Infective endocarditis complicated with intracranial hemorrhage: A report of three cases_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

QING Hongkun ,  JIAN Xuhua

Department of Cardiac Surgery, Guangdong Cardiovascular Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, 510010, P. R. China;

Corresponding author：

JIAN Xuhua, Email: jianxuhua@gdph.org.cn

Keywords：

Infective endocarditis; intracranial hemorrhage; infectious intracranial aneurysm; surgical timing; review

DOI：

10.7507/1007-4848.202406033

Video：

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Intracranial hemorrhage (ICH) represents a severe complication of infective endocarditis (IE) and stands as a significant contributor to the poor prognosis associated with IE. Current guidelines suggested a delay of 4 weeks for cardiac surgery in patients with ICH, but these recommendations were based on insufficient clinical evidence, and recent studies have yielded different opinions. In this paper, we thoroughly reviewed relevant guidelines and their references in conjunction with 3 typical cases with IE and ICH, discussed the recommendations with controversy, and proposed a process for the management of IE with ICH.

1.	Delgado V, Ajmone MN, de Waha S, et al. 2023 ESC guidelines for the management of endocarditis. Eur Heart J, 2023, 44(39): 3948-4042.
2.	Lee J, Lim H A, Hong S B, et al. Is preoperative intracranial hemorrhage a surgical contraindication in infective endocarditis with stroke? J Thorac Dis, 2023, 15(9): 4765-4774.
3.	García-Cabrera E, Fernández-Hidalgo N, Almirante B, et al. Neurological complications of infective endocarditis. Circulation, 2013, 127(23): 2272-2284.
4.	Nakatani S, Ohara T, Ashihara K, et al. JCS 2017 guideline on prevention and treatment of infective endocarditis. Circ J, 2019, 83(8): 1767-1809.
5.	Otto CM, Nishimura RA, Bonow RO, et al. 2020 ACC/AHA guideline for the management of patients with valvular heart disease. J Thorac Cardiovasc Surg, 2021, 162(2): e183-e353.
6.	中华医学会胸心血管外科分会瓣膜病外科学组. 感染性心内膜炎外科治疗中国专家共识. 中华胸心血管外科杂志, 2022, 38(3): 146-155.Group of Valve Surgery, Chinese Society for Thoracic and Cardiovascular Surgery. Chinese expert consensus on surgical treatment of infective endocarditis. Chin J Thorac Cardiovasc Surg, 2022, 38(3): 146-155.
7.	Pettersson GB, Coselli JS, et al. 2016 the American Association for Thoracic Surgery (AATS) consensus guidelines: Surgical treatment of infective endocarditis: Executive summary. J Thorac Cardiovasc Surg, 2017, 153(6): 1241-1258.
8.	Eishi K, Kawazoe K, Kuriyama Y, et al. Surgical management of infective endocarditis associated with cerebral complications. Multi-center retrospective study in Japan. J Thorac Cardiovasc Surg, 1995, 110(6): 1745-1755.
9.	Habib G, Lancellotti P, Antunes MJ, et al. 2015 ESC guidelines for the management of infective endocarditis. Eur Heart J, 2015, 36(44): 3075-3128.
10.	Shang E, Forrest GN, Chizmar T, et al. Mitral valve infective endocarditis: benefit of early operation and aggressive use of repair. Ann Thorac Surg, 2009, 87(6): 1728-1733,1734.
11.	Wilbring M, Irmscher L, Alexiou K, et al. The impact of preoperative neurological events in patients suffering from native infective valve endocarditis. Interact Cardiovasc Thorac Surg, 2014, 18(6): 740-747.
12.	Yoshioka D, Toda K, Sakaguchi T, et al. Valve surgery in active endocarditis patients complicated by intracranial haemorrhage: The influence of the timing of surgery on neurological outcomes. Eur J Cardiothorac Surg, 2014, 45(6): 1082-1088.
13.	Okita Y, Minakata K, Yasuno S, et al. Optimal timing of surgery for active infective endocarditis with cerebral complications: A Japanese multicentre study. Eur J Cardiothorac Surg, 2016, 50(2): 374-382.
14.	Kume Y, Fujita T, Fukushima S, et al. Intracranial mycotic aneurysm is associated with cerebral bleeding post-valve surgery for infective endocarditis. Interact Cardiovasc Thorac Surg, 2018, 27(5): 635-641.
15.	Salaun E, Touil A, Hubert S, et al. Intracranial haemorrhage in infective endocarditis. Arch Cardiovasc Dis, 2018, 111(12): 712-721.
16.	Diab M, Musleh R, Lehmann T, et al. Risk of postoperative neurological exacerbation in patients with infective endocarditis and intracranial haemorrhage. Eur J Cardiothorac Surg, 2021, 59(2): 426-433.
17.	Tam DY, Yanagawa B, Verma S, et al. Early vs. late surgery for patients with endocarditis and neurological injury: a systematic review and meta-analysis. Can J Cardiol, 2018, 34(9): 1185-1199.
18.	Musleh R, Schlattmann P, Caldonazo T, et al. Surgical timing in patients with infective endocarditis and with intracranial hemorrhage: A systematic review and meta‐analysis. J Am Heart Assoc, 2022, 11(10).
19.	Suzuki M, Takanashi S, Ohshima Y, et al. Critical potential of early cardiac surgery for infective endocarditis with cardio-embolic strokes. Int J Cardiol, 2017, 227: 222-224.
20.	Klug D, Lacroix D, Savoye C, et al. Systemic infection related to endocarditis on pacemaker leads: Clinical presentation and management. Circulation, 1997, 95(8): 2098-2107.
21.	Arregle F, Martel H, Philip M, et al. Infective endocarditis with neurological complications: Delaying cardiac surgery is associated with worse outcome. Arch Cardiovasc Dis, 2021, 114(8-9): 527-536.
22.	álvarez ZS, Vazquez AP, Muñoz P, et al. Prevalence and prognostic impact of stroke in a national cohort of infective endocarditis. Int J Stroke, 2024. [Epub ahead of print].
23.	de Miguel M, López J, Vilacosta I, et al. Clinical profile and prognosis of patients with left-sided infective endocarditis with surgical indication who are not operated. Microorganisms, 2024, 12(3): 607.
24.	Rost NS, Smith EE, Chang Y, et al. Prediction of functional outcome in patients with primary intracerebral hemorrhage: The FUNC score. Stroke, 2008, 39(8): 2304-2309.
25.	Venn RA, Ning M, Vlahakes GJ, et al. Surgical timing in infective endocarditis complicated by intracranial hemorrhage. Am Heart J, 2019, 216: 102-112.
26.	Runde D. Calculated decisions: NIH Stroke Scale/Score (NIHSS). Emerg Med Pract, 2021, 23(Suppl 6): CD3-CD5.
27.	Hui FK, Bain M, Obuchowski NA, et al. Mycotic aneurysm detection rates with cerebral angiography in patients with infective endocarditis. J Neurointerv Surg, 2015, 7(6): 449-452.
28.	Peters PJ, Harrison T, Lennox JL. A dangerous dilemma: Management of infectious intracranial aneurysms complicating endocarditis. Lancet Infect Dis, 2006, 6(11): 742-748.
29.	Alawieh AM, Dimisko L, Newman S, et al. Management and long-term outcomes of patients with infectious intracranial aneurysms. Neurosurgery, 2023, 92(3): 515-523.
30.	Ragulojan R, Grupke S, Fraser JF. Systematic review of endovascular, surgical, and conservative options for infectious intracranial aneurysms and cardiac considerations. J Stroke Cerebrovasc Dis, 2019, 28(3): 838-844.
31.	Ducruet AF, Hickman ZL, Zacharia BE, et al. Intracranial infectious aneurysms: A comprehensive review. Neurosurg Rev, 2010, 33(1): 37-46.
32.	Petr O, Brinjikji W, Burrows AM, et al. Safety and efficacy of endovascular treatment for intracranial infectious aneurysms: A systematic review and meta-analysis. J Neuroradiol, 2016, 43(5): 309-316.
33.	Cheng-Ching E, John S, Bain M, et al. Endovascular embolization of intracranial infectious aneurysms in patients undergoing open heart surgery using n-butyl cyanoacrylate. Interv Neurol, 2017, 6(1-2): 82-89.
34.	Serrano F, Guédon A, Saint-Maurice J, et al. Endovascular treatment of infectious intracranial aneurysms complicating infective endocarditis: A series of 31 patients with 55 aneurysms. Neuroradiology, 2022, 64(2): 353-360.
35.	卿洪琨, 王维腾, 陈帆宇, 等. 感染性心内膜炎相关颅内动脉瘤的特征和治疗. 中国胸心血管外科临床杂志, 2024. Epub ahead of print.Qing HK, Wang WT, Chen FY, et al. Clinical characteristics and treatment of infectious intracranial aneurysm related to infective endocarditis. Chin J Clin Thorac Cardiovasc Surg, 2024. Epub ahead of print.
36.	Klein I, Iung B, Labreuche J, et al. Cerebral microbleeds are frequent in infective endocarditis. Stroke, 2009, 40(11): 3461-3465.
37.	Okazaki S, Sakaguchi M, Hyun B, et al. Cerebral microbleeds predict impending intracranial hemorrhage in infective endocarditis. Cerebrovasc Dis, 2011, 32(5): 483-488.
38.	Murai R, Kaji S, Kitai T, et al. The clinical significance of cerebral microbleeds in infective endocarditis patients. Semin Thorac Cardiovasc Surg, 2019, 31(1): 51-58.
39.	Goulenok T, Klein I, Mazighi M, et al. Infective endocarditis with symptomatic cerebral complications: Contribution of cerebral magnetic resonance imaging. Cerebrovasc Dis, 2013, 35(4): 327-336.
40.	Sorabella RA, Han SM, Grbic M, et al. Early operation for endocarditis complicated by preoperative cerebral emboli is not associated with worsened outcomes. Ann Thorac Surg, 2015, 100(2): 501-508.
41.	Yamazato T, Oyama N, Fujii T, et al. Aggressive early surgical strategy in patients with intracranial hemorrhage: A new cardiopulmonary bypass option. Gen Thorac Cardiovasc Surg, 2022, 70(7): 602-610.

1. Delgado V, Ajmone MN, de Waha S, et al. 2023 ESC guidelines for the management of endocarditis. Eur Heart J, 2023, 44(39): 3948-4042.
2. Lee J, Lim H A, Hong S B, et al. Is preoperative intracranial hemorrhage a surgical contraindication in infective endocarditis with stroke? J Thorac Dis, 2023, 15(9): 4765-4774.
3. García-Cabrera E, Fernández-Hidalgo N, Almirante B, et al. Neurological complications of infective endocarditis. Circulation, 2013, 127(23): 2272-2284.
4. Nakatani S, Ohara T, Ashihara K, et al. JCS 2017 guideline on prevention and treatment of infective endocarditis. Circ J, 2019, 83(8): 1767-1809.
5. Otto CM, Nishimura RA, Bonow RO, et al. 2020 ACC/AHA guideline for the management of patients with valvular heart disease. J Thorac Cardiovasc Surg, 2021, 162(2): e183-e353.
6. 中华医学会胸心血管外科分会瓣膜病外科学组. 感染性心内膜炎外科治疗中国专家共识. 中华胸心血管外科杂志, 2022, 38(3): 146-155.Group of Valve Surgery, Chinese Society for Thoracic and Cardiovascular Surgery. Chinese expert consensus on surgical treatment of infective endocarditis. Chin J Thorac Cardiovasc Surg, 2022, 38(3): 146-155.
7. Pettersson GB, Coselli JS, et al. 2016 the American Association for Thoracic Surgery (AATS) consensus guidelines: Surgical treatment of infective endocarditis: Executive summary. J Thorac Cardiovasc Surg, 2017, 153(6): 1241-1258.
8. Eishi K, Kawazoe K, Kuriyama Y, et al. Surgical management of infective endocarditis associated with cerebral complications. Multi-center retrospective study in Japan. J Thorac Cardiovasc Surg, 1995, 110(6): 1745-1755.
9. Habib G, Lancellotti P, Antunes MJ, et al. 2015 ESC guidelines for the management of infective endocarditis. Eur Heart J, 2015, 36(44): 3075-3128.
10. Shang E, Forrest GN, Chizmar T, et al. Mitral valve infective endocarditis: benefit of early operation and aggressive use of repair. Ann Thorac Surg, 2009, 87(6): 1728-1733,1734.
11. Wilbring M, Irmscher L, Alexiou K, et al. The impact of preoperative neurological events in patients suffering from native infective valve endocarditis. Interact Cardiovasc Thorac Surg, 2014, 18(6): 740-747.
12. Yoshioka D, Toda K, Sakaguchi T, et al. Valve surgery in active endocarditis patients complicated by intracranial haemorrhage: The influence of the timing of surgery on neurological outcomes. Eur J Cardiothorac Surg, 2014, 45(6): 1082-1088.
13. Okita Y, Minakata K, Yasuno S, et al. Optimal timing of surgery for active infective endocarditis with cerebral complications: A Japanese multicentre study. Eur J Cardiothorac Surg, 2016, 50(2): 374-382.
14. Kume Y, Fujita T, Fukushima S, et al. Intracranial mycotic aneurysm is associated with cerebral bleeding post-valve surgery for infective endocarditis. Interact Cardiovasc Thorac Surg, 2018, 27(5): 635-641.
15. Salaun E, Touil A, Hubert S, et al. Intracranial haemorrhage in infective endocarditis. Arch Cardiovasc Dis, 2018, 111(12): 712-721.
16. Diab M, Musleh R, Lehmann T, et al. Risk of postoperative neurological exacerbation in patients with infective endocarditis and intracranial haemorrhage. Eur J Cardiothorac Surg, 2021, 59(2): 426-433.
17. Tam DY, Yanagawa B, Verma S, et al. Early vs. late surgery for patients with endocarditis and neurological injury: a systematic review and meta-analysis. Can J Cardiol, 2018, 34(9): 1185-1199.
18. Musleh R, Schlattmann P, Caldonazo T, et al. Surgical timing in patients with infective endocarditis and with intracranial hemorrhage: A systematic review and meta‐analysis. J Am Heart Assoc, 2022, 11(10).
19. Suzuki M, Takanashi S, Ohshima Y, et al. Critical potential of early cardiac surgery for infective endocarditis with cardio-embolic strokes. Int J Cardiol, 2017, 227: 222-224.
20. Klug D, Lacroix D, Savoye C, et al. Systemic infection related to endocarditis on pacemaker leads: Clinical presentation and management. Circulation, 1997, 95(8): 2098-2107.
21. Arregle F, Martel H, Philip M, et al. Infective endocarditis with neurological complications: Delaying cardiac surgery is associated with worse outcome. Arch Cardiovasc Dis, 2021, 114(8-9): 527-536.
22. álvarez ZS, Vazquez AP, Muñoz P, et al. Prevalence and prognostic impact of stroke in a national cohort of infective endocarditis. Int J Stroke, 2024. [Epub ahead of print].
23. de Miguel M, López J, Vilacosta I, et al. Clinical profile and prognosis of patients with left-sided infective endocarditis with surgical indication who are not operated. Microorganisms, 2024, 12(3): 607.
24. Rost NS, Smith EE, Chang Y, et al. Prediction of functional outcome in patients with primary intracerebral hemorrhage: The FUNC score. Stroke, 2008, 39(8): 2304-2309.
25. Venn RA, Ning M, Vlahakes GJ, et al. Surgical timing in infective endocarditis complicated by intracranial hemorrhage. Am Heart J, 2019, 216: 102-112.
26. Runde D. Calculated decisions: NIH Stroke Scale/Score (NIHSS). Emerg Med Pract, 2021, 23(Suppl 6): CD3-CD5.
27. Hui FK, Bain M, Obuchowski NA, et al. Mycotic aneurysm detection rates with cerebral angiography in patients with infective endocarditis. J Neurointerv Surg, 2015, 7(6): 449-452.
28. Peters PJ, Harrison T, Lennox JL. A dangerous dilemma: Management of infectious intracranial aneurysms complicating endocarditis. Lancet Infect Dis, 2006, 6(11): 742-748.
29. Alawieh AM, Dimisko L, Newman S, et al. Management and long-term outcomes of patients with infectious intracranial aneurysms. Neurosurgery, 2023, 92(3): 515-523.
30. Ragulojan R, Grupke S, Fraser JF. Systematic review of endovascular, surgical, and conservative options for infectious intracranial aneurysms and cardiac considerations. J Stroke Cerebrovasc Dis, 2019, 28(3): 838-844.
31. Ducruet AF, Hickman ZL, Zacharia BE, et al. Intracranial infectious aneurysms: A comprehensive review. Neurosurg Rev, 2010, 33(1): 37-46.
32. Petr O, Brinjikji W, Burrows AM, et al. Safety and efficacy of endovascular treatment for intracranial infectious aneurysms: A systematic review and meta-analysis. J Neuroradiol, 2016, 43(5): 309-316.
33. Cheng-Ching E, John S, Bain M, et al. Endovascular embolization of intracranial infectious aneurysms in patients undergoing open heart surgery using n-butyl cyanoacrylate. Interv Neurol, 2017, 6(1-2): 82-89.
34. Serrano F, Guédon A, Saint-Maurice J, et al. Endovascular treatment of infectious intracranial aneurysms complicating infective endocarditis: A series of 31 patients with 55 aneurysms. Neuroradiology, 2022, 64(2): 353-360.
35. 卿洪琨, 王维腾, 陈帆宇, 等. 感染性心内膜炎相关颅内动脉瘤的特征和治疗. 中国胸心血管外科临床杂志, 2024. Epub ahead of print.Qing HK, Wang WT, Chen FY, et al. Clinical characteristics and treatment of infectious intracranial aneurysm related to infective endocarditis. Chin J Clin Thorac Cardiovasc Surg, 2024. Epub ahead of print.
36. Klein I, Iung B, Labreuche J, et al. Cerebral microbleeds are frequent in infective endocarditis. Stroke, 2009, 40(11): 3461-3465.
37. Okazaki S, Sakaguchi M, Hyun B, et al. Cerebral microbleeds predict impending intracranial hemorrhage in infective endocarditis. Cerebrovasc Dis, 2011, 32(5): 483-488.
38. Murai R, Kaji S, Kitai T, et al. The clinical significance of cerebral microbleeds in infective endocarditis patients. Semin Thorac Cardiovasc Surg, 2019, 31(1): 51-58.
39. Goulenok T, Klein I, Mazighi M, et al. Infective endocarditis with symptomatic cerebral complications: Contribution of cerebral magnetic resonance imaging. Cerebrovasc Dis, 2013, 35(4): 327-336.
40. Sorabella RA, Han SM, Grbic M, et al. Early operation for endocarditis complicated by preoperative cerebral emboli is not associated with worsened outcomes. Ann Thorac Surg, 2015, 100(2): 501-508.
41. Yamazato T, Oyama N, Fujii T, et al. Aggressive early surgical strategy in patients with intracranial hemorrhage: A new cardiopulmonary bypass option. Gen Thorac Cardiovasc Surg, 2022, 70(7): 602-610.

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