Dataset Information

Covert Consciousness in Acute Brain Injury Revealed by Automated Pupillometry and Cognitive Paradigms.

ABSTRACT:

Background

Identifying covert consciousness in intensive care unit (ICU) patients with coma and other disorders of consciousness (DoC) is crucial for treatment decisions, but sensitive low-cost bedside markers are missing. We investigated whether automated pupillometry combined with passive and active cognitive paradigms can detect residual consciousness in ICU patients with DoC.

Methods

We prospectively enrolled clinically low-response or unresponsive patients with traumatic or nontraumatic DoC from ICUs of a tertiary referral center. Age-matched and sex-matched healthy volunteers served as controls. Patients were categorized into clinically unresponsive (coma or unresponsive wakefulness syndrome) or clinically low-responsive (minimally conscious state or better). Using automated pupillometry, we recorded pupillary dilation to passive (visual and auditory stimuli) and active (mental arithmetic) cognitive paradigms, with task-specific success criteria (e.g., ≥ 3 of 5 pupillary dilations on five consecutive mental arithmetic tasks).

Results

We obtained 699 pupillometry recordings at 178 time points from 91 ICU patients with brain injury (mean age 60 ± 13.8 years, 31% women, and 49.5% nontraumatic brain injuries). Recordings were also obtained from 26 matched controls (59 ± 14.8 years, 38% women). Passive paradigms yielded limited distinctions between patients and controls. However, active paradigms enabled discrimination between different states of consciousness. With mental arithmetic of moderate complexity, ≥ 3 pupillary dilations were seen in 17.8% of clinically unresponsive patients and 50.0% of clinically low-responsive patients (odds ratio 4.56, 95% confidence interval 2.09-10.10; p < 0.001). In comparison, 76.9% healthy controls responded with ≥ 3 pupillary dilations (p = 0.028). Results remained consistent across sensitivity analyses using different thresholds for success. Spearman's rank analysis underscored the robust association between pupillary dilations during mental arithmetic and consciousness levels (rho = 1, p = 0.017). Notably, one behaviorally unresponsive patient demonstrated persistent command-following behavior 2 weeks before overt signs of awareness, suggesting prolonged cognitive motor dissociation.

Conclusions

Automated pupillometry combined with mental arithmetic can identify cognitive efforts, and hence covert consciousness, in ICU patients with acute DoC.

SUBMITTER: Othman MH

PROVIDER: S-EPMC11335945 | biostudies-literature | 2024 Apr

REPOSITORIES: biostudies-literature

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Publications

Covert Consciousness in Acute Brain Injury Revealed by Automated Pupillometry and Cognitive Paradigms.

Othman Marwan H MH Olsen Markus Harboe MH Hansen Karen Irgens Tanderup KIT Amiri Moshgan M Jensen Helene Ravnholt HR Nyholm Benjamin B Møller Kirsten K Kjaergaard Jesper J Kondziella Daniel D

Neurocritical care 20240411 1

<h4>Background</h4>Identifying covert consciousness in intensive care unit (ICU) patients with coma and other disorders of consciousness (DoC) is crucial for treatment decisions, but sensitive low-cost bedside markers are missing. We investigated whether automated pupillometry combined with passive and active cognitive paradigms can detect residual consciousness in ICU patients with DoC.<h4>Methods</h4>We prospectively enrolled clinically low-response or unresponsive patients with traumatic or n ...[more]

PMID: 38605221

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Project description:BackgroundSevere brain injury is a leading cause of death and disability. Diagnosis and prognostication are difficult, and errors occur often. Novel neuroimaging methods can improve diagnostic and prognostic accuracy, especially in patients with prolonged disorders of consciousness (PDoC). Yet it is currently unknown how family caregivers understand this information, raising ethical concerns that disclosure of neuroimaging results could result in therapeutic misconception or false hope.MethodsTo examine these ethical concerns, we conducted semi-structured interviews with caregivers of patients with PDoC who were enrolled in a concurrent neuroimaging research program designed to detect covert consciousness following severe brain injury. Caregivers held surrogate decision-making status for a patient. Interviews were conducted at two time points for each caregiver. The first interview occurred before the disclosure of neuroimaging results. The second occurred after disclosure. Descriptive analysis was applied to the data of four interview topics: (1) expectations for neuroimaging; (2) reactions to evidence of preserved cognition; (3) reactions to null results; and (4) understanding of the results and study.ResultsTwelve caregivers participated in the study; two caregivers shared surrogate decision-making status for one patient with PDoC. Twenty-one interviews were completed; one caregiver declined to participate in the post-disclosure interview. Three patients with PDoC associated with the study displayed evidence of covert consciousness. Overall, caregivers understood the neuroimaging research and results. Caregivers who received results of covert consciousness were generally pleased. However, there was some variation in expectations and reactions to these data and null results.ConclusionThis study, for the first time, reveals caregiver expectations for and reactions to neuroimaging evidence of covert consciousness in patients with PDoC. Caregivers understood the neuroimaging research and results, casting doubt on speculative ethical concerns regarding therapeutic misconception and false hope. However, disclosure of neuroimaging result could be improved. Pre-disclosure consultations might assist professionals in shaping caregiver expectations. Standardization of disclosure might also improve comprehension of the results.

Project description:See Schiff (doi:10.1093/awx209) for a scientific commentary on this article. Patients with acute severe traumatic brain injury may recover consciousness before self-expression. Without behavioural evidence of consciousness at the bedside, clinicians may render an inaccurate prognosis, increasing the likelihood of withholding life-sustaining therapies or denying rehabilitative services. Task-based functional magnetic resonance imaging and electroencephalography techniques have revealed covert consciousness in the chronic setting, but these techniques have not been tested in the intensive care unit. We prospectively enrolled 16 patients admitted to the intensive care unit for acute severe traumatic brain injury to test two hypotheses: (i) in patients who lack behavioural evidence of language expression and comprehension, functional magnetic resonance imaging and electroencephalography detect command-following during a motor imagery task (i.e. cognitive motor dissociation) and association cortex responses during language and music stimuli (i.e. higher-order cortex motor dissociation); and (ii) early responses to these paradigms are associated with better 6-month outcomes on the Glasgow Outcome Scale-Extended. Patients underwent functional magnetic resonance imaging on post-injury Day 9.2 ± 5.0 and electroencephalography on Day 9.8 ± 4.6. At the time of imaging, behavioural evaluation with the Coma Recovery Scale-Revised indicated coma (n = 2), vegetative state (n = 3), minimally conscious state without language (n = 3), minimally conscious state with language (n = 4) or post-traumatic confusional state (n = 4). Cognitive motor dissociation was identified in four patients, including three whose behavioural diagnosis suggested a vegetative state. Higher-order cortex motor dissociation was identified in two additional patients. Complete absence of responses to language, music and motor imagery was only observed in coma patients. In patients with behavioural evidence of language function, responses to language and music were more frequently observed than responses to motor imagery (62.5-80% versus 33.3-42.9%). Similarly, in 16 matched healthy subjects, responses to language and music were more frequently observed than responses to motor imagery (87.5-100% versus 68.8-75.0%). Except for one patient who died in the intensive care unit, all patients with cognitive motor dissociation and higher-order cortex motor dissociation recovered beyond a confusional state by 6 months. However, 6-month outcomes were not associated with early functional magnetic resonance imaging and electroencephalography responses for the entire cohort. These observations suggest that functional magnetic resonance imaging and electroencephalography can detect command-following and higher-order cortical function in patients with acute severe traumatic brain injury. Early detection of covert consciousness and cortical responses in the intensive care unit could alter time-sensitive decisions about withholding life-sustaining therapies.

Project description:Purpose Listening effort is quickly becoming an important metric for assessing speech perception in less-than-ideal situations. However, the relationship between the construct of listening effort and the measures used to assess it remains unclear. We compared two measures of listening effort: a cognitive dual task and a physiological pupillometry task. We sought to investigate the relationship between these measures of effort and whether engaging effort impacts speech accuracy. Method In Experiment 1, 30 participants completed a dual task and a pupillometry task that were carefully matched in stimuli and design. The dual task consisted of a spoken word recognition task and a visual match-to-sample task. In the pupillometry task, pupil size was monitored while participants completed a spoken word recognition task. Both tasks presented words at three levels of listening difficulty (unmodified, eight-channel vocoding, and four-channel vocoding) and provided response feedback on every trial. We refined the pupillometry task in Experiment 2 (n = 31); crucially, participants no longer received response feedback. Finally, we ran a new group of subjects on both tasks in Experiment 3 (n = 30). Results In Experiment 1, accuracy in the visual task decreased with increased signal degradation in the dual task, but pupil size was sensitive to accuracy and not vocoding condition. After removing feedback in Experiment 2, changes in pupil size were predicted by listening condition, suggesting the task was now sensitive to engaged effort. Both tasks were sensitive to listening difficulty in Experiment 3, but there was no relationship between the tasks and neither task predicted speech accuracy. Conclusions Consistent with previous work, we found little evidence for a relationship between different measures of listening effort. We also found no evidence that effort predicts speech accuracy, suggesting that engaging more effort does not lead to improved speech recognition. Cognitive and physiological measures of listening effort are likely sensitive to different aspects of the construct of listening effort. Supplemental Material https://doi.org/10.23641/asha.16455900.

Dataset Information

Covert Consciousness in Acute Brain Injury Revealed by Automated Pupillometry and Cognitive Paradigms.

Background

Methods

Results

Conclusions

Publications

Covert Consciousness in Acute Brain Injury Revealed by Automated Pupillometry and Cognitive Paradigms.

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