CC BY-NC-ND 4.0 · Asian J Neurosurg 2024; 19(04): 812-815
DOI: 10.1055/s-0044-1791189
Case Report

Successful Microsurgical Clipping under Extracorporeal Membrane Oxygenation Treatment for a Poor-Grade Subarachnoid Hemorrhage Patient with Severe Pulmonary Neurogenic Lung

1   Department of Neurosurgery, Saiseikai Utsunomiya Hospital, Utsunomiya, Tochigi, Japan
2   Department of Neurosurgery, Dokkyo Medical University, Shimotsugagun, Tochigi, Japan
,
Shoko Ito
1   Department of Neurosurgery, Saiseikai Utsunomiya Hospital, Utsunomiya, Tochigi, Japan
,
Takahiro Miyata
1   Department of Neurosurgery, Saiseikai Utsunomiya Hospital, Utsunomiya, Tochigi, Japan
,
Keita Mayanagi
1   Department of Neurosurgery, Saiseikai Utsunomiya Hospital, Utsunomiya, Tochigi, Japan
,
1   Department of Neurosurgery, Saiseikai Utsunomiya Hospital, Utsunomiya, Tochigi, Japan
,
Masashi Nakatsukasa
1   Department of Neurosurgery, Saiseikai Utsunomiya Hospital, Utsunomiya, Tochigi, Japan
› Author Affiliations
Funding None.
 

Abstract

Hemorrhagic strokes are considered as contraindications of extracorporeal membrane oxygenation (ECMO) therapy because of anticoagulant administration and ECMO-associated coagulopathy. We present a rare case of successful microsurgical clipping under ECMO for a poor-grade subarachnoid hemorrhage (SAH) patient with severe neurogenic pulmonary edema (NPE). A 50-year-old man presenting with the sudden loss of consciousness was diagnosed with poor-grade SAH with severe NPE, and was intubated. Because of severe hypoxemia refractory to conventional treatment, venovenous ECMO was used 6 hours after admission. To avoid thrombosis inside the ECMO circuit despite no anticoagulants, a heparin-bonded ECMO was maintained at a comparatively high blood flow rate. Subsequently, the patient underwent a microsurgical clipping under ECMO. Intraoperatively we had difficulty in bleeding control, and therefore the multiple transfusions were necessary to correct anemia and ECMO-associated coagulopathy. The aneurysmal clipping was accomplished without hemorrhagic intracranial complications. After 2 years from onset, his activities of daily life were independent. To our knowledge, this is the first report of successful microsurgical clipping for poor-grade SAH under ECMO without any anticoagulants. The use of a heparin-bonded ECMO tubing, maintenance of a slightly higher ECMO pump speed, and multiple transfusions to correct ECMO-associated coagulopathy could make the micro-neurosurgical procedures under ECMO possible. This report demonstrated the possibility to extend the range of application of microsurgical clipping for poor-grade SAH patients requiring ECMO treatment.


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Introduction

In the acute neurocritical care region, extracorporeal membrane oxygenation (ECMO) has been thought to be of limited use due to the concomitant need for anticoagulation.[1] [2] [3] Thus, the accumulation of clinical evidence about ECMO management in the neurosurgical intervention is essential. Here, we present a successful case of microsurgical aneurysmal clipping during venovenous ECMO for World Federation of Neurological Societies (WFNS) grade V subarachnoid hemorrhage (SAH) with severe neurogenic pulmonary edema (NPE).


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Case Presentation

A 50-year-old man was admitted to our hospital due to sudden loss of consciousness. His vital signs were as follows: blood pressure 80/58 mm Hg, heart rate 65 beats/min, and oxygen saturation 85% under 10 L/min oxygen in a reservoir mask. A chest computed tomography (CT; [Fig. 1a]) and an echocardiography revealed an NPE and a stress-induced cardiomyopathy, and the patient was intubated. Head CT and CT angiography ([Fig. 1b, c]) showed SAH with multiple aneurysms. Because of poor clinical course at admission, this patient was diagnosed as WFNS grade V SAH. Owing to the aneurysmal size, shape, and location, microsurgical clipping was considered to be preferable to endovascular treatment, which is the preferred treatment in serious systemic conditions. Repeated arterial blood gas analyses showed severe hypoxemia refractory to conventional treatment. Therefore, we initiated venovenous ECMO ([Fig. 2]). To avoid thrombosis inside the ECMO circuit despite no anticoagulants, a heparin-bonded ECMO was maintained at a comparatively high flow rate (4.2 L/min). Gradually, low blood pressure improved without vasopressor administration. On day 3, we decided to perform a microsurgical clipping on ECMO. Intraoperatively we had difficulty in bleeding control because of low platelet count, and a very bloody surgical field led to poor vision of the microscope ([Fig. 3a]). After the transfusion of 6 units red blood cells and 20 units platelets to correct anemia and coagulopathy, we managed to apply clips for all the aneurysms ([Fig. 3b]). Intraoperative blood loss was approximately 640 mL. Postoperatively ECMO weaning was successful. The patient was doing well except for lenticulostriate artery (LSA) infarction ([Fig. 3c]). After 2 years from onset, his neurological examination showed only a slight hemiparesis. His activities of daily life were independent (modified ranking scale 1).

Zoom Image
Fig. 1 (A) Chest computed tomography (CT) on admission shows neurogenic pulmonary edema in both lungs. (B) Head CT and (C) CT angiography on admission show diffuse subarachnoid hemorrhage and an anterior choroidal artery aneurysm and two middle cerebral artery aneurysms (red arrows).
Zoom Image
Fig. 2 Chest X-ray after the extracorporeal membrane oxygenation cannulation shows two single lumen cannulas, draining from the inferior vena cava (IVC) and reinfusing into the IVC/right atrium. The black arrow shows the tip of the draining venous cannula, and the two black arrowheads show the reinfusion cannula.
Zoom Image
Fig. 3 (A) An intraoperative photograph during the dissection of sylvian fissure shows very bloody surgical field and poor vision of the microscope. (B) The anteroposterior view of postoperative computed tomography angiography shows complete neck clipping. (C) A head computed tomography performed 1 month after the operation shows a right lenticulostriate artery infarction.

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Discussion

Although ECMO can be a last-resort treatment for patients with severe acute respiratory failure, neurosurgical interventions are generally considered contraindications for ECMO therapy because ECMO may increase additional neurological injuries such as intracranial hemorrhage and ischemic stroke.[4] [5] [6] In particular, the use of systemic anticoagulation and impaired hemostasis due to platelet consumption and its dysfunction during ECMO can increase intracranial hemorrhagic complication. Thus, avoiding systemic anticoagulation and considering platelet transfusion are desirable when neurosurgical interventions are performed for intracranial hemorrhagic patients on ECMO.

The recent improvements in ECMO devices may make the use of heparin-free ECMO possible.[1] [6] [7] Arlt et al[8] reported that heparin-free ECMO could be a safe alternate rescue treatment in patients with severe trauma and hemorrhagic shock. Faulkner et al[1] also reported the successful utilization of venovenous ECMO for severe respiratory failure secondary to aneurysmal SAH after endovascular coiling. To reduce the risk of clot formation in the oxygenator and venous thromboembolism even without any anticoagulants, they used short lengths of heparin-bonded venovenous ECMO tubing and maintained the venovenous ECMO pump speed at a slightly higher-than-normal speed for increased flow throughout the ECMO circuit.[1] However, most of such successful reports about the utilization of ECMO in the acute neurocritical care region were dominantly limited to macro-neurosurgical interventions and postmicrosurgical management.[1] [9] [10] There was an extremely rare report of a successful microsurgical intervention under ECMO.

According to our literature review, Hwang et al[11] were the first to report successful aneurysmal clipping under ECMO by using nafamostat mesylate alternatively as a regional anticoagulant for an SAH patient with NPE. To our knowledge, the present case is the first report of successful microsurgical clipping for SAH during ECMO without any anticoagulants.

Preoperative management should begin with a critical evaluation of whether the patient can be weaned from ECMO prior to the cerebral aneurysm surgery. If weaning from ECMO is possible, careful attention to ECMO-associated coagulopathy is not needed and, therefore, surgery can be performed under standard general anesthesia management for cerebral aneurysmal clipping surgery. The next step is to determine the feasibility of endovascular treatment. If ECMO weaning is not possible and the ruptured cerebral aneurysm can be fully treatable with the endovascular treatment, this approach is preferable to the direct surgery. In the cases where direct surgery is unavoidable, it is crucial to plan a preoperative simulation so that the surgical procedures can be conducted minimally invasively in the shortest possible time.

According to the Extracorporeal Life Support Organization (ELSO) guidelines,[12] relevant literature,[13] and our experience with this case, intraoperative management by anesthesiologists should include red blood cell transfusion to maintain hemoglobin levels between 7 and 9 g/dL. Platelet transfusions should be administered based on the extent of intraoperative bleeding; however, it is essential to maintain a platelet count above 100,000/µL to avoid a bloody surgical field, especially during microscopic procedures. Fresh frozen plasma transfusion is recommended to maintain fibrinogen levels between 250 and 300 mg/dL. For neurosurgeons, the primary focus during surgery must be on meticulous bleeding control. In the direct surgery for ruptured middle cerebral artery aneurysms like the present case, a distal sylvian approach should be selected whenever possible, because the extent of microsurgical dissection is minimally required. In addition, proximal control should be achieved with minimal exposure of the M1 segment for the application of a temporary clip. If the surgical field becomes bloody, timely replacement of platelets and coagulation factors is essential, along with precise bipolar coagulation and the use of suitable hemostatic agents. In the present case, the bipolar coagulation in a bloody surgical field during M1 exposure may have contributed to LSA infarction. Among hemostatic agents, a topical gelatin-thrombin hemostatic matrix such as FLOSEAL appears to be particularly effective. Literature[14] supports FLOSEAL's efficacy in achieving hemostasis, especially in cases of diffuse bleeding or when bleeding points are difficult to identify. FLOSEAL's effectiveness has been demonstrated even in patients under heparinization.[15] Such a hemostatic agent is likely well suited for use in microsurgical procedures for patients with bleeding tendencies on ECMO.


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Conclusion

The use of a heparin-bonded ECMO tubing, maintenance of a slightly higher ECMO pump speed, and preparation of enough platelet transfusion to correct coagulopathy are essential to perform a safe and precise microsurgical procedure for SAH patients on ECMO without any anticoagulants. This report demonstrated the possibility to extend the range of application of microsurgical clipping for poor-grade SAH patients requiring ECMO treatment.


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Conflict of Interest

None declared.

Authors' Contributions

K.S. was responsible for conceptualization, formal analysis, project administration, visualization, writing the original draft, writing, review, and editing of manuscript. Data curation was done by K.S. and S.I. Methodology was developed by K.S., T.M., K.M., J.I., and M.N.


  • References

  • 1 Faulkner AL, Bacon JD, Fischer BA, Grupke SL, Hatton KW. Successful extracorporeal membrane oxygenation (ECMO) use without systemic anticoagulation for acute respiratory distress syndrome in a patient with aneurysmal subarachnoid hemorrhage. Case Rep Neurol Med 2019; 2019: 9537453
  • 2 Lorusso R, Gelsomino S, Parise O. et al. Neurologic injury in adults supported with veno-venous extracorporeal membrane oxygenation for respiratory failure: findings from the Extracorporeal Life Support Organization Database. Crit Care Med 2017; 45 (08) 1389-1397
  • 3 Tonna JE, Abrams D, Brodie D. et al. Management of adult patients supported with venovenous extracorporeal membrane oxygenation (VV ECMO): Guideline from the Extracorporeal Life Support Organization (ELSO). ASAIO J 2021; 67 (06) 601-610
  • 4 Cartwright B, Bruce HM, Kershaw G. et al. Hemostasis, coagulation and thrombin in venoarterial and venovenous extracorporeal membrane oxygenation: the HECTIC study. Sci Rep 2021; 11 (01) 7975
  • 5 Kalbhenn J, Wittau N, Schmutz A, Zieger B, Schmidt R. Identification of acquired coagulation disorders and effects of target-controlled coagulation factor substitution on the incidence and severity of spontaneous intracranial bleeding during veno-venous ECMO therapy. Perfusion 2015; 30 (08) 675-682
  • 6 Olson SR, Murphree CR, Zonies D. et al. Thrombosis and bleeding in extracorporeal membrane oxygenation (ECMO) without anticoagulation: a systematic review. ASAIO J 2021; 67 (03) 290-296
  • 7 Sy E, Sklar MC, Lequier L, Fan E, Kanji HD. Anticoagulation practices and the prevalence of major bleeding, thromboembolic events, and mortality in venoarterial extracorporeal membrane oxygenation: a systematic review and meta-analysis. J Crit Care 2017; 39: 87-96
  • 8 Arlt M, Philipp A, Voelkel S. et al. Extracorporeal membrane oxygenation in severe trauma patients with bleeding shock. Resuscitation 2010; 81 (07) 804-809
  • 9 Anton-Martin P, Braga B, Megison S, Journeycake J, Moreland J. Craniectomy and traumatic brain injury in children on extracorporeal membrane oxygenation support. Pediatr Emerg Care 2018; 34 (11) e204-e210
  • 10 Bindal S, Conner CR, Akkanti B. et al. Multiple decompressive craniectomies and hematoma evacuation in a patient undergoing extracorporeal membrane oxygenation. Interdiscip Neurosurg 2022; 30: 101610
  • 11 Hwang GJ, Sheen SH, Kim HS. et al. Extracorporeal membrane oxygenation for acute life-threatening neurogenic pulmonary edema following rupture of an intracranial aneurysm. J Korean Med Sci 2013; 28 (06) 962-964
  • 12 ELSO. ELSO Guidelines for Cardiopulmonary Extracorporeal Life Support Extracorporeal Life Support Organization. Version 1.4. 2017 . Accessed August 15, 2024 at: https://www.elso.org/Resources/Guidelines.aspx
  • 13 Olek E, Pasierski M, Słomka A. et al. Blood product transfusions on extracorporeal membrane oxygenation: a narrative review. Ann Blood 2023; 8: 16
  • 14 Kamamoto D, Kanazawa T, Ishihara E. et al. Efficacy of a topical gelatin-thrombin hemostatic matrix, FLOSEAL®, in intracranial tumor resection. Surg Neurol Int 2020; 11: 16
  • 15 Oz MC, Rondinone JF, Shargill NS. FloSeal matrix: new generation topical hemostatic sealant. J Card Surg 2003; 18 (06) 486-493

Address for correspondence

Katsuya Saito, MD, PhD
Department of Neurosurgery, Dokkyo Medical University
880 Kitakobayashi, Mibu, Shimotsugagun, Tochigi 321-0293
Japan   

Publication History

Article published online:
19 September 2024

© 2024. Asian Congress of Neurological Surgeons. This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/)

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  • References

  • 1 Faulkner AL, Bacon JD, Fischer BA, Grupke SL, Hatton KW. Successful extracorporeal membrane oxygenation (ECMO) use without systemic anticoagulation for acute respiratory distress syndrome in a patient with aneurysmal subarachnoid hemorrhage. Case Rep Neurol Med 2019; 2019: 9537453
  • 2 Lorusso R, Gelsomino S, Parise O. et al. Neurologic injury in adults supported with veno-venous extracorporeal membrane oxygenation for respiratory failure: findings from the Extracorporeal Life Support Organization Database. Crit Care Med 2017; 45 (08) 1389-1397
  • 3 Tonna JE, Abrams D, Brodie D. et al. Management of adult patients supported with venovenous extracorporeal membrane oxygenation (VV ECMO): Guideline from the Extracorporeal Life Support Organization (ELSO). ASAIO J 2021; 67 (06) 601-610
  • 4 Cartwright B, Bruce HM, Kershaw G. et al. Hemostasis, coagulation and thrombin in venoarterial and venovenous extracorporeal membrane oxygenation: the HECTIC study. Sci Rep 2021; 11 (01) 7975
  • 5 Kalbhenn J, Wittau N, Schmutz A, Zieger B, Schmidt R. Identification of acquired coagulation disorders and effects of target-controlled coagulation factor substitution on the incidence and severity of spontaneous intracranial bleeding during veno-venous ECMO therapy. Perfusion 2015; 30 (08) 675-682
  • 6 Olson SR, Murphree CR, Zonies D. et al. Thrombosis and bleeding in extracorporeal membrane oxygenation (ECMO) without anticoagulation: a systematic review. ASAIO J 2021; 67 (03) 290-296
  • 7 Sy E, Sklar MC, Lequier L, Fan E, Kanji HD. Anticoagulation practices and the prevalence of major bleeding, thromboembolic events, and mortality in venoarterial extracorporeal membrane oxygenation: a systematic review and meta-analysis. J Crit Care 2017; 39: 87-96
  • 8 Arlt M, Philipp A, Voelkel S. et al. Extracorporeal membrane oxygenation in severe trauma patients with bleeding shock. Resuscitation 2010; 81 (07) 804-809
  • 9 Anton-Martin P, Braga B, Megison S, Journeycake J, Moreland J. Craniectomy and traumatic brain injury in children on extracorporeal membrane oxygenation support. Pediatr Emerg Care 2018; 34 (11) e204-e210
  • 10 Bindal S, Conner CR, Akkanti B. et al. Multiple decompressive craniectomies and hematoma evacuation in a patient undergoing extracorporeal membrane oxygenation. Interdiscip Neurosurg 2022; 30: 101610
  • 11 Hwang GJ, Sheen SH, Kim HS. et al. Extracorporeal membrane oxygenation for acute life-threatening neurogenic pulmonary edema following rupture of an intracranial aneurysm. J Korean Med Sci 2013; 28 (06) 962-964
  • 12 ELSO. ELSO Guidelines for Cardiopulmonary Extracorporeal Life Support Extracorporeal Life Support Organization. Version 1.4. 2017 . Accessed August 15, 2024 at: https://www.elso.org/Resources/Guidelines.aspx
  • 13 Olek E, Pasierski M, Słomka A. et al. Blood product transfusions on extracorporeal membrane oxygenation: a narrative review. Ann Blood 2023; 8: 16
  • 14 Kamamoto D, Kanazawa T, Ishihara E. et al. Efficacy of a topical gelatin-thrombin hemostatic matrix, FLOSEAL®, in intracranial tumor resection. Surg Neurol Int 2020; 11: 16
  • 15 Oz MC, Rondinone JF, Shargill NS. FloSeal matrix: new generation topical hemostatic sealant. J Card Surg 2003; 18 (06) 486-493

Zoom Image
Fig. 1 (A) Chest computed tomography (CT) on admission shows neurogenic pulmonary edema in both lungs. (B) Head CT and (C) CT angiography on admission show diffuse subarachnoid hemorrhage and an anterior choroidal artery aneurysm and two middle cerebral artery aneurysms (red arrows).
Zoom Image
Fig. 2 Chest X-ray after the extracorporeal membrane oxygenation cannulation shows two single lumen cannulas, draining from the inferior vena cava (IVC) and reinfusing into the IVC/right atrium. The black arrow shows the tip of the draining venous cannula, and the two black arrowheads show the reinfusion cannula.
Zoom Image
Fig. 3 (A) An intraoperative photograph during the dissection of sylvian fissure shows very bloody surgical field and poor vision of the microscope. (B) The anteroposterior view of postoperative computed tomography angiography shows complete neck clipping. (C) A head computed tomography performed 1 month after the operation shows a right lenticulostriate artery infarction.