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ORIGINAL RESEARCH |
From the 1Department of Obstetrics and Gynecology, University of São Paulo, São Paulo, Brazil.
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ABSTRACT |
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 ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS: Ninety-one fetuses from singleton pregnancies without fetal malformations with a diagnosis of absent or reversed end-diastolic flow in the umbilical arteries were prospectively studied. On the day of delivery, Doppler velocimetry of the umbilical arteries, middle cerebral artery, and ductus venosus was performed and the results were correlated with umbilical artery pH at birth at the following cutoff levels: pH < 7.20, < 7.15, < 7.10, and < 7.05. The association between fetal arterial and venous Doppler velocimetry and acidosis was then individually analyzed by the 
2 and Fisher exact tests. The ability of these tests to predict the probability of acidosis at birth was estimated using a logistic regression model.
RESULTS: There was a negative correlation between pH at birth and umbilical artery pulsatility index (r = –0.39; P < .001) and pulsatility index for veins in the ductus venosus (r = –0.63; P < .001). Assessment of the fetal arterial circulation (middle cerebral artery) showed no statistical correlation with pH at birth. Using logistic regression analysis, probability curves were constructed for pH values less than 7.20 (odds ratio [OR] 8.03), less than 7.15 (OR 11.92), less than 7.10 (OR 12.16), and less than 7.05 (OR 8.20).
CONCLUSION: The pulsatility index for veins of the ductus venosus was related to pH at birth, demonstrating that the higher the ductus venosus pulsatility index for veins, the lower the pH at birth. Once the pulsatility index for veins in the ductus venosus is known, the probability of acidosis at birth can be estimated.
LEVEL OF EVIDENCE: II-2
To this end, studies have been conducted to estimate the relationship between tests for the assessment of fetal well-being and the presence of acidosis at birth. Although no consensus exists in the literature as to which pH values indicate acidosis, acidosis at birth is useful to confirm the diagnosis of fetal distress. The relationship between umbilical blood pH and adverse outcomes, especially neurologic damage, is well known and depends on the degree and duration of acidosis.10 Among the tests for the assessment of fetal well-being, abnormal ductus venosus Doppler velocimetry has been associated with the presence of acidosis at birth, suggesting that this method is an important tool to define the best time for delivery.
The aim of the present study was to investigate arterial and venous blood flow in fetuses with absent or reversed end-diastolic flow velocity and to correlate the Doppler results with umbilical artery blood pH at birth to predict the probability of acidosis at birth.
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MATERIALS AND METHODS |
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ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Pregnant women at high risk for placental insufficiency were referred by the Prenatal Care Units for the assessment of fetal well-being. If absent or reversed end-diastolic flow velocity was diagnosed, the woman was hospitalized for bed rest and clinical monitoring until delivery. Color pulsed Doppler studies were performed by 1 of the authors (R.P.V.F.) with a 3.5-MHz curved-array probe (ATL Ultramark 9 HDI, Advanced Technology Laboratories, Dee Why, NSW, Australia, and Ecocee, Toshiba, Tokyo, Japan). The high-pass filter was set at 50 Hz to 100 Hz. All recordings used for analysis were obtained in the absence of fetal breathing movements.
Placental and fetal evaluation consisted of arterial Doppler velocimetry (umbilical arteries and middle cerebral artery; MCA) and venous Doppler velocimetry (ductus venosus) performed at maximal intervals of 72 hours in all cases. In the umbilical arteries, the sample volume was positioned 3 cm from the placental insertion of the umbilical cord and in the ductus venosus at its origin from the umbilical vein. Between the 20th and 27th weeks of gestation, the amniotic fluid index (AFI) was assessed every 72 hours. From the 27th week on, the following exams were performed daily: AFI measurement, cardiotocography, and fetal biophysical profile scores. Each woman was thus examined until a reason to deliver was observed. On the day of delivery, all examinations were repeated regardless of the time elapsed since the previous assessment. The presence of at least 1 of the following indications was required before delivery: gestational age of 34 weeks or more, severe maternal disease that would be life-threatening to the patient if the pregnancy continued, late fetal heart decelerations, AFI lower than 3.0, and fetal biophysical profile scores below 6. No prenatal steroids were used in any case.
All newborns were delivered by cesarean. After delivery, the following immediate neonatal outcomes of interest were obtained: gestational age at the time of delivery, 1- and 5-minute Apgar scores, umbilical artery pH and base excess, and newborn weight. Newborns were followed up during their stay at the hospital nursery, and any neonatal death was recorded.
The sample size was calculated to obtain a minimum of 10 cases for each event (pH at birth) so that at least 1 variable could be included in the logistic regression model.11,12 Thus, the selection of patients was extended until a minimal number of 10 cases was obtained for pH < 7.05, which was the rarest event.
To predict acidosis at birth the cases were classified according to umbilical artery pH at birth: group 1A: pH < 7.20 (48 cases), group 1B: pH 
7.20 (43 cases), group 2A: pH < 7.15 (25 cases), group 2B: pH 7.15 (66 cases), group 3A: pH < 7.10 (15 cases), group 3B: pH 7.10 (76 cases), group 4A: pH < 7.05 (10 cases), and group 4B: pH 7.05 (81 cases).
The following variables were submitted to univariate analysis, comparing the groups: fetal well-being assessment data—presence of reversed end-diastolic flow velocity in the umbilical arteries, pulsatility index in the umbilical arteries and MCA, pulsatility index for veins in the ductus venosus, and neonatal data—gestational age at delivery (weeks) and newborn weight.
All of the above-mentioned variables were submitted to comparative studies. The 2, Fisher exact tests, Student t tests, and correlation (Pearson) were used to estimate the association of these variables with umbilical artery blood gas values at birth. The level of significance was set at .05. The following criteria were applied to the selection of the variables for logistic regression: variables showing a statistical significance of less than .15 upon univariate analysis and that are related to acidosis at birth according to the medical literature were selected for the stepwise procedure (logistic regression model with a 95% confidence interval [CI] and odds ratio [OR] calculation) to predict the probability of acidosis at birth. In addition, it was necessary to determine the maximal number of variables eligible for inclusion in the multiple or univariate logistic regression model. As a general rule, there must be at least 10 outcomes for each independent variable eligible for inclusion.11 Thus, the maximum number of variables eligible for the different regression models was 4 variables for pH < 7.20, 2 variables for pH 7.15, 1 variable for pH < 7.10, and 1 variable for pH < 7.05.
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RESULTS |
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ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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7.20; group 2A, pH < 7.15, compared with group 2B, pH 7.15; group 3A, pH < 7.10, compared with group 3B, pH 7.10; group 4A, pH < 7.05, compared with group 4B, pH 7.05).
Umbilical artery Doppler velocimetry demonstrated a reversed diastolic flow in 37 of 91 (40.7%) cases. The correlations between other Doppler velocimetry results and pH at birth are shown in Figures 1 to 3. To predict the probability of pH values at birth of less than 7.20, 7.15, 7.10 and 7.05, the Doppler velocimetry results were compared between the different groups (group 1A, pH < 7.20, compared with group 1B, pH 7.20; group 2A, pH < 7.15, compared with group 2B, pH 7.15; group 3A, pH < 7.10, compared with group 3B, pH 7.10; group 4A, pH < 7.05, compared with group 4B, pH 7.05).
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7.20, 43 cases) revealed no difference in the frequency of cases with reversed diastolic flow (23 of 48 [47.9%] and 14 of 43 [32.6%], P = .136), umbilical artery pulsatility index (3.52 ± 1.31 and 3.25 ± 1.32, P = .330), or pulsatility index of the MCA (1.13 ± 0.24 and 1.19 ± 0.25, P = .294). The pulsatility index for veins in the ductus venosus was significantly higher in group 1A than in group 1B (1.48 ± 0.90 compared with 0.81 ± 0.29, P < .001). Variables showing clinical relevance and significance of less than 0.15, ie, the presence of reversed diastolic flow and ductus venosus pulsatility index for veins, were eligible for the stepwise selection process. The variable selected by the logistic regression model as being able to predict the probability of a pH < 7.20 at birth was ductus venosus pulsatility index for veins (OR 8.031, 95% CI 2.370–27.208).
No difference in pulsatility index of the MCA (1.11 ± 0.22 and 1.18 ± 0.25, P = .209) was observed when comparing group 2A (pH < 7.15, 25 cases) and group 2B (pH 7.15, 66 cases). The frequency of cases with reversed diastolic flow was higher in group 2A (18 of 25 [72.0%]) compared with group 2B (19 of 66 [28.8%], P = .001), as was the umbilical artery pulsatility index, which was higher in the group with a pH < 7.15 (4.12 ± 1.45 compared with 3.12 ± 1.16, P < .001). Ductus venosus pulsatility index for veins was higher in group 2A than in group 2B (1.96 ± 0.93 compared with 0.86 ± 0.37, P < .001). Considering the sample size and clinical relevance reported in the medical literature, the 2 variables eligible for stepwise selection were presence of reversed diastolic flow and ductus venosus pulsatility index for veins. The variable selected by the logistic regression model as being able to predict the probability of a pH < 7.15 at birth was ductus venosus pulsatility index for veins (OR 11.924, 95% CI 3.979–35.736).
Comparison between group 3A (pH < 7.10, 15 cases) and group 3B (pH 7.10, 76 cases) showed no difference in pulsatility index of the MCA between groups (1.10 ± 0.22 and 1.17 ± 0.25, P = .306). The frequency of cases with reversed diastolic flow (12 of 15 [80.0%] and 25 of 76 [32.9%], P = .001) and umbilical artery pulsatility index (4.63 ± 1.47 and 3.15 ± 1.15, P < .001) were higher in group 3A compared with group 3B. Ductus venosus pulsatility index for veins was higher in group 3A than in group 3B (2.34 ± 0.84 compared with 0.93 ± 0.47, P < .001). Considering the sample size and clinical relevance reported in the medical literature, ductus venosus pulsatility index for veins was the variable entered in the logistic regression model and was able to predict the probability of a pH < 7.10 at birth (OR 12.160, 95% CI: 4.267–34.650).
When comparing group 4A (pH < 7.05, 10 cases) and group 4B (pH 7.05, 81 cases), no difference in pulsatility index of the MCA (1.10 ± 0.24 and 1.17 ± 0.25, P = .406) was observed. The frequency of cases with reversed diastolic flow (9 of 10 [90.0%] and 28 of 81 [34.6%], P = .001) and umbilical artery pulsatility index (5.04 ± 1.22 and 3.19 ± 1.19, P < .001) were higher in group 4A than in group 4B. The ductus venosus pulsatility index for veins was higher in group 4A than in group 4B (2.46 ± 0.92 compared with 1.0 ± 0.56, P < .001). Considering the sample size and clinical relevance reported in the medical literature, ductus venosus pulsatility index for veins was the variable entered in the logistic regression model and was able to predict the probability of a pH < 7.05 at birth (OR 8.201, 95% CI: 2.948–22.813).
The logistic regression models then permitted the construction of probability curves for each preestablished pH at birth according to the ductus venosus pulsatility index for veins on the day of delivery. Thus, once the ductus venosus pulsatility index for veins is known, the probability of pH values at birth less than 7.20, 7.15, 7.10, and 7.05 can be estimated (Fig. 4).
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DISCUSSION |
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The presence of acidosis at birth has been considered to be the standard for the diagnosis of fetal distress, and the relationship between the occurrence of acidosis and neonatal morbidity, especially neurologic damage, is well known and depends on the degree and duration of acidosis.10 However, the literature does not agree as to which pH values at birth are considered abnormal. Values below 7.20 have been cited, but other authors have reported different values, which in most cases range from 7.11 to 7.20. In addition, there is no agreement as to which pH values are related to adverse outcomes, with the worst neonatal outcomes being reported for values less than 7,15, 7.10, or 7.05. The possibility of demonstrating the risk of the occurrence of different pH values by means of a probability curve enables the obstetrician to estimate the probability of acidosis at birth as well as its severity, thus providing another tool that can be used in the difficult task to determine the best time for the delivery of these fetuses, which are often extremely premature.
Fetal blood samples for pH analysis can be obtained at 3 different stages: antepartum (cordocentesis), intrapartum (scalp blood microsampling), and postpartum (double clamping of the umbilical cord). The ideal would be, upon a diagnostic suspicion of fetal acidosis, to be able to obtain immediately a fetal blood sample that would permit a precise diagnosis of acidosis. However, this is only possible with cordocentesis, which is associated with numerous risks, a fact that led us to investigate noninvasive methods that can predict the occurrence of acidosis at birth. The method of blood sample collection for measuring pH at birth chosen in the present study permits appropriate correlation between acidosis and fetal well-being assessment tests in the antepartum stage, provided that all patients are delivered by cesarean and all exams are performed up to 24 hours before delivery.
All patients had a diagnosis of absent or reversed end-diastolic flow velocity determined by umbilical artery Doppler velocimetry, with the sample volume being placed 3 cm from the placental insertion, thus avoiding differences resulting from variations in umbilical cord size.20 Despite the long period that elapsed for selection of the cases, a fact explained by the rarity of absent or reversed end-diastolic flow in the umbilical arteries, care was taken to insure that the selected cases had undergone Doppler velocimetry using an ultrasound apparatus with similar technology. Comparison between groups showed that they were similar in terms of gestational age at delivery and newborn birth weight.
No prenatal steroids were used, because no consensus exists at our service regarding their routine use due to doubts about the possibility of adverse effects in relation to their true beneficial effects, especially in small for gestational age newborns at that time.21 Thus, we did not interfere with the conduct already established at our service. The lack of application of steroids by the service was not imposed by the research protocol but provided a unique opportunity to obtain the true correlation between ductus venosus values and pH at birth. Indeed, the use of steroids might have altered the Doppler velocimetry results of the umbilical arteries and ductus venosus.
In most cases, fetuses with absent or reversed end-diastolic flow velocity present hypoxemia due to a reduced gas exchange surface between the mother and the fetus, whereas the occurrence of acidosis shows wide variation. Weiner25 did not observe acidosis in pregnancies with absent or reversed end-diastolic flow velocity submitted to cordocentesis, despite a diagnosis of hypoxemia in all fetuses evaluated. In contrast, other authors found acidosis in approximately 50% of pregnancies with absent end-diastolic flow velocity.1,2 Therefore, the evaluation of umbilical artery Doppler velocimetry findings alone, without differentiating fetuses according to their response to hypoxemia, may lead to the fact that fetuses with initial hemodynamic abnormalities (such as centralization), who show compensated fetal distress (normal cardiotocography and fetal biophysical profile scores), and fetuses with later abnormalities (abnormal ductus venosus, cardiotocography, fetal biophysical profile scores) will be mistakenly considered to be similar.
Previously evaluated only in experimental animal models, the emergence of Doppler velocimetry now permits assessment of the fetal hemodynamic response to hypoxemia in humans. This response has been reported to maintain an established sequence of abnormalities in the fetal arterial and venous circulation. Hypoxemic fetuses show changes in arterial circulation (an increase in the pulsatility index of the descending thoracic aorta and a decrease in the pulsatility index of the MCA), which precede venous abnormalities (an increase in ductus venosus pulsatility index for veins).16
In the present study, the association between fetal arterial and venous Doppler velocimetry findings and acidosis was analyzed individually. Subsequently, the ability of these tests to predict the probability of acidosis at birth was verified by logistic regression.
Analysis of the umbilical arteries demonstrated a correlation with pH at birth both when the pulsatility index of the umbilical arteries was evaluated and when it was categorized by qualitative analysis into absent or reversed end-diastolic flow in the umbilical arteries.
Salafia et al,26 separately studying 20 cases of absent and 8 cases of reversed end-diastolic flow in the umbilical arteries, observed a mean pH of 7.15 and 6.94, respectively, emphasizing that cases of reversed end-diastolic flow may reflect more serious fetal impairment.
The assessment of the fetal arterial circulation (MCA) showed no correlation with pH at birth as observed in other studies. The association between centralization (vasodilatation in the MCA) and hypoxemia at birth has been well established. However, similar to other investigations, no relationship between brain-sparing effects and acidosis was observed in the present study.27,28 The absence of a correlation between the results of the analysis of the MCA and the occurrence of acidosis at birth observed in the present study is probably due to the fact that arterial vessels are the first to show abnormalities as a fetal response to hypoxemia. To ensure good oxygenation of the central nervous system, peripheral vasoconstriction occurs (an increase in the pulsatility index of the descending thoracic aorta), followed by cerebral vasodilatation (an increase in the pulsatility index of the MCA) and, if an appropriate oxygen supply is obtained, no acidosis will occur.
The relationship between ductus venosus Doppler abnormalities and the occurrence of acidosis is supported by Hecher et al,29 who reported that abnormalities in the ductus venosus result from an increased pressure in the right fetal chambers caused by excess peripheral vasoconstriction due to hypoxemia. Moreover, statistical analysis of Doppler velocimetry findings indicates that ductus venosus results are the only ones related to acidosis at birth.30 Recent studies have proposed the existence of an important association between ductus venosus abnormalities and adverse neonatal outcomes, suggesting that the assessment of this vessel is important to determine the timing of delivery.3,4
The pulsatility index for veins of the ductus venosus was related to pH at birth, demonstrating that the higher the ductus venosus pulsatility index for veins, the lower the pH at birth. In the present study involving cases of absent or reversed end-diastolic flow velocity, statistical analysis of fetal well-being assessment tests permitted the construction of probability curves for acidosis at birth (pH < 7.20, pH < 7.15, pH < 7.10, and pH < 7.05) according to the pulsatility index for veins in the ductus venosus.
Once the pulsatility index for veins in the ductus venosus is known, the probability curve for acidosis at birth of the model constructed makes it possible to estimate this probability in pregnancies with absent or reversed end-diastolic flow velocity. In these cases, knowledge of a factor predicting acidosis at birth, especially at different cutoff levels, facilitates the choice of the ideal timing for delivery, particularly in the case of very premature fetuses.
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Footnotes |
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doi:10.1097/01.AOG.0000209192.00890.3a
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REFERENCES |
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2. Farine D, Ryan G, Kelly EN, Morrow RJ, Laskin C, Ritchie JW. Absent end-diastolic flow velocity waveforms in the umbilical artery—the subsequent pregnancy. Am J Obstet Gynecol 1993;168:637–40.[Medline]
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