A 54-year-old male with a past medical history of polysubstance abuse and a gunshot wound (GSW) to the left eye presented with sudden altered mentation and right-sided hemiparesis. Computed tomography (CT) imaging revealed a large left frontal lobe ICH with intraventricular hemorrhage (IVH). There were no reported ocular symptoms. Visual examination was significant for left eye enucleation, an intact pupillary light reflex and extraocular movements in the right eye. Visual acuity could not be assessed secondary to agitation. There was no evidence of exophthalmos in the right eye nor was there any evidence of chemosis.

Initial CT-angiogram (CTA) of the head and neck revealed decreased caliber of the left common carotid artery with concern for internal carotid artery (ICA) occlusion. There was evidence of significantly dilated vessels near the left CS and basal venous system and distended varices near the hemorrhage (Fig. 1). The patient’s lesion was thought to represent either a CCF or arteriovenous malformation. An emergent external ventricular drain (EVD) was placed and the patient was taken to the angiography suite.

Diagnostic cerebral angiogram confirmed chronic left ICA occlusion and the presence of a large, left-sided CCF. There was evidence of enlarged external carotid artery (ECA) branches which anastomosed with the distal ICA as well as multiple fistulous connections to the CS with occlusion of the cavernous ICA (Fig. 2). Right-sided ICA injections demonstrated an enlarged right ICA with filling across the anterior communicating artery complex to the left hemisphere and retrograde flow within the left ICA with a CCF and significant venous hypertension. There was evidence of reflux into the superficial and deep venous systems. This included the basal vein of Rosenthal, the middle cerebral vein and several frontal cortical veins. This resulted in venous ectasia and a large venous aneurysm of the thalamostriate vein in the white matter adjacent to the left frontal horn, which corresponded to the site of hemorrhage.

Upon diagnosis of the left CCF, transarterial embolization was performed using a transcirculation route via the anterior communicating artery. Two echelon (MicroTherapeutics, Irvine, CA, USA) microcatheters were navigated into the left supraclinoid ICA to the CS and into the origin of draining vein connecting to the CS. The vein was initially embolized with coils to optimize the delivery of the subsequent embolysate, Onyx (ethylene-vinyl alcohol copolymer (EVOH), ev3 Neurovascular, Irvine, CA, USA). This resulted in near-complete occlusion of the CCF with no further evidence of cortical venous reflux (Fig. 3).

Intraprocedurally, the patient experienced transient intracranial pressure (ICP) elevations which were responsive to medical therapy. Upon completion of the embolization, these elevations became refractory and a post-procedural CT scan demonstrated expansion of the hematoma and IVH (Fig. 4). The decision was made to perform an emergent decompressive hemicraniectomy and hematoma evacuation. Post-operatively, the patient did not have significant improvement in clinical examination. Given the patient’s persistent poor neurological examination over the next several days the family decided to withdraw care. The patient ultimately expired on hospital day 20.

Historically, CCF(s) were classified by their etiology (traumatic vs. spontaneous), hemodynamic properties (high flow vs. low flow), or anatomic characteristics. The Barrow classification groups CCF(s) into four objective angiographic categories based on arterial supply [4]. This classification is more relevant to the patient’s clinical presentation, prognosis, and treatment. Type A fistulas describe direct shunts between the cavernous ICA and the CS which are high-flow and almost never resolve spontaneously. In contrast, Type B, C and D fistulas are indirect shunts between the ICA, ECA and both respectively. These tend to be more insidious in onset, low-flow and sometimes can resolve without treatment.

With increasing understanding of the pathophysiology of CCF(s), the significance of venous outflow pathways became clear. Moreover, the importance of venous drainage patterns was highlighted as treatment paradigms shifted away from parent artery occlusion and transarterial detachable balloon embolization to more contemporary transvenous endovascular therapy using coils or liquid embolic agents. Venous outflow patterns in a CCF can be divided into five types: anteriorly into ophthalmic veins, inferiorly into the pterygoid plexus or inferior petrosal sinus, posteriorly into the deep venous system or superior petrosal sinus, superficially towards the superficial sylvian vein and contralaterally [3]. In the case of posterior drainage, as in our patient, arterial pressure is more easily transmitted to the cerebral veins. Previous reports have correlated the site of the ICH to that of venous engorgement [12,23]. Thomas et al. recently developed a venous-drainage based classification system which has been shown to correlate with symptomatology and treatment approach [22]. Whereas the Barrow classification system focuses on arterial supply, this newer system emphasizes how in current endovascular management, venous drainage patterns may have more significance than arterial ones.

The illustrated case presents a complex CCF that can be characterized as Type A & D. While the patient likely developed a characteristic Type A fistula secondary to his initial GSW, subsequent carotid occlusion masked any acute symptomatology at the time. Furthermore, enucleation eliminated anterior pathways of venous egress from the CS. On angiography, the ipsilateral supraclinoid ICA remained patent due to the low-resistance circuit via the anterior communicating artery complex. The left common carotid angiogram demonstrated ICA occlusion with the development of collateral arterial feeders from the ECA supplying the fistula. Moreover, extracranial-intracranial collateral circulation arising from the internal maxillary and ascending pharyngeal arteries likely contributed to the persistent filling of the distal ICA. The combination of these feeders resulted in a high-flow CCF as evidenced by multiple flow-related aneurysms and severe cortical venous hypertension. In the aforementioned venous classification scheme, our patient would fall into type IV which involves retrograde drainage into cortical veins. This type of CCF can be successfully treated by occlusion of the draining venous channel immediately distal to the fistulous point

The majority of patients develop a direct CCF secondary to trauma and most commonly present with symptoms related to ocular hypertension—the absence of ocular symptoms in a direct CCF is very rare. Due to the configuration of anastomoses to the CS, high pressure can be transmitted to cerebellar veins, temporal lobe veins, and the deep venous system. Venous hypertension can lead to venous ectasia or even ICH. Venous ectasia in turn can produce deficits from mass effect on critical structures [5]. We present a case of a patient with a history of a GSW to the left orbit and a delayed left-sided ICH with no sentinel symptoms. Enucleation led to masking of ocular symptoms, and undiagnosed venous hypertension manifested as ICH. Delayed ICH secondary to absence of ocular symptoms makes this a unique presentation.

Our literature review identified only 4 cases with no symptoms prior to ICH. The first patient had undergone a major maxillofacial surgery with iatrogenic trauma; however, significant facial swelling made assessment of symptoms difficult [12]. The second patient was involved in a MVA with facial trauma, also limiting assessment [11]. In the third case, D’Angelo et al described a 76-year-old female who sustained maxillofacial trauma after a MVA and suffered an ICH with no preceding ocular symptoms [8]. This was attributed to a low-flow venous drainage pattern although no posterior cortical venous outflow could be identified by the authors. The fourth case involved a Type A fistula treated with ICA ligation that later recanalized due to development of ECA collaterals [24].

The time between initial symptoms of a CCF and hemorrhage was reported to range between several days to 6 years with a median of 7 weeks in our review. However, in the illustrated case, a 38-year time span marked the interval between the inciting trauma and resultant ICH from a traumatic CCF. Workman et al described an interesting delayed presentation with a comparable timeline to ours: a 9-year-old male who sustained a GSW to the head, immediately developed a CCF, and underwent surgical ligation of the left ICA [24]. He later presented at the age of 35 with a cerebellar ICH. It was found that he had developed ECA collaterals, which re-constituted the cavernous ICA and re-formed the fistula over time. In a similar fashion, our patient appeared to have developed venous hypertension over a long period of time, explaining the occurrence of ICH after a long absence of symptoms. The delayed presentation in these cases highlights the need for a long-term follow-up in this patient population.

Venous hemorrhage from a CCF can progress rapidly. Half of the patients we identified required a surgical procedure and a majority suffered a permanent deficit or death. This highlights the importance of intracranial vascular surveillance in patients with traumatic maxillofacial and orbital history, particularly in those where symptoms of ocular hypertension may not be obvious. Endovascular occlusion of the CCF should ideally precede an open surgical evacuation of the ICH so as to avoid intraoperative venous hemorrhage [9,16].