Oculomotor Nerve Palsy Induced by a Cerebral Developmental Venous Anomaly: A Case Report and Comprehensive Review

Introduction

Developmental venous anomalies (DVAs) are relatively common cerebrovascular malformations that are often encountered incidentally during routine brain imaging [1] and affect approximately 2% of the general population [2]. DVAs, initially known as cerebral venous angiomas, are extreme anatomical variations of medullary veins that represent a convergence of venous drainage from normal cerebral white and gray matter [3,4]. They generally appear to be non-symptomatic. Despite their benign nature, DVAs can occasionally be symptomatic. To the best of our knowledge, there are no theories regarding the role of DVAs in oculomotor nerve palsy (ONP). Here, we present a case of sudden diplopia and eyelid ptosis associated with symptomatic DVA-induced mechanical compression of the oculomotor nerve. The case report was approved by the ethics review committee of Huashan Hospital affiliated to Fudan University.

Case Report

A 67-year-old woman was admitted to our hospital with a sudden onset of diplopia and ptosis in the left eyelid for 10 days.

The patient had a medical history of well-controlled hypertension and diabetes for 5 years. Neurological examination revealed pupil-involving left complete ONP (Figure 1C). The abducent, trochlear, and trigeminal nerves were spared. Furthermore, the visual acuity was normal. No retinal hemorrhage, venous dilatation, or fundus tortuosity were observed in fundus photography. Other neurologic deficits, including eye pain or pulsatile tinnitus, were undetected. All laboratory examinations, including erythrocyte sediment rate, and electroencephalogram results, were within the normal limits. Additionally, post-contrast T1-weighted images demonstrated no widening or enhancement of the cavernous sinus (not shown), and no ischemia lesions or neoplasms observable in MRI, but an offending vessel (Figure 1A, 1B, arrow) compressing the left oculomotor nerve (Figure 1A, 1B, arrowhead) in the fossa interpeduncular at the root entry zone of the brainstem was identified using magnetic resonance tomography cerebral angiography (MRTA) and maximum intensity projection (MIP) of the MRA. Therefore, we hypothesized that ONP was caused by an abnormal arterial structure. However, digital subtraction angiography (DSA) revealed no aneurysm or abnormal arterial structure in the arterial phase, while a tortuous and dilated collecting vein was detected in the venous phase, connecting the left temporal lobe to the left cavernous sinus (Figure 2A, 2B, arrow). This indicated a typical caput medusae appearance (Figure 2A, square), suggesting the mechanism of oculomotor palsy caused by compressive impairment of the DVA. The patient refused micro-vascular decompression surgery, and ONP persisted after 30 days. Management was conservative, with spontaneous resolution at 60 days and no recurrence during the 2-year follow-up.

Discussion

RELEVANT ANATOMY BLOOD SUPPLY OF OCULOMOTOR NERVE:

Acute ONP with pupil-involving is always related to mechanical compression, such as intracranial aneurysms. Meanwhile, most isolated pupil-sparing cases are typically due to microvascular ischemia, which is frequently associated with diabetes mellitus or other vascular risk factors. These discrepancies may be due to the distinct vascular supplies of the somatic and autonomic components of the oculomotor nerve. Anatomically, the vasa vasorum supplies the inner somatic nerve fibers, whereas the outer autonomic nerve fibers are supplied by the pia mater blood vessels [15,16]. According to the above mechanism, we concluded as follows. A complete ONP accompanied by a dilated pupil may be the first sign of external compressive lesions in the subarachnoid space due to the dorsal and peripheral locations of the pupillary fibers. Microvascular diseases caused by diabetes primarily involve the vasa vasorum, resulting in pupil sparing.

Pupil sparing is critical in determining the etiology of oculo-motor nerve dysfunction. It is a crucial clinical manifestation that can be fatal in certain situations. However, certain unusual conditions also exist [17,18]. For example, diabetes can cause pupil dilation, and mechanical compression can also display pupil sparing, as listed in Table 2.

SPECIFIC CONSIDERATIONS FOR PHYSIOPATHOLOGY MECHANISMS OF SYMPTOMATIC DVAS:

Despite their benign nature, DVAs may be symptomatic due to mechanical compression or flow-related pathological mechanisms. Mechanical complications usually lead to nerve compression syndromes, whereas flow-related mechanisms can be categorized as those caused by increased drainage into the DVA or outflow occlusion [19–21]. Patients without these mechanisms are considered to have idiopathic symptomatologies [22]. As a variation in venous drainage during fetal development, the single venous collector in DVAs can be overloaded due to dilated radial veins and a more fragile venous outflow system or outflow restriction [22]. We believe that the simultaneous occurrence of ONP could have been caused by inadequate distal drainage, and vascular lumen diameter enlarged, which increases the conflict between nerves and vessels. A previous study demonstrated that most patients (63%) with acquired isolated ONP have complete recovery in the overall population [23], while 95% with a microvascular ONP had complete recovery, indicated the microvascular compression is the etiology predicting favorable outcome. The post-contrast T1-weighted images demonstrated no sign of the cerebral cavernous malformations (CCMs), but the most common mixed form of intracranial vascular malformations is the coexistence of DVAs and CCM. Moreover, mixed CCM with DVA has a higher risk of hemorrhage, and DVAs are considered to play an evolutional role in the development and growth of CCM [24].

In summary, our case report highlighted 2 important points. First, external compression easily leads to complete ONP with pupil involvement, consistent with the findings of previous studies. Second, direct venous compression should be considered in patients with unilateral complete ONP when other pathologies have been ruled out. Most current theories support the role of DVAs in normal cerebral venous drainage; therefore, surgical resection or endovascular obliteration of DVAs can lead to venous infarction in draining areas, and conservative management is one of the therapeutic options for these vascular lesions [4,25].

Conclusions

In conclusion, we present a case of symptomatic cerebral DVA associated with ONP. Despite the benign nature of DVAs, when the cause of clinical symptoms cannot be identified, symptomatic DVAs should be considered, which is crucial for clinical decision-making. As for the existing role of venous drainage in the normal brain tissue, conservative management is an alternative approach for DVAs to avoid the complication secondary to the disturbance of blood circulation in draining areas.