One-stop hybrid operation versus microsurgery for treating brain arteriovenous malformation in children--A retrospective case series

doi:10.21203/rs.3.rs-3873336/v1

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One-stop hybrid operation versus microsurgery for treating brain arteriovenous malformation in children--A retrospective case series

https://doi.org/10.21203/rs.3.rs-3873336/v1

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Background

Brain arteriovenous malformation (AVM) is one of the most common causes of cerebral hemorrhage in children. The effectiveness of one-stop hybrid operation in the treatment of AVMs in adults has been widely confirmed, but there are few studies in children. This study intends to analyze the role and significance of one-stop hybrid operation versus microsurgery in the treatment of AVMs in children by retrospective analysis.

Methods

A total of 57 children (≤ 18 years old) with AVMs who were admitted to the 900th Hospital of United Logistics Support Forces and Fujian Children's Hospital between September 2018 and August 2022 were retrospectively analyzed. According to the inclusive criteria and exclusion criteria, 38 cases were included, and they were divided into microsurgery group (25 cases) and hybrid operation group (13 cases) according to the different treatment modalities. Observation indicators included clinical characteristics: gender, age, initial symptom, presence or absence of signs, GCS score, Hunt-Hess grade; imaging characteristics such as the location of AVMs, Spetzler-Martin (S-M) grade, whether accompanied by intraventricular hemorrhage, treatment and prognosis indicators such as intraoperative blood loss, operation time, imaging cure, postoperative complications, hospital stay, and 3 months and 6 months mRS after operation.

Results

The proportion of female patients (P = 0.042), the proportion of patients whose AVMs was located on the supratentorial (P = 0.034) and the proportion of patients whose S-M grade was above grade III (P = 0.003) in the hybrid operation group were higher than those of the microsurgery group. The intraoperative blood loss (P < 0.001), operation time (P < 0.001) and postoperative hospital stay (P = 0.024) of patients in the microsurgery group were higher than those in the hybrid operation group. The presence of signs and S-M grade may be relevant factors in predicting the surgical approach, and the probability of selecting hybrid operation for each step of increasing S-M grade is 3.046 times that of microsurgery.

Conclusions

One-stop hybrid operation is effective and safe for the treatment of brain AVMs in children. High S-M grade of AVMs is more suitable for hybrid operation.

One-stop hybrid operation

microsurgery

brain arteriovenous malformations

children

Brain arteriovenous malformation (AVM) is a cerebrovascular structural developmental abnormality characterized by abnormal connection between the arterial and venous systems, with an annual incidence of about 1.12–1.42 per 100,000 people, including the most common manifestations such as intracranial hemorrhage, epilepsy, headache, and neurological dysfunction ^[1–3]. AVMs are considered the primary etiology of hemorrhagic stroke in children. The annual risk of hemorrhage is 6.3%, and the annual risk of re-hemorrhage is 14.8%^[4], significantly higher than the overall risk of annual hemorrhage and re-hemorrhage in adults of 3% and 4.5% respectively ^[5]. Brain AVMs result in 35% -55% of children with hemorrhagic strokes, with significant mortalities and morbidities ^{[6, 7]}. In a series, the average mortality rate over the past 40 years reached 25%, decreasing from 39–16% during this period, which is consistent with technological progress ^[8]. Previous study has shown that increased neuroplasticity in children may reduce the morbidity of endovascular and surgical procedures ^[9]. With an inherent long life expectancy, even in unruptured AVMs, there may be stronger indications to intervene in the pediatric population.

The primary goal of AVM treatment is angiographic cure, which is abolition of arterio-venous shunting with no or minimal risk. The treatment methods of AVMs include surgical excision of the AVM nidus, endovascular complete AVM nidus embolization, radiosurgical thrombo-obliteration or by a combination of these modalities. According to reports, 18% of children with AVMs were considered untreatable ^{[10, 11]}. Addressing such complex cases, multidisciplinary methods with flexibility and expertise may improve the outcomes and reduce morbidity and mortality ^{[12, 13]}. The combination of embolization and microsurgery can effectively improve the obliteration rate and reduce complications. Previous studies recommended microsurgery several days or weeks after embolization, when the angioarchitecture and hemodynamic changes in the peripheral vessels surrounding the AVM nidus have stabilized. This staged treatment can reduce the chance of normal perfusion pressure breakthrough after surgery ^[14]. 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 ^[14–17]. The risk of AVM rupture during the perioperative period is as high as 4% -16% ^[18]. 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 ^{[19, 20]}. It can also supplement the resection of incomplete AVMs ^[21]. One-stop hOR is often used for the treatment of adult AVMs, while pediatric AVMs is rarely used. This study aims to retrospectively analyze the clinical data and short-term prognosis of pediatric cerebral AVMs, and compare the short-term prognosis and safety of hOR and microsurgery in the treatment of pediatric cerebral AVMs.

2.1 Patients and Study Design

Patients with AVMs aged 1–18 years who underwent AVM treatment in the Fujian Children's Hospital and the 900th Hospital of Joint Logistics Support Forces between September 2018 and August 2022. A total of 57 children with diagnosed cerebral vascular malformations were treated. According to the inclusion and exclusion criteria, a total of 38 cases meet the criteria, including 25 cases in the microsurgery group, 13 cases in the hybrid operation group (Fig. 1). BAVMs were diagnosed using digital subtraction angiography (DSA), magnetic resonance angiography (MRA), or computed tomography angiography (CTA) and graded by Spetzler-Martin (S-M) grade. The following patient data were recorded: age, gender, whether headache, neurological dysfunction, Glasgow coma scale (GCS) score and Hunt-Hess score (H-H score) at the time of admission. Informed consent was obtained from all individual participants included in the study, and informed written consent was obtained from the parents and/or legal guardians. This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Fujian Children's Hospital(2023ETKLR05084).

2.2 Surgical Procedure

1. 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 the temporary aneurysm clips were selected and loaded. The craniotomy was performed to ensure that the margins of the lesion lay well within the margins of the operative exposure. Once the dura was opened, the dissection was performed under the 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. An anatomical, circumferential cortical and subcortical dissection was performed with serial coagulation of supplying arterial pedicles before disconnecting the venous drainage. If AVMs were combined with intracranial hematoma, the hematoma was usually removed to increase the exposure space before the AVMs were removed.
2. One-stop hybrid operation (embolization + microsurgery): The surgery was performed in the hOR. After a total cerebral angiography was performed via femoral artery intubation, the feeding artery and draining vein of the AVMs were confirmed. First, embolization was performed with ONYX (Covidien/ev3, Irvine, California, USA). If the AVM 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 AVM was removed by microsurgery via craniotomy in the hOR. After the removal of the AVM, another angiography was performed to confirm the result of resection (Fig. 2). The surgery was continued for those who still had residues.

2.3 Outcome evaluation and follow-up

Outcome evaluation including intraoperation blood loss, operation time (only the microsurgery time is calculated in case of hybrid operation group), imaging cure, postoperative complications, hospital stay, modified Rankin Score (mRS) 3 months and 6 months after operation were recorded. All patients were followed up for 6 months – 4 years, MRA or CTA was reexamined 1 week after operation, and DSA was performed for imaging evaluation 3 months after operation. The neurological functional recovery was assessed with the mRS 3 months and 6 months after operation, respectively. mRS score ≦ 2 indicated good neurological function, and it was considered as neurological dysfunction.

2.4 Statistical analysis

H-H score and S-M grade were classified into grade data, and ridit analysis was adopted. Count data were expressed by case numbers and Fisher's exact test was adopted. Measurement data were expressed as mean standard deviation, and pairwise comparison was conducted with two independent sets of t test. The operation mode was used as the dependent variable in the prediction model for selection of operation mode, and clinical and imaging characteristics such as gender, age, whether headache, neurological dysfunction, GCS, intraventricular hemorrhage or not, location of AVMs, H-H score, S-M grade and others were used as the independent variables. The logistics 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 multi-factor analysis were performed, respectively. P ≦ 0.05 was defined as statistically significant difference, and SPSS26.0 software was used for statistical analysis.

3.1 Clinical and imaging features of the patient

A total of 57 children with diagnosed brain AVMs were treated. According to the inclusion and exclusion criteria, a total of 38 cases meet the criteria, including 25 cases in the microsurgery group, 13 cases in the hybrid operation group (Fig. 1). Male: female = 21:17, age: 1–18 years old, with the average age of 9.72 ± 4.22 vs 10.85 ± 4.67 years old. In the clinical and imaging characteristics of patients in the two groups, the distribution of gender, the location of AVM and S-M grade was inconsistent. The proportion of female patients (P = 0.042), the location of AVMs (P = 0.034) and the proportion of S-M grade above Grade 3 (P = 0.003) in the hybrid operation group were higher than those in the microsurgery group, and the differences were statistically significant. There were no significant differences in age, headache, neurological impairment, GCS, Hunt-Hess and intraventricular hemorrhage between the two groups (Table 1).

Table 1

Clinical and Imaging Characteristics of Patients
Characteristic		microsurgery	hybrid operation	Sum	χ²/Hc Value	P Value
Characteristic		n = 25	n = 13	Sum	χ²/Hc Value	P Value
Gender	Female	8	9	17		0.042
Gender	Male	17	4	21		0.042
Age		9.72 ± 4.22	10.85 ± 4.67			0.456
Headache	No	11	4	15		0.501
Headache	Yes	14	9	23		0.501
GCS		12.68 ± 3.44	12.38 ± 3.23		0.256	0.799
Neurological impairment	No	15	8	23		1.000
Neurological impairment	Yes	10	5	15		1.000
intraventricular hemorrhage	No	12	4	16		0.490
intraventricular hemorrhage	Yes	13	9	22		0.490
AVM location	Supratentorial	17	13	30		0.034
AVM location	Subtentorial	8	0	8		0.034
H-H score	1	1	0	1	1.476	0.224
	2	8	3	11
	3	10	4	14
	4	5	6	11
	5	1	0	1
S-M grade	1	8	0	8	8.941	0.003
	2	9	2	11
	3	6	8	14
	4	1	3	4
	5	1	0	1

3.2 Prognostic analysis of patients undergoing different surgical procedures

All patients were treated with microsurgery or hybrid operation. In the hybrid operation group, only the time of microsurgery of was calculated in the operation time. Postoperative complications included intracranial or incision infection, epilepsy, hydrocephalus, etc. There was no death in all patients. Imaging cure was confirmed by MRA, CTA or DSA showing no abnormal vascular mass after operation. Statistical results showed that the intraoperative blood loss (P < 0.001), operation time (P < 0.001) and postoperative hospital stay (P = 0.024) of patients in the microsurgery group were higher than those in the hybrid operation group. There was no significant difference between the two groups in postoperative imaging cure, postoperative complication, neurological function 3m and 6m after operation (Table 2).

Table 2

Prognostic analysis of patients undergoing different surgical procedures
Characteristic		Microsurgery	Hybrid operation	t Value	P Value
Characteristic		n = 25	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	0.024
Postoperative imaging cure	Yes	23	11		0.595
Postoperative imaging cure	No	2	2		0.595
mRS (3months after operation)	≤ 2	16	10		0.486
mRS (3months after operation)	>2	9	3		0.486
mRS (6months after operation)	≤ 2	22	12		1.000
mRS (6months after operation)	>2	3	1		1.000
Postoperative complication	Yes	12	4		0.490
Postoperative complication	No	13	9		0.490

3.3 Prediction model for surgical approach selection

Univariate analysis of the logistics regression analysis revealed the presence of neurological dysfunction (P = 0.026) and S-M grade (P = 0.047) may be a relevant factor in predicting the surgical approach (Table 3). The results of multivariate analysis showed that the probability of patients choosing hybrid operation was 3.046 times as high as that of microsurgery for each higher S-M grade, indicating that the higher S-M grade was, the higher the probability of choosing hybrid operation was (Table 4). The following prediction equation can be derived:

Table 3

Prediction model for surgical method selection (univariate analysis of logistic regression analysis)
Predictor	Estimate	S.E.	Χ² Value	df	P Value	OR	95%CI
Predictor	Estimate	S.E.	Χ² Value	df	P Value	OR	Lower	Upper
Gender	-1.618	1.441	1.260	1	0.262	0.198	0.012		3.343
Age	0.195	0.159	1.507	1	0.220	1.216	0.890		1.660
Headache	0.665	1.774	0.140	1	0.708	1.944	0.060		62.884
Signs	-5.008	2.250	4.951	1	0.026	0.007	0.000		0.551
GCS score	0.308	0.515	0.358	1	0.550	1.360	0.496		3.730
Intraventricular hemorrhage	-1.248	1.399	0.795	1	0.373	0.287	0.019		4.457
Location of malformed vascular mass	-22.604	11812.866	0.000	1	0.998	0.000	0.000
H-H score	3.120	1.755	3.159	1	0.076	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	0.143	0.000

Table 4

Prediction model for surgical method selection (multivariate analysis of logistic regression analysis)
Predictor	Estimate	S.E.	Χ² Value	df	P Value	OR	95%CI
Predictor	Estimate	S.E.	Χ² Value	df	P Value	OR	Lower	Upper
S-M grade	1.114	0.454	6.024	1	0.014	3.046	1.251	7.412
Constant	-3.544	1.287	7.589	1	0.006	0.029

$$\frac{p}{1-p}={\text{e}}^{-3.544+1.114\ast SMgrade}$$

$\varvec{p}$ was the probability to select the hybrid operation, and could to predict the surgery method.

The estimated annual hemorrhagic risk for unruptured AVMs in children is 6.3%, significantly higher than in adults (2–4%) ^[22]. In some series, the total mortality rate caused by ruptured AVMs in children is as high as 21% ^[11]. In addition, as patients age, AVMs may undergo dynamic morphological changes and develop associated aneurysms, venous malformations, and venous stenosis. Additionally, the longer expectation of life in children further increases their risk of AVM rupture and intracranial hemorrhage^[23]. Studies showed that 49% of children with AVM rupture presented with severe disability (mRS > 3) and/or required emergency hematoma evacuation ^[24], and all children with AVMs must bear the psychological burden of the disease, which may cause neurological damage or even death at any time in their life. Young women must also anticipate an increased risk of intracranial hemorrhage during pregnancy ^[25]. The higher annual risk of AVM rupture with associated increased complications and morbidity as well as the significant cumulative lifetime risk in children demonstrates the value of AVM obliteration in this population. In our opinion, regardless of rupture status, all AVMs in children should be evaluated for potential treatment. Previous studies have demonstrated favorable clinical outcomes after pediatric AVM treatment relative to adults ^{[26, 27]}, which may be attributed to greater neuroplasticity in children ^[26].

Multidisciplinary review and the use of a balanced multimodality approach in the management of pediatric brain AVMs can improve treatment outcomes, reduce procedure-related morbidity and mortality. It has been reported that AVMs of SM I-II grade are low-risk lesions that can be safely treated by microsurgery, and 92–100% of patients have obtained good results^[28]. At the same time, in the case of acute AVM rupture complicated with large hematoma, the AVM can be surgically removed together with the hematoma. For AVMs above SM grade III, microsurgery alone had high risk, and required multiple models or treatments. Endovascular embolization is also a common treatment for AVMs, which can be used to occlude AVMs as a simple treatment. It can also be used as an adjunct to surgery or radiosurgery. Pre-operative endovascular embolization can reduce the volume of AVMs and reduce the risk of blood flow-related aneurysm rupture in endovascular, while reducing blood theft and related complications. During microsurgery, the 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.

Few studies have examined outcomes in AVM pediatric patients treated in a hOR ^{[29, 30]}. Our retrospective study included 13 AVM pediatric patients who underwent one-stop hybrid treatment. Compared with microsurgery group, hOR patients had smaller intraoperative blood loss (P < 0.001), operation time (P < 0.001) and postoperative hospital stay (P = 0.024), which showed the advantages of the hybrid operation in AVMs for children. Univariate analysis showed that the presence of neurological dysfunction (P = 0.026) and 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 higher the probability of choosing hybrid operation was. It indicated that hybrid operation should be selected for high-grade AVMs in children.

The advantages of the one-staged hOR for treating AVMs were proposed ^[20], including (1) preoperative embolization helps to reduce the blood flow of the nidus, (2) could avoid additional anesthesia of subsequent operations, (3) the extent of AVM obliteration can be observed immediately, (4) avoids the transportation of patients between the intervention room and the operating room, and can effectively reduce the anesthesia risk during transportation, and (6) patients' medical expenses could be reduced due to the operation completed under anesthesia only once. Rutledge et al. reported that using hOR could improve the cure rate and reduce the incidence of AVMs ^[31]. Grüter et al performed routine DSA after AVM operation through a hOR, and found two cases of residual malformed vascular masses during the operation, followed by remedial resection, and one case successfully underwent surgical resection with preoperative embolization to reduce blood flow of the AVM ^[20]. Song et al. used hOR to treat low-grade and high-grade AVMs, significantly reducing the risk of postoperative rebleeding ^[32].

All the studies in this group were completed in hOR. The results showed that there were no significant differences in age, initial symptoms, presence of neurological dysfunction, GCS score, Hunt-Hess classification, and intraventricular hemorrhage between the two groups. Those suggest that the baseline situation before surgery is basically the same between the two groups. Only the proportion of female patients in the hybrid operation group was higher than that in the microsurgery group (8/25 vs 9/13). The proportion of AVMs located on the supratentorial (P = 0.034) and the proportion of S-M above grade III (P = 0.003) in the hybrid operation group were higher than those in the microsurgery group. There was no significant difference in postoperative cure rate in imaging, incidence of postoperative complications, and mRS 3 months and 6 months after operation. It indicated that although the complexity of AVMs treated in the hybrid operation group was higher than that in the microsurgery group, the prognosis could reach the same level.

This was a retrospective study with a small number of cases. The neurological deficits of 3 months and 6 months after surgery were only observed, and the long-term prognosis and recurrence of AVMs were not observed. The results obtained have certain limitations, and prospective studies of large numbers of multi-center cases are needed to obtain more clinical evidence.

Children with brain AVMs have a higher risk of bleeding, and active treatment has a better prognosis than conservative treatment. Our results demonstrate that One-stop hybrid operation is safe for children and more suitable for higher S-M grade AVMs applications. The advantages of One-stop hybrid operation are also reflected in reducing intraoperative blood loss, shortening operation time and postoperative hospital stay.

Data availability

The data used to support the findings of this study are available from the corresponding author upon request.

Author contributions CF, LQC, JJJ conducted the literature search and wrote the initial draft of the paper. YJB, LHB, HJF, JJJ participated in all surgeries. CKM, ZQS, YJB participated in data collection and follow up. All authors reviewed the manuscript and approved the final manuscript.

Funding Fujian Province Key Clinical Specialty Construction Project - Pediatric Neurosurgery of Fujian Children’s Hospital [MWYZ (2023) No.1163]

Conflict of interest The authors declare that they have no conflict of interest.

Acknowledgments

The authors would like to thank Chen Jinhua Senior Statistician from Fujian Medical University Affiliated Union Hospital for his assistance in data statistics and analysis.

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No competing interests reported.

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One-stop hybrid operation versus microsurgery for treating brain arteriovenous malformation in children--A retrospective case series

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Abstract

Background

Methods

Results

Conclusions

Figures

1. Introduction

2. Methods

2.1 Patients and Study Design

2.2 Surgical Procedure

2.3 Outcome evaluation and follow-up

2.4 Statistical analysis

3. Results

3.1 Clinical and imaging features of the patient

3.2 Prognostic analysis of patients undergoing different surgical procedures

3.3 Prediction model for surgical approach selection

4. Discussion

5. Limitations

6. Conclusion

Declarations

References

Additional Declarations

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