|Year : 2019 | Volume
| Issue : 1 | Page : 20-27
Neuromonitoring in Malignant Middle Cerebral Artery Infarction: A Review of Literature
Songyu Chen, Ke Wang, Chengcheng Zhou, Sajan Pandey, Liang Gao
Department of Neurosurgery, Shanghai Tenth People's Hospital, Tongji University, China
|Date of Web Publication||4-Jan-2019|
Dr. Liang Gao
Department of Neurosurgery, Shanghai Tenth People's Hospital, Tongji University
Source of Support: None, Conflict of Interest: None
Malignant middle cerebral artery infarction is a devastating subtype of ischemic stroke, which carries a significant mortality rate (up to 80%) despite of conservative treatment. On the other hand, surgical decompressive procedure is the only established therapy to rescue the adverse effects of malignant edema and thus improve outcome. Accordingly, the early recognition of a possible malignant course as well as prediction of outcome is crucial for clinical decision-making. Numerous neuromonitoring techniques have been applied to address this issue. In theory, these techniques have the potential to present the information needed to guide targeted and timely intervention before irreversible damage takes place. However, the results were heterogeneous yet conflicting. We examined and summarized the recent evidence in this review, which may shed light on current trends.
Keywords: Brain oxygenation, cerebral hemodynamics, computed tomography, electroencephalography, intracranial pressure, magnetic resonance imaging, malignant middle cerebral artery infarction, microdialysis, multimodal monitoring
|How to cite this article:|
Chen S, Wang K, Zhou C, Pandey S, Gao L. Neuromonitoring in Malignant Middle Cerebral Artery Infarction: A Review of Literature. J Transl Crit Care Med 2019;1:20-7
|How to cite this URL:|
Chen S, Wang K, Zhou C, Pandey S, Gao L. Neuromonitoring in Malignant Middle Cerebral Artery Infarction: A Review of Literature. J Transl Crit Care Med [serial online] 2019 [cited 2022 Jun 29];1:20-7. Available from: http://www.tccmjournal.com/text.asp?2019/1/1/20/249336
| Introduction|| |
Malignant middle cerebral artery (MCA) infarction, also known as large hemispheric infarction (LHI), is a notorious disease associated with high mortality and morbidity. It accounts for about 2% to 8% of all hospitalized ischemic stroke. The term malignant MCA infarction (MMI) was introduced in 1996 and defined as infarction of the entire MCA territory appearing on computed tomography (CT) within 48 h, with or without infarction in other vascular territories. The term was used in the subsequent literature, but usually in a study-specific context with a different degree of modification from the original definition. The reported incidence of MMI varies from 18% to 31% of all ischemic stroke caused by MCA occlusion.,, It has a mortality of around 80% when treated medically.,, Space-occupying cerebral edema is a typical pathophysiological process after MMI, and it usually peaks 2–5 days after onset., Most of the patients experienced clinical deterioration in this period, and brain herniation is the major cause of death in patients suffered from this disease.
In the recent decades, accumulating evidence shows that surgical treatment may play a more important role in the management of patients with MMI. A pooled analysis of three randomized controlled trials shows that early decompressive hemicraniectomy (<48 h after stroke onset) significantly reduces mortality and improves functional outcome in patients with MMI who are 60 years or younger when compared with medical treatment. The following DESTINY II trial also gives evidence for early decompressive hemicraniectomy in patients of 61 years or older. Despite surgery plays a positive role in the treatment of MMI, selection of surgical candidates is a key decision for neurologists, neurosurgeons, and intensive care physicians. Therefore, close monitoring for the patients at risk of a malignant course after the MCA infarction is critical. Of note, survivors may live with severe disability after surgical treatment. Postoperative monitoring may help in the so-called “titrated treatment” and provide some clues to predict a favorable or unfavorable outcome. This review is focused on current brain monitoring approaches which may predict the “malignant” course or have prognostic values for the patients with MMI. The major information is summarized in [Table 1].
| Intracranial Pressure Monitoring|| |
Intracranial pressure (ICP) monitoring is considered to be fundamental to the management of patients with traumatic brain injury (TBI) as well as other acute brain injuries. Currently recommended ICP monitoring devices include intraventricular catheters and parenchymal ICP monitors. However, data challenged its routine use in the management of MMI. Only one prospective study in the 1990s reported increased ICP correlated with outcome, whereas in all patients clinical manifestations of brain herniation preceded an elevated ICP. Moreover, ICP monitoring within 3 h of deterioration to stupor revealed that 14 out of 19 patients had a normal ICP (within 15 mm Hg), and only two patients had a compromised cerebral perfusion pressure (CPP) of lower than 55 mm Hg. Another prospective study included 19 patients with a marked midline shift caused by malignant edema, whereas ICP values of 12 patients remained normal (<20 mm Hg) all the time. Of note, the 19 patients were presurgical and under moderate hypothermia, which might mask an increased ICP. The postulated mechanism is while the patient could be still at the initial stage of the ICP-volume curve, displacement caused by mass effect worsens. On the other hand, a recent study confirmed that 75% (9/12) patients had at least one episode of ICP elevation (>20 mm Hg) after hemicraniectomy, standard therapies to decrease ICP such as cerebrospinal fluid drainage were effective. Although it was a small retrospective study, its value in preserving the penumbra of brain tissue could not be ignored. An earlier case series of 10 patients also suggested ICP monitoring combined with microdialysis might help discern the development of malignant edema. In addition, hemorrhagic transformation or other new mass lesions can be timely discovered on the basis of continuous ICP monitoring.
The American Heart Association/American Stroke Association (AHA/ASA) stated that routine ICP monitoring is not indicated in hemispheric ischemic stroke. The neurocritical care society (NCS) guidelines for LHI claimed the value of ICP measurement in MMI remains unclear. Moreover, the two recommendations are both weak without solid evidence. From our view, continuous ICP monitoring in the postoperative period may help to establish the management strategy; however, its correlation with outcome needs further investigation. As for ICP gradients between affected and unaffected hemispheres can exist, a parenchymal ICP sensor in the peri-infarct zone might be a better choice.
| Electrophysiology|| |
It was believed that seizures were uncommon after hemispheric infarctions. However, recent data showed that around a half of patients with MMI developed seizures hours to days after decompressive hemicraniectomy. Electroencephalography (EEG) monitoring is generally accepted in all patients with acute brain injury and unexplained/persistent altered consciousness, besides continuous EEG monitoring are preferred. The NCS guidelines for LHI suggested considering EEG in the first 24 h after stroke to assist with predicting clinical course and continuous and quantitative EEG was a promising technique. Diedler et al. prospectively performed continuous EEG in 20 ventilated and sedated patients, among which 9 had LHI and the others suffered hemorrhagic stroke. A significant decrease in faster EEG activity (3.5–20.7 Hz) was observed during episodes of CPP lower than 60 mm Hg (both in affected and unaffected hemispheres, both P < 0.01). A further study of 10 sedated patients with MMI was conducted by the same group. Spectral analysis of EEG monitoring early (6 h) after hemicraniectomy were evaluated and revealed that a peak of faster EEG activity (5–10 Hz) was associated with a better outcome. A study included 21 patients with large cerebral infarction found a decent positive correlation between brain symmetry index and National Institutes of Health Stroke Scale (P < 0.01). However, Burghaus et al. reviewed early EEGs (within 24 h) of 25 patients with large MCA infarction. Both a slowing of background activity <8 Hz and a slowing of beta frequencies ≤20 Hz were associated with a malignant course (P < 0.05); however, the predictive values were relatively low to guide management.
In conclusion, we recommend the use of continuous EEG monitoring after decompressive hemicraniectomy. The preliminary results of early continuous and quantitative EEG monitoring are encouraging and require further validation.
Advances in neuroimaging have restricted the application of evoked potentials (EPs) in the Neonatal Intensive Care Unit setting. For selected patients, EPs can help in management and outcome prediction. Burghaus et al. reviewed brainstem auditory EPs (BAEP) of 30 patients with large MCA infarction. A pathologic BAEP was defined as abnormal amplitudes with side-to-side differences of >50% compared to the contralateral response. Eleven out of 14 patients with a malignant course showed a pathologic BAEP while 5 out of 16 patients with a benign course (P < 0.05). The report suggested that an early pathologic BAEP within 24 h might predict malignant edema; however, the prognostic value was limited.
| Transcranial Doppler Ultrasonography|| |
Transcranial Doppler ultrasonography in hemodynamics
In terms of hemodynamic monitoring, transcranial Doppler ultrasonography (TCD) has been the mainstay in vasospasm monitoring after subarachnoid hemorrhage (SAH) and in certain CPP-driven protocols of TBI management. However, TCD has limited evidence in the setting of MMI. Reinhard et al. reviewed dynamic cerebral autoregulation of 45 patients with acute MCA infarction, among which 16 severe cases underwent thrombolysis. The results showed that lower ipsilateral phase within 48 h after onset was significantly related to both larger infarction and poorer outcome. The area of significant decrease in ultrasound perfusion imaging within 40 h (11.3 ± 10.9 h) after onset correlated with follow-up CT scan and 4-month outcome. A new real-time ultrasound perfusion can visualize cerebral microbubbles and its quantitative measurement of replenishment kinetics was similar to perfusion magnetic resonance imaging (MRI); however, the correlation with course of disease was not described. For patients suffering from acute large infarction, TCD can assist in evaluating effect and tailoring dosage of mannitol by monitoring the hemodynamics of MCA.
Transcranial Doppler ultrasonography in neuroimaging
In critical patients with high risks of repeating CT scans, TCD can be used as a bedside and noninvasive alternative. Although its precision needs improvement, TCD can estimate ICP by measuring optic nerve sheath diameter, midline shift, ventricular width, etc., Reports confirmed that TCD could reliably measure midline shift.,,, Gerriets et al. conducted a prospective study on 16 patients suffering from acute MCA occlusion found that 5 out of 6 patients with a midline shift >4 mm at 32 h after onset died, except for one patient who underwent hemicraniectomy. A further prospective study of 42 patients with acute MCA or ICA occlusion confirmed this correlation. What's more, a midline shift ≥2.5 mm at 16 h after onset could predict brain herniation. Nevertheless, the two studies were conducted by the same group in the 1990s. and the sample sizes were small. Midline shifts measured by TCD might help in foreseeing malignant edema; however, further validation is necessary.
In general speaking, TCD is a powerful and pluripotent monitoring technique for neurocritical care. Of note, an examiner with expertise is required, and certain patients do not have sufficient bone windows. Emerging techniques and accumulating data of ultrasonography may confirm its value not only in detecting midline shifts but also in predication of malignant edema and outcome.
| Neuroimaging: Computed Tomography and Magnetic Resonance Imaging|| |
MMI presents with progressive brain edema and mass effect which results in a rapid rise in compartmental pressure and brain displacement leading to herniation. Noncontrast brain CT is the first-line screening examination for the suspected cerebral infarction cases. Frank hypodensity on brain CT involved ≥1/3 MCA territory can predict a malignant course., A hyperdense-vessel sign or midline shift ≥5 mm is also associated with poor prognosis. Moreover, CT scoring systems are expected to estimate the severity of the stroke and help peer review. Alberta Stroke Program Early CT Score (ASPECTS) was a semi-quantitative measurement of infarct extent which was correlated with functional outcome of acute ischemia stroke. ASPECTS ≤7 indicate more extensive MCA involvement and poor prognosis.
MMI accompanied by distal ICA or proximal MCA occlusion is correlated with poor outcome. It's known that collateral blood flow can prevent the extension of infarction. Evaluating collateral flow by CT angiography may provide information for assessing permanent ischemic injury in an emergency setting. A low collateral score demonstrated a trend to malignant edema and poor outcome.,
CT perfusion has been increasingly applied in the setting of acute ischemic stroke. Cerebral blood volume (CBV) is associated with the final infarct volume which determines the infarction core and reversible penumbra. In the hyperacute phase, large hypoperfusion (≥2/3 MCA territory) revealed by reduced CBV and CBF could predict MMI., CTP also can assess the extent of blood–brain barrier breakdown, increased permeability of infarct area, could predict the need for hemicraniectomy. If the CTP parameters were significantly improved after a hemicraniectomy, the patient was likely to have a favorable outcome. Due to an insufficient reliability of CTP, it cannot substitute the DWI, especially in acute ischemic stroke by now.
Magnetic resonance imaging
Magnetic resonance imaging (MRI) is more sensitive than CT for the early detection of acute ischemic stroke. Emerging protocols, for example, a 6-min MRI protocol showed promising results. However, we shall not neglect contraindications such as cardiac pacemakers, metal implants, and unstable patients. A diffusion-weighted imaging (DWI) lesion with a volume of 145 mL within 14 h (6.5 ± 3.5 h) after onset was predictive of a malignant course (100% sensitivity, 94% specificity). A recent study also reviewed MRI data within 14 h after onset, and a DWI volume >160 mL achieved a 97% specificity and 76% sensitivity, while a DWI volume >135 mL achieved an 86% specificity and 91% sensitivity. Notably, the determination of DWI volume relies on the threshold of the reduction of the apparent diffusion coefficient (ADC) used. A prospective, multicenter, observational cohort study reviewed MRI images of 140 patients. By applying an ADC cutoff value of 80% compared the contralateral healthy hemisphere, a DWI volume of >82 mL within 6 h of onset predicted malignant infarction with a high specificity of 98% but a low sensitivity of 52%. The authors further analyzed the data by adding intercaudate distance (ICD), a linear brain atrophy marker. A DWI lesion volume >87 mL plus a hemi-ICD ≤9.4 mm achieved a positive predictive value of 0.93 for an MMI. On the other hand, the predictive value of perfusion-weighted imaging (PWI) and susceptibility-weighted imaging (SWI) in MMI demands more evidence. A PWI (Tmax >8 s) volume of >85 mL had an area under curve of 0.82, which was better than a DWI volume of >80 mL. A recent retrospective study of PWI within 12 h after onset revealed a cerebral blood flow and volume ratio <0.85 correlated with a malignant course (odds ratio: 6.57; 95% confidence interval: 1.4–30.27). The extent of prominent vessel sign (PVS) on SWI imaging could predict infarct growth with an imperfect accuracy (r = 0.82). Moreover, an SWI-based scoring system was reported to be a better predictor of poor outcome compared with DWI in a pilot study of 16 patients.
To sum up, CT and MRI are established neuroimaging techniques in the setting of MMI. Both AHA/ASA and NCS recommended employing early changes on CT and MRI to predict MMI., New as well as simplified CT and MRI techniques are promising yet require further study.
| Microdialysis|| |
Microdialysis is a well-established bedside monitor of the brain tissue biochemistry that was introduced >20 years ago. The technique typically monitors lactate, pyruvate, glucose, glutamate, and glycerol. Glucose is the major substrate for brain metabolism. Lactate, pyruvate, and the lactate-to-pyruvate ratio (LPR) are often interpreted as markers of hypoxia or ischemia if mitochondrial function is normal. Glutamate is an excitatory neurotransmitter reflecting injury and inflammatory cascades. Glycerol is a membranal component of neurons and is a marker of central nervous system cellular breakdown. As for guidelines, the consensus of NCS and the European Society of Intensive Care Medicine (ESICM) recommended monitoring microdialysis in patients with or at risk of cerebral ischemia/hypoxia, energy failure, and glucose deprivation. To facilitate focal measurement of biochemical changes in the area most susceptible to secondary injury, placement of the microdialysis catheter in at-risk tissue is generally recommended, i.e., peri-infarct zone. Because microdialysis detects changes at the cellular level, theoretically, it can identify cerebral injury before clinically evident or detectable by other techniques. Several studies addressed in vivo regional neurochemistry as well as oxygenation concerning large cerebral infarction.
Berger et al., measured microdialysis parameters in patients with large MCA infarction undergoing therapeutic moderate hypothermia (33°:C) or hemicraniectomy. The results demonstrated that hypothermia and hemicraniectomy both significantly decreased glutamate, glycerol, lactate, and pyruvate in the peri-infarct zone. In terms of course of disease, a recent study revealed that lower peri-infarct glucose and individual pyruvate levels as well as higher glutamate and LPR were associated with delayed infarct progression. However, Dohmen et al. prospectively included 34 patients with infarctions covering >50% of the MCA territory and started multimodal neuromonitoring in frontal peri-infarct regions around 24 h (12–34 h) after onset. They discovered that multimodal neuromonitoring did not predict devastating outcomes early enough compared to PET conducted within 24 h after onset. For patients with a malignant course, CPP rapidly fell below the threshold of 50–60 mm Hg, and concentrations of excitotoxic neurotransmitters (e.g., glutamate), metabolic products (e.g., LPR, glycerol) significantly increased while brain parenchymal oxygen tension (PbtO2) fell to hypoxic levels (<10 mm Hg) around 48 h (22–72 h) after onset. Bosche et al. analyzed the same group of patients and found that lower peri-infarct concentrations of nontransmitter amino acids correlated with both malignant development of MCA infarction and the size of infarction, whereas the levels of PbtO2 did not show significance. This phenomenon occurred in the first 12 h of monitoring in advance of CBF alterations measured by PET, which might reflect an early expansion of the extracellular space caused by vasogenic edema. Notably, the panel of nontransmitter amino acids were measured post hoc by high-performance liquid chromatography, which may not be feasible in routine practice.
| Conclusion|| |
Microdialysis confirmed the effects of therapies such as hypothermia and hemicraniectomy in pilot studies. As for a powerful yet complicated technique, its early prognostic value in malignant edema and outcome is still controversial. Further studies as well as new biomarkers are necessary before microdialysis could be applied in routine practice.
| Brain Oxygenation|| |
Brain oxygen measurements include two invasive bedside techniques, PbtO2 and jugular bulb oxygen saturation (SjvO2). Noninvasive techniques such as PET, MR spectroscopy, and near-infrared spectroscopy (NIRS) can also be considered. PET is considered the gold standard. However, imaging provides only a snapshot of cerebral pathophysiology at a particular time point, thus it is not continuous and often requires transport of critical patients. NIRS is promising but immature in the setting of adult neurocritical care. SjvO2 reflects global cerebral oxygenation; however, its precision and safety are limited compared to PbtO2 monitoring.
Brain parenchymal oxygen tension monitoring
PbtO2 monitoring is a regional measurement of interstitial and capillary O2. PbtO2 is not a blood flow monitor, but a product of CBF and arteriovenous tension of O2. In other words, brain oxygenation depends on both oxygen supply (perfusion/oxygenation) and extraction (diffusion). The consensus of NCS and ESICM recommended monitoring brain oxygen in patients with or at risk of cerebral ischemia and/or hypoxia. PbtO2 has been used as a target for CPP-driven therapy and improved outcomes in TBI and SAH. However, few data focused on MMI. According to the data obtained from 11 patients with large MCA infarction, PbtO2 monitoring in the contralateral “healthy” frontal lobe can be applied to monitor osmotic drug effects and might predict brain herniation. Although ICP was decreased in every case, mannitol was most often (50%–60% of episodes) associated with an increase in both CPP and PbtO2, which may help avoid drug-associated ischemic events. 6–18 h before transtentorial herniation, pattern changes such as a sudden increase in the PbtO2 curve could be observed in 6 out of 9 patients. Moreover, Dohmen et al. included 15 patients with MMI and calculated their CPP–oxygen reactivity index (COR) from combined monitoring of PbtO2 and CPP. The majority of patients with a malignant course showed COR values above 1 at 24 h after stroke, which revealed impaired cerebrovascular autoregulation and correlated with a worse outcome. A malignant course could be predicted by a COR of 0.99 or less with sensitivity and specificity both >80%.
In conclusion, PbtO2 monitoring remains promising not only in evaluating therapeutic effect but also in predicting malignant development and outcome. However, the evidence is limited by small sample sizes and the nature of pilot studies, consequently larger prospective studies are demanded.
Near-infrared spectroscopy-based monitoring
To the best of our knowledge, NIRS-based cerebral oximetry is the only noninvasive, bedside monitoring technique available for cerebral oxygenation. Commercial devices measure regional cerebral oxygen saturation (rScO2) with high temporal and spatial resolution and permit simultaneous measurement over multiple regions of interest. However, known commercial devices are prone to extracerebral contamination as well as disturbance of intracranial hematoma. In animal TBI models, novel wireless NIRS systems successfully estimated PbtO2 in a noninvasive way., Terborg et al. applied NIRS in monitoring cerebral kinetics of indocyanine green, and the results correlated well with those obtained by PWI in patients with MCA infarction. For hyperacute stroke patients receiving endovascular recanalization, a bi-channel NIRS system showed the potential for guiding neuroanesthesia and predicting outcome. Damian and Schlosser reviewed 35 patients with complete MCA infarction who were monitored by bilateral NIRS monitoring. The average difference in rSO2(rSO2-diff) between infarcted and contralateral hemisphere reflected changes in hemodynamics and consumption of O2, which were influenced by hemispheric swelling. The rSO2-diff typically decreased with brain swelling, disappeared in patients who developed herniation, but increased significantly after successful management, for example, hemicraniectomy (preoperative rSO2-diff 8.0% ±7.3% vs. postoperative rSO2-diff 21.2 ± 8.0%, P = 0.005). Besides, a higher rSO2-diff at the end of monitoring was in line with a better outcome (15.2% ± 6.2% for GOS (Glasgow scale of outcome) 3–4 vs. 2.5% ± 5.8% for GOS 1–2; P < 0.001). Thus, further study combined with technical development may prove that noninvasive NIRS can predict malignant edema and outcome early enough, and in turn assist in clinical decision-making.
| Is Multimodal Neuromonitoring the Right Path to Choose?|| |
The NCS guideline for LHI could not recommend routine use of invasive multimodal neuromonitoring because of limited evidence. We have reviewed data concerning available monitoring techniques, but no strong recommendation could be made for a single technique. Although reports focusing on other types of acute injuries showed promising results, when and how to incorporate these techniques in the setting of MMI is largely unknown. We shall also keep in mind that multimodal neuromonitoring produces complex and large datasets. The risk of “information overload” cannot be ignored. Specialized informatics is required for timely integration and interpretation of various information.
In terms of safety, the pilot studies focusing on MMI revealed good safety profiles, probably due to limited sample size. However, data obtained from larger studies demonstrated that placing external ventricular drainage (EVD), i.e., an intraventricular ICP catheter had an infectious rate of 0%–27%. Postoperative CT scans discovered hemorrhages in up to one-third of the EVDs, whereas only <1% of them required surgical intervention. Other monitoring modalities, including intraparenchyal ICP probes, are safer. Careful manipulation and expertise would help reduce these complications.
In summary, we still lack enough and robust evidence to support the use of multimodal neuromonitoring in the setting of MMI. Only a handful of studies compared multimodal neuromonitoring with PET, which is the gold standard in quantifying infarct volume. From bench to bedside is never easy. The pilot studies suggested that this invasive and expensive method could provide data that help clinicians to know more about the injured brain, which in turn facilitates individualized and targeted management. An early CT followed by MRI scanning (unless contradicted) is fundamental to evaluation. We suggest considering placement of an ICP probe and a PbtO2 probe in the peri-infarct zone when feasible. Despite good safety profiles, probe locations shall always be confirmed with a nonenhanced CT scan after careful insertion. We also suggest noninvasive techniques such as qualitative EEG monitoring and TCD monitoring of hemodynamics can be routinely applied in the acute phase, especially in the setting of perioperative care. We believe a better understanding of MMI will be achieved by innovated and improved monitoring techniques as well as biomarkers. High-quality randomized clinical trials and advanced informatics are needed to determine the value and cost-effectiveness of multimodal neuromonitoring.
We thank the personnel of our department who dedicated to neurosurgical and neurocritical care.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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