Cerebral arteriovenous malformations (AVMs), characterized by the feeding arteries, nidus and draining veins, are a congenital disease [19,28]. Their most common and serious presentation is the intracerebral hemorrhage (ICH) at the age between 20 and 40 years old [9,28]. So, it is general to examine the probably accompanying AVM when ICH occurs in young patients [9,33]. AVMs are easily diagnosed with radiological tools such as computed tomography (CT), magnetic resonance (MR) imaging and digital subtraction angiography (DSA). However, there is a rare entity of occult AVMs, also called crypt AVMs, which are histologically present but invisible on radiologic examinations [4,22]. With the development of brain MR imaging, the identification of occult AVM has significantly improved [13]. Nonetheless, there are still occult AVMs not detected with DSA and brain MR imaging. We are to introduce a case presenting with cryptogenic ICH 11 years ago and epilepsy recently which were caused by radiologically occult AVM, with review of the literature.

An 18-year-old male patient with no underlying medical history presented with a sudden severe headache, vomiting and altered mentality. On the radiological examination, a 45-cm³ sized ICH was identified in the right temporal lobe with a 9-mm midline shift to the left. The patient underwent craniotomy and ICH removal. During the surgery, an arterialized vein was identified on the temporal surface (Fig. 1), suspected of a shunt of vascular malformation. Hematoma evacuation alone was done, remaining the abnormal vascular lesion, in order to escape from the catastrophic situation such as AVM rupture without grasping the angioarchitecture. On the postoperative DSA, however, there was no clear evidence of vascular malformation except a slow shunt flow which was identified later. There was no evidence of AVM on the pathologic examination. Antiepileptic drug was discontinued in 7 months after surgery, however, it was restarted in 5 months due to the occurrence of epileptic seizure. Brain MR imaging at that time showed no abnormal findings except the cerebromalacia in the right anterior temporal lobe (Fig. 2A). Antiepileptic drug was discontinued again in 10 months. Thereafter, the patient was lost to follow up on his own will, during which the patient said that there was no seizure event.

In 91 months after the initial surgery, the patient revisited, presenting with recurrent seizures. On a brain MR imaging, multiple signal voids and the enlarged vessels were shown in the right anterior temporal area. A DSA showed a 3.4-cm sized AVM of the Spetzler-Martin grade 2, fed by multiple branches from the right middle and posterior cerebral arteries, and middle meningeal arteries, with the venous drainage into the vein of Labbe and cavernous sinus via the right superficial sylvian vein (Fig. 2). Presurgical glue embolization with Onyx^® (ev3, Irvine, CA, USA) was partially performed 1 day before surgery. On the next day, removal of the AVM and right anterior temporal lobe were performed (Fig. 2). The patient was discharged with no additional complication, maintaining the antiepileptic drugs.

The annual incidence of ICHs in young adults (<50 years of age) is known about 5 per 100000 individuals [12]. Hypertension and vascular malformations are the most common causes of ICHs in young adults [11,14]. AVMs are the leading cause in a third of the patients with ICHs under 40 years of age [23,29]. Therefore, it is important to confirm the underlying lesions through radiological examinations when young adults present with the ICH [21]. Initially in this case, an AVM was suspicious during the surgery, however, it was not identified on the preoperative and postoperative imaging work-up. There were no abnormal structural lesions even on 1-year follow-up brain MR imaging after the surgery. However, the patient visited again with recurrent seizure and an AVM was finally identified on brain MR imaging and DSA in 11 years after the occurrence of ICH.

The AVMs are intermingled into the brain parenchyme, consisting of arteries, nidus and draining veins with no capillary beds [3]. Diagnosis of the AVMs is usually made with the aid of radiological tools such as brain CT, MR imaging and DSA. However, there have been rare cases diagnosed only by the pathologic examinations after the surgical acquisition of the specimen, with no radiological evidences of the AVMs [2,5,6,20,22,24,26,27,32]. In the pre-MR era when lesions were evaluated with brain CT and DSA alone, such rare cases were called angiographically occult AVMs [22]. Crawford and Russell [4] firstly used the term “cryptic” for small angiomatous malformation that could not be localized due to hematoma and small size. Lobato et al. [17] analyzed 126 cases of angiographically occult AVMs. The mean age at diagnosis was 31.9 years old. The most common clinical symptom was a seizure in 47% of the patients, followed by neurological deficits in 42% and headache in 35%. Microhemorrhage was accompanied on the histological examinations in 80% of occult AVMs. The possible mechanisms by which angiographically occult AVM occurs include small size, mass effect by the adjacent hematoma, and thrombosis of the AVM [18,22]. In this case, it can be speculated that the AVM was not found on the initial radiological work-up because of the small size, mass effect compressing the nidus or thrombus formation within the feeding arteries. As time went on, the AVM grew and the feeding arteries blocked by the thrombus were recanalized, and finally the AVM could be identifiable on the brain MR imaging and DSA. Reports of the growing AVMs are also rare but well known [1,10,25,31]. If the size of the AVM in our case was not small from the initial hemorrhage, pathological angioarchitecture would have been found in brain MR imaging regardless of the mass effect or intravascular thrombosis.

Real occult AVMs have decreased with the introduction of the brain MR imaging [13]. Typical MR findings of AVMs are enlarged and tortuous flow void lesions on T2-weighted images with hemorrhage, adjacent edema and cerebromalacia [7,21]. In addition, abnormal shunting flow is well demonstrated on MR arterial spin labeling which is used to diagnose the small AVMs and dural arteriovenous fistulas, and to evaluate the treatment outcome and recurrence of them [8,16,30]. However, there are still several reports about the occult AVMs undetected on the brain MR imaging and DSA, including this case (Table 1). So, we renamed these as “radiologically occult AVM”. Mean age of the cases was 34 years and 41% were male. As for clinical symptoms, headache was the most common (53% of the cases), followed by seizure (41%). On the brain CT and MR imaging, intracranial hemorrhage including ICH, subdural hemorrhage and subarachnoid hemorrhage, was found in 65%, and calcification was in 42%. Considering that clinical presentations of the usual AVMs are hemorrhage in 50% and seizures in 20–25% [15], radiologically occult AVMs showed a higher tendency of seizure presentation. All cases were finally confirmed as an AVM on pathologic examination. Thrombotic vessels were identified during the surgery in six cases. The prognosis was good in most of cases.

Radiologically occult AVMs are very rare with the development of radiological tools. They usually tend to present with cerebral hemorrhage and seizure. Especially in young patients with the ICHs, the causes of ICHs should be initially investigated in order to prevent from recurrence. Even if there are no abnormal findings in the initial radiological examinations, long-term follow-up is recommendable with the possibility of radiologically occult AVMs in mind.