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ARTICLES Correlation Between 3D Transvaginal First-Trimester Neuroimaging and Embryonic Development According to Carnegie Stadiation
GABRIELE TONNI, MD, PhD* D. AZZONI, MD* G. CENTINI, MD ALESSANDRO VENTURA, MD*

Sonoembryology is a recent application of sonography that systematically examines the developmental stages of the embryo and fetus. In this study, the authors found correlations between 3D transvaginal first-trimester neuroimaging and embryonic development, as described by the Carnegie staging system. Forty healthy, singleton pregnant women with known last normal menstrual period were enrolled and examined prospectively by serial weekly 3D transvaginal sonography between weeks 6.5 and 12 of gestation to assess development of embryonic and early fetal brain structures in vivo. The rhombencephalic cavity, visible from week 7 onward, was initially in the superior position in the embryo head. The mesencephalic and diencephalic cavities were identified by weeks 8 to 9. The cerebral hemispheres and the choroid plexuses of the lateral ventricles were regularly visualized from week 9 onward. The cerebellum started to be distinguishable by week 10. The shape and the size of the different brain structures and their relation to each other changed during the embryonic and early fetal period. The 3D sonographic description of embryo brain development matched that of classical embryology. Sonoembryology has great potential for detecting anomalous central nervous system development. Key words: embryo, 3D neuroimaging, transvaginal sonography, sonoembryology, Carnegie stages

From *Guastella Civil Hospital, Guastella, Italy, and University of Siena, Italy. Correspondence: Gabriele Tonni, MD, PhD, Guastella Provinical HospitalASL, Via Donatori Sangue 2, Guastalla, Italy. E-mail: Tonni .Gabriele@ausl.re.it. DOI: 10.1177/8756479308317419

Embryologists divide development from fertilization to 10 weeks (postmenstrual) into 23 different stages, according to the Carnegie staging system.1 Classification is based on external form and development of the organ systems analyzed by

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light microscopy. The stages are delineated through the development of structures, not by size or the number of days of development. The system covers only the first 60 days of development; at that point, the term embryo is replaced with the term fetus. The Carnegie stages provide a universal system of staging and comparing the embryonic development of most vertebrates, whereas other systems (i.e., Hamburger-Hamilton) are used in the chick.2 Franklin P. Mall (18621917) made a critical contribution to the Carnegie classification by basing his staging scheme on morphologic characteristics rather than age and size, which proved to be a poor method to organize embryos.3 Early research on the human embryo used horizons to track development. In 1996, DuBose4 was the first to attempt a correlation between transabdominal sonographic images and embryo development week by week, including Streeters horizons in approximation with the week, and dated gestation from the last normal menstrual period (LNMP).5 Instead of using greatest embryo length (EGL), crown rump length (CRL) was used, and CRL is proven to be the most accurate measurement from the sixth week (34 days). Cyr et al.6 first published the sonographic identification of the fetal rhombencephalon. The introduction of high-frequency transvaginal sonography has considerably improved the study of early gestation, allowing visualization of embryo development and detection of many central nervous system (CNS) malformations in the first trimester of pregnancy.7,8 Timor-Tritsch7,9 first demonstrated the utility of scanning with a high-frequency transvaginal probe for an early systematic survey of embryo and fetal anatomy, using textbooks and atlases for comparative purposes. He described first the single ventricle, or primitive rhomboencephalic cavity, and the other cerebral structures that appear progressively from weeks 7 to 12 of gestation. In 1990, Timor-Tritsch10 coined the word sonoembryology to underline the potential of this sonographic technique in the first trimester of pregnancy. Blaas et al.1113 demonstrated that structures measuring very few millimeters can be imaged in vivo in 3D with a quality that resembles the meticulously assembled plaster figures seen in embryo laboratories. The aim of the present,

prospective longitudinal study was to visualize the development and volume of embryo structures and confirm the correlation described between 3D transvaginal neuroimaging and Carnegie stages, using direct, online calculation software included in the sonographic equipment.

Materials and Methods

Forty women with spontaneous, uncomplicated, singleton pregnancies and a mean maternal age of 28 2.3 years were recruited for a longitudinal 3D transvaginal ultrasound (3DTVUS) study in which the relationship between embryo brain development, as described by the Carnegie system, and 3DTVUS neuroimaging was evaluated. The women had known their LNMP, and dating of gestation was thus based on LNMP. Women with a difference > 7 days between LNMP and CRL dating were not included in the study. The Hospital Health Board Committee approved the study design, and written consent was obtained from all patients. Embryos were examined weekly, starting at week 6.5 and ending at week 12 of gestation. The women were subject to follow-up until delivery, and none had maternal or obstetric complications. The fetuses were all healthy at birth, as documented by a oneand five-minute Apgar score 7 and umbilical cord artery pH >7.20. There were no admissions to the neonatal intensive care unit (NICU), and all babies were sent home on day 3. 3DTVUS sonoembryology took 15 to 20 minutes. Two high multifrequency (58 MHz) 3D transvaginal probes were used: a SA 9900 Kretztechnike and a General Electric 730 Expert. These probes have an axial resolution of 0.4 mm and a lateral resolution of 0.8 mm. Data acquisition for 3D volumetric reconstruction took an average of 1.8 seconds, and 6 to 12 volumes per second were recorded in the region of interest. Mechanical and thermal indexes were set according to US Food and Drug Administration recommendations. Volumetric 3D reconstruction was started when the embryo was not moving so that errors would be avoided in volume measurement. Sagittal and coronal planes were found according to the scanning sections classification of

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FIGURE 1.

Three-dimensional volume calculation of the diencephalic cavity using VOCAL.

Monteagudo and Timor-Tritsh.14 These sections, obtained by transvaginal sonography, radiate in a fan-like manner from the small region of the anterior fontanelle. Unlike classical coronal and sagittal sections, which are parallel to each other, they are oblique sections. Coronal sections include frontal sections 1 and 2 anterior to the corpus callosum, midcoronal sections 1 and 2 passing through the body of the lateral ventricle, midcoronal section 3 through the atrium of the lateral ventricle, and occipital sections 1 and 2 passing through the posterior fossa and its contents as well as the posterior horns of the lateral ventricles, the most posterior being occipital section 2. Sagittal sections include the median oblique section 1 and the more lateral section 2 through the insula and lateral sulcus. In

sagittal sections, the length and height or depth of the different brain structures were measured, whereas the width was done for the coronal section. Volumetric data of the brain cavity, choroid plexuses, and cerebellar hemispheres were obtained directly online using the VOCAL (Volume Calculation) software installed in the sonography equipment. This software allows manual drawing of the contours of the anatomic structures and calculates the volume in mm (Figure 1).

Results
6.5 to 7 weeks (Carnegie stages 1517). CRL ranged from 8 to 14 mm (Table 1). The cavity of the rhombencephalon, or future fourth ventricle, was

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TABLE 1. Correlation Between Carnegie Stages and 3D Transvaginal Neuroimaging Gestational Age, Weeks 6.57 Carnegie stage CRL, mm Transverse diameter of the head, mm Single ventricle Mesencephalon Diencephalon and third ventricle Choroid plexuses of the lateral ventricles Cerebral hemisphere Cerebellar hemisphere Cerebral falx Cisterna magna Cavum septi pellucidi 1517 914 V NAV NAV NAV NV NV NV NV NV 8 1820 1621 68 V V NAV NAV NV NV NV NV 9 2122 2229 912 V V V V NAV V NV NV 10 23 >30 13 V V V V V V NAV NAV 1112

1520 V NV V V V V V V

V, visible; NV, not visible; NAV, not always visible; CRL, crown rump length.

FIGURE 2. Embryo at week 6.5. The single rhombencephalic ventricle (SV) is clearly imaged.

visible from 6.5 weeks onward in coronal occipital section 1 and median sections (Table 1, Figure 2). It was the largest cavity in the cranial pole of the embryo with a pyramid-like shape and a mean length of 3.7 mm (Table 2). Mean volumes ranged from 8.5 to 20 mm. At 7 weeks and 5 days, in 20% of cases, it was possible to see the diencephalic cavity (future third ventricle), with mean volumes of

2.5 to 5 mm, and a curved, mesencephalic cavity anterior to it, with mean volumes of 0.8 to 5.7 mm (Table 3, Figure 3). In midcoronal sections, the dividing telencephalon (future cerebral hemispheres with lateral ventricles) could be recognized as a Y-shaped anechogenic structure. 8 weeks (Carnegie stages 1820). CRL ranged from 16 to 21 mm, and head transverse diameter measured 6 to 8 mm (Table 1). The prosencephalic, mesencephalic, and rhombencephalic cavities were visible from 8 weeks + 3 days (Table 1) as wide anechogenic areas in the head, with mean volumes as reported in Table 3. The mesencephalon, initially situated in the anterior part of the embryonic head, was now in the superior position and clearly visible in sagittal view (Figure 4), because of deflection of the brain as described by embryologists (Carnegie stages 1618). The mean length of the diencephalic cavity or future third ventricle was 2.2 mm (1.3), increasing to 3.5 mm (1.4) at 10 weeks. Mean width was 1.1 mm (0.6), decreasing to 1 mm (0.8) at 10 weeks. Mean height was 1.1 mm (0.7) and 2.0 mm (0.6) at 10 weeks (Table 2). Mean volume of the diencephalic cavity was 6.5 to 8 mm (Table 3). The cerebral hemispheres were detectable in only 40% of cases, and choroid plexuses of the lateral ventricles could not yet be visualized (Table 1).

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TABLE 2. Measurement of the Main Brain Structures, Expressed in mm as Mean Values SD Gestational Age, Weeks 6.57 Rombencephalon Length Width Depth Cerebellum Width Height Mesencephalon Length Width Height Diencephalon Length Width Height Lateral choroid plexuses Length Width Height 3.7 1.5 2.0 1.4 1.6 1.2 8 3.8 1.5 3.0 1.5 2.0 1.0 9 3.9 1.6 3.8 1.6 2.5 1.0 10 4.0 1.5 4.2 1.5 2.8 1.0 5.8 2.5 1.8 0.8 2.7 1.1 1.2 0.6 1.2 0.6 2.0 1.2 1.2 0.6 1.1 0.7 2.8 1.2 1.3 0.6 1.3 0.5 2.2 1.3 1.1 0.6 1.1 0.7 2.9 1.2 1.3 0.5 1.4 0.5 2.5 1.3 1.1 0.7 1.1 0.7 2.7 1.3 1.3 0.9 1.8 1.2 3.1 1.1 1.4 0.5 1.5 0.5 3.5 1.4 1.0 0.8 2.0 0.6 3.6 1.9 1.6 0.8 2.2 1.2 7.1 3.5 3.1 1.4 3.5 2.0 11 4.3 1.5 4.5 1.6 3.0 1.0 6.8 2.7 2.0 0.6 3.3 1.0 1.5 0.5 1.6 0.6 1112 4.4 1.5 4.5 1.6 3.2 1.0 8.0 2.8 2.4 0.7 4.0 1.9 1.7 0.5 2.0 0.6 0.8 0.5 12.5 4.5 4.4 1.6 5.2 1.9

TABLE 3. Mean Volumes of Mesencephalon, Diencephalons, Rhombencephalon Cavities, Lateral Ventricles, and Lateral Choroid Plexuses at Different Gestational Weeks Embryonic Period, Weeks 6.57 Carnegie stages CRL, mm Transverse diameter of the head, mm Cavity of mesencephalon, mean volume, mm Cavity of diencephalon, mean volume, mm Lateral ventricles, mean volume, mm Lateral choroid plexuses, mean volume, mm CRL, crown rump length. 1517 914 0.85.7 2.55 8 1820 1621 5 68 6.58 9.560 9 2122 2229 9 920 8 10 23 >30 3 20 7.5 FIGURE 3. Embryo at week 7the stage of three vesicles and the two isthmus are visible within the cephalic pole: prosencephalic (P), mesencephalic (M), and rhombencephalic (R) cavities (rostro-caudal direction). VD, vitelline ductus; YS, yolk sac.

70200 >350 40120 >280

9 weeks (Carnegie stages 2122). CRL was 22 to 29 mm with a head transverse diameter of 9 to 12 mm (Table 1). All embryos showed lateral ventricles containing choroid plexuses (Table 1). They

were best seen in sagittal oblique section 1, with mean volumes varying from 70 to 200 mm at this gestational age (Table 3). Mean length, width, and height were 2.7, 1.3, and 1.8 mm, respectively (Table 2). In midcoronal section 2, the characteristic

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FIGURE 5. Transverse section of embryo at week 9.5. The choroid plexuses (CP) of the lateral ventricles (LV) with their club shape, with sharp extremity at the level of the frontal horn, are visualized together with the falx cerebri (F). FIGURE 4. Embryo at week 8 in sagittal section: the prosencephalic (P), mesencephalic (M), and rhombencephalic (R) cavities and their isthmus are shown. A comparison with the dimension of the adjacent yolk sac (YS) can be made.

club shape became apparent from stage 20 (Figure 5). Mean volumes of lateral choroid plexuses were 40 to 120 mm (Table 3). In the oblique section, C-shaped cerebral hemispheres were always detectable (Table 1), with the cortex appearing as a hypoechogenic mass. The mesencephalic cavity was still wide with distinct isthmus rhombencephali and isthmus prosencephali. During stage 22, the cerebral hemispheres covered about three quarters of the diencephalons. In 15 embryos, we identified the rhomboencephalic cavity dividing into the metencephalon (future cerebellum and pons) and myelencephalon (medulla oblongata). 10 weeks (Carnegie stage 23). CRL was about 30 mm and head transverse diameter 13 mm (Table 1). The lateral ventricles in midcoronal section 2 and median sagittal sections were almost filled by the large choroid plexuses, which occupied the anterior horn and diencephalic cavity, with mean volumes >280 mm (Table 3). The diencephalon was often hidden by the cerebral hemispheres, so it became difficult to measure its length, height, and volume. The falx began developing

along the midline in line with embryologic staging (Carnegie stage 23). The cerebellar hemispheres were always detected and measured (Tables 2 and 3, Figure 6). They appeared separated along the midline and joined at the velo medullare. 1112 weeks (early fetal period). The transverse diameter of the head was 15 mm at 11 weeks and 20 mm at 12 weeks. The cerebral hemispheres were the major visible structures. Mean length, width, and height of the lateral ventricle choroid plexuses were 12.5, 4.4, and 5.2 mm, respectively (Table 2). The third ventricle was too narrow to be visualized at this stage, but the thalamic-diencephalic structures were clearly visible. In coronal occipital section 2, cerebellar hemispheres joined along the midline. The rhombencephalic cavity was detectable from weeks 7 to 12. At week 12, the cerebellar hemispheres and the cisterna magna (Figure 7) were easily imaged, and the cavum septi pellucidi was visualized as a box-like cavity near the anterior horn and anterior to the diencephalon (Table 1).

Discussion
The pioneering works of Timor-Tritsch7,10 and Cyr et al.6 have allowed sonoembryology to be used

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FIGURE 6. Coronal section of the fetus at week 11 (early fetal period): hyperechogenic superior and inferior cerebellar hemispheres are visible in the occipital region together with anechogenic cisterna magna.

for a targeted fetal examination, demonstrating a close correlation between sonographic images and biologic development of the human brain. The possibility of detecting the single ventricle was also emphasized by the work of Cullen et al.,15 Takeuchi,16 and Achiron and Achiron,17 who interpreted the single ventricle at week 7 as the forebrain, which divided by week 8. Blaas et al.1113,18,19 confirmed the conclusions by Timor-Tritsch7,10 and demonstrated in different articles the correspondence between the sonographic description of brain development and that of Carnegie staging. In 1995, 3D sonography was introduced, hosting further development in

sonoembryology and enhancing recognition of developmental defects.11,13,2022 In conclusion, our observational study confirmed that the rhombencephalic, mesencephalic, and prosencephalic cavities can be visualized by weeks 7 to 8 with 3D sonography. The cerebral hemispheres were visible from week 9 onward, starting their development at about week 6 (Carnegie stage 10).1 With 2D sonography, the rhomboid cavity or single ventricle becomes apparent at Carnegie stage 14,1 and its length, using CRL as an independent variable, shows a rapid increase to 18 mm, followed by a less rapid increase to 22 mm. This may be due to the deflection of the embryo brain caused by varying

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visible by 12 weeks. The posterior horns of the lateral ventricles were not visualized because they were still undeveloped at the early stage.

References
1. ORahilly R, Muller F: The Embryonic Human Brain: An Atlas of Developmental Stages. 2nd ed. Toronto, Wiley-Liss, 1999. 2. Carnegie stages. Available at: http://en.wikipedia.org/wiki/ Carnegie_stages. 3. UNSW embryology: about the Carnegie Institute. Available at: http://embryology.med.unsw.edu.au/wwwhuman/ Stages/carnegie.htm. 4. DuBose TJ: Fetal Sonography. Philadelphia, W. B. Saunders, 1996. 5. Bartone JC: Application of the Streeter developmental horizons for the classification of chick, frog and pig embryos in teaching and research. Trans Am Microsc Soc 1960;3: 253256. 6. Cyr DR, Mack LA, Nyberg DA, Shepard TH, Shuman WP: Fetal rhombencephalon: normal US findings. Radiology 1988;166:691692. 7. Timor-Tritsch I: A close look at early embryonic development with the high-frequency transvaginal transducer. Am J Obstet Gynecol 1988;159:676681. 8. Fujiwaki R, Hata T, Hata K, Kitao M: Intrauterine ultrasonographic assessments of embryonic development. Am J Obst Gynecol 1995;173:17701174. 9. Timor-Tritsch I: Transvaginal ultrasonographic definition of the central nervous system in the first and early second trimester. Am J Obst Gynecol 1991;164:497503. 10. Timor-Tritsch I: Sonoembryology: an organ-oriented approach using a high-frequency vaginal probe. J Clin Ultrasound 1990;18:286298. 11. Blaas HG, Eik-Nes SH, Kiserud T, Hellevik LR: Three dimensional imaging of the brain cavities in human embryos. Ultrasonography Obstet Gynecol 1995;5:228232. 12. Blaas HG, Eik-Nes SH: Advances in the imaging of embryonic brain. Croatian Med J 1998;39:128131. 13. Blaas HG, Eik-Nes SH, Berg S, Torp H: In-vivo three dimensional ultrasound reconstructions of embryos and fetuses. Lancet 1998;352:11821186. 14. Monteagudo A, Timor-Tritsch IE: Antenatal brain assessment, in Kurjak A (ed): Textbook of Perinatal Medicine. New York, Parthenon, 1998, pp 281286. 15. Cullen MT, Green J, Whethem J, Salafia C, Gabrielli S, Hobbins JC: Transvaginal ultrasonographic detection of congenital anomalies in the first trimester. Am J Obstet Gynecol 1990;163:466476. 16. Takeuchi H: Transvaginal ultrasound in the first trimester of pregnancy. Early Hum Dev 1992;29:381384. 17. Achiron R, Achiron A: Transvaginal ultrasonic assessment of the early fetal brain. Ultrasound Obstet Gynecol 1991;1: 336344.

FIGURE 7. Hyperechogenic cerebellar hemispheres with the anechogenic cisterna magna at 12 weeks (early fetal period).

rates of growth of its compartments and by deepening of the pontine flexure (Carnegie stages 1618).1 The diencephalic cavity appeared slit-shaped in older embryos and in the late embryologic period because of growth of the dorsal and ventral thalami. This change in shape explains the decreasing volume of the cavity. The low rate of visualization of the choroid plexuses of the lateral ventricle before week 9 and the cerebellum before week 10 may be related to our learning curve. The cerebellum and the cerebral hemispheres start to develop at 32 to 33 days postfertilization (Carnegie stages 1314), and the choroid plexuses of the lateral and fourth ventricles develop 8 weeks after the last menstrual period (Carnegie stages 1618).1 Growth of the cerebellar hemispheres further restricted the volume of the fourth ventricle, and the rhombencephalic cavity therefore did not increase in volume despite the rapid growth of the brain. With their progressive migration from the lateral recesses to the midline, the choroid plexuses of the fourth ventricle could not be demonstrated by us, in contrast to Blaas and Eik-Nes12 and Blaas et al.19 From week 10 onward, the falx, the cisterna magna, and the cavum septi pellucidi were always

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18. Blaas HG, Eik-Nes SH, Kiserud T, Hellevik LR: Early development of forebrain and midbrain: a longitudinal study from 7 to 12 weeks of gestation. Ultrasound Obstet Gynecol 1994;4:183192. 19. Blaas HG, Eik-Nes SH, Kiserud T, Hellevik LR: Early development of the hindbrain: a longitudinal study from 7 to 12 weeks of gestation. Ultrasound Obstet Gynecol 1995;5:151160. 20. Bonilla-Musoles F, Raga F, Osborne NG, Blanes J: Use of three-dimensional ultrasonography for the study of

normal and pathologic morphology of the human embryo and fetus: preliminary report. J Ultrasonography Med 1995;14:757765. 21. Hata T, Aoki S, Manabe A, Hata K, Miyazaki K: Three dimensional ultrasonography in the first trimester of human pregnancy. Hum Reprod 1997;12:18001804. 22. Hata T, Aoki S, Hata K, Miyazaki K, Akahane M, Mochizuki T: Three dimensional ultrasonographic assessment of fetal development. Obstet Gynecol 1998;91: 218223.

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Article: Correlation Between 3D Transvaginal FirstTrimester Neuroimaging and Embryonic Development According to Carnegie Stadiation Authors: Gabriele Tonni, MD, PhD D. Azzoni, MD G. Centini, MD Alessandro Ventura, MD Category: Obstetric (OB) Credit: 1.0 Objectives: After studying the article titled Correlation Between 3D Transvaginal First-Trimester Neuroimaging and Embryonic Development According to Carnegie Stadiation, you will be able to: 1. Describe the application of sonoembryology. 2. Provide a correlation between 3D transvaginal firsttrimester neuroimaging and embryonic development. 3. Discuss the sonographic appearance at each developmental stage.
c. 2 minutes d. 5 minutes 7. At 6.5 to 7 weeks, the rhombencephalon has which of the following appearance? a. Pyramid-like shape b. Elliptically shaped c. y shaped d. Club shaped By 8 weeks in the study, the cerebral hemispheres were detectable in what percentage of cases? a. 20% b. 40% c. 60% d. 80% By 9 weeks, the cerebral hemispheres were always detectable by what shape? a. Pyramid-like shape b. Elliptically shaped c. y shaped d. c shaped By sonography, the falx was visualized as beginning to develop along the midline in line with embryological staging at what week? a. 8 b. 9 c. 10 d. 11 Detecting the single ventricle as the forebrain can be first evaluated at which weeks of development? a. 45 b. 78 c. 1011 d. 1314 With 3D sonography, which of the following cavities can be identified at 7 to 8 weeks? a. Rhomboencephalic b. Mesencephalic c. Interpeduncular d. Prosencephalic The lateral ventricles are not well visualized for measuring at which of the following weeks? a. 7 b. 8 c. 9 d. 10 Which of the following best describes the cerebellar hemisphere appearance? a. Homoechogenic b. Hyperechogenic c. Hypoechogenic d. Anechogenic At 12 weeks, which of the following structures provides the largest length? a. Rhombencephalon b. Mesencephalon c. Cerebellum d. Lateral choroid plexus

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Stages of development according to the Carnegie staging system are based on which of the following? a. External form and development of the organ system analyzed by light microscopy b. Sonographic characterization of brain development c. X-ray delineation of embryonic size d. Postmortem evaluation of age, development, and size DuBose first correlated transabdominal sonographic images with embryo development in what year? a. 1969 b. 1974 c. 1988 d. 1996 Timor-Tritsch used the word sonoembryology to describe which of the following? a. Evaluation of fetal chick embryology b. Use of sonographic techniques in the first trimester of pregnancy c. Sonographic evaluation of organ systems d. Comparative description of central nervous versus organ system development What length of scan time was needed to perform the 3D sonoembryology study? a. 510 b. 1015 c. 1520 d. 2025 The axial and lateral resolution of the equipment used for the study was which of the following? a. 0.2 and 0.1 mm b. 0.4 and 0.8 mm c. 1.5 and 2.2 mm d. 3.1 and 5.0 mm Data acquisition for 3D volumetric reconstruction took how long for the study described? a. 2 seconds b. 30 seconds

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