Effects of burr-hole surgery on MRI cerebral perfusion and stroke risk in adults with moyamoya angiopathy

doi:10.21203/rs.3.rs-5140048/v1

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Effects of burr-hole surgery on MRI cerebral perfusion and stroke risk in adults with moyamoya angiopathy

https://doi.org/10.21203/rs.3.rs-5140048/v1

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Purpose. Several surgical techniques have been proposed in moyamoya angiopathy (MMA) to reduce stroke risk; nevertheless, no one has clearly demonstrated its superiority. Burr-hole surgery allows the revascularization of large frontal areas and thus is increasingly used, but it has not been systematically evaluated in adults. We assessed the effect of burr-hole surgery as the only revascularization technique on MRI brain perfusion and stroke recurrence in adult patients with MMA.

Methods. Retrospective study of consecutive adults patients with MMA and predominant frontal hypoperfusion treated by burr-hole surgery in a tertiary hospital. Parenchymal hypoperfusion rate on perfusion-weighted imaging (PWI) was compared using TMax before and 6 months after surgery. Perioperative complications and long-term risk of stroke/transient ischemic attack (TIA) were reviewed.

Results. A total of 19 patients (11 women, mean age at surgery ± SD 42.4 ± 8.6 years) were included. A median of 7 (4–9) burr holes/hemisphere were performed on 34 hemispheres. Perioperative cerebral infarction occurred in 3 (15.9%) patients on 3 hemispheres (8.8%/hemisphere). The volume of slightly (Tmax ˃ 4 s) and severely (Tmax ˃ 6 s) hypoperfused parenchyma significantly decreased after surgery (p = 0.003 and p = 0.008, respectively). After a median follow-up of 72 (IQR 24.6) months, 4 strokes occurred in 3 patients (11.7%/hemisphere). The 2-year survival probability free of stroke/TIA was 85%.

Conclusion. In adults with MMA and predominant frontal hypoperfusion, burr-hole surgery as the sole revascularization technique improved brain perfusion as measured with Tmax. Moreover the long-term risk of ischemic events and the rate of complications seemed similar to other techniques.

Moyamoya angiopathy (MMA) is characterized by progressive stenosis and occlusion of the intracranial carotid artery and its main branches, with the development of a basal collateral network (1). These occlusive arterial lesions lead to chronic impairment of cerebral perfusion, essentially in frontal areas, resulting in ischemic or hemorrhagic strokes (2). Surgical revascularization procedures have been developed aiming to improve cerebral perfusion and decrease the risk of stroke and death (3). Among them, multiple burr-hole surgery (MBH) allows for the indirect revascularization of large frontal areas through cortical neoangiogenesis from external carotid artery branches (4). This technique is increasingly used alone or in combination, particularly in children (5). However, data describing its effect in adults are scarce.

Typically, the efficacy of a surgical technique in moyamoya patients is assessed by the risk of stroke recurrence (6). Perfusion imaging and vascular reserve measurement before and after surgery can be used as surrogate markers since brain hemodynamic disturbances are associated with an increased risk of stroke (7, 8). Several imaging modalities are available to assess perfusion changes in MMA, but nuclear imaging such as xenon CT (XeCT), PET scan and scintigraphy remain the most used (9,10,11). Few centers use perfusion MRI, whereas it is widely used and routinely available in cerebrovascular pathologies. In acute stroke, some Tmax thresholds have been well correlated with absolute CBF measurements on XeCT (12). Tmax is used in clinical practice to assess the volume of critical hypoperfusion during acute stroke (13).

The aim of this study was to assess the effect of burr-hole surgery, as the only surgical technique, on brain perfusion measured on MRI and on occurrence stroke/TIA during follow-up in consecutive adults with MMA.

Study design:

We conducted a retrospective study of consecutive adults with MMA (moyamoya syndrome and moyamoya disease) treated in our tertiary hospital by MBH between March 2012 and June 2021.

Population

We included adult patients registered in our database with an MMA treated by MBH.

MMA was diagnosed using established criteria (1). The indication for surgery was based on the usual recommendations and French guidelines (14): recent ischemic events (TIA or stroke) with hypoperfusion and/or vascular reserve impairment or severe vascular reserve impairment with clinical symptom other than stroke.

During the study period, patients with a surgical indication according to our multidisciplinary assessment, no hemorrhagic presentation and predominant frontal hypoperfusion were treated by MBH surgery. French guidelines do not impose a specific technique for revascularization in adults with MMA (14). Studies in children and a few in adults have suggested considering burr holes as an option for moyamoya patients (4, 5). This technique allows for a large-scale revascularization of frontal areas, unlike other techniques, which are more efficient for improving the perfusion of the peri-sylvian parenchyma in lateral hemispheres. Based on these characteristics, it was a hospital decision to choose multiple burr-hole surgery as a first line of treatment for patients with predominant frontal hypoperfusion. Patients with hemorrhagic presentation or more diffuse hypoperfusion were treated by direct or indirect by-pass.

Surgical modalities:

Under general anesthesia, with careful blood pressure monitoring during induction and the surgical procedure, all patients were treated with the same surgical technique of multiple burr holes (MBH). Surgery was performed by 3 experienced neurosurgeons (JCS, PB, SB). After coronal incision, the epicranium was exposed. In front of the hypoperfused region, an epicranial flap was prepared and a burr hole was performed. The dura and arachnoid meningeal layers were carefully opened under microscope and the epicranial flap was deposited against the cerebral cortex in the subdural space (Fig. 1).

Clinical Data collection:

Baseline demographic, clinical and radiological data were recorded in our database.

Follow-up:

All periprocedural (< 7 days post-operation) and pre-discharge complications were collected. All patients were assessed during clinical visits, at least every 6 months. During follow-up, TIA and symptomatic stroke (cerebral infarction and intracerebral hemorrhage) were reviewed to calculate the risk of stroke recurrence after discharge. Stroke was defined as an acute neurological symptom associated with neuroimaging evidence of corresponding acute infarction (symptomatic cerebral infarction) or hemorrhage (symptomatic intracerebral hemorrhage). The number of subsequent recurrent events was also recorded. Functional independence was assessed using the modified Rankin score (mRS), both before surgery and at the end of follow-up.

Radiological data collection:

All included patients underwent DSA (digital subtraction angiography), perfusion-weighted imaging, both before and 6 months after surgery.

DSA :

The development of transdural anastomoses was assessed on digital subtraction angiography 6 months after surgery using a modified Matshushima score.

Matsushima score (15) :

Grade A: area vascularized by the external carotid branches (EC) corresponding to more than 2/3 of the territory irrigated by the middle cerebral artery
Grade B: area vascularized by the EC branches is between 1/3 and 2/3 of the territory irrigated by the middle cerebral artery
Grade C: area vascularized by the EC branches is less than 1/3 of the territory irrigated by the middle cerebral artery

We used the Matshushima score by performing two separate analyses of the middle and anterior cerebral artery territories and adding a Grade 0. Grade 0 corresponded to no area vascularized by the external carotid branches

Perfusion imaging acquisition and analyses:

Perfusion-weighted images were acquired using a gradient echo sequence with the following parameters: TR 1710, TE 20 ms, FOV 100, matrix 108 x 108, flip angle 90°, 4-mm-thick contiguous sections, NEX 1. We measured cerebral perfusion using dynamic susceptibility contrast-enhanced MRI.

TMax maps on baseline and post-surgery MRIs were processed using Olea Sphere® software. Tmax below 2 secondes is usually considered normal perfusion. In patients with chronic hypoperfusion (moyamoya and others), a TMax threshold above 6 s correlates with critical hypoperfusion as assessed using XeCT (13). TMax maps were created using increasing 2 s step thresholds, from 2 s to 10 s. To assess perfusion improvement, we performed a visual qualitative analysis. It was performed by two investigators (PB, CM) by consensus. Then, we performed a quantitative analysis of the hypoperfused parenchyma volume according to TMax thresholds. The distribution of these hypoperfused volumes was converted into a percentage by hemisphere in order to homogenize the results.

Ethical considerations:

According to French ethical and regulatory law (Public Health Code), retrospective studies based on the exploitation of usual care data not need be submitted to an ethics committee, but they have to be declared or covered using the reference methodology of the French National Commission for Informatics and Liberties (CNIL). Toulouse University Hospital signed a commitment of compliance with the reference methodology MR-004 of the CNIL. After evaluation and validation by the data protection officer and according to the General Data Protection Regulation, this study fulfilled all the criteria. It is registered in the register of retrospective studies of the Toulouse University Hospital (register no.: RnIPH 2021-66) and covered by MR-004 (CNIL number: 2121529 v1). This study was approved by Toulouse University Hospital and confirms that the ethical requirements were totally respected in the above report.

Statistical analysis:

We considered each hemisphere separately as an independent parameter, as is usually proposed in MMA. Because of the small number of subjects and the abnormal distribution, we performed non-parametric tests.

The probability of survival without stroke/TIA recurrence after surgery was calculated with Kaplan Meier analysis. Survival time was calculated from date of discharge after surgery until date of stroke/TIA occurrence at follow-up or the last known date without stroke/TIA during follow-up. For patients experiencing multiple stroke/TIA events during follow-up, data were censored after the first event.

The parenchymal hypoperfusion rate in each 2 seconds interval (0–2; 2–4, etc.) were compared before and after surgery by the Wilcoxon test for matched groups. The difference of pre- and post-operative variations between each interval has been evaluated by a Kruskal-Wallis test.

We compared the percentages of normally perfused parenchyma volume (Tmax < 2 s) and hypoperfused parenchyma volumes with Tmax > 2 s: Tmax > 4 s (slightly hypoperfused), Tmax > 6 s (severely hypoperfused) and Tmax > 8 s (critically hypoperfused) before and after surgery using the Wilcoxon test.

The association between improvement of hypoperfusion and collateral development or Suzuki grade was assessed using Fisher’s test.

Values are given as median (range) or means ± SD except where specified. All tests were bilateral. A p-value < 0.05 was considered statistically significant.

Patients:

During this period, 61 patients were registered in our database. Nineteen patients receiving MBH (11 women, 8 men; mean age at the time of surgery: 42.4 +/- 8.6 years) were included. Fifteen patients (79%) had a bilateral MMA. Fourteen (74%) patients had moyamoya disease and 5 (26%) moyamoya syndrome. The presentation was an ischemic stroke in 17 patients (89%). The median time between the first clinical symptoms and surgery was 38.9 months (0.5 to 276.9 +/- 60.9). The median mRS before surgery was 2 (IQR 0–4). Burr-hole surgery was proposed to these patients because of predominant frontal hypoperfusion and ischemic stroke or TIA (n = 17) or headache and cognitive troubles (n = 2) with vascular reserve impairment.

The clinical and radiological characteristics of the patients are summarized in Table 1.

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Table 1

Clinical and radiological characteristics of the study patients.
Data	Values
Patients (N subjects; %) Man (N; %) Female (N; %) Mean age at diagnosis (years; +/- SD):	19 (100) 8 (42) 11 (58) 41.1 (+/- 8.5)
Number of hemispheres (N; %) Man (N; %) Female (N; %)	34 (100) 14 (41) 20 (59)
Initial symptoms: Ischemic event (cerebral infarction/TIA) (N; %) Headache (N; %) Intracerebral Hemorrhage (N; %)	17 (89) 2 (11) 0
Moyamoya disease (N; %) Moyamoya syndrome (N; %) - atherosclerosis - post-radiation - sickle cell disease - dysmorphic syndrome - carotid dissection Bilateral form (N; %)	14 (74) 5 (26) 1 1 1 1 1 15 (79)
Hemispheres studied by angiography (N; %) Initial Suzuki grade per hemisphere (N; %) Grade 1 Grade 2 Grade 3 Grade 4 Grade 5 Preoperative Matsushima score per hemisphere (N; %) MCA area A B C 0 ACA area A B C 0	34 (100) 6 (18) 12 (35) 12 (35) 4 (12) 0 (0) 0 (0) 0 (0) 2 (6) 32 (94) 0 (0) 1 (3) 2 (6) 31 (91)

Surgical treatment:

A total of 34 hemispheres received a median of 7 (range 4–9) burr holes. Mean operative time (+/- SD) was 122 +/- 36 min per surgery and 71.4 +/- 21.3 min per hemisphere. The median length of hospitalization in the neurosurgery department was 11.3 days (range 5 to 30).

The overall rate of periprocedural complications was 26%/patient, (14.7%/operated hemisphere). Three patients (15.7%) experienced a periprocedural cerebral infarction (8.8%/hemisphere). At discharge, two patients (10.5%) had a persistent neurological deficit, one with moderate distal arm weakness and the other with severe aphasia. Two patients (10.5%) presented a post-operative meningocele that did not require surgery (5.8%/hemisphere). Neither hematoma nor death occurred before hospital discharge.

Clinical follow-up:

After a median follow-up time of 93,3 months (IQR: 54,3–153.7 months), 4 symptomatic cerebral infarctions occurred in 3 patients (11.7%/hemisphere). One patient presented a minor stroke in the context of a hemorrhagic collapsus related to splenic traumatism and acute subdural hematoma on the side of the revascularization. The second required a second surgery with superficial temporal artery to middle cerebral artery anastomosis. His disease had progressed in the basilar and posterior cerebral arteries, resulting in decompensation of cerebral perfusion and 2 severe cerebral infarctions. The last patient presented with worsening carotid stenosis and delayed deterioration of her cerebral perfusion with minor stroke. She was operated on with direct anastomosis.

The 2-year and 5-year survival probability free of stroke/TIA were respectively 85% and 80%. Neither intracerebral hemorrhage events nor death occurred during follow-up. The median mRS after the last follow-up was 2 (0–5). Compared with pre-procedural mRS, scores decreased in 6 patients (31.6%) and increased in 3 patients (15.8%). There was no change in 10 patients (52.6%).

Radiological outcome:

Angiographic follow-up

At 6 months after surgery, every patient underwent a cerebral arteriogram allowing analysis of the 34 operated hemispheres (Fig. 2). We observed a modified Matsushima score of A or B in 27/34 studied hemispheres (79%), corresponding to brain revascularization by external carotid. More precisely, with the modification of the Matsushima score, we observe an improvement of this score after surgery in 91% (31/34) of the operated hemispheres in the territory of the MCA and 60% (20/34) in the territory of the ACA.

Perfusion analysis

Three hemispheres were excluded from perfusion analysis due to inadequate quality of the MRI. An overall number of 31 hemispheres were analyzed in perfusion MRI.

Qualitative analysis of Tmax maps, using several color threshold values, showed an improvement of the chronic hypoperfusion in 28 hemispheres (90%) (Fig. 3).

Quantitative analysis:

Six months after surgery, the volume of slightly hypoperfused (Tmax > 4 s) and severely hypoperfused (Tmax > 6 s) parenchyma significantly decreased from 15.4% +/- 12.9–8.6% +/- 7.6% (p = 0.003) and from 3.6% +/- 5.6–1.2% +/- 1.7% (p = 0.004), respectively. There was no significant difference concerning the volume of critically hypoperfused parenchyma (Tmax > 8 s).

Quantitative analysis of these data showed that brain hypoperfused volumes shifted from a level of Tmax > 4 s and 6 s to lower thresholds of hypoperfusion with a Tmax < 4 s.

The volume of normally perfused parenchyma with Tmax < 2 s increased at 6 months after surgery (51.7% +/- 20.8–61.3% +/- 19.4% (p = 0.04).

We did not find any association between the improvement of hypoperfusion and preoperative Suzuki grade or revascularization defined by Matsushima score.

The main finding of our study is that burr-hole surgery as the only revascularization technique is effective to improve MRI brain perfusion as measured with Tmax and is associated with a low rate of incident stroke/TIA during follow-up. When we started treating patients with Moyamoyas, this technique was the only one available in our center.

After discharge, the 2-year survival probability free of stroke/TIA recurrence was 85% per patient. This result is higher than those reported in medical cohorts. In 20 non-operated patients diagnosed after an ischemic event, Hallemeier et al. described a probability of survival without stroke at 2 years of 60% (16). After a first ischemic event, Kraemeer et al. reported 61.9% ischemic recurrence at one year and 80% at 5 years on European non-operated adults (17).

There is no large follow-up study of adult patients treated by burr-hole surgery except two series of 10 and 24 patients that respectively showed no recurrence during a mean follow-up of 34 months (18) and good clinical outcomes for 78.9% of patients (19). In the pediatric population, Blauwbome et al. reported that 89.1% of 64 patients were free of recurrence at 2 years with a mean follow-up of 4.2 years (20). All these data concur with the results of our study.

On the other hand, our results are in line with those using other revascularization techniques. Abla et al. reported a rate of recurrence-free survival at 3 years of 88% after direct anastomosis (21). With an indirect technique of revascularization by EDAS, Bao et al. published a 2-year survival probability free of recurrence of 90% (22).

Even if we observed a perioperative ischemic rate of 8.8%/hemisphere, MBH seemed to be a safe technique. Using the same MBH technique in adults, Zhao et al. reported a complication rate of 8.7%/hemisphere (19). These results are quite similar to other techniques and may be acceptable according to the risk of stroke recurrence reported without surgery. After direct anastomosis, Mesiwala reported a rate of 7.7% perioperative ischemic strokes per hemisphere (22). Using other indirect revascularizations or combined techniques, some authors have reported a rate of periprocedural stroke varying from 3–13% per hemisphere (23, 24, 25). Steinberg et al published results for 450 revascularization procedures, which included direct revascularization in 95.1% adults and 76.2% pediatric patients, in which the surgical morbidity rate was 3.5% and mortality was 0.7% per treated hemisphere (26). Without craniotomy, burr-hole surgery is reported to be easier than other techniques. The ischemic complication rate may not differ because the major mechanisms of perioperative ischemia in MMA is hypotension during anesthesia and vasoconstriction due to hypocapnia. This highlights the need for specialized and multidisciplinary management of these patients.

Improvement of cerebral perfusion after revascularization due to the development of anastomotic networks from the external carotid artery score may explain the decrease in stroke recurrence and the differences in ischemic recurrence between operated and non-operated patients. MBH allowed for the proper development of collaterals in our cohort since we found an improved modified Matsushima score in 79% of the hemispheres operated on. Moreover, the ischemic stroke recurrence in our cohort may not reflect the failure of burr-hole surgery. One patient had recurrence because of collapsus, which caused severe brain hypoperfusion, and the 2 others presented worsening of the disease with the impairment of other arteries. Collaterals through burr hole aimed to improve cerebral perfusion. Using perfusion MRI with Tmax measurement, we demonstrated a decrease in the volume of hypoperfused parenchyma. Visual qualitative analysis of Tmax maps showed improved perfusion in 90% of hemispheres six months after surgery. Previously, using SPECT, Sainte Rose et al. demonstrated similar improvement of cerebral hemodynamics after MBH surgery in children (27). Using perfusion CT scan or monophotonic emission tomography, Liu et al. described improved brain perfusion in 73.2% of hemispheres after direct or combined surgery (28). Cerebral perfusion MRI improved 65% of hemispheres in a South Korean study performing EDAS (29). Quantitative analysis of Tmax volume with a standardized threshold every 2 s confirmed and precised the decrease of hypoperfused parenchyma. In acute ischemia, Tmax > 6 s is used to identify parenchyma suffering from critical hypoperfusion and at a high risk of evolving toward infarction. This threshold is now used in some conditions to select patients for thrombectomy (30). In patients with chronic hypoperfusion, including moyamoya, a 4 to 6 s threshold has been associated with chronic cerebral hypoperfusion lower than 20 mL/100 g/min on XeCT (12). In this study, the Tmax parameter appeared to be more reliable than MTT or CBF to assess hypoperfusion. To our knowledge, no study has evaluated MRI Tmax as a surrogate for ischemic risk or revascularization impact on hypoperfusion in a chronic situation, as encountered in MMA. A recent study using ASL showed improvement of absolute and normalized CBF after direct revascularization (31). Our findings concur with this study’s results. We demonstrated a decrease in the volumes of slightly (Tmax > 4 s) and severely (Tmax > 6 s) hypoperfused parenchyma. This redistribution of severely hypoperfused values of Tmax to hypoperfused values below 4 s highlighted the reversibility of hypoperfusion after surgery. Thus, it may be relevant to set hypoperfusion thresholds > 4 s so that it is possible to act and prevent the stroke risk in MMA. MR perfusion imaging using automatized Tmax measurement of the brain parenchyma volume may be an interesting noninvasive monitoring tool to identify perfusion changes after revascularization in patients with MMA. Contrary to other techniques such as XeCT, PWI-MR is a simple method, available in many centers, free of radiation and easily reproducible, with a short acquisition time, already widely used in stroke cases.

Our study suffers from several limitations. Firstly, the results have to be considered with caution because of the small sample size and the monocentric design. Second, we were not able to segment the perfusion analysis by brain areas to establish a correlation between the location of collateral development and focal perfusion improvement. Third, we did not study the efficacy of surgery on vascular reserve. Finally, the population was selected, composed of patients with mainly frontal hypoperfusion treated by burr-hole surgery. Thus, the generalization of our results to other techniques has to be cautious.

This study does not aim to demonstrate the superiority of the burr hole technique over other techniques. We especially wanted to show the effects of this technique on improving cerebral perfusion. The bibliography is often unclear on the superiority of one technique over others. Today, it seems that the direct technique by temporo-sylvian anastomosis combined with an indirect technique is the most complete revascularization technique, offering the advantages of both techniques. Today, it is also the technique that we choose in first intention in our center to treat our new patients with Moyamoya disease.

In a population of adults with MMA and predominant frontal hypoperfusion, MBH surgery improves frontal cerebral perfusion assessed on perfusion MRI. The long-term risk of incident ischemic event seems low, suggesting that this improvement of perfusion is effective to prevent new cerebrovascular events. Nevertheless MBH was associated with a significant rate of periprocedural cerebral infarction, similar to other revascularization techniques. Burr-hole surgery may be considered as surgical option in adults with MMA.

Ethical Approval

Retrospective study

Competing interests

No competing interests

Authors' contributions

PB and LC wrote the main manuscript. SB and JCS were the neurosurgeon who treated the patients. CC, JD and FB were the radiologist who performed the arteriography and perfusion MRI. JFA, JMO, NR and AV were the neurologist who follow the patients. CM made the angiographic analysis. All other authors reviewed the maniscript

Funding

No funfing

Availability of data and materials

All data used in this study were found in patients' medical records

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No competing interests reported.

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Effects of burr-hole surgery on MRI cerebral perfusion and stroke risk in adults with moyamoya angiopathy

Status:

Version 1

Abstract

Figures

Introduction

Material and methods

Study design:

Population

Surgical modalities:

Clinical Data collection:

Follow-up:

Radiological data collection:

DSA :

Perfusion imaging acquisition and analyses:

Ethical considerations:

Statistical analysis:

Results

Patients:

`

Surgical treatment:

Clinical follow-up:

Radiological outcome:

Angiographic follow-up

Perfusion analysis

Quantitative analysis:

Discussion

Conclusion

Declarations

References

Additional Declarations

Status:

Version 1