Quantitative assessment of white matter injury in preterm neonates

Guo, Ting; Duerden, Emma G.; Adams, Elysia; Chau, Vann; Branson, Helen M.; Chakravarty, M. Mallar; Poskitt, Kenneth J.; Synnes, Anne; Grunau, Ruth E.; Miller, Steven P.

doi:10.1212/wnl.0000000000003606

Cited by 116 publications

(119 citation statements)

References 38 publications

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“…repetitive self-grooming and a reduction in social play behavior. In line with these findings, recent clinical studies revealed an association between diffuse WMI and motor abnormalities in preterm infants (Guo et al, 2017;Peyton et al, 2016Peyton et al, , 2017. Also, multiple studies have demonstrated that preterm infants are at risk to develop ASD later in life (Dudova et al, 2014;Johnson et al, 2010;Joseph et al, 2017;Kuzniewicz et al, 2014;Limperopoulos et al, 2008;Pritchard et al, 2016;Treyvaud et al, 2013).…”

Section: Discussionmentioning

confidence: 84%

“…Additionally, activation of microglia and astrogliosis are important pathophysiological hallmarks of diffuse WMI (Buser et al, ; Haynes et al, ; Verney et al, ). Functionally, WMI is associated with behavioral, cognitive, motor and psychological problems, like autism spectrum disorders (ASD), later in life (Back & Miller, ; Dudova et al, ; Guo et al, ; Johnson, Hollis, Kochhar, Hennessy, Wolke, & Marlow, ; Joseph et al, ; Kuzniewicz et al, ; Limperopoulos et al, ; Peyton et al, ; Pritchard et al, ; Treyvaud et al, ). While antenatal administration of magnesium sulfate in women at risk for preterm delivery reduces the risk of cerebral palsy in the fetus (Crowther, Hiller, Doyle, & Haslam, ; Doyle, Crowther, Middleton, Marret, & Rouse, ; Gano et al, ; Rouse et al, ), limited treatment options are currently available to protect preterm infants against diffuse WMI.…”

Section: Introductionmentioning

confidence: 99%

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Combined fetal inflammation and postnatal hypoxia causes myelin deficits and autism‐like behavior in a rat model of diffuse white matter injury

Tilborg

Achterberg

Kammen

et al. 2017

Glia

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Diffuse white matter injury (WMI) is a serious problem in extremely preterm infants, and is associated with adverse neurodevelopmental outcome, including cognitive impairments and an increased risk of autism‐spectrum disorders. Important risk factors include fetal or perinatal inflammatory insults and fluctuating cerebral oxygenation. However, the exact mechanisms underlying diffuse WMI are not fully understood and no treatment options are currently available. The use of clinically relevant animal models is crucial to advance knowledge on the pathophysiology of diffuse WMI, allowing the definition of novel therapeutic targets. In the present study, we developed a multiple‐hit animal model of diffuse WMI by combining fetal inflammation and postnatal hypoxia in rats. We characterized the effects on white matter development and functional outcome by immunohistochemistry, MRI and behavioral paradigms. Combined fetal inflammation and postnatal hypoxia resulted in delayed cortical myelination, microglia activation and astrogliosis at P18, together with long‐term changes in oligodendrocyte maturation as observed in 10 week old animals. Furthermore, rats with WMI showed impaired motor performance, increased anxiety and signs of autism‐like behavior, i.e. reduced social play behavior and increased repetitive grooming. In conclusion, the combination of fetal inflammation and postnatal hypoxia in rats induces a pattern of brain injury and functional impairments that closely resembles the clinical situation of diffuse WMI. This animal model provides the opportunity to elucidate pathophysiological mechanisms underlying WMI, and can be used to develop novel treatment options for diffuse WMI in preterm infants.

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Section: Discussionmentioning

confidence: 84%

Section: Introductionmentioning

confidence: 99%

Combined fetal inflammation and postnatal hypoxia causes myelin deficits and autism‐like behavior in a rat model of diffuse white matter injury

Tilborg

Achterberg

Kammen

et al. 2017

Glia

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“…PWML appear as focal signal intensity changes on conventional MRI and as restricted diffusion when the MRI is performed within a week after the presumed insult suggestive of ischemic injury (Kersbergen et al, 2014). Compared to cPVL, diffuse WMI and PWML are related to a milder degree of neurological impairment affecting mostly cognitive functioning and increased risk of psychological disorders later in life (Back & Miller, 2014;Guo et al, 2017;Keunen et al, 2017;Woodward, Clark, Bora, & Inder, 2012).…”

mentioning

confidence: 99%

Origin and dynamics of oligodendrocytes in the developing brain: Implications for perinatal white matter injury

Tilborg

Theije

Hal

et al. 2017

Glia

193

184

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Infants born prematurely are at high risk to develop white matter injury (WMI), due to exposure to hypoxic and/or inflammatory insults. Such perinatal insults negatively impact the maturation of oligodendrocytes (OLs), thereby causing deficits in myelination. To elucidate the precise pathophysiology underlying perinatal WMI, it is essential to fully understand the cellular mechanisms contributing to healthy/normal white matter development. OLs are responsible for myelination of axons. During brain development, OLs are generally derived from neuroepithelial zones, where neural stem cells committed to the OL lineage differentiate into OL precursor cells (OPCs). OPCs, in turn, develop into premyelinating OLs and finally mature into myelinating OLs. Recent studies revealed that OPCs develop in multiple waves and form potentially heterogeneous populations. Furthermore, it has been shown that myelination is a dynamic and plastic process with an excess of OPCs being generated and then abolished if not integrated into neural circuits. Myelination patterns between rodents and humans show high spatial and temporal similarity. Therefore, experimental studies on OL biology may provide novel insights into the pathophysiology of WMI in the preterm infant and offers new perspectives on potential treatments for these patients.

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“…Evidence of white matter injury was predominantly related to poorer motor outcomes. A white matter injury severity score was associated with adverse motor outcomes in three studies but not in two other studies . Greater white matter injury volumes in frontal, parietal, and temporal, but not occipital, lobes were associated with adverse motor outcomes .…”

Section: Resultsmentioning

confidence: 72%

“…Twenty‐six studies acquired early structural MRI data . Results of meta‐analyses are presented in Table and Figure .…”

Section: Resultsmentioning

confidence: 99%

Diagnostic accuracy of early magnetic resonance imaging to determine motor outcomes in infants born preterm: a systematic review and meta‐analysis

George

Pannek

Rose

et al. 2017

Develop Med Child Neuro

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Early magnetic resonance imaging (MRI) has reasonable sensitivity and specificity to determine later adverse motor outcomes and cerebral palsy (CP). Detection of infants who progressed to CP was stronger than motor outcomes. Global MRI scores determined adverse motor outcomes more accurately than white matter scores. Few studies report diagnostic accuracy of early MRI findings. Diagnostic accuracy is required to draw clinically meaningful conclusions from early MRI studies.

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Quantitative assessment of white matter injury in preterm neonates

Abstract: The predictive value of frontal lobe WMI volume highlights the importance of lesion location when considering the neurodevelopmental significance of WMI. Frontal lobe lesions are of particular concern.

Cited by 116 publications

References 38 publications

Combined fetal inflammation and postnatal hypoxia causes myelin deficits and autism‐like behavior in a rat model of diffuse white matter injury

Combined fetal inflammation and postnatal hypoxia causes myelin deficits and autism‐like behavior in a rat model of diffuse white matter injury

Origin and dynamics of oligodendrocytes in the developing brain: Implications for perinatal white matter injury

Diagnostic accuracy of early magnetic resonance imaging to determine motor outcomes in infants born preterm: a systematic review and meta‐analysis

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