Intracranial Doppler studies of human fetuses were done mainly by observation of cerebral arteries; however, previous studies on the relationship between cerebral arterial flow and intracranial abnormalities failed to find any significant results.1–4
The intracranial major venous system might be affected by increased intracranial pressure because of the wall structure of the venous vessel and its anatomic location in the skull. The major veins, including the superior sagittal sinus, vein of Galen, and transverse and straight sinus, gather the cerebral venous streams and run along the convex hemispheres, fixed between two layers of dura mater. The venous flow of the dural sinus is the last segment of the blood circulation in the brain before it leaves the skull, indicating the importance of observing intracranial venous circulation. There has been little focus on fetal intracranial venous flow, possibly because of its anatomic location, an intracranial system, which is imaged poorly in the axial section of the brain by transabdominal sonography generally used. Recent advances in high-frequency transvaginal scanning enabled us to show detailed structures of the fetal brain in the sagittal and coronal planes.5–7 The combined transvaginal approach and color or power Doppler imaging has produced clear images of intracerebral vascularization.8 In the present study, transvaginal Doppler was used to investigate intracranial venous-blood-flow velocity waveforms.
The aim of this study was to investigate the physiologic blood-flow velocity waveform pattern of the fetal cerebral venous system during normal pregnancy and to evaluate abnormal venous flow patterns as a function of intracranial abnormality.
This study was done in the ultrasound units of our institutes from October 1996 to March 1998. The devices used were LOGIQ 400 and LOGIQ 500 (GE Yokogawa Medical Systems Ltd, Tokyo, Japan) with 6.5-MHz transvaginal transducers. Every sonographic observation was made by one examiner (R.K.P.). After explanation of the examination, women were examined in the dorsal lithotomy position with empty bladder, and scanning was done with thermal and mechanical indices of 0.6 or less, which were monitored on the screen. The duration of transvaginal Doppler exposure was less than 90 seconds. The images were saved to hard disk, and blood flow analyses were done off-line.
The first study included 63 normal fetuses in cephalic presentation from 20–40 weeks' gestation, in whom the intracranial cerebral veins were recognizable in the median7 section of the fetal head. All 63 fetuses were appropriate-for-gestational-age, singleton fetuses without complications. All were delivered at term and confirmed to be normal after birth. Doppler studies of internal cerebral veins, including the dural sinuses of the superior sagittal sinuses, veins of Galen, and straight sinuses, were done in the median sections of fetal brains through ultrasound windows of the fontanel or the sagittal suture. To analyze the venous-blood-flow velocity waveforms, the venous index was defined as maximum minus minimum velocity divided by maximum velocity. A t test for paired data was used for statistical evaluation.
The next study was done to evaluate changes in venous index during pregnancy in the superior sagittal sinus, the most accessible cerebral vein by transvaginal approach, which can be depicted in the median and oblique sections. We examined a total of 201 fetuses from noncomplicated gestations at 20–40 weeks delivered at term and without postnatal abnormalities. Venous-flow velocity waveforms of 12 cases complicated by intracranial structural abnormalities between 20 and 40 weeks' gestation were also studied.
During normal pregnancies, pulsatile patterns of the three dural venous flows were observed in all fetuses. The internal cerebral vein had pulsatile patterns in 30 fetuses (47.6%) and the remaining 33 fetuses showed continuous flat patterns. Color Doppler images in the median section and flow patterns of each vein are shown in Figure 1. Thirty fetuses with pulsatile patterns in the internal cerebral vein during the three periods of 20–27, 28–31, and 32–40 weeks' gestation had increased detection rates of pulsations of 31.5%, 40.9%, and 68.2%, respectively. For 30 fetuses with pulsations in internal cerebral veins, mean venous indices in each period were 0.20, 0.25, and 0.22, respectively (Table 1). When the venous pulsations among three dural veins were compared, the vein of Galen had a venous index of 0.31, which was significantly lower than that of the superior sagittal sinus (0.39) and the straight sinus (0.36) (Table 2), indicating that the venous index increases as venous flow approaches its final segment. Mean venous indices in the three gestational periods were 0.36, 0.41, and 0.40 in the superior sagittal sinus, 0.30, 0.35, and 0.29 in the vein of Galen, and 0.34, 0.40, and 0.35 in the straight sinus. Although all four cerebral veins showed higher venous indices in the period from 28–31 weeks' gestation compared with those before and after that period, comparisons were not statistically significant.
The regression analysis of the venous index of the superior sagittal sinus as a function of gestational age, a statistically significant regression line (P < .001) was calculated (Figure 2), indicating stability of venous pulsatile waveform patterns during normal pregnancy.
There were 12 fetuses with intracranial abnormal structures, including two cases of cerebellar hypoplasia, two of mild ventriculomegaly, one of excencephaly, one of holoprosencephaly, one of brain atrophy, one of unclassified brain anomaly, three of hydrocephalus, and one of craniosynostosis. Superior sagittal sinuses were recognizable in ten fetuses, except for the cases with excencephaly and the unclassified brain anomaly. Six cases of cerebellar hypoplasia, mild ventriculomegaly, holoprosencephaly, and brain atrophy showed normal pulsatile patterns, whereas the three cases with hydrocephalus and one with craniosynostosis had constant flat waveforms. The sonographic appearance of intracranial abnormalities and the venous waveforms of superior sagittal sinuses in those four cases are shown in Figure 3 and the cases are summarized in Table 3.
Case 1 was referred to us for symmetric hydrocephalus. At 30 weeks' gestation, the superior sagittal sinus had a normal pulsatile pattern with a venous index of 0.38; however, the hydrocephalus was exacerbated during the next 2 weeks with rapidly increasing biparietal diameter and disappearance of pulsation in the superior sagittal sinus at 32 weeks. Case 2, asymmetric hydrocephalus, was referred at 35 weeks. An enlarged right ventricle, a deformed left ventricle, and a large frontal cystic area connecting with the right ventricle were found. The superior sagittal sinus had a flat flow pattern from the first examination. Postnatal diagnosis was asymmetric hydrocephalus and agenesis of the corpus callosum. Case 3, asymmetric hydrocephalus with a large parietal cystic area fused with the right ventricle and cerebellar hypoplasia, was referred to us at 30 weeks. The superior sagittal sinus had a flat pattern. Postnatal diagnosis was asymmetric hydrocephalus with agenesis of the corpus callosum, parietofrontal cortical aplasia, and cerebellar hypoplasia. In case 4, craniosynostosis was suspected at 19 weeks because of an abnormal skull shape. The cerebrum, lateral ventricles, corpus callosum, and septum pellucidi were deformed due to the abnormal shape of the calvarium. Mild ventriculomegaly was also found. Although the waveforms of the superior sagittal sinus had a pulsatile pattern with a venous index of 0.35 at 20 weeks, pulsation disappeared at 25 weeks. Postnatal diagnosis was Apert syndrome. All four cases had abnormal head structures associated with increased intracranial pressure. There was no growth restriction or chromosomal aberration. All cases had normal blood-flow velocity waveforms in the umbilical and middle cerebral arteries.
In our study of normal pregnancies, the internal cerebral vein, which is located more distal and closer to venules, had no pulsatile patterns or lower amplitude pulsations than dural sinuses. Among dural sinuses, the vein of Galen has lower amplitude pulsations than the other dural sinuses, which indicates that the amplitude of intracranial venous pulsations might increase as the flow runs from the periphery toward the proximal portion. Similar results were reported in newborns.9 Intracranial venous pulsations can be explained as passive pulsations transmitted from the heart or brain. The fact that brain pulsations exist was known, and a pulsatile brain can be seen after craniotomy. Brain pulsations associated with cardiac cycles were proved by studying epidural pulse waves,10 cerebrospinal pulse waveforms,11,12 and anterior fontanel pulsations.13,14 Hirai and colleagues10 investigated the origin of epidural-pressure pulse waveforms. They measured the epidural-pulse wave and pressure waveforms of the cortical artery and vein simultaneously and found that pulsatile arterial blood flow into the brain can generate brain pulsations and that the cortical venous pulse can be affected passively by brain pulsations.10 The cerebral veins can also have a passive pulsation directly transmitted from the heart. Whether cerebral venous flow is influenced by brain pulsations or heartbeat, it is reasonable to suggest that the amplitude of venous pulsations increases from the distal to the proximal portion of cerebral venous circulation, as our results showed.
Because of the anatomic location of intracranial veins, the median section of the brain is the most practical section that can show multiple veins simultaneously, but it is not always possible to view the median section of the fetal brain because of head position and movement. Among fetal intracerebral veins imaged by transvaginal scan, the superior sagittal sinus is the most accessible because of its proximity to the vaginal transducer. This sinus can be approached in the median and oblique sections. Considering the results of the first study and easy detection of the superior sagittal sinus, we conducted further examination of that sinus, the results of which can be applied to the dural sinuses. Our results showed the stability of major venous pulsations during pregnancy and we suggest that venous pulsation is a good indicator of the intracranial condition of fetuses.
The most controversial point in evaluation and treatment of fetuses with intracranial abnormalities is how much the intracranial condition affects brain development. Transvaginal B-mode ultrasound showed intracranial abnormal morphology, including obliteration of the subarachnoid space by hydrocephalus.15 Several reports on Doppler assessment of arterial circulation in hydrocephalic cases attempted to evaluate intracranial conditions. Although the first report showed progressive elevation of pulsatility index of the internal carotid artery with development of ventriculomegaly,16 the reports thereafter found no typical waveform-pattern relationship between arterial flow pattern and hydrocephalus.1–3 Wladimiroff and colleagues4 reported that color Doppler flow mapping provided only limited information on intracranial structural abnormality.
The veins, which have thin walls, are easily affected by outside pressure. The intracranial dural sinuses, such as the superior sagittal sinus, are outside the convexity between hemispheres; therefore, venous circulation can be subject to a larger effect than arterial circulation because of the increased pressure around it.
Our four cases with continuous flat patterns in superior sagittal sinuses had common intracranial conditions. Severe hydrocephalus and craniosynostosis cause increased intracranial pressure. In two cases we observed the disappearance of pulsatile patterns that were initially detected. That phenomenon is similar to the anterior fontanel skin pulsations that are usually seen in normal neonates but are not visible in hydrocephalic neonates because the anterior fontanel is bulging. Besides elevated intracranial pressure, another important factor regulating transmission of brain pulsations to the brain surface is in the subarachnoid space, which functions as a buffer zone. The superior sagittal sinus is within the dura mater that covers the buffer zone, which absorbs pressure transmitted to it by moderately increased intracranial pressure. When that pressure increases, it progressively obliterates this buffer zone; thus the pressure stretches the dura and sinus and brain pulsations are not transmitted to them. That explanation might account for the flattered venous waveforms in the sinus. Kuramoto and colleagues14 reported that waveforms of intracranial pressure were influenced by intracranial constituents and compliance of the container, so disappearance of venous pulsations might indicate high intracranial pressure.
Despite changes in venous flow, all four cases had normal waveform patterns in the middle cerebral arteries, so intracranial venous waveforms might indicate more precise or earlier intracranial pressure changes than arterial waveforms.
Because of the easy detection of the superior sagittal sinus and its stable flow pattern during pregnancy, assessment of it could be introduced easily and accepted in clinical practice. Doppler evaluation of the intracranial venous system might have a value in clinical determination of the prognoses of intracranial abnormalities. Further studies are needed of the relationship between the fetal cerebral-venous-flow velocity patterns and neurologic prognoses of infants with brain abnormalities.
1. van den Wijngaard JA, Reuss A, Wladimiroff JW. The blood flow velocity waveform in the fetal internal carotid artery in the presence of hydrocephaly. Early Hum Dev 1988;18:95–9.
2. Kirkinen P, Muller R, Baumann H, Briner J, Lang W, Huch R, et al. Cerebral blood flow velocity waveforms in hydrocephalic fetuses. J Clin Ultrasound 1988;16:493–8.
3. Mai R, Rempen A, Kristen P. Color flow mapping of the middle cerebral artery in 23 hydrocephalic fetuses. Arch Gynecol Obstet 1995;256:155–8.
4. Wladimiroff JW, Heydanus R, Stewart P. Doppler colour flow mapping of fetal intracerebral arteries in the presence of central nervous system anomalies. Ultrasound Med Biol 1993;19:355–7.
5. Monteagudo A, Reuss ML, Timor-Tritsch IE. Imaging the fetal brain in the second and third trimesters using transvaginal sonography. Obstet Gynecol 1991;77:27–32.
6. Monteagudo A, Timor-Tritsch IE, Moomjy M. In utero detection of ventriculomegaly during the second and third trimesters by transvaginal sonography. Ultrasound Obstet Gynecol 1994;4:193–8.
7. Timor-Tritsch IE, Monteagudo A. Transvaginal fetal neurosonography: Standardization of the planes and secretions by anatomic landmarks. Ultrasound Obstet Gynecol 1996;8:42–7.
8. Pooh RK, Aono T. Transvaginal power Doppler angiography of the fetal brain. Ultrasound Obstet Gynecol 1996;8:417–21.
9. Taylor GA. Intracranial venous system in the newborn: Evaluation of normal anatomy and flow characteristics with color Doppler US. Radiology 1992;183:449–52.
10. Hirai O, Handa H, Ishikawa M. Intracranial pressure pulse waveform: Considerations about its origin and methods of estimating intracranial pressure dynamics. No to Shinkei 1982;34:1059–65.
11. Hamer J, Alberti E, Hoyer S, Wiedemann K. Influence of systemic and cerebral vascular factors on the cerebrospinal fluid pulse waves. J Neurosurg 1977;46:36–45.
12. Nakamura K, Urayama K, Hoshino Y. Lumbar cerebrospinal fluid pulse wave rising from pulsations of both the spinal cord and the brain in humans. Spinal Cord 1997;35:735–9.
13. Hayashi T, Shirozu T, Shojima T, Watanabe M, Takagi S. Analysis of anterior fontanelle pulsation wave. 1. Relationship between the pulsation wave and intracranial pressure. No to Shinkei 1976;28:271–7.
14. Kuramoto S, Moritaka K, Hayashi T, Honda E, Shojima T. Non-invasive measurement in intracranial pressure and analysis of the pulse waveform. Neurolog Res 1986;8:93–6.
15. Pooh RK, Nakagawa Y, Nagamachi N, Pooh KH, Nakagawa Y, Maeda, K, et al. Transvaginal sonography of the fetal brain: Detection of abnormal morphology and circulation. Croat Med J 1998;39:147–57.
© 1999 The American College of Obstetricians and Gynecologists
16. Degani S, Lewinski R, Shapiro I, Sharf M. Decrease in pulsatile flow in the internal carotid artery in fetal hydrocephalus. Br J Obstet Gynaecol 1988;95:138–41.