PEDIATRICS Vol. 123 No. 1 January 2009, pp. 319-326 (doi:10.1542/peds.2008-0283)
ARTICLE |
Comparison of Computer Tomography and Magnetic Resonance Imaging Scans on the Third Day of Life in Term Newborns With Neonatal Encephalopathy
Departments of a Pediatrics
b Radiology, University of British Columbia, Vancouver, British Columbia, Canada
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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OBJECTIVE. Our goal was to compare the patterns of brain injury detected by computed tomography, conventional MRI (T1- and T2-weighted sequences), and diffusion-weighted MRI in a cohort of term newborns with neonatal encephalopathy studied uniformly with all 3 modalities on the third day of life.
METHODS. Term newborns (
36 weeks' gestation) admitted to our center with neonatal encephalopathy were scanned with computed tomography, MRI, and diffusion-weighted MRI at 72 (±12) hours of life (n = 48). Each modality was scored independently of the other with previously validated scoring systems. The predominant pattern of brain injury was classified as: normal, watershed, basal nuclei, total (maximal basal nuclei and watershed), and focal-multifocal (presence of strokes and/or white matter injury alone).
RESULTS. The agreement for the predominant pattern of injury was excellent between MRI and diffusion-weighted MRI (77% agreement). The agreement for the pattern of injury was also good for computed tomography and diffusion-weighted MRI (67% agreement). The extent of cortical injury and focal-multifocal lesions, such as strokes and white matter injury, were less apparent on computed tomography than diffusion-weighted MRI. In 19 newborns with a repeat MRI in the second week of life, the predominant pattern seen on the day 3 diffusion-weighted MRI was confirmed.
CONCLUSIONS. Diffusion-weighted MRI is the most sensitive technique with which to assess brain injury on day 3 of life in term newborns with neonatal encephalopathy, particularly for cortical injury and focal-multifocal lesions such as stroke and white matter injury. All 3 modalities identify the most serious patterns of brain injury similarly.
Key Words: brain imaging • diffusion-weighted MRI • hypoxic-ischemic encephalopathy • magnetic resonance • neonatal, hypoglycemia
Abbreviations: NE—neonatal encephalopathy • CT—computed tomography • DW—diffusion-weighted • BN—basal nuclei • WMI—white matter injury • ADC—apparent diffusion coefficient • RS—resuscitation score
Neonatal encephalopathy (NE) is a major cause of mortality and morbidity in newborns and occurs in 6 per 1000 live term births.1–3 Management of affected newborns includes identification of the underlying etiology, the timing of brain injury, and the prediction of neurodevelopmental outcome. Current guidelines for neuroimaging in NE states that "a noncontrast computed-tomography (CT) should be performed to detect hemorrhagic lesions in the encephalopathic term infant with a history of birth trauma, and evidence of low hematocrit or coagulopathy. If CT findings are inconclusive, magnetic resonance (MR) imaging (MRI) should be performed. For other neonates with acute NE, MRI should be performed between days 2 and 8 to assess the location and extent of injury."4 Very few studies have directly compared CT and MRI.5,6 Since the publication of the Practice Parameter, additional studies have demonstrated that the extent of brain injury on MRI is an important predictor of neurodevelopmental outcome in affected newborns.7,8 More recently, the predominant pattern of brain injury was found to be more strongly associated with neurodevelopmental outcome than the severity of injury in any given region.9 Consequently, the main objective of this study is to compare the predominant pattern of injury detected with CT, conventional MRI (T1- and T2-weighted sequences), and diffusion-weighted MRI (DW MRI) in a series of term newborns consecutively admitted with encephalopathy and examined with all 3 modalities on the third day of life.
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MATERIALS AND METHODS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Study Population
This study was approved by the University of British Columbia Clinical Research Ethics Board. The study population consisted of term newborns with NE cared for between 2004 and 2007 at Children's and Women's Hospital of British Columbia, a provincial tertiary level neonatal referral center. Standard care at this center for all newborns with suspected NE is CT scan and T1/T2-MRI with DW MRI day 3 of life (72 ± 12 hours). This time window was chosen because previous CT studies demonstrated that brain imaging abnormalities after perinatal hypoxic-ischemic insult are maximal in this period.10,11
Inclusion criteria comprised gestational age 36 weeks and encephalopathy clinically recognizable, and at least 1 of the following criteria: (1) fetal distress at delivery; (2) requirement for resuscitation at birth; (3) Apgar score of 
5 at 5 minutes; or (4) metabolic acidosis. Newborns with clinical evidence of congenital malformations, genetic abnormalities, and antenatal infections were excluded. These criteria were meant to identify a cohort of NE of presumed hypoxic-ischemic origin.
Imaging Technique and Image Review
All CT studies were performed on a Philips Brilliance 16-slice multidetector CT scanner using the same procedure used at our institution since 1986. The scanner was calibrated to a water phantom or an acrylic head phantom embedded with acrylic of 20, 25, 35, and 40 Hounsfield units before every study. All CT studies were performed without sedation at 72 ± 12 hours after birth with axial 3-mm slices angled at 20° from the canthomeatal line and using these factors: 120 kV at 300 mA/second.
MRI studies were performed with sedation administered by an anesthesiologist immediately after the CT study. The examinations were conducted on a Siemens 1.5 Tesla Avanto using VB 13A software and included the following sequences (time of relaxation/time of echo/averages/field of view/thickness/gap): axial and coronal T1-weighted spin echo images (800/20/1/230/4 mm/0.2 mm), axial fast spin echo T2-weighted images (4000/101/2/230/4 mm/0.5 mm), and isotropic diffusion-weighted images b = 700, 1000, with apparent diffusion coefficient (ADC) maps (3300/82/4/210/4 mm/0.2 mm). A follow-up T1/T2-MRI was performed on days 8 to 10 in 19 newborns based on clinical indications, such as when the newborn's neurologic condition remained abnormal or when there was discrepancy between the medical history and the neurologic status.
Imaging review was conducted sequentially with the coding of CT images performed 1 to 2 months before analyzing the T1/T2-MRI data. An experienced neuroradiologist, blinded to the newborn's medical history, coded each CT study according to an established CT scoring system employed at our institution since 1994.12 The severity of injury to the basal nuclei (BN), white matter, and cerebral cortex were each coded separately on a 4-point scoring system. The BN involvement was assessed as (0) normal, (1) questionable, minimal involvement, (2) definite involvement, but attenuation not as low as the white matter, and (3) definite involvement, with attenuation as low as the white matter. White matter involvement was assessed as (0) normal, (1) patchy, questionable low density, (2) definite white matter low density, patchy, with intermediate attenuation, and (3) severe and extensive white matter low attenuation throughout both cerebral hemispheres. Cortical involvement was defined as (0) normal, (1) definite patchy edema, 25% of the cortex, (2) definite edema involving 25% to 50% of the cortex, and (3) definite edema involving >50% of the cortex. The MRI data were reviewed later by 2 of the investigators and classified by consensus. The T1- and T2-weighted images were first reviewed without the diffusion data and scored according to a previously validated system for acute and subacute signal abnormalities.13 The extent of injury was scored 0 to 4 in the basal ganglia/thalamus region and 0 to 5 in the watershed region. Later, the DW MRI with the ADC maps were reviewed and coded as described earlier.13
Because the predominant pattern of brain injury on MRI has previously been found to be a strong predictor of neurodevelopmental outcome in newborns with encephalopathy, the subjects were then classified according to their predominant pattern of injury: normal, watershed, BN (Fig 1), total injury, and focal-multifocal injury (Fig 2). 9 Newborns had the watershed pattern if the white matter/cortex scores on CT (or the watershed scores on MRI) were higher than the BN scores. Newborns had the BN pattern if the BN scores were equal or higher than the white matter/cortex scores on CT (or the watershed scores on MRI). The total pattern included newborns with maximal injury in the BN and watershed/white matter. Focal-multifocal injury was added as a fifth pattern to account for focal and multifocal white matter injury (WMI, Fig 3) 14 and strokes (Fig 4) 15–17. Strokes were defined as focal parenchymal infarcts, either in an arterial or venous distribution.18 These focal and multifocal injuries were distinct in location from the abnormalities classified as the watershed-predominant pattern. Findings that could not be classified in these categories were described separately as "other pattern of injury."
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Because the scoring systems for CT and MRI were different, the former being based on the severity and the latter on the extent of injury, we applied the CT scoring system to MRI and confirmed that the predominant pattern of injury was similar with each system.12,13 In this study, findings on CT and T1/T2-MRI are described relatively to those on DW MRI because previous studies suggest that this modality is most sensitive to injury in its earliest phase.15,19–22 Thus, for the comparisons in this study we considered DW MRI as the gold standard.
Clinical Data Collection
Medical charts were reviewed systematically for information about pregnancy, labor, delivery, and perinatal course. A resuscitation score (RS) was used to summarize management at birth, ranging from no intervention to endotracheal intubation with ventilation and medication (score: 1–6).23 An encephalopathy score was calculated (range: 0–7) to grade the newborn's neurologic status in the first 3 days of life,24,25 assigning 1 point each for abnormalities in feeding, alertness, tone, respiratory status, and reflexes, and 2 points for clinical seizures. A seizure score was used to grade the severity of clinical seizures (none [0] to severe [10]).23
Data Analysis
Statistical analysis was performed with Stata 9.2 software (Stata Corporation, College Station, TX). Agreement between findings on the imaging modalities was described with the kappa (
) coefficient. The strength of agreement was interpreted by the scale proposed by Landis and Koch,26 which spectrum of agreement ranges from poor/fair ( = 0.00–0.40) to almost perfect ( = 0.81–1.00), with in-between agreement defined as good ( = 0.41–0.60) and excellent ( = 0.61–0.80). Clinical characteristics of the newborns were compared by using Fisher's exact test and Kruskal-Wallis test for categorical and continuous data, respectively.
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RESULTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Clinical Features and Patterns of Brain Injury on DW MRI
From January 2004 to January 2007, 48 term newborns (29 boys) met our inclusion criteria. On DW MRI of the brain, 16 infants had normal findings. Watershed-predominant injury was seen in 4 newborns, whereas BN and total patterns were identified in 8 and 7, respectively. The remaining subjects (13) were classified as having a focal-multifocal pattern of injury. Table 1 illustrates the clinical features of these infants according to their predominant pattern of brain injury on DW MRI. All newborns required resuscitation at delivery (RS
4); the only neonate who did not receive respiratory support in the delivery room had significant fetal decelerations during the labor, was encephalopathic, and rapidly developed seizures. Newborns with BN and total patterns had lower Apgar score at 5 minutes (P = .001) and more severe encephalopathy (P = .005). Newborns with cortical involvement (watershed and total) more frequently had seizures (P = .002). In addition, those with total injury were more likely to remain intubated on day 3 (P < .001). Among those with focal-multifocal injuries, seizures were recognized in 3 of 7 newborns with strokes and 3 of 11 with WMI. Other clinical variables were similar across patterns of brain injury (Table 1). In this cohort, only 6 newborns received systemic hypothermia as part of a concomitant randomized trial (Infant Cooling Evaluation (ICE) study). Of these, 3 had the BN pattern, whereas the other 3 had, respectively, normal, total, and focal-multifocal patterns. The 3 newborns with BN injury and the 1 with focal-multifocal injury had a repeat MRI scan in the second week of life, which demonstrated the same pattern of injury identified on the day 3 DW MRI.
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CT Compared With DW MRI
Agreement
Using the scale proposed by Landis and Koch26 for assessing agreement, there was good agreement for the predominant pattern of brain injury on CT and DW MRI (67% agreement;
= 0.56; Table 2) . Concordant results were observed in 32 of 48 paired studies. Comparing CT with DW-MRI agreement was noted in 13 of 16 infants with Normal DW MRI, 3 of 4 with the watershed pattern, 6 of 8 with the BN pattern, and 6 of 7 with the total pattern. There was only agreement in 4 of 13 cases of focal-multifocal injury on DW MRI. All 6 infants with concordant BN on CT and DW MRI had the pattern of injury confirmed on repeat MR studies between days 8 and10 of life.
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Disagreement by Pattern of Injury on DW MRI
Normal DW MRI
Three newborns with normal DW MRI were classified as having a watershed pattern on CT because of mild to moderate white matter abnormalities (Table 2). None of these newborns had a repeat MRI scan.
Watershed-Predominant Pattern on DW MRI
One newborn had the watershed pattern on DW MRI and a normal CT; a follow-up scan in this newborn on day of life 9 confirmed the watershed pattern.
BN-Predominant Pattern on DW MRI
Two newborns had the BN pattern on DW MRI yet had normal CT scans. Only 1 of these newborns had a day 10 MRI; the follow-up MRI in this newborn confirmed the BN pattern.
Total Pattern on DW MRI
One newborn was classified as total by DW MRI, but only BN by CT as more extensive cortical injury was evident on DW MRI. A day 10 MRI in this newborn confirmed a total pattern of injury with T1 shortening in both the BN and cortex.
Focal-Multifocal Injury on DW MRI
Most disagreements between CT and DW MRI involved the focal-multifocal pattern. Thirteen newborns had isolated focal or multifocal injuries on DW MRI: 8 with WMI, 3 with stroke, and 2 with WMI and stroke (Table 3). Furthermore, 3 other newborns had focal or multifocal abnormalities in combination with BN pattern. These 16 subjects had a total of 8 focal strokes in 7 subjects and 11 areas of focal or multifocal WMI. Five of these 8 strokes, ranging in size from 4 to 36 mm on DW MRI (mean size: 20 mm), were identified by CT. Two strokes were not recognized on initial CT scoring but were evident in retrospect, whereas 1 cortical lesion was not visible at all. All strokes recognized on CT measured >10 mm; the average size of the unrecognized strokes was 6 mm. WMI was focal (ie, 1 lesion per hemisphere) in 5 cases and multifocal in 6. None of the focal-multifocal WMIs were observed on CT.
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MRI Compared With DW MRI
Agreement
As shown in Table 4, agreement for the predominant pattern of injury for MRI versus DW MRI was excellent, seen in 37 of 48 infants (77% agreement;
= 0.70). MRI and DW MRI agreed in 12 of 16 newborns with normal DW MRI, 1 of 4 with the watershed pattern, 7 of 8 with the BN pattern, 6 of 7 with the total pattern, and 11 of 13 newborns with focal-multifocal injuries. In the 7 newborns with BN pattern on both MRI and DW MRI, the follow-up scan demonstrated the same extent of BN injury between day 3 DW MRI and day 10 MRI.
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Disagreement by Pattern of Injury on DW MRI
Normal DW MRI
Four newborns with normal DW MRI were classified as having a BN pattern on MRI (Table 2). Only 1 of them had a repeat MRI scan on day 9 of life that was normal.
Watershed-Predominant Pattern on DW MRI
Two newborns had the watershed pattern on DW MRI and the total pattern on MRI; follow-up scans on day of life 10 confirmed the watershed pattern in both infants. One newborn had the watershed pattern on DW MRI and a normal MRI; follow-up scan on day of life 9 confirmed the watershed pattern.
BN-Predominant Pattern on DW MRI
One newborn had the BN pattern on DW MRI and a normal MRI; this infant did not have a follow-up scan.
Total Pattern on DW MRI
One newborn had the total pattern on DW MRI and the BN pattern on MRI; follow-up scan on day of life 10 confirmed the total pattern.
Focal-Multifocal Injury on DW MRI
As outlined earlier, a total of 16 subjects had focal-multifocal injuries on DW MRI (Table 3): 8 focal-multifocal strokes in 7 subjects and 11 areas of focal-multifocal WMI. T1 changes were observed prospectively in 5 of 8 strokes and T2 changes in 4 of 8 strokes, whereas DW MRI and ADC maps were positive in all. T1 changes were observed in 10 of 11 WMI, but T2 changes were seen in only 4 of 11 infants. There was a single WMI case of a solitary 2-mm focus of T1 shortening that did not show a corresponding abnormality on DW-MRI or ADC maps.
Other Patterns of Injury
Seventeen newborns of this cohort had hypoglycemia during the first 3 days of life (median glucose: 1.8 mmol/L; interquartile: 0.9–2.2 mmol/L). The predominant pattern of injury in these newborns were as follows: 7 normal, 3 watershed, 3 BN, 2 total, and 2 focal-multifocal. Of these 17 newborns, 8 had a pattern of injury on CT that was concordant with hypoglycemia: the injury involved predominantly the pulvinar and the antero-medial nuclei of the thalamus or widespread areas of the white matter in the occipital lobes. This pattern of abnormality is distinct from the BN, watershed, and total patterns described earlier. Although this pattern was most commonly recognized on CT, it was noted in 4 of the 8 newborns on DW MRI and 6 newborns on MRI. Hypoglycemia was documented clinically in all 8 subjects. This pattern of abnormality occurred in 1 newborn with a normal DW-MRI scan, in 2 with coexisting BN pattern, in 3 with the watershed pattern, and in 2 with focal-multifocal injuries. As described earlier, 2 newborns had the total pattern on MRI but the watershed pattern on DW MRI. In retrospect, these 2 cases had abnormalities of the pulvinar and the antero-medial nuclei of the thalamus on the day 3 MRI that were no longer evident in the second week of life.
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Over the last decade, MRI has been shown to be of predictive value in NE.7,8,27 In the present study comparing CT, MRI, and DW MRI performed uniformly on day 3 of life, all 3 imaging modalities identify central injuries to the deep gray nuclei similarly. However, when looking at the entire brain, the overall agreement between the modalities is higher between DW MRI and MRI than between DW MRI and CT. This difference is largely because of cortical injuries, stroke, and WMI being more frequently seen on DW MRI and MRI (Fig 4). We found that cortical lesions and strokes of small dimensions may not be identified by CT. Furthermore, WMI may not be identified by CT, even if the injury is multifocal and widespread. When follow-up scans were available in the second week of life, the patterns of injury identified by DW MRI on day 3 were confirmed. This corroborates previous studies suggesting that DW MRI is most sensitive in identifying brain injuries at an early phase.15,19–22 In a recent prospective longitudinal diffusion tensor imaging study of brain injury in newborns with a defined timing of injury, average diffusivity values were found to reach nadir between days 2 and 4 after hypoxic-ischemic insult.28
Recent studies have found that the predominant pattern of brain injury has greater value for predicting neurodevelopmental outcome than the severity of injury in a given region.9,29,30 However, focal and multifocal lesions such as strokes are increasingly recognized to occur concomitantly with NE.18,31 In this study, the "focal-multifocal" category was created to assemble outlying cases that generally are included with the classically recognized patterns of brain injury in NE.5,29,32–34 More than one third of newborns in this cohort had focal or multifocal stroke or WMI. Despite the lack of data from term infants, the severity of noncystic WMI is a strong predictor of neurodevelopmental outcome in the premature newborn.14,35 Although the clinical significance of these relatively small lesions requires better definition, the recognition of this additional category may enhance our ability to define important subgroups of newborns with NE. Furthermore, the emergence of potential therapeutic interventions increases the importance of developing improved categorizations of risk.36
To our knowledge, this is the first study to directly compare the predominant pattern of brain injury identified by CT, MRI, and DW MRI in a homogeneous time frame. There is only 1 other published study that has addressed this issue by assessing the cross-modality and interobserver agreements between CT and MRI in a group of 48 newborns examined with both techniques.6 That study found that CT and MRI demonstrated similar brain abnormalities, but that interobserver agreement was significantly greater with MRI. However, that study differed from the present one in that it included also other clinical diagnoses and the comparison was categorized only as normal or abnormal. In addition, the entry criteria concerning the timing of scanning were less restrictive in that study: CT and MRI were performed within 72 hours of each other and at <2 weeks of age. Eight newborns of this cohort had a pattern of injury that conformed closely to that described in hypoglycemia.37–39 Hypoglycemia was documented clinically in all of these newborns. These newborns had predominant injury in the pulvinar and the antero-medial nuclei of the thalamus, rather than the ventrolateral thalamus and lentiform nuclei, or they had preferential involvement of the white matter in the parietal and occipital lobes, as opposed to the typical watershed pattern. This subset of newborns highlights the potential for hypoglycemic brain injury to coexist with hypoxic-ischemic brain injury, and suggests that the temporal evolution of these lesions may differ from that secondary to hypoxia-ischemia. Given its retrospective nature, our study was limited by the absence of systematic clinical follow-up and repeat brain imaging in all newborns. In particular, we were unable to address the potential for overdiagnosis with CT or MRI in relation to DWI findings as follow-up MRI scans were not available in the newborns with positive CT (n = 3) or MRI (n = 4) and normal DW MRI. Compared with other studies, our cohort has a different distribution of the frequency with which each of the predominant patterns was observed. Although the watershed-predominant pattern is the most common type of injury encountered by other studies, accounting for about one third of cases, only 4 newborns in our cohort showed that pattern of injury.9,29 This finding is surprising and may be explained, in part, by the severity of encephalopathy that prompted clinical imaging. Because scans were ordered clinically, our cohort may underrepresent newborns with the watershed-predominant pattern, because these newborns may have milder encephalopathy than those with the BN or total patterns.14 However, if that were the only explanation, one might not have expected that a substantial proportion of the infants enrolled in this study would have normal scans or only focal and multifocal brain injuries, as was the case. We note that this cohort originates from the provincial referral center for high-risk obstetric care and neonatal intensive care. It is possible that in this demographic situation, cases of acute profound asphyxia are proportionally overrepresented.
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CONCLUSIONS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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In evaluating newborns with NE on the third day of life, DW MRI more readily detects cortical injury and focal or multifocal lesions (strokes and WMI) and is thus the most sensitive imaging modality at this early time. However, in situations where this technology may not be available, or the critical condition of the newborn precludes safe transport to the MR scanner, CT with proper calibration may be used on the third day of life to accurately detect the most serious patterns of brain injury. The risk of transport and sedation for MRI and DW MRI should be balanced against the risk of ionizing radiation.40–45 However, with the development of MR-compatible neonatal incubators for transportation and monitoring of newborns the capacity to image critically ill infants has improved.46,47 Additional improvements in imaging speed may also be realized with novel fast MR sequences and 3 Tesla scanner technology.48–50
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ACKNOWLEDGMENTS |
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Dr Chau is supported by the Bourse McLaughlin de l'Université Laval and the Fondation pour la recherche sur les maladies infantiles. Dr Miller is a Canadian Institutes for Health Research (CIHR) Clinician Scientist and Michael Smith Foundation for Health Research) Scholar. This work was supported in part by SickKids Foundation and Institute of Human Development, Child and Youth Health-CIHR National Grants Program.
We are grateful to Dr Donna Ferriero for critical review of the manuscript.
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FOOTNOTES |
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Accepted Apr 22, 2008.
Address correspondence to Steven Paul Miller, MAS, MDCM, FRCPC, British Columbia Children's Hospital, Division of Neurology, K3-180, 4480 Oak St, Vancouver, British Columbia, Canada V6H 3V4. E-mail: smiller6{at}cw.bc.ca
The authors have indicated they have no financial relationships relevant to this article to disclose.
| What's Known on This Subject NE is a common condition with high morbidity. Neuroimaging is important in the management of this condition. Despite current guidelines for choosing the proper neuroimaging test in newborns with encephalopathy, CT and MRI are used variably in clinical practice.
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| What This Study Adds Comparing the patterns of brain injury on CT, MRI, and DW MRI in term newborns with encephalopathy scanned uniformly with these modalities on the third day of life, we determined the strengths and limitations of these tests for clinical practice.
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