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. 2024 May 23;14(1):11827.
doi: 10.1038/s41598-024-60968-w.

Transfontanellar shear wave elastography of the neonatal brain for quantitative evaluation of white matter damage

Flora Faure #  1 , Marianne Alison #  2 , Mariantonietta Francavilla  3 , Priscilla Boizeau  4 , Sophie Guilmin Crepon  4 , Chung Lim  2 , Gregory Planchette  2 , Mickael Prigent  2 , Alice Frérot  5 , Mickael Tanter  1 , Charlie Demené  1 , Olivier Baud  6 , Valérie Biran  7   8
Affiliations

Transfontanellar shear wave elastography of the neonatal brain for quantitative evaluation of white matter damage

Flora Faure et al. Sci Rep. .

Abstract

Cerebral white matter damage (WMD) is the most frequent brain lesion observed in infants surviving premature birth. Qualitative B-mode cranial ultrasound (cUS) is widely used to assess brain integrity at bedside. Its limitations include lower discriminatory power to predict long-term outcomes compared to magnetic resonance imaging (MRI). Shear wave elastography (SWE), a promising ultrasound imaging modality, might improve this limitation by detecting quantitative differences in tissue stiffness. The study enrolled 90 neonates (52% female, mean gestational age = 30.1 ± 4.5 weeks), including 78 preterm and 12 term controls. Preterm neonates underwent B-mode and SWE assessments in frontal white matter (WM), parietal WM, and thalami on day of life (DOL) 3, DOL8, DOL21, 40 weeks, and MRI at term equivalent age (TEA). Term infants were assessed on DOL3 only. Our data revealed that brain stiffness increased with gestational age in preterm infants but remained lower at TEA compared to the control group. In the frontal WM, elasticity values were lower in preterm infants with WMD detected on B-mode or MRI at TEA and show a good predictive value at DOL3. Thus, brain stiffness measurement using SWE could be a useful screening method for early identification of preterm infants at high WMD risk.Registration numbers: EudraCT number ID-RCB: 2012-A01530-43, ClinicalTrial.gov number NCT02042716.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Patient flow diagram Abbreviations: ELGAN extremely low gestational neonate; VLGAN very low gestational neonate; DOL day of life; TEA term equivalent age.
Figure 2
Figure 2
Inter- and intra-operators reproducibility. (a) Intra-operator reproducibility: for each operator and regions, the mean concordance correlation coefficient (CCC) was calculated over all available measurements. The green points represent the mean Concordance correlation coefficient (CCC) and the green bars represent the 95% confidence interval. (b) Inter-operator reproducibility: Bland Altman plot based on elasticity measurements performed by two operators on 10 neonates (randomly selected). The red line represents the bias or the mean difference between operators and the dotted lines represent the 95% confidence interval. (c) Values of bias, standard deviation and CCC for each brain regions. FWM = Frontal white matter; PWM = Parietal white matter; Thal = Thalamus.
Figure 3
Figure 3
Evolution of the difference of the elasticity of brain regions between preterm and term neonates. (a–c) Frontal white matter (a), parietal white matter (b) and thalamus (c) elasticity values in preterm infants according to gestational age at birth (240/7–276/7 and 280/7–316/7 weeks) at each measurement time (DOL 3, DOL 8, DOL 21, TEA) compared to the control term newborn group (390/7–406/7 weeks) at DOL3. Blue stars represent significant differences with the term group (ANOVA), red stars represent significant differences between the two groups of preterm (ANOVA: ***p < 0.001, **p < 0.01, *p < 0.05). DOL day of life; TEA term equivalent age. (d–f) Linear model regression (red line) of Elasticity vs Gestational age in each brain regions for preterm neonates. For all regions, p < 0.001.
Figure 4
Figure 4
B-mode cranial ultrasound (cUS) images with overlaid shear wave elastography (SWE) measurements at DOL 3 in the right frontal white matter for two patients. B-mode cUS images are shown in grayscale and with overlaid SWE measurements in color-coded map for (a) Patient 1 with normal echogenicity on B-mode cUS image and (b) Patient 2 with abnormal echogenicity on the B-mode cUS image. The information in the Q-box is the summary of the SWE measurements. The corresponding mean elasticity values show that the elasticity is lower in the frontal white matter of Patient 2 with detected abnormal echogenicity (6.8 ± 2.7 kPa) compared to Patient 1 with normal echogenicity (12.1 ± 1.5 kPa).
Figure 5
Figure 5
Comparison of white matter elasticity values measured on days 3, 8, 21 according to B-mode cUS abnormalities. (a) Elasticity in the left (L) and right (R) frontal white matter (**, p < 0.01). (b) Elasticity in the left (L) and right (R) parietal white matter. n represents the number of considered hemispheres as each patient contributes two times, one for each hemisphere) DOL: day of life.
Figure 6
Figure 6
White matter elasticity comparison based on MRI classification (a) Comparison between elasticity values measured in the frontal white matter on day of life (DOL) 3, 8, 21 in preterm infants according to MRI scoring (normal vs abnormal) at term equivalent age (TEA) (n represents the number of considered hemispheres as each patient contributes two times, one for each hemisphere; **p < 0.01). (b) Receiver operating characteristic (ROC) curve analysis for frontal white matter lesion prediction based on elasticity values of the frontal white matter at DOL 3: (AUC of 0.89, max Youden index: sensitivity 100% and specificity 72% for a threshold of 8.4 kPa). (c) Linear regression of elasticity of frontal white matter on DOL 3 vs frontal apparent diffusion coefficient (ADC) from MRI at TEA in preterm infants. (d) Comparison between elasticity values measured in the parietal white matter on DOL 3, 8, 21 in preterm infants according to MRI scoring (normal vs abnormal) at TEA (n represents the number of considered hemispheres as each patient contributes two times, one for each hemisphere).
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