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Combat-related blast exposure and traumatic brain injury influence brain glucose metabolism during REM sleep in military veterans.

ABSTRACT: Traumatic brain injury (TBI), a signature wound of Operations Enduring and Iraqi Freedom, can result from blunt head trauma or exposure to a blast/explosion. While TBI affects sleep, the neurobiological underpinnings between TBI and sleep are largely unknown. To examine the neurobiological underpinnings of this relationship in military veterans, [(18)F]-fluorodeoxyglucose positron emission tomography (FDG PET) was used to compare mTBI-related changes in relative cerebral metabolic rate of glucose (rCMRglc) during wakefulness, Rapid Eye Movement (REM) sleep, and non-REM (NREM) sleep, after adjusting for the effects of posttraumatic stress (PTS). Fourteen veterans with a history of blast exposure and/or mTBI (B/mTBI) (age 27.5±3.9) and eleven veterans with no history (No B/mTBI) (age 28.1±4.3) completed FDG PET studies during wakefulness, REM sleep, and NREM sleep. Whole-brain analyses were conducted using Statistical Parametric Mapping (SPM8). Between group comparisons revealed that B/mTBI was associated with significantly lower rCMRglc during wakefulness and REM sleep in the amygdala, hippocampus, parahippocampal gyrus, thalamus, insula, uncus, culmen, visual association cortices, and midline medial frontal cortices. These results suggest that alterations in neurobiological networks during wakefulness and REM sleep subsequent to B/mTBI exposure may contribute to chronic sleep disturbances and differ in individuals with acute symptoms.

SUBMITTER: Stocker RP

PROVIDER: S-EPMC4112017 | biostudies-literature | 2014 Oct

REPOSITORIES: biostudies-literature

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Combat-related blast exposure and traumatic brain injury influence brain glucose metabolism during REM sleep in military veterans.

Stocker Ryan P J RP Cieply Marissa A MA Paul Benjamin B Khan Hassen H Henry Luke L Kontos Anthony P AP Germain Anne A

NeuroImage 20140602

Traumatic brain injury (TBI), a signature wound of Operations Enduring and Iraqi Freedom, can result from blunt head trauma or exposure to a blast/explosion. While TBI affects sleep, the neurobiological underpinnings between TBI and sleep are largely unknown. To examine the neurobiological underpinnings of this relationship in military veterans, [(18)F]-fluorodeoxyglucose positron emission tomography (FDG PET) was used to compare mTBI-related changes in relative cerebral metabolic rate of glucos ...[more]

PMID: 24893322

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Project description:In the military, explosive blasts are a significant cause of mild traumatic brain injuries (mTBIs). The symptoms associated with blast mTBIs causes significant economic burdens and a diminished quality of life for many service members. At present, the distinction of the injury mechanism (blast versus non-blast) may not influence TBI diagnosis. However, using noninvasive imaging, this study reveals significant distinctions between the blast and non-blast TBI mechanisms. A cortical whole-brain thickness analysis was performed using structural high-resolution T1-weighted MRI to identify the effects of blasts in persistent mTBI (pmTBI) subjects. A total of 41 blast pmTBI subjects were individually age- and gender-matched to 41 non-blast pmTBI subjects. Using FreeSurfer, cortical thickness was quantified for the blast group, relative to the non-blast group. Cortical thinning was identified within the blast mTBI group, in two clusters bilaterally. In the left hemisphere, the cluster overlapped with the lateral orbitofrontal, rostral middle frontal, medial orbitofrontal, superior frontal, rostral anterior cingulate and frontal pole cortices (p < 0.02, two-tailed, size = 1680 mm2). In the right hemisphere, the cluster overlapped with the lateral orbitofrontal, rostral middle frontal, medial orbitofrontal, pars orbitalis, pars triangularis and insula cortices (p < 0.002, two-tailed, cluster size = 2453 mm2). Self-report assessments suggest significant differences in the Post-Traumatic Stress Disorder Checklist-Civilian Version (p < 0.05, Bonferroni-corrected) and the Neurobehavioral Symptom Inventory (p < 0.01, uncorrected) between the blast and non-blast mTBI groups. These results suggest that blast may cause a unique injury pattern related to a reduction in cortical thickness within specific brain regions which could affect symptoms. No other study has found cortical thickness difference between blast and non-blast mTBI groups and further replication is needed to confirm these initial observations.

Project description:Blast-related traumatic brain injuries have been common in the Iraq and Afghanistan wars, but fundamental questions about the nature of these injuries remain unanswered.We tested the hypothesis that blast-related traumatic brain injury causes traumatic axonal injury, using diffusion tensor imaging (DTI), an advanced form of magnetic resonance imaging that is sensitive to axonal injury. The subjects were 63 U.S. military personnel who had a clinical diagnosis of mild, uncomplicated traumatic brain injury. They were evacuated from the field to the Landstuhl Regional Medical Center in Landstuhl, Germany, where they underwent DTI scanning within 90 days after the injury. All the subjects had primary blast exposure plus another, blast-related mechanism of injury (e.g., being struck by a blunt object or injured in a fall or motor vehicle crash). Controls consisted of 21 military personnel who had blast exposure and other injuries but no clinical diagnosis of traumatic brain injury.Abnormalities revealed on DTI were consistent with traumatic axonal injury in many of the subjects with traumatic brain injury. None had detectable intracranial injury on computed tomography. As compared with DTI scans in controls, the scans in the subjects with traumatic brain injury showed marked abnormalities in the middle cerebellar peduncles (P<0.001), in cingulum bundles (P=0.002), and in the right orbitofrontal white matter (P=0.007). In 18 of the 63 subjects with traumatic brain injury, a significantly greater number of abnormalities were found on DTI than would be expected by chance (P<0.001). Follow-up DTI scans in 47 subjects with traumatic brain injury 6 to 12 months after enrollment showed persistent abnormalities that were consistent with evolving injuries.DTI findings in U.S. military personnel support the hypothesis that blast-related mild traumatic brain injury can involve axonal injury. However, the contribution of primary blast exposure as compared with that of other types of injury could not be determined directly, since none of the subjects with traumatic brain injury had isolated primary blast injury. Furthermore, many of these subjects did not have abnormalities on DTI. Thus, traumatic brain injury remains a clinical diagnosis. (Funded by the Congressionally Directed Medical Research Program and the National Institutes of Health; ClinicalTrials.gov number, NCT00785304.).

Project description:ObjectiveTo determine whether a structured and quantitative assessment of differential olfactory performance-recognized between a blast-injured traumatic brain injury (TBI) group and a demographically comparable blast-injured control group-can serve as a reliable antecedent marker for preclinical detection of intracranial neurotrauma.MethodsWe prospectively and consecutively enrolled 231 polytrauma inpatients, acutely injured from explosions during combat operations in either Afghanistan or Iraq and requiring immediate stateside evacuation and sequential admission to our tertiary care medical center over a 2½-year period. This study correlates olfactometric scores with both contemporaneous neuroimaging findings as well as the clinical diagnosis of TBI, tabulates population-specific incidence data, and investigates return of olfactory function.ResultsOlfactometric score predicted abnormal neuroimaging significantly better than chance alone (area under the curve = 0.78, 95% confidence interval [CI] 0.70-0.87). Normosmia was present in all troops with mild TBI (i.e., concussion) and all control subjects. Troops with radiographic evidence of frontal lobe injuries were 3 times more likely to have olfactory impairment than troops with injuries to other brain regions (relative risk 3.0, 95% CI 0.98-9.14). Normalization of scores occurred in all anosmic troops available for follow-up testing.ConclusionQuantitative identification olfactometry has limited sensitivity but high specificity as a marker for detecting acute structural neuropathology from trauma. When considering whether to order advanced neuroimaging, a functional disturbance with central olfactory impairment should be regarded as an important tool to inform the decision process.Classification of evidenceThis study provides Class III evidence that central olfactory dysfunction identifies patients with TBI who have intracranial radiographic abnormalities with a sensitivity of 35% (95% CI 20.6%-51.7%) and specificity of 100% (95% CI 97.7%-100.0%).

Dataset Information

Combat-related blast exposure and traumatic brain injury influence brain glucose metabolism during REM sleep in military veterans.

Publications

Combat-related blast exposure and traumatic brain injury influence brain glucose metabolism during REM sleep in military veterans.

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