Back To Search Results

Encephalopathic EEG Patterns

Editor: Kesava Mandalaneni Updated: 3/4/2023 7:43:22 PM

Introduction

Encephalopathy is described clinically as an alteration in generalized attention, cognition, or consciousness. It is a form of diffuse cerebral dysfunction with varying severities. The acute form of encephalopathy can range from mild confusion and delirium to coma. In the more chronic, slowly progressive, or static conditions of encephalopathy, there may be retention of attention initially with loss of cognitive capacity.

Electroencephalography (EEG) is useful in evaluating patients with acute and chronic encephalopathies. The primary role of EEG in this setting is to rule out seizures as a cause of altered mental status. Various patterns can be seen in patients with encephalopathy. Abnormal patterns, especially in an acute to subacute onset, are sensitive to encephalopathy but not specific to diagnosing causes. Most encephalopathies are associated with the slowing of dominant rhythms, as well as background activity. This is most likely due to the involvement of both the cortical neurons and the subcortical white matter dysfunction. Overall, EEG is useful for assessing the degree of cerebral dysfunction in encephalopathy and monitoring the changes along with clinical progression.

Function

Register For Free And Read The Full Article
Get the answers you need instantly with the StatPearls Clinical Decision Support tool. StatPearls spent the last decade developing the largest and most updated Point-of Care resource ever developed. Earn CME/CE by searching and reading articles.
  • Dropdown arrow Search engine and full access to all medical articles
  • Dropdown arrow 10 free questions in your specialty
  • Dropdown arrow Free CME/CE Activities
  • Dropdown arrow Free daily question in your email
  • Dropdown arrow Save favorite articles to your dashboard
  • Dropdown arrow Emails offering discounts

Learn more about a Subscription to StatPearls Point-of-Care

Function

Electroencephalogram (EEG)

EEG is usually requested to assess the brain's electrical activity and correlate the findings to physiological and disease states. Although it is mostly used to rule in or rule out seizures, it can also be useful in diagnosing encephalopathy, as well as nonepileptic spells. A standard EEG usually lasts for 30 mins to an hour; however, depending on the patient's clinical status, as well as the findings of the initial EEG if done, the total duration of the EEG may be longer. In the inpatient setting, with patients having extended alteration in sensorium, a longer EEG, usually accompanied by video monitoring, is requested. It is useful to assess various encephalopathic states and use advanced software to review the prolonged studies appropriately and in a timely manner.[1][2]

The EEG background activity varies with age. In individuals older than eight years old, the usual background activity in relaxed wakefulness consists of alpha waves ranging from 8.5 to 12Hz, with a posterior dominant rhythm that reacts to eye-opening and closure.[3]  In children below eight years, the posterior dominant rhythm is slower. There is an anterior-to-posterior gradient with faster beta range frequency waveforms over the frontal regions and slower waveforms over the posterior regions. There is only a small amount of theta activity (4-8Hz) during wakefulness with no delta activity. During drowsiness, there is an appearance of theta activity, predominantly in the central or parasagittal regions. As the individual falls asleep, non-rapid eye movement (NREM) and rapid eye movement (REM) sleep appear and alternate. Delta activity is predominantly seen in NREM sleep.[3]

The video recording, along with the EEG recording, allows the reviewer to access and review any clinical events and their associated waveforms in a time-locked fashion to determine if they are associated.[4] The typical EEG duration for encephalopathic patients is longer than routine EEG evaluation on an outpatient basis. Encephalopathic patients are usually seen in acute hospital settings and typically require a longer duration EEG of at least 24 to 48 hours to assess and understand the condition completely. This also helps in monitoring their progress and assessing for non-convulsive status epilepticus.[5][6][7]

Issues of Concern

Characteristic EEG Patterns Encountered in Acute Encephalopathy

Diffuse Slowing: 

In any acute encephalopathy, slowing of the background frequencies is a common EEG finding. The severity of the impairment in attention or consciousness is related to the degree of slowing. The initial changes in mild encephalopathy are typically slowing of the posterior dominant rhythm and reduction in the beta activity in the frontal regions.[8][9] Except in benzodiazepine or barbiturate-related cases, fast beta activity is abundant.[10] As encephalopathy worsens, there is an increase in theta and delta activity. These could be intermittent and then progress to being more continuous as the severity increases. In comatose patients, the delta activity predominates and becomes more continuous and slower as the coma deepens. Other changes include loss of reactivity. As the coma deepens further, the EEG background becomes discontinuous and is called the burst-suppression pattern. The inter-burst intervals increase in duration as the severity of the coma increases further before becoming flat ultimately. This stage is called electrocerebral inactivity or silence.[11]

Triphasic Waves (TWs)

TWs are characterized by a waveform with a triphasic morphology, with a blunt and broad contour, typically frontally dominant with an anterior to posterior phase lag. These could appear in a periodic pattern up to 2.5 Hz in frequency and may have a generalized distribution.[12] These waveforms were initially well associated with hepatic encephalopathy and were, at one point, considered a finding pathognomonic to this condition. The TWs were also associated with stages of progression of encephalopathy and elevated ammonia levels.[13] Studies have later highlighted the coexistence of various etiologies leading to metabolic abnormalities and diffuse white matter changes associated with this pattern.[12] TWs tend to appear more commonly with stimulation or state changes, often overriding a slow background EEG activity.[14][15]

Generalized Rhythmic Delta Activity (GRDA) 

Frontally dominant generalized rhythmic delta activity, previously referred to as frontal intermittent rhythmic delta activity (FIRDA), is a 2 to 3 Hz high amplitude rhythmic to semi-rhythmic activity with anterior predominance.[16][17] This pattern was commonly felt to be a diagnostic indicator of a midline cerebral pathology, like a 3 ventricle region tumor, but is now well recognized as a non-specific finding in encephalopathic EEGs. It is associated with encephalopathic states due to various etiologies like toxic, metabolic, infectious, neoplastic, and epileptic entities. GRDA, with a posterior emphasis that is commonly referred to as occipital intermittent rhythmic delta activity (OIRDA), is commonly seen in children with absence epilepsy.[18]

Lateralized Periodic Discharges (LPDs) or Periodic Lateralized Epileptiform Discharges (PLED) 

This EEG pattern is characterized by sharp waves or spikes of complexes 1-3Hz frequency in a semi-rhythmic pattern with no clear progression or spread.[19][20] These are usually associated with a subacute structural lesion. The most common condition associated with this pattern is stroke, among several other etiologies.[21] It is still debated whether this pattern is associated with seizures.[22] In one retrospective study, LPDs were associated with the development of epilepsy in one-third of the cohort and associated with markers of epileptogenicity in about 18% of the patients.[23]

Generalized Periodic Epileptiform Discharges (GPEDs) and Bilateral Independent Periodic Epileptiform Discharges (BiPEDs): 

As the names indicate, the GPEDs and BiPEDs are generalized and bilateral independent periodic epileptiform discharges, respectively. These patterns are seen in several conditions, including anoxic brain injury with severe diffuse cerebral dysfunction.[24][25]

Alpha Coma and Spindle Coma

In comatose individuals, diffuse alpha frequency activity can be seen. When the predominant alpha activity is noted in the posterior head regions and varies with noxious external stimuli, the etiology of the coma may be secondary to a brainstem lesion; this is associated with a poor prognosis.[26] More diffuse alpha activity with less reactivity to external stimuli is seen in anoxic injury after cardiac arrest and is commonly associated with a poor prognosis. When alpha coma is noted on EEG, the overall outcome depends on the etiology and reactivity to external stimuli, with a better prognosis in toxic encephalopathies and worse in anoxic encephalopathies.[26][27] Spindle coma consists of paroxysmal bursts of 11-14Hz activity appearing on a delta background and is usually known to occur in cases of anoxic injury, intracranial hemorrhage, diffuse cerebral insults, and head trauma.[28][29] EEG pattern spindle coma is associated with the involvement of the ponto-mesencephalic junction.[30]

Burst Suppression

Burst-suppression pattern consists of periods of mixed frequency activity (bursts) and inactivity periods or suppressing the background.[31] The bursts can have sharp and epileptiform discharges. This pattern can be seen in comatose individuals from various etiologies like toxic encephalopathies and anoxic encephalopathy due to cardiac arrest.[32] As the coma worsens, the interval between the bursts progressively increases, correlating with the clinical condition's severity.[33]

Electrocerebral Inactivity (ECI) or Silence (ECS)

Electrocerebral inactivity (ECI) or electrocerebral silence (ECS) is encountered when there is no EEG activity over 2 mV when recorded from scalp electrode pairs equal to or over 10 cm apart and with interelectrode impedances below 10,000 Ohms (10KOhms), but above 100 Ohms for at least 30 minutes of the recording. A qualified technologist should perform these types of recordings. When other causes like drug overdose are excluded, this pattern is associated with brain death.[34]

Clinical Significance

Encephalopathy is commonly described as an alteration of consciousness or attention ranging from mild to severe. Severe cases may be associated with poor prognosis and even death. It is secondary to various etiologies and can manifest in acute and chronic forms. EEG is usually requested to assess for pattern and rhythm abnormality, which may or may not be associated with ictal states. Continuous monitoring is also used to assess for progression and response to treatment. 

EEG in Common Acute Encephalopathies

Hepatic Encephalopathy

  • Encountered in patients with liver failure or insufficiency from any cause.
  • The EEG changes in the beginning commonly include slowing of the posterior dominant rhythm, followed by a gradual slowing of the background with the appearance of theta and delta activity.[8] The frontal intermittent rhythmic delta activity (FIRDA) can appear even in the presence of the posterior dominant rhythm.
  • The classic triphasic waves are best viewed with worsening of the encephalopathy and higher ammonia levels. As the severity worsens, sleep architecture is sparse.[9]

Renal or Uremic Encephalopathy

  • Encountered in patients with renal dysfunction of any cause with increased blood urea nitrogen level.[35]
  • These patients' EEGs are also similar to hepatic encephalopathic EEGs characterized by triphasic waveforms and slow background.
  • Often high-voltage rhythmic delta activity with bilateral spike-slow-wave complexes is seen in patients with dialysis disequilibrium syndrome associated with obtundation after a dialysis session.[36]
  • These events may or may not be associated with clinical seizures.[37][38]

Hypocalcemia

  • Hypocalcemia is, by definition, a corrected total serum calcium level below 2.2 mmol/L. It is most commonly associated with vitamin D deficiency and hypoparathyroidism, among several other etiologies.[39]
  • Initially, the most common EEG change is progressive slowing through theta and delta frequency activity dominance. There is also an association with generalized spikes and sharp waves with a burst of delta activity. A 3 to 4 Hz spike and wave discharges have been reported in neonatal EEG records.[40] 'Absence status' has also been reported in these patients.[41]

Hypercalcemia

  • Hypercalcemia is, by definition, encountered when the serum calcium levels are above 10.5 mg/dL.[42][41] This derangement is usually seen in patients with renal failure, hyperparathyroidism, and malignancies with an invasion of bony structures.
  • The EEG background changes with an increase in theta activity and delta activity are seen when serum calcium levels reach over 13 mg/dL.[8] The EEG can be associated with spikes and sharp waves as well. With an even further increase in calcium levels, the background slowing increases mostly in the frontal regions with the appearance of a paroxysmal burst of theta and delta activity along with triphasic waves.[43][44]
  • Association with diffuse and more posterior occipital spike and slow-wave activity has also been reported suggesting a posterior reversible encephalopathy syndrome-like presentation with hypercalcemia.[45][46]

Hypoglycemia

  • A blood glucose level below 70 mg/dL is usually defined as hypoglycemia. The correlation between blood glucose level, consciousness or attention level, and EEG changes are associated with a marked variation among individuals.[47]
  • The lowest blood glucose level where detectable EEG changes may be seen is between 29 to 40 mg/dl.[48]
  • The blood glucose level threshold is slightly higher in hypoglycemic individuals with diabetes, where EEG changes can be seen.[49]
  • The common finding associated with a lower glucose level is slowing of the background, mostly in the theta frequency range. This is noted in both adults and children.[50]

Hyperglycemia

  • There may be no or little slowing of the EEG background activity with a milder degree of hyperglycemia. As glucose levels increase, the diffuse delta slowing increases, and when a level of about 400 mg/dL is crossed, a sporadic spike can be seen.
  • Epilepsia partialis continua (EPC), clinically defined as a syndrome with continuous jerking of a body part, commonly a limb, is well associated with non-ketotic hyperglycemia and EEG focal spikes and focal slow waves in addition to a slower background.[51][52]

Hypernatremia

  • EEG changes in hypernatremia are characterized by diffuse slowing of the background activity.[53][54]

Hyponatremia

  • EEG changes in hyponatremia are associated with background slowing in theta to delta range frequencies as serum sodium levels fall, typically below 116 mg/dL.
  • The EEG may be associated with a stimulus-induced paroxysm of delta activity and central high-voltage theta activity between 6 to 7 Hz.[55] Triphasic waved and lateralized periodic discharges have also been described to occur.[56]
  • Absence status epilepticus with focal EEG discharge activity have also been reported to be associated with hyponatremia.[57][58]

Hypothyroidism

  • EEG in hypothyroid states is commonly associated with a low voltage activity, predominantly in the theta frequency range. Comatose individuals in this condition may show diffuse suppression with minimal activity. Sporadically, periodic sharp waves may be encountered.[59]

Hyperthyroidism

  • EEG changes in hyperthyroidism include an increased alpha activity with prominent central beta activity. A sporadic burst of theta or delta activity anteriorly has been described.[60] Triphasic waves have been noted as well.[61]
  • In acute thyrotoxicosis cases, EEG characterized by spikes and sharps with paroxysmal delta activity often associated with clinical seizures has been described.[8][62]

Hashimoto's Encephalopathy

  • This is a chronic, relapsing autoimmune thyroid disorder associated with antithyroid antibodies. It is usually associated with other autoimmune disorders like systemic lupus erythematosus and rheumatoid arthritis, which are usually steroid responsive.
  • EEG is associated with generalized slowing and frontally intermittent rhythmic delta activity in these patients. Often triphasic waves are also seen.[63]

Hypoxic (anoxic) Encephalopathy

  • Anoxic or hypoxic injury is encountered in cardiac arrest, and the extent of brain injury correlates with the severity of anoxia. This includes a wide spectrum from mild, slowing to severe suppression. Poor prognostic EEG findings include alpha or spindle coma with poor reactivity, burst suppression pattern with longer interburst intervals, and electrocerebral inactivity or silence.[8][64]
  • Hypoxic-ischemic encephalopathy in neonates is associated with a favorable outcome if the EEG performed within the first 8 hours after birth shows an active, normal background and portends a poorer outcome if the background activity is grossly abnormal or inactive.[65]

Infections Associated with the Central Nervous System (CNS)

  • CNS infections such as encephalitis, cerebral abscess, meningoencephalitis, or meningitis can manifest with diffuse changes and focal findings on the EEG. These can be associated with both generalized and focal epileptiform discharges with corresponding slowing.
  • A commonly encountered example is herpes simplex encephalitis, typically associated with lateralized periodic discharges over the affected temporal lobe.[66]

Trauma and Intracranial Hemorrhage

  • Traumatic brain injuries (TBI) can be associated with focal and diffuse changes based on the injury's extent and the affected intracranial structures. Global damages like diffuse axonal injury are typically associated with diffuse slowing, whereas contusion and hemorrhages are associated with focal slowing and epileptiform discharges.[67][68]
  • In extreme TBI cases, different EEG patterns can be encountered, including alpha or spindle coma due to brainstem injury, burst suppression, and even electrocerebral inactivity.

Drug-induced or Toxic Encephalopathy

  • The etiology of this type of encephalopathy is numerous. The EEG changes in this setting can range from the diffuse slowing of the background in theta and delta frequency activity along with an abundance of superimposed beta activity, especially with benzodiazepine and barbiturate overdoses. Some drugs are associated with focal, multifocal, or diffuse epileptic activity and seizures as well (ex: lithium). Triphasic waves are also seen in drug-induced encephalopathies.[9]

Other Issues

EEG in Chronic Encephalopathies

Chronic encephalopathies can also show EEG changes. The most common finding is slowing of the background in theta and delta range as the encephalopathy, or the disease, worsens. In neurodegenerative diseases like Alzheimer disease, Pick disease, Parkinson disease, and vascular dementia, EEG findings are typically normal at the initial stages.[69][70][71][72] A low amplitude EEG background activity is common in Huntington disease.[73] Periodic complexes with very high amplitude 2-4 delta waveforms intermixed with epileptiform or sharp discharges appearing every 5 to 7 seconds are seen in subacute sclerosing panencephalitis (SSPE). Clinically, these complexes can be associated with myoclonic jerks.[74]

Creutzfeldt-Jakob disease (CJD)

CJD is a rapidly progressive neurodegenerative disorder associated with prion protein (PrP), an abnormal isoform of a cellular glycoprotein. The majority of patients with CJD typically die within one year of contracting the illness. Clinically, in addition to rapidly progressive dementia, there can be myoclonus, visual or cerebellar signs, pyramidal/extrapyramidal signs, and akinetic mutism with variable association. EEG changes are commonly seen in this condition and are characterized by diffuse slowing, the appearance of periodic complexes, and generalized rhythmic delta activity.[75] The periodic complexes in CJD appear more frequently, usually at 1Hz. These complexes typically contain a sharp and slow wave and can be either unilateral initially or bilateral as the disease progresses.[76]

EEG Changes in Encephalopathy Associated with COVID-19 or SARS-CoV2 Infection

The common EEG changes noted in patients with 2019 novel coronavirus (COVID-19) related encephalopathy include generalized slowing of the background.[77][78][79] In another cohort of 18 patients, there was a direct correlation between oxygen saturation levels at the time of presentation and EEG changes. Lower oxygen levels were associated with more severe EEG patterns, like the association with epileptiform discharges.[80] Another cohort of 15 patients with COVID-19-related encephalopathy from a population of 873 patients admitted for SARS-CoV2 infection reported rather homogenous EEG changes mainly comprising of a diffuse background activity slowing and loss of reactivity towards external stimulation. 2 patients in this cohort were comatose from post anoxic injury with one case associated with a suppressed background and other with a discontinuous activity consistent with post-anoxic status epilepticus.[81]

Enhancing Healthcare Team Outcomes

EEG is a standard procedure required to assess the patients presenting to the emergency department with altered mentation and changes in awareness. An interprofessional team of caregivers is necessary to investigate and appropriately treat patients with encephalopathy who present to the hospitals in acute situations to achieve the best outcomes.[82][5] [Level 3] In addition to the primary clinicians, consultants, and neurologists, staff nurses, support medical staff, and well-qualified EEG technologists are necessary to provide interprofessional team care to these patients.

References


[1]

Sarkis RA, Lee JW. Quantitative EEG in hospital encephalopathy: review and microstate analysis. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2013 Oct:30(5):526-30. doi: 10.1097/WNP.0b013e3182a73dd5. Epub     [PubMed PMID: 24084185]


[2]

Rayi A, Murr N. Electroencephalogram. StatPearls. 2022 Jan:():     [PubMed PMID: 33085442]


[3]

St. Louis EK, Frey LC, Britton JW, Frey LC, Hopp JL, Korb P, Koubeissi MZ, Lievens WE, Pestana-Knight EM, St. Louis EK. Electroencephalography (EEG): An Introductory Text and Atlas of Normal and Abnormal Findings in Adults, Children, and Infants. 2016:():     [PubMed PMID: 27748095]


[4]

Nordli DR Jr. Usefulness of video-EEG monitoring. Epilepsia. 2006:47 Suppl 1():26-30     [PubMed PMID: 17044822]


[5]

Abend NS, Dlugos DJ, Hahn CD, Hirsch LJ, Herman ST. Use of EEG monitoring and management of non-convulsive seizures in critically ill patients: a survey of neurologists. Neurocritical care. 2010 Jun:12(3):382-9. doi: 10.1007/s12028-010-9337-2. Epub     [PubMed PMID: 20198513]

Level 3 (low-level) evidence

[6]

Schreiber JM, Zelleke T, Gaillard WD, Kaulas H, Dean N, Carpenter JL. Continuous video EEG for patients with acute encephalopathy in a pediatric intensive care unit. Neurocritical care. 2012 Aug:17(1):31-8. doi: 10.1007/s12028-012-9715-z. Epub     [PubMed PMID: 22565632]


[7]

Malhotra K, Rayi A. Gyriform Infarction in Cerebral Air Embolism: Imaging Mimicker of Status Epilepticus. Annals of Indian Academy of Neurology. 2017 Jul-Sep:20(3):313-315. doi: 10.4103/aian.AIAN_94_17. Epub     [PubMed PMID: 28904468]


[8]

Kaplan PW. The EEG in metabolic encephalopathy and coma. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2004 Sep-Oct:21(5):307-18     [PubMed PMID: 15592005]


[9]

Kaplan PW, Rossetti AO. EEG patterns and imaging correlations in encephalopathy: encephalopathy part II. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2011 Jun:28(3):233-51. doi: 10.1097/WNP.0b013e31821c33a0. Epub     [PubMed PMID: 21633250]


[10]

Feyissa AM, Tatum WO. Adult EEG. Handbook of clinical neurology. 2019:160():103-124. doi: 10.1016/B978-0-444-64032-1.00007-2. Epub     [PubMed PMID: 31277842]


[11]

Young GB. The EEG in coma. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2000 Sep:17(5):473-85     [PubMed PMID: 11085551]


[12]

Butterworth RF, Lavoie J, Giguère JF, Layrargues GP, Bergeron M. Cerebral GABA-ergic and glutamatergic function in hepatic encephalopathy. Neurochemical pathology. 1987 Feb-Apr:6(1-2):131-44     [PubMed PMID: 2888065]

Level 3 (low-level) evidence

[13]

Bermeo-Ovalle A. Triphasic Waves: Swinging the Pendulum Back in this Diagnostic Dilemma. Epilepsy currents. 2017 Jan-Feb:17(1):40-42. doi: 10.5698/1535-7511-17.1.40. Epub     [PubMed PMID: 28331470]


[14]

Brigo F, Storti M. Triphasic waves. American journal of electroneurodiagnostic technology. 2011 Mar:51(1):16-25     [PubMed PMID: 21516927]


[15]

Emmady PD, Murr N. EEG Triphasic Waves. StatPearls. 2022 Jan:():     [PubMed PMID: 32491611]


[16]

Hirsch LJ, Brenner RP, Drislane FW, So E, Kaplan PW, Jordan KG, Herman ST, LaRoche SM, Young B, Bleck TP, Scheuer ML, Emerson RG. The ACNS subcommittee on research terminology for continuous EEG monitoring: proposed standardized terminology for rhythmic and periodic EEG patterns encountered in critically ill patients. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2005 Apr:22(2):128-35     [PubMed PMID: 15805813]

Level 1 (high-level) evidence

[17]

Schmitt SE. Generalized and Lateralized Rhythmic Patterns. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2018 May:35(3):218-228. doi: 10.1097/WNP.0000000000000446. Epub     [PubMed PMID: 29718831]


[18]

Watemberg N, Linder I, Dabby R, Blumkin L, Lerman-Sagie T. Clinical correlates of occipital intermittent rhythmic delta activity (OIRDA) in children. Epilepsia. 2007 Feb:48(2):330-4     [PubMed PMID: 17295627]


[19]

CHATRIAN GE, SHAW CM, LEFFMAN H. THE SIGNIFICANCE OF PERIODIC LATERALIZED EPILEPTIFORM DISCHARGES IN EEG: AN ELECTROGRAPHIC, CLINICAL AND PATHOLOGICAL STUDY. Electroencephalography and clinical neurophysiology. 1964 Aug:17():177-93     [PubMed PMID: 14204927]


[20]

Newey CR, Sahota P, Hantus S. Electrographic Features of Lateralized Periodic Discharges Stratify Risk in the Interictal-Ictal Continuum. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2017 Jul:34(4):365-369. doi: 10.1097/WNP.0000000000000370. Epub     [PubMed PMID: 28166083]


[21]

Pohlmann-Eden B, Hoch DB, Cochius JI, Chiappa KH. Periodic lateralized epileptiform discharges--a critical review. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 1996 Nov:13(6):519-30     [PubMed PMID: 8978624]

Level 3 (low-level) evidence

[22]

Lin L, Drislane FW. Lateralized Periodic Discharges: A Literature Review. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2018 May:35(3):189-198. doi: 10.1097/WNP.0000000000000448. Epub     [PubMed PMID: 29718828]


[23]

Punia V, Vakani R, Burgess R, Hantus S. Electrographic and Clinical Natural History of Lateralized Periodic Discharges. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2018 Jan:35(1):71-76. doi: 10.1097/WNP.0000000000000428. Epub     [PubMed PMID: 29099408]


[24]

Sully KE, Husain AM. Generalized Periodic Discharges: A Topical Review. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2018 May:35(3):199-207. doi: 10.1097/WNP.0000000000000460. Epub     [PubMed PMID: 29718829]


[25]

Ruijter BJ, van Putten MJ, Hofmeijer J. Generalized epileptiform discharges in postanoxic encephalopathy: Quantitative characterization in relation to outcome. Epilepsia. 2015 Nov:56(11):1845-54. doi: 10.1111/epi.13202. Epub 2015 Sep 19     [PubMed PMID: 26384469]


[26]

Westmoreland BF, Klass DW, Sharbrough FW, Reagan TJ. Alpha-coma. Electroencephalographic, clinical, pathologic, and etiologic correlations. Archives of neurology. 1975 Nov:32(11):713-8     [PubMed PMID: 1180739]


[27]

Kaplan PW, Genoud D, Ho TW, Jallon P. Etiology, neurologic correlations, and prognosis in alpha coma. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 1999 Feb:110(2):205-13     [PubMed PMID: 10210610]


[28]

Hansotia P, Gottschalk P, Green P, Zais D. Spindle coma: incidence, clinicopathologic correlates, and prognostic value. Neurology. 1981 Jan:31(1):83-7     [PubMed PMID: 7192831]


[29]

Kaplan PW, Genoud D, Ho TW, Jallon P. Clinical correlates and prognosis in early spindle coma. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2000 Apr:111(4):584-90     [PubMed PMID: 10727908]

Level 2 (mid-level) evidence

[30]

Bergamasco B, Bergamini L, Doriguzzi T, Fabiani D. EEG sleep patterns as a prognostic criterion in post-traumatic coma. Electroencephalography and clinical neurophysiology. 1968 Apr:24(4):374-7     [PubMed PMID: 4174009]


[31]

Niedermeyer E. The burst-suppression electroencephalogram. American journal of electroneurodiagnostic technology. 2009 Dec:49(4):333-41     [PubMed PMID: 20073416]


[32]

Reeves AL, Westmoreland BF, Klass DW. Clinical accompaniments of the burst-suppression EEG pattern. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 1997 Mar:14(2):150-3     [PubMed PMID: 9165410]

Level 3 (low-level) evidence

[33]

Hofmeijer J, Tjepkema-Cloostermans MC, van Putten MJ. Burst-suppression with identical bursts: a distinct EEG pattern with poor outcome in postanoxic coma. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2014 May:125(5):947-54. doi: 10.1016/j.clinph.2013.10.017. Epub 2013 Oct 26     [PubMed PMID: 24286857]

Level 2 (mid-level) evidence

[34]

Stecker MM, Sabau D, Sullivan L, Das RR, Selioutski O, Drislane FW, Tsuchida TN, Tatum WO 4th. American Clinical Neurophysiology Society Guideline 6: Minimum Technical Standards for EEG Recording in Suspected Cerebral Death. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2016 Aug:33(4):324-7. doi: 10.1097/WNP.0000000000000322. Epub     [PubMed PMID: 27482789]


[35]

Glaser GH. Brain dysfunction in uremia. Research publications - Association for Research in Nervous and Mental Disease. 1974:53():173-99     [PubMed PMID: 4612659]

Level 3 (low-level) evidence

[36]

Hughes JR. Correlations between EEG and chemical changes in uremia. Electroencephalography and clinical neurophysiology. 1980 May:48(5):583-94     [PubMed PMID: 6153966]


[37]

Noriega-Sanchez A, Martinez-Maldonado M, Haiffe RM. Clinical and electroencephalographic changes in progressive uremic encephalopathy. Neurology. 1978 Jul:28(7):667-9     [PubMed PMID: 566866]


[38]

Gadewar P, Acharya S, Khairkar P, Shukla S, Mahajan SN. Dynamics of electroencephalogram (EEG) in different stages of chronic kidney disease. Journal of clinical and diagnostic research : JCDR. 2015 Mar:9(3):OC25-7. doi: 10.7860/JCDR/2015/11257.5705. Epub 2015 Mar 1     [PubMed PMID: 25954651]


[39]

Fong J, Khan A. Hypocalcemia: updates in diagnosis and management for primary care. Canadian family physician Medecin de famille canadien. 2012 Feb:58(2):158-62     [PubMed PMID: 22439169]


[40]

Kossoff EH, Silvia MT, Maret A, Carakushansky M, Vining EP. Neonatal hypocalcemic seizures: case report and literature review. Journal of child neurology. 2002 Mar:17(3):236-9     [PubMed PMID: 12026245]

Level 3 (low-level) evidence

[41]

Vignaendra V, Frank AO. Absence status in a patient with hypocalcemia. Electroencephalography and clinical neurophysiology. 1977 Sep:43(3):429-33     [PubMed PMID: 70344]

Level 3 (low-level) evidence

[42]

Maier JD, Levine SN. Hypercalcemia in the Intensive Care Unit: A Review of Pathophysiology, Diagnosis, and Modern Therapy. Journal of intensive care medicine. 2015 Jul:30(5):235-52. doi: 10.1177/0885066613507530. Epub 2013 Oct 15     [PubMed PMID: 24130250]


[43]

Swash M, Rowan AJ. Electroencephalographic criteria of hypocalcemia and hypercalcemia. Archives of neurology. 1972 Mar:26(3):218-28     [PubMed PMID: 4536776]


[44]

Moure JM. The electroencephalogram in hypercalcemia. Archives of neurology. 1967 Jul:17(1):34-51     [PubMed PMID: 6026171]


[45]

Kaplan PW. Reversible hypercalcemic cerebral vasoconstriction with seizures and blindness: a paradigm for eclampsia? Clinical EEG (electroencephalography). 1998 Jul:29(3):120-3     [PubMed PMID: 9660011]

Level 3 (low-level) evidence

[46]

Chen TH, Huang CC, Chang YY, Chen YF, Chen WH, Lai SL. Vasoconstriction as the etiology of hypercalcemia-induced seizures. Epilepsia. 2004 May:45(5):551-4     [PubMed PMID: 15101837]

Level 3 (low-level) evidence

[47]

Osorio I, Arafah BM, Mayor C, Troster AI. Plasma glucose alone does not predict neurologic dysfunction in hypoglycemic nondiabetic subjects. Annals of emergency medicine. 1999 Mar:33(3):291-8     [PubMed PMID: 10036343]


[48]

Blaabjerg L, Juhl CB. Hypoglycemia-Induced Changes in the Electroencephalogram: An Overview. Journal of diabetes science and technology. 2016 Nov:10(6):1259-1267     [PubMed PMID: 27464753]

Level 3 (low-level) evidence

[49]

Sejling AS, Kjær TW, Pedersen-Bjergaard U, Diemar SS, Frandsen CS, Hilsted L, Faber J, Holst JJ, Tarnow L, Nielsen MN, Remvig LS, Thorsteinsson B, Juhl CB. Hypoglycemia-associated changes in the electroencephalogram in patients with type 1 diabetes and normal hypoglycemia awareness or unawareness. Diabetes. 2015 May:64(5):1760-9. doi: 10.2337/db14-1359. Epub 2014 Dec 8     [PubMed PMID: 25488900]


[50]

Bjørgaas M, Sand T, Vik T, Jorde R. Quantitative EEG during controlled hypoglycaemia in diabetic and non-diabetic children. Diabetic medicine : a journal of the British Diabetic Association. 1998 Jan:15(1):30-7     [PubMed PMID: 9472861]

Level 2 (mid-level) evidence

[51]

Singh BM, Strobos RJ. Epilepsia partialis continua associated with nonketotic hyperglycemia: clinical and biochemical profile of 21 patients. Annals of neurology. 1980 Aug:8(2):155-60     [PubMed PMID: 6775582]


[52]

Kamha A. Non Ketotic Hyperosmolar Hyperglycemia presenting as Epilepsia Partialis Continua: An unusual presentation of a common disorder. The Libyan journal of medicine. 2008 Jun 1:3(2):111-2. doi: 10.4176/080420. Epub 2008 Jun 1     [PubMed PMID: 21516157]


[53]

Bhatia S, Kapoor AK, Sharma A, Gupta R, Kataria S. Cerebral encephalopathy with extrapontine myelinolysis in a case of postpartum hypernatremia. The Indian journal of radiology & imaging. 2014 Jan:24(1):57-60. doi: 10.4103/0971-3026.130697. Epub     [PubMed PMID: 24851006]

Level 3 (low-level) evidence

[54]

Tekgunduz KŞ, Caner I, Eras Z, Taştekin A, Tan H, Dinlen N. Prognostic value of amplitude-integrated electroencephalography in neonates with hypernatremic dehydration. The journal of maternal-fetal & neonatal medicine : the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstetricians. 2014 May:27(7):658-63. doi: 10.3109/14767058.2013.825603. Epub 2013 Aug 15     [PubMed PMID: 23919742]


[55]

CRAWFORD JD, DODGE P. COMPLICATIONS OF FLUID THERAPY IN NEUROLOGIC DISEASE; WATER INTOXICATION AND HYPERTONIC DEHYDRATION. Pediatric clinics of North America. 1964 Nov:11():1029-52     [PubMed PMID: 14219222]


[56]

Itoh N, Matsui N, Matsui S. Periodic lateralized epileptiform discharges in EEG during recovery from hyponatremia: a case report. Clinical EEG (electroencephalography). 1994 Oct:25(4):164-9     [PubMed PMID: 7813098]

Level 3 (low-level) evidence

[57]

Azuma H, Akechi T, Furukawa TA. Absence status associated with focal activity and polydipsia-induced hyponatremia. Neuropsychiatric disease and treatment. 2008 Apr:4(2):495-8     [PubMed PMID: 18728738]

Level 3 (low-level) evidence

[58]

Primavera A, Fonti A, Giberti L, Cocito L. Recurrent absence status epilepticus and hyponatremia in a patient with polydipsia. Biological psychiatry. 1995 Aug 1:38(3):189-91     [PubMed PMID: 7578663]

Level 3 (low-level) evidence

[59]

Gupta SP, Gupta PC, Kumar V, Ahuja MM. Electroencephalographic changes in hypothyroidism. The Indian journal of medical research. 1972 Jul:60(7):1101-6     [PubMed PMID: 4661458]


[60]

Hirano M, Endo M, Kubo T. Triphasic delta waves in a case of hyperthyroidism with psychotic symptoms. Clinical EEG (electroencephalography). 1982 Apr:13(2):97-102     [PubMed PMID: 7094359]

Level 3 (low-level) evidence

[61]

Faigle R, Sutter R, Kaplan PW. Electroencephalography of encephalopathy in patients with endocrine and metabolic disorders. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2013 Oct:30(5):505-16. doi: 10.1097/WNP.0b013e3182a73db9. Epub     [PubMed PMID: 24084183]


[62]

Kollmannsberger A, Kugler J, Scriba PC, Schwarz K. Thyrotoxic encephalopathy. Electroencephalography and clinical neurophysiology. 1967 Oct:23(4):384     [PubMed PMID: 4167789]


[63]

Henchey R, Cibula J, Helveston W, Malone J, Gilmore RL. Electroencephalographic findings in Hashimoto's encephalopathy. Neurology. 1995 May:45(5):977-81     [PubMed PMID: 7746418]

Level 3 (low-level) evidence

[64]

Sivaraju A, Gilmore EJ, Wira CR, Stevens A, Rampal N, Moeller JJ, Greer DM, Hirsch LJ, Gaspard N. Prognostication of post-cardiac arrest coma: early clinical and electroencephalographic predictors of outcome. Intensive care medicine. 2015 Jul:41(7):1264-72. doi: 10.1007/s00134-015-3834-x. Epub 2015 May 5     [PubMed PMID: 25940963]


[65]

Pressler RM, Boylan GB, Morton M, Binnie CD, Rennie JM. Early serial EEG in hypoxic ischaemic encephalopathy. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2001 Jan:112(1):31-7     [PubMed PMID: 11137658]


[66]

Singh TD, Fugate JE, Hocker S, Wijdicks EFM, Aksamit AJ Jr, Rabinstein AA. Predictors of outcome in HSV encephalitis. Journal of neurology. 2016 Feb:263(2):277-289. doi: 10.1007/s00415-015-7960-8. Epub 2015 Nov 14     [PubMed PMID: 26568560]


[67]

Ronne-Engstrom E, Winkler T. Continuous EEG monitoring in patients with traumatic brain injury reveals a high incidence of epileptiform activity. Acta neurologica Scandinavica. 2006 Jul:114(1):47-53     [PubMed PMID: 16774627]


[68]

Ianof JN, Anghinah R. Traumatic brain injury: An EEG point of view. Dementia & neuropsychologia. 2017 Jan-Mar:11(1):3-5. doi: 10.1590/1980-57642016dn11-010002. Epub     [PubMed PMID: 29213487]


[69]

Soininen H, Partanen J, Laulumaa V, Pääkkönen A, Helkala EL, Riekkinen PJ. Serial EEG in Alzheimer's disease: 3 year follow-up and clinical outcome. Electroencephalography and clinical neurophysiology. 1991 Nov:79(5):342-8     [PubMed PMID: 1718706]

Level 2 (mid-level) evidence

[70]

Yener GG, Leuchter AF, Jenden D, Read SL, Cummings JL, Miller BL. Quantitative EEG in frontotemporal dementia. Clinical EEG (electroencephalography). 1996 Apr:27(2):61-8     [PubMed PMID: 8681464]


[71]

Soikkeli R, Partanen J, Soininen H, Pääkkönen A, Riekkinen P Sr. Slowing of EEG in Parkinson's disease. Electroencephalography and clinical neurophysiology. 1991 Sep:79(3):159-65     [PubMed PMID: 1714807]


[72]

Signorino M, Pucci E, Belardinelli N, Nolfe G, Angeleri F. EEG spectral analysis in vascular and Alzheimer dementia. Electroencephalography and clinical neurophysiology. 1995 May:94(5):313-25     [PubMed PMID: 7774518]

Level 2 (mid-level) evidence

[73]

Scott DF, Heathfield KW, Toone B, Margerison JH. The EEG in Huntington's chorea: a clinical and neuropathological study. Journal of neurology, neurosurgery, and psychiatry. 1972 Feb:35(1):97-102     [PubMed PMID: 4260288]


[74]

Markand ON, Panszi JG. The electroencephalogram in subacute sclerosing panencephalitis. Archives of neurology. 1975 Nov:32(11):719-26     [PubMed PMID: 1180740]


[75]

Cambier DM, Kantarci K, Worrell GA, Westmoreland BF, Aksamit AJ. Lateralized and focal clinical, EEG, and FLAIR MRI abnormalities in Creutzfeldt-Jakob disease. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2003 Sep:114(9):1724-8     [PubMed PMID: 12948802]


[76]

Wieser HG, Schindler K, Zumsteg D. EEG in Creutzfeldt-Jakob disease. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2006 May:117(5):935-51     [PubMed PMID: 16442343]

Level 3 (low-level) evidence

[77]

Canham LJW, Staniaszek LE, Mortimer AM, Nouri LF, Kane NM. Electroencephalographic (EEG) features of encephalopathy in the setting of Covid-19: A case series. Clinical neurophysiology practice. 2020:5():199-205. doi: 10.1016/j.cnp.2020.06.001. Epub 2020 Jul 2     [PubMed PMID: 32838076]

Level 2 (mid-level) evidence

[78]

Pastor J, Vega-Zelaya L, Martín Abad E. Specific EEG Encephalopathy Pattern in SARS-CoV-2 Patients. Journal of clinical medicine. 2020 May 20:9(5):. doi: 10.3390/jcm9051545. Epub 2020 May 20     [PubMed PMID: 32443834]


[79]

Vellieux G, Rouvel-Tallec A, Jaquet P, Grinea A, Sonneville R, d'Ortho MP. COVID-19 associated encephalopathy: Is there a specific EEG pattern? Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2020 Aug:131(8):1928-1930. doi: 10.1016/j.clinph.2020.06.005. Epub 2020 Jun 24     [PubMed PMID: 32615526]


[80]

Cecchetti G, Vabanesi M, Chieffo R, Fanelli G, Minicucci F, Agosta F, Tresoldi M, Zangrillo A, Filippi M. Cerebral involvement in COVID-19 is associated with metabolic and coagulation derangements: an EEG study. Journal of neurology. 2020 Nov:267(11):3130-3134. doi: 10.1007/s00415-020-09958-2. Epub 2020 Jun 15     [PubMed PMID: 32556572]


[81]

Pasini E, Bisulli F, Volpi L, Minardi I, Tappatà M, Muccioli L, Pensato U, Riguzzi P, Tinuper P, Michelucci R. EEG findings in COVID-19 related encephalopathy. Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology. 2020 Sep:131(9):2265-2267. doi: 10.1016/j.clinph.2020.07.003. Epub 2020 Jul 18     [PubMed PMID: 32736327]


[82]

Herman ST, Abend NS, Bleck TP, Chapman KE, Drislane FW, Emerson RG, Gerard EE, Hahn CD, Husain AM, Kaplan PW, LaRoche SM, Nuwer MR, Quigg M, Riviello JJ, Schmitt SE, Simmons LA, Tsuchida TN, Hirsch LJ, Critical Care Continuous EEG Task Force of the American Clinical Neurophysiology Society. Consensus statement on continuous EEG in critically ill adults and children, part II: personnel, technical specifications, and clinical practice. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2015 Apr:32(2):96-108. doi: 10.1097/WNP.0000000000000165. Epub     [PubMed PMID: 25626777]

Level 3 (low-level) evidence