Ischemic stroke following STA–MCA double bypass

2.1 Patient population and inclusion criteria

We included patients who underwent STA–MCA double bypass surgery at Tianjin Huanhu Hospital from January 2016 to December 2020. Before surgery, patients were assessed by a neurologist using the National Institutes of Health Stroke Scale (NIHSS) and modified Barther scores to evaluate neurological function. The criteria for inclusion are as follows: (1) patients with ICAO had deteriorating neurological function due to recurrent ischemic stroke and episodes more than twice within 6 months (our treatment began with BMT). (2) Symptoms (ischemic stroke or transient ischemic attack) are due to atherosclerotic ICAO rather than other factors (e.g., cardiogenic embolism). (3) DWI-MRI proved the ischemia in all recurrent events. The ICAO patients with poor blood supply to the CoW and an area of cerebral hypoperfusion exceeded the area supplied by the MCA. (4) Modified Rankin scale ≤ 3; 40–70 years of age (inclusive); and no severe heart disease.

The integrity of CoW has the potential to protect against recurrent ischemic strokes. The CoW score is based on the assumption of the CoW integrity [7]. Conventional angiography evaluates the anterior and posterior communicating arteries and gives each artery a score of 2. A maximum score of 6 indicates a fully intact CoW. If the contralateral intracranial internal carotid artery stenosis exceeded 70%, the anterior and posterior communicating artery scores on the side of the stenosis were considered 0 in this study. This change is necessary because if the contralateral internal carotid artery has severe stenosis (>70%), we consider that the collateral blood flow through the anterior or posterior communicating artery may be compromised. Such changes were also applied in the posterior circulation assessment. If one vertebral artery was occluded and the other vertebral artery had stenosis of >70%, or if the basilar artery had stenosis of >70%, the collateral flow through the posterior communicating artery might be affected. All were considered to have a score of 0 for the posterior communicating artery. Patients with a 0–3 were in the poor CoW integrity group, and those with a 4–6 were in the good CoW integrity group.

1. Informed consent: Informed consent has been obtained from all individuals included in this study.

2. Ethical approval: The research related to human use has been complied with all the relevant national regulations, institutional policies and in accordance with the tenets of the Helsinki Declaration, and has been approved by the Institutional Review Board of Tianjin Huanhu Hospital.

2.2 Hemodynamic evaluation

Dynamic susceptibility contrast-enhanced perfusion-weighted magnetic resonance imaging (DSC-PWI) is a relatively newly available tool with a high degree of feasibility and safety that can be used to assess whether a patient needs direct bypass surgery [8]. It also can be used to evaluate the need for direct bypass surgery and evaluate a patient’s long-term prognosis. The DSC-PWI study (repetition time = 2,500 ms, echo time = 80 ms, and flip angle = 90°) was performed preoperatively and postoperatively using a Siemens 3.0T Trio TIM system magnetic resonance imaging (MRI) scanner. The MRI scan included the area from the skull base to the parietal cortex. After scanning, a hydrodynamic injection (3 mL/s) of gadolinium contrast (0.1 mmol/kg body weight) was administered through the antecubital vein. Perfusion source images were obtained using a gradient-echo-echo-planar imaging sequence scanning the whole brain with the following parameters: interlayer spacing = 1.8 mm, layer thickness = 6 mm, and field of view = 230 mm × 230 mm. Perfusion data were processed and converted into parameter maps for cerebral blood volume (CBV), cerebral blood flow (CBF), time to peak (TTP), and mean transit time (MTT).

The Alberta Stroke Program Early CT Score (ASPECTS) is determined by assessing the MCA supply area at two standardized regions (basal ganglia level and supra-ganglionic level) [9]. Combined with the DSC-PWI, it is an innovative, quantitative, and valuable grading scale for patients with ischemic cerebrovascular disease [8]. The standardized areas are divided into ten sections (Figure 1). The same standardized regional locations were selected for each measurement preoperatively and postoperatively, avoiding infarct locations and large vessel regions compared to the reference regions. The four-color map derived from the DSC-PWI described above can also be scored in this way. CBV-ASPECTS, CBF-ASPECTS, TTP-ASPECTS, and MTT-ASPECTS were measured preoperatively and postoperatively. One score is subtracted if one of the ten MCA supply areas shows perfusion abnormalities. Ten points indicate no ischemic changes in the MCA area, whereas one point indicates a state of severe ischemia and occlusion.

Figure 1

According to the ASPECTS study [9], the MCA supply area is at two standardized regions (basal ganglia and supra-ganglionic levels). The standardized areas are divided into ten sections: C, L, IC, I, M1, M2, and aM3 at the level of basal ganglia area and M4, M5 and, M6 at the level of the supra-ganglionic area. Legend: A, the anterior cerebral artery supplied areas; P, the posterior cerebral artery supplied areas; C, the areas of the caudate nucleus; L, the areas of the lenticular nucleus; IC, the areas of the internal capsule; I, the areas of the insular zone. M1–M6 represent the MCA supplied areas.

2.3 Surgical strategies

The superficial temporal artery course was mapped using a Doppler flow detector and separated through a curved incision behind the hairline (Figure 2). The vessels were stripped from the subcutaneous tissue under the microscope. We use a combination of bipolar cautery and scissor-dilated dissection to access the superficial temporal artery from the connective tissue attachment and separate small branches from the main trunk. When the trunk and two branches of the superficial temporal artery were separated, they were flushed with heparinized saline, cut distally, and protected with poppy-impregnated cotton.

Figure 2

Intraoperative images of the STA–MCA double bypass. (a) The position used and planning for the flap incision. (b) The bone flap and preservation of the middle meningeal artery. (c) Anastomosis between the branches of the STA and the cortical branches of the MCA. (d) Demonstration of patency using indocyanine green angiography.

The donor artery is prepared by removing the connective tissue distal to the donor’s vessel. The end of the donor artery was increased with an oblique 45–60° dissection to increase vascular anastomosis. The caliber on the selected recipient vessel was similar to that of the superficial temporal artery. A white latex glove piece was placed between the recipient artery and the adjacent brain surface to protect the brain tissue and optimize the field of view. After cross-clamping the recipient vessel with an aneurysm-blocking clip, the recipient’s vessel was dissected with a T-shaped incision, and the arterial lumen was flushed with heparinized saline. Each end-lateral anastomosis was performed separately, with each superficial temporal artery donor being anastomosed to each MCA recipient using a double 10-0 nylon interrupted suture technique. Each anastomosis was blocked for 20–30 min. Indocyanine green (ICG) angiography was performed inter-operatively (Zeiss Pentero Flow 800 microscope; Zeiss Corporation, Oberkochen, Germany/ICG dye; Buffalo Grove, Illinois [Akorn]).

2.4 Postoperative management

Patients undergoing STA–MCA double bypass surgery were treated with the BMT before surgery. Our treatment optimized all medical therapeutic options, including judicious blood pressure control, aggressive lipid lowering with statins, glycemic control, and smoking cessation. One hundred milligrams of aspirin per day were prescribed for 1 year. The patients received CT angiography (CTA) to assess graft patency. Postoperative angiography and DSC-PWI were performed to evaluate the hemodynamic improvement. All patients were followed up in our outpatient clinic for at least 36 months. Patients’ neurological function was scored on the NIHSS and statistically analyzed. Patency of the bypass and changes in collateral vessels were assessed by CTA or digital subtraction angiography (DSA).

2.5 Statistical analysis

Fisher’s exact probability method is used for statistical tests of count data. The statistical test for measurement data was t-test or ANOVA if they conformed to a normal distribution; the rank-sum test was used if they did not conform to a normal distribution. The test level α was set at 0.05. IBM SPSS Statistics for Windows, version 27.0 (IBM Corp, Armonk, NY, USA) and R software version 4.0.3 (R Core Team, 2014) were used for statistical analysis and graphing.

3.1 Perioperative consequences and complications

According to the inclusion criteria, 12 ICAO patients were treated with STA–MCA double bypass surgery (Table 1). The patency of each anastomotic stoma was confirmed by intraoperative ICG injection. The complication was subdural hemorrhage in one patient (out of ten patients) in the operative area and received conservative therapy (Table 2). No intracranial infections or acute ischemic events occurred. No patient in our cohort suffered epileptic seizures; patients were given regular anti-epileptic treatment after surgery, even when the operated area was limited to the cortex.

3.2 Improving neurological function

NIHSS scores and modified Barther scores were calculated for all patients perioperatively and in follow-up. The mean NIHSS score was 6.50 [5.75; 7.25] preoperatively. During follow-up, the mean NIHSS score was 4.50 [4.00; 5.00]. Statistical analysis revealed statistically significant differences in the NIHSS scores measured in the preoperative and follow-up periods (P < 0.005). The mean modified Barther score was significantly improved from 41.00 [35.00; 50.25] preoperatively to 82.50 [75.00; 90.00] at the last follow-up (P < 0.005). Whether a patient received any benefit from the surgery depended on their preoperative neurological status. Those with higher initial NIHSS scores and lower initial modified Barther scores experienced more significant improvements in their NIHSS scores and modified Barther scores after surgery.

Ten (83.3%) of the 12 patients who had a history of ischemic stroke with limb weakness showed improvement in muscle strength. Eight (80.0%) of the 10 patients who had residual neurological deficits with partial motor aphasia and/or dysarthria showed improved neurological function or language function progress. All these patients had improved neurological function or decreased occurrence of transient ischemia attack (TIA) during the follow-up period.

3.3 Bypass patency

One week after surgery, CTA revealed a 100% patency rate for the anastomotic stomas. Twelve patients (24 anastomoses in total) underwent DSA of 6 vessels for at least 6 months after surgery to determine the surgically induced collateral circulation status (Figure 3). All operated hemispheres were predominantly supplied by the external carotid artery system in this series. Twenty three (96%) anastomoses remained patent, and circulating blood flow entered the MCA region. One patient had occlusion of a bypass vessel at the 1 year follow-up evaluation. No new infarct foci were seen on the MRI scan, and the patient had no new neurological deficits.

Figure 3

Patient with left ICAO. DSA imaging before (a–d) and after (e–f) STA–MCA double bypass. CTA images (g–h) were obtained 1 year after the bypass surgery.

3.4 Hemodynamic changes in the operated side

Table 3 summarizes the analysis of PWI-ASPECTS score data before and after bypass surgery. Postoperative DSC-PWI showed hemodynamic improvement in all 12 patients (Figure 4). The CBF-ASPECTS increased from 5.00 [5.00; 6.00] to 8.00 [8.00; 9.00], the MTT-ASPECTS increased from 2.00 [2.00; 3.00] to 7.00 [6.00; 8.00] and TTP-ASPECTS increased from 3.00 [3.00; 3.00] to 6.00 [5.00; 8.00] postoperatively, with a statistically significant difference. However, the CBV-ASPECTS did not significantly differ before and after the bypass surgery. These changes in PWI-ASPECTS score parameters after direct hematopoietic reconstruction suggest that significant improvements in cerebral perfusion in the surgical hemisphere can be expected after surgery. The patients with lower preoperative PWI-ASPECTS score have more significantly improved postoperative cerebral perfusion.

Figure 4

A 64-year-old woman with recurrent ischemic stroke. Cerebral perfusion imaging before (a) and after (b) STA–MCA double bypass.