6
Asterios Pigadas 1 Joseph R. Thompson 1 Gerald L. Grube 2 Receive d Oc t ober 26 . 1979; acce pt ed after revision Feb ruary 10, 198 1. Presented at the an nual meetin gs of the Amer- ican Ins ti tute of Ull raso und in Medicine, Mo ntr eal, August 1979 and the Wes tern Neuroradiolog ica l Soc iely. Carmel, California, October 1979. 'Depar lmen t of Radiati on Sciences, Sec ti on of Neuroradiol ogy, Lorn a Lind a University Sc hool of Medicine, Lorn a Lind a, CA 92350. Address reprint requests to J. R. Thompson. 2Department of Radiation Sciences, Sec tion of Di agnos ti c Ullrasound, Lo rn a Linda University Sc hoo l of Medicine, Lorn a Lind a, CA 92350. This paper app ears in the July / August 198 1 issue of AJNR and the October 198 1 issue of AJR. AJNR 2:339-344 , July / AU9ust 1981 0195 -6108 /81/ 0204 - 0339 $00.00 © Ameri ca n Roentge n Ray Soc iety Normal Infant Brain Anatomy: Correlated Real-Time Sonograms and Brain Specimens 339 An investigation of the identifiable real-time sonographic features of the normal infant brain in the horizontal , coronal , inclined coronal , and midsagittal planes was undertaken . Correlations were made of sonograms of intact brains in vitro , correspond- ing brain sections , and sonograms in vivo . A large number of anatomic structures could be consistently depicted including cisterns , fissures , falx cerebri , tentorium cerebelli , ventricles , brainstem , cerebellum , basal ganglia , thalami , and corpus callosum . Pulsa- tions of intracranial arteries , visible by real-time sonography , were of considerable help in identifying various structures. The investigation provides a reference of sonographic anatomy of the brain displayed in four clinically useful imaging planes. Early investigator s of diagno stic sonogr aphy were f ace d with the pro bl ems of sma ll -ape rture unf oc used tr ansdu ce r s. In 19 67 , Whit e et a l. [1] summ ari zed these problems. In 1972, K osso ff and Ga rr ett [2] reported intr ac ranial deta il in fet al echograms using a wea kly f oc used 2 MHz tr ansdu ce r. Th ey subsequently published a sono gr a phic atlas of the norm al br ain of inf ant s using a f oc used 3 MHz tr ansducer- c ont act C.A.L. echo sc op e [3]. McR ae [4] and Whit e [5], ho w- eve r, questioned their ability to ide ntif y th ose intr ac ranial struc tur es. In 1976, Heimberger et a l. [6] , using large-ape rtur e tr ansdu ce r s, managed to dis play the outlin es of the thalamus, internal capsul e, and sub stantia nigra in isolated ex cised brain s. Rece ntly Johnson et a l. [7] showed sonog raphic anatomy in the axial plane and exa mples of intr aventricular hemorrhage in high ri sk inf a nt s using B-mode co nt ac t transdu ce r s. The adve nt of versatile real-time tr ansdu ce rs has stimulated us to do more de tailed imaging in several planes to est ab li sh a b asic anatomy for use in clini ca l work. Real-time as opp osed to static sca nning was chose n b eca use: 1. Rec ogniz able pulsations of the intr acranial vessels within fi ss ur es and c istern s and of the c hor oid plexuses within the ventricles pr ovides eas ier identi- fication of these s tructur es. 2. The real-time probe ca n be eas il y maneuvered so that the ultr aso nic beam is perpendicul ar to the intr ac ranial struc tur e under study, theref ore r eceiv ing stronger refle cting echoes for better images. Skolnick et a l. [8] used a servo- co ntrolled real-time sca nn er to det ec t dilated ventricles and c orr elated the findin gs with co mputed tomography. We thought it would be mor e useful to cor relate real-time sonog raphy and anatomic sec ti ons, in planes ava il able for c lini ca l exam inati on. Materals and Methods The so nographic exa minations we re pe rformed by using eit her a linear phased array tr ansdu ce r operating at 2.25 MH z and disp lay ing 84 0 fan-s haped i mages at a fr ame rate of 30/ sec (Vari an V- 3000), or an annular arr ay tr ansd ucer opera t ing at 2.25 MHz ± 15%

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Page 1: Normal Infant Brain Anatomy - · PDF fileNormal Infant Brain Anatomy: ... brainstem, cerebellum, basal ganglia ... detailed imaging in several planes to establish a basic anatomy for

Asterios Pigadas 1

Joseph R. Thompson 1

Gerald L. Grube2

Received October 26 . 1979; accepted after rev ision Febru ary 10, 1981.

Presented at the annual meetings of the Amer­ican Insti tute o f Ull rasound in Medic ine, Montrea l, August 1979 and the Western Neuroradio log ica l Soc iely. Carm el, Ca lifornia, October 1979.

' Deparlment of Radiati on Sciences, Sec ti on of Neuroradiology, Lorn a Linda Universi ty School of Medic ine, Lorn a Linda, CA 92350. Address reprint requests to J . R. Thompson.

2Departm ent of Radiat ion Sciences, Sec tion of Diagnosti c Ullrasound, Lorn a Li nda Unive rsity Schoo l of Medic ine, Lorn a Linda, CA 92350.

This paper appears in the July / August 1981 issue of AJNR and the October 1981 issue of AJR .

AJNR 2:339-344, July / AU9ust 1981 0 195- 6 108 / 8 1/ 0204 - 0339 $00.00 © American Roentgen Ray Society

Normal Infant Brain Anatomy: Correlated Real-Time Sonograms and Brain Specimens

339

An investigation of the identifiable real-time sonographic features of the normal infant brain in the horizontal , coronal , inclined coronal , and midsagittal planes was

undertaken. Correlations were made of sonograms of intact brains in vitro, correspond­ing brain sections, and sonograms in vivo. A large number of anatomic structures could be consistently depicted including cisterns , fissures , falx cerebri , tentorium cerebelli , ventricles, brainstem, cerebellum , basal ganglia , thalami , and corpus callosum . Pulsa­tions of intracranial arteries, visible by real-time sonography, were of considerable help in identifying various structures. The investigation provides a reference of sonographic anatomy of the brain displayed in four clinically useful imaging planes.

Early investigators of diagnosti c sonography were faced with the probl ems of small-aperture unfocused transducers. In 1967 , White et al. [1] summari zed these problems. In 1972, Kossoff and Garrett [2] reported intracranial detail in fetal echograms using a weakl y focused 2 MHz transducer. They subsequently published a sonographic atl as of the normal brain of infants using a focused 3 MHz transducer-contact C.A.L. echoscope [3]. McRae [4] and White [5], how­ever, questioned their ability to identify those intracranial structures . In 1976 , Heimberger et al. [6] , using larg e-aperture focus~9 transducers, managed to display the outlines of the thalamus, intern al capsule, and substanti a nigra in isolated excised brains. Recentl y Johnson et al. [7] showed sonographic anatomy in the axial plane and examples of intraventric ul ar hemorrhage in hi gh ri sk infants using B-mode contact transducers.

The advent of versatil e real-time transducers has stimul ated us to do more detailed imaging in several planes to establish a basic anatomy for use in c linical work. Real-time as opposed to stati c scanning was chosen because:

1. Recognizabl e pulsati ons of the intrac ranial vesse ls within fi ssures and c isterns and of the choroid plexuses w ithin the ventric les provides easier identi­fication of these structures .

2 . The real-tim e probe can be easil y maneuve red so that the ultrasonic beam is perpendicular to the intracranial struc ture under study, therefore receiving stronger reflec ting echoes for better images.

Skolnick et al. [8 ] used a servo-controlled rea l-time scanner to detect dilated ventri c les and correlated the findings with computed tomog raphy. We thought it would be more useful to correlate rea l-t ime sonography and anatomic secti ons, in planes availabl e for c linical exam inati on.

Materals and Methods

The sonog raphic examinations were performed by using either a linear phased array transducer operating at 2.25 MHz and d isplaying 84 0 fan-shaped images at a frame rate of 30 / sec (Varian V-3000), or an annular array transducer operating at 2.25 MHz ± 15%

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340 PIGADAS ET AL AJNR:2, Ju ly / August 1981

A B

A B Fig . 2.-Horizonta l p lane at leve l of c hiasmat ic c istern . A, In vitro rea l­

time sonog ram. B , Anatomic sect ion . C, In vivo. CC = chiasmati c c istern ; Int F = interh emispheric fi ssure; Syl F = sy lvian fissure. M es = mesencephalon;

and displaying 24 0 angle sector images at a selec table frame rate of 1 or 12 / sec (Xerox 1505-4).

Three excised brain spec imens were fi xed in formalin for 2 weeks and th en immersed in tap water. Care was taken to exclude air bubbles from th e fi eld of view. Th e probe (Xerox 1505-4) was then placed over th e temporal lobe and serial images were obtained in the ho ri zontal p lane at 1 cm incremen ts from the level of the lower cerebellum to th e high convex ities of the cerebrum . For th e next spec imen, th e probe was pl aced in a position assumed to simu late th e anterior fontanelle and serial 1 c m images were obtained in the coronal plane. For the third spec imen, th e transducer was placed in the position of th e anterio r fontanelle and th e beam was directed toward the fourth ventric le giving a modified coronal image (inclined coronal plane). Finally, images were obtained with th e beam di­rec ted in the midsag ittal p lane. After the in vitro scanning was completed, the spec imens were sectioned in the correspond ing planes.

Fifteen normal infants aged up to 15 months (average, 5 months) were also examined. Each had a normal CT study . The probe

c

Fig . 1.- Transducer placemenl for multiplanar imag ing .

Ten = tentorium. Opt ic chiasm (black arrow); aqueducl of Sylvius (white arrow); temporal horn (arrowhead).

(Varian V-3000) was placed over the temporal squama for the horizontal planes and over the anterior fontanelle for the coronal, inc lined co ronal, and midsag ittal planes (fig . 1). Adequate ultrasonic gel was app lied between th e probe and skin for optimal acoustical coupling . No sedation or anesth esia was necessary. Postprand ial

scanning or the use of a pacifier was adequate to obtain opt imal images. All real-time sonograms were displayed on a video screen and permanent records were made on Polaroid film and video tape.

Horizontal Plane

Level of the Chiasmatic Cistern

The chiasmatic (suprase llar) c istern is shown as a penta­gonal , strongly echogenic structure in the center of the image, with the similarly echogenic interhemispheric and Sylvian fissures originating from the anterior and both lateral corners of the pentagon (fig. 2) . Posteriorly, the circumme-

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AJNR:2. July / August 1981 INFANT CRANIAL ANATOMY 3 41

A B Fig. 3. -Hori zontal plane at level of cerebral pedunc les. A, In vit ro . B,

Anatomic sec ti on . C, In vivo . AC = ambient c istern ; Cer V = cerebellar vermis; Cir S = circ ular sulcu s; qc = quadri geminal c istern ; 3 = third

A B Fig . 4 .-Horizontal plane at level of thalami . A , In vitro. B , Anatomic

sec tion . C, In vivo. T = trigone; Tha = th alamus; vgc = ve in o f Galen c istern ;

sencephalic cisterns are continuous with the posterior cor­ners of the c isternal pentagon and outline a V-shaped ane­choic structure, the mesencephalon .

In the center of the pentagon , a low-amplitude-echo struc­ture is constantly seen and represents the optic chiasm . The relatively hypoechoic optic chiasm appears to be di­vided by a thin midline linear echogenic structure which can be shown to be the anterior inferior part of third ventricl e. Immed iate ly ventral to the mesencephalon, the basilar artery

c ventri c le ; Int F = interhemispheric fi ssure. Choroid plexus of temporal horn ( arrowhead ); aqueduc t ( arrow ).

c Cir S = c irc ular sulcus. Forn ix (") ; co rpus ca llosum (long arrow) ; anterio r horn s ( short arrows ).

can be seen to be pulsating within the interpeduncular c istern .

Pul sati ons are seen with in the Sylvian, in te rhemispheri c , and c ircummesencephalic c istern s from the middle ce rebral , anteri or ce rebral, and ci rcummesencephalic arteri es, re­spectively . Posteri orl y, the low amplitude echogenic ce re­bellum is outlined by obliquely ori ented echoes representing the leaves of the tentorium . The frontal and temporal lobes are depicted by low amplitude echoes.

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34 2 PIGADAS ET AL. AJNR:2. July / August 1981

A B c Fig . 5. -Horizontal plane at level o f lateral vent ric les. A, In vitro. B , Anatomic sec ti on. C, In vivo. Lateral wa ll of lateral ventric les (paramedian echoes); fa lx

ce rebri (m id line echo).

Level of the Cerebral Peduncles

The anechoic V-shaped mesencephalon is in the center of the image, with the constantly seen single strong echo of the aq ueduct of Sylvius in the center of the tectum (fig . 3). Posteriorl y, the echogenic tentori al hiatus outlines the su­peri or vermi s, which is separated from the mesencephalon by the quadrigeminal c istern . The lateral margins of the mesencephalon are outlined by the ambient c istern s, whi ch are situated medial to the parahippocampal gyri. The am­bient c istern s appear to join the choroid plexuses of the temporal horn s by their continuation with the transverse cerebral fi ssures. The linear echogenic struc ture in front of the midbrain represents a combinati on of third ventric le and interhemispheric fi ssure. The c ircul ar sulc i are also seen as strong curvilinear pul satil e echoes at the med ial aspects of the Sy lvian fi ssures.

Level of the Thalami

The mid line echogenic third ventric le is seen in the center of the image (fi g. 4) . Near its anteri or end , the forni x, a bul bous hyperechoic struc ture, separates the posteri or parts of the frontal horns and blends with the echoes of the septum pe lluc idum and interhemispheri c fi ssure. On each side of the third ventric le, a well defined , low amplitude, oval structure represents the thalamus. Just posteri or to the thalami , the transversely ori ented, echogenic, retrothalamic fi ssures run toward the choroid plexuses of the ventricular atri a and ou tline the calcar avis. The echogenic ity of the lentiform nucleus is similar to that of the thalamus. The two structures are occasionall y seen to be separated by the posteri or limb of the intern al capsule. Laterall y the basal ganglia and thalami are distinc tl y outlined by the c ircul ar su lc i.

Level o f Lateral Ventricles

The midline, echogenic , interhemi spheric fi ssure is seen accommodating the fal x cerebri (fig. 5) . Parallel , paramedial , linear echogenic struc tures are also seen which represent the lateral wall s of the lateral ventric les. The inner table of the parietal bone is sharpl y defined. Soft echoes interposed between the falx cerebri and lateral wall of the lateral ven­tri c le represent combination echoes of the medial wall of the lateral ventric le and of the parietal cortex .

Coronal Plane

Level of the Chiasmatic Cis tern

The anechoic opti c chiasm is readily seen within the strongly echogenic and pulsatil e chiasmatic c istern (fig . 6). Superi orly, one can see the midline echo of the third ventri­c le. The roof of the third ventric le refl ects strong echoes due to the tela choroidea. Just above it, a thin, anechoic , hori zontal stri pe is constantly seen which represents the corpu s callosum. Superiorly , two pulsatile echogenic struc­tures, the peri callosal and callosomargin al arteri es, can be identified within the peri callosa l and c ingulate sulc i. Lat­era ll y, the c ircular sulc i mark the outer margins of the basa l ganglia and thalami.

Level of Crural and Interpeduncular Cis terns

The centrall y placed interpeduncular c istern " stands out " due to strong refl ections from the pulsations of the basilar artery (fi g. 7). Just inferi or to thi s c istern , a faintly outlined brai nstem is seen. On each side of the interpeduncular c istern , the mediall y convex c rural c istern outlining the uncus continues laterally and blends with the echoes of the choroid plexus of the temporal horn . The low amplitude thalamic echoes are seen above the interpeduncular c istern

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AJNR:2 . July / Augusl1981 INFANT CRANIAL ANATOMY 343

Fig . 5 .-Coronal plane al level of chiasmal ic cislern . A, In vitro. B, Analomic sec l ion. C, In vivo . BG = basa l ganglia; CC = chiasmalic cislern ; C. c =

cingulale sulcus; Cir S = c ircular sulcus; p . p = peri callosal sulcus; 3 = third ventric le; oc = opt ic chiasm. Corpus ca llosum (arrow) .

B c Fig . 7 .- Coronal plane at level of c rural and in te rpeduncular c iste rn s (IC) . A, In vil ro. B, Anatomic spec imen. C , In vivo. Cr C = crural cistern ; Tha =

thalamus; C. c = c ingulate sulcus; p . p = perica llosal sulcus. Corpus callosum (arro w) .

and, more superiorly , the lateral ventric les, corpus callosum , and supracallosal sulci.

Inclined Coronal Plane

The inclined coronal plane (fig . 8) is extremely helpful in outlining the posterior fossa . The obliquely oriented echo­genic tentorial leaves outline the upper cerebellum, which is characterized by uniform, low to medium amplitude echoes. The fourth ventricle is a round and highly echogenic midline structure .

Midsagittal Plane

The midsagittal plane (fig. 9) exquisitely outlines midline structures such as the third ventricle, corpus callosum , and brainstem. It is interesting that the third ventricle is depicted in this plane as an anechoic structure except for the massa intermedia. Its anechoic appearance is probably explained by the sagittal orientation of the walls of the third ventri c le and the depth of cerebrospinal fluid (CSF) within it. Often the opti c and infundibular recesses of the third ventricle can be seen. Inferiorly, the mesencephalon , pons, and medulla oblongata are seen as fairly uniform , hypoechoic struc tures.

Anterior to the brainstem are the echogenic and pul satile interpeduncul ar , prepontine, and medullary c istern s. Pos­teri or to the brainstem are the relatively high amplitude echoes of the cerebellar ve rmi s.

Discussion

The echogenic ity of an intracranial structure depends on its abrupt interface with neighborin g struc tures. Struc tures with abrupt interfaces inc lude: (1) lateral walls of lateral ventric les against the cerebrospinal flu id ; (2) vessels and nerves within fi ssures and c istern s; (3) the myriad frondlike interdi gi tati ons of the ventricular choroid plex us within the cerebrospinal fluid ; and (4) falx cerebri and tentorium against ce rebrospinal fluid . Fissures, c istern s, choroid plexus, lateral ventricular wall s, falx, and tentoriu m, there­fore, are always depic ted as strongly echogenic structures which can be used reliably as anatomic landmark s. The ., c rowded ." strongly echogenic appearance of c isterns re­sulting from interposition of meninges, veins, and pulsating arteries is in contrast to the usual conception of their bei ng " empty " CSF-filled spaces on computed tomog raphy or pneumoencephalog raphy .

In our experi ence , the midline third ventric le creates a single linear echo due to its c losely spaced ependymal

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344 PIGADAS ET AL. AJNR :2. July / August 1981

A B c Fig. 8. - lnc lined coronal plane through anteri or fontanelle . w ith beam d irec ted toward fourth ventric le . A, In vitro . B, Anatomic section. C, In vivo . Tr F =

transverse fissue; mes = mesencephalon; Ten = tentorium ; Tha = th alamus; 3 = third ventric le; 4 = fourth ventric le .

A B c Fig . 9 .- Midsag ittal plane. A, In vitro. B, An atomic sec tion. C, In vivo. Cer V = cerebellar vermis; C, c = cingulate sulc us; Cli = c livus; mes = mesencephalon ;

oc = optic chiasm; p = perica llosa l sulcus ; po = pons; 3 = third ventric le; 4 = fourth ventric le . Massa intermedia (short arrow ); corpus ca llosum (long arrow ).

surfaces. Thi s is similar to the midline echo pattern of the uterine cervica l canal on pelvic sonography . A slitlike ane­choic third ventric le , in fact , represents an early dilatation of its lumen. The fourth ventric le is depicted as a round ed echogenic struc ture due to the enorm ous ref lecting echoes of the c horoid plexus and the rh omboid ventric ul ar walls. Struc tures w ith homogeneous texture such as brainstem, thalamus, and corpu s ca llosum , on the other hand , produce unifo rm low amplitude echoes.

The far side of the sonographic image (w ithin the foca l d istance of the transducer) always shows more reliable inform ati on than the near side due to the inherent limited near-f ield reso lution of the phased-array real-time trans­ducers. Scanning through both temporal sq uama, therefore, is essentia l in order to obtain prec ise inform ati on from both hemispheres . Whil e stati c scanning does show intrac ranial struc tures , real-time sonog raphy has the advantage of quick and accurate struc ture identificati on because of vascular pu lsati ons and instantaneous display .

ACKNOWLEDGMENTS

We thank Abraham Lu fo r performing th e brain sectioning , Marie De Lange for the RTU scanning , and Sheila Wi ll s for assistance in preparing the manusc ri pt.

REFERENCES

1. White ON , Clark JM, White MN . Studies in ultrasonic echoen­cephalog raph y; VII. General princ iples of record ing information in ultrasonic B and C scanning and th e effects of scatter , refl ec tion and refrac tion by cadaver sku ll on this information . M ed 8 io l Eng 1967 ;5;3-1 4

2. Kossoff G, Garrett WJ . Intrac ranial detail in fetal echog rams. Inves t Radiol 1972;7 : 159 -1 63

3. Kossoff G, Garrett WJ , Radavanovich G. Ultrasoni c atlas of normal bra in of infant. Ultrasound Med 8 io /1974 ; 1 :259- 266

4. Mc Rea DL. Letters to th e ed ito r. Ultrasound Med 8 io/ 1975 ;1 : 41 1

5. White ON . Letters to the ed ito r. Ultrasound Med 8 io l 1975 ;2: 45-46

6. Heimburger RF , Fry FJ , Franklin TO , et al. Two dimensional ultrasound scanning of exc ised brains: I. Normal anatomy. Ultrasound Med 8 io/ 1977;2:279- 285

7. Johnson ML, Mack LA , Rumack CM , Frost M , Rashbaum C. B­

mode echoencephalog raphy in the normal and high risk infant. AJR 1979;133 :37 5- 38 1

8. Skolnic k ML, Rosenbaum AE , Matzuk T, Guthkelch AN, Hein z ER. Detection of d ilated cerebral ventric les in infants: a correl­ative study between ultrasound and computed tomography. Radiology 1979; 131 :447-451