The Advantages of Using Intraoperative

Indocyanine Green Fluorescence

Angiography for Upper Extremity
Arteriovenous Malformation:
A Case Report
€
Hakan Akbayrak, Omer Faruk Çiçek, Atilla Orhan, and Mustafa B€
uy€
ukateş, Konya, Turkey

Vascular anomaly is a general term that includes all vascular malformations, vascular tumors,
and other congenital vascular defects. Vascular malformation is the most common term, and
it describes blood vessels that are abnormally formed at birth. Vascular malformations can
develop in any part of the body. The most common location is in the lower extremities. Vascular
malformations involve arteries, veins, or lymphatic vessels, or a combination of these. Our pa-
tient was a 22-year-old man with an arteriovenous malformation in his left forearm. He was
admitted due to increased pain and swelling on his left forearm over the previous 9 months.
He had 1 arterial feeder derived from the ulnar artery and 2 venous drainage systems at the
magnetic resonance angiography. We used indocyanine green fluorescence angiography to
assess the arteriovenous malformation during surgery. We found that it was a very useful and
unique technique for assessing the anomalies of the vascular anatomy and eradicating the nidus
of the arteriovenous malformation. It could prove to be very helpful in avoiding significant blood
loss during surgery.

Vascular malformation is the most common term
used to describe blood vessels that are abnormally
formed at birth. More than 70% of congenital
vascular malformations (CVMs) are complex and
rare lesions that affect only 0.8e1% of the popula-
tion. They may present serious hazards in their diag-
nosis and treatment management.1,2 CVMs consist
of arteries, veins, or lymphatic vessels, or a combina-
tion of these.3 CVMs especially in the hand or fore-
arm are some of the most difficult vascular diseases
to treat.4 CVM, which can be categorized according
Presented at the 15th Turkish Society of Cardiovascular Surgery
Congress, Antalya, October 26e29, 2018.
Faculty of Medicine, Department of Cardiovascular Surgery, Selcuk
University, Konya, Turkey.
Correspondence to: Hakan Akbayrak, MD, Faculty of Medicine,
Department of Cardiovascular Surgery, Selcuk University, Konya,
Turkey; E-mail: hakanakbayrak@gmail.com
Ann Vasc Surg 2019; 59: 306.e7–306.e10
https://doi.org/10.1016/j.avsg.2019.02.040
Ó 2019 Elsevier Inc. All rights reserved.
Manuscript received: December 28, 2018; manuscript accepted: February
13, 2019; published online: 7 May 2019
to their hemodynamic status as low-flow or high-
flow lesion, can be usually treated with transcuta-
neous sclerotherapy, transarterial catheter-based
interventions (e.g., embolization), radiation ther-
apy, surgical resection, or a combination of these
treatment modalities.1,3,5 Indocyanine green fluo-
rescence angiography (ICGFA) was approved as an
alternative intraoperative anatomical imaging
modality to conventional procedures. ICCFA allows
the best visualization of blood flow through the
vessels with the injected tri-carbocyanine dye.
Consequently, it helps to show the complete
angioarchitecture of the CVM.6 ICGFA has been
widely used in plastic surgery and neurosurgery
for many years.6e10 ICGFA achieves an intraopera-
tive real-time evaluation of the complete removal
of the nidus. However, we could not find the use
of ICGFA for congenital arteriovenous malforma-
tions (AVMs) located on other body surfaces in
our search of the literature.7,8 We report on the sur-
gical management of the congenital AVM in the
forearm that was operated on while using ICGFA.

306.e7
306.e8 Case reports Annals of Vascular Surgery

CASE REPORT
Patient Information

A 22-year-old man was admitted to our clinic for

increased pain and swelling on his left forearm over the
previous 9 months. He had tenderness on the lesion and
increased pain because of superficial vein thrombosis on
his forearm. He had no earlier intervention and no family
history of genetic disorders.

Clinical Findings

The patient’s symptoms were tenderness on the mass,

increased pain on the distal forearm, enlarged mass effect,
and pulsatility on the mass. The lesions were first assessed
by a physical examination. The physical examination
revealed a 6e7 cm pulsatile mass on his forearm, tender-
ness, and a painful solid mass with palpation. There were
no changing of the bones, no ulceration, and no bleeding
at the lesion site. There were no symptoms of congestive
heart failure such as breathlessness, orthopnea, reduced
exercise tolerance, fatigue, or ankle swelling in our pa-
tient. He had no signs of congestive heart failure such as
tachycardia, tachypnea, hepatomegaly, or peripheral
edema. His ejection fraction (60%) was normal in a trans-
thoracic echocardiography.
Diagnostic Assessment
The lesion on his forearm was evaluated for detailed
anatomical and hemodynamic information with color
flow Doppler ultrasonography (USG) and magnetic reso-
nance angiography (MRA) before surgery. USG was
used to measure the diameter and flow volume of primary
lesions, peak systolic velocities, resistive indexes, and the
diameters of the feeding arteries. According to USG,
thrombosis-like tortuous structures measuring approxi-
mately 6e7 cm were observed under the skin. The throm-
bosed vascular malformation was observed in the middle
part of the flexor face on the ulnar side of the left forearm
with the MRA (Fig. 1). The mass size associated with the
median cubital vein and the basilic vein was approxi-
mately 6.5 cm.
Fig. 1. The preoperative image of MRA.
We excised the AVM as one piece without significant
bleeding with ICGFA screening (Fig. 3). ICGFA was
repeated when the AVM was believed to be totally
resected. There were no complications due to the admin-
istration of the indocyanine green (ICG) dye. The total
blood loss did not amount to more than 100 cc during sur-
gery. The tissue specimen was sent to pathology for
confirmation.
The surgery time was very short for our case (less than
1 hr). It was a very useful technique for screening the
nidus of the AVM. There was no need for a blood transfu-
sion in the perioperative period. There was no need to use
the drainage system for bleeding after the operation. The
patient was discharged on the first postoperative day.
Follow-up and Outcomes
The patient had no complaints at the postoperative 1- and
6-month follow-up. There was no residual lesion at the
postoperative lesion site during the follow-up period.

Therapeutic Intervention DISCUSSION

The patient was operated on under general anesthesia.
ICGFA was used to assess and eradicate the nidus of the
AVM during surgery. All procedures were performed us-
ing an SPY Elite System for laser imaging (LifeCell Corp.,
Branchburg, NJ). ICGFA was injected into the peripheral
vein as a bolus (at a concentration of 25 mg in 5 mL of
saline) and 20 sec later the nidus of the AVM was illumi-
nated by a near-infrared light source. ICGFA was per-
formed in order to identify the feeding arteries and the
draining veins. Following this, the feeding artery (afferent
branch) and the draining veins (efferent branches) were
explored (Fig. 2) at which time the video was recorded.
Vascular anomalies are very rare lesions, and the
most commonly used term for them is CVM.
Vascular anomalies occur in barely 0.8e1% of all
births.1 CVM results from an abnormal vascular
development in which large connecting channels
or shunts between future arteries and veins are
formed during the early developmental stages.2
We can explain the development of the vascular sys-
tem in 3 stages. In the first stage, undifferentiated
cells condense into the capillary blood spaces.
Then there is the formation of a retiform plexus
Volume 59, August 2019
Fig. 2. (A) Intraoperative image from the lesion site
before resection. Big arrow shows feeding artery (afferent
branch) and small arrows show draining veins (efferent
Fig. 3. (A) Intraoperative image after surgical resection. No residual tissue at the lesion site. (B) Intraoperative ICGFA
image after surgical resection. No residual tissue at the lesion site.
from which blood is taken from an artery to a
venous side, which occurs in the second stage. The
development of axial arteries in the extremity
buds occurs in the final stage. Various types of
vascular malformations occur as a result of arrested
development at any point during vascular forma-
tion.3 The different types of CVM include infantile
hemangioma, arteriovenous fistula, congenital
AVM, and venous lesions (venous dysplasia or
cavernous venous malformations).4 CVM can be
also classified according to their hemodynamic sta-
tus, which contains low-flow (venous, lymphatic,
capillary) or high-flow (arteriovenous) lesions.1,5
The most common sites for AVM are the lower
and upper extremities. AVMs of the extremities
have also been categorized according to the angio-
graphic morphology of the nidus. The 4 types of
AVMs based on nidus morphology7 are as follows:
 Type I: arteriovenous fistulae
 Type II: arteriolovenous fistulae
 Type IIIa: arteriolovenulous fistulae with nondi-
lated fistula
 Type IIIb: arteriolovenulous fistulae with dilated
fistula
Case reports 306.e9
branches). (B) Intraoperative image with ICGFA. Big ar-
row shows feeding artery (afferent branch) and small ar-
rows show draining veins (efferent branches).
According to this classification, our patient was
type IIIb AVM. There were multiple shunts present
between the arterioles and the venules that
appeared as a complex vascular network on the
angiography. Type IIIb AVM has a significant
bleeding potential during an operation. Therefore,
we thought that we could use ICGFA to assess the
anomalies of the vascular anatomy and eradicate
the nidus and borders of the AVM. ICGFA could
be helpful in avoiding significant blood loss during
an operation as well.
Most CVMs are asymptomatic or they need to be
observed for minimal symptoms only. CVMs that
are located in the hand and forearm are one of the
most difficult vascular diseases in terms of manage-
ment of the treatment.2,4 The therapeutic modalities
for AVM include endovascular interventions (e.g.,
embolization), a surgical approach, radiation ther-
apy, or a combination of these treatment modalities.
Angiographic interventions are usually employed
for super-selective endovascular embolization
before surgery.3 Although the patients with
high-flow lesions are usually treated with transarte-
rial catheter-based interventions (e.g., emboliza-
tion) and/or surgical resection, the best treatment
306.e10 Case reports
modalities for the low-flow vascular malformations
are transcutaneous sclerotherapy and/or surgical
resection.1,3,5 In this case, we aimed to assess the
usefulness and effectiveness of ICGFA in the surgical
treatment of the AVM on the extremity.
Although MRA and computed tomography angi-
ography provide more precise images preopera-
tively, real-time imaging with these methods is
not possible intraoperatively. ICGFA provides real-
time imaging of the borders, neighborhood, and
feeding artery (afferent branch) and draining veins
(efferent branches) of the lesion. There is no need
for a specific set-up for using ICGFA in the operating
room. Digital subtraction angiography (DSA) can
produce 2-dimensional imaging during surgery;
however, the nidus, the borders, and the neighbor-
hoods of the AVM can be assessed 3-dimensionally
with ICGFA intraoperatively. On the other hand,
the use of ICGFA is safer in patients with impaired
renal functions or borderline renal failure compared
with DSA.
The major limitation of the use of ICGFA is
the lack of access to the device in the operating
room. Although the use of ICGFA is increasing in
specific centers, it is not still used routinely in
many hospitals. Additionally, another limitation is
that the borders of the lesion cannot be precisely
determined by surrounding tissue or intravascular
clots in deep-seated atypical lesions.11
ICG is a stable tri-carbocyanine dye at the room
temperature. ICG is easily soluble in water. ICG
occurs prominently in the arterial phase within
10e20 sec after the venous injection. ICG can bind
very quickly to the plasma proteins, particularly to
the lipoproteins. Consequently, it could be possible
to facilitate repetition in clinical administrations.8
ICGFA has been widely used by plastic surgery and
neurosurgery for many years. ICGFA achieves intra-
operative real-time evaluation of the complete
removal of the nidus of AVM. ICG started to be
used to evaluate cardiovascular and liver functions
from the middle of the 1950s. ICG can bind almost
completely to globulin; hence, ICG remains at
the intravascular site under normal vascular perme-
ability. The plasma half-life of ICG is about 3e4 min.
ICG is completely excreted by liver without being
metabolized.9
In recent studies, the technique of fluorescence
video angiography for visualizing vascular struc-
tures has become a safe and effective alternative to
DSA.8 The usefulness and the effective role of
ICGFA in different surgeries have been shown in
the recent studies.6e10
Annals of Vascular Surgery
CONCLUSIONS
We aimed to assess the usefulness of ICGFA in the
surgical treatment of AVM on an extremity. As we
thought, the intraoperative use of the ICGFA was
very helpful in assessing the nidus of the AVM on
an extremity. At the same time, it was also very
beneficial in avoiding significant blood loss.
Although the lesion site in this patient was in an
easily accessible area, ICGFA use has made it
much easier to screen the nidus of the AVM. In pe-
ripheral AVM cases in which it is much more diffi-
cult to reach the AVM nidus, we think that the
intraoperative use of ICGFA will make the AVM
resection operation easier for surgeons. According
to our limited experience, ICGFA can be used in
selected peripheral AVMs; however, the need for
the routine use of ICGFA in these cases should be
investigated in further studies.
REFERENCES
1. Lidsky ME, Markovic JN, Miller MJ Jr, et al. Analysis of the
treatment of congenital vascular malformations using a
multidisciplinary approach. J Vasc Surg 2012;56:1355e62.
2. Toker ME, Eren E, Akbayrak H, et al. Combined approach to
a peripheral congenital arteriovenous malformation: surgery
and embolization. Heart Vessels 2006;21:127e30.
3. Parida S, Gupta S, Chandran BV. Are congenital arteriove-
nous malformations of proximal upper extremity, more on
the right: case report and literature review. Int J Angiol
2016;25:e29e31.
4. Sofocleous CT, Rosen RJ, Raskin K, et al. Congenital
vascular malformations in the hand and forearm. J Endovasc
Ther 2001;8:484e94.
5. Ek ET, Suh N, Carlson MG. Vascular anomalies of the hand
and wrist. J Am Acad Orthop Surg 2014;22:352e60.
6. Bretonnier M, Henaux PL, Morandi X, et al. Fluorescein-
guided resection of brain arteriovenous malformations: a
short series. J Clin Neurosci 2018;52:37e40.
7. Cho SK, Do YS, Shin SW, et al. Arteriovenous malforma-
tions of the body and extremities: analysis of therapeutic
outcomes and approaches according to a modified angio-
graphic classification. J Endovasc Ther 2006;13:527e38.
8. Bilbao CJ, Bhalla T, Dalal S, et al. Comparison of indocya-
nine green fluorescent angiography to digital subtraction
angiography in brain arteriovenous malformation surgery.
Acta Neurochir (Wien) 2015;157:351e9.
9. Taddei G, Tommasi CD, Ricci A, et al. Arteriovenous malfor-
mations and intraoperative indocyanine green videoangiog-
raphy: preliminary experience. Neurol India 2011;59:
97e100.
10. Burnier P, Niddam J, Bosc R, et al. Indocyanine green appli-
cations in plastic surgery: a review of the literature. J Plast
Reconstr Aesthet Surg 2017;70:814e27.
11. Ng YP, King NK, Wan KR, et al. Uses and limitations of
indocyanine green videoangiography for flow analysis in
arteriovenous malformation surgery. J Clin Neurosci
2013;20:224e32.