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12 Use ofFluorescence Guidance inPediatric Surgery
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351
the time of ureteral reconstruction by allowing the identication
of diseased areas of the ureter, which would be marked by signicant devascularization [27].
Our own protocol at the Children’s Hospital of Pittsburgh
includes that the patient is placed in the lithotomy position. A
pediatric urologist or surgeon performs cystoscopy and places a 5
Fr open-tip ureteral catheter under uoroscopy guidance. The tip
is placed before or at the level of the renal pelvis. ICG is injected
(2.5 mg/mL; 2 mL per ureter) and catheter clamped for the
duration of the operation. Fluorescence-guided detection of the
ureter using ICG is safe and ready for use and there is no systemic
exposure. The disadvantage is that a ureteral catheter needs to be
placed at the start of the procedure. ICG allows to “ip the switch
to see the ureter” at any time during the procedure (Fig.12.5).
Fig. 12.5 A 6-year-old girl with large left retroperitoneal mass displacing
the ureter. A ureteral catheter was placed and ICG injected. The ureter could
be easily identied during the laparoscopic removal of the mass and spared
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S. Scholz et al.
Partial Nephrectomies
A wide array of literature is published regarding the benets of
using FGS in pediatric and adult partial nephrectomies. ICG is
often considered a valuable tool when challenging vascular anatomy is encountered. Diana et al. performed a sizeable multiinstitutional study evaluating robot-assisted partial nephrectomies
in adults after administering ICG, allowing for the evaluation of
kidney perfusion intraoperatively. Their group evaluated 318
patients between 2010 and 2016 (with a median age of 61). This
group performed partial nephrectomies for tumors with an average size of 30mm, administering 2–4mL of 2.5mg/mL solution
of ICG before or after renal artery clamping. They noted that the
peak uorescence occurred 2min after injection. They performed
a logistic regression analysis and found that ICG use independently predicted achieving the trifecta (warm ischemia time
<25min, no positive surgical margins, and absence of ClavienDindo > two complications) [28].
Similar success has been seen extensively in the realm of pediatric surgery. Because ICG allows for faster identication of intraoperative landmarks, it facilitates accurate dissection and
resection, resulting in shorter operating times. Over four years,
Esposito etal. performed a laparoscopic partial nephrectomy on
22 patients with a median age of 3.9years for a nonfunctioning
moiety of a duplex kidney. They prepared ICG to a concentration
of 2.5mg/mL and administered it via peripheral IV to identify the
vasculature or ureteral catheter to delineate the ureter. Structures
of interest became apparent within 30–60s of the ICG injection.
They administered the ICG in three phases: rst, to identify ureter
pre-op; second, to identify the vasculature; and lastly, to identify
the avascular kidney after ligation. Overall, they found that ICG
near-infrared laparoscopic partial nephrectomy led to shorter
operative times [29]. In the same way, a separate group has used
ICG to evaluate the vascular anatomy intraoperatively during a
robot-assisted laparoscopic heminephrectomy. Herz etal. evaluated and operated on six patients with a median age of 4.75, diagnosed with an obstructed duplex ectopic ureter, duplex ureterocele,
or duplex kidney. Interestingly, in certain patients, they found that
12 Use ofFluorescence Guidance inPediatric Surgery
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segmental arterial mapping was more informative than a preoperative 3D CTA. Importantly, they noted avoidance of a critical
complication by applying this system. They administered
0.5–1mL of ICG (concentration of 2.5mg/mL) and then waited
30–60 s, and then they activated the near-infrared uorescence
system [30]. Abdelhafeez etal. used ICG (administering a dose of
1.5mg/kg the day before surgery) in eight pediatric patients with
a median age of three years (seven had Wilms tumor and one had
epithelioid angiomyolipoma). They routinely found that the normal kidney had higher uptake (uorescence) compared to the kidney tumor, making the differentiation of renal tumor from normal
kidney both easier and safer [31].
ICG allows for safer surgery because it allows for clear visualization of the ureter, clearly displays the blood supply, and demarcates the tissues of interest, more precisely identifying the area of
excision. Furthermore, ICG allows for identifying abnormal vascular anatomy and permits early detection of iatrogenic injury.
Interestingly, despite making surgery faster and safer, Esposito
etal. found FGS resulted in a comparable length of stay, analgesia, and time to initiating feeding [29].
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Varicocele
A common intervention that employs the use of FGS is varicocele repair. Esposito et al. evaluated lymphography with ICG
(1mg of ICG injected directly into the left testicle with the uorescence of the lymphatics becoming apparent after 20–30 s).
They evaluated 25 patients with an average age of 13.7, whom all
had symptomatic high-degree varicoceles associated with testicular hypotrophy [32]. In a separate cohort, the same group performed a Palomo varicocelectomy in 30 boys with an average
age of 16.7. Again, the lymphatic vessels demonstrated uorescence and were accordingly spared [33]. In both cohorts, there
was no conversion to open surgery, and at the time of follow-up,
there was neither recurrence of the varicocele nor evidence of a
postoperative hydrocele. They also evaluated their postoperative
complications using ICG compared to isosulfan blue based on
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their previously published data, and they found that complications were lower in the ICG group. However, they were not statistically signicant [34].
S. Scholz et al.
Cyst Deroong
Comparably, there is great utility to using ICG in renal cyst
deroong. Fluorescence highlights the normal renal parenchyma
within seconds, while the avascular cyst remains nonuorescent.
Because of excellent visualization, signicant bleeding or damage
was prevented, especially to the renal parenchyma [35].
Furthermore, the postoperative complication rate was lower and
statistically different when evaluating renal cyst deroong with
ICG to no ICG [34].
Pediatric Thoracic Surgery Clinical Applications
ICG is also a valuable tool when performing thoracic surgery,
allowing for the performance of a segmentectomy or wedge resection over a lobectomy or a more extensive resection. Sekine etal.
evaluated the utilization of ICG for thoracoscopic segmentectomy
in ten patients with a mean age of 72.8 with early lung cancer. To
isolate pulmonary segments, ICG was injected directly into the
implicated bronchioles. The target segments of the lung were then
identied using the ICG uorescence, obviating the intersegmental lines and planes. This is especially valuable in patients with
emphysema, who may have anatomy with distorted segmental
planes because of emphysematous changes. The segments were
removed with either a stapler or electric cautery. They report that
ICG did not shorten OR time or result in decreased blood loss
[36]. Another group has also used ICG to evaluate the feasibility
of using FGS to treat lung cancer. Tarumi etal. performed VATS
segmentectomy with ICG to identify segmental ssures for lung
cancer. However, unlike the previous group who had administered
ICG directly into the bronchi, Tarumi etal. administered a dose of
3mg/kg of ICG via peripheral IV after ligating the dominant pul-
12 Use ofFluorescence Guidance inPediatric Surgery
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monary arteries. They noted uorescence within minutes and
marked the visceral pleura with electrocautery. This allowed them
to maintain an excellent surgical view and identify the intersegmental line without re-inating the lung [37].
FGS may hold a signicant benet in treating congenital pulmonary lesions. Shirota et al. evaluated and treated a group of
pediatric patients with lung cysts. The authors used a thoracoscopic approach to treat congenital lung cysts, employing ICG
(administering one to ve IV 0.01 to 0.02mg/kg injections) to
perform a segmentectomy or partial lung resection instead of a
traditional lobectomy [38]. The ICG allowed them to visualize
blood ow easily. This would be a valuable tool for treating small
lesions across multiple lobes.
Another group applied FGS in the setting of a thoracoscopic
lobectomy to treat two patients with a mean age of 15.5months,
one with a congenital cystic adenomatoid malformation and the
other with pulmonary extra-lobar sequestration. ICG (0.25mg/
mL/kg IV intraoperatively) was used to identify a plane between
the cystic malformation and normal long parenchyma to elucidate the resection margins [12]. The same group also applied the
utility of FGS in the setting of a thoracoscopic lymph node
biopsy. Specically, this was used in one six-year-old boy suspected of lymphoma with a noted malignant 2cm hilar lymph
node. ICG (0.5 mg/mL/kg intraparenchymal lung injection)
facilitated identication and subsequent removal of the pathological lymph node [12].
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Lung Metastasis
In the realm of pediatric surgery, hepatoblastoma frequently
metastasizes to the lungs. Cho etal. evaluated 22 cases of hepatoblastoma; six of these patients had lung metastasis at the time of
surgery, and two of these patients underwent thoracic surgery
using ICG.ICG allowed for easy identication of the pulmonary
lesions, given the lack of ICG uptake in normal lung tissue [21].
Yamamichi etal. evaluated a smaller cohort of three patients with
hepatoblastoma: one with a primary tumor, another with a recur-
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rent tumor, and a third with a metastatic lesion to the lung. All
patients were evaluated with ICG (administered 0.5 mg/kg IV
three to four days before the operation). In the patient with lung
metastases, they were able to identify multiple metastatic lesions
by positive uorescence, and all were completely resected. These
uorescence-positive lesions were found to be consistent with
hepatoblastoma tumor cells. They were able to resect a total of 24
nodules. Unfortunately, the patient subsequently developed recurrent lung metastases two months later and died of recurrent tumors
[17]. Yoshida etal. used ICG (0.5mg/kg the day prior to surgery)
for lung metastasectomy of hepatoblastoma. In 16 patients (age
range between 4months and 11years), they performed 61 ICGassisted pulmonary metastasectomies (obtaining a total of 373
specimens). With ICG, their sensitivity was 92.6%, specicity
2.9%, PPV 71.4%, and NPV 13%. They noted they had 100 ICGpositive specimens histologically negative for tumor, noting
changes consistent with regression of a metastatic tumor and nonspecic changes of brosis and hemorrhage, representing ICG
labeling of pulmonary tissue with abnormal blood ow [39].
S. Scholz et al.
Chylothorax
ICG can also be a valuable tool for evaluating the lymphatic system. Thus, it may have additional value in evaluating patients with
chylothoraces. Shibasaki etal. used ICG lymphography to evaluate lymphatic dysfunction in patients with congenital chylothoraces, evaluating ten neonates with a median age of 29.5days after
birth and median gestation age of 35.5weeks. They administered
subcutaneous ICG (0.25mg in the second interdigit regions of the
hands and the rst interdigit space of the feet). They then evaluated the trunk and extremities using an infrared camera. This
allowed them to determine normal lymphatic ow from abnormal
or pathological lymphatic ow, grading the lymphatic dysplasia
as mild, moderate, severe, or lymphatic hypoplasia. Images and
videos were obtained immediately, 3–6h after, and 24h after ICG
[40]. Another group shared their experience using ICG to evaluate
a six-month-old patient with Noonan syndrome. They used ICG
12 Use ofFluorescence Guidance inPediatric Surgery
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to evaluate lymphatic ow after the patient developed bilateral
chylothoraces after cardiac surgery. They administered 0.05mL
intradermally of 0.25mg/mL of ICG to each dorsal foot, waited
1 h, administered a dose to each hand, and waited for 20 min.
They noted diffuse uptake into the lymphatics of bilateral lower
extremity lymphatics and inguinal lymph nodes. However, no
meaningful uorescence was appreciated in the upper extremities.
They believe the impaired visualization of abnormal drainage pattern may have been secondary to the known lymphatic aberrations
in patients with Noonan syndrome. More specically, they believe
they could not use this system to determine the site of leakage in
the thoracic duct because of congenital lymphatic abnormalities
or high cardiovascular pressures [41]. However, ICG may still
hold value in evaluating patients with normal lymphatic anatomy
or those patients with localized aberrant lymphatic anatomy.
Chylothoraces may occur not only after cardiac surgery but
also after pediatric thoracic surgery. Postoperative chylothorax
after esophageal atresia/tracheoesophageal stula surgical repair
is a severe complication. Another group used ICG and nearinfrared uorescence imaging to identify and ligate sites of chylous leakage. They performed ICG-NIR in ten patients (seven
patients had their thoracic duct evaluated at the initial operation,
and three patients were taken back to OR after conservative management failed to treat chylothorax) after awaiting 1h after intertoe ICG injection (0.025 mg of ICG). Using this system, they
were able to identify the thoracic duct or the site of lymphatic
leakage in each patient, and they appropriately sutured or ligated
the area of concern [42]. Overall, despite the potential benets,
given the small numbers in pediatric cases, it is difcult to strongly
recommend FGS for thoracic surgery at present. Additional ongoing research may change this in the future.
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Pediatric Liver Transplant Surgery
Hepatic necrosis is a feared complication of liver transplant surgery. However, hepatic necrosis may also result in patients undergoing surgery for gastric adenocarcinoma. Lee, J.H., et al.
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S. Scholz et al.
identied 31 patients with aberrant left hepatic arteries undergoing resection for gastric adenocarcinoma. The aberrant artery was
identied in 19% preoperatively; the remainder of cases were
found intraoperatively. They were able to appropriately preserve
the aberrant left hepatic artery in cases where there was inadequate ow based on the uorescence, thus preventing hepatic
necrosis [43].
As discussed elsewhere, ICG cholangiography is a valuable
tool when performing hepatobiliary surgery. Mizuno, S., et al.
evaluated 108 patients who underwent a living donor liver transplantation. They reported that only 18 of the 108 underwent ICG
cholangiography (0.025mg/mL directly into the bile duct through
a transcystic tube), and bile leakage occurred in 5.6% of the recipients, strictures occurred in 13.9% of the recipients, and 2.7% of
the donors developed a biliary leak. However, the 18 that underwent ICG cholangiography did not develop any biliary complications in donors or recipients [44].
Quintero, J., etal. evaluated the use of ICG in the setting of
liver failure. Pediatric acute liver failure is uncommon but results
in death or the need for a liver transplant in 25–50% of cases.
Indocyanine green plasma disappearance rate (ICG-PDR) may be
used to predict the degree of liver damage. ICG-PDR was obtained
upon admission when ALF was diagnosed, and it was repeated
every 24h until ALF resolution, liver transplant, or death. A lower
ICG-PDR score translated to signicant irreversible liver damage.
The sensitivity was 92.3% and specicity was 97.1%, which are
higher than King’s College and Clichy’s criteria. Additionally,
PPV was 92.3%, and NPV was 97% [45].
In liver transplantation, patency of the hepatic artery, portal
vein, and bile duct is important. Panaro, F., etal. used ICG uorescence to evaluate the degree of perfusion in six liver transplantation procedures. Specically, they aimed to evaluate the graft
bile duct perfusion to determine the most appropriate area of duct
transection prior to creating the anastomosis. They intravenously
administered ICG (0.5mg/kg) after liver transplant and revascularizing the organ. In 47s, they were able to identify and differentiate the vascularized portion from the non-vascularized portion
12 Use ofFluorescence Guidance inPediatric Surgery
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of the graft bile duct, which allowed them to determine where to
transect the duct and create the appropriate anastomosis. They
noted anomalies in two of their six patients regarding the vascularization of the bile duct, requiring them to resect the bile duct.
By 12-month follow-up, none of the patients had any biliary
complications [46]. Portal vein thrombosis is another severe complication that may lead to graft failure. Portal vein thrombosis is a
severe complication after liver transplantation. Kawaguchi, Y.,
etal. report the case of a 60-year-old female who underwent a living donor liver transplant and immediately underwent ICG
(0.93mg) uorescence imaging, which demonstrated inadequate
perfusion of segment 4. Subsequent ultrasound demonstrated a
thrombus in the portal vein of segment 4, which they were able to
be removed successfully [47].
Thus, ICG has a broad range of uses in the setting of liver
transplant in addition to the evaluation of hepatic artery, portal
vein, and bile ducts intraoperatively. ICG may be used for preoperative evaluation of potential surgical candidates as a dynamic
study as opposed to other scoring systems as well as for the preoperative evaluation of graft, allowing surgeons to exclude grafts
that may be high risk or ineffective. Intraoperatively, it may play
an additional role in liver mapping, cholangiography, tumor visualization, and partial liver graft evaluation. Additionally, it may
allow for early identication of thrombosis, kinking, or changes
in ow that would potentially prevent serious complications.
Postoperatively, it may help predict early morbidity and mortality
and it may also be used to assess graft function and regeneration
[48, 49].
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Pediatric Surgical Oncology Applications
Fluorescence-guided surgery has been used with increasing frequency for various applications in pediatric surgical oncology.
ICG uorescence can facilitate tumor identication, oncologic
resection, margin delineation, and metastasectomy. Furthermore,
as ICG has been documented to detect lesions as small as
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0.062mm, ICG uorescence may allow for detection of lesions
that might otherwise have been missed by preoperative imaging
or intraoperative inspection or palpation [50].
S. Scholz et al.
Primary Hepatic Tumor Resection
One of the more established applications of ICG uorescence in
pediatric surgical oncology is resection of primary hepatic tumors
in children specically hepatoblastoma and hepatocellular carcinoma [22, 51, 52].
Intravenous injection of ICG 0.5mg/kg is recommended 72 to
96h prior to hepatic tumor resection [51, 53]. Hepatic tumors are
more cholestatic and have a decreased ability to excrete ICG relative to normal liver parenchyma. This 72- to 96-h delay allows for
optimal visualization of the hepatic tumor with decreased background noise [18]. However, if patients are unable to receive their
ICG injection that far in advance, a lower dose of ICG can be
administered closer to the time of their operation (e.g., 0.2–
0.3mg/kg of ICG 24–48h before surgery), although there may
still be a poor signal-to-noise ratio even with the lower dosing
[22]. Similarly, patients with underlying liver disease, including
liver cirrhosis as seen in biliary atresia, may retain ICG longer,
contributing to increased background noise if ICG is administered
too soon before an operation [54].
There are multiple reports documenting the successful use of
ICG for resection of hepatoblastoma. ICG demonstrates excellent
sensitivity for detecting hepatoblastoma tumors, particularly
masses within 10mm of the liver surface [19, 20]. In a case series
of 11 patients undergoing hepatic resection with ICG guidance,
ICG was 100% sensitive in identifying malignant lesions with
high sensitivity across various histologic types (fetal hepatoblastoma, 100%; embryonal hepatoblastoma, 100%; mixed fetalembryonal hepatoblastoma, 83%). However, specicity was low:
seven of 16 lesions were ICG positive despite not demonstrating
viable tumor on surgical pathology [6]. In addition, ICG may
identify remote satellite lesions within the liver that may be too
small for detection on preoperative cross-sectional imaging or
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