Neurological Pupil Index and Delayed Cerebral Ischemia After Subarachnoid Hemorrhage: A Retrospective Multicentric Study

Overview

Journal Neurocrit Care

Specialty Critical Care

Date 2023 May 24

PMID 37225941

Authors

Elisa Gouvea Bogossian

Aaron Blandino Ortiz

Valentina Esposito

Anselmo Caricato

Cassia Righy Shinotsuka

Berta Monleon Lopez

Giuseppina Gianni

Elisabetta Macchini

Raul de Pablo Sanchez

Luca Pisapia

Ricardo Turon

Bruno Goncalves

Rafael Badenes

Pedro Kurtz

Fabio Silvio Taccone

Affiliations

Soon will be listed here.

Abstract

Background: Delayed cerebral ischemia (DCI) occurs in around 30% of patients suffering from nontraumatic subarachnoid hemorrhage (SAH) and is associated with poor neurological outcome. Whether the Neurological Pupil index (NPi) derived from the automated pupillometry could help to diagnose the occurrence of DCI remains unknown. The aim of this study was to investigate the association of NPi with the occurrence of DCI in patients with SAH.

Methods: This was a multicenter, retrospective cohort study of consecutive patients with SAH admitted to the intensive care units of five hospitals between January 2018 and December 2020 who underwent daily NPi recordings (every 8 h) during the first 10 days of admission. DCI was diagnosed according to standard definitions (in awake patients) or based on neuroimaging and neuromonitoring (in sedated or unconscious patients). An NPi < 3 was defined as abnormal. The primary outcome of the study was to assess the time course of daily NPi between patients with DCI and patients without DCI. Secondary outcome included the number of patients who had an NPi < 3 before DCI.

Results: A total of 210 patients were eligible for the final analysis; DCI occurred in 85 (41%) patients. Patients who developed DCI had similar values of mean and worst daily NPi over time when compared with patients without DCI. Patients with DCI had a higher proportion of at least one NPi < 3 at any moment before DCI when compared with others (39/85, 46% vs. 35/125, 38%, p = 0.009). Similarly, the worst NPi before DCI diagnosis was lower in the DCI group when compared with others (3.1 [2.5-3.8] vs. 3.7 [2.7-4.1], p = 0.05). In the multivariable logistic regression analysis, the presence of NPi < 3 was not independently associated with the development of DCI (odds ratio 1.52 [95% confidence interval 0.80-2.88]).

Conclusions: In this study, NPi measured three times a day and derived from the automated pupillometry had a limited value for the diagnosis of DCI in patients with SAH.

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References

Etminan N, Chang H, Hackenberg K, de Rooij N, Vergouwen M, Rinkel G . Worldwide Incidence of Aneurysmal Subarachnoid Hemorrhage According to Region, Time Period, Blood Pressure, and Smoking Prevalence in the Population: A Systematic Review and Meta-analysis. JAMA Neurol. 2019; 76(5):588-597. PMC: 6515606. DOI: 10.1001/jamaneurol.2019.0006. View

Wartenberg K, Mayer S . Medical complications after subarachnoid hemorrhage. Neurosurg Clin N Am. 2010; 21(2):325-38. DOI: 10.1016/j.nec.2009.10.012. View

Velat G, Kimball M, Mocco J, Hoh B . Vasospasm after aneurysmal subarachnoid hemorrhage: review of randomized controlled trials and meta-analyses in the literature. World Neurosurg. 2011; 76(5):446-54. DOI: 10.1016/j.wneu.2011.02.030. View

Thompson J, Chalet F, Manalastas E, Hawkins N, Sarri G, Talbot D . Economic and Humanistic Burden of Cerebral Vasospasm and Its Related Complications after Aneurysmal Subarachnoid Hemorrhage: A Systematic Literature Review. Neurol Ther. 2022; 11(2):597-620. PMC: 9095797. DOI: 10.1007/s40120-022-00348-6. View

Dodd W, Laurent D, Dumont A, Hasan D, Jabbour P, Starke R . Pathophysiology of Delayed Cerebral Ischemia After Subarachnoid Hemorrhage: A Review. J Am Heart Assoc. 2021; 10(15):e021845. PMC: 8475656. DOI: 10.1161/JAHA.121.021845. View

Washington C, Zipfel G . Detection and monitoring of vasospasm and delayed cerebral ischemia: a review and assessment of the literature. Neurocrit Care. 2011; 15(2):312-7. DOI: 10.1007/s12028-011-9594-8. View

Bower M, Sweidan A, Xu J, Stern-Neze S, Yu W, Groysman L . Quantitative Pupillometry in the Intensive Care Unit. J Intensive Care Med. 2019; 36(4):383-391. DOI: 10.1177/0885066619881124. View

Natzeder S, Mack D, Maissen G, Strassle C, Keller E, Muroi C . Portable Infrared Pupillometer in Patients With Subarachnoid Hemorrhage: Prognostic Value and Circadian Rhythm of the Neurological Pupil Index (NPi). J Neurosurg Anesthesiol. 2018; 31(4):428-433. DOI: 10.1097/ANA.0000000000000553. View

Aoun S, Stutzman S, Vo P, El Ahmadieh T, Osman M, Neeley O . Detection of delayed cerebral ischemia using objective pupillometry in patients with aneurysmal subarachnoid hemorrhage. J Neurosurg. 2019; 132(1):27-32. DOI: 10.3171/2018.9.JNS181928. View

10.

Connolly Jr E, Rabinstein A, Carhuapoma J, Derdeyn C, Dion J, Higashida R . Guidelines for the management of aneurysmal subarachnoid hemorrhage: a guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke. 2012; 43(6):1711-37. DOI: 10.1161/STR.0b013e3182587839. View

11.

Vergouwen M, Vermeulen M, van Gijn J, Rinkel G, Wijdicks E, Muizelaar J . Definition of delayed cerebral ischemia after aneurysmal subarachnoid hemorrhage as an outcome event in clinical trials and observational studies: proposal of a multidisciplinary research group. Stroke. 2010; 41(10):2391-5. DOI: 10.1161/STROKEAHA.110.589275. View

12.

Quispe Cornejo A, Fernandes Vilarinho C, Crippa I, Peluso L, Calabro L, Vincent J . The use of automated pupillometry to assess cerebral autoregulation: a retrospective study. J Intensive Care. 2020; 8:57. PMC: 7395368. DOI: 10.1186/s40560-020-00474-z. View

13.

Olson D, Fishel M . The Use of Automated Pupillometry in Critical Care. Crit Care Nurs Clin North Am. 2016; 28(1):101-7. DOI: 10.1016/j.cnc.2015.09.003. View

14.

Frontera J, Claassen J, Schmidt J, Wartenberg K, Temes R, Connolly Jr E . Prediction of symptomatic vasospasm after subarachnoid hemorrhage: the modified fisher scale. Neurosurgery. 2006; 59(1):21-7. DOI: 10.1227/01.neu.0000243277.86222.6c. View

15.

RITTER A, Muizelaar J, Barnes T, Choi S, Fatouros P, Ward J . Brain stem blood flow, pupillary response, and outcome in patients with severe head injuries. Neurosurgery. 1999; 44(5):941-8. DOI: 10.1097/00006123-199905000-00005. View

16.

Peluso L, Ferlini L, Talamonti M, Ndieugnou Djangang N, Gouvea Bogossian E, Menozzi M . Automated Pupillometry for Prediction of Electroencephalographic Reactivity in Critically Ill Patients: A Prospective Cohort Study. Front Neurol. 2022; 13:867603. PMC: 8977520. DOI: 10.3389/fneur.2022.867603. View

17.

Hasan S, Peluso L, Ferlini L, Legros B, Calabro L, Oddo M . Correlation Between Electroencephalography and Automated Pupillometry in Critically Ill Patients: A Pilot Study. J Neurosurg Anesthesiol. 2019; 33(2):161-166. DOI: 10.1097/ANA.0000000000000633. View

18.

Campos Y, Rana P, Reyes R, Mazhar K, Stutzman S, Atem F . Relationship Between Automated Pupillometry Measurements and Ventricular Volume in Patients With Aneurysmal Subarachnoid Hemorrhage. J Neurosci Nurs. 2022; 54(4):166-170. DOI: 10.1097/JNN.0000000000000657. View

19.

Robba C, Pozzebon S, Moro B, Vincent J, Creteur J, Taccone F . Multimodal non-invasive assessment of intracranial hypertension: an observational study. Crit Care. 2020; 24(1):379. PMC: 7318399. DOI: 10.1186/s13054-020-03105-z. View

20.

Pansell J, Hack R, Rudberg P, Bell M, Cooray C . Can Quantitative Pupillometry be used to Screen for Elevated Intracranial Pressure? A Retrospective Cohort Study. Neurocrit Care. 2022; 37(2):531-537. PMC: 9519702. DOI: 10.1007/s12028-022-01518-y. View