Skip to main content

Advertisement

Log in

Neurogenic pulmonary edema and Takotsubo cardiomyopathy in aneurysmal subarachnoid hemorrhage

  • Original Article
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Purpose

Neurogenic pulmonary edema (NPE) combined with Takotsubo cardiomyopathy (TCM) is a rare condition associated with aneurysmal subarachnoid hemorrhage (aSAH). Although several mechanisms have been proposed, the pathophysiology and management strategies are not yet fully established. We aimed to determine the radiological and clinical outcomes of patients with NPE and with TCM after aSAH to propose management strategies.

Methods

We analyzed the data of 564 patients with aSAH recorded at a single medical center from February 2015 to July 2022. This study retrospectively investigated the incidence and demographics of SAH combined with both NPE and TCM and the clinical outcomes of the patients. Correlating factors, independently associated with NPE-TCM, were also investigated.

Results

During the 7 years, 11 (2.0%) of 564 patients had NPE complicated with TCM after aSAH. Seven of 11 (63.6%) patients had poor-grade SAH (Hunt–Hess Grade 4 to 5). Three of 11 patients had a posterior circulation in the NPE-TCM group. The most prevalent treatment option was endovascular coil embolization, except for one case of clip. Long-term outcomes were favorable in 6 of 11 patients, and there was one case of mortality. Age, troponin I level, and alveolar-arterial oxygen gradient were correlating factors of NPE-TCM.

Conclusion

Although NPE-TCM represents a rare complication associated with aSAH, achieving active resolution of underlying neurological causes through early and appropriate treatment may contribute to a favorable prognosis. Considering the limited incidence of SAH complicated with NPE-TCM, a multi-center study may be needed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Data Availability

According to the medical laws in South Korea, the data used in this study cannot be freely disclosed. However, pseudonymized datasets can be shared after obtaining formal approval for the scientific research plan and data management plan from the Ajou University Hospital’s Institutional Review Board (IRB).

References

  1. Busl KM, Bleck TP (2015) Neurogenic pulmonary edema. Crit Care Med 43:1710–1715

    Article  PubMed  Google Scholar 

  2. Chen WL, Chang SH, Chen JH, Tai HC, Chan CM, Wang YC (2016) Heart rate variability predicts neurogenic pulmonary edema in patients with subarachnoid hemorrhage. Neurocrit Care 25:71–78

    Article  PubMed  Google Scholar 

  3. Davison DL, Terek M, Chawla LS (2012) Neurogenic pulmonary edema. Crit Care 16:212

    Article  PubMed  PubMed Central  Google Scholar 

  4. de Lucia C, Piedepalumbo M, Paolisso G, Koch WJ (2019) Sympathetic nervous system in age-related cardiovascular dysfunction: pathophysiology and therapeutic perspective. Int J Biochem Cell Biol 108:29–33

    Article  PubMed  PubMed Central  Google Scholar 

  5. Finsterer J (2019) Neurological perspectives of neurogenic pulmonary edema. Eur Neurol 81:94–102

    Article  CAS  PubMed  Google Scholar 

  6. Fontes RB, Aguiar PH, Zanetti MV, Andrade F, Mandel M, Teixeira MJ (2003) Acute neurogenic pulmonary edema: case reports and literature review. J Neurosurg Anesthesiol 15:144–150

    Article  PubMed  Google Scholar 

  7. Garcia-Uria J, Hoff JT, Miranda S, Nishimura M (1981) Experimental neurogenic pulmonary edema part 2: the role of cardiopulmonary pressure change. J Neurosurg 54:632–636

    Article  CAS  PubMed  Google Scholar 

  8. Gherasim L (2020) Takotsubo syndrome versus neurogenic stunned myocardium. Maedica (Bucur) 15:288–296

    PubMed  Google Scholar 

  9. Gupta S, Gupta MM (2018) Takotsubo syndrome. Indian Heart J 70:165–174

    Article  PubMed  Google Scholar 

  10. Hunt WE, Hess RM (1968) Surgical risk as related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14–20

    Article  CAS  PubMed  Google Scholar 

  11. Inamasu J, Nakatsukasa M, Mayanagi K, Miyatake S, Sugimoto K, Hayashi T, Kato Y, Hirose Y (2012) Subarachnoid hemorrhage complicated with neurogenic pulmonary edema and takotsubo-like cardiomyopathy. Neurol Med Chir (Tokyo) 52:49–55

    Article  PubMed  Google Scholar 

  12. Inamasu J, Sugimoto K, Yamada Y, Ganaha T, Ito K, Watabe T, Hayashi T, Kato Y, Ozaki Y, Hirose Y (2012) The role of catecholamines in the pathogenesis of neurogenic pulmonary edema associated with subarachnoid hemorrhage. Acta Neurochir (Wien) 154:2179–2185

    Article  PubMed  Google Scholar 

  13. Kimura T, Kamide T, Onodera K, Tabata S, Shibata A, Suzuki K, Takeda R, Ikeda T, Kikkawa Y, Iihoshi S, Kohyama S, Kurita H (2020) Clinical features of neurogenic pulmonary edema in patients with subarachnoid hemorrhage. World Neurosurg 135:e505–e509

    Article  PubMed  Google Scholar 

  14. Kramer AH, Bleck TP, Dumont AS, Kassell NF, Olson C, Nathan B (2009) Implications of early versus late bilateral pulmonary infiltrates in patients with aneurysmal subarachnoid hemorrhage. Neurocrit Care 10:20–27

    Article  PubMed  Google Scholar 

  15. Krishnamoorthy V, Mackensen GB, Gibbons EF, Vavilala MS (2016) Cardiac dysfunction after neurologic injury: what do we know and where are we going? Chest 149:1325–1331

    Article  PubMed  Google Scholar 

  16. Kurisu S, Inoue I, Kawagoe T, Ishihara M, Shimatani Y, Nakamura S, Yoshida M, Mitsuba N, Hata T, Sato H (2004) Time course of electrocardiographic changes in patients with tako-tsubo syndrome: comparison with acute myocardial infarction with minimal enzymatic release. Circ J 68:77–81

    Article  PubMed  Google Scholar 

  17. Lee VH, Connolly HM, Fulgham JR, Manno EM, Brown RD Jr, Wijdicks EF (2006) Tako-tsubo cardiomyopathy in aneurysmal subarachnoid hemorrhage: an underappreciated ventricular dysfunction. J Neurosurg 105:264–270

    Article  PubMed  Google Scholar 

  18. Lozada-Martínez ID, Rodríguez-Gutiérrez MM, Ospina-Rios J, Ortega-Sierra MG, González-Herazo MA, Ortiz-Roncallo LM, Martínez-Imbett R, Llamas-Nieves AE, Janjua T, Moscote-Salazar LR (2021) Neurogenic pulmonary edema in subarachnoid hemorrhage: relevant clinical concepts. Egypt J Neurosurg 36:27

    Article  PubMed  PubMed Central  Google Scholar 

  19. Manto A, De Gennaro A, Manzo G, Serino A, Quaranta G, Cancella C (2014) Early endovascular treatment of aneurysmal subarachnoid hemorrhage complicated by neurogenic pulmonary edema and Takotsubo-like cardiomyopathy. Neuroradiol J 27:356–360

    Article  PubMed  PubMed Central  Google Scholar 

  20. Meguro T, Tanabe T, Muraoka K, Terada K, Hirotsune N, Nishino S (2016) Endovascular treatment for aneurysmal subarachnoid hemorrhage with neurogenic pulmonary edema in the acute stage. Turk Neurosurg 26:849–853

    PubMed  Google Scholar 

  21. Mori H, Ishikawa S, Kojima S, Hayashi J, Watanabe Y, Hoffman JI, Okino H (1993) Increased responsiveness of left ventricular apical myocardium to adrenergic stimuli. Cardiovasc Res 27:192–198

    Article  CAS  PubMed  Google Scholar 

  22. Nastasovic T, Milakovic B, Marinkovic JE, Grujicic D, Stosic M (2017) Could cardiac biomarkers predict neurogenic pulmonary edema in aneurysmal subarachnoid hemorrhage? Acta Neurochir (Wien) 159:705–712

    Article  PubMed  Google Scholar 

  23. Naum R, Filatov A, Alusma-Hibbert K, Espinosa PS (2020) Pulmonary edema and stunned myocardium in subarachnoid hemorrhage. Cureus 12:e7746

    PubMed  PubMed Central  Google Scholar 

  24. Nonaka S, Oishi H, Tsutsumi S, Ishii H (2020) Endovascular therapy for aneurysmal subarachnoid hemorrhage complicated by neurogenic pulmonary edema and takotsubo-like cardiomyopathy: a report of ten cases. Asian J Neurosurg 15:113–119

    Article  PubMed  PubMed Central  Google Scholar 

  25. Ochiai H, Yamakawa Y, Kubota E (2001) Deformation of the ventrolateral medulla oblongata by subarachnoid hemorrhage from ruptured vertebral artery aneurysms causes neurogenic pulmonary edema. Neurol Med Chir (Tokyo) 41:529–535

    Article  CAS  PubMed  Google Scholar 

  26. Sato H, Tateishi H, Uchida T, Dote K, Ishihara M (1990) Tako-tsubo-like left ventricular dysfunction due to multivessel coronary spasm. In: Kodama K, Haze K, Hori M (eds) Clinical aspect of myocardial injury: from ischemia to heart failure. Kagakuhyoronsha Publishing Co, Tokyo, pp 56–64

    Google Scholar 

  27. Sattar Y, Siew KSW, Connerney M, Ullah W, Alraies MC (2020) Management of Takotsubo syndrome: a comprehensive review. Cureus 12:e6556

    PubMed  PubMed Central  Google Scholar 

  28. Secco G, Salinaro F, Bellazzi C, La Salvia M, Delorenzo M, Zattera C, Barcella B, Resta F, Vezzoni G, Bonzano M, Cappa G, Bruno R, Casagranda I, Perlini S (2021) Can alveolar-arterial difference and lung ultrasound help the clinical decision making in patients with COVID-19? Diagnostics (Basel) 11:761

    Article  CAS  PubMed  Google Scholar 

  29. Singh T, Khan H, Gamble DT, Scally C, Newby DE, Dawson D (2022) Takotsubo syndrome: pathophysiology, emerging concepts, and clinical implications. Circulation 145:1002–1019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Talahma M, Alkhachroum AM, Alyahya M, Manjila S, Xiong W (2016) Takotsubo cardiomyopathy in aneurysmal subarachnoid hemorrhage: institutional experience and literature review. Clin Neurol Neurosurg 141:65–70

    Article  PubMed  Google Scholar 

  31. Tan CK, Lai CC (2007) Neurogenic pulmonary edema. CMAJ 177:249–250

    Article  PubMed  PubMed Central  Google Scholar 

  32. Templin C, Ghadri JR, Diekmann J, Napp LC, Bataiosu DR, Jaguszewski M, Cammann VL, Sarcon A, Geyer V, Neumann CA, Seifert B, Hellermann J, Schwyzer M, Eisenhardt K, Jenewein J, Franke J, Katus HA, Burgdorf C, Schunkert H, Moeller C, Thiele H, Bauersachs J, Tschöpe C, Schultheiss HP, Laney CA, Rajan L, Michels G, Pfister R, Ukena C, Böhm M, Erbel R, Cuneo A, Kuck KH, Jacobshagen C, Hasenfuss G, Karakas M, Koenig W, Rottbauer W, Said SM, Braun-Dullaeus RC, Cuculi F, Banning A, Fischer TA, Vasankari T, Airaksinen KE, Fijalkowski M, Rynkiewicz A, Pawlak M, Opolski G, Dworakowski R, MacCarthy P, Kaiser C, Osswald S, Galiuto L, Crea F, Dichtl W, Franz WM, Empen K, Felix SB, Delmas C, Lairez O, Erne P, Bax JJ, Ford I, Ruschitzka F, Prasad A, Lüscher TF (2015) Clinical features and outcomes of takotsubo (stress) cardiomyopathy. N Engl J Med 373:929–938

    Article  CAS  PubMed  Google Scholar 

  33. Vespa PM, Bleck TP (2004) Neurogenic pulmonary edema and other mechanisms of impaired oxygenation after aneurysmal subarachnoid hemorrhage. Neurocrit Care 1:157–170

    Article  PubMed  Google Scholar 

  34. Wybraniec MT, Mizia-Stec K, Krzych Ł (2014) Neurocardiogenic injury in subarachnoid hemorrhage: a wide spectrum of catecholamin-mediated brain-heart interactions. Cardiol J 21:220–228

    Article  PubMed  Google Scholar 

  35. Y-Hassan S, Tornvall P, (2018) Epidemiology, pathogenesis, and management of takotsubo syndrome. Clin Auton Res 28:53–65

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study’s conception and design. Material preparation, data collection, and analysis were performed by Eui-Hyun Hwang. The first draft of the manuscript was written by Eui-Hyun Hwang, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Conceptualization: Eui-Hyun Hwang, Yeon Hu Lee, Yong Cheol Lim.

Methodology: Eui-Hyun Hwang, Ja Ho Koo.

Formal analysis and investigation: Eui-Hyun Hwang.

Writing – original draft preparation: Eui-Hyun Hwang.

Writing—review and editing: Eui-Hyun Hwang. Ji Hye Song, Yong Cheol Lim.

Funding acquisition: none.

Resources: Eui-Hyun Hwang.

Supervision: Ji Hye Song, Yong Cheol Lim.

Corresponding author

Correspondence to Yong Cheol Lim.

Ethics declarations

Ethics approval

This study was approved by the Institutional Review Board Ajou University Hospital (AJOUIRB-DB-2022–384) and conducted in accordance with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hwang, EH., Koo, J.H., Lee, Y.H. et al. Neurogenic pulmonary edema and Takotsubo cardiomyopathy in aneurysmal subarachnoid hemorrhage. Acta Neurochir 165, 3677–3684 (2023). https://doi.org/10.1007/s00701-023-05824-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-023-05824-y

Keywords

Navigation