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Volume 12 No. 06
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Case Reports

Altered Sleep Spindles in Delayed Encephalopathy after Acute Carbon Monoxide Poisoning

http://dx.doi.org/10.5664/jcsm.5900

Takuya Yoshiike, MD, PhD1; Masaki Nishida, MD, PhD1; Kazuyoshi Yagishita, MD, PhD2; Tadashi Nariai, MD, PhD3; Kenji Ishii, MD, PhD4; Toru Nishikawa, MD, PhD1
1Department of Psychiatry and Behavioral Sciences, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, Tokyo, Japan; 2Hyperbaric Medical Center, Medical Hospital, Tokyo Medical and Dental University, Tokyo, Japan; 3Department of Neurosurgery, Tokyo Medical and Dental University, Tokyo, Japan; 4Research Team for Neuroimaging, Tokyo Metropolitan Institute of Gerontology, Tokyo, Japan

ABSTRACT

Delayed encephalopathy (DE) affects not only the cerebral white matter and globus pallidus but also the cortex and thalamus. However, it remains unknown whether these brain lesions alter sleep along with clinical manifestations of DE. A 46-year-old man with DE underwent repetitive hyperbaric oxygen therapy. The patient was evaluated by not only neuropsychological and neuroimaging testing but polysomnography over the clinical course. Neurological symptoms improved markedly; however, profound frontal cognitive deficits continued. The polysomnography revealed prolonged absence and delayed recovery of sleep spindles across recordings. Alterations in spindle oscillations in DE could provide further insight into sleep regulatory networks.

Citation:

Yoshiike T, Nishida M, Yagishita K, Nariai T, Ishii K, Nishikawa T. Altered sleep spindles in delayed encephalopathy after acute carbon monoxide poisoning. J Clin Sleep Med 2016;12(6):913–915.


INTRODUCTION

Carbon monoxide (CO) poisoning causes persistent or delayed cognitive sequelae. Delayed encephalopathy (DE), characterized by sudden onset of neuropsychiatric symptoms days to weeks after apparent recovery from acute neurological symptoms, commonly causes subcortical demyelination that is mostly reversible.

Prior magnetic resonance imaging (MRI) research on DE due to CO intoxication has identified several brain regions that are typically affected: the globus pallidus (GP), frontal cortex, and thalamus.1 Although these brain structures are suggested to play reciprocal roles in neural regulation of sleep,2 no previous study conducted consecutive neurophysiological assessments using polysomnography (PSG) in CO-poisoned DE. We expected that PSG contributes to providing further mechanistic insight into sleep regulatory networks and more valid outcome prediction.

REPORT OF CASE

A 46-year-old man with depression attempted suicide by CO poisoning from burning charcoal in a sealed room. More than 24 h later, he was found in a state of coma and admitted to the emergency department. After 2 sessions of hyperbaric oxygen (HBO2) therapy, his carboxyhemoglobin level decreased from 32.9% to 0.9%. He regained consciousness on day 3. On day 26, aphasia, visuospatial cognitive impairment and gait disturbance suddenly occurred. Hence, he was transferred to our psychiatric department on day 59.

On readmission, he was mute and unable to obey any commands. Brain T2-weighted magnetic resonance imaging revealed white matter hyperintensities located in the periventricular and centrum semiovale regions, hypointensities in the thalamus, and hyperintensities in the GP bilaterally, suggesting DE after CO intoxication. He received HBO2 therapy 5 times a week, over a 9-month period, with a total of 136 sessions. We observed remarkable improvements in his neurological symptoms. However, he required nursing home admission after hospital discharge on day 622 due to residual frontal cognitive deficits (Table 1). Brain MRI on days 257, 315, and 538 showed no signs of improvement in the bilateral frontal lobes as compared with those on readmission (day 59). The 18F fluorodeoxyglucose positron emission tomography conducted on day 348 confirmed the presence of severely reduced glucose metabolism in bilateral frontal lobes.

Changes in cognitive function and sleep structure over the clinical course.

jcsm.12.6.913.t01.jpg

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Table 1

Changes in cognitive function and sleep structure over the clinical course.

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PSG was recorded on days 222, 342, and 571 to identify objective sleep quality and neurophysiological states of the CO-poisoned brain. The stage of sleep was scored and sleep spindles were manually identified in accordance with The American Academy of Sleep Medicine Manual for the Scoring of Sleep and Associated Events.3 The results revealed signifi-cant alterations in NREM sleep structures (Table 1). Initially, there was a near complete absence of sleep spindles in the first and second PSG recordings, and this significantly increased in the third recording. In contrast, a limited amount of slow wave sleep (SWS) was observed in the first PSG, and did not increase thereafter.

DISCUSSION

The possible mechanism underlying loss of sleep spindles in DE after CO intoxication is most likely to result from direct disruption of spindle generation associated with thalamic injury.4 Furthermore, GP lesions can lead to a loss of sleep spindles through interactions with the subthalamic nucleus and frontal cortex.2 As the frontal cortex was severely deactivated, the GP-subthalamic nucleus networks that regulate partially sleep spindles and SWS could be largely disrupted, resulting in a significant reduction in these specific oscillations. Given that the sleep spindles are known to require the cortex for their propagation, CO-related disruptions of the thalamocortical and corticocortical networks can inhibit their spread.5

The delayed recovery of sleep spindles and global clinical improvements in this patient can be attributed to the slow repair mechanisms underlying subcortical demyelination. Moreover, numerous human studies have indicated a robust association between spindle and slow oscillations and neural plasticity. This association underlies the consolidation of memory during sleep.6 Therefore, the present alterations in sleep structure could disturb the neuroplastic processes in the patient's brain, resulting in poor prognosis.

It should be noted that our investigation lacks a control group. Hence, alternative explanations cannot be ruled out. Further research is needed to investigate the underlying mechanisms of DE in order to successfully manage it.

DISCLOSURE STATEMENT

This was not an industry supported study. The authors have indicated no financial conflicts of interest. The written consent was obtained from the patient.

ABBREVIATIONS

CO

carbon monoxide

DE

delayed encephalopathy

GP

globus pallidus

HBO2

hyperbaric oxygen

MRI

magnetic resonance imaging

PSG

polysomnography

REM

rapid eye movement

SWS

slow wave sleep

ACKNOWLEDGMENTS

The authors thank the patient for corporation and consent. Author contributions: All authors made substantial contributions to the conception or design of the work, or the acquisition, analysis or interpretation of data. All authors contributed to drafting the work or revising it critically for important intellectual content. All authors approve the final version published. All authors are accountable for the accuracy and integrity of any part of the work. Specific coauthors responsibilities include the following: Dr. Yoshiike, Dr. Nishida, and Dr. Yagishita - patient management; Dr. Nariai andsDr. Ishii - neuroradiology; Dr. Yoshiike and Nr. Nishida - manuscript drafting; Dr. Yoshiike, Dr. Nariai, Dr. Ishii, and Dr. Nishikawa - critical revision of the manuscript.

REFERENCES

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