Open Access

Early identification of hypoxic‑ischemic encephalopathy by combination of magnetic resonance (MR) imaging and proton MR spectroscopy

  • Authors:
    • Lili Guo
    • Dehang Wang
    • Genji Bo
    • Hui Zhang
    • Weijing Tao
    • Ying Shi
  • View Affiliations

  • Published online on: September 21, 2016     https://doi.org/10.3892/etm.2016.3740
  • Pages: 2835-2842
  • Copyright: © Guo et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Brain damage following a perinatal hypoxic‑ischemic encephalopathy (HIE) can be diagnosed by different techniques. The aim of the present study was to combine magnetic resonance (MR) imaging with proton MR spectroscopy in HIE diagnosis and to evaluate their correlation with outcome. A prospective observational cohort study was performed between February 2012 and February 2013. Consecutive newborns, 24 full‑term neonates with HIE (mild to moderate and severe group) and 5 normal neonates, were included. Two sequential MR studies were performed; a conventional MR imaging for observation in T1 weighted image (WI) and T2WI, and proton MR spectroscopy for observation in the left or right basal ganglia and thalamus. MR images were assessed and scored by two neuroradiologists who were blinded to the clinical condition of the infants. The mild to moderate group (n=13) and severe group (n=11) were similar in the visualization of punctate hyperintensity lesions on T1WI and brain edema on T2WI. The differences of N‑acetylaspartate/creatine (Cr), choline/Cr and lactate/Cr in the basal ganglia and thalamus in the HIE group were significantly different (P<0.05) compared with the control group, while no significant difference was identified between the mild to moderate and severe group (P>0.05). In conclusion, MR spectroscopy is a complementary tool for the diagnosis of HIE.

Introduction

Hypoxic-ischemic encephalopathy (HIE), secondary to perinatal asphyxia, is a primary cause of pediatric mortality and morbidity, and results in neurologic outcomes, such as cerebral palsy, mental retardation and epilepsy (1). Timely prognostic information is important in counseling parents and in determining the appropriate level of treatment. Consequently, reliable early examinations are urgently required. During the last decade, advances have been achieved in the field of diagnosis and prognosis of HIE (2).

Clinicians use prognostic tests, including magnetic resonance (MR) imaging (MRI), to help determine the prognosis and decide whether to consider treatment withdrawal. It is understood that MRI serves an increasing important role for imaging the neonatal brain (36). However, proton MR spectroscopy has been developed for clinical use. This allows real-time analyses of the metabolites in the human brain. It has been widely reported that the potential utility of proton MR spectroscopy could reveal brain ischemic injuries in asphyxiated neonates earlier than T1- or T2-weighted MR imaging (711). Whether MR spectroscopy prior to conventional MR imaging should be used in the early diagnosis of neonate with HIE remains unknown. How to select the imaging technique between the two methods in different conditions? Therefore, the aim of the present study was to evaluate the value of MR spectroscopy and MR imaging for the diagnosis of HIE.

Subjects and methods

Subject selection

The protocol was approved by the review board of Nanjing Medical University (Nanjing, China). Participants in the study were voluntary; the study was performed after obtaining informed consent from the infants' parents. In this study, 24 full term infants (17 males, 7 females; age range,0–15 days) with HIE were collected from the Department of Pediatrics in Huai'an First People's Hospital Affiliated to Nanjing Medical University (Huai'an, China) between February 2012 and February 2013. All of the cases had perinatal asphyxia, and were defined as having at least three of the following criteria (12): i) Fetal heart rate abnormalities; ii) meconium staining of amniotic fluid; iii) delayed onset of respiration; iv) early postnatal blood pH level <7.1; v) Apgar score at 5 min of <5; or vi) multiorgan failure. Furthermore, all neonates had signs of neonatal encephalopathy (13).

Neonates with congenital malformation, trauma, metabolic or infective diseases, and patients born prior to reaching a 36-week gestational age, were excluded from this study. Five healthy term infants (3 males, 2 females; age range, 0–15 days) were recruited in the control group. The patients underwent MRI examination for scalp hematoma or slight neonatal jaundice.

MRI examinations

During the MRI procedures, all neonates were sedated with chloral hydrate 10 mg/kg (Sigma-Aldrich, St. Louis, MO, USA) orally, or rectally as a suppository. Vacuum pillows were used to prevent patients movement during MR examinations. Ear protection to noise exposure was provided by using neonatal ear muffs. A pediatrician was present throughout the investigation. The neonates were monitored by MR-compatible pulse oximetry during the examination procedure. For those neonates with severe encephalopathy who were in a coma or who were ventilator-dependent, hand-bag ventilator equipment was used.

All images in these series were obtained with superconducting magnets (MAGNETOM Avanto; Siemens Healthcare GmbH, Erlangen, Germany) operating at a field-strength of 1.5T magnet. All infants were in the axial plane. The total duration of the examination is 8 min.

Conventional MRI methods

MRI protocols included 4.0 mm transverse and sagittal T1-weighted spin-echo sequences [repetition time (TR)/echo time (TE), 468/11 and 400/8.1 ms, respectively]; 4.0 mm transverse T2-weighted fast spin-echo sequence (TR/TE, 4000/101 ms); and an echo-planar imaging technique was used for diffusion weighted imaging (DWI; repetition time msec/echo time msec = 3300/93), with a 180×180 mm field of view, 4.0 mm section thickness and b values of 0 and 1,000 sec/mm2.

Proton MR spectroscopy methods

MR spectroscopy was performed similarly to the routine MR protocol. Spectra were acquired by using a single-voxel technique to select a single volume of interest (voxel dimensions, 10 mm3, 1 ml) in the left or right basal ganglia and thalamus, as reported previously. The basal ganglia and thalamus are most sensitive to the effects of acute anoxia (14). This single voxel can reflect the global disturbances, such as cortical gray matter and the frontal and occipital white matter. Placement was performed carefully to avoid contact with cerebral spinal fluid.

The parameters of single-voxel MR spectroscopy were as follows: TR, 1,500 ms; TE, 35 ms; 128 signals acquired; and 8NEX. Water suppression was achieved by applying chemical shift selective saturation pulses. Metabolites of biologic importance, such as N-acetylaspartate (NAA), creatine (Cr), and choline (Cho) peaks were identified at 2.02, 3.02 and 3.24 ppm, respectively. When present, lactate (Lac) was identified as a doublet at 1.33 ppm.

Automated curve was performed on an MRI operator console by using proprietary software (Siemens Healthcare GmbH). Manual phase adjustment was applied if necessary. In all cases, peak surface area was used to calculate metabolite ratios for metabolite quantification. As for Lac, the combined area under the doublet was used for calculations.

Conventional MRI

The MR images obtained in all neonates were analyzed independently by a senior radiologist (Dr. Dehang Wang) who was experienced in neonatal neuroimaging, blinded to the clinical outcomes and MR spectroscopy information, and who analyzed the images according to MRI scores (15). This score (range, 0–22; Table I) was generated according to a report on MRI and DWI abnormalities in neonates with HIE (16). The following predefined structures were analyzed: Basal ganglia regions (including thalamus); cerebral cortex; periventricular and subcortical white matter; corpus callosum; and brainstem. For each structure, any MR signal intensity abnormality irrelevant to injury was documented as a high-signal intensity (SI) lesion on T1 weighted image (WI).

Table I.

Magnetic resonance imaging score criteria.

Table I.

Magnetic resonance imaging score criteria.

CategoryScore criteria
ABrain swelling: 0, Not present; 2, present
BGrey/white matter differentiation: 0, Present; 1, absent in one localization; 2, absent in more than one localization
CHigh signal in the posterior limb of the internal capsule on T1WI: 0, Normal; 1, mild decrease; 2, absent
DHyperintensity on T1WI sequences on PP and T: 0, None; 1, one localization; 2, more than one localization
EHyperintensity on T2 sequences on PP and T: 0, None; 1, one localization; 2, more than one localization
FBrain stem abnormalities on T1WI and/or T2WI sequences: 0, None; 1, present
GCortex abnormalities on T1 and/or T2 sequences: 0, None; 1, one localization; 2, more than one localization
HWhite matter petechial abnormalities: 0, None; 1, one localization; 2, more than one localization
ISubarachnoid hemorrhages: 0, None; 1, present
JWhite-matter abnormalities in DWI: 0, None; 1, one localization; 2, more than one localization
KBasal ganglia abnormalities in DWI: 0, None; 1, one localization; 2, more than one localization
LCerebral cortex abnormalities in DWI: 0, None; 1, one localization; 2, more than one localization

[i] T1WI, T1 weighted image; T2WI, T2 weighted image; DWI, diffusion weighted imaging; PP, putamen and pallidum; T, thalamus.

MR spectroscopy quantifications

The spectra was reviewed by an MR specialist (Dr. Genji Bo) who had 10 years of experience in interpreting brain MR spectroscopy and who was blinded to the clinical outcomes and the MR images. All 1H-MR spectroscopic data were included in the analysis (n=29) and all findings were pooled. Cr was used as a reference to measure the ratios of NAA/Cr, Cho/Cr and Lac/Cr. These ratios were compared in the 29 neonates to select a perspective indicator of the neonates with HIE.

Statistical analysis

Data obtained were expressed as the mean ± standard deviation, and all data were analyzed using SPSS version 15.0 statistical software (SPSS, Inc., Chicago, IL, USA). P<0.05 were considered to indicate a statistically significant difference. The comparison between the control and HIE group was performed by a two-tailed t-test. The paired comparisons among the control group and each HIE group were performed by two-way analysis of variance and the Student-Newman-Keuls method.

Results

Clinical characteristics

The neurologic examinations were routinely performed by the pediatricians in charge of the neonates. Knowledge of the outcomes, including seizures, sensory impairment and encephalodysplasia, were collected from the medical records by these pediatricians.

Two cases with severe HIE succumbed to irreversible cerebral injury and withdrawal of the life-sustaining treatments. The decision to withdraw treatment was based on the combination results of clinical examination, cerebral MRI, 1H-MR spectroscopy and electroencephalography, as reported previously (17). The remaining cases received suitable HIE treatment. The average number of days spent in hospital were as follows: Mild to moderate group, 11.5 days (range, 6–18 days); severe group, 19.6 days (range, 8–25 days). Four cases of severe HIE neonates still had weak nerve reaction upon discharge from the hospital. The neurological system symptoms of the remaining participants disappeared prior to leaving the hospital. No abnormal nervous system signs were detected in the control group.

Neonatal HIE severity was graded clinically according to Sarnat-Sarnat classification (18). The general condition of the HIE neonates were as follows (Table II): Mild to moderate (stages I–II), 13 cases; severe (stage III), 11 cases.

Table II.

Clinical data and magnetic resonance findings of all participants in the study.

Table II.

Clinical data and magnetic resonance findings of all participants in the study.

Case no.GenderAge (days)Number of PWMLSignal on DWI (reduced diffusion)Body weight (g)Outcome
  1M34Yes3350Minor or moderate abnormalities
  2M713Yes3000Minor or moderate abnormalities
  3M10No3630No abnormalities
  4F30No3070No abnormalities
  5M150No3040No abnormalities
  6M56Yes4000Minor or moderate abnormalities
  7M108No3620Minor or moderate abnormalities
  8M235Yes2380Mortality on day 6
  9F313Yes3760Severe abnormalities
10F18Yes3510Minor or moderate abnormalities
11M31Yes2800No abnormalities
12M11Yes3710No abnormalities
13M312Yes3560Minor or moderate abnormalities
14F56Yes3450No abnormalities
15M10Yes2565No abnormalities
16M122Yes2570Minor or moderate abnormalities
17F1120Yes2850Severe abnormalities
18F1114Yes2560Severe abnormalities
19M82Yes4480No abnormalities
20F40Yes3100No abnormalities
21M124Yes3000Severe abnormalities
22F559Yes2050Mortality on day 12
23M81Yes3570No abnormalities
24M151No3450No abnormalities
25M31Yes2860No abnormalities
26M611Yes3600Minor or moderate abnormalities
27M105Yes4000Minor or moderate abnormalities
28F31Yes2850No abnormalities
29M213Yes3600Minor or moderate abnormalities

[i] PWML, punctate white matter lesions; DWI, diffusion weighted image; M, male; F, female.

MR imaging data

According to the MRI data, abnormal imaging was not identified in the control group. Four types of images in HIE groups were observed. Cerebral hyperintensity lesions (according to the site of lesions, two subtypes could be detected), cortex and/or watershed area lesions (Fig. 1) and periventricular white matter lesions (Fig. 2) were detected. These characteristic abnormalities were visible as early as the first day of life. However, these lesions identified by punctuate hypersignal on T1WI and hyposignal on T2WI were assumed to be petechial hemorrhage, gliotic scarring, scarring or mineralization, which are impossible to distinguish on T1- and T2WI (19,20). Longitudinal imaging showed a decrease in the number of punctate white matter lesions (PWML) over time, without hypersignal of PWML on T1WI, suggesting hemorrhage; a number of PWML did not change hypersignal on T1WI, suggesting early gliosis (21). In addition, basal ganglia, thalamic, corpus callosum or mesencephalic injury (Fig. 3) was identified on conventional and diffusion-weighted MR images. Furthermore, subarachnoid haemorrhage, in which short T1 high signal was manifested in the posterior sagittal sinus, horizontal sinus, cerebellar tentorium or confluence of sinus (Fig. 4), was detected. Finally, intraventricular haemorrhage (Fig. 5) could be observed.

Compared with the images of the two HIE groups, punctate hyperintensity lesions on T1WI in the cortex or subcortical white matter and brain edema on T2WI were visually similar. Abnormal SI of the thalamus, corpus callosum or brain stem on conventional and diffusion-weighted MR images were significantly different in the severe group (P=0.001). Abnormal SI within the basal ganglia and thalami may predict the severity outcome.

Unilateral parenchymal hemorrhage was identified in four infants in the HIE group. The mean number of PWML in the mild to moderate group (stages I–II) was 5.38±4.68 (range, 1–13). The mean number of PWML in the severe group (stage III) was 16.82±17.66 (range, 4–59). A significant difference was identified between these two groups in regard to the number of PWML (P=0.035). The majority of PWML were identified close to the medullary veins and showed restricted diffusion on early MRI; two infants did not have restricted diffusion on early MRI (identified as hyposignal on DWI).

The neonatal MR score was obtained from the scan images. Points were awarded for the presence of brain swelling and abnormal SI within the cortex, subcortical and periventricular white matter, basal ganglia and thalamus, brain stem, and from the posterior limb of the internal capsule. The MR scores (Table III) of the two HIE groups were compared. The mean MR imaging score was 6.20±1.75 for cases of stage I–II and 9.78±3.64 for cases of stage III. There was a significant difference between the two groups (P=0.009).

Table III.

Magnetic resonance scores for all participants.

Table III.

Magnetic resonance scores for all participants.

Category

Case no.ABCDEFGHIJKLScoreStage
  120200002120091–2
  220200002020081–2
  300000000000000
  400000000000000
  500000000000000
  600100002120053
  700200002000041–2
  8202000020220103
  9221000220222153
1000200002020061–2
1120200001110071–2
1221200001010061–2
13222021020220153
14202000221202133
1500000000000000
1600100002020051–2
1720200002020083
1800000022120293
1920200001010041–2
2000000000000000
21202000221222153
2220000012020183
23222000111101113
2422200001110093
2500100001010031–2
2620100002020071–2
2721000002100061–2
2822200001010081–2
2920200002020081–2

MR spectroscopy. In the control and HIE groups, the peaks of metabolites of biologic importance, such as NAA (2.02 ppm), Cr (3.02 ppm) and Cho (3.24 ppm), were identified. The Cr was used as a reference to measure NAA/Cr, Cho/Cr and Lac/Cr ratios (Table IV). In the control group, the values of NAA/Cr and Cho/Cr were 1.60±0.47 and 1.67±0.81, respectively, while Lac/Cr was not detected. In the HIE groups, Lac was identified as a doublet at 1.33 ppm, and the values of NAA/Cr, Cho/Cr and Lac/Cr were 1.09±0.4, 2.12±0.87 and 0.14±0.26, respectively. In the mild to moderate group (stages I–II), the ratios showed NAA/Cr of 1.23±0.35, Cho/Cr of 1.84±0.37 and Lac/Cr of 0.03±0.06. In the severe group (stage III), the ratios showed NAA/Cr of 0.97±0.41, Cho/Cr of 2.43±1.16 and Lac/Cr of 0.26±0.34.

Table IV.

Quantitative analyses of the metabolic compounds used in the study.

Table IV.

Quantitative analyses of the metabolic compounds used in the study.

GroupsNumberNAA/CrCho/CrLac/Cr
Control  51.60±0.471.67±0.81
HIE241.09±0.412.12±0.870.14±0.26
Mild to moderate131.23±0.351.84±0.370.03±0.06
Severe110.97±0.412.43±1.160.26±0.34

[i] Data was expressed as the mean ± standard deviation. HIE, hypoxic-ischemic encephalopathy; NAA, N-acetylaspartate; Cr, creatinine; Cho, choline; Lac, lactate.

Between control and HIE groups, the differences of NAA/Cr, Cho/Cr and Lac/Cr in the basal ganglia and thalamus were statistically significant (P<0.05). Multiple comparisons were performed among control and HIE groups (Table V). The differences of NAA/Cr, Cho/Cr and Lac/Cr between the control and mild to moderate groups, and control and severe groups, were statistically significant (P<0.05). The differences of NAA/Cr, Cho/Cr and Lac/Cr between mild to moderate and severe groups was not statistically significant (P>0.05).

Table V.

Comparison of magnetic resonance spectroscopy metabolites between control and HIE groups.

Table V.

Comparison of magnetic resonance spectroscopy metabolites between control and HIE groups.

GroupsNAA/Cr PCho/Cr PLac/Cr P
Control vs. HIE0.0150.0290.020
Control vs. Mild to moderate0.0160.0400.048
Control vs. severe0.0100.0100.050
Mild to moderate vs. severe0.1710.1380.380

[i] The t-test was used to compare the quantity of the metabolic compounds among the control and HIE groups. P<0.05 was considered to indicate a statistically significant difference. HIE, hypoxic-ischemic encephalopathy; NAA, N-acetylaspartate; Cr, creatinine; Cho, choline; Lac, lactate; P, P-values.

Discussion

MR imaging technology, which is thought to show brain morphology at a high resolution in the clinic, has been developed rapidly in the past decades. It is superior to cerebral CT and ultrasound examination in displaying lesions in the basal ganglia or deep white matter, and multi-cystic encephalomalacia around the ventricle (22).

T1WI could provide essential information for the diagnosis and depicting typical MRI features of hypoxic-ischemic injury (3,56). The imaging pattern of HIE has been classified into three types (4,23); parasagittal lesions, involving cortico-subcortical regions, profound lesions located in the basal ganglia or thalamus, and multi-cystic encephalomalacia. Parasagittal lesions are typically associated with milder HIE (24). In the present study, the T1 images in the mild to moderate (n=13) and severe group (n=11) were similar, with punctate hyperintensity in the cortex or subcortical white matter (P>0.05). Profound lesions in the basal ganglia and thalamus are often associated with serious HIE (25). The results in the present study showed unequivocally that lesions in the basal ganglia and thalamus were associated with the severe group. Finally, multi-cystic encephalomalacia are typically connected with an end-stage finding of severe HIE. Multiple cysts in the brain were not detected in the current study.

Previously, a meta-analysis (14) reported the prognostic utilities of various quantitative cerebral MR biomarkers in neonatal encephalopathy. Thirty-two studies were included that were performed between January 1990 and July 2008. Regarding predicting adverse outcome, T1WIs during the first 30 days had a pooled sensitivity of 91% (95% confidence interval [CI], 87–94%). The pattern of injury identified with T1WI may provide diagnostic and prognostic information for neonatal encephalopathy (20,14). Infants who show abnormal SI in the basal ganglia/thalami typically undergo an adverse outcome (1226). The changes in routine T1WIs are characteristic, but a question is put forward as to whether MRS biomarkers may be available in T1WI in the evaluation of infants.

MRS is a non-invasive technique that allows real-time analysis of metabolites in the human brain (27). Cho is a marker for membrane synthesis and Cr (3.0 ppm) is chosen as the reference because of its stability. Due to the rapid growth of the membranes in the neonatal brain, the NAA (2.01 ppm) level is much lower than Cho (3.02 ppm) (28). Reportedly, Lac (1.33 ppm) is not present in great quantities in normal neonates and is rarely detected by MRS (11). In the present study, Lac in the control group was not observed.

The ascent of Lac/Cr, presumably because of energy failure and the necessity to metabolize glucose anaerobically, was not marked as elucidated by Hanrahan et al (12), in contrast to the results of the present study. It seems likely that this difference of results is related to the time of the MRS examination with respect to the hypoxic-ischemic event. The mean time from injury to MRS in patients in the current study was 7 days; for patients in Hanrahan et al (12), the mean time was <24 h. The precise time at which lactate levels become lower after hypoxic-ischemic injury in neonates is unknown. Indeed, in the study by Xu and Vigneron (29), although the presence of lactate persisted, the Lac level always dropped on follow-up spectra performed weeks after the injury. Hence, it can be suggested that the Lac level would have been higher if the patients had been studied earlier following perinatal hypoxic-ischaemic injury in the present study. The results in the present study were consistent with those of Barkovich et al (30) and Alderliesten et al (31), who found associations with NAA levels in HIE. Similarly, the patients in the study by Barkovich et al (30) experienced injury within an average of 7 days prior to MRS and those of Alderliesten et al (31) experienced a hypoxic-ischemic event at an average of 6 days. Surprisingly, no statistically significant differences in NAA/Cr and Lac/Cr were identified between the mild to moderate and severe group. In comparison with MR performances, results of proton MRS had a number of limitations in distinguishing mild from moderate to severe injury.

In conclusion, 1H-MRS is a useful technique for distinguishing between HIE and normal newborns; however, with regard to differentiating between grades, 1H-MRS should be interpreted in conjunction with performances on T1WI.

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November-2016
Volume 12 Issue 5

Print ISSN: 1792-0981
Online ISSN:1792-1015

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Copy and paste a formatted citation
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Spandidos Publications style
Guo L, Wang D, Bo G, Zhang H, Tao W and Shi Y: Early identification of hypoxic‑ischemic encephalopathy by combination of magnetic resonance (MR) imaging and proton MR spectroscopy. Exp Ther Med 12: 2835-2842, 2016
APA
Guo, L., Wang, D., Bo, G., Zhang, H., Tao, W., & Shi, Y. (2016). Early identification of hypoxic‑ischemic encephalopathy by combination of magnetic resonance (MR) imaging and proton MR spectroscopy. Experimental and Therapeutic Medicine, 12, 2835-2842. https://doi.org/10.3892/etm.2016.3740
MLA
Guo, L., Wang, D., Bo, G., Zhang, H., Tao, W., Shi, Y."Early identification of hypoxic‑ischemic encephalopathy by combination of magnetic resonance (MR) imaging and proton MR spectroscopy". Experimental and Therapeutic Medicine 12.5 (2016): 2835-2842.
Chicago
Guo, L., Wang, D., Bo, G., Zhang, H., Tao, W., Shi, Y."Early identification of hypoxic‑ischemic encephalopathy by combination of magnetic resonance (MR) imaging and proton MR spectroscopy". Experimental and Therapeutic Medicine 12, no. 5 (2016): 2835-2842. https://doi.org/10.3892/etm.2016.3740