One-stop hybrid operation versus microsurgery for treating brain arteriovenous malformation in children—a retrospective case series
Highlight box
Key findings
• The advantages of one-stop hybrid operation include reducing intraoperative blood loss and shortening the operation time and postoperative hospital stay.
• High Spetzler-Martin grade brain arteriovenous malformation (BAVM) is more suitable for hybrid operation.
What is known and what is new?
• Children with BAVM have a greater risk of bleeding, and there may be stronger indications for intervention in the pediatric population.
• A one-stop hybrid operation is effective and safe for the treatment of BAVM in children.
What are the implications, and what should change now?
• The application of a one-stop hybrid operating room may be the best way to provide immediate treatment by combining embolization and microsurgery in a single procedure and multidisciplinary environment.
Introduction
Brain arteriovenous malformation (BAVM) is a cerebrovascular structural developmental abnormality characterized by an abnormal connection between the arterial and venous systems, with an annual incidence of approximately 1.12–1.42 per 100,000 people; the most common manifestations are intracranial hemorrhage, epilepsy, headache, and neurological dysfunction (1-3). BAVM are considered the primary etiology of hemorrhagic stroke in children. The annual risk of hemorrhage is 6.3%, and the annual risk of rehemorrhage is 14.8% (4), which is significantly greater than the overall risk of annual hemorrhage and rehemorrhage in adults (3% and 4.5%, respectively) (5). BAVM are found in 35–55% of children with hemorrhagic stroke and are associated with significant mortality and morbidity (6,7). Overall, the average mortality rate over the past 40 years reached 25%, decreasing from 39% to 16% during this period, which is consistent with technological progress (8). With an inherent long-life expectancy, even in patients with unruptured BAVM, there may be stronger indications for intervention in the pediatric population. A previous study showed pediatric and adolescent patients are prone to develop recurrent AVMs, even after complete AVM obliteration verified by angiography (9).
The primary goal of BAVM treatment is angiographic cure, which is the abolition of arteriovenous shunting with no or minimal risk. Multidisciplinary methods with flexibility and expertise may improve patient outcomes and reduce morbidity and mortality (10,11). The combination of embolization and microsurgery can effectively improve the obliteration rate and reduce complications. Kinouchi et al. (12) recommended microsurgery several days or weeks after embolization, when the angioarchitecture and hemodynamic changes in the peripheral vessels surrounding the BAVM nidus stabilize. This staged treatment can reduce the chance of normal perfusion pressure breakthrough after surgery. However, the incidence of various complications, such as hemorrhage caused by rapid hemodynamic changes, epileptic seizures, or neurological dysfunction, can reach up to 3–8% during the interval between embolization and microsurgery (12-15). The risk of BAVM rupture during the perioperative period is as high as 4–16% (16). Therefore, the application of a one-stop hybrid operating room (hOR) may be the best way to provide immediate treatment by combining embolization and microsurgery in a single procedure and multidisciplinary environment (17,18). The extent of BAVM obliteration can be observed immediately after a hybrid operation. One-stop hOR is often used for the treatment of adult BAVM, while it is rarely used for the treatment of pediatric BAVM. The aim of this study was to retrospectively analyze the clinical data and short-term prognosis of pediatric cerebral BAVM and compare the short-term prognosis and safety of hOR and microsurgery in the treatment of pediatric cerebral BAVM. We present this article in accordance with the AME Case Series and STROBE reporting checklists (available at https://tp.amegroups.com/article/view/10.21037/tp-24-68/rc).
Methods
Patients and study design
Patients aged 1–18 years who underwent BAVM treatment at The 900th Hospital and Fujian Children’s Hospital between September 2018 and August 2022 were included. A total of 57 children with cerebral vascular malformations were treated. According to the inclusion and exclusion criteria, patients with cerebrovascular malformation but not BAVM or with inadequate clinical data or receiving monotherapies of embolization were excluded. Thirty-eight patients met the inclusion criteria, including 25 patients in the microsurgical group and 13 patients in the hybrid operation group (Figure 1). BAVM were diagnosed using digital subtraction angiography (DSA), magnetic resonance angiography (MRA), or computed tomography angiography (CTA) and graded by the Spetzler-Martin (S-M) grading system. The following patient data were recorded: age, sex, headache status, neurological dysfunction status, Glasgow Coma Scale (GCS) score and Hunt-Hess score (H-H score) at the time of admission. Informed written consent was obtained from the patients’ parents and/or legal guardians. This study was performed in accordance with the principles of the Declaration of Helsinki (as revised in 2013). Approval was granted by the Ethics Committee of Fujian Children’s Hospital (No. 2023ETKLR05084), and The 900th Hospital was informed and agreed with the study.
![Click on image to zoom](http://cdn.amegroups.cn/journals/amepc/files/journals/6/articles/126592/public/126592-PB7-9174-R1.jpg/w300)
Surgical procedure
Microsurgery
The surgical incision was designed according to the preoperative images. Prior to incision, the matched blood products were prepared in the operating room, and temporary aneurysm clips were selected and loaded. Craniotomy was performed to ensure that the margins of the lesion were within the margins of the operative exposure. Once the dura was opened, dissection was performed under an operating microscope. An early identified superficial draining vein could be followed proximally to localize the nidus. Then, the major arterial feeders were coagulated and cut. Anatomical, circumferential cortical and subcortical dissection was performed with serial coagulation of the supplying arterial pedicles before the venous drainage was disconnected. If BAVM were combined with intracranial hematoma, the hematoma was usually removed to increase the exposure space before the BAVM were removed.
One-stop hybrid operation (embolization + microsurgery)
The operation was performed in the hOR. After total cerebral angiography was performed via femoral access, the feeding artery and draining vein of the BAVM were confirmed. Angiography and embolization were performed using Philippe (FD20). After general anesthesia, the right femoral artery was punctured using a suitable arterial sheath. Initially, all patients did not undergo heparinization considering that further craniotomy might be required after angiography. The decision to undergo heparinization will be made later based on the embolization situation. Specific catheters, microcatheters, microwires, and Onyx embolic agents (Covidien/ev3, Irvine, California, USA) were selected based on the preferences of the attending neurosurgeon and the characteristics of BAVM. During embolization, the deformed blood vessels were approached as closely as possible, and the tip of the microcatheter should be as close to the lesion as possible. The embolic glue was injected gradually under dynamic visualization, attempting to completely occlude the proximal drainage vein. If the BAVM could not be completely embolized or a part of the supplying arteries could not be embolized, the femoral artery sheath was retained, and then the BAVM was removed by microsurgery via craniotomy in the hOR. After the removal of the BAVM, another DSA was performed to confirm the resection results (Figure 2). Surgery was continued for those who still had residual disease.
![Click on image to zoom](http://cdn.amegroups.cn/journals/amepc/files/journals/6/articles/126592/public/126592-PB8-1912-R1.jpg/w300)
Outcome evaluation and follow-up
Outcome data, including intraoperative blood loss, operation time (only the microsurgery time was calculated for the hybrid operation group), imaging results, postoperative complications, length of hospital stay, and modified Rankin score (mRS) 3 and 6 months after the operation, were recorded. All patients were followed up for 6 months to 4 years, MRA or CTA was reexamined 1 week after the operation, and DSA was performed for imaging evaluation 3 months after the operation. Neurological functional recovery was assessed with the mRS 3 and 6 months after the operation. Immediate worsening of a pre-existing/presenting neurological deficits or pre-operative (baseline) mRS was considered a major post-embolization or post-operative complication. The final clinical outcome was considered dependent (disabling neurological deficit) if the final mRS was >2 and unfavorable if there was any increase in the baseline mRS.
Statistical analysis
The H-H score and S-M grade were classified into grade data, and Ridge analysis was adopted. Count data were expressed as case numbers, and Fisher’s exact test was used for analysis. The measurement data were expressed as the mean and standard deviation, and pairwise comparisons were conducted with two independent sets of t-tests. The operation mode was used as the dependent variable in the prediction model for the selection of the operation mode, and clinical and imaging characteristics such as sex, age, presence of headache, neurological dysfunction, GCS score, presence of intraventricular hemorrhage, location of BAVM, H-H score, and S-M grade were used as the independent variables. The logistic regression analysis method (input method and forward likelihood ratio method) was used. The inclusion and exclusion criteria were all 0.05, and single-factor analysis and multifactor analysis were performed. P≤0.05 was considered to indicate a statistically significant difference, and SPSS 26.0 software was used for statistical analysis.
Results
Clinical features of the patients and treatment complications
A total of 57 children with diagnosed BAVM were treated. According to the inclusion and exclusion criteria, 38 patients met the inclusion criteria, including 25 patients in the microsurgical group and 13 patients in the hybrid operation group (Figure 1). Male:female =21:17, age: 1–18 years old, with an average age of 9.72±4.22 vs. 10.85±4.67 years old. In terms of the clinical and imaging characteristics of the patients in the two groups, the distributions of sex, the location of the BAVM and the S-M grade were inconsistent. The proportion of female patients (P=0.04), the location of BAVM (P=0.03) and the proportion of patients with an S-M grade above 3 (P=0.003) in the hybrid operation group were significantly greater than those in the microsurgical group. There were no significant differences in age, headache, neurological impairment, GCS score, H-H score or incidence of intraventricular hemorrhage between the two groups (Table 1). In the microsurgical group, three neurological complications were observed (12/25, 48%). In the hybrid operation cohort, 4 postsurgical neurological deficits/seizures (4/9, 44%) occurred.
Table 1
Characteristic | Microsurgery (n=25) | Hybrid operation (n=13) | Sum | χ2/Hc value | P value |
---|---|---|---|---|---|
Gender | 0.04 | ||||
Female | 8 | 9 | 17 | ||
Male | 17 | 4 | 21 | ||
Age, years | 9.72±4.22 | 10.85±4.67 | 0.46 | ||
Headache | 0.50 | ||||
No | 11 | 4 | 15 | ||
Yes | 14 | 9 | 23 | ||
GCS | 12.68±3.44 | 12.38±3.23 | 0.256 | 0.80 | |
Neurological impairment | >0.99 | ||||
No | 15 | 8 | 23 | ||
Yes | 10 | 5 | 15 | ||
Intraventricular hemorrhage | 0.49 | ||||
No | 12 | 4 | 16 | ||
Yes | 13 | 9 | 22 | ||
BAVM location | 0.03 | ||||
Supratentorial | 17 | 13 | 30 | ||
Infratentorial | 8 | 0 | 8 | ||
H-H score | 1.476 | 0.22 | |||
1 | 1 | 0 | 1 | ||
2 | 8 | 3 | 11 | ||
3 | 10 | 4 | 14 | ||
4 | 5 | 6 | 11 | ||
5 | 1 | 0 | 1 | ||
S-M grade | 8.941 | 0.003 | |||
1 | 8 | 0 | 8 | ||
2 | 9 | 2 | 11 | ||
3 | 6 | 8 | 14 | ||
4 | 1 | 3 | 4 | ||
5 | 1 | 0 | 1 |
Data are presented as number or mean ± standard deviation. GCS, Glasgow Coma Scale; BAVM, brain arteriovenous malformation; H-H, Hunt-Hess; S-M, Spetzler-Martin.
Prognostic analysis of patients undergoing different surgical procedures
All patients were treated with microsurgery or a hybrid operation. In the hybrid operation group, only the operation time of microsurgery was calculated. Postoperative complications included intracranial or incisional infection, epilepsy, and hydrocephalus. There were no deaths. An imaging cure was confirmed by MRA, CTA or DSA, which revealed no abnormal vascular mass after the operation. The statistical results showed that the intraoperative blood loss (P<0.001), operation time (P<0.001) and postoperative hospital stay (P=0.02) of patients in the microsurgical group were greater than those in the hybrid operation group. There was no significant difference between the two groups in terms of postoperative imaging resolution, postoperative complications, or neurological function 3 or 6 months after the operation (Table 2).
Table 2
Characteristic | Microsurgery (n=25) | Hybrid operation (n=13) | t value | P value |
---|---|---|---|---|
Intraoperative blood loss (mL) | 190.00±55.90 | 110.00±31.09 | 4.770 | <0.001 |
Operation time (min) | 137.40±17.51 | 109.23±8.38 | 5.459 | <0.001 |
Postoperative hospital stay (d) | 22.88±8.42 | 16.85±5.10 | 2.359 | 0.02 |
Postoperative imaging cure | 0.60 | |||
Yes | 23 | 11 | ||
No | 2 | 2 | ||
mRS (3 months after operation) | 0.49 | |||
≤2 | 16 | 10 | ||
>2 | 9 | 3 | ||
mRS (6 months after operation) | >0.99 | |||
≤2 | 22 | 12 | ||
>2 | 3 | 1 | ||
Postoperative complication | 0.49 | |||
Yes | 12 | 4 | ||
No | 13 | 9 |
Data are presented as number or mean ± standard deviation. mRS, modified Rankin score.
Prediction model for surgical approach selection
Univariate logistic regression analysis revealed that the presence of neurological dysfunction (P=0.03) and the S-M grade (P=0.047) may be relevant factors for predicting the surgical approach (Table 3). The results of multivariate analysis showed that the probability of patients choosing the hybrid operation was 3.046 times greater than that of microsurgery for each higher S-M grade, indicating that the higher the S-M grade was, the greater the probability of choosing the hybrid operation (Table 4).
Table 3
Predictor | Estimate | S.E. | χ2 value | df | P value | OR | 95% CI | |
---|---|---|---|---|---|---|---|---|
Lower | Upper | |||||||
Gender | −1.618 | 1.441 | 1.260 | 1 | 0.26 | 0.198 | 0.012 | 3.343 |
Age | 0.195 | 0.159 | 1.507 | 1 | 0.22 | 1.216 | 0.890 | 1.660 |
Headache | 0.665 | 1.774 | 0.140 | 1 | 0.71 | 1.944 | 0.060 | 62.884 |
Signs | −5.008 | 2.250 | 4.951 | 1 | 0.03 | 0.007 | 0.000 | 0.551 |
GCS score | 0.308 | 0.515 | 0.358 | 1 | 0.55 | 1.360 | 0.496 | 3.730 |
Intraventricular hemorrhage | −1.248 | 1.399 | 0.795 | 1 | 0.37 | 0.287 | 0.019 | 4.457 |
Location of malformed vascular mass | −22.604 | 11,812.866 | 0.000 | 1 | >0.99 | 0.000 | 0.000 | |
H-H score | 3.120 | 1.755 | 3.159 | 1 | 0.08 | 22.638 | 0.726 | 706.181 |
S-M grade | 1.811 | 0.912 | 3.944 | 1 | 0.047 | 6.115 | 1.024 | 36.521 |
Constant | −17.007 | 11.599 | 2.150 | 1 | 0.14 | 0.000 |
S.E., standard error; OR, odds ratio; CI, confidence interval; GCS, Glasgow Coma Scale; H-H, Hunt-Hess; S-M, Spetzler-Martin.
Table 4
Predictor | Estimate | S.E. | χ2 value | df | P value | OR | 95% CI | |
---|---|---|---|---|---|---|---|---|
Lower | Upper | |||||||
S-M grade | 1.114 | 0.454 | 6.024 | 1 | 0.01 | 3.046 | 1.251 | 7.412 |
Constant | −3.544 | 1.287 | 7.589 | 1 | 0.006 | 0.029 |
S.E., standard error; OR, odds ratio; CI, confidence interval; S-M, Spetzler-Martin.
Discussion
The estimated annual hemorrhagic risk for unruptured BAVM in children is 6.3%, which is significantly greater than that in adults (2–4%) (19). In some series, the total mortality rate caused by ruptured BAVM in children was as high as 23.1% (20). In addition, as patients age, BAVM may undergo dynamic morphological changes and develop associated aneurysms, venous malformations, and venous stenosis. Additionally, longer life expectancy in children further increases their risk of BAVM rupture and intracranial hemorrhage (21). Ma et al. (22) have shown that 49% of children with BAVM rupture present with severe disability (mRS >3) and/or require emergency hematoma evacuation, and all children with BAVM bear the psychological burden of the disease, which may cause neurological damage or even death at any time in their life. The higher annual risk of BAVM rupture with associated increased complications and morbidity, as well as the significant cumulative lifetime risk in children, demonstrates the value of BAVM obliteration in this population. See et al. (23) pointed most pediatric AVMs should be considered for treatment, including incidentally found, asymptomatic lesions. In our opinion, regardless of rupture status, all BAVM in children should be evaluated for potential treatment.
Multidisciplinary review and the use of a balanced multimodality approach in the management of pediatric BAVM can improve treatment outcomes and reduce procedure-related morbidity and mortality. Preoperative endovascular embolization can reduce the volume of BAVM and reduce the risk of blood flow-related aneurysm rupture during surgery while reducing blood loss and related complications (11). During microsurgery, embolization provides a bloodless surgical plane for surgical resection and avoids sacrificing the parenchyma for hemostasis manipulations. The embolic agents act as markers of arterial feeders, preventing inadvertent damage to nearby arteries (24).
Few studies have examined outcomes in BAVM pediatric patients treated with an hOR (25,26). Our retrospective study included 13 BAVM pediatric patients who underwent one-stop hybrid treatment. Compared with microsurgical patients, hOR patients had less intraoperative blood loss (P<0.001), shorter operation times (P<0.001) and shorter postoperative hospital stays (P=0.02), which showed the advantages of the hybrid operation for children with BAVM. Univariate analysis revealed that the presence of neurological dysfunction (P=0.03) and the S-M grade (P=0.047) may be relevant factors for predicting the surgical approach. The results of multivariate analysis showed that the probability of patients choosing composite surgery was 3.046 times that of microsurgery for each step of increase in S-M grade, indicating that the higher the S-M grade was, the greater the probability of choosing hybrid surgery. This finding indicates that the higher the grade of the arteriovenous malformation, the more children should be treated with composite procedures, particularly for operable high-flow arteriovenous malformations. Furthermore, it suggests that aiming for total resection wherever possible improves the prognosis of the child and reduces the risk of recurrence and rupture.
The advantages of the one-stage hOR for treating BAVM include the following (18): (I) preoperative embolization helps to reduce the blood flow of the nidus; (II) additional anesthesia of subsequent operations can be avoided; (III) the extent of BAVM obliteration can be observed immediately; (IV) the transportation of patients between the intervention room and the operating room can be avoided, the anesthesia risk during transportation can be effectively reduced.
All operations were completed in the hOR. There were no significant differences in age, initial symptoms, presence of neurological dysfunction, GCS score, Hunt-Hess classification, or incidence of intraventricular hemorrhage between the two groups. These findings suggest that the baseline situation before surgery was basically the same between the two groups. Only the proportion of female patients in the hybrid operation group was greater than that in the microsurgical group (8/25 vs. 9/13). The proportion of BAVM located on the supratentorial region (P=0.03) and the proportion of S-M above grade III (P=0.003) in the hybrid operation group were greater than those in the microsurgical group. There was no significant difference in the postoperative cure rate according to imaging, incidence of postoperative complications, or mRS score 3 months or 6 months after the operation. Although the complexity of BAVM treated in the hybrid operation group was greater than that in the microsurgical group, the prognosis reached the same level.
Limitations
This was a retrospective nonrandomized study with a small sample size of pediatric patients. Only neurological deficits at 3 and 6 months after surgery were observed, and the long-term prognosis and recurrence of BAVM were not observed. The clinical outcomes were assessed diligently from medical record review but were prone to bias without blinded assessment and documentation errors. The results obtained have certain limitations, and prospective studies of large numbers of multicenter patients are needed to obtain more clinical evidence.
Conclusions
Children with BAVM have a greater risk of bleeding, and there may be stronger indications for intervention in the pediatric population. Our results demonstrate that one-stop hybrid operation is safe for children and more suitable for higher S-M grade BAVM. The advantages of the one-stop hybrid operation include reducing intraoperative blood loss and shortening the operation time and postoperative hospital stay.
Acknowledgments
The authors would like to thank Jinhua Chen, the Senior Statistician from Fujian Medical University Affiliated Union Hospital for his assistance in data statistics and analysis.
Funding: This study was supported by
Footnote
Reporting Checklist: The authors have completed the AME Case Series and STROBE reporting checklists. Available at https://tp.amegroups.com/article/view/10.21037/tp-24-68/rc
Data Sharing Statement: Available at https://tp.amegroups.com/article/view/10.21037/tp-24-68/dss
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Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://tp.amegroups.com/article/view/10.21037/tp-24-68/coif). The authors have no conflicts of interest to declare.
Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Informed written consent was obtained from the patients’ parents and/or legal guardians. This study was performed in accordance with the principles of the Declaration of Helsinki (as revised in 2013). Approval was granted by the Ethics Committee of Fujian Children’s Hospital (No. 2023ETKLR05084), and The 900th Hospital was informed and agreed with the study.
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