, 3
centers
Ris (2018)
[27]
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Non-PINPOINT
Anastomotic
Colectomy, anterior
347 (238
No. of
patients Operations Endpoint Conclusions
group 5.5%
anastomotic failure.
PINPOINT group
0.84% anastomotic
leakage or
stricture
resection, reversal of
Hartmann’s
ICG, 109
control)
failure, 4.6% had
change in resection
margin based on
uorescence; none
had anastomotic
M. R. Freund et al.
failure
Anastomotic leak 9%
in control group vs
5% in ICG group
Primary:
Anastomotic leak
Secondary:
Intraoperative
decision- making
Left-sided and rectal
resections
ICG, 122
control)
For Clavien-Dindo
grade ≥3 anastomotic
leaks, leak rate 9.5%
in control group and
2.8% in ICG group.
Primary:
Anastomotic leak
Secondary:
Intraoperative
change of surgical
Laparoscopic low
anterior resections
for rectal cancer
each
group, ICG
vs control,
propensity
OR 0.280 (p=0.007)
plan
score
matched)
PINPOINT—
Novadaq
Retrospective,
single center
Starker
(2018) [32]
Author/year Study type System used
Table 3.2 (continued)
Multicenter Karl Storz 240 (118
De Nardi
(2020) [33]
Karl Storz 422 (211in
Retrospective
study, 3 centers
Watanabe
(2020_ [34]
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Anastomotic leak 6%
in control group, 0%
in ICG group
Overall anastomotic
leak rate 5.4%. For
patients with low
anterior resection,
leak rate 4.5%
compared to 13.6% in
control group
Anastomotic leak
13.6% in control,
Primary:
Anastomotic leak
Primary:
Left hemicolectomy,
sigmoid colectomy,
anterior resection
Right and left
ICG, 98
control)
296
Intraoperative
decision- making
Secondary:
colectomy, anterior
resection,
Hartmann’s reversal
assessed
with ICG
2.8% in ICG group
Anastomotic leak
Primary:
Anastomotic leak
Laparoscopic
anterior resection or
intersphincteric
420 (141
ICG, 279
control,
resection for rectal
propensity
Anastomotic leak
10.7% in control
Primary:
Anastomotic leak
cancer
Left colectomy,
anterior resection
score
matched)
384 (197
ICG, 187
99
group, 3.3% in ICG
group
control)
Karl Storz 196 (98
Retrospective
Impellizzeri
SPY—Novadaq/
study, 1 center
Retrospective
(2020) [26]
Marquardt
Firey for
robotic
study, 1 center
(2020) [35]
Karl Storz/
Mizuho medical
SPY—Stryker
Retrospective
study, 1 center
Hasegawa
(2020) [36]
Karl Storz/
Mizuho Medical
Prospective
collected data,
retrospective
analyzed study,
Yanagita
(2021) [37]
1 center
RCT randomized controlled trial, ICG indocyanine green, OR odds ratio. Reused with permission. Copyright 2021 Springer Nature
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M. R. Freund et al.
AL requiring surgical intervention and showed that this rate was
lower in the ICG study group (3.5% vs 7.5%). Although this difference did not reach statistical signicance, subgroup analysis
revealed that in elective resections the rate of revision was 3.1%
in the ICG study group compared to 7.7% in the control group
(p=0.04), amounting to a reduced risk of revision by 60%. This
study is classied as level of evidence IV as it is a well-designed
case-control study.
The rst large-scale clinical trial that investigated the use of
ICG uorescence perfusion assessment and its impact on AL rate
was the PILLAR II trial study [31]. This was a prospective, multicenter, open- label trial consisting of 139 patients who underwent intraoperative ICG perfusion assessment during left-sided
colectomy and anterior resection. The most common indications
were diverticulitis (44%), rectal cancer (25%), and colon cancer
(21%). ICG perfusion assessment was successful in 99% of
patients and dictated a change in the operative plan in 7.9%, with
the majority of changes related to the transection of the proximal
margin (7%). Overall anastomotic leak rate was quite low (1.4%),
and there were no anastomotic leaks in those patients in which
ICG dictated a change in surgical plan. This study is considered
level of evidence III as it lacked randomization and included both
left-sided resections and anterior resections, as well as laparoscopic and robotic procedures in its analysis.
Ris etal. [27] published a prospective phase II study which
included 504 patients from three European referral centers who
underwent elective colorectal surgery with anastomosis using
ICG perfusion assessment over a 3-year interval. Indications for
surgery included 330 patients with rectal cancer and 174 patients
with benign pathology. ICG perfusion assessment was successful
in all patients and dictated a change in the site of bowel resection
margins in 5.8% of patients with no anastomotic leaks detected
in this group of patients. Overall leak rates were again quite low
(2.4%) including 2.6% for colorectal anastomosis and 3% for
LAR anastomoses. When comparing this data to over 1000 similar procedures performed in the participating centers without
ICG, they showed a reduced overall leak rate for colorectal procedures from 5.8 to 2.6%, and reduced the leak rate for LAR
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101
from 10.7 to 3%. This study is also considered level of evidence
III as it lacked randomization and consisted of a relatively low
proportion of low anterior resections (only 17.9% of the study
group).
Starker etal. [32] described a retrospective single institution
experience of 347 patients undergoing colectomy with primary
anastomosis. Two hundred thirty-eight patients underwent intraoperative ICG perfusion assessment and 109 patients were in the
control group. ICG perfusion assessment dictated a change in
resection margin in 4.6% of patients, and none of these patients
developed AL.Anastomotic leak rate was 0.84% in the ICG group
and 5.5% in the control group. Since this publication was a retrospective descriptive study from a single center, it is assigned the
level of evidence VI.
A more recent multicentered randomized controlled trial from
Italy by De Nardi etal. [33] focused on patients undergoing laparoscopic left-sided colon resections and LAR for rectal cancer.
After randomization, a total of 240 patients were included in the
analysis, 118in the ICG perfusion assessment study group and
122 in the control group. ICG perfusion assessment dictated a
change in proximal resection margin in 11% of patients. AL rates
were lower in the study group (5%) than in the control group
(9%), but this difference was not statistically signicant due to
this study having been underpowered. This large multi-site randomized controlled trial is considered level II evidence.
Another larger multicenter retrospective study from Japan by
Watanabe et al. [34] focused on the effect of ICG uorescence
perfusion assessment on reducing the risk of AL in LAR for rectal
cancer. A total of 211 patients from three institutions were
matched into the ICG study and the control group by propensity
score. ICG perfusion assessment dictated a change in proximal
resection margin in 5.7% of patients. The reported clinical leak
rate was 9.5% in the control group and 2.8% in the ICG group.
This well-designed case-control study is classied as level of evidence IV.
Four additional retrospective single center studies by
Impellizzeri etal. [26], Yanagita etal. [37], Marquardt etal. [35],
and Hasegawa etal. [36] looked at the effect of ICG uorescence
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M. R. Freund et al.
perfusion assessment in patients undergoing colon and rectal
resections (summarized in Table3.1). They all reported statistically signicant reduced anastomotic leak rates in the ICG group
compared to the control group. Since they were all single center
descriptive non-randomized studies, they are classied as level of
evidence VI.
A consensus conference statement on the general use of nearinfrared uorescence imaging and ICG-guided surgery showed the
result of a modied Delphi study [39]. Experts from ve continents
reached consensus on 41 of 44 statements, including strong consensus that near-infrared uorescence- guided surgery is both effective
and safe across a broad variety of clinical settings, including the
assessment of tissue perfusion and anastomotic leaks. This report of
an expert committee is assigned a level of evidence VII. More
recently, the results of an intercontinental Delphi survey including
35 experts from ve continents regarding the use of uorescence
imaging and ICG during colorectal surgery were published [40]. At
least 70% consensus was reached on 60 statements and all seven
statements regarding ICG being used to assess anastomoses reached
a consensus. There was a 100% consensus regarding that statement
that conrming adequate perfusion of the anastomosis is a reason
for ICG use during colorectal surgery. There was also a 96% consensus regarding the statement that use of ICG potentially decreases
the risk of anastomotic leakage. Some of the statements also
included a recommendation for using ICG to also assess right-sided
anastomoses when there is indecision regarding adequate or optimal anastomosis perfusion or when there is signicant atherosclerosis and mesenteric occlusion. This report of an expert committee
is also assigned a level of evidence VII.
The most recently debated randomized controlled trial focusing on perfusion assessment in left- sided resections and LAR was
the PILLAR III trial [41]. This multicenter study planned to
recruit 450 to 1000 patients and randomize them with a 1:1 ratio.
This study was concluded early because of decreasing accrual
rates. A total of 25 centers recruited 347 patients, of whom 178
were randomly assigned to the ICG perfusion group and 169 to
the control group. Anastomotic leak rate was 9.0% in the study
group compared with 9.6% of standard (p=0.37). Unfortunately,
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this trial was heavily underpowered as it was originally designed
to enroll up to 1000 patients. Nevertheless, the level of evidence
assigned for this well-designed albeit vastly underpowered RCT
is level II.
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Treatment ofMetastatic Colorectal Cancer
Indocyanine green uorescence imaging (ICG-FI) has recently
emerged as a tool for the detection of metastatic lesions, primary
tumors, and lymph nodes in several entities. In the following section, the opportunities for tumor detection in colorectal carcinoma
(CRC) is reviewed.
Peritoneal Carcinomatosis
Cytoreductive surgery (CRS) combined with hyperthermic intraperitoneal chemotherapy (HIPEC) remains an important therapeutic option that prolongs overall survival (OS) in select patients
with peritoneal carcinomatosis (PC) from colorectal carcinoma
(CRC). To clinically quantify and classify PC, Paul Sugarbaker
established the peritoneal carcinomatosis index (PCI) in 1966
[42]. The main goal of CRS is complete macroscopic resection of
all peritoneal metastatic lesions [43–45].
Preoperative computed tomography (CT) and positron-emission tomography CT (PET-CT) scans to determine the extent of
PC are unreliable. Sensitivities range between 30% to 47% for CT
and 20% to 57% for PET-CT scans [46–49].
To achieve complete macroscopic resection, the intraoperative
visualization of peritoneal metastatic lesions using ICG-FI has
been investigated. Liberale and colleagues performed one of the
rst studies, including 17 patients in a prospective evaluation. In a
pilot case, ICG was administered 24h prior to surgery, analogous
to the ICG administration procedure for hepatic lesions. In this
study, there were no uorescent signals from peritoneal lesions.
The following patients received an intravenous dose of 0.25mg/
kg of body weight after initial exploration of the abdominal cav-
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M. R. Freund et al.
ity. As a result, additional lesions that could not be detected under
white light and manual palpation were identied in 4 out of 14
patients (29%) with non-mucinous colorectal cancer. Because of
the associated hypervascularization of these lesions, they appeared
to be isouorescent or hyperuorescent. Sensitivity and specicity were 87.5% and 100%, respectively. In contrast to the detection of lesions from non-mucinous tumors, sensitivity was 0% for
mucinous tumors [50].
Likewise, Lieto etal. report an increased intraoperative detection sensitivity using ICG-FI in patients with PC from CRC.A
total of 65 peritoneal lesions could be identied in the seven
included patients. Sixteen lesions (25%) could not be identied
by surgical exploration alone. The same dosage was used as in the
previously described study. Analysis occurred at a median of
50 min after administration. Compared to the preoperative CT
scan and the clinical evaluation, ICG-FI showed the highest sensitivity (43.1%, 76.9%, and 96.9%, respectively) [51].
Barabino etal. also reported the use of ICG-FI in patients with
PC from CRC.They administered 0.25mg of ICG per kg of body
weight 24h prior to surgery. The authors were unable to identify
additional lesions, the sensitivity of ICG-FI was 72.4%, and the
specicity was 60.0% [52].
In summary, there is currently little data with level V evidence
on the intraoperative use of ICG-FI to detect peritoneal metastatic
lesions from CRC [53], and the sensitivity and specicity vary
greatly between studies. However, there is an overall benet due
to the potentially increased detection rate of PC lesions.
Taking these ndings into consideration, we propose the intraoperative administration of ICG with a dose of 0.25mg/kg of
body weight before abdominal exploration. Injection after adhesiolysis or intrabdominal bleeding (associated with excretion of
ICG) can make the subsequent detection of the PC impossible.
Detection should be performed within 60min after administration. The current literature suggests that ICG-FI might lead to the
detection of additional lesions, especially in non-mucinous CRCs.
Thus, the use of ICG-FI may result in a more accurate identication and resection of peritoneal metastatic lesions.
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105
Liver Metastasis
The liver is the most common site of CRC metastasis [54, 55].
The recommended therapeutic approach for patients with synchronous or metachronous liver metastasis in the absence of
extrahepatic metastatic lesions is an R0 resection if technically
possible. There are several approaches including portal vein ligation, perioperative chemotherapy to downsize the lesions for
resectability, and step-up approaches with sequential resections of
bilobar metastasis. Preoperative high-resolution magnetic resonance imaging (MRI) and CT scans are recommended to determine the extent of metastasis [56–58]. Surgical resection of
colorectal liver metastasis (CRLM) is associated with a prolonged
5-year OS (40%) and 10-year OS (25%) [56, 59].
Regarding preoperative imaging of CRLM, MRI is preferable
to a CT scan. A recently published meta- analysis on the detection
rate of CRLM with MRI showed a sensitivity and specicity of
90% and 88%, respectively [60]. For additional detection, intraoperative ultrasound (IOUS) is recommended, especially for
lesions smaller than 10mm in diameter, which are detected much
more frequently using IOUS when compared to CT and MRI [61].
Fluorescence Pattern ofCRLM
To understand the uorescent appearance of CRLM after ICG
injection, the mechanism of ICG metabolism in the liver parenchyma must be explained. ICG is physiologically excreted via the
biliary tract starting several minutes after injection [62]. Due to
this fact, there are different uorescence patterns depending on
the tumor entity. A study published in 2009 by Ishizawa and colleagues investigated the real-time identication of liver cancers
using ICG-FI.A dose of 0.5mg ICG per kg of body weight was
administered between 1 and 7days before surgical resection. A
total of 91 resected hepatic lesions were analyzed and three different uorescence patterns could be identied: a total uorescent
type with a homogeneous hyperuorescence pattern, a partial
uorescent type with inhomogeneous uorescence pattern, and a
rim uorescent type.
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