The risk of hemorrhage in pregnant cerebral arteriovenous malformation patients: a systematic review_Chinese Journal of Evidence-Based Medicine

Authors：

LI Xinghong ¹ ,  LI Chenxi ^1,2 , WANG Zhengye ³ , HUANG Dishu ⁴ , DING Yi ⁵ , ZHOU Yuchuan ¹

1. Department of Oral and Maxillofacial Oncology & Surgery, the First Affiliated Hospital / Affiliated Stomatological Hospital of Xinjiang Medical University, Stomatology Research Institute of Xinjiang Uygur Autonomous Region, Urumqi 830054, P. R. China;
2. Hubei Province Key Laboratory of Oral and Maxillofacial Development and Regeneration, School of Stomatology, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430022, P. R. China;
3. Center for Disease Control and Prevention, Xinjiang Production and Construction Corps, Urumqi 830092, P. R. China;
4. Department of Neurology, Children's Hospital of Chongqing Medical University, Chongqing 400014, P. R. China;
5. Department of Obstetrics and Gynecology, University Hospital Hamburg-Eppendorf (UKE), Hamburg 20246, Germany;

Corresponding author：

LI Chenxi, Email: lichenximed@163.com

Keywords：

Cerebral arteriovenous malformation; Pregnancy; Incidence; Systemic review; Meta-analysis

DOI：

10.7507/1672-2531.202312131

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Objective To systematically review the the risk of hemorrhage in pregnant cerebral arteriovenous malformation (CAVM) patients. Methods The Web of Science, PubMed, Cochrane Library, WanFang Data, VIP and CNKI databases were electronically searched to collect clinical studies related to hemorrhage in pregnant CAVM patients from inception to June, 2023. Two reviewers independently screened literature, extracted data and assessed the risk of bias of the included studies. Meta-analysis was then performed by using Stata 13.1 and R 4.0.4 software. Results A total of 13 studies involving 2 273 patients were included. The results of meta-analysis showed that the pooled incidence of hemorrhage in pregnant CAVM patients was 0.18 (95%CI 0.12 to 0.24). The subgroup analyses were carried out based on world regions and the study duration, with the higher pooled incidence was Europe 0.37 (95%CI 0.05 to 0.80) and 10 to 20 years of study duration 0.37 (95%CI 0.17 to 0.57). Conclusion Current evidence shows that the incidence of hemorrhage in pregnant CAVM patients is about 18%. Due to the limited quality and quantity of the included studies, more high quality studies are needed to verify the above conclusion.

1.	Lawton MT, Rutledge WC, Kim H, et al. Brain arteriovenous malformations. Nat Rev Dis Primers, 2015, 1: 15008.
2.	Davidoff CL, Lo Presti A, Rogers JM, et al. Risk of first hemorrhage of brain arteriovenous malformations during pregnancy: a systematic review of the literature. Neurosurgery, 2019, 85(5): E806-E814.
3.	Hongo H, Miyawaki S, Teranishi Y, et al. Genetics of brain arteriovenous malformations and cerebral cavernous malformations. J Hum Genet, 2023, 68(3): 157-167.
4.	Lv X, Li Y. The clinical characteristics and treatment of cerebral AVM in pregnancy. Neuroradiol J, 2015, 28(4): 385-388.
5.	Trivedi RA, Kirkpatrick PJ. Arteriovenous malformations of the cerebral circulation that rupture in pregnancy. J Obstet Gynaecol, 2003, 23(5): 484-489.
6.	Liu J, Luo C, Guo Y, et al. Individual trigger factors for hemorrhagic stroke: Evidence from case-crossover and self-controlled case series studies. Eur Stroke J, 2023, 8(3): 808-818.
7.	Zhong Z, Ni H, Zhu J, et al. Management of acute hemorrhage caused by cerebral arteriovenous malformation during pregnancy-case series and literature review. World Neurosurg, 2021, 152: e688-e699.
8.	Can A, Du R. Neurosurgical issues in pregnancy. Semin Neurol, 2017, 37(6): 689-693.
9.	吕宪利, 刘鹏, 李佑祥. 妊娠期颅内动静脉畸形的临床特征和治疗进展. 中华神经外科杂志, 2015, 31(6): 633-635.
10.	Yih PS, Cheong KF. Anaesthesia for caesarean section in a patient with an intracranial arteriovenous malformation. Anaesth Intensive Care, 1999, 27(1): 66-68.
11.	Coskun D, Mahli A, Yilmaz Z, et al. Anesthetic management of caesarean section of a pregnant woman with cerebral arteriovenous malformation: a case report. Cases J, 2008, 1(1): 327.
12.	De Maria L, Serioli S, Fontanella MM. Brain arteriovenous malformations and pregnancy: a systematic review of the literature. World Neurosurg, 2023, 177: 100-108.
13.	Zeng X, Zhang Y, Kwong JS, et al. The methodological quality assessment tools for preclinical and clinical studies, systematic review and meta-analysis, and clinical practice guideline: a systematic review. J Evid Based Med, 2015, 8(1): 2-10.
14.	Algra AM, Lindgren A, Vergouwen MDI, et al. Procedural clinical complications, case-fatality risks, and risk factors in endovascular and neurosurgical treatment of unruptured intracranial aneurysms: a systematic review and meta-analysis. JAMA Neurol, 2019, 76(3): 282-293.
15.	Li C, Matthies L, Hou X, et al. A meta-analysis of the pros and cons of partial superficial parotidectomy versus superficial parotidectomy for the treatment of benign parotid neoplasms. J Craniomaxillofac Surg, 2020, 48(6): 590-598.
16.	Robinson JL, Hall CS, Sedzimir CB. Arteriovenous malformations, aneurysms, and pregnancy. J Neurosurg, 1974, 41(1): 63-70.
17.	Horton JC, Chambers WA, Lyons SL, et al. Pregnancy and the risk of hemorrhage from cerebral arteriovenous malformations. Neurosurgery, 1990, 27(6): 867-871.
18.	Katsuragi S, Yoshimatsu J, Tanaka H, et al. Management of pregnancy complicated with intracranial arteriovenous malformation. J Obstet Gynaecol Res, 2018, 44(4): 673-680.
19.	Forster DM, Kunkler IH, Hartland P. Risk of cerebral bleeding from arteriovenous malformations in pregnancy: the Sheffield experience. Stereotact Funct Neurosurg, 1993, 61(Suppl 1): 20-22.
20.	van Beijnum J, Wilkinson T, Whitaker HJ, et al. Relative risk of hemorrhage during pregnancy in patients with brain arteriovenous malformations. Int J Stroke, 2017, 12(7): 741-747.
21.	Gross BA, Du R. Hemorrhage from arteriovenous malformations during pregnancy. Neurosurgery, 2012, 71(2): 349-355.
22.	Tonetti D, Kano H, Bowden G, et al. Hemorrhage during pregnancy in the latency interval after stereotactic radiosurgery for arteriovenous malformations. J Neurosurg, 2014, 121(Suppl): 226-231.
23.	Yan KL, Ko NU, Hetts SW, et al. Maternal and fetal outcomes in women with brain arteriovenous malformation rupture during pregnancy. Cerebrovasc Dis, 2021, 50(3): 296-302.
24.	Porras JL, Yang W, Philadelphia E, et al. Hemorrhage risk of brain arteriovenous malformations during pregnancy and puerperium in a north American cohort. Stroke, 2017, 48(6): 1507-1513.
25.	Liu XJ, Wang S, Zhao YL, et al. Risk of cerebral arteriovenous malformation rupture during pregnancy and puerperium. Neurology, 2014, 82(20): 1798-1803.
26.	Lv X, Li W, He H, et al. Known and unknown cerebral arteriovenous malformations in pregnancies: haemorrhage risk and influence on obstetric management. Neuroradiol J, 2017, 30(5): 437-441.
27.	Zhu D, Zhao P, Lv N, et al. Rupture risk of cerebral arteriovenous malformations during pregnancy and puerperium: a single-center experience and pooled data analysis. World Neurosurg, 2018, 111: e308-e315.
28.	Liu J, Zhang H, Luo C, et al. Haemorrhage risk of brain arteriovenous malformation during pregnancy and puerperium. Stroke Vasc Neurol, 2023, 8(4): 307-317.
29.	李晨曦, 陈程, 吕小毅, 等. 拉曼光谱辅助诊断结肠癌准确性的Meta分析. 中国循证医学杂志, 2022, 22(6): 649-654.
30.	van Beijnum J, van der Worp HB, Schippers HM, et al. Familial occurrence of brain arteriovenous malformations: a systematic review. J Neurol Neurosurg Psychiatry, 2007, 78(11): 1213-1217.
31.	Hashimoto T, Lawton MT, Wen G, et al. Gene microarray analysis of human brain arteriovenous malformations. Neurosurgery, 2004, 54(2): 410-423.
32.	Pawlikowska L, Tran MN, Achrol AS, et al. Polymorphisms in genes involved in inflammatory and angiogenic pathways and the risk of hemorrhagic presentation of brain arteriovenous malformations. Stroke, 2004, 35(10): 2294-2300.
33.	Kato Y, Dong VH, Chaddad F, et al. Expert consensus on the management of brain arteriovenous malformations. Asian J Neurosurg, 2019, 14(4): 1074-1081.
34.	Etter MM, Nguyen A, Brehm A, et al. Endovascular treatment and peri-interventional management of ruptured cerebrovascular lesions during pregnancy: case series and case-based systematic review. Clin Neuroradiol, 2023, 33(3): 833-842.
35.	Richardson M, Garner P, Donegan S. Interpretation of subgroup analyses in systematic reviews: a tutorial. Clin Epidemiol Glob Health, 2019, 7: 192-198.

1. Lawton MT, Rutledge WC, Kim H, et al. Brain arteriovenous malformations. Nat Rev Dis Primers, 2015, 1: 15008.
2. Davidoff CL, Lo Presti A, Rogers JM, et al. Risk of first hemorrhage of brain arteriovenous malformations during pregnancy: a systematic review of the literature. Neurosurgery, 2019, 85(5): E806-E814.
3. Hongo H, Miyawaki S, Teranishi Y, et al. Genetics of brain arteriovenous malformations and cerebral cavernous malformations. J Hum Genet, 2023, 68(3): 157-167.
4. Lv X, Li Y. The clinical characteristics and treatment of cerebral AVM in pregnancy. Neuroradiol J, 2015, 28(4): 385-388.
5. Trivedi RA, Kirkpatrick PJ. Arteriovenous malformations of the cerebral circulation that rupture in pregnancy. J Obstet Gynaecol, 2003, 23(5): 484-489.
6. Liu J, Luo C, Guo Y, et al. Individual trigger factors for hemorrhagic stroke: Evidence from case-crossover and self-controlled case series studies. Eur Stroke J, 2023, 8(3): 808-818.
7. Zhong Z, Ni H, Zhu J, et al. Management of acute hemorrhage caused by cerebral arteriovenous malformation during pregnancy-case series and literature review. World Neurosurg, 2021, 152: e688-e699.
8. Can A, Du R. Neurosurgical issues in pregnancy. Semin Neurol, 2017, 37(6): 689-693.
9. 吕宪利, 刘鹏, 李佑祥. 妊娠期颅内动静脉畸形的临床特征和治疗进展. 中华神经外科杂志, 2015, 31(6): 633-635.
10. Yih PS, Cheong KF. Anaesthesia for caesarean section in a patient with an intracranial arteriovenous malformation. Anaesth Intensive Care, 1999, 27(1): 66-68.
11. Coskun D, Mahli A, Yilmaz Z, et al. Anesthetic management of caesarean section of a pregnant woman with cerebral arteriovenous malformation: a case report. Cases J, 2008, 1(1): 327.
12. De Maria L, Serioli S, Fontanella MM. Brain arteriovenous malformations and pregnancy: a systematic review of the literature. World Neurosurg, 2023, 177: 100-108.
13. Zeng X, Zhang Y, Kwong JS, et al. The methodological quality assessment tools for preclinical and clinical studies, systematic review and meta-analysis, and clinical practice guideline: a systematic review. J Evid Based Med, 2015, 8(1): 2-10.
14. Algra AM, Lindgren A, Vergouwen MDI, et al. Procedural clinical complications, case-fatality risks, and risk factors in endovascular and neurosurgical treatment of unruptured intracranial aneurysms: a systematic review and meta-analysis. JAMA Neurol, 2019, 76(3): 282-293.
15. Li C, Matthies L, Hou X, et al. A meta-analysis of the pros and cons of partial superficial parotidectomy versus superficial parotidectomy for the treatment of benign parotid neoplasms. J Craniomaxillofac Surg, 2020, 48(6): 590-598.
16. Robinson JL, Hall CS, Sedzimir CB. Arteriovenous malformations, aneurysms, and pregnancy. J Neurosurg, 1974, 41(1): 63-70.
17. Horton JC, Chambers WA, Lyons SL, et al. Pregnancy and the risk of hemorrhage from cerebral arteriovenous malformations. Neurosurgery, 1990, 27(6): 867-871.
18. Katsuragi S, Yoshimatsu J, Tanaka H, et al. Management of pregnancy complicated with intracranial arteriovenous malformation. J Obstet Gynaecol Res, 2018, 44(4): 673-680.
19. Forster DM, Kunkler IH, Hartland P. Risk of cerebral bleeding from arteriovenous malformations in pregnancy: the Sheffield experience. Stereotact Funct Neurosurg, 1993, 61(Suppl 1): 20-22.
20. van Beijnum J, Wilkinson T, Whitaker HJ, et al. Relative risk of hemorrhage during pregnancy in patients with brain arteriovenous malformations. Int J Stroke, 2017, 12(7): 741-747.
21. Gross BA, Du R. Hemorrhage from arteriovenous malformations during pregnancy. Neurosurgery, 2012, 71(2): 349-355.
22. Tonetti D, Kano H, Bowden G, et al. Hemorrhage during pregnancy in the latency interval after stereotactic radiosurgery for arteriovenous malformations. J Neurosurg, 2014, 121(Suppl): 226-231.
23. Yan KL, Ko NU, Hetts SW, et al. Maternal and fetal outcomes in women with brain arteriovenous malformation rupture during pregnancy. Cerebrovasc Dis, 2021, 50(3): 296-302.
24. Porras JL, Yang W, Philadelphia E, et al. Hemorrhage risk of brain arteriovenous malformations during pregnancy and puerperium in a north American cohort. Stroke, 2017, 48(6): 1507-1513.
25. Liu XJ, Wang S, Zhao YL, et al. Risk of cerebral arteriovenous malformation rupture during pregnancy and puerperium. Neurology, 2014, 82(20): 1798-1803.
26. Lv X, Li W, He H, et al. Known and unknown cerebral arteriovenous malformations in pregnancies: haemorrhage risk and influence on obstetric management. Neuroradiol J, 2017, 30(5): 437-441.
27. Zhu D, Zhao P, Lv N, et al. Rupture risk of cerebral arteriovenous malformations during pregnancy and puerperium: a single-center experience and pooled data analysis. World Neurosurg, 2018, 111: e308-e315.
28. Liu J, Zhang H, Luo C, et al. Haemorrhage risk of brain arteriovenous malformation during pregnancy and puerperium. Stroke Vasc Neurol, 2023, 8(4): 307-317.
29. 李晨曦, 陈程, 吕小毅, 等. 拉曼光谱辅助诊断结肠癌准确性的Meta分析. 中国循证医学杂志, 2022, 22(6): 649-654.
30. van Beijnum J, van der Worp HB, Schippers HM, et al. Familial occurrence of brain arteriovenous malformations: a systematic review. J Neurol Neurosurg Psychiatry, 2007, 78(11): 1213-1217.
31. Hashimoto T, Lawton MT, Wen G, et al. Gene microarray analysis of human brain arteriovenous malformations. Neurosurgery, 2004, 54(2): 410-423.
32. Pawlikowska L, Tran MN, Achrol AS, et al. Polymorphisms in genes involved in inflammatory and angiogenic pathways and the risk of hemorrhagic presentation of brain arteriovenous malformations. Stroke, 2004, 35(10): 2294-2300.
33. Kato Y, Dong VH, Chaddad F, et al. Expert consensus on the management of brain arteriovenous malformations. Asian J Neurosurg, 2019, 14(4): 1074-1081.
34. Etter MM, Nguyen A, Brehm A, et al. Endovascular treatment and peri-interventional management of ruptured cerebrovascular lesions during pregnancy: case series and case-based systematic review. Clin Neuroradiol, 2023, 33(3): 833-842.
35. Richardson M, Garner P, Donegan S. Interpretation of subgroup analyses in systematic reviews: a tutorial. Clin Epidemiol Glob Health, 2019, 7: 192-198.

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