Successful Management of Unilateral Direct Carotid Cavernous Fistula With Bilateral

Ocular Manifestation

Danty Indriastuty1,4, Suliati Amir1,2,4, Halimah Pagarra1,2,4, Andi Pratiwi1,2,4, Ashari Bahar3,4
1
Department of Ophthalmology, Hasanuddin University, Makassar, Indonesia
2
Department of Oculoplastic, Reconstruction, and Ophthalmic Oncology, Hasanuddin University, Makassar, Indonesia
3
Department of Neurology, Hasanuddin University, Makassar, Indonesia
4
Wahidin Sudirohusodo Hospital, Makassar, Indonesia

ABSTRACT

Introduction:

Carotid cavernous malformations (CCM) categorized into four types, with type A featuring
direct connections between internal carotid artery (ICA) and cavernous sinus (CS). Direct and
indirect fistulas have different origins, with the latter arising from meningeal arteries of the
external and/or ICA. Direct connections have high blood flow through the ICA wall and are
caused by trauma in 75% of cases. Other causes include rupture of a cavernous ICA aneurysm,
arterial dissection, connective tissue disorders, iatrogenic factors, and fibromuscular dysplasia.
We present a case of a patient with a traumatic unilateral direct CCM and bilateral ocular
symptoms.

Case Illustration:

A 20-year-old male was complained about dropping of both eyelids since 14 days prior along
with gradual decrease of visual acuity in both eyes. He had a history of traffic accident 2 months
before and undergone mandibular open reduction and internal fixation (ORIF). Best corrected
visual acuity (BCVA) was 20/60 and 3/60 on the right and left eye respectively with normal
intraocular pressure (IOP). The ophthalmologic examination showed conjunctival chemosis on
both eyes and proptosis on the right eye, followed by the left eye six day later. Afferent pupillary
defect was found during swinging light test and ocular movement in both eyes was restricted in
all directions. Funduscopy examination revealed normal posterior segment. The treatment was
delayed due to positive Covid-19 test result which may lead to the contralateral CF involvement
through the intercavernous sinus connection. Digital subtraction angiography (DSA) was
performed later and showed right internal carotid artery (RICA) segment C4 that has ruptured
and formed a fistula towards the right sinus cavernous. Embolization with Goldball balloon was
conducted by neuro-interventionist, and the patient showed resolution after the embolization
procedure was performed.

Conclusion:
 Endovascular management showed a good result for ocular manifestation including functional
and cosmetic appearance. Despite the prolong time from diagnosis to treatment.

Keyword: Carotid cavernous fistula, direct carotid cavernous fistula, embolization.

Introduction injuries, and iatrogenic injuries. CCFs are

30% spontaneous, as a result of vascular
The cavernous sinus CS term first
traumas such as aneurysm rupture or genetic
described by James Winslow in 1734. Later
predispositions and females are the most
in 1835, Baron reported a case of pulsating
affected by them in older ages. Additionally,
exophthalmos and discovered abnormal
in patients with connective tissue disease,
connection of internal carotid artery (ICA)
spontaneous fistulas may form as a result of
and cavernous sinus during the autopsy.
ruptures of artery wall with structural
Carotid cavernous fistulas (CCF) are
weakness.2,5
vascular shunts allowing blood to flow from
the carotid artery into the cavernous sinus.1 Venous and arterial blood conflux will
progress into ophthalmic manifestation due
CCF categorized as direct (Type A) and
to increased venous tension. Majority of
indirect (Type B, C, and D) according to the
CCFs are not life-threatening, but prompt
dural shunt. Direct connection are 75%
treatment to avoid irreversible damage to the
traumatic and have a high flow through the
afflicted eye is needed. Complications
internal carotid artery wall. Direct CCFs, in
includes intracerebral hemorrhage,
contrast to indirect CCFs (types B, C, and
subarachnoid hemorrhage, epistaxis, vision
D), are less likely to resolve on their own
loss, and cranial nerve palsies.3,5
and typically require therapy in symptomatic
individuals. The rate of spontaneous closure The gold-standard imaging modality for
of direct CCFs was estimated to be between CCF is cerebral angiography. CT or MRI
1.2 and 4% in several large series. The exact shows proptosis, cavernous sinus
mechanism of these rare events remains a enlargement, extraocular muscle (EOM)
controversial topic.2,3,4 enlargement, superior ophthalmic vein
dilation, or dilation of cortical or
The most frequent cause of direct CCF are
leptomeningeal vessels, as well as associated
basilar skull fractures, projectile or slash
skull fractures, which can be suggestive of
CCF.1

Case

A 20-year-old male complained about

protruding of both eyes since 2 weeks
before.

Symptoms accompanied by decreased

visual acuity and ptosis. The symptoms
started in the left eye and followed the right
Figure 1. Examination on both eyes on June 29rd 2022
eye six days later. There was a history of
traffic accident 2 months before, and the During initial ophthalmologic
patient underwent mandibular open examination on March 11, 2022, the visual
reduction and internal fixation the next acuity was 20/80 and 5/60 on the right and
month. There is no history of vision of left eye respectively. Intra ocular pressure
floaters or flashes of light, nor of diabetes (IOP) was normal for both eye. The eyelid
mellitus, trauma, eye surgery, or prescription was swollen and ptotic on both eyes. The
glasses. conjunctiva was hyperemia, with chemosis
mostly in the inferior area. Afferent
pupillary defect was found during swinging
light test and ocular movement in both eyes
was restricted in all directions.
Confrontation test gave an impression of
narrowed vision in superior and inferior
directions on both eye. Funduscopy
examination revealed normal posterior
segment.

Figure 2. Cerebral arteries arteriography (red arrow).
Cerebral arteries arteriography on March
st
31 2022 showed direct fistula arise from
left internal carotid artery (LICA) C4
segment through the left cavernous sinus.
There was reflux and dilation of superior
ophthalmic vein (SOV), inferior ophthalmic
vein, and intercavernous sinus. Collateral
flow through left anterior cerebral artery
(ACA) and medial cerebral artery through
anterior communicans artery (AcomA) was
also found. Patient was diagnosed with
direct carotid cavernous fistula after DSA
conducted.
Figure 3. GoldBalloon detachable balloon. A type of
embolization to close a carotid cavernous fistula.
Since Serbinenko first introduced
detachable balloons in 1974, this
endovascular approach has long been
preferred in the treatment of CCF before
being modified by new technologies such as
coils and stents. A removable balloon covers
the fistula while maintaining patency of the
ICA.11,12 This method is inflexible, so it
depends on the structure of the ICA. In
addition, there are a few things to consider
before choosing this treatment method for
CCF: 1) the diameter of the fistula is about
the same as an inflated balloon, but large
enough to use an empty or partially inflated
balloon; 2) The volume of blood through the
fistula is sufficient to reach the basket; and
3) the CS is large enough to accommodate
the balloon for complete occlusion of the
fistula. Technical failure to place the stent
across the fistula opening results in an end
leak, resulting in fistula retention. Another
disadvantage that some studies have
reported is the complexity of this technique;
because it can block the vena cava and cause
cranial paralysis. This is usually resolved by
inserting a larger balloon and re-expanding
the stent. 11,13,14

Embolization with Goldbal balloon

(Figure 3) was performed at LICA segment
C4 up to the SAC of the aneurysm and the
fistula are closed. Patient tolerated entire
procedure, there was no new neurologic
Figure 4. Cerebral arteries arteriography post balloon
deficit, the sheath was removed (Figure 4). embolization. The marker of Goldbal balloon (red arrow).

Post embolization follow up found

improvement in both eyes. Ocular symptoms
diminished and the visual acuity in both eyes
were 20/25 on the ninth day. The ocular
movement was also improved in both eyes
but there was still restriction to the lateral
sides indicating residual sixth cranial nerve
palsy.
Discussion
Patients with unilateral fistulas rarely
present with bilateral symptoms. Despite
communication between cavernous sinus
through the intercavernous sinus, anterior
and posterior to the pituitary gland’s
infundibulum, the ophthalmic veins act as an
ipsilateral major decompressive route.
Tomsick et a1 reported 89% of Type A
CCFs had drainage into the SOV, 83% into
the IPS, and 49% into the sphenoparietal
sinus as well as pial drainage into the
posterior fossa (27%) and middle cerebral
veins (32%).6,7

Figure 5. Examination on both eyes after embolization
using Goldbal balloon
There are four interconnection within both
cavernous sinus. The widest connection in
most of the cases is with the basilar plexus,
present in 100% of the cases. Other
communications vary in size; the anterior
and posterior inter-CS are always present,
whereas inferior inter-CS sinus is present in
97% of the cases. Contralateral sinus
involvement might result from
communication between cavernous sinus or
atypical arterial wall defect that lead the
inflow directly to the intercavernous sinus.
Most direct CCFs will present with a
combination of chemosis (90%), proptosis
(90%), diplopia (50%), pain (25%), bruit
(25%) increased ocular pressure, visual loss,
and dysfunction of the trigeminal nerve (up
to 50%).8
In this patient, there was a significant
disturbance of eye movement on both eyes,
therefore it can be concluded that there was
compression around the neural structures.
Cranial nerves III, IV, VI, V 1, and
sympathetic/parasympathetic connections
are present in the CS. CN III (oculomotor)
courses in the CS lateral wall along the
inferolateral surface of the anterior clinoid
process and enters the superior orbital
fissure through the annulus of Zinn. CN IV
(trochlear) enters the CS lateral wall
posterolateral to CN III and crosses CN III
proximal to entering the superior orbital
fissure (and enters the orbit outside the
annulus of Zinn).6
Recent meta-analysis and systematic
review found that the most prevalent
symptom of CCF was exophthalmos (89%)
wide followed by chemosis, proptosis, bruits,
diplopia, cranial nerve palsy, visual decline,
tinnitus, elevated intraocular pressure,
1
orbital and periorbital pain, and headache
respectively. Drainage of the anterior part of
the orbit gives rise to congestion of the
orbital vein and subsequent fluids
transudation, the elevation of intraocular
pressure, laceration of dilated veins, and
impairment in perfusion of the retina.
Proptosis results from elevated orbital
pressure, diplopia from paralysis of cranial
nerves, a visual decline from ischemia in the
retina or optic nerve, pain from aqueous
return decline, and elevation in intraocular
pressure.8 As we observed in the patient
there was chemosis, ptosis, diplopia, and
decreased visual acuity, but the intraocular
pressure was still normal.
The gold-standard imaging modality is
cerebral angiography. CT or MRI shows
proptosis, cavernous sinus enlargement,
extraocular muscle (EOM) enlargement,
superior ophthalmic vein dilation, or dilation
of cortical or leptomeningeal vessels, as well
as associated skull fractures, which can be
suggestive of CCF. A dilated superior
ophthalmic vein is often the initial finding
on imaging, which can be found in 86%–
100% cases on contrast-enhanced CT and in
75%–100% on T1W or post-contrast MRI.
Moreover, CT allows easier identification of
fractures and complications such as
haemorrhage, whereas MRI allows detecting
References
1. Demartini Z Jr, Liebert F, Gatto LA, et al. Unilateral
Direct Carotid Cavernous Fistula Causing Bilateral
Ocular Manifestation. Case Rep Ophthalmol.
abnormal flow voids within the cavernous
sinus (CS).5 We had performed CT and
cerebral angiography on this patient, which
revealed type A CCF.
Direct CCFs definitive treatment remains
endovascular intervention ligation to close
the fistula and preserving the ICA. This
includes embolization with particles
(polyvinyl alcohol particles or n-BCA
n-Butyl cyano-acrylate mixed with lipiodol),
glue, detachable balloons and thrombogenic
micro coils, best of which is the detachable
balloon through an end arterial route.5 In this
case, embolization was performed using
GoldBal balloon.
Early suspection, diagnosis, and prompt
treatment for carotid cavernous fistula will
result in better outcome, whereas in this
patient, the treatment was delayed due to
positive Covid-19 test result which may lead
to the contralateral CF involvement through
the intercavernous sinus connection.
Delayed endovascular intervention was also
reported to increase the complexity of the
procedure and resulted in poorer outcome.9
2015;6(3):482-487. Published 2015 Dec 24.
doi:10.1159/000443141
2. Henderson AD, Miller NR. Carotid-cavernous fistula:
current concepts in aetiology, investigation, and
management. Eye. 2018 Feb 3;32(2):164–72.
3. Iampreechakul P, Tirakotai W, Tanpun A. outcomes of carotid cavernous fistula in Makassar,
Spontaneous resolution of direct carotid-cavernous Indonesia: a single-centre experience. Egypt J Neurol
fistulas: case series and literature review. Psychiatry Neurosurg 59, 29 (2023).
Interventional Neuroradiology. 2019 Feb 23;25(1):71– https://doi.org/10.1186/s41983-023-00630-w
89.
4. Calafiore S, Perdicchi A, Scuderi G, Contestabile MT. 10. Debrun GM: Treatment of traumatic carotid-cavernous
Glaucoma Management in Carotid Cavernous Fistula. fistula using detachable balloon catheters. AJNR Am J
Case Rep Ophthalmol. 2016 Jun 2;7(2):296–302. Neuroradiol 1983;4:355–356.
5. Das D, Bajaj MS, Modaboyina S, Singh P, Gupta S, 11. Halbach VV, Higashida RT, Hieshima GB, Hardin C
Agrawal S. Carotico-cavernous fistula - From the eye W, Pribram H. Transvenous embolization of dural
of an ophthalmologist. TNOA J Ophthalmic Sci Res fistulas involving the cavernous sinus. AJNR Am J
2022;60:30-7 Neuroradiol. 1989;10(2):377–383.2494857 [Web of
6. Tytle, T. L., & Punukollu, P. K. (2001). Carotid Science ®], [Google Scholar]
cavernous fistula. Seminars in Cerebrovascular 12. Wolpert SMIR. In re: Serbinenko FA. Balloon
Diseases and Stroke, 1(1), 83–111. catheterization and occlusion of major cerebral
doi:10.1053/scds.2001.24080 vessels. J Neurosurg 1974;41:1974. AJNR Am J
7. Ernst RJ, Tomsick TA: Classification and Neuroradiol. 2000;21(7):1359–1360.10954296 [Web
Angiography of Carotid Cavernous Fistulas, in of Science ®], [Google Scholar]
Tomsick TA (ed): Carotid Cavernous Fistula. 13. Li J, Lan Z-G, Xie X-D, et al. Traumatic carotid-
Cincinnati, OH, Digital Educa- tion,1997, pp 13-22 cavernous fistulas treated with covered stents:
8. Rahmatian A, Yaghoobpoor S, Tavasol A, Aghazadeh- experience of 12 cases. World
Habashi K, Hasanabadi Z, Bidares M, Safari-kish B, Neurosurg. 2010;73(5):514–519.
Starke RM, Luther EM, Hajiesmaeili M, Sodeifian F, doi:10.1016/j.wneu.2010.02.06220920935 [Crossref],
Fazel T, Dehghani M, Ramezan R, Zangi M, Deravi N, [Web of Science ®], [Google Scholar]
Goharani R, Fathi M, Clinical efficacy of endovascular 14. Wang C, Xie X, You C, et al. Placement of covered
treatment approach in patients with carotid cavernous stents for the treatment of direct carotid cavernous
fistula: A systematic review and meta-analysis, World fistulas. AJNR Am J Neuroradiol. 2009;30(7):1342–
Neurosurgery: X (2023).. 1346.
9. Bahar, A., Pranata, J., Gunawan, A. et al. Clinical doi:10.3174/ajnr.A158319342540 [Crossref], [Web of
characteristics, angiographic findings and treatment Science ®], [Google Scholar]