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ORIGINAL RESEARCH |
From the Department of Obstetrics and Gynecology, Clinical Research Institute, National Zentsuji Hospital, Kagawa, Japan; Department of Neurosurgery, National Kagawa Children’s Hospital, Kagawa, Japan; Department of Obstetrics and Gynecology, University of Tokushima, Tokushima, Japan.
Address reprint requests to: Ritsuko Pooh, MD Department of Obstetrics and Gynecology Clinical Research Institute National Zentsuji Hospital 2-1-1, Senyucho Zentsuji City, Kagawa #765-8507 Japan E-mail: rkpooh{at}jun.ncvc.go.jp
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Abstract |
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Methods: Internal cerebral veins and the three dural sinuses, those of the superior sagittal sinus, vein of Galen, and straight sinus, were examined in normal cephalic-presenting fetuses of 20–40 weeks’ gestation. For analysis, the venous index was defined as maximum minus minimum velocity divided by maximum velocity. Different cases with intracranial abnormalities were evaluated with emphasis on abnormal venous blood-flow patterns.
Results: Internal cerebral veins had pulsatile patterns with a venous index of 0.22 in 47.6% of fetuses, whereas all fetuses had pulsations in the dural sinuses. The vein of Galen had a significantly lower venous index (0.31) than the superior sagittal sinus (0.39) and the straight sinus (0.36), indicating that the amplitude of the intracranial venous pulsation might increase as the flow runs from the periphery toward the proximal portion. Significant regression lines of venous index were obtained, indicating the stability of the pulsation during pregnancy. A flat pattern of superior sagittal sinus flow was found in three cases of hydrocephalus and one of craniosynostosis.
Conclusion: We showed the normal patterns of fetal cerebral venous blood-flow velocity and the abnormal patterns which might be associated with increased intracranial pressure. Doppler assessment of the intracranial venous system enabled us to evaluate intracranial abnormalities accompanied by increased intracranial pressure that might have prognostic clinical importance.
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.
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Methods |
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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.
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. 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.
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), indicating stability of venous pulsatile waveform patterns during normal pregnancy.
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and the cases are summarized in Table 3.
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Discussion |
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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.
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Received June 26, 1998. Received in revised form October 5, 1998. Accepted October 29, 1998.
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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.[Medline]
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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.[Medline]
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