Intraoperative Low Alpha Power in the Electroencephalogram Is Associated With Postoperative Subsyndromal Delirium

Rodrigo Gutierrez, Jose I Egaña, Iván Saez, Fernando Reyes, Constanza Briceño, Mariana Venegas, Isidora Lavado, Antonello Penna, Rodrigo Gutierrez, Jose I Egaña, Iván Saez, Fernando Reyes, Constanza Briceño, Mariana Venegas, Isidora Lavado, Antonello Penna

Abstract

Background: Postoperative delirium (PD) and subsyndromal delirium (PSSD) are frequent complications in older patients associated with poor long-term outcome. It has been suggested that certain electroencephalogram features may be capable of identifying patients at risk during surgery. Thus, the goal of this study was to characterize intraoperative electroencephalographic markers to identify patients prone to develop PD or PSSD.

Methods: We conducted an exploratory observational study in older patients scheduled for elective major abdominal surgery. Intraoperative 16 channels electroencephalogram was recorded, and PD/PSSD were diagnosed after surgery with the confusion assessment method (CAM). The total power spectra and relative power of alpha band were calculated.

Results: PD was diagnosed in 2 patients (6.7%), and 11 patients (36.7%) developed PSSD. All of them (13 patients, PD/PSSD group) were compared with patients without any alterations in CAM (17 patients, control group). There were no detectable power spectrum differences before anesthesia between both groups of patients. However, PD/PSSD group in comparison with control group had a lower intraoperative absolute alpha power during anesthesia (4.4 ± 3.8 dB vs. 9.6 ± 3.2 dB, p = 0.0004) and a lower relative alpha power (0.09 ± 0.06 vs. 0.21 ± 0.08, p < 0.0001). These differences were independent of the anesthetic dose. Finally, relative alpha power had a good ability to identify patients with CAM alterations in the ROC analysis (area under the curve 0.90 (CI 0.78-1), p < 0.001).

Discussion: In conclusion, a low intraoperative alpha power is a novel electroencephalogram marker to identify patients who will develop alterations in CAM - i.e., with PD or PSSD - after surgery.

Keywords: alpha oscillations; anesthesia; delirium; electroencephalogram; power spectra; subsyndromal delirium.

Copyright © 2019 Gutierrez, Egaña, Saez, Reyes, Briceño, Venegas, Lavado and Penna.

Figures

FIGURE 1
FIGURE 1
Frequency analysis from EEG records from control and PD/PSSD patients. (A) EEG spectrum before anesthesia. (B) EEG spectrum 60 min after anesthesia induction. Both spectra depict mean (thick central line) and 95% interval of confidence (colored area). Power (dB) is shown from 1 to 40 Hz. PD/PSSD patients are represented in blue and control patients in red. Black bar represent significant difference between 9 and 12.75 Hz. ∗∗∗p < 0.001. (C) Representative spectrogram (Fp1 electrode) of a 64-year-old control patient. (D) Representative spectrogram (Fp1 electrode) of a 67-year-old PSSD patient. Both spectrograms depict power according to the color scale in dB between 1 and 40 Hz frequencies and time expressed in minutes. (E) Absolute alpha power before (gray) and under anesthesia (black) in control and PD/PSSD patients. (F) Absolute delta power before (gray) and under anesthesia (black) in control and PD/PSSD patients. Each bar depicts mean and standard deviation. ∗∗∗p < 0.001.
FIGURE 2
FIGURE 2
Relative alpha power in different brain region and its ability to discriminate between control and PD/PSSD patients. Relative alpha power in (A) global EEG, (B) frontal electrodes (Fp1 and Fp2), and (C) occipital (O1, Oz, and O2) electrodes. Control and PD/PSSD patients represented by blue and red bars, respectively. Each bar depicts mean and standard deviation. ∗∗∗p < 0.001. (D) ROC curves to calculate the ability to discriminate between control and PD/PSSD patients. ROC curve of alpha power is shown in red (AUC = 0.90, p < 0.001), of age in gray (AUC = 0.75, p = 0.02), and of MoCA in black (AUC = 0.76, p = 0.02), while dash line represents the reference line for no discrimination. X axis depicts 100-specificity (%) and y axis the sensitivity (%).
FIGURE 3
FIGURE 3
Correlation between frontal relative alpha power and age-adjusted MAC in both groups of patients. (A) Correlation of control patients showing in blue. (B) Correlation of PD/PSSD patients representing in red. Pearson coefficient, regression line, and p-value are shown in each graph.

References

    1. Aime I., Gayat E., Fermanian C., Cook F., Peuch C., Laloe P. A., et al. (2012). Effect of age on the comparability of bispectral and state entropy indices during the maintenance of propofol-sufentanil anaesthesia. Br. J. Anaesth. 108 638–643. 10.1093/bja/aer457
    1. Aldecoa C., Bettelli G., Bilotta F., Sanders R. D., Audisio R., Borozdina A., et al. (2017). European society of anaesthesiology evidence-based and consensus-based guideline on postoperative delirium. Eur. J. Anaesthesiol. 34 192–214. 10.1097/EJA.0000000000000594
    1. Alvarez E. A., Garrido M. A., Tobar E. A., Prieto S. A., Vergara S. O., Briceno C. D., et al. (2017). Occupational therapy for delirium management in elderly patients without mechanical ventilation in an intensive care unit: a pilot randomized clinical trial. J. Crit. Care 37 85–90. 10.1016/j.jcrc.2016.09.002
    1. American Psychiatric Association (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th Edn, Washington, DC: American Psychiatric Association.
    1. Boettger S., Nunez D. G., Meyer R., Richter A., Schubert M., Jenewein J. (2018). Subsyndromal delirium in the intensive care setting: phenomenological characteristics and discrimination of subsyndromal delirium versus no and full-syndromal delirium. Palliat. Support. Care 16 3–13. 10.1017/S1478951517000104
    1. Bokil H., Andrews P., Kulkarni J. E., Mehta S., Mitra P. P. (2010). Chronux: a platform for analyzing neural signals. J. Neurosci. Methods 192 146–151. 10.1016/j.jneumeth.2010.06.020
    1. Brown E. N., Lydic R., Schiff N. D. (2010). General anesthesia, sleep, and coma. N. Engl. J. Med. 363 2638–2650. 10.1056/NEJMra0808281
    1. Brummel N. E., Boehm L. M., Girard T. D., Pandharipande P. P., Jackson J. C., Hughes C. G., et al. (2017). Subsyndromal delirium and institutionalization among patients with critical illness. Am. J. Crit. Care 26 447–455. 10.4037/ajcc2017263
    1. Chan M. T., Cheng B. C., Lee T. M., Gin T., Group C. T. (2013). BIS-guided anesthesia decreases postoperative delirium and cognitive decline. J. Neurosurg. Anesthesiol. 25 33–42. 10.1097/ANA.0b013e3182712fba
    1. Charlson M. E., Pompei P., Ales K. L., MacKenzie C. R. (1987). A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J. Chronic Dis. 40 373–383. 10.1016/0021-9681(87)90171-8
    1. Ching S., Cimenser A., Purdon P. L., Brown E. N., Kopell N. J. (2010). Thalamocortical model for a propofol-induced alpha-rhythm associated with loss of consciousness. Proc. Natl. Acad. Sci. U.S.A. 107 22665–22670. 10.1073/pnas.1017069108
    1. Ching S., Purdon P. L., Vijayan S., Kopell N. J., Brown E. N. (2012). A neurophysiological-metabolic model for burst suppression. Proc. Natl. Acad. Sci. U.S.A. 109 3095–3100. 10.1073/pnas.1121461109
    1. Cole M., McCusker J., Dendukuri N., Han L. (2003). The prognostic significance of subsyndromal delirium in elderly medical inpatients. J. Am. Geriatr. Soc. 51 754–760. 10.1046/j.1365-2389.2003.51255.x
    1. Cole M. G., Ciampi A., Belzile E., Dubuc-Sarrasin M. (2013). Subsyndromal delirium in older people: a systematic review of frequency, risk factors, course and outcomes. Int. J. Geriatr. Psychiatry 28 771–780. 10.1002/gps.3891
    1. DeCrane S. K., Culp K. R., Wakefield B. (2012). Twelve-month fall outcomes among delirium subtypes. J. Healthc. Qual. 34 13–20. 10.1111/j.1945-1474.2011.00162.x
    1. Delgado C., Araneda A., Behrens M. I. (2017). Validation of the spanish-language version of the montreal cognitive assessment test in adults older than 60 years. Neurologia 34 376–385. 10.1016/j.nrl.2017.01.013
    1. Delorme A., Makeig S. (2004). EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Methods 134 9–21. 10.1016/j.jneumeth.2003.10.009
    1. Denny D. L., Lindseth G. (2017). Preoperative risk factors for subsyndromal delirium in older adults who undergo joint replacement surgery. Orthop. Nurs. 36 402–411. 10.1097/NOR.0000000000000401
    1. Eger E. I., II (2001). Age, minimum alveolar anesthetic concentration, and minimum alveolar anesthetic concentration-awake. Anesth. Analg. 93 947–953. 10.1097/00000539-200110000-00029
    1. Evered L., Silbert B., Knopman D. S., Scott D. A., DeKosky S. T., Rasmussen L. S., et al. (2018). Recommendations for the nomenclature of cognitive change associated with anaesthesia and surgery-2018. Br. J. Anaesth. 121 1005–1012. 10.1016/j.bja.2017.11.087
    1. Fritz B. A., Kalarickal P. L., Maybrier H. R., Muench M. R., Dearth D., Chen Y., et al. (2016). Intraoperative electroencephalogram suppression predicts postoperative delirium. Anesth. Analg. 122 234–242. 10.1213/ANE.0000000000000989
    1. Galvin J. E., Roe C. M., Powlishta K. K., Coats M. A., Muich S. J., Grant E., et al. (2005). The AD8: a brief informant interview to detect dementia. Neurology 65 559–564. 10.1212/01.wnl.0000172958.95282.2a
    1. Giattino C. M., Gardner J. E., Sbahi F. M., Roberts K. C., Cooter M., Moretti E., et al. (2017). Intraoperative frontal alpha-band power correlates with preoperative neurocognitive function in older adults. Front. Syst. Neurosci. 11:24. 10.3389/fnsys.2017.00024
    1. Gottesman R. F., Grega M. A., Bailey M. M., Pham L. D., Zeger S. L., Baumgartner W. A., et al. (2010). Delirium after coronary artery bypass graft surgery and late mortality. Ann. Neurol. 67 338–344. 10.1002/ana.21899
    1. Gutierrez R. G., Reyes F. I., Penna A. (2018). Delirium in the post-anesthesia care unit may be associated with the development of postoperative delirium in a cohort of elderly patients. Minerva Anestesiol. 85 326–327. 10.23736/S0375-9393.18.13304-9
    1. Hajat Z., Ahmad N., Andrzejowski J. (2017). The role and limitations of EEG-based depth of anaesthesia monitoring in theatres and intensive care. Anaesthesia 72(Suppl. 1), 38–47. 10.1111/anae.13739
    1. Hesse S., Kreuzer M., Hight D., Gaskell A., Devari P., Singh D., et al. (2019). Association of electroencephalogram trajectories during emergence from anaesthesia with delirium in the postanaesthesia care unit: an early sign of postoperative complications. Br. J. Anaesth. 122 622–634. 10.1016/j.bja.2018.09.016
    1. Hight D. F., Gaskell A. L., Kreuzer M., Voss L. J., Garcia P. S., Sleigh J. W. (2019). Transient electroencephalographic alpha power loss during maintenance of general anaesthesia. Br. J. Anaesth. 122 635–642. 10.1016/j.bja.2018.11.029
    1. Inouye S. K., Kosar C. M., Tommet D., Schmitt E. M., Puelle M. R., Saczynski J. S., et al. (2014a). The CAM-S: development and validation of a new scoring system for delirium severity in 2 cohorts. Ann. Intern. Med. 160 526–533. 10.7326/M13-1927
    1. Inouye S. K., Westendorp R. G., Saczynski J. S. (2014b). Delirium in elderly people. Lancet 383 911–922. 10.1016/S0140-6736(13)60688-1
    1. Inouye S. K., van Dyck C. H., Alessi C. A., Balkin S., Siegal A. P., Horwitz R. I. (1990). Clarifying confusion: the confusion assessment method. A new method for detection of delirium. Ann. Intern. Med. 113 941–948.
    1. Klimiec-Moskal E., Lis A., Pera J., Slowik A., Dziedzic T. (2019). Subsyndromal delirium is associated with poor functional outcome after ischaemic stroke. Eur. J. Neurol. 26 927–934. 10.1111/ene.13912
    1. Koponen H., Partanen J., Paakkonen A., Mattila E., Riekkinen P. J. (1989). EEG spectral analysis in delirium. J. Neurol. Neurosurg. Psychiatry 52 980–985. 10.1136/jnnp.52.8.980
    1. Levkoff S. E., Liptzin B., Cleary P. D., Wetle T., Evans D. A., Rowe J. W., et al. (1996). Subsyndromal delirium. Am. J. Geriatr. Psychiatry 4 320–329. 10.1097/00019442-199622440-00006
    1. Marcantonio E., Ta T., Duthie E., Resnick N. M. (2002). Delirium severity and psychomotor types: their relationship with outcomes after hip fracture repair. J. Am. Geriatr. Soc. 50 850–857. 10.1046/j.1532-5415.2002.50210.x
    1. Mashour G. A., Woodrum D. T., Avidan M. S. (2015). Neurological complications of surgery and anaesthesia. Br. J. Anaesth. 114 194–203. 10.1093/bja/aeu296
    1. Meagher D., O’Regan N., Ryan D., Connolly W., Boland E., O’Caoimhe R., et al. (2014). Frequency of delirium and subsyndromal delirium in an adult acute hospital population. Br. J. Psychiatry 205 478–485. 10.1192/bjp.bp.113.139865
    1. Minto C. F., Schnider T. W., Egan T. D., Youngs E., Lemmens H. J., Gambus P. L., et al. (1997). Influence of age and gender on the pharmacokinetics and pharmacodynamics of remifentanil. I. model development. Anesthesiology 86 10–23. 10.1097/00000542-199701000-00004
    1. Nasreddine Z. S., Phillips N. A., Bedirian V., Charbonneau S., Whitehead V., Collin I., et al. (2005). The montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J. Am. Geriatr. Soc. 53 695–699. 10.1111/j.1532-5415.2005.53221.x
    1. Ni K., Cooter M., Gupta D. K., Thomas J., Hopkins T. J., Miller T. E., et al. (2019). Paradox of age: older patients receive higher age-adjusted minimum alveolar concentration fractions of volatile anaesthetics yet display higher bispectral index values. Br. J. Anaesth. 123 288–297. 10.1016/j.bja.2019.05.040
    1. Ouimet S., Riker R., Bergeron N., Cossette M., Kavanagh B., Skrobik Y. (2007). Subsyndromal delirium in the ICU: evidence for a disease spectrum. Intensive Care Med. 33 1007–1013. 10.1007/s00134-007-0618-y
    1. Petersen R. C., Caracciolo B., Brayne C., Gauthier S., Jelic V., Fratiglioni L. (2014). Mild cognitive impairment: a concept in evolution. J. Intern. Med. 275 214–228. 10.1111/joim.12190
    1. Pfeffer R. I., Kurosaki T. T., Harrah C. H., Jr., Chance J. M., Filos S. (1982). Measurement of functional activities in older adults in the community. J. Gerontol. 37 323–329. 10.1093/geronj/37.3.323
    1. Purdon P. L., Pavone K. J., Akeju O., Smith A. C., Sampson A. L., Lee J., et al. (2015a). The ageing brain: age-dependent changes in the electroencephalogram during propofol and sevoflurane general anaesthesia. Br. J. Anaesth. 115(Suppl. 1), i46–i57. 10.1093/bja/aev213
    1. Purdon P. L., Sampson A., Pavone K. J., Brown E. N. (2015b). Clinical Electroencephalography for anesthesiologists: part i: background and basic signatures. Anesthesiology 123 937–960. 10.1097/ALN.0000000000000841
    1. Purdon P. L., Pierce E. T., Mukamel E. A., Prerau M. J., Walsh J. L., Wong K. F., et al. (2013). Electroencephalogram signatures of loss and recovery of consciousness from propofol. Proc. Natl. Acad. Sci. U.S.A. 110 E1142–E1151. 10.1073/pnas.1221180110
    1. Radtke F. M., Franck M., Lendner J., Kruger S., Wernecke K. D., Spies C. D. (2013). Monitoring depth of anaesthesia in a randomized trial decreases the rate of postoperative delirium but not postoperative cognitive dysfunction. Br. J. Anaesth. 110(Suppl. 1), i98–i105. 10.1093/bja/aet055
    1. Rampil I. J. (1998). A primer for EEG signal processing in anesthesia. Anesthesiology 89 980–1002. 10.1097/00000542-199810000-00023
    1. Renna M., Handy J., Shah A. (2003). Low baseline bispectral index of the electroencephalogram in patients with dementia. Anesth. Analg. 96 1380–1385. 10.1213/01.ane.0000059223.78879.0f
    1. Saczynski J. S., Marcantonio E. R., Quach L., Fong T. G., Gross A., Inouye S. K., et al. (2012). Cognitive trajectories after postoperative delirium. N. Engl. J. Med. 367 30–39. 10.1056/NEJMoa1112923
    1. Schuller P. J., Newell S., Strickland P. A., Barry J. J. (2015). Response of bispectral index to neuromuscular block in awake volunteers. Br. J. Anaesth. 115(Suppl. 1), i95–i103. 10.1093/bja/aev072
    1. Serafim R. B., Soares M., Bozza F. A., Lapa E. S. J. R., Dal-Pizzol F., Paulino M. C., et al. (2017). Outcomes of subsyndromal delirium in ICU: a systematic review and meta-analysis. Crit. Care 21:179. 10.1186/s13054-017-1765-3
    1. Sessler D. I., Sigl J. C., Kelley S. D., Chamoun N. G., Manberg P. J., Saager L., et al. (2012). Hospital stay and mortality are increased in patients having a “triple low” of low blood pressure, low bispectral index, and low minimum alveolar concentration of volatile anesthesia. Anesthesiology 116 1195–1203. 10.1097/ALN.0b013e31825683dc
    1. Shim J., DePalma G., Sands L. P., Leung J. M. (2015). Prognostic Significance of postoperative subsyndromal delirium. Psychosomatics 56 644–651. 10.1016/j.psym.2015.05.002
    1. Tobar E., Abedrapo M. A., Godoy J. A., Llanos J. L., Diaz M. J., Azolas R., et al. (2018). Impact of hypotension and global hypoperfusion in postoperative delirium: a pilot study in older adults undergoing open colon surgery. Rev. Bras. Anestesiol. 68 135–141. 10.1016/j.bjan.2017.10.002
    1. Tobar E., Romero C., Galleguillos T., Fuentes P., Cornejo R., Lira M. T., et al. (2010). Confusion assessment method for diagnosing delirium in ICU patients (CAM-ICU): cultural adaptation and validation of the Spanish version. Med. Intensiva 34 4–13. 10.1016/j.medin.2009.04.003
    1. Whitlock E. L., Sleigh J. (2019). Are we overdosing older patients? Br. J. Anaesth. 123 257–258. 10.1016/j.bja.2018.12.012
    1. Wildes T. S., Mickle A. M., Ben Abdallah A., Maybrier H. R., Oberhaus J., Budelier T. P., et al. (2019). Effect of electroencephalography-guided anesthetic administration on postoperative delirium among older adults undergoing major surgery: the ENGAGES randomized clinical trial. JAMA 321 473–483. 10.1001/jama.2018.22005
    1. Yesavage J. A., Brink T. L., Rose T. L., Lum O., Huang V., Adey M., et al. (1982). Development and validation of a geriatric depression screening scale: a preliminary report. J. Psychiatr. Res. 17 37–49.

Source: PubMed

Sponsoren und Mitarbeiter

Krankheiten

Drogeninterventionen

3
Abonnieren