State-of-the-Art Cranial Sonography: Part 1, Modern Techniques and Image Interpretation

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1 Pediatric Imaging Review Lowe and ailey Cranial Sonography Pediatric Imaging Review Downloaded from by on 02/10/18 from IP address Copyright RRS. For personal use only; all rights reserved FOCUS ON: Lisa H. Lowe 1,2 Zachary ailey 3 Lowe LH, ailey Z Keywords: cranial anatomy, Doppler sonography, pediatrics, ultrasound DOI: /JR Received November 18, 2010; accepted after revision January 7, Department of Radiology, University of Missouri Kansas City, Kansas City, MO. 2 Department of Radiology, Children s Mercy Hospitals and Clinics, 2401 Gillham Rd, Kansas City, MO ddress correspondence to L. H. Lowe (lhlowe@cmh.edu). 3 Kansas City University of Medicine and iosciences, Kansas City, MO. JR 2011; 196: X/11/ merican Roentgen Ray Society State-of-the-rt Cranial Sonography: Part 1, Modern Techniques and Image Interpretation OJECTIVE. In this era of radiation awareness, high-quality ultrasound is more important than ever. lthough cranial sonography equipment has advanced greatly, application of modern techniques has not been utilized in a fashion commensurate to other cross-sectional modalities. This article will describe modern cranial sonography techniques, including the utility of linear imaging, use of additional fontanels, and screening Doppler imaging. CONCLUSION. When modern protocols are used, cranial sonography is highly accurate for the detection of cranial abnormalities. lthough MRI is the reference standard for infant brain imaging, it is expensive, often requires sedation, and may not be possible to perform on critically ill patients. Cranial ultrasound is relatively inexpensive, does not require sedation or radiation, and offers the important benefit of being portable. Past studies comparing the utility of cranial ultrasound to MRI have not taken into account modern technology and rigorous ultrasound scanning technique. Recent studies using such techniques have shown that cranial ultrasound is diagnostically accurate compared with MRI and useful to determine initial clinical management [1, 2]. The objective of this article is to discuss a modern approach for cranial ultrasound, including a brief review of gray-scale technique and interpretation, followed by a discussion of linear imaging, use of multiple fontanels, and screening Doppler techniques. Cranial Ultrasound Technique: eyond the asics Cranial ultrasound begins with basic grayscale imaging performed using a linear-array transducer via the anterior fontanel in the coronal and sagittal planes [2, 3]. Typically, six to eight coronal images are obtained beginning at the frontal lobes just anterior to the frontal horns and extending to the occipital lobes posterior to the lateral ventricle trigones [4] (Fig. 1). The transducer is then rotated 90, and approximately five images are obtained, including a midline sagittal view of the corpus callosum and cerebellar vermis in addition to bilateral parasagittal images beginning in the midline and progressing laterally through the peripheral cortex [3, 4] (Fig. 2). Next, four color Doppler images may be obtained for screening vascular structures [5]. The arterial system is assessed for patency and resistance to flow by obtaining a color Doppler image of the circle of Willis (Fig. 3). This image, obtained via the anterior or temporal fontanel, is used to localize the middle or internal cerebral artery to obtain a spectral tracing with peak systolic velocity (PSV), end-diastolic velocity (EDV), and resistive index (RI), which are discussed in more detail later in this article. The venous system is evaluated for patency by obtaining a color Doppler image of the sagittal sinus and vein of Galen in the sagittal plane. Last, some authors have advocated the use of power Doppler imaging to search for areas of hyper- or hypovascularity, as may occur with various forms of vascular occlusion, ischemia, or infarction [2]. To complete the modern head ultrasound, screening images via other supplemental fontanels and high-resolution linear images are needed. Visualization of the cerebellar hemispheres is optimized by obtaining images through the right and left mastoid fontanels. This technique has been shown to improve detection of posterior fossa hemorrhages [6] (Figs. 4 and 5). djunct color Doppler images via the posterior fontanel or foramen magnum can also be used to screen for patency of 1028 JR:196, May 2011

2 Cranial Sonography Downloaded from by on 02/10/18 from IP address Copyright RRS. For personal use only; all rights reserved the transverse sinuses [2, 7, 8]. Finally, completion of the modern cranial ultrasound requires switching from a curved- to a linear-array transducer, which allows high-resolution imaging of the brain. Linear images obtained via the anterior fontanel allow detailed interrogation of the convexity subarachnoid space and superficial cortex as well as deeper brain structures [2] (Fig. 6). Linear images can be adjunctively obtained via any fontanel. Cranial Ultrasound Interpretation: Gray-Scale Imaging With advances in technology allowing improved sonographic resolution, it is more important than ever to be aware of the normal echogenicity of various anatomic structures in the brain. To reinforce these basic cranial ultrasound principles, there are some helpful interpretation concepts [5]. First, gray matter tends to be hypoechoic and white matter tends to be hyperechoic. When this pattern is reversed, abnormality is indicated (Fig. 7). Second, the normal brain is always symmetric, but symmetric is not always normal. This principle is helpful to avoid overlooking symmetric abnormalities such as bilateral hyperechoic thalami as can occur with thalamic edema, ischemia, or infarct [5, 9] (Fig. 8). third principle involves visualization of all layers of the normal cortex. The superficial pia mater should be seen as a thin welldefined hyperechoic layer overlying the hypoechoic cortical gray matter, which in turn overlies the hyperechoic white matter [10]. Failure to distinctly visualize these normal layers is helpful to identify areas of abnormality, such as focal hemorrhage or infarct [11] (Fig. 9). Fourth, the periventricular white matter is normally homogeneous in echogenicity and is equal to or less echogenic than the adjacent choroid plexus [3, 5]. symmetry or heterogeneity of the periventricular white matter suggests an abnormality, as can occur with periventricular leukomalacia (Fig. 10). Cranial Ultrasound Interpretation: Doppler Imaging lthough a complete discussion of Doppler techniques is beyond the scope of this article, addition of screening Doppler images to develop a modern head ultrasound protocol is easy to implement if one is familiar with some basic principles. Color, spectral, and power Doppler imaging can be performed in the coronal or transverse plane via the anterior or temporal fontanels, respectively. The choice of which fontanel to use is based on convenience as well as which vessels the operator wishes to interrogate [7]. oth fontanels allow visualization of the circle of Willis. However, the internal cerebral arteries are more easily seen via the anterior fontanel [3, 4]. The arterial and venous structures can be screened for patency with color Doppler techniques, typically in the coronal and sagittal planes, respectively. Power Doppler is less often used but may be applied to screen for regions of hyper- or hypovascularity. RI and systolic and diastolic velocities can be evaluated using spectral Doppler tracings, most often measured within the middle or internal cerebral arteries. The RI (defined as PSV EDV / PSV) is influenced by many factors, such as flow velocity, blood volume, presence of congenital cardiac anomalies, and peripheral vascular resistance [12, 13]. Increasing diastolic flow, secondary to changing from fetal to newborn circulation, causes the average RI to decline with age from 0.77 (± 0.15) in premature infants to 0.73 (± 0.57) in term infants to approximately 0.6 in children 1 year old and eventually reaching in children over 2 years [7, 14]. n RI between 0.6 and 0.9 can be used as an approximate value to encompass normal values for both term and preterm infants. The RI becomes lower with increases in diastolic flow. n example of this occurs when there is cerebral vascular dilatation resulting from acute hypoxia or ischemia of any cause (Fig. 11). The RI becomes higher with decreases in diastolic flow. n example of this occurs when cerebral swelling causes intracranial pressure to exceed systemic pressures, impeding cranial flow during diastole [5]. One caveat that is very important to keep in mind is that in children with cardiac disease, particularly those with left to right shunts and extra cardiac shunts, the RI is unreliable and cannot be used [15]. Perhaps the most common cause for an elevated RI in the neonatal ICU is a patent ductus arteriosus (Fig. 12). nother caveat with Doppler imaging is that velocities may vary somewhat over time. Thus, it is useful to obtain two or more measurements in each vessel to confirm the measurement. Conclusion Ultrasound technology has advanced significantly in recent years, although application of newer imaging protocols has been slow to catch on. With implementation of modern protocols, ultrasound is highly sensitive and accurate for the detection of pediatric cranial abnormalities. References 1. Daneman, Epelman M, laser S, Jarrin JR. Imaging of the brain in full-term neonates: does sonography still play a role? Pediatr Radiol 2006; 36: Epelman M, Daneman, Kellenberger CJ, et al. Neonatal encephalopathy: a prospective comparison of head US and MRI. Pediatr Radiol 2010; 40: Seigel M, ed. Pediatric sonography, 3rd ed. Philadelphia, P: Lippincott Williams & Wilkins, Rumack C, Wilson S, Charboneau J. Diagnostic ultrasound. St. Louis, MO: Mosby, North K, Lowe L. Modern head ultrasound: normal anatomy, variants, and pitfalls that may simulate disease. Ultrasound Clin 2009; 4: Di Salvo DN. new view of the neonatal brain: clinical utility of supplemental neurologic US imaging windows. RadioGraphics 2001; 21: Lowe LH, ulas DI. Transcranial Doppler imaging in children: sickle cell screening and beyond. Pediatr Radiol 2005; 35: Sudakoff GS, Montazemi M, Rifkin MD. The foramen magnum: the underutilized acoustic window to the posterior fossa. J Ultrasound Med 1993; 12: Huang Y, Castillo M. Hypoxic-ischemic brain injury: imaging findings from birth to adulthood. RadioGraphics 2008; 28: ; quiz, Slovis TL, Kuhns LR. Real-time sonography of the brain through the anterior fontanelle. JR 1981; 136: Grant EG, Schellinger D, orts FT, et al. Realtime sonography of the neonatal and infant head. JR 1981; 136: ulas DI, Vezina GL. Preterm anoxic injury: radiologic evaluation. Radiol Clin North m 1999; 37: Soetaert M, Lowe LH, Formen C. Pediatric cranial Doppler sonography in children: non-sickle cell applications. Curr Probl Diagn Radiol 2009; 38: llison JW, Faddis L, Kinder DL, Roberson PK, Glasier CM, Seibert JJ. Intracranial resistive index (RI) values in normal term infants during the first day of life. Pediatr Radiol 2000; 30: Lipman, Serwer G, razy JE. bnormal cerebral hemodynamics in preterm infants with patent ductus arteriosus. Pediatrics 1982; 69: JR:196, May

3 Lowe and ailey Downloaded from by on 02/10/18 from IP address Copyright RRS. For personal use only; all rights reserved D Fig. 1 Normal coronal gray-scale images of 7-day-old boy with seizures., Sonogram through frontal lobes (F) shows orbits (O) and hyperechoic falx cerebri (arrow) located within interhemispheric fissure., Sonogram through frontal horns shows corpus callosum, seen as hypoechoic midline structure outlined by echogenic superior and inferior borders (arrow). Frontal horns (F), cavum septum pellucidum (asterisk), globus pallidus (G), putamen (P), caudate nucleus (C), temporal lobes (T), and Sylvian fissure (dotted line) are seen. C, Sonogram at level of cerebral peduncles identifies hyperechoic choroid plexus along roof of third ventricle (straight arrow) and floor of lateral ventricles (curved arrows). lso noted are left cerebral peduncle (CP), thalamus (T), cerebellar hemispheres (Cb), and cisterna magna (arrowhead). D, Sonogram at level of quadrigeminal plate (Q) illustrates temporal lobes (TL), cerebellar hemispheres (Cb), thalamus (T), hippocampus (H), and third ventricle (3). E, Sonogram obtained through hyperechoic choroid plexus (asterisks) within lateral ventricles. Note less echogenic adjacent periventricular white matter (arrows). Periventricular white matter halo should normally be less echogenic than adjacent choroid plexus. F, Sonogram through cerebral convexities reveals normal layers of cortex, which should be seen throughout brain. Well-defined hyperechoic pia (curved arrow) on surface of cortex overlies hypoechoic cortical gray matter (straight arrow), which overlies slightly hyperechoic white matter (arrowhead). E C F 1030 JR:196, May 2011

4 Cranial Sonography Downloaded from by on 02/10/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig. 2 Normal sagittal gray-scale images of 7-day-old boy with seizures (same patient as Fig. 1)., Sonogram through midline shows corpus callosum (straight arrows), hypoechoic structure bound by echogenic superior and inferior borders, cingulate gyrus (arrowheads), cavum septi pellucidi (asterisk), occipital lobe (O), third ventricle (3) with choroid plexus in its roof (curved arrow), and fourth ventricle (4). lso noted are hypoechoic midbrain (M); pons (P), which has hyperechoic ventral and hypoechoic dorsal regions; and cerebellar vermis (V)., Parasagittal sonogram through lateral ventricles shows caudothalamic groove (arrow), separating caudate nucleus (C) from thalamus (T), and choroid plexus along posterior margin of thalamus (dotted line). Note hyperechoic focus adjacent to lateral ventricle trigone that was not seen on coronal view (not shown). This periventricular pseudolesion (arrowhead) is common artifact on this view. C, Normal peripheral sagittal gray-scale sonogram through Sylvian sulcus (dotted line) reveals temporal lobe (T), frontal lobe (F), and parietal lobe (P). Note normal hypoechoic gray matter (arrow) between superficial hyperechoic pia and slightly hyperechoic white matter. Fig. 3 Normal color Doppler sonography of 8-day-old premature girl being screened for intracranial hemorrhage., Sonogram obtained through circle of Willis illustrates right (Rt) and left (Lt) internal carotid arteries (IC), right and left middle cerebral arteries (MC), and anterior cerebral (C) arteries. Distinguishing between right versus left C is often difficult, but usually unnecessary. Thus, they are labeled together., Spectral Doppler tracing of circle of Willis obtained via anterior fontanel shows normal arterial flow pattern in MC. Note continuous flow above baseline, including rapid systolic upstroke (arrow) followed by gradual decline in flow during diastole (arrowhead). Normal peak systolic velocity (PSV), end-diastolic velocity (EDV), and resistive index (RI) are indicated. C, Sagittal Doppler sonogram of venous system shows patent deep venous system, including vein of Galen (VOG) (arrow). Pericallosal branch of C (arrowhead) is noted. D, Sonogram of superficial venous system, including sagittal sinus (arrow), is shown. Observe normal venous spectrum showing continuous undulating venous flow. Incidentally noted is reversal of color map. C C D JR:196, May

5 Lowe and ailey Downloaded from by on 02/10/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig. 4 Normal gray-scale posterior fossa sonogram obtained via mastoid fontanel in 3-day-old infant, on extracorporeal membrane oxygenation therapy screened for intracranial hemorrhage. Cerebellar hemispheres (Cb), fourth ventricle (4), cistern magna (asterisk), quadrigeminal plate (Q), vermis (V), and temporal lobes (T) are shown. Fig. 6 Normal linear sonographic image in coronal plane in 6-week-old girl with macrocephaly. Color Doppler linear image of superficial cortex reveals prominence of subarachnoid space. Normal vessels (arrows) are present. Fig. 5 Posterior fossa hemorrhage in 2-week-old boy born at 27 weeks gestational age. and, Coronal sonogram via anterior fontanel shows area of hypoechogenicity in right cerebellum (arrow), concerning for hemorrhage. Note developing posthemorrhagic hydrocephalus. When evaluated via mastoid fontanel (), right cerebellar hemorrhage (arrow) is confirmed. Fig. 7 Cortical necrosis in 5-week-old girl with septic shock due to group streptococcus sepsis. Coronal sonogram shows symmetric hyperechogenicity of cortex (arrows). Gray matter echogenicity is reversed from hypo- to hyperechoic, causing it to be abnormally similar in appearance to white matter versus gray matter JR:196, May 2011

6 Cranial Sonography Downloaded from by on 02/10/18 from IP address Copyright RRS. For personal use only; all rights reserved Fig. 8 Hypoxic ischemic brain injury in 2-day-old boy with seizures., Coronal sonogram reveals bilateral increased thalamic echogenicity (arrows). MRI (not shown) confirmed restricted diffusion in dorsal putamina and ventrolateral thalami., Coronal power Doppler image using linear-array transducer reveals hyperemic flow in lenticulostriate and thalamoperforate arteries of basal ganglia and thalami. Fig. 10 Periventricular leukomalacia in 6-week-old premature girl. Coronal sonogram identifies bilateral periventricular hyperechogenicity and subtle periventricular cystic encephalomalacia (arrows). MRI (not shown) confirmed diffuse abnormal signal in white matter and some periventricular hemorrhage. Fig. 11 Low resistive index (RI) in 2-day-old infant with hypoxic ischemic brain injury. Spectral Doppler tracing of middle cerebral artery (MC) obtained via temporal fontanel reveals elevated diastolic flow (arrow) and low RI of 0.53 (normal RI, approximately ). Gray-scale images (not shown) revealed diffuse increased echogenicity suggesting cerebral edema. PSV = peak systolic velocity, EDV = enddiastolic velocity. Fig. 9 Right middle cerebral artery stroke in 1-week-old boy. Coronal sonogram shows loss of normal cortex in right cerebrum (arrows). Compare with normal cortex on left. Fig. 12 Elevated resistive index (RI) in 8-day-old preterm infant due to patent ductus arteriosus. Spectral Doppler tracing obtained from middle cerebral artery (MC) shows elevated RI of 1.34 (normal preterm RI, 0.77 ± 0.15). Note normal rapid systolic upstroke followed by abnormally rapid decline with reversal of flow during diastole (arrow). PSV = peak systolic velocity, EDV = end-diastolic velocity. FOR YOUR INFORMTION The reader s attention is directed to part 2 accompanying this article, titled State-of-the-rt Cranial Sonography: Part 2, Pitfalls and Variants, which begins on page JR:196, May