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ORIGINAL RESEARCH |
From the Department of Obstetrics and Gynecology, Haemek Medical Center, Afula, Israel.
Address reprint requests to: Zeev Weiner, MD Haemek Medical Center Department of Obstetrics and Gynecology Afula, 18101 Israel
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Abstract |
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Methods: We did Doppler ultrasound studies of internal jugular veins and the inferior vena cavas longitudinally on 21 normal singleton fetuses from 20 weeks to term, and on eight growth-restricted fetuses with absent end-diastolic flow at the umbilical artery (UA). The three components of the venous flow velocity waveforms were used to calculate peak velocity ratio: Peak systolic velocity (S wave) minus reverse peak velocity (R wave) divided by peak velocity during early diastole (D wave) and velocity time integral ratio: systolic velocity time integral minus reverse velocity time integral divided by velocity time integral during early diastole. Statistical analysis of longitudinal measurements used K-related samples Friedman test; groups were compared with Mann-Whitney U test and 
2 test.
Results: In normal fetuses we found significant increases in peak velocity ratio and velocity time integral ratio of internal jugular veins and the inferior vena cavas throughout gestation. The mean ± standard deviation (SD) of the internal jugular veins peak velocity ratio (1.12 ± 0.4 versus 1.46 ± 0.15, P < .05) and velocity time integral ratio (1.1 ± 0.2 versus 1.55 ± 0.17, P < .05) were significantly lower in growth-restricted fetuses compared with normal fetuses at 28–32 weeks’ gestation but inferior vena cava indices were not. None of the eight growth-restricted fetuses had umbilical venous pulsations or changes in inferior vena cava or ductus venosus blood flow patterns. All had arterial pH above 7.15 at birth.
Conclusion: Growth-restricted fetuses with absent end-diastolic velocity in the UA have changes in internal jugular vein blood flow patterns that probably indicate increased cerebral blood flow, more evidence of redistribution of blood flow in growth-restricted fetuses that can be used to maintain them.
Doppler ultrasound studies of growth-restricted hypoxic fetuses have found increased resistance to blood flow in the umbilical artery (UA), shown by absent or reversed diastolic flow.1–3 This situation is usually associated with redistribution of the fetal blood flow indicated by decreased resistance to blood flow in the fetal internal carotid and middle cerebral arteries.4,5 We also observed blood flow changes in the venous system of growth-restricted fetuses. Doppler changes in venous return related to fetal hypoxia were described as umbilical vein (UV) pulsations, reversed flow in the ductus venosus, and a characteristic flow pattern in the inferior vena cava.6,7
Although the arterial component of the cerebral circulation and abdominal arterial and venous circulation have been studied extensively,8–10 information about the venous side of brain circulation is limited. The internal jugular vein is the main blood drain of the brain hemispheres and of large parts of the midbrain. The objective of the present study was to define the Doppler indices of the internal jugular vein blood flow during normal pregnancies and those characterized by fetal growth restriction (FGR).
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Materials and Methods |
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Doppler ultrasound examinations of the internal jugular vein and inferior vena cava were done trans-abdominally with a 3.5- or 5-MHz transducer (128 XP10; Acuson, Mountain View, CA) with color and pulsed Doppler ultrasound. For studying the internal jugular vein, the sample volume was positioned near the jaw angle, before the point where it unites with the superior vena cava. As for the inferior vena cava, identification was done in a longitudinal plane on sagittal view of the fetal trunk, and the sample volume was positioned in a portion of the vein between the entrance of the renal veins and the entrance of the ductus venosus. The three components of the venous flow velocity waveforms were used to calculate peak systolic velocity (S wave) minus reverse peak velocity (R wave) divided by peak velocity during early diastole (D wave), and systolic velocity time integral minus reverse velocity time integral divided by velocity time integral during early diastole. Doppler studies of the middle cerebral artery were done on all fetuses with absent end-diastolic velocity in the UA and in all normal fetuses between 28 and 32 weeks’ gestation. All Doppler recordings were done when the fetus was in a resting period, without breathing movements. Measurements were made only with five equal Doppler waveforms. Recordings were done by one of two examiners (WZ or YG).
Data were entered in a computer database and analyzed. Statistical analysis of the longitudinal measurements was done with K-related samples Friedman test. The groups were compared by Mann-Whitney U test and 2 test. We expected a difference of more than three standard deviations between normal fetuses and fetuses with absent end-diastolic velocity in the UA, so eight fetuses with absent end-diastolic velocity in UA were enough to achieve power of more than 80%.
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Results |
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Changes in internal jugular venous and inferior vena caval indices throughout gestation are summarized in Table 1
. We found a significant increase in those indices throughout gestation.
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. Internal jugular venous indices were significantly lower in growth-restricted fetuses compared with normal fetuses, but not inferior vena caval indices. The middle cerebral artery pulsatility index was also significantly lower in growth-restricted fetuses compared with normal fetuses. None of the eight growth-restricted fetuses had umbilical venous pulsations or changes in inferior vena caval or ductus venosus blood flow patterns. Each had arterial pH above 7.15 at birth.
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) and late (Figure 2) gestation and of growth-restricted fetuses (Figure 3) are presented. The different patterns of the internal jugular venous waveforms are shown in Figure 4.
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Discussion |
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A central venous waveform usually consists of three waves, two forward and one backward. They are inversely related to the atrial contraction cycle. The first forward venous wave represents the ventricular systole (S wave). The second forward venous wave occurs during early diastole (D wave). The backward venous wave represents the late diastole with atrial contraction (R wave).13–15 Specific ratios between those waves indicate changes in venous blood flow patterns.7,16,17 In the current study, we used the peak velocity ratio, which has been used before. We also used measurements of the area under the curve of each wave, which correlate with volume flow and the ratio between the area of measurements.
It has been shown that the patterns of fetal venous waveforms change throughout pregnancy.17 One of the most prominent changes was a gradual decrease throughout gestation of the amount of reverse venous flow during atrial contraction. In a study using an invasive animal model, it was suggested that this was related to two important cardiovascular changes that occur throughout gestation, improvement in ventricular compliance and decreased ventricular end-diastolic pressure, as a result of reduction of placental resistance (decreased afterload). Another possible mechanism that contributes to venous blood flow patterns is the preloading condition.18 Those mechanisms cannot be easily separated in noninvasive human studies,18 but we believe they contribute to changes in venous blood flow patterns with gestation.13,19,20
Information about upper body venous circulation in fetuses is limited. In animal studies, the superior vena cava had the same blood flow pattern as the inferior vena cava.13 However, the superior vena cava, which does not drain only brain circulation, cannot indicate specific changes in cerebral blood flow like the internal jugular vein, the main venous return from the brain hemispheres. A previous study showed that internal jugular vein blood flow patterns consisted of three phases similar to those of other central veins.21 In that study, the internal jugular venous blood flow patterns measured by Doppler ultrasound were established in normal fetuses throughout gestation. Changes of internal jugular venous flow velocity waveforms measured by Doppler indices were similar to changes in Doppler indices throughout gestation in other central veins, probably because of changes of the central venous blood flow pattern indicating changes in fetal cardiac function throughout gestation.18
In growth-restricted fetuses with absent end-diastolic velocity in the UA, Doppler indices of internal jugular veins had a significant decrease parallel to decreased resistance in the middle cerebral artery. Those changes probably are because of increased cerebral venous blood flow, a known phenomenon in that situation. At the same time, no changes were found in inferior vena caval Doppler indices, indicating that changes in internal jugular venous Doppler indices were not related to changes in cardiac function.
We found that changes in internal jugular venous blood flow appear early in growth-restricted fetuses with absent end-diastolic velocity in UA. We did not find pulsations in the UV or reverse flow in the inferior vena cava or ductus venosus in the growth-restricted fetuses. Those are usually late findings characteristic of growth-restricted fetuses who are in an immediate jeopardy. The growth-restricted fetuses in this study were delivered before that stage of deterioration.
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Footnotes |
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Received September 23, 1999. Received in revised form February 16, 2000. Accepted March 2, 2000.
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References |
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2. Groenenberg IAL, Wladimiroff JW, Hop WCJ. Fetal cardiac and peripheral arterial flow velocity waveform in intrauterine growth retardation. Circulation 1989;80:1711–7.
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6. Rizzo G, Capponi A, Arduini D, Romanini C. Ductus venosus velocity waveforms in appropriate and small for gestational age fetus. Early Hum Dev 1994;39:15–26.[Medline]
7. Rizzo G, Arduini D, Romanini C. Inferior vena cava flow velocity waveforms in appropriate and small-for-gestational-age fetuses. Am J Obstet Gynecol 1992;166:1271–80.[Medline]
8. Woo JS, Liang ST, Lo RL, Chan FY. Middle cerebral artery Doppler flow velocity waveforms. Obstet Gynecol 1987;70:613– 6.
9. Mari G, Moise KJ, Deter RL, Kirshon B, Carpenter RJ Jr, Huhta JC. Doppler assessment of the pulsatility index incerebral circulation of the human fetus. Am J Obstet Gynecol 1989;160:698–703.[Medline]
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16. Kanzaki T, Chiba Y. Evaluation of preload condition of the fetus by inferior vena caval blood flow pattern. Fetal Diagn Ther 1990;5: 168–74[Medline]
17. Huisman TWA, Stewart PA, Wladimiroff JW. Flow velocity waveform in the fetal inferior vena cava during the second half of normal pregnancy. Ultrasound Med Biol 1991;17:679–82.[Medline]
18. Weiner Z, Efrat Z, Zimmer EZ, Itskovitz-Eldor J. Fetal atrioventricular blood flow throughout gestation. Am J Cardiol 1997;80: 658–62.[Medline]
19. Romero T, Covell J, Friedman WF. A comparison of pressure-volume relations of the fetal, newborn and adult heart. Am J Physiol 1972;222:1285–90.
20. Reed KL, Sahn D, Scagnelli S, Anderson CF, Shenker L. Doppler echocardiographic studies of diastolic function in the human fetal heart: Changes during gestation. J Am Coll Cardiol 1986;391–5.
21. Gross B, Petrikovsky BM, Forman F, Pellerito J, Mandel FS, Goldman M. Jugular venous blood flow velocity waveforms in human fetuses between 20 and 42 weeks of pregnancy. Acta Obstet Gynecol Scand 1997;76:923–7.[Medline]
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