Clinical Application of Three-dimensional Ultrasound in Fetal Brain Assessment

41(3):245-251,2000 CLINICAL SCIENCES Clinical Application of Three-dimensional Ultrasound in Fetal Brain Assessment Ritsuko K. Pooh, KyongHon Pooh 1, Yoshinobu Nakagawa 1, Souya Nishida, Yoshio Ohno Department of Obstetrics and Gynecology, The Taijukai Foundation, Kaisei Hospital; and 1 Department of Neurosurgery, National Kagawa Children s Hospital, Kagawa, Japan Aim. To clar ify the use ful ness of three-dimensional (3D) ul tra sound in the as sess ment of the fe t al head and brain, ac cord ing to 3D ul tra sound sur face re con struc tion, multiplanar im age anal y sis, three-dimensional angiography, and vol ume cal cu la tion. Methods. We ex am ined 326 nor mal fe tuses be tween 10 and 40 weeks of ges ta tion us ing 3D ul tra sound (Voluson, 530D, Medison, Se oul, Ko rea), mainly with transvaginal 3D trans ducer. Fe tal head struc tures, such as skull, brain struc ture, and brain cir cu la tion, were pre sented by sur face mode, multiplanar im ag ing mode, and three-dimensional Dopp ler mode. Af ter au to - matic vol ume ac qui si tion of the fe tal head, im age anal y ses were per formed off-line, and 3D View soft ware was used for vol - ume im ag ing of the lateral ventricle and choroid plexus in randomly selected 30 normal fet uses. Seven fetuses with intracranial ab nor mal i ties were eval u ated by 3D ul tra sound func tions. Re sults. Sur face mode of 3D ul tra sound ob jec tively de picted in vivo de vel op ment of the cra nial bones and for ma tion of the cra nial su tures and fon ta nelles in nor mal fe tuses. Multiplanar im age anal y sis of the brain struc ture pre sented a fe tal brain in more cut ting sec tions than con ven tional 2D ul tra sound. Transvaginal 3D angiography was suc cess ful in 13% of nor mal fe - tuses and ro ta tion of 3D cir cu la tory im age al lowed the anal y sis of the intracranial ves sels. Vol ume im ag ing showed the in di - vid ual intracranial struc tures, such as the lat eral ven tri cle and choroid plexus. Intracranial ab nor mal i ties were lon gi tu di nally eval u ated by 3D ul tra sound and ob jec tive im ages helped in reach ing pre na tal di ag no ses. Con clu sion. Ad vanced 3D ultrasonography and soft ware for vol ume anal y sis can pro vide ad di tional ob jec tive in for ma tion about the fe tal skull for ma tion, brain struc ture, and brain cir cu la tion. Key words: blood ves sels; brain, ultrasonography; Dopp ler ultrasonography, color; em bry onic struc tures; fe tal ultrasonography; sonography, transvaginal Dopp ler; ultrasonography, Dopp ler, transvaginal The intrauterine de vel op ment of the cen tral ner vous sys tem is one of the most in ter est ing fields in perinatology. Transvaginal sonographic ap proach to the fe tal brain pro vides de tailed in for ma tion about the fe tal intracranial mor phol ogy and cir cu la tion. It de picts the fe tal brain in the sagittal and co ro nal sec tions from the pa ri etal di rec tion, us ing fon ta nelles and cra nial su tures as ul tra sound win dows. Transvaginal sonography of the fe tal brain opened a new field in medicine, neurosonography (1), and its use had al lowed de tec - tion of many intracranial nor mal and ab nor mal con di - tions. Clin i cal sig nif i cance of 3D ul tra sound for pre na tal di - ag no sis has been dis cussed since three- dimensional (3D) ul tra sound was introduced in obstetrics (2-4). 3D ul tra - sound has several func tions: sur face reonstruction, multiplanar image analysis, three-dimensional angiography, and vol ume calculation. The aim of this study was to clar ify the use ful ness of all these func tions of trans vaginal 3D ul tra sound in the as sess ment of the fe tal head and brain. Methods From Jan u ary 1999 to March 2000, we ex am ined the head and brain of 326 nor mal sin gle ton fe tuses be tween 10 and 40 weeks of ges ta tion by transvaginal 3D ul tra sound. The ul tra sound de vice we used in our study was Voluson 530D (Medison, Se oul, Ko rea). In 64 cases, as transvaginal sono graphy failed to de pict the cra nial su ture, transabdominal vol ume scan was added for sur face re con struc tion of the calvaria. Intracranial struc tures were as sessed by transvaginal ap - proach in all cases. Af ter transvaginal two-dimensional (2D) ap - proach to the fe tal head, au to matic vol ume ac qui si tion was per formed and all the data were saved on the mag neto-optical disks. The im age anal y ses were done off-line. Sur face mode was used for as sess ment of the superficial structure of the fetal cranial bone, whereas multiplanar image analysis was used for the assessment of the intracranial mor pho log i cal de vel op ment. 3D color/angio mode was used for the demonstration of the brain circulation. Thirty normal cases be tween 12 and 34 weeks of ges ta tion were ran domly se lected for vol ume im ag ing. Brain vol ume data were re-formatted for vol ume anal y sis on Vaio PCV-R71, a per sonal com puter (Sony, To kyo, Ja - pan). Volume imaging and vol ume es ti ma tion of the intracerebral http://www.vms.hr/cmj 245

struc tures, i.e., the lateral ven tri cle and choroid plexus, were done with 3D View ver sion 3.2 soft ware (Kretztechnik AG, Zipf, Aus tria). Seven cases with ab nor mal brain struc ture were ex am ined dur - ing the study pe riod. Cen tral ner vous sys tem in each case was eval u - ated by use of all 3D ultrasound func tions men tioned ear lier. Results Ex am ining the fe tal cra nial bone struc tures by sur - face mode, we were able to de tect more than one of the su tures (sagittal, co ro nal, fron tal, and lambdoid) and fon - ta nelles (an te rior, pos te rior, and anterolateral) in 265 fe - tuses (81%). Sometimes, the cra nial for ma tion was de - tect able at as early as 10 or 11 weeks of ges ta tion, but in most cases it was pos si ble only af ter 12 weeks of ges ta - tion (Fig. 1). The sagittal su ture could be first rec og nized at 13 weeks as a wide and short space be tween pa ri etal bones. At 12 weeks, metopic su ture was rec og niz able as a very short space be tween the bi lat eral or bits, whereas wide an te rior fon ta nelle oc cu pied most of the cra nium from the top of the head to fore head. With the de vel op - ment of the bi lat eral fron tal bones, the metopic su ture was rap idly formed as a lin ear su ture be tween 13 and 17 weeks of ges ta tion. The an te rior fon ta nelle was rec og - niz able by its di a mond shape af ter 15 weeks of ges ta tion. The co ro nal su tures could be clearly de tected from 12 weeks of ges ta tion on. The lambdoid su ture was de tect - able af ter 12 weeks, and the pos te rior fon ta nelle grad u - ally took a tri an gu lar shape. By 23 weeks of ges ta tion, the skull shape re sem bled a neo na tal cra nial for ma tion. In fe tal brain scan ning, the mean ac qui si tion time was 1.84, 3.30, 4.76, and 6.07 sec onds at 15, 20, 30, and 40 weeks of ges ta tion, re spec tively. The brain struc ture was si - mul ta neously de tect able in the sagittal, coronal, and axial sec tions (Fig. 2) by ro tat ing the brain im ages un der var i ous an gles, and par al lel dis place ment of each sec tion showed the brain struc ture as it would be seen by mag netic res o - nance im ag ing (Fig. 3). By multiplanar image analysis, intracranial mor phol ogy could be con firmed in more than 80% of the cases at median, oblique-coronal, parallel sagittal, and par al lel co ro nal sec tions, and 59% at par al lel ax ial sec tions. Transvaginal 3D multiplanar im ag ing could demonstrate the brain struc tures in more cut ting sec tions than con ven tional 2D transvaginal sono graphy (Ta ble 1). The 3D color/power angiography could dem on - strate the intracranial cir cu la tion. The mean vol ume ac - qui si tion time of the brain cir cu la tion by transvaginal 3D color/power Dopp ler mode was 23.94 sec onds be tween 20 and 30 weeks of ges ta tion. The suc cess ful ori en ta tion of the brain cir cu la tion with me dian ves sels and bi lat eral sym met ri cal mid dle ce re bral ar ter ies and their branches (Fig. 4) was ob tained in 42 cases (13%). By ro tat ing 3D cir cu la tory im age, the intracranial ves sels could be con - firmed from var i ous di rec tions. Volume im ag ing and vol ume cal cu la tion with 3D View soft ware (Fig. 5) were suc cess fully per formed in all 30 cases. Vol ume im ag ing showed changes in ap pear - ance of the lat eral ven tri cle and choroid plexus dur ing preg nancy (Fig. 6). Es ti mated vol umes of both struc tures in creased dur ing preg nancy. In all 7 cases with intracranial ab nor mal i ties a hy - dro ceph a lus with myelomeningocele; peri ven tricular leukomalacia; intraventricular hemorrhage; Dandy-Walker vari ant; asym met ri cal ce re bral hypo plasia with myelomeningocele; agenesis of the cor pus cal lo sum with interhemispheric cyst; and partial fusion of hemi - sphere with cerebellar fusion lon gi tu di nal multiplanar im age anal y ses were suc cess ful and the ob jec tive im ages and vol ume data ob tained by ro ta tion of the brain helped in reaching prenatal diagnosis and con sid er ing postnatal treatment (Fig. 7). Sur face re con struc tion was used for ob - jective demonstration of the craniofacial abnormality and spinal abnormality of myelomeningocele (Fig. 8). Three-dimensional angiography showed displacement of intra cranial ves sels due to the brain ab nor mal i ties. 3D vol - ume analysis was used for the evaluation of the lateral ventri culo megaly (Fig. 9) and intra cranial le sion. Discussion In this study, we showed the nor mal cra nial bone for ma tion in vivo us ing 3D-ultrasound sur face mode. The calvaria and its ma jor su tures de velop be tween 12 and 18 weeks of fe tal life, with dura as guid ing tis sue in the morphogenesis of the skull (5). The cra nial su tures serve as ul tra sound win dows for ob ser va tion of the intracranial struc tures. So far, the sutural fu sion has not been dem on strated in vivo and pre na tal di ag no sis of cranio synostosis was al ways made on in di rect ev i dence of craniofacial ab nor mal shape and intracranial ab nor - mal mor phol ogy (6). Al though a fe tus with fron tal boss - ing and low na sal bridge in our study (Fig. 8) had in tact cra nial su tures, the cra nial ab nor mal ity could be de tected in utero by 3D sur face mode. Table 1. Detection rate of intracranial structure by transvaginal 2D and 3D approach in 326 normal fetuses a Sections Detectable structures No. (%) of cases detected by transvaginal Doppler approach 2D 3D Median (mid-sagittal) CC, SP, C, IV 287 (88) 287 (88) Serial oblique-sagittal LV, SAS, Hemisphere 287 (88) 285 (87) Serial oblique-sagittal (opposite) LV, SAS, Hemisphere 213 (65) 264 (81) Oblique-coronal bilateral AH, PH, hemisphere 232 (71) 261 (80) Parallel sagittal LV, SAS, hemisphere (0) 285 (87) Parallel coronal bilateral AH, PH, hemisphere (0) 264 (81) Parallel axial Falx, bilateral LV (0) 192 (59) a CC cor pus cal lo sum; SP sep tum pellucidum; C cer e bel lum; IV fourth ven tri cle; LV lat eral ven tri cle; SAS subarachnoid space; AH an te rior horn; PH pos te rior horn. 246

both transvaginal Dopp ler angiography Fig ure 1. Fe tal and cra nial 3D bone ul for tra - ma tion de picted by 3D sur - face-rendering mode: (a) 10 weeks of ges ta tion from frontal di rec tion; (b) 12 weeks of ges ta - tion from fron tal oblique di rec - tion. Short metopic su ture, wide co ro nal su ture and bi lat eral fron tal bones are seen; (c) 13 weeks of ges ta tion, from oc cip i - tal di rec tion. Sagittal and lambdoid su tures and oc cip i tal and pa ri etal bones are seen; (d) 16 weeks of ges ta tion, from pa - rietal di rec tion. Di a mond- shaped an te rior fon ta nelle and sagittal and co ro nal su tures are seen; (e) 18 weeks of ges ta tion, from fron tal oblique di rec tion. Metopic su ture is formed by the de vel op ment of bi lat eral fron tal bones; (f) 23 weeks of ges ta tion, from fron tal oblique di rec tion. Anterior fon ta nelle shape be comes sim i lar to neo na - tal fon ta nelle shape, and metopic su ture be comes linear. The in tro duc tion of high fre quency 2D trans vaginal trans ducer opened a new field in med i cal im ag ing sono embry ology (7). The new tech nique made a de tailed vi su al iza tion of the brain struc ture of early fe tuses pos si - ble (8-10). A case of intracranial ab nor mal ity di ag nosed in the sec ond tri mes ter transvaginally was first re ported in 1989 (11). Transvaginal ap proach to the nor mal fe tal brain dur ing the sec ond and third tri mes ter was in tro - duced in the early 1990s. It was the first prac ti cal ap pli - ca tion of 2D ul tra sound in three-di men sional cen tral ner - vous sys tem as sess ment (12). Transvaginal ob ser va tion of the fe tal brain of fered sagittal and co ro nal views of the brain from fetal parietal direction (1,13-17), whereas sonographic images through the fon ta nelles and/or the sagittal suture de picted brain struc tures in de tail. This method con trib uted to the pre na tal sono graphic as sess - ment of con gen i tal cen tral ner vous sys tem anom a lies and ac quired brain dam age in utero, es pe cially when com - pared with con ven tional trans ab dominal method. Trans vaginal 2D as sess ment of the fe tal brain has its lim i ta tions. With 2D transvaginal im ag ing of the fe tal brain, we can pro duce se ries of oblique sec tions from the same ul tra sound win dow by shift ing and chang ing the an gle of the trans ducer within the nar row space of the va gina. Some times, how ever, it is im pos si ble to ob tain in for ma tion on the whole brain when the fe tal head is in the oblique po si tion to the vag i nal trans ducer. For the ac - cu rate iden ti fi ca tion of the brain struc ture and data stor - age, transvaginal 2D ap proach to the fe tal brain re quires con sid er able scan ning time and skill ful use of the trans - ducer. Also, it oc ca sion ally causes moth ers dis com fort. On the other hand, trans vaginal 3D au to matic vol ume ac - qui si tion re quires only 1.84 to 6.07 sec onds for scan ning with out a shift and an gle-change of the trans ducer. By multiplanar im age anal y sis, it is pos si ble to dem on strate not only the sagittal and co ro nal sec tions but also the ax - ial sec tion of the brain, which can not be dem on strated from pa ri etal di rec tion by a con ven tional 2D transvaginal sonography. Par al lel slic ing and ro tat ing of brain vol ume data pro vides ob jec tive vi su al iza tion of in - ter nal mor phol ogy sim i larly to mag netic res o nance im - ag ing. Par al lel slices, which can not be dem on strated by con ven tional 2D sonography, are the ad van tage of 3D ul - tra sound. Since the brain structure can be ob served in any cut ting sec tion, an ab nor mal brain im age is com pa ra - ble with a nor mal im age in the ex actly same sec tion, and a lon gi tu di nal ob ser va tion in an ex actly same sec tion is also pos si ble. In short, this new method of 3D multiplanar anal y sis pro vides an in tel li gi ble in for ma - tion, has a short scan ning time, is easy to han dle, and causes al most no dis com fort to the mother. Ac cord ing to the an a tom i cal lo ca tion of the brain ves sels, the Wil lis ring, the source of the ce re bral ar ter - ies and trans verse si nus is lo cated at the ax ial plane of the head. But, there are many other brain ves sels which rise and fall within the sagittal and co ro nal planes. There fore, trans vagi nal ap proach to the fe tal brain from the fe tal pa - ri etal di rec tion plays an im por tant role in a brain cir cu la - tory as sess ment as well. Transvaginal 2D color/power Dopp ler angiography of the brain cir cu la tion shows the ce re bral ves sels and their lo ca tion (18,19). How ever, it is dif fi cult to pres ent the com plex 3D struc ture of the brain ves sels in a sin gle two-dimensional plane. Three-dimensional re con struc tion of the brain cir cu la - tion in ne o nate has been re ported (20). Com bi na tion of 247

Fig ure 2. Multiplanar im age anal y sis of the fe tal brain at 20 weeks of ges ta tion. Co ro nal (up per left), sagittal (up per right) and ax ial (lower left) planes of the brain are shown. Fig ure 3. Par al lel slic ing of each sec tion of the brain. Intracranial mor phol ogy can be shown in the same way with mag netic res o - nance im ag ing. 248

Fig ure 4. Brain cir cu la tion re vealed by 3D Dopp ler an gio - graphy. 3D power Dopp ler re con structed im age of brain cir cu - la tion can be seen from any di rec tion. These 4 fig ures show the y-axis ro ta tion of same 3D im age. sound may con trib ute to the fe tal brain cir cu la tory as - sess ment, since the 3D vas cu lar im age can be ro tated in any di rec tion, and the ves sels can be ob served from the fron tal, oc cip i tal, lat eral, oblique, pa ri etal, or bas i lar part of the brain (21). There are several problems with 3D color/ power Dopp ler, such as am bi gu ity of color/ power sig nals and long scan ning time. Be cause of these prob lems, the suc - cess rate of 3D angiograpy in our study was much lower than that of 3D B-mode scan. Fur ther de vice de vel op - ment and more clin i cal stud ies will be re quired to find a clin i cal sig nif i cance in the ap pli ca tion of 3D angiography. 3D vol ume im ag ing of fe tus brain cav i ties at 7, 9, and 10 weeks of ges ta tion was first re ported in 1995 by Blaas et al (22). They ex tracted the de tailed struc ture of pre ma ture hemi sphere, dien cephalon, mesencephalon, and rhombencephalon in vivo by 3D ul tra sound. There - af ter, they re ported vol ume es ti ma tion of the fe tal brain cav i ties in early fetuses (23). In low-birth-weight ne o - nates, a vol ume dif fer ence be tween up per and lower ven - tri cles due to the head po si tion was re ported by free hand 3D ul tra sound vol ume cal cu la tion (24). In this study, we Fig ure 5. The vol ume im ag ing and vol ume cal cu la tion of the lat eral ven tri cle (left) and choroid plexus (right) by 3D View (17 weeks of ges ta tion). Fig ure 6. Changing ap pear ance of the lat eral ven tri cle and choroid plexus dur ing preg nancy. 249

Fig ure 7. Parallel slicing in sagittal, coronal, and axial planes and multiplanar im age anal y sis in a fetus with asymmetrical ventriculomegaly and agenesis of the cor pus cal lo sum and interhemispheric cyst. Fig ure 8. Fe tal ab nor mal ity re vealed by 3D sur face mode. Left: a case with fron tal boss ing and low na sal bridge at 24 weeks of ges - ta tion; transabdominal scan. The co ro nal and lambdoid su tures are de tect able. Right: myelomeningocele at 18 weeks of ges ta tion. Fig ure 9. Vol ume im age and vol ume es ti ma tion of the ven tri cle in a fe tus with ventriculomegaly (the same case as in Fig. 7). chose to pro duce the vol ume im ages and es ti mated vol - ume of the lat eral ven tri cle and choroid plexus in fe tuses from 12 to 34 weeks of ges ta tion. Vol ume anal y sis of the struc ture of in ter est pro vides an in tel li gi ble eval u a tion of the brain structure in total and ob jec tive as sess ment of ab nor mal brain mor phol ogy, such as ventri culo megaly and intracranial oc cu py ing le sion. In con clu sion, transvaginal 3D sonography is an easy, non-invasive, and re pro duc ible method with lit tle tech ni cal re quire ments and a short sca n ning time which pro duces com pre hen si ble and ob jec tive in for ma tion. Sur - face re con struc tion, mul ti pla nar anal y sis, angiography, and vol ume im ag ing are use ful for the as sess ment of the fe tal skull for ma tion, intracranial mor phol ogy, cir cu la - tion, and vol ume es ti ma tion. Stor age/ex trac tion of raw vol ume data sets and off-line anal y sis of the fe tal head struc ture are quick and easy. There fore, in sono-evaluation of cen tral ner vous sys tem ab nor mal i - ties, neurospecialists can find the data ac quired by 3D vol ume much more ob jec tive than the data ob tained by con ven tional 2D im ages. 250

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