Skip to main content
Erschienen in: Acta Neurochirurgica 4/2017

30.01.2017 | Original Article - Vascular

Could cardiac biomarkers predict neurogenic pulmonary edema in aneurysmal subarachnoid hemorrhage?

verfasst von: Tijana Nastasovic, Branko Milakovic, Jelena Eric Marinkovic, Danica Grujicic, Mila Stosic

Erschienen in: Acta Neurochirurgica | Ausgabe 4/2017

Einloggen, um Zugang zu erhalten

Abstract

Background

Neurogenic pulmonary edema (NPE) is a clinical syndrome characterized by the acute onset of pulmonary edema after a significant central nervous system (CNS) insult. NPE occurs as a result of release of catecholamines into the blood immediately after aneurysm rupture. The aim of this study is to investigate the connection between the value of cardiac biomarkers on admission and incidence of NPE in patients with aneurysmal subarachnoid hemorrhage (SAH).

Methods

A total of 262 SAH patients (162 women, 100 men) were prospectively included in the study. Clinical characteristics, electrocardiographic (ECG) changes, serum cardiac and inflammatory biomarkers were measured on admission and on the day of development of NPE. These data were analyzed in order to predict the development NPE.

Results

Nineteen patients (7.25%) developed NPE. Comparison revealed that patients who subsequently developed NPE, sustained more severe SAH. Cardiac damage was more severe in these patients, as represented by significantly higher mean values of all examined cardiac biomarkers (P = 0.000), except for troponin I value that was significantly lower (P = 0.000). Multivariate regression analysis revealed that elevated troponin I (OR, 4.980; 95% CI, 1.27-19.49; P = 0.021) and white blood cell count (OR, 22.195; 95% CI, 3.99-123.50; P = 0.000) are predictors of NPE.

Conclusions

Significantly higher values of cardiac biomarkers were observed in SAH patients complicated with NPE. Elevated values of cardiac biomarkers appear to play an active role in prediction of NPE, although white blood cell count may be involved in the prediction of NPE. There is an influence of SAH therapy on predictors of NPE.
Literatur
1.
Zurück zum Zitat Bahloul M, Chaari AN, Kallel H, Khabir A, Ayadi A, Charfeddine F, Hergafi L, Chaari AD, Chelly HE, Ben Hamida C, Rekik N, Bouaziz M (2006) Neurogenic pulmonary edema due to traumatic brain injury: evidence of cardiac dysfunction. Am J Crit Care 15:462–470PubMed Bahloul M, Chaari AN, Kallel H, Khabir A, Ayadi A, Charfeddine F, Hergafi L, Chaari AD, Chelly HE, Ben Hamida C, Rekik N, Bouaziz M (2006) Neurogenic pulmonary edema due to traumatic brain injury: evidence of cardiac dysfunction. Am J Crit Care 15:462–470PubMed
2.
Zurück zum Zitat Baumann A, Audibert G, McDonnell J, Mertes PM (2007) Neurogenic pulmonary edema. Acta Anaesthesiol Scand 51:447–455CrossRefPubMed Baumann A, Audibert G, McDonnell J, Mertes PM (2007) Neurogenic pulmonary edema. Acta Anaesthesiol Scand 51:447–455CrossRefPubMed
3.
Zurück zum Zitat Brouwers PJ, Wijdicks EF, Hasan D, Vermeulen M, Wever EF, Frericks H, van Gijn J (1989) Serial electrocardiographic recording in aneurysmal subarachnoid hemorrhage. Stroke 20:1162–1167CrossRefPubMed Brouwers PJ, Wijdicks EF, Hasan D, Vermeulen M, Wever EF, Frericks H, van Gijn J (1989) Serial electrocardiographic recording in aneurysmal subarachnoid hemorrhage. Stroke 20:1162–1167CrossRefPubMed
4.
Zurück zum Zitat Chen J, Qian C, Duan H, Cao S, Yu X, Li J, Gu C, Yan F, Wang L, Chen G (2015) Melatonin attenuates neurogenic pulmonary edema via the regulation of inflammation and apoptosis after subarachnoid hemorrhage in rats. J Pineal Res 59(4):469–477CrossRefPubMed Chen J, Qian C, Duan H, Cao S, Yu X, Li J, Gu C, Yan F, Wang L, Chen G (2015) Melatonin attenuates neurogenic pulmonary edema via the regulation of inflammation and apoptosis after subarachnoid hemorrhage in rats. J Pineal Res 59(4):469–477CrossRefPubMed
5.
Zurück zum Zitat Chen S, Zhu Z, Klebe D, Bian H, Krafft PR, Tang J, Zhang J, Zhang JH (2014) Role of P2X purinoceptor 7 in neurogenic pulmonary edema after subarachnoid hemorrhage in rats. PLoS One 12;9(2):e89042. doi:10.1371/journal.pone.0089042, eCollection 2014CrossRef Chen S, Zhu Z, Klebe D, Bian H, Krafft PR, Tang J, Zhang J, Zhang JH (2014) Role of P2X purinoceptor 7 in neurogenic pulmonary edema after subarachnoid hemorrhage in rats. PLoS One 12;9(2):e89042. doi:10.​1371/​journal.​pone.​0089042, eCollection 2014CrossRef
6.
7.
Zurück zum Zitat Davison DL, Terek M, Chawla LS. Neurogenic pulmonary edema (2012) Critical Care 16:212. Davison DL, Terek M, Chawla LS. Neurogenic pulmonary edema (2012) Critical Care 16:212.
8.
Zurück zum Zitat Di Pasquale G, Andreoli A, Lusa AM, Urbinati S, Biancoli S, Cere E, Borgatti ML, Pinelli G (1998) Cardiologic complications of subarachnoid hemorrhage. J Neurosurg Sci 42(Suppl 1):33–36PubMed Di Pasquale G, Andreoli A, Lusa AM, Urbinati S, Biancoli S, Cere E, Borgatti ML, Pinelli G (1998) Cardiologic complications of subarachnoid hemorrhage. J Neurosurg Sci 42(Suppl 1):33–36PubMed
9.
Zurück zum Zitat Ducker TB, Simmons RL (1968) Increased intracranial pressure and pulmonary edema. 2.The hemodynamic response of dogs and monkeys to increased intracranial pressure. J Neurosurg 28:118–123CrossRefPubMed Ducker TB, Simmons RL (1968) Increased intracranial pressure and pulmonary edema. 2.The hemodynamic response of dogs and monkeys to increased intracranial pressure. J Neurosurg 28:118–123CrossRefPubMed
10.
Zurück zum Zitat Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6(1):1–9CrossRefPubMed Fisher CM, Kistler JP, Davis JM (1980) Relation of cerebral vasospasm to subarachnoid hemorrhage visualized by computerized tomographic scanning. Neurosurgery 6(1):1–9CrossRefPubMed
11.
Zurück zum Zitat Fontes RB, Agular PH, Zanetti MV, Andrade F, Mandel M, Texeira MJ (2003) Acute neurogenic pulmonary edema: case reports and literature review. J Neurosurg Anesthesiol 15:144–150CrossRefPubMed Fontes RB, Agular PH, Zanetti MV, Andrade F, Mandel M, Texeira MJ (2003) Acute neurogenic pulmonary edema: case reports and literature review. J Neurosurg Anesthesiol 15:144–150CrossRefPubMed
12.
Zurück zum Zitat Friedman JA, Pichelmann MA, Piepgras DG, McIver JI, Toussaint LG 3rd, McClelland RL, Nichols DA, Meyer FB, Atkinson JL, Wijdicks EF (2003) Pulmonary complications of aneurysmal subarachnoid hemorrhage. Neuorsurgery 52:1025–1031 Friedman JA, Pichelmann MA, Piepgras DG, McIver JI, Toussaint LG 3rd, McClelland RL, Nichols DA, Meyer FB, Atkinson JL, Wijdicks EF (2003) Pulmonary complications of aneurysmal subarachnoid hemorrhage. Neuorsurgery 52:1025–1031
13.
Zurück zum Zitat Fujii M, Sherchan P, Soejima Y, Doycheva D, Zhao D, Zhang JH (2016) Cannabinoid receptor type 2 agonist attenuates acute neurogenic pulmonary edema by preventing neutrophil migration after subarachnoid hemorrhage in rats. Acta Neurochir Suppl 121:135–139. doi:10.1007/978-3-319-18497-5_24 PubMed Fujii M, Sherchan P, Soejima Y, Doycheva D, Zhao D, Zhang JH (2016) Cannabinoid receptor type 2 agonist attenuates acute neurogenic pulmonary edema by preventing neutrophil migration after subarachnoid hemorrhage in rats. Acta Neurochir Suppl 121:135–139. doi:10.​1007/​978-3-319-18497-5_​24 PubMed
14.
Zurück zum Zitat Hunt WE, Hess RM (1968) Surgical risk is related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14–20CrossRefPubMed Hunt WE, Hess RM (1968) Surgical risk is related to time of intervention in the repair of intracranial aneurysms. J Neurosurg 28:14–20CrossRefPubMed
15.
Zurück zum Zitat Inamasu J, Miyatake S, Tomioka H, Suzuki M, Nakatsukasa M, Maeda N, Ito T, Arai K, Komura M, Kase K, Kobayashi K (2009) Subarachnoid hemorrhage as a cause of out-of-hospital cardiac arrest: a prospective computed tomography study. Resuscitation 80:977–980CrossRefPubMed Inamasu J, Miyatake S, Tomioka H, Suzuki M, Nakatsukasa M, Maeda N, Ito T, Arai K, Komura M, Kase K, Kobayashi K (2009) Subarachnoid hemorrhage as a cause of out-of-hospital cardiac arrest: a prospective computed tomography study. Resuscitation 80:977–980CrossRefPubMed
16.
Zurück zum Zitat Inamasu J, Nakamura Y, Saito R, Kuroshima R, Mayanagi K, Ohba S, Ichikizaki K (2002) Normokalemia and hyperglycemia in subarachnoid hemorrhage patients resuscitated from prehospital cardiopulmonary arrest. Resuscitation 54:255–258CrossRefPubMed Inamasu J, Nakamura Y, Saito R, Kuroshima R, Mayanagi K, Ohba S, Ichikizaki K (2002) Normokalemia and hyperglycemia in subarachnoid hemorrhage patients resuscitated from prehospital cardiopulmonary arrest. Resuscitation 54:255–258CrossRefPubMed
17.
Zurück zum Zitat 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) 52:49–55CrossRef 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) 52:49–55CrossRef
18.
Zurück zum Zitat 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 154:2179–2185CrossRefPubMed 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 154:2179–2185CrossRefPubMed
19.
Zurück zum Zitat Kosnik EJ, Paul SE, Rossel CW, Sayers MP (1977) Central neurogenic pulmonary edema: with a review of its pathogenesis and treatment. Childs Brain 3:37–47PubMed Kosnik EJ, Paul SE, Rossel CW, Sayers MP (1977) Central neurogenic pulmonary edema: with a review of its pathogenesis and treatment. Childs Brain 3:37–47PubMed
20.
Zurück zum Zitat Macmillan CS, Grant IS, Andrews PJ (2002) Pulmonary and cardiac sequelae of subarachnoid hemorrhage: time for active management? Intensive Care Med 28:1012–1023CrossRefPubMed Macmillan CS, Grant IS, Andrews PJ (2002) Pulmonary and cardiac sequelae of subarachnoid hemorrhage: time for active management? Intensive Care Med 28:1012–1023CrossRefPubMed
21.
Zurück zum Zitat Mayer SA, Lin J, Homma S, Solomon RA, Lennihan L, Sherman D, Fink ME, Beckford A, Klebanoff LM (1999) Myocardial injury and left ventricular performance after subarachnoid hemorrhage. Stroke 30:780–786CrossRefPubMed Mayer SA, Lin J, Homma S, Solomon RA, Lennihan L, Sherman D, Fink ME, Beckford A, Klebanoff LM (1999) Myocardial injury and left ventricular performance after subarachnoid hemorrhage. Stroke 30:780–786CrossRefPubMed
22.
Zurück zum Zitat Menke J, Larsen J, Kallenberg K (2011) Diagnosing cerebral aneurysms by computed tomographic angiography: meta-analysis. Ann Neurol 69:646–654CrossRefPubMed Menke J, Larsen J, Kallenberg K (2011) Diagnosing cerebral aneurysms by computed tomographic angiography: meta-analysis. Ann Neurol 69:646–654CrossRefPubMed
23.
Zurück zum Zitat Muroi C, Keller M, Pangalu A, Fortunati M, Yonekawa Y, Keller E (2008) Neurogenic pulmonary edema in patients with subarachnoid hemorrhage. J Neurosurg Anesthesiol 20:199–192CrossRef Muroi C, Keller M, Pangalu A, Fortunati M, Yonekawa Y, Keller E (2008) Neurogenic pulmonary edema in patients with subarachnoid hemorrhage. J Neurosurg Anesthesiol 20:199–192CrossRef
24.
Zurück zum Zitat Naidech AM, Kreiter KT, Janjua N, Ostapkovich ND, Parra A, Commichau C, Fitzsimmons BFM, Connolly ES, Mayer SA (2005) Cardiac troponin elevation, cardiovascular morbidity, and outcome after subarachnoid hemorrhage. Circulation 112:2851–2856CrossRefPubMed Naidech AM, Kreiter KT, Janjua N, Ostapkovich ND, Parra A, Commichau C, Fitzsimmons BFM, Connolly ES, Mayer SA (2005) Cardiac troponin elevation, cardiovascular morbidity, and outcome after subarachnoid hemorrhage. Circulation 112:2851–2856CrossRefPubMed
25.
Zurück zum Zitat Ochiai H, Yamakawa Y, Kubota E (2001) Deformation of the ventrolateral medulla oblongata by subarachnoid hemorrhage from ruptured vertebral artery aneurysm causes neurogenic pulmonary edema. Neurol Med Chir (Tokyo) 41:529–534CrossRef Ochiai H, Yamakawa Y, Kubota E (2001) Deformation of the ventrolateral medulla oblongata by subarachnoid hemorrhage from ruptured vertebral artery aneurysm causes neurogenic pulmonary edema. Neurol Med Chir (Tokyo) 41:529–534CrossRef
26.
Zurück zum Zitat Solenski NJ, Haley EC Jr, Kassell NF, Kongable G, Germanson T, Truskowski L, Torner JC (1995) Medical complications of aneurysmal subarachnoid hemorrhage: a report of the multicenter, cooperative aneurysm study. Participants of the Multicenter Cooperative Aneurysm Study. Crit Care Med 23:1007–1017CrossRefPubMed Solenski NJ, Haley EC Jr, Kassell NF, Kongable G, Germanson T, Truskowski L, Torner JC (1995) Medical complications of aneurysmal subarachnoid hemorrhage: a report of the multicenter, cooperative aneurysm study. Participants of the Multicenter Cooperative Aneurysm Study. Crit Care Med 23:1007–1017CrossRefPubMed
27.
Zurück zum Zitat Sugimoto K, Inamasu J, Hirose J, Kato Y, Ito K, Iwase M, Sugimoto K, Watanabe E, Takahashi A, Ozaki Y (2012) The role of norepinephrine and estradiol in the pathogenesis of cardiac wall motion abnormality associated with subarachnoid hemorrhage. Stroke 43:1897–1903CrossRefPubMed Sugimoto K, Inamasu J, Hirose J, Kato Y, Ito K, Iwase M, Sugimoto K, Watanabe E, Takahashi A, Ozaki Y (2012) The role of norepinephrine and estradiol in the pathogenesis of cardiac wall motion abnormality associated with subarachnoid hemorrhage. Stroke 43:1897–1903CrossRefPubMed
28.
Zurück zum Zitat Sommargren CE, Zaroff JG, Banki N, Drew BJ (2002) Electrocardiographic repolarization abnormalities in subarachnoid hemorrhage. J Electrocardiol 35(Suppl):257–262CrossRefPubMed Sommargren CE, Zaroff JG, Banki N, Drew BJ (2002) Electrocardiographic repolarization abnormalities in subarachnoid hemorrhage. J Electrocardiol 35(Suppl):257–262CrossRefPubMed
29.
Zurück zum Zitat Tanabe M, Crago EA, Suffoletto MS, Hravnak M, Frangiskakis JM, Kassam AB, Horowitz MB, Gorcsan J III (2008) Relation of elevation in cardiac troponin I to clinical severity, cardiac dysfunction, and pulmonary congestion in patients with subarachnoid hemorrhage. Am J Cardiol 102(11):1545–1550CrossRefPubMedPubMedCentral Tanabe M, Crago EA, Suffoletto MS, Hravnak M, Frangiskakis JM, Kassam AB, Horowitz MB, Gorcsan J III (2008) Relation of elevation in cardiac troponin I to clinical severity, cardiac dysfunction, and pulmonary congestion in patients with subarachnoid hemorrhage. Am J Cardiol 102(11):1545–1550CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Tung PP, Olmsted E, Kopelnik A, Banki NM, Drew BJ, Ko N, Lawton MT, Smith W, Foster E, Young WL, Zaroff JG (2005) Plasma B-type natriuretic peptide levels are associated with early cardiac dysfunction after subarachnoid hemorrhage. Stroke 36:1567–1571CrossRefPubMed Tung PP, Olmsted E, Kopelnik A, Banki NM, Drew BJ, Ko N, Lawton MT, Smith W, Foster E, Young WL, Zaroff JG (2005) Plasma B-type natriuretic peptide levels are associated with early cardiac dysfunction after subarachnoid hemorrhage. Stroke 36:1567–1571CrossRefPubMed
31.
Zurück zum Zitat Zaroff JG, Rordorf GA, Newell JB, Ogilvy CS, Levinson JR (1999) Cardiac outcome in patients with subarachnoid hemorrhage and electrocardiographic abnormalities. Neurosurgery 44:34–39CrossRefPubMed Zaroff JG, Rordorf GA, Newell JB, Ogilvy CS, Levinson JR (1999) Cardiac outcome in patients with subarachnoid hemorrhage and electrocardiographic abnormalities. Neurosurgery 44:34–39CrossRefPubMed
32.
Zurück zum Zitat Zaroff JG, Rordorf GA, Ogilvy CS, Picard MH (2000) Regional patterns of left ventricular systolic dysfunction after subarachnoid hemorrhage: evidence for neurally mediated cardiac injury. J Am Soc Echocardiogr 13:774–779CrossRefPubMed Zaroff JG, Rordorf GA, Ogilvy CS, Picard MH (2000) Regional patterns of left ventricular systolic dysfunction after subarachnoid hemorrhage: evidence for neurally mediated cardiac injury. J Am Soc Echocardiogr 13:774–779CrossRefPubMed
Metadaten
Titel
Could cardiac biomarkers predict neurogenic pulmonary edema in aneurysmal subarachnoid hemorrhage?
verfasst von
Tijana Nastasovic
Branko Milakovic
Jelena Eric Marinkovic
Danica Grujicic
Mila Stosic
Publikationsdatum
30.01.2017
Verlag
Springer Vienna
Erschienen in
Acta Neurochirurgica / Ausgabe 4/2017
Print ISSN: 0001-6268
Elektronische ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-017-3091-6

Weitere Artikel der Ausgabe 4/2017

Acta Neurochirurgica 4/2017 Zur Ausgabe

Letter to the editor - Editorial

Letter to the Editor: WhatsAPP in neurosurgery

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.