Cerebral edema is defined as an increase in brain volume due to abnormal accumulation of fluid within the brain parenchyma [
11], and it is classified as vasogenic, cytotoxic, hydrocephalic and osmotic edema, despite the acknowledgment that multiple types of cerebral edema are involved in most clinical situations. Regarding the mechanism, vasogenic edema is associated with micro destructions that allow increased plasma proteins and water across the blood-brain-barrier, while cytotoxic edema is accompanied by abnormal water uptake into injured brain cells [
12]. Diagnostically, unlike cytotoxic edema associated with hyperintensity in DWI and decline in Apparent Diffusion Coefficient, vasogenic edema presents a variable weak change in DWI and a relative increase in water diffusion [
13]. The existence of hyperintensity on T2-weighted MRI accompanied by the lack of typical hyperintensity lesions in DWI indicates that this area mainly refers to vasogenic edema (Fig.
3a and b). Postoperative cerebral edema mostly occur in MMD or those with CEA or CAS [
6,
14,
15]. This condition is rare after surgery for the patients with carotid occlusive disease. The region of edema resulting from CHS is often limited to the territories near the surgical area, and hyperintensity lesions can be found in perfusion images. Among MMDs with combined bypass, retrospective analysis found that hyperperfusion-related symptoms generally occur in the first week and are entirely ameliorated during the second postoperative week [
15]. Presenting neurological deficits 6 days after bypass, this patient began improving on the 17th day and completely recovered on the 40th day after surgery. The procedure to alleviate symptoms does not exactly conform to the course of postoperative CHS among MMDs. However, the dual branches of STA were anastomosed to M4 segments, making “watershed shift” possible structurally. Normalized CBF (nCBF) calculated by MRI 3D-ASL near the operative area showed an early decrease and delayed increase (Table
1) by manually choosing the region of interest in MRI 3D-ASL [
16]. Meanwhile, T2-weighted MRI on the 3rd day after surgery showed early focal cerebral edema at the sites of anastomosis (Fig.
2b). In addition to transient aphasia and hemiplegia, cerebral edema and changes in perioperative nCBF can be explained by the “watershed shift”. Nevertheless, a classical “watershed shift” is defined basis on CHS, which requires ≥50% increase in the CBF at the site of anastomosis [
17]. However, the absolute values of CBF on the 3rd or 21st day after surgery were both decreased below the preoperative level, even on the normal side. T1-weighted MRI on the 21st day presented mild migration of the middle line to the right side (Fig.
3c), indicating increased intracranial pressure likely still played a role in affecting cerebral perfusion in the whole brain. The steal phenomenon was thought to result in hypoperfusion on the right side. The dual bypass associated with EDMS changed the previous hemodynamics balance between the stenotic side and right side. It reduced the vascular resistance on the left side and released blood flowing into the left rather than the right hemisphere. In contrast to contralateral nCBF, we found that nCBF on the affected side increased to different degrees. Among them, the most significant difference was 1.374 vs. 0.987, which presented on the 21st day after surgery (Table
1). Different from the classical “watershed shift”, a large amount of brain tissues were involved in cerebral edema. Thus, other mechanisms may explain the progression of cerebral edema. In addition to the “watershed shift”, a swollen temporal muscle was also considered to induce focal edema. During the acute stage, a relatively narrow free bone flap could magnify the compression of the swollen temporal muscle, influencing regional cerebral circulation and resulting in local brain edema [
18]. The swollen temporal muscle found on the postoperative T2-weighted MRI may exacerbate the situation. However, its effect was temporary and limited because the temporal muscle had already shrunken to normal size when the patient began to recover on the 17th day after surgery. Venous congestion was once considered as the primary cause because such massive cerebral edema associated with CHS has not been reported previously. However, venous congestion is generally related to cerebral hypoperfusion, and it seems impossible for venous congestion to be involved. Additionally, epilepsy was unrelated to severe cerebral edema in the patient in the lack of obvious symptoms of epilepsy, which has been reported as a possible cause of vasogenic edema [
19]. It remains a mystery why reversible cerebral edema could lead to such severe clinical symptoms, even requiring surgical intervention. To prevent such severe cerebral edema from further into brain hernia or causing subsequent hemorrhage, one possible approach is a strict perioperative strategy. As standardized management to prevent CHS, the blood pressure should be below 130 mmHg. However, extensive low blood pressure could lead to cerebral infarction [
20], and so the blood pressure of this patient was controlled under 140 mmHg by nimodipine rather than 130 mmHg. Fluid intake and hydroelectrolytic equilibration should also be considered cautiously every day. We regulated fluid intake and focused on blood tests to maintain homeostasis. Additionally, the combination of mannitol and furosemide was employed to lower intracranial pressure when clinical symptoms presented and MRI-DWI confirmed focal cerebral edema. Another possible approach is the use of edaravone, which is an antioxidant to prevent reperfusion-associated hemorrhage that can be administered to reduce effects from huge changes in CBF [
21]. Additionally, quantitative magnetic resonance angiography may potentially identify patients at risk for CHS by assessing mean flow differences between ICA and MCA [
22]. By applying multiple strategies, the complete disappearance of focal cerebral edema was obtained without permanent neurological deficits. Therefore, further study with a larger number of patients is necessary to validate the relationship between cerebral edema and the “watershed shift”.
Table 1
Cerebral perfusion calculated on MRI 3D-ASL
L | MCA (mean ± SD) (a) | 40.999 ± 21.104 | 31.981 ± 22.397 | 25.802 ± 12.429 | 47.109 ± 18.265 |
Cerebellum (mean ± SD) (a) | 29.406 ± 9.695 | 27.204 ± 9.943 | 18.782 ± 6.519 | 36.485 ± 8.837 |
nCBF (b) | 1.394 | 1.176 | 1.374 | 1.291 |
R | MCA (mean ± SD) (a) | 44.554 ± 12.035 | 32.945 ± 20.146 | 24.473 ± 13.416 | 44.421 ± 16.137 |
Cerebellum (mean ± SD) (a) | 39.079 ± 11.926 | 31.380 ± 8.041 | 31.380 ± 8.041 | 37.683 ± 12.200 |
nCBF (b) | 1.140 | 1.051 | 0.987 | 1.179 |
In conclusion, this case presents massive cerebral edema after bypass. Based on changes in cerebral blood flow and reversible symptoms, the “watershed shift” may explain this severe deficit. However, this deficit is not the same as the classical presentation resulting from the “watershed shift”, which does not involve brain tissues and presents significant increases in CBF compared with the preoperative level. In addition to the “watershed shift”, the swollen temporal muscle also participated in the progression of focal edema.