Transtemporal brain contrast-enhanced ultrasound in children: preliminary experience in patients without neurological disorders

Luis Octavio Tierradentro-García, Anush Sridharan, Misun Hwang, Luis Octavio Tierradentro-García, Anush Sridharan, Misun Hwang

Abstract

Aim: To evaluate the use of transtemporal brain contrast-enhanced ultrasound (CEUS) to assess cerebral blood perfusion in a cohort of children without neurological disorders.

Methods: We included pediatric patients who were undergoing a clinically-indicated CEUS study. Brain scans were performed with a Siemens Sequoia scanner and a 4V1 transducer, that was placed on the left transtemporal bone. Brain scans were performed simultaneously with the images of the clinically-indicated organ of interest. Qualitative and quantitative analysis was performed to evaluate the hemispherical blood flow at the level of the midbrain during the wash-in and wash-out phases of the time-intensity curve. Clinical charts were reviewed to evaluate post-CEUS adverse events.

Results: Five patients were evaluated (mean age 5.8 ± 5.1 years). Qualitatively, more avid enhancement in the midbrain than the cortex was observed. Structures depicted ranged between the centrum semiovale at the level of the lateral ventricles and the midbrain. A quantitative analysis conducted on four patients demonstrated less avid perfusion on the contralateral (i.e. right) side, with a mean left/right ratio ranging between 1.51 and 4.07. In general, there was a steep positive wash-in slope starting at approximately 10 s after contrast injection, reaching a peak intensity around 15-26 s on the left side, and 17-29 s on the right side. No adverse events were reported.

Conclusion: Transtemporal brain CEUS is feasible and safe in the pediatric population and allows qualitative and quantitative assessment of cerebral perfusion.

Keywords: Brain ultrasound; Contrast-enhanced ultrasound; Normal population; Transtemporal ultrasound.

Conflict of interest statement

Grants from: NIH R01, Bracco, Children’s Hospital of Philadelphia, University of Pennsylvania. Lecture honorarium from the Korean Society of Ultrasound in Medicine. Vice Chair, Society of Pediatric Radiology (SPR) Neonatal Imaging Committee. Equipment/material from: Bracco, Siemens (Misun Hwang). The other coathors declare no conflicts of interest.

© 2022. Società Italiana di Ultrasonologia in Medicina e Biologia (SIUMB).

Figures

Fig. 1
Fig. 1
Determination of regions of interest (ROIs) for quantitative analysis in transtemporal brain contrast-enhanced ultrasound at the level of the midbrain. On the left side, an image in the axial plane shows contrast enhancement in the left hemisphere (upper ROI) and the right hemisphere (lower ROI). On the right, a grayscale image in the axial view is presented for confirmation of anatomical structures
Fig. 2
Fig. 2
Range of visualization of structures in the axial plane. A 1.5-year-old boy underwent transtemporal brain contrast-enhanced ultrasound in the axial plane; the transducer was placed over the squamous portion of the temporal bone and swept up and down. The following structures were visualized: a centrum semiovale (arrows), b thalami (arrows), c midbrain (arrows) at the level of the circle of Willis (dotted arrows), and d lower midbrain (arrows)
Fig. 3
Fig. 3
Temporal evolution of parenchymal enhancement using transtemporal brain contrast-enhanced ultrasound (CEUS). A 2-year-old boy underwent transtemporal brain CEUS. Images during the wash-in phase were acquired at the level of the midbrain in the axial plane at a 10 s, b 14 s, c 18 s, d 22 s, e 26 s, and f 30 s after contrast injection
Fig. 4
Fig. 4
Time-intensity curves and hemisphere differences in contrast enhancement. ad Intensity in the left hemisphere was consistently higher than in the right during the wash-in and early wash-out phases. au arbitrary units
Fig. 5
Fig. 5
Left/right (LR) hemisphere enhancement ratio across ages. Note that the LR ratio in Patient C was markedly different from the other patients. This may be due to the skull thickness and/or hair
Fig. 6
Fig. 6
Comparison of regions of interest at peak enhancement. a A 1.5-year-old boy versus b a 13-year-old boy. Note that the contralateral hemisphere is more obscured in the older patient due to technical factors rather than perfussion differences. This explains the marked differences in left/right ratios as represented in the time-intensity curves

References

    1. Hwang M, Tierradentro-García LO, Hussaini SH, Cajigas-Loyola SC, Kaplan SL, Otero HJ, et al. Ultrasound imaging of preterm brain injury: fundamentals and updates. Pediatr Radiol. 2022;52:817–836. doi: 10.1007/s00247-021-05191-9.
    1. Vitale V, Rossi E, Di Serafino M, Minelli R, Acampora C, Iacobellis F, et al. Pediatric encephalic ultrasonography: the essentials. J Ultrasound. 2018 doi: 10.1007/s40477-018-0349-7.
    1. Piskunowicz M, Sridharan A, Poznick L, Silvestro E, Hwang M. Optimization of mechanical indices for clinical contrast-enhanced ultrasound. J Ultrasound Med. 2021;40:1963–1970. doi: 10.1002/jum.15578.
    1. Hwang M, Barnewolt CE, Jüngert J, Prada F, Sridharan A, Didier RA. Contrast-enhanced ultrasound of the pediatric brain. Pediatr Radiol. 2021;51:2270–2283. doi: 10.1007/s00247-021-04974-4.
    1. Squires JH, Beluk NH, Lee VK, Yanowitz TD, Gumus S, Subramanian S, et al. Feasibility and safety of contrast-enhanced ultrasound of the neonatal brain: a prospective study using MRI as the reference standard. AJR Am J Roentgenol. 2022;218:152–161. doi: 10.2214/AJR.21.26274.
    1. Hwang M, Sridharan A, Darge K, Riggs B, Sehgal C, Flibotte J, et al. Novel quantitative contrast-enhanced ultrasound detection of hypoxic ischemic injury in neonates and infants: pilot study 1. J Ultrasound Med. 2019;38:2025–2038. doi: 10.1002/jum.14892.
    1. Kastler A, Manzoni P, Chapuy S, Cattin F, Billon-Grand C, Aubry S, et al. Transfontanellar contrast enhanced ultrasound in infants: initial experience. J Neuroradiol. 2014;41:251–258. doi: 10.1016/j.neurad.2013.11.001.
    1. Vinke EJ, Kortenbout AJ, Eyding J, Slump CH, van der Hoeven JG, de Korte CL, et al. Potential of contrast-enhanced ultrasound as a bedside monitoring technique in cerebral perfusion: a systematic review. Ultrasound Med Biol. 2017;43:2751–2757. doi: 10.1016/j.ultrasmedbio.2017.08.935.
    1. Kerscher SR, Schweizer LL, Nägele T, Bevot A, Alber M, Schuhmann MU. Transtemporal ultrasound (US) assessment of third ventricle diameter (TVD): comparison of US and MRI TVD in pediatric patients. Neuropediatrics. 2020;51:185–191. doi: 10.1055/s-0039-3400978.
    1. Hwang M, Tierradentro-Garcia LO. A concise guide to transtemporal contrast-enhanced ultrasound in children. J Ultrasound. 2022 doi: 10.1007/s40477-022-00690-3.
    1. Ntoulia A, Anupindi SA, Back SJ, Didier RA, Hwang M, Johnson AM, et al. Contrast-enhanced ultrasound: a comprehensive review of safety in children. Pediatr Radiol. 2021;51:2161–2180. doi: 10.1007/s00247-021-05223-4.
    1. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, et al. Fiji: an open-source platform for biological-image analysis. Nat Methods. 2012;9:676–682. doi: 10.1038/nmeth.2019.
    1. Qiu W, Bouakaz A, Konofagou EE, Zheng H. Ultrasound for the brain: a review of physical and engineering principles, and clinical applications. IEEE Trans Ultrason Ferroelectr Freq Control. 2021;68:6–20. doi: 10.1109/TUFFC.2020.3019932.
    1. Kearns KN, Sokolowski JD, Chadwell K, Chandler M, Kiernan T, Prada F, et al. The role of contrast-enhanced ultrasound in neurosurgical disease. Neurosurg Focus. 2019;47:E8. doi: 10.3171/2019.9.FOCUS19624.
    1. Freeman CW, Hwang M (2022) Advanced ultrasound techniques for neuroimaging in pediatric critical care: A review. Children (Basel) 9: 1–89
    1. Simms DL, Neely JG. Thickness of the lateral surface of the temporal bone in children. Ann Otol Rhinol Laryngol. 1989;98:726–731. doi: 10.1177/000348948909800913.
    1. Sridharan A, Riggs B, Darge K, Huisman TAGM, Hwang M. The Wash-Out of Contrast-Enhanced Ultrasound for Evaluation of Hypoxic Ischemic Injury in Neonates and Infants: Preliminary Findings. Ultrasound Q. 2021;38:36–42. doi: 10.1097/RUQ.0000000000000560.
    1. Seidel G, Meairs S. Ultrasound contrast agents in ischemic stroke. Cerebrovasc Dis. 2009;27(Suppl 2):25–39. doi: 10.1159/000203124.
    1. Meairs S. Contrast-enhanced ultrasound perfusion imaging in acute stroke patients. Eur Neurol. 2008;59(Suppl 1):17–26. doi: 10.1159/000114456.
    1. Wiesmann M, Meyer K, Albers T, Seidel G. Parametric perfusion imaging with contrast-enhanced ultrasound in acute ischemic stroke. Stroke. 2004;35:508–513. doi: 10.1161/01.STR.0000114877.58809.3D.
    1. Kern R, Diels A, Pettenpohl J, Kablau M, Brade J, Hennerici MG, et al. Real-time ultrasound brain perfusion imaging with analysis of microbubble replenishment in acute MCA stroke. J Cereb Blood Flow Metab. 2011;31:1716–1724. doi: 10.1038/jcbfm.2011.14.
    1. Higgins AM, Harris AH. Health economic methods: cost-minimization, cost-effectiveness, cost-utility, and cost-benefit evaluations. Crit Care Clin. 2012;28(11–24):v. doi: 10.1016/j.ccc.2011.10.002.
    1. Hwang M, Tierradentro-García LO, Haddad S, Poznick L, Kilbaugh T, Chiotos K. Feasibility of contrast-enhanced ultrasound for assessing cardiac and renal microvascular flow in patients with multisystem inflammatory syndrome in children. Clin Pediatr (Phila) 2022;61:241–247. doi: 10.1177/00099228211073288.
    1. Gumus M, Oommen KC, Squires JH. Contrast-enhanced ultrasound of the neonatal brain. Pediatr Radiol. 2021 doi: 10.1007/s00247-021-05157-x.
    1. Yusuf GT, Sellars ME, Deganello A, Cosgrove DO, Sidhu PS. Retrospective analysis of the safety and cost implications of pediatric contrast-enhanced ultrasound at a single center. AJR Am J Roentgenol. 2017;208:446–452. doi: 10.2214/AJR.16.16700.
    1. Darge K, Papadopoulou F, Ntoulia A, Bulas DI, Coley BD, Fordham LA, et al. Safety of contrast-enhanced ultrasound in children for non-cardiac applications: a review by the Society for Pediatric Radiology (SPR) and the International Contrast Ultrasound Society (ICUS) Pediatr Radiol. 2013;43:1063–1073. doi: 10.1007/s00247-013-2746-6.

Source: PubMed

3
Subscribe