The results of this study showed that in early stages of hypoxia, the fetal brain veins reflect the increment in cerebral blood flow as an increase in velocity and a reduction in the pulsatility index. In more advanced hypoxic stages, there is an increase in pulsatility, similarly to other veins such as the ductus venosus, and a trend for reduced velocities, suggesting a subclinical state of hypoxic cardiac dysfunction.
The transverse sinus was the first fetal brain vein to be systematically studied. Laurichesse-Delmas and cols. constructed normal reference velocity and PI values, and Senat et al. found a significant association between TS-PIV with DVPI and low Apgar scores. Conversely, Cheema and cols. in a group of 109 high risk pregnancies, found that only 9 of them showed an abnormal TS-PI with no increment in the prevalence of adverse perinatal outcome. In our study, we found a significantly reduced PI value in the TS-PI from IUGR fetuses with a biphasic trend in relation to the progression of hypoxia. The reduced PI values in stage 2 reflected the enhanced cerebral flow observed in the arterial system, and their further increment might correspond to the reduction of right heart compliance in the context of fetal hypoxic deterioration. Other potentially contributing factors could be a progressive lack of compliance of the vein wall.
Dubiel et al. studied the blood flow pattern in the Galen vein and found an increase in the prevalence of pulsations in high risk pregnancies associated with a higher risk of perinatal complications. These results were later corroborated by Cheema et al. who also pointed at the Galen vein as the more robust parameter associated with an adverse perinatal outcome.
According to our study, a pulsatile blood flow pattern in the Galen vein was statistically more frequent in IUGR fetuses and its prevalence increased as the hypoxic insult progressed.
However, the relatively high frequency of a pulsatile blood flow pattern of the GV in normal pregnancies precludes its clinical application. We observed a significantly increased PSV and TAMV in the GV from IUGR fetuses. While the presence of a pulsatile pattern is not a clear indicator of the risk, the combined estimation of increased velocity and presence/ absence of a pulsatile blood flow pattern might offer better clinical information in cases at a higher risk of perinatal complications.
The superior sagittal sinus and the straight sinus were the most difficult veins to locate in normal pregnancies, while in the IUGR they were easier to find, due to increased velocities, together with fewer fetal movements. One of the drawbacks in locating the SS, is that for a clear recording, a clear complete mid-sagittal view of the fetal head is needed. Similar to the other brain veins, the blood flow pattern was not always pulsatile, in normal pregnancies was about 60% whereas in IUGR fetuses, increased up to 80%. In relation to the progression of hypoxia, SS showed the same trend as the Galen vein.
The straight sinus was also studied by Cheema et al. They could not find an increased prevalence in the adverse perinatal outcome in cases with increased maximum velocity in this vein. In their study, as in ours, the STR was recorded less successfully than the TS and the Galen vein. In relation to the progression of hypoxia, we observed a continuous increment in the STR blood velocities, starting from hypoxic stage 2 onwards, probably reflecting the vascular response to the overall enhanced brain blood flow. The blood flow pattern in this vein was almost always pulsatile in normally grown and IUGR fetuses. However, cases with no-pulsatile blood flow were more often seen after 31 weeks of gestation. Variations in the presence of a pulsatile blood flow pattern in normal fetuses can be mainly related to gestational age, as previously suggested by Laurichesse-Delmas and cols. A continuous blood flow is more frequently observed towards the end of pregnancy in all fetal cerebral veins. Nevertheless, it appears that the Galen vein shows preferentially a continuous blood flow pattern, regardless of the stage of pregnancy whereas the transverse and straight sinuses showed preferentially a pulsatile pattern. The sagittal sinus showed a wide variation in its blood flow pattern.
Feasibility to record the Doppler waveforms from the brain vessels has previously been addressed by different authors. Laurichesse-Delmas reported a 98% success rate to obtain the Doppler waveform from the TS and Cheema and cols reported a 100% success in getting signals form the Galen vein and 82% success rate for the straight sinus. We were able to record all veins from all IUGR fetuses, and in nearly 85% of the normally grown fetuses. The most challenging vessel to record was the SS, followed by the STR, as previously mentioned. We were always able to obtain recordings from the GV, and TS in both groups. Reproducibility analyses showed a small disagreement when two operators measured the TSPI, and a good agreement in defining a pulsatile blood flow pattern, meaning that in the hands of trained operators the venous cerebral circulation can be reliably evaluated. While in clinical practice it seems that the GV and TS might offer potentially useful information, the evaluation of the straight and sagittal sinuses might contribute important physiological information concerning the cerebral vascular redistribution process.
In this study, we measured all main cerebral vessels, which allowed us to get a full picture of brain venous changes under hypoxia. Interpretation of changes in venous vessels is difficult and several factors must be considered. Firstly, the territories drained are ill-defined and therefore, interpretation of regional changes is even more limited than with arteries. Secondly, while changes observed in velocity are probably mainly determined by blood flow, the changes in pulsatility have a mixed component. In early stages of hypoxic deterioration, the PI tended to decrease, as opposite to vessels from the inferior venous circulation, such as DV suggesting that PI changes are probably influenced by the increase in blood flow. However, in more advanced stages of hypoxic deterioration, the influence of reduced cardiac compliance seems to prevail over increased flow, and brain veins follow the pattern of the ductus venosus, though probably with a lower magnitude.
Our definition of the progression of hypoxia was based on experimental and clinical studies where, in the presence of a continuous hypoxic insult, the cardio-vascular adaptation is first manifested as changes in the umbilical artery (UA) blood flow, followed by a vascular centralisation process and finally, as changes in the fetal venous return. While by noninvasive methods, it is extremely difficult to properly classify a fetus in relation to its hypoxic status, we considered that using this stratification allowed us to reliable include cases in similar stages of the hypoxic progression. Nevertheless, we must accept some degree of overlapping in the stages described here. In summary, from our results we can conclude that the fetal cerebral vascular redistribution process in IUGR is also expressed as an increment in the venous blood flow velocities in all cerebral veins, as an increased pulsatility index in the transverse sinus and as an increment in the prevalence of a pulsatile blood flow pattern in the Galen vein. These results may suggest that in venous vessels velocity estimations are probably a more reliable indicator of increased blood flow in the chronically hypoxic fetus. This information should be analysed in conjunction with arterial blood flow changes and with other techniques addressing regional blood flow perfusion, to better understand the cerebral vascular adaptive process in fetuses complicated with severe growth restriction.
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