Association of network connectivity via resting state functional MRI with consciousness, mortality, and outcomes in neonatal acute brain injury

Boerwinkle, Varina L.; Sussman, Bethany L.; Manjón, Iliana; Mirea, Lucia; Suleman, Saher; Wyckoff, Sarah; Bonnell, Alexandra; Orgill, Andrew; Tom, Deborah

doi:10.1016/j.nicl.2022.102962

Cited by 19 publications

(37 citation statements)

References 86 publications

(113 reference statements)

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“…Study patients were 40 consecutive ABI neonates previously included in Boerwinkle et al 35 who received clinical resting state fMRI (RS) with MRI during the acute period hospitalization of a suspected brain insult as part of clinical care between March 2018 and July 2019 at Phoenix Children’s Hospital (PCH).…”

Section: Methodsmentioning

confidence: 99%

“…Test safety, timing and anesthesia are described in detail in Boerwinkle et al, 35 . Briefly, all participants were considered safe and stable to transport to the MR scanner for clinical MRI by the neonatologist and received continuous observation for the exams.…”

Section: Methodsmentioning

confidence: 99%

“…In neonates with HIE, MRI with RS scanning was performed after a 72-h period of therapeutic hypothermia and medications for symptomatic relief of cold temperature. In neonates with non-HIE brain MRI indications, MRI with RS occurred at a more variable time according to clinical indication see 35 for details . EEG was recorded using a standard array of 19 leads and continuous video (cv-EEG).…”

Section: Methodsmentioning

confidence: 99%

“…Data from the acute period were collected as described previously from the medical record 35 , and follow up data were included through December 8, 2021. The PCH IRB approved this retrospective follow-up analysis (PCH IRB-20-331) and waived consent for this study.…”

Section: Data Collectionmentioning

confidence: 99%

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Resting State Functional MRI Connectivity Association with Consciousness, Mortality, Longitudinal and Two-Year Outcomes in Neonatal Acute Brain Injury

Boerwinkle

Sussman

Manjón

et al. 2022

Preprint

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Background: An accurate and comprehensive test of integrated brain network function is needed for neonates during the acute brain injury period to inform on morbidity. In our first term neonatal acute brain injury (ABI) study we demonstrated resting state functional MRI (RS) acquired within 31 days of life, results in disrupted connectivity of the resting state fMRI networks, incrementally associated with consciousness, mortality, cognitive and motor development, and ongoing concern for seizures at 6 months post-gestation. In this retrospective cohort study, we evaluate extended 2-year outcomes in the same patients. Methods: Study subjects included the same 40 consecutive neonates from our prior study, with resting state functional MRI acquired within 31 days after suspected brain insult from March 2018 to July 2019. Acute-period exam and test results were assigned ordinal scores based on severity as documented by respective treating specialists. Analyses (Fisher exact, Wilcox Sum-Rank test ordinal/multinomial logistic regression) examined association of resting state networks with demographics, presentation, neurological exam, electroencephalogram, anatomical MRI, magnetic resonance spectroscopy, passive task functional MRI, and outcomes of inpatient and outpatient mortality, outpatient development measured by exam and the Pediatric Cerebral Performance Category Scale (PCPC), motor development and tone, and ongoing concern for seizure at up to 42 months of age. All statistical tests were 2-sided, with statistical significance and CI adjusted using a Bonferroni correction to account for multiple test comparisons for each network and other modality. Results: Subjects had a mean (standard deviation) gestational age of 37.8 (2.6) weeks, follow-up median age follow-up median age (interquartile range) 30.5 (23.6, 36.7) months, 68% were male, with a diagnosis of hypoxic ischemic encephalopathy (60%). Of the 40 patients, three died prior to discharge, and another four between 6-42 months, and 5 were lost to follow-up. Of the followed, findings at birth included mild distress (46%), moderately abnormal neurological exam (34%), and consciousness characterized as awake but irritable (37%). Significant associations after multiple testing corrections were detected for resting state networks: basal ganglia with PCPC (odds ratio [OR], 9.54; 99.4% confidence interval [CI], 1.89-48.1; P = 0.0003), inpatient mortality (OR, 57.5; 99% CI, 1.35->999; P = 0.006), outpatient mortality (OR, 65.7; 99% CI 1.47->999; P = 0.005), and motor tone/weakness (OR, 17.8; 99% CI, 2.2-143; P = 0.0004); language/frontoparietal network with developmental delay (OR, 3.64; 99% CI, 1.02-13.05; P = 0.009), PCPC (OR, 3.98; 99% CI, 1.09-14.45; P = 0.006), and outpatient mortality (OR, 9.2; 99% CI, 0.91-92.6; P = 0.01); default mode network with developmental delay (OR, 4.14; 99% CI, 1.19-14.43; P = 0.003); PCPC (OR, 4.1; 99% CI, 1.2-14.2; P = 0.004), inpatient mortality (OR, 20.41; 99% CI, 0.89-468; P = 0.01), and motor tone/weakness (OR, 3.35; 99% CI, 1.01-11.12; P = 0.009); and seizure onset zone with concern for seizures (OR, 4.02; 99% CI, 1.0-16.15; P = 0.01). Of the other acute phase tests, only anatomical MRI was showed association with and outcome, concern for seizure (OR, 2.40; 99% CI, 0.94-6.13; P = 0.01). Conclusions: This study provides level 3 evidence (OCEBM Levels of Evidence Working Group) demonstrating that in neonatal acute brain injury, the degree of abnormality of resting state networks is associated with mortality, ongoing concern for seizure and 2 year outcomes. These findings suggest RS is feasible and safe to implement in a busy tertiary neonatal ICU and the findings are of at least equivalent value to other standard of care diagnostics.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Data Collectionmentioning

confidence: 99%

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Resting State Functional MRI Connectivity Association with Consciousness, Mortality, Longitudinal and Two-Year Outcomes in Neonatal Acute Brain Injury

Boerwinkle

Sussman

Manjón

et al. 2022

Preprint

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“…In a systematic review, neonatal diaschisis resulting in later outcomes of severe childhood motor impairments were associated with MN FC ( 32 ). Furthermore, a recent study demonstrated that the presence and typicality of FC BG networks (identified from independent component analysis; ICA) in neonates during the acute period of brain injury predicted clinically noted developmental delay and motor-tone outcomes within 6 months ( 33 ). Finally, severity of motor deficits (chronic spastic quadriplegia) after anoxic brain injury from drowning have also been correlated with the “health” of motor rs-fMRI ICA networks in children and that this can be independent of cognitive function and cognitive networks ( 34 ).…”

Section: Functional Connectivitymentioning

confidence: 99%

Is Resting State Functional MRI Effective Connectivity in Movement Disorders Helpful? A Focused Review Across Lifespan and Disease

et al. 2022

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In the evolving modern era of neuromodulation for movement disorders in adults and children, much progress has been made recently characterizing the human motor network (MN) with potentially important treatment implications. Herein is a focused review of relevant resting state fMRI functional and effective connectivity of the human motor network across the lifespan in health and disease. The goal is to examine how the transition from functional connectivity to dynamic effective connectivity may be especially informative of network-targeted movement disorder therapies, with hopeful implications for children.

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Opioid neurotoxicity: A case series and review from members of the Child Neurology Society Neurocritical Care Special Interest Group

Boerwinkle,

Sweatt,

Grzezulkowska

et al. 2024

Annals of the Child Neurology Society

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ObjectiveThe Child Neurology Society 2023 Annual Meeting Neurocritical Care Special Interest Group discussed pediatric opioid use–associated neurotoxicity with cerebellar edema (POUNCE). Inspired by the discussion and the suspicion of an underrecognized severe form of the disorder, we provide a case series and literature review on this important and emerging topic.MethodsThe meeting was moderated by coauthor DSM, with formal presentation by coauthor AG, and supplemented with a supporting case by coauthor VLB. The attendees, by show of hand, were queried for experience with direct care of children in the critical care unit with neurotoxicity from opioid exposure. These meeting elements informed our literature review and case series.ResultsA key focus of the meeting was the importance of interdisciplinary communication regarding POUNCE, emphasizing the necessity for neurosurgical assessment due to mass effect. Approximately 10 of 40 attendees, representing different US hospitals, reported caring for children with opioid neurotoxicity and concern for increased intracranial pressure. Described during the meeting was a 2‐year‐old girl with opioid exposure, rapidly worsening neurological exam, and transforaminal herniation concerning for severe POUNCE syndrome and impact on brain networks by resting‐state functional magnetic resonanance imaging (rs‐MRI). After surgical decompression did not improve her neurological function, she underwent rs‐MRI, electroencephalogram, and MRI. The networks indicated better neurological function than the exam, consistent with outcome. In contrast, the second patient, was an 11‐month‐old boy with fentanyl exposure who was treated for opioid overdose and closely monitored clinically. He did not require surgical intervention and has recovered well.InterpretationThese patients add to the few publications documenting the management of POUNCE, which may require urgent posterior cranial fossa decompression, and highlight the potential for good outcomes. Additionally, this is the first report documenting rs‐fMRI for this condition, which was consistent with the patient's outcome.

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Association of network connectivity via resting state functional MRI with consciousness, mortality, and outcomes in neonatal acute brain injury

Cited by 19 publications

References 86 publications

Resting State Functional MRI Connectivity Association with Consciousness, Mortality, Longitudinal and Two-Year Outcomes in Neonatal Acute Brain Injury

Resting State Functional MRI Connectivity Association with Consciousness, Mortality, Longitudinal and Two-Year Outcomes in Neonatal Acute Brain Injury

Is Resting State Functional MRI Effective Connectivity in Movement Disorders Helpful? A Focused Review Across Lifespan and Disease

Opioid neurotoxicity: A case series and review from members of the Child Neurology Society Neurocritical Care Special Interest Group

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