Abstract

Background: Cerebral arteriovenous malformation (AVM) is a significant cause of hemorrhagic stroke in pregnant women. The risk of rebleeding after an initial hemorrhage during pregnancy is high, necessitating aggressive intervention and careful management. However, the optimal timing and method of intervention remain unclear. In particular, there has been little discussion regarding cases in which rebleeding occurred despite aggressive intervention. We present a case of cerebral AVM with intraventricular hemorrhage during pregnancy, which subsequently rebled after a cesarean section.

Case Description: A 30-year-old primigravida at 27 weeks of gestation presented with a sudden headache and was diagnosed with intraventricular hemorrhage. Magnetic resonance imaging revealed a flow void in the left fusiform gyrus, confirming a Spetzler–Martin Grade 2 AVM. Due to the deep location and limited safety data on Onyx use during pregnancy, surgery was postponed until after delivery. Cesarean section was planned at 32 weeks to ensure fetal viability. No rebleeding occurred preoperatively. At 32 weeks and 2 days, a cesarean section was performed under spinal anesthesia, delivering a male infant weighing 1,567 g. Postoperative computed tomography revealed intraventricular rebleeding, although no neurological deterioration occurred. Emergency transarterial embolization (TAE) with Onyx was performed the following day, followed by another TAE and AVM resection. Angiography confirmed complete lesion removal, and both the mother and child recovered favorably.

Conclusion: Considering the high rates of rebleeding and the significant maternal and fetal mortality, prioritizing rebleeding prevention may be a key component of the intervention strategy for ruptured AVMs during pregnancy.

Keywords: Arteriovenous malformation, Hemorrhagic stroke, Maternal stroke, Pregnancy

INTRODUCTION

Cerebral arteriovenous malformation (AVM), along with cerebral aneurysms, is the leading cause of hemorrhagic stroke in pregnant women.[ 5 ] Ruptured AVMs during pregnancy have a high risk of rerupture, with recurrence rates ranging from 27% to 30%.[ 9 , 17 , 19 ] Moreover, when AVM rupture occurs during pregnancy, maternal mortality is significantly higher than that in nonpregnant women, ranging from 10% to 40%,[ 9 , 22 , 25 ] and fetal mortality has been reported to be as high as 14%.[ 22 ] Therefore, aggressive and careful intervention should be considered in cases of AVM rupture during pregnancy. However, the optimal timing and method of intervention for ruptured AVMs during pregnancy has yet to be established.[ 28 ] In particular, there has been little discussion regarding cases in which rebleeding occurred despite aggressive intervention. Here, we report a case of AVM that initially presented with intraventricular hemorrhage during pregnancy and subsequently rebled immediately after cesarean section performed under spinal anesthesia.

CASE DESCRIPTION

A 30-year-old primigravida with no significant medical history developed an intraventricular hemorrhage at 25 weeks of pregnancy following sudden headache [ Figures 1a - c ]. Acute management was performed at another institution, and the patient was transferred to our hospital at 27 weeks of gestation. Upon admission, the patient was fully conscious and showed no neurological deficits. T2-weighted magnetic resonance imaging (MRI) revealed a flow void in the left fusiform gyrus, suggesting a possible AVM [ Figures 1d and e ]. Cerebral angiography performed at 28 weeks confirmed the presence of an AVM in the left medial temporal lobe. The feeder vessels originated from the posterior temporal artery, and the draining vein was the basal vein. The nidus had a maximum diameter of 16 mm and was associated with intranidal aneurysms in the upper lateral aspect. The straight sinus showed severe stenosis, and blood flow from the basal vein was diverted through the contralateral basal vein [ Figure 2 ]. The AVM was classified as Spetzler–Martin Grade 2 (S1E0V1).

Figure 1:

(a-c) Computed tomography images at 25 weeks of gestation show intraventricular hemorrhage from the left lateral ventricle to the third ventricle. (d and e) Magnetic resonance imaging taken upon transfer to our hospital at 27 weeks of gestation reveals a flow void in the fusiform gyrus of the left medial temporal lobe on T2-weighted imaging.

Figure 2:

Cerebral angiography images taken at 28 weeks of gestation. (a and b) Anteroposterior (a) and lateral views (b) in the arterial phase. The black arrow indicates the feeder, which is the posterior temporal artery. (c and d) Anteroposterior (c) and lateral views (d) in the late arterial phase. The black arrowheads indicate the drainer, which is the basal vein, and the black arrows indicate the highly narrowed straight sinus. (e and f) Anteroposterior (e) and lateral views (f) of 3D digital subtraction angiography. The white arrows indicate intranidal aneurysms.

A treatment plan involving resection was considered due to the hemorrhagic nature of AVM. Owing to its deep location, preoperative embolization with Onyx was deemed appropriate. However, concerns regarding the safety of Onyx use during pregnancy and the fact that the condition of the patient had stabilized 2 weeks after the initial hemorrhage led to a decision to delay surgery until after delivery. A cesarean section was planned at 32 weeks to ensure fetal viability, followed by transarterial embolization (TAE) and AVM resection, which were performed 4 and 5 days later, respectively.

At 32 weeks and 2 days, a cesarean section was performed under spinal anesthesia, resulting in the delivery of a 1,567 g male infant. However, during surgery, the patient developed headache, and postoperative computed tomography revealed rebleeding into the ventricles [ Figures 3a and b ]. Sedation management was initiated immediately. An emergency TAE was performed the following day, targeting the distal branches of the left posterior temporal artery, which were occluded with Onyx. A second TAE was performed on day 4, targeting the feeders supplying the lower aspect of the AVM [ Figures 3c - f ]. Following sufficient flow reduction, the AVM was resected on day 5. Surgery was performed with the patient in the prone position using a posterior interhemispheric approach. The nidus was located in the fusiform gyrus and Onyx embolization sites served as landmarks for resection. Resection reached the lateral ventricle, where an intranidal aneurysm was observed [ Figure 4 ]. Postoperative cerebral angiography confirmed complete lesion removal [ Figure 5a ], and MRI confirmed the absence of a nidus and no postoperative complications [ Figures 5b and c ]. Both the mother and child recovered uneventfully, and the patient was discharged on the 18^th postoperative day without neurological deficits.

Figure 3:

(a and b) Computed tomography images immediately after cesarean delivery show rebleeding within the left lateral ventricle. (c-f) Final images from the transarterial embolization performed in two stages. The feeder branching from the left posterior temporal artery was occluded using Onyx.

Figure 4:

Intraoperative findings during arteriovenous malformation resection. (a) The medial aspect was dissected along the collateral sulcus, and the lateral aspect was along the occipitotemporal sulcus. (b) Using the embolized Onyx as a marker, the extent of resection anteriorly was defined. (c) Reaching the lateral ventricle in the deep areas, the intranidal aneurysm within the lateral ventricle was confirmed. (d) As the dissection plane developed, a viable nidus was exposed. (e) The main drainer was clipped and subsequently transected. (f) The resected nidus. It is associated with an intranidal aneurysm as depicted in the digital subtraction angiography.

Figure 5:

(a) Intraoperative cerebral angiography confirmed the absence of any residual lesions. (b and c) Postoperative magnetic resonance imaging demonstrated the absence of residual lesions, as well as the absence of any complications.

DISCUSSION

The optimal timing and method of intervention for hemorrhagic AVM during pregnancy are yet to be definitively established. Zhong et al. conducted a review of 112 cases of AVM hemorrhage during pregnancy, published between 1970 and 2020, and reported their findings in 2021.[ 28 ] Among these 112 patients, eight patients experienced rebleeding.[ 5 , 7 , 8 , 11 , 13 , 18 , 20 ] The detailed course and management of the seven cases with available information are presented in Table 1 . Five of these cases occurred during early or midpregnancy, and rebleeding occurred during conservative management (Cases 1, 3, 4, 5, and 7). One case involved a callosal AVM that bled at 36 weeks; following cesarean section, severe rebleeding occurred 6 days postoperatively, leading to craniotomy for hematoma removal and AVM resection (Case 2). Another case involved a callosal AVM that bled at 17 weeks, and pregnancy was terminated to reduce the risk of rebleeding. Gamma knife treatment was planned for the AVM, and an abortion was performed under general anesthesia at 19 weeks. However, rebleeding occurred 2 days postabortion, with minor intraventricular hemorrhage. Two months later, gamma knife surgery was performed, and subsequent angiography confirmed AVM disappearance (Case 6). Thus, reports on rebleeding cases are limited, and no clear guidelines exist regarding the optimal intervention following the initial hemorrhage. Therefore, the best approach must be determined based on the specific circumstances of each case. Issues requiring careful consideration can be categorized into three areas depending on the medical specialty involved.

Table 1:

Case reports of cerebral arteriovenous malformations with rebleeding during pregnancy.

First, regarding neurosurgical interventions, past reports have suggested that surgical intervention for cerebral AVM can improve both maternal and fetal outcomes.[ 6 ] However, there is an ongoing debate about whether direct surgical resection should be performed before delivery.[ 4 , 15 ] Emergency surgery is a viable option for rapidly saving the mother’s life; however, it carries risks such as pregnancy termination and abortion.[ 4 , 26 ] Conversely, elective surgery may be a better choice for fetal maturation; however, it also carries the risk of rebleeding during the waiting period. If the pregnancy has reached a gestational age at which the infant can survive outside the womb, options such as delivery first or simultaneous delivery and resection may also be considered.[ 23 ]

Preoperative TAE is a favorable option for reducing intraoperative blood loss and minimizing surgical risks. However, potential concerns associated with the use of radiation, contrast agents, heparin, and embolic materials must be carefully considered. Rupture of AVMs during pregnancy predominantly occurs during the late gestational period, after the completion of organogenesis.[ 4 ] Although the risk of fetal malformations due to radiation exposure decreases following organogenesis, high-dose exposure may still lead to mental developmental delay beyond this stage.[ 27 ] Iodinated contrast agents are known to cross the placental barrier. While their effects on the fetus have not been fully elucidated, some reports suggest that their use may induce neonatal hypothyroidism.[ 1 ] Standard systemic heparinization is generally considered safe for unruptured AVMs; however, its safety in the context of ruptured AVMs remains controversial and lacks consensus. [ 21 ] Since Onyx contains dimethyl sulfoxide as a solvent, which has not been approved for pediatric use, delivery of the infant should be prioritized before its application.[ 2 ]

Second, regarding obstetric interventions, there are no clear criteria regarding the delivery method before cerebral AVM resection.[ 16 , 23 ] However, some reports have suggested a higher likelihood of bleeding during vaginal delivery,[ 24 ] which often leads to a preference for cesarean section.[ 23 ] Cesarean delivery is considered advantageous compared to vaginal delivery as it helps avoid fluctuations in blood pressure and intracranial pressure and generally results in a shorter delivery time.

Third, regarding anesthetic interventions, there are no established guidelines regarding anesthetic methods during delivery.[ 16 ] In practice, general anesthesia is often preferred for deliveries before AVM resection because of the need to manage respiration and circulation, avoid rebleeding, and maintain uteroplacental blood flow.[ 10 ] However, general anesthesia carries risks, such as a sudden increase in blood pressure from elevated airway pressure during endotracheal intubation[ 12 ] and the potential for the crossing of systemic anesthetics to the infant, leading to the risk of the “neonatal depression” phenomenon,[ 3 ] which requires careful monitoring. However, spinal anesthesia has its own risks, including potential fluctuations in respiration and blood pressure due to the emotional responses associated with delivery. Furthermore, spinal anesthesia is contraindicated in cases of increased intracranial pressure because rebleeding of the AVM during delivery can result in brain herniation.[ 14 ]

It is widely accepted that aggressive intervention should be considered for ruptured AVMs during pregnancy; however, cases of rebleeding despite such intervention have received little attention in the literature.[ 11 , 20 ] In the present case, a cesarean section was scheduled at 32 weeks of gestation, when fetal viability is generally established, followed by an interval planned for surgical intervention. This approach represented a well-balanced strategy, taking into account the maternal condition, AVM localization, risk of rebleeding, and potential fetal impact. However, in practice, rebleeding from the AVM occurred during cesarean delivery under spinal anesthesia. It is conceivable that rebleeding might have been avoided if delivery had been performed under general anesthesia, with continued sedation for immediate surgical intervention targeting the AVM. In obstetrics, the “principle of maternal priority” is a widely accepted concept in which maternal safety takes precedence over fetal well-being when the lives or health of both are at risk. Given the high rate of rebleeding and the substantial maternal and fetal mortality associated with ruptured AVMs during pregnancy, an intervention strategy that prioritizes the prevention of rebleeding may be more appropriate.

CONCLUSION

We reported a case of a cerebral AVM that initially presented with intraventricular hemorrhage during pregnancy and subsequently rebled immediately after a cesarean section performed under spinal anesthesia. In cases of ruptured AVMs during pregnancy, the timing and method of intervention should be considered not only from a neurosurgical perspective but also from obstetric and anesthetic viewpoints. Considering the high rates of rebleeding and the significant maternal and fetal mortality associated with such cases, prioritizing the prevention of rebleeding may be an important aspect of the intervention strategy.

Ethical approval:

Institutional Review Board approval is not required.

Declaration of patient consent:

The authors certify that they have obtained all appropriate patient consent.

Financial support and sponsorship:

Nil.

Conflicts of interest:

There are no conflicts of interest.

Use of artificial intelligence (AI)-assisted technology for manuscript preparation:

The authors confirms that there was no use of AI-assisted technology in the writing or editing of the manuscript, and no images were manipulated using AI.

Disclaimer

The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.

References

1. Ahmet A, Lawson ML, Babyn P, Tricco AC. Hypothyroidism in neonates post-iodinated contrast media: A systematic review. Acta Paediatr. 2009. 98: 1568-74

2. Chen K, Lu X, Xu D, Guo Y, Ao Y, Wang H. Prenatal exposure to corn oil, CMC-Na or DMSO affects physical development and multi-organ functions in fetal mice. Reprod Toxicol. 2023. 118: 108366

3. D’Alessio JG, Ramanathan J. Effects of maternal anesthesia in the neonate. Semin Perinatol. 1998. 22: 350-62

4. De Maria L, Serioli S, Fontanella MM. Brain arteriovenous malformations and pregnancy: A systematic review of the literature. World Neurosurg. 2023. 177: 100-8

5. Dias MS. Neurovascular emergencies in pregnancy. Clin Obstetr Gynecol. 1994. 37: 337-54

6. Fukuda K, Hamano E, Nakajima N, Katsuragi S, Ikeda T, Takahashi JC. Pregnancy and delivery management in patients with cerebral arteriovenous malformation: A single-center experience. Neurol Med Chir (Tokyo). 2013. 53: 565-70

7. Garza-Mercado R, Cavazos E, Tamez-Montes D. Cerebral arteriovenous malformations in children and adolescents. Surg Neurol. 1987. 27: 131-40

8. Gross BA, Du R. Hemorrhage from arteriovenous malformations during pregnancy. Neurosurgery. 2012. 71: 349-55 discussion 355-6

9. Jermakowicz WJ, Tomycz LD, Ghiassi M, Singer RJ. Use of endovascular embolization to treat a ruptured arteriovenous malformation in a pregnant woman: A case report. J Med Case Rep. 2012. 6: 113

10. Ji Y, Liang Y, Liu B, Wang Y, Li L, Liu Y. Anaesthetic management of cerebral arteriovenous malformation hemorrhage during pregnancy: A case series. Medicine (Baltimore). 2023. 102: e32753

11. Karakida S, Sasaki T, Kai K, Harada K, Yoshimura S, Kono M. Vaginal cesarean section for second-trimester therapeutic abortion. Taiwan J Obstet Gynecol. 2013. 52: 564-7

12. King BD, Harris LC, Greifenstein FE, Elder JD, Dripps RD. Reflex circulatory responses to direct laryngoscopy and tracheal intubation performed during general anesthesia. Anesthesiology. 1951. 12: 556-66

13. Lanzino G, Jensen ME, Cappelletto B, Kassell NF. Arteriovenous malformations that rupture during pregnancy: A management dilemma. Acta Neurochir (Wien). 1994. 126: 102-6

14. Leffert LR, Schwamm LH. Neuraxial anesthesia in parturients with intracranial pathology: A comprehensive review and reassessment of risk. Anesthesiology. 2013. 119: 703-18

15. Liu XJ, Wang S, Zhao YL, Teo M, Guo P, Zhang D. Risk of cerebral arteriovenous malformation rupture during pregnancy and puerperium. Neurology. 2014. 82: 1798-803

16. Mrowczynski OD, McNutt S, Bourcier AJ, Jafrani R, Lane JR, Padmanaban V. Aneurysmal and arteriovenous malformation hemorrhage during pregnancy: An update on the epidemiology, risk factors and prognosis. Clin Neurol Neurosurg. 2021. 208: 106897

17. Ogilvy CS, Stieg PE, Awad I, Brown RD, Kondziolka D, Rosenwasser R. Recommendations for the management of intracranial arteriovenous malformations: A statement for healthcare professionals from a special writing group of the Stroke council, American stroke association. Circulation. 2001. 103: 2644-57

18. Porras JL, Yang W, Philadelphia E, Law J, Garzon-Muvdi T, Caplan JM. Hemorrhage risk of brain arteriovenous malformations during pregnancy and puerperium in a North American cohort. Stroke. 2017. 48: 1507-13

19. Robinson JL, Hall CJ, Sedzimir CB. Subarachnoid hemorrhage in pregnancy. J Neurosurg. 1972. 36: 27-33

20. Sadasivan B, Malik GM, Lee C, Ausman JI. Vascular malformations and pregnancy. Surg Neurol. 1990. 33: 305-13

21. Schirmer CM, Bulsara KR, Al-Mufti F, Haranhalli N, Thibault L, Hetts SW. Antiplatelets and antithrombotics in neurointerventional procedures: Guideline update. J Neurointerv Surg. 2023. 15: 1155-62

22. Sharshar T, Lamy C, Mas JL. Incidence and causes of strokes associated with pregnancy and puerperium. A study in public hospitals of Ile de France. Stroke in Pregnancy Study Group. Stroke. 1995. 26: 930-6

23. Trivedi RA, Kirkpatrick PJ. Arteriovenous malformations of the cerebral circulation that rupture in pregnancy. J Obstetr Gynaecol. 2003. 23: 484-9

24. Wei HY, Lien YS, Tee YT, Shih YT, Wang PH, Chen GD. Intracerebral hemorrhage with cerebral arteriovenous malformation rupture during pregnancy. Taiwan J Obstet Gynecol. 2008. 47: 460-2

25. Wilkins RH. Natural history of intracranial vascular malformations: A review. Neurosurgery. 1985. 16: 421-30

26. Yan KL, Ko NU, Hetts SW, Weinsheimer S, Abla AA, Lawton MT. Maternal and fetal outcomes in women with brain arteriovenous malformation rupture during pregnancy. Cerebrovasc Dis. 2021. 50: 296-302

27. Yoon I, Slesinger TL, editors. Radiation exposure in pregnancy. StatPearls. Treasure Island, FL: StatPearls Publishing; 2025. p. Available from: https://www.ncbi.nlm.nih.gov/books/NBK532276 [Last accessed on 2025 Mar 22]

28. Zhong Z, Ni H, Zhu J, Jiang H, Hu J, Lin D. Management of acute hemorrhage caused by cerebral arteriovenous malformation during pregnancy-case series and literature review. World Neurosurg. 2021. 152: e688-99