Predictors of dura-brain neoangiogenesis after combined revascularization for patients with symptomatic atherosclerotic cerebral artery occlusion: A multivariate regression analysis

doi:10.21203/rs.3.rs-4857974/v1

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Predictors of dura-brain neoangiogenesis after combined revascularization for patients with symptomatic atherosclerotic cerebral artery occlusion: A multivariate regression analysis

https://doi.org/10.21203/rs.3.rs-4857974/v1

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Background

The predictors of the efficacy of indirect revascularization in nonmoyamoya patients have not been determined. Our study was designed to investigate the independent predictors of dura-brain neoangiogenesis (DBN) after superficial temporal artery-to-middle cerebral artery (STA-MCA) bypass combined with dural inversion (DI) in patients with symptomatic atherosclerotic cerebral arterial occlusion (SACAO).

Methods

We retrospectively analyzed SACAO patients who had undergone STA-MCA bypass combined with DI at our center between November 2014 and October 2021. DBN was evaluated by super-selective digital subtraction angiography and scored by the DBN scoring system. Independent predictors of DBN were identified by multivariate logistic regression analysis. The differences in clinical outcomes between patients with “good” and “poor” DBN were also analyzed.

Results

A total of 179 SACAO patients with an average age of 61.3 ± 7.0 years and an average follow-up of 63.0 ± 22.0 months were studied. Ninety-nine patients (55.3%) had good DBN, and 80 patients (44.7%) had poor DBN. Multivariate analysis revealed that old age (p < 0.001, OR [95% CI] 1.288 [1.184–1.400]) was an independent predictor of poor DBN, with an optimal cutoff of 64.5 years. Diabetes (p = 0.005, OR [95% CI] 3.358 [1.434–7.867]) also independently predicted poor DBN. The recurrence rate of ischemic events in the good DBN group was significantly lower than that in the poor DBN group (2.0% vs. 10.0%, p = 0.044). The neurological status of patients in the good DBN group was significantly better than that of patients in the poor DBN group.

Conclusion

Old age and diabetes status were found to be independent predictors of poor DBN after combined revascularization in SACAO patients. Good DBN was associated with a lower recurrence rate of stroke and better neurological status. Future studies are needed to clarify the underlying pathophysiological mechanisms involved.

atherosclerosis

cerebral artery occlusion

dura-brain neoangiogenesis

indirect revascularization

multivariate logistic regression analysis

stroke

Although there are no trials showing that extracranial-to-intracranial (EC-IC) bypass is definitely beneficial for patients with symptomatic atherosclerotic cerebral arterial occlusion (SACAO), the most recent randomized clinical trial suggested that not only did EC-IC bypass combined with medical therapy have efficacy comparable to that of medical therapy alone but also that the risk of ipsilateral ischemic stroke beyond 30 days through 2 years in the surgical group was significantly lower than that in the medical group. This result indicated that the extra blood perfusion brought by bypass grafts may be beneficial for reducing the long-term stroke rate, and subsequently, EC-IC bypass could be a potential option for SACAO patients.(1–4) Moreover, recent studies have suggested that dural inversion (DI), an indirect revascularization method, can also significantly increase cerebral blood flow in SACAO patients.(5–7) Combined with the recent research on the efficacy of combined revascularization surgery,(8, 9) we speculate that, direct EC-IC bypass combined with DI has the potential to be an ideal surgical strategy for supplementing cerebral blood perfusion (CBP) in patients with SACAO.

Implementation of DI during direct EC-IC bypass is relatively simple and convenient.(8, 9) However, the risk of subdural hemorrhage caused by covering the vessel-rich layer of dura mater (DM) on the brain surface and by the larger DM opening resulting from DI cannot be ignored.(10) It must also be considered that indirect revascularization is reported to be effective in only approximately half of adult patients.(11, 12) Therefore, it is crucial to understand the potential predictors of dura-brain neoangiogenesis (DBN) in DI patients to determine which SACAO patients may benefit from this procedure.

Therefore, we retrospectively studied patients with SACAO, including both internal carotid artery occlusion (ICAO) and middle cerebral artery occlusion (MCAO), who were treated with superficial temporal artery-to-middle cerebral artery (STA-MCA) bypass combined with DI at our center between November 2014 and October 2021. We used multivariate logistic regression analysis to explore the independent predictors of DBN to help neurosurgeons predict the effect of DI on SACAO patients before surgery. Based on this, neurosurgeons can selectively perform DI on patients who may substantially benefit from this procedure. Conversely, for patients for whom DBN is predicted to be poor, neurosurgeons may choose not to perform DI during STA-MCA bypass, minimizing the need for DM manipulation and reducing the risk of postoperative subdural hematoma. To our knowledge, no similar reports have been published.

Patient Selection

A retrospective analysis of consecutive SACAO patients treated with STA-MCA bypass combined with DI between November 2014 and October 2021 at our center was conducted. The exclusion criteria were as follows: 1) young age with no underlying atherosclerosis-related diseases or atherosclerosis-related risk factors (e.g., moyamoya disease (MMD), inflammation or an unknown etiology); 2) coincident occlusion or moderate to severe stenosis of another cerebral artery; 3) previous treatment with another revascularization surgery; 4) history of head or neck radiation therapy; 5) postoperative complications (either hemorrhagic or ischemic complications) < 30 days after surgery; 6) STA-MCA bypass occlusion revealed by computed tomography angiography (CTA) or digital subtraction angiography (DSA); or 7) follow-up (FU) period < 2 years or loss to FU. The human ethics of this study was approved by the Ethics Committee of the Third Affiliated Hospital of Sun Yat-sen University (No. SL-II2024-091-02) and was performed in accordance with the ethical standards established by the 1964 Declaration of Helsinki and its later amendments. Written informed consent was obtained, and the patients consented to the publication of their images.

Surgical Indications

The surgical indications were as follows: 1) < 75 years of age; 2) symptoms of ischemia occurring in the last 6 months, including transient ischemic attack (TIA), aphasia, and minor ischemic stroke (including limb numbness and hemiplegia), with or without dizziness and headache; 3) symptoms believed to be caused by hypoperfusion resulting from SACAO while receiving antiplatelet and statin therapy; 4) a modified Rankin scale (mRS) score ≤ 2 and a National Institute of Health Stroke Scale (NIHSS) score ≤ 3 on admission;(13, 14) and 5) computed tomography perfusion (CTP) images showing a ratio of ipsilateral/contralateral mean transit time (I/C MTT) in the posterior part of the inferior frontal gyrus > 1.13.(15)

Surgical Procedures

Hypertension, diabetes, and hyperlipidemia were corrected preoperatively when necessary. Aspirin (100 mg/d) and atorvastatin (20 mg/d) were prescribed at least 5 days prior to surgery. The patient was placed in the supine position, and general anesthesia was administered. After the skin was incised, a triangular opening was created for craniotomy. Then, the DM was opened radially to create 6 flaps in total (2 flaps on each side), and all the DM flaps were inverted to the subdural space. Maintaining the main trunk of the meningeal middle artery (MMA) while opening the DM was recommended. After STA-MCA bypass was performed, the DM opening was covered with gel foam. Finally, the bone flap was fixed, and the incision was closed (Fig. 1). Patients continued to take aspirin (100 mg/day) throughout their lifetime after surgery.

Assessment of DBN and Direct Bypass

The revascularization effect was evaluated according to DSA results 2 years after surgery. During DSA, superselective angiography was performed on the STA and MMA. In the assessment of DBN, if any degree of neoangiogenesis was observed between a certain inverted DM flap and its covered brain tissue, 1 point was recorded, and 0 points were recorded if no neoangiogenesis was found. For each patient, the DM was cut relatively equally into 6 flaps, and each flap was inverted independently; thus, the DBN score ranged from 0 to 6 points. We defined good DBN as 4 to 6 points and poor DBN as 0 to 3 points (Fig. 2). A neurosurgeon (C.T.), a neurologist (L.W.), and a radiologist (Y.Y.) reviewed the DSA imaging data together to calculate the DBN score. All three doctors were attending physicians and worked for more than 10 years. The rating is based on the majority opinion. The effect of STA-MCA bypass was assessed by the Matsushima classification, as follows: Grade A, more than two-thirds of the MCA supplying distribution was filled; Grade B, one-third to two-thirds filled; and Grade C, less than one-third filled.(16)

Follow-up Protocol

CTA (combined with CTP sequence) was performed on postoperative day 1 and postoperative day 180 (outpatient FU). DSA was also performed 2 years after surgery to assess DBN and the patency of the STA-MCA bypass. The mRS score were used to assess the patients’ neurological status. When recurrent ischemic stroke was suspected, magnetic resonance angiography plus diffusion-weighted imaging was performed to rule out the possibility of new cerebral infarctions.

Statistical Analysis

Student’s t test was used to compare the continuous variables. The Pearson Chi-square test or Fisher’s exact test was used to analyze the enumeration data. The Mann‒Whitney test was used to compare the mRS scores between the different groups. Multivariate logistic regression analysis was also conducted on factors for which P < 0.05 was achieved in the univariate analysis and factors that were considered highly likely to be related to the outcome of DBN according to clinical experience (i.e., hypertension, hyperlipidemia and occlusion artery). Odds ratios (ORs) and 95% confidence intervals (CIs) for good neoangiogenesis were calculated. P < 0.05 was considered indicative of statistical significance. The data were analyzed using SPSS, version 25.0.

Demographic Data

After exclusion of patients according to the exclusion criteria, 179 patients with SACAO who were treated with STA-MCA bypass combined with DI between November 2014 and October 2021 were selected for this study (Fig. 3). The patient characteristics are listed in Table 1. A total of 99 men and 80 women were included in this study, with an average age of 61.3 ± 7.0 years. The onset symptoms included dizziness (18.4%), headache (19.0%), TIA (37.4%), amaurosis fugax (5.0%), aphasia (12.8%), limb numbness (24.6%) and hemiplegia (22.3%). The duration from first onset to surgery was 91.6 ± 49.1 days. ICAO occurred in 71 patients (39.7%), and the other patients (60.3%) had MCAO. Revascularization surgery was performed on the left side in 98 (54.7%) patients. The preoperative I/C MTT ratio in this cohort averaged 1.24 ± 0.03.

Table 1

Demographic data and clinical characteristics
	Value
No. of patients	179
Age, years	61.3 ± 7.0
Sex, male	99 (55.3%)
Hypertension	126 (70.4%)
Diabetes	62 (34.6%)
Hyperlipidemia	90 (50.3%)
Smoking	89 (49.7%)
Alcohol	36 (20.1%)
Onset Symptoms
Dizzy	33 (18.4%)
Headache	34 (19.0%)
Amaurosis fugax	9 (5.0%)
Transient ischemic attack	67 (37.4%)
Aphasia	23 (12.8%)
Limb numbness	44 (24.6%)
Hemiplegia	40 (22.3%)
Duration from first onset to surgery, days	91.6 ± 49.1
Occlusion artery
ICAO	71 (39.7%)
MCAO	108 (60.3%)
Occlusion side, left	98 (54.7%)
I/C MTT Ratio	1.24 ± 0.03
mRS score
0	30 (16.8%)
1	89 (49.7%)
2	60 (33.5%)
≥ 3	0 (0%)
NIHSS score
0	25 (14.0%)
1	64 (35.8%)
2	71 (39.6%)
≥ 3	19 (10.6%)

No., number; ICAO, internal carotid artery occlusion; MCAO, middle cerebral artery occlusion; I/C MTT, ipsilateral/contralateral mean transit time; mRS, modified Rankin scale; NIHSS, National Institute of Health Stroke Scale

The FU information is listed in Table 2. The average FU period was 63.0 ± 22.0 months. A total of 169 patients (94.4%) were free of ischemic events beyond 30 days through the FU period. The I/C MTT ratio on day 180 averaged 1.08 ± 0.04, which was significantly lower than the preoperative I/C MTT ratio (p < 0.001). The effect of STA-MCA bypass reached Matsushima grade B in 72 patients (40.2%) and Matsushima grade C in 107 patients (59.8%). No patients reached Matsushima grade A. There were 99 patients (55.3%) who had good DBN (DBN score ranging from 4–6), and the other 80 patients (44.7%) had poor DBN (DBN score ranging from 0–3). The neurological status (mRS score) at the last FU was significantly better than that before surgery (p < 0.001).

Table 2

Follow-up information
	Value
Follow-up period, months	63.0 ± 22.0
Recurrent cases of ischemic events (> 30 days)	10 (5.6%)
I/C MTT Ratio on day 180	1.08 ± 0.04
Matsushima grade of STA-MCA bypass
Grade A	0 (0%)
Grade B	72 (40.2%)
Grade C	107 (59.8%)
DBN score
0	4 (2.2%)
1	14 (7.8%)
2	25 (14.0%)
3	37 (20.7%)
4	46 (25.7%)
5	36 (20.1%)
6	17 (9.5%)
mRS score
0	42 (23.5%)
1	83 (46.4%)
2	49 (27.4%)
≥ 3	5 (2.8%)

I/C MTT, ipsilateral/contralateral mean transit time; STA, superficial temporal artery; MCA, middle cerebral artery; DBN, dura-brain neoangiogenesis; mRS, modified Rankin scale

Potential Predictors of DBN

The patients were categorized into two subgroups according to DBN status. Univariate analysis was used to initially identify the factors significantly related to the outcome of neoangiogenesis. The results showed that old age, smoking status and diabetes status were significantly related to poor neoangiogenesis (p < 0.001, p = 0.042 and p = 0.001, respectively). The extent of preoperative CBP impairment was significantly correlated with the outcome of neovascularization; that is, a higher I/C MTT ratio predicted better DBN (p = 0.039).

To further rule out the effects of various factors, multivariate analysis was conducted (Table 3). Old age (p < 0.001, OR [95% CI] 1.288 [1.184–1.400]) was identified as an independent predictor of poor DBN after indirect bypass surgery, and according to the results of the receiver operating characteristic (ROC) curve (Fig. 4), the optimal cutoff value for age was 64.5 years. Diabetes (p = 0.005, OR [95% CI] 3.358 [1.434–7.867]) also independently predicted poor DBN.

Table 3

Logistic regression analysis of potential predictors of DBN after combined revascularization
	DBN			P Value
	Good (n = 99)		Poor (n = 80)	Univariate	Multivariate	OR (95% CI)
Age, years (per 1 year)	58.1 ± 6.9	65.3 ± 4.7		< 0.001*	< 0.001*	1.288 (1.184-1.400)
Sex, male	50 (50.5%)	49 (61.3%)		0.151	/
Hypertension	67 (67.7%)	59 (73.8%)		0.376	0.446
Diabetes	24 (24.2%)	38 (47.5%)		0.001*	0.005*	3.358 (1.434–7.867)
Hyperlipidemia	52 (52.5%)	38 (61.3%)		0.504	0.397
Smoking	42 (42.4%)	47 (58.8%)		0.042*	0.052
Alcohol	19 (19.2%)	17 (21.3%)		0.732	/
Duration from first onset to surgery, days	93.2 ± 48.9	86.6 ± 49.5		0.627	/
Occlusion artery				0.595	0.848
ICAO	41 (41.4%)	30 (37.5%)
MCAO	58 (58.6%)	50 (62.5%)
Occlusion side, left	59 (59.6%)	49 (61.3%)		0. 822	/
I/C MTT Ratio	1.23 ± 0.03	1.24 ± 0.03		0.039*	0.412
mRS score (per 1)				0.317	/
0	19 (19.2%)	11 (13.6%)
1	49 (49.5%)	40 (50.0%)
2	31 (31.3%)	29 (36.4%)
≥ 3	0 (0%)	0 (0%)
DBN, dura-brain neoangiogenesis; OR: odds ratio; ICAO, internal carotid artery occlusion; MCAO, middle cerebral artery occlusion; I/C MTT, ipsilateral/contralateral mean transit time; mRS, modified Rankin scale

Long-Term Outcomes with Different DBN Conditions

The long-term outcomes of patients with different neoangiogenesis conditions are shown in Table 4. There was no significant difference in the FU duration between the two groups (p = 0.611). The I/C MTT ratios and Matsushima grades of the STA-MCA bypass did not significantly differ between the two groups (p = 0.241, p = 0.879, respectively). However, the recurrence rate of ischemic events in the good DBN group was significantly lower than that in the poor DBN group (p = 0.044). The neurological status (mRS score) was significantly better in the good DBN group than in the poor DBN group (p = 0.012).

Table 4

Long-term outcomes of patients with good and poor DBN
	Good DBN (n = 99)	Poor DBN (n = 80)	P Value
Follow-up period, months	66.9 ± 22.4	58.1 ± 20.7	0.611
I/C MTT ratio	1.08 ± 0.04	1.09 ± 0.04	0.241
Recurrence rate of ischemic event (> 30 days)	2 (2.0%)	8 (10.0%)	0.044*
Matsushima grade of STA-MCA bypass			0.879
Grade A	0 (0%)	0 (0%)
Grade B	41 (41.4%)	32 (40.0%)
Grade C	58 (58.6%)	48 (60.0%)
mRS score			0.012*
0	30 (30.3%)	12 (15.0%)
1	45 (45.5%)	38 (47.5%)
2	21 (21.2%)	28 (35.0%)
≥ 3	3 (3.0%)	2 (2.5%)

DBN, dura-brain neoangiogenesis; I/C MTT, ipsilateral/contralateral mean transit time; STA, superficial temporal artery; MCA, middle cerebral artery; mRS, modified Rankin scale

To our knowledge, the present study is the first specific study focusing on the independent predictors of DBN after combined revascularization in SACAO patients. Our study included factors very likely to be related to the outcome of indirect bypass in previous studies or according to clinical experience, and the results indicated that old age and diabetes were independent predictors of poor DBN. The conclusion of this study is helpful for neurosurgeons to selectively perform DI on SACAO patients who are expected to have good DBN according to these independent predictors. A detailed discussion is presented below.

Independent Predictors of DBN in SACAO Patients

Indirect revascularization is most widely performed on MMD patients. Evidence-based medicine has shown that not only is the indirect revascularization effect significantly better in pediatric MMD patients than in adult MMD patients but also that younger age is an independent predictor of good indirect neoangiogenesis in adult MMD patients. In addition, J. R. Dusick's research showed that indirect revascularization could also achieve ideal anastomosis in young patients (38.5 ± 8.6 years in his study) with nonmoyamoya disease.(6) The above studies suggested that the younger the patient is, the greater the potential for intracranial-extracranial neoangiogenesis is. However, this perspective has not been indicated for SACAO patients. Considering that most SACAO patients are middle-aged or elderly, their age of onset is in a much narrower range than that of MMD patients. Therefore, the influence of age on neoangiogenesis in SACAO patients is usually overlooked. Our results showed that in SACAO patients, 55.3% (99/179) achieved good DBN, and old age was an independent predictor of poor DBN (the optimal cutoff value was 64.5 years). This result indicated that in SACAO patients, indirect revascularization procedures can also play an important role as long as there is a need to supplement cerebral blood perfusion to the ischemic brain. Moreover, the efficacy of indirect revascularization is better in younger SACAO patients. However, the mechanism of the impact of age on DBN is still unclear. It is probably related to the Netrin-1 signaling insufficiency.(19)

Diabetes is one of the confirmed risk factors for atherosclerosis,(1, 17, 18) and the proportion of patients with diabetes among SACAO patients (21.0-38.8%) is greater than that among MMD patients (2.6–13.1%).(19, 20) A total of 34.6% of the SACAO patients in our study had diabetes, and clinically, SACAO patients with diabetes tended to have a worse cortex arterial network on DSA images. Therefore, diabetes was listed as one of the influencing factors that needed to be analyzed. Our results showed that diabetes was an independent predictor of poor DBN, which meant that the DI could achieve a better effect in SACAO patients who were not diagnosed with diabetes. The results of previously published basic studies have revealed that diabetes might induce pathological changes such as oxidative stress and endoplasmic reticulum stress, which are not conducive to the proliferation of vascular endothelial cells.(21–23) Moreover, Yamaguchi's research showed that diabetes was an independent predictor of poor graft development after direct revascularization in SACAO patients.(18) The results of the above studies could explain and support our conclusion that diabetes has a negative impact on DBN.

In addition, we believe that postoperative hemorrhage (whether intracerebral or subdural hemorrhage) or infarction may also be a potential factor affecting postoperative DBN despite the lack of current evidence-based medical evidence to support this view. However, the main focus of this study is the impact of patient characteristics on DBN. Therefore, we excluded 12 patients who experienced hemorrhage (4 cases) and infarction (8 cases) within 30 days after surgery. This will be the focus of subsequent research.

The Potential Influences of Combined STA-MCA Bypass

Since blood flow was supplemented in the SACAO patients in this study by both STA-MCA bypass and DBN, we speculated that there might be an inverse relationship between these two factors. This was the reason for our analyzing the relationship between the Matsushima grade of STA-MCA bypass and DBN status. However, the results revealed that better DBN was not associated with a worse Matsushima grade for STA-MCA bypass (p = 0.879), which indicated that the DBN status did not correlate with the blood flow supplement provided by STA-MCA bypass. In addition, our results showed that patients with good DBN had a better prognosis than patients with poor DBN; however, there was no significant difference in postoperative CBP between the two groups (p = 0.611). The reason may be that 1) DBN was able to provide blood flow supplementation to protect a larger area of the cerebral cortex than was the STA-MCA bypass, which may be more essential for preventing symptomatic stroke, and 2) the difference in postoperative CBP improvement caused by DBN between these two groups was probably diluted by the effect of the blood supply provided by the combined STA-MCA bypass in both groups.

The DBN Scoring System

The Matsushima standard is usually used to evaluate overall blood flow supplementation during surgical revascularization. However, in our study, we needed an evaluation system to assess the efficacy of DI surgery along the three sides of the triangular opening created for craniotomy, involving consideration of a local effect after subtracting the blood flow supplementation of STA-MCA bypass from the overall surgical revascularization. If possible, the evaluation system would have to fit the way we cut and inverted the DM. Therefore, the Matsushima standard was not applicable to the SACAO patients in the present study. Based on this, we proposed the DBN scoring system. Given that the DM was cut radially into six equal flaps during surgery, we took the three sides of the triangular opening created for craniotomy on the DSA image as the reference, and we used superselective angiography to confirm whether there was any degree of DBN in the area covered by each DM flap (Fig. 5). Considering that the area of each DM flap is small and that the degree of DBN generated from each DM flap is limited, we did not use a more detailed scoring system to determine the degree to which DBN was generated from each DM flap. We believe that such a DBN scoring system is more suitable for assessing the efficacy of DI therapy in our research than the Matsushima standard.

Limitations

The current study has a few limitations. First, the study was limited by its single institution, retrospective design; thus, potential selection bias and possible confounding factors cannot be excluded. Second, due to the similar stroke-related risk factors and surgical procedures, both ICAO patients and MCAO patients were included in this study. However, the different compensation patterns for these two kinds of patients may bias the results. Third, considering the fine condition of cortical arteries in SACAO patients and according to the latest clinical consensus,(1) performing indirect revascularization alone does not appear to be ethical for SACAO patients. The blood supply provided by combined STA-MCA bypass may have some impact on the degree of DBN.

Old age and diabetes status were found to be independent predictors of poor DBN after combined revascularization in SACAO patients. Good DBN was associated with a lower stroke recurrence rate and better neurological status. These considerations are important for neurosurgeons when choosing DI candidates among SACAO patients undergoing direct bypass.

CBP: cerebral blood perfusion,

CIs: confidence intervals,

CTA: computed tomography angiography,

CTP: computed tomography perfusion,

DBN: dura-brain neoangiogenesis,

DI: dural inversion,

DM: dura mater,

DSA: digital subtraction angiography,

EC-IC: extracranial-to-intracranial,

FU: follow-up,

ICAO: internal carotid artery occlusion,

I/C MTT: ipsilateral/contralateral mean transit time,

MCAO: middle cerebral artery occlusion,

MMA: meningeal middle artery,

MMD: moyamoya disease,

mRS: modified Rankin scale,

NIHSS: National Institute of Health Stroke Scale,

ORs: Odds ratios,

SACAO: symptomatic atherosclerotic cerebral arterial occlusion,

STA-MCA: superficial temporal artery-to-middle cerebral artery,

TIA: transient ischemic attack.

Ethics approval and consent to participate

This study was approved by the Ethics Committee of the Third Affiliated Hospital of Sun Yat-sen University (No. SL-II2024-091-02) and was performed in accordance with the ethical standards established by the 1964 Declaration of Helsinki and its later amendments. Written informed consent to participate was obtained from all the patients.

Consent for publication

Written informed consent to participate was obtained from all the patients, and the patients consented to the publication of their images.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

This work was supported by Guangzhou Key Research and Development Program [grant number 2023B03J0191]; and by Research Project of Yuedong Hospital, the Third Affiliated Hospital of Sun Yat-sen University [grant number YDC2022001].

Authors' contributions

C.L.: Writing – original draft, Formal analysis, Methodology; N.M.: Writing – original draft, Formal analysis, Methodology; B.Z.: Writing – original draft, Formal analysis, Methodology; C.T.: Writing – review & editing, Data curation; Y.Y.: Writing – review & editing, Data curation; L.W.: Writing – review & editing, Data curation; H.W.: Writing – review & editing, Conceptualization, Supervision; C.C.: Writing – review & editing, Conceptualization, Supervision, Funding acquisition.

Acknowledgements

The authors wish to thank Qingyang Liu for the excellent technical support.

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No competing interests reported.

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Predictors of dura-brain neoangiogenesis after combined revascularization for patients with symptomatic atherosclerotic cerebral artery occlusion: A multivariate regression analysis

Status:

Version 1

Abstract

Background

Methods

Results

Conclusion

Figures

BACKGROUND

METHODS

Patient Selection

Surgical Indications

Surgical Procedures

Assessment of DBN and Direct Bypass

Follow-up Protocol

Statistical Analysis

RESULTS

Demographic Data

Potential Predictors of DBN

Long-Term Outcomes with Different DBN Conditions

DISCUSSION

Independent Predictors of DBN in SACAO Patients

The Potential Influences of Combined STA-MCA Bypass

The DBN Scoring System

Limitations

CONCLUSION

Abbreviations

Declarations

References

Additional Declarations

Status:

Version 1