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    1732 FTP

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    Ultrasound Obstet. Gynecol. 6 (1995) 19-28 Changes observed in Doppler studies of the fetal circulation in pregnancies complicated by pre-eclampsia or the delivery of a small-for-gestational-age baby. I. Cross-sectional analysis K. Harrington, R. G. Carpenter*, M. Nguyen* and 8, Campbell Department of Obstetrics and Gynaecology, King’s College School of Medicine and Dentistry. London: and Department of Medical Statistics, London Schoo! of Hygiene and Tropical Medicine, London, UK ‘Key words: PRE-ECLAMPSIA, SMALL FOR GESTATIONAL AGE, INTRAUTERINE GROW!tt RELARDATION, UMBILICAL ARTERY DOPPLER, MIDDLE CEREBRAL ARTERY DoreLek, AORTA DOPPLER, FETAL DoreLek Ratios ABSTRACT The aim of this study was to compare changes in Doppler ultrasound studies of the fetal circulation in normal preg- nancies with a group of pregnancies complicated by pro- teinurie pregnancy-induced hypertension ( PPIH), delivery of a small-or-gestational-age (SGA) haby, or both. A total of 167 uncomplicated pregnancies with a term delivery of an appropriately grown baby (AGA) were used to define the normal range. Altogether, 123 high-risk pregnancies with a known outcome constinuted the study group. A color duplex: ultrasound machine was used to perform biometry turd fetal Doppler studies. Measurements obtained from the fetal circulation included the umbilical artery (UA) ppulsatility index (PL), the middle cerebral artery (MCA) PI and time-averaged velocity (TAV), the thoracic aorta (AO) PI and TAV. In addition, the ratio between the MCA PI and UA PI, the MCA PI and the AO PI, and the product of the MCA Pland AO TAY were used in the analysis. A total of 103 pregnancies had a complicated outcome. They were divided into three categories: PPIH only (pregnancies complicated by PPIFT with the delivery of an AGA fetus, n= 17). SGA only (delivery of an SGA baby, with no evidence of PPIH, w= 55), and PPIH + SGA (pregnancies complicated by pre-eclampsia and delivery of an SGA baby, 1 = 37). The PPIH + SGA group repre- sented true clinical intrauterine growth retardation. Cross-sectional reference ranges were created using the ‘observations from the normal group. 2-scores (standard deviation from the mean of the normal range) of the last observations made before delivery were caleulated for each of the vessel velocimetry measurements and ratios. The statistical significance of 2-score values was calculated using analysis of variance ‘The MCA and UA PI values showed the greatest deweation for any single-vessel parameter. The ratios of ‘fetal Doppler indices (MCA/UA PI ratto, MCA/AO PL ratio and the MCA PUAO TAV index) demonstrated greater deviation from normal than any individual vessel The UA Plu-score for PPLH + SGA delivering < 34 weeks gestation (2.92) was significantly greater than the z-score for PPII + SGA delivering = 34 weeks (1.20, p < 0.05). Fetal Doppler indices, in particular ratios that include ‘measurements obtained from the cerebral circulation, help in the recognition of the small fetus that is growth-retarded. At term, evidence of fetal hemodynamic redistribution may exist in the presence of a normal umbilical artery PL. Fetal Doppler indices provide information that is not readily obtained fram mare conventional tests of fetal well-being. It therefore has an important role to play in the manage- ‘ment of the growth-retarded fetus. INTRODUCTION The short-term morbidity associated with being born small for gestational age is well recognized, and more recent evidence suggests that long-term morbidity is also increased in this group of babies'. Children with lower th weight have higher blood pressure at 4 years of age when compared to children with an appropriate birth weight? If a haby is both small and growth-retarded at birth, the risk of developing long-term complications appears to be increased. Pre-eclampsia/proteinuric preg Corespondcnce, Dr K. Haningion, Departnent of Obstetrics and Gynaccology, King’s College Hospital, London SES BRX, UK 9 Received 21.98 Revised 17-5-95, Accepted 205.95, Fetal circulation in complicated pregnancies nancy-induced hypertension (PPIH) is associated with a high morbidity for both mother and fetus’, and remains the most common single cause of being horn small secondary to intrauterine growth retardation. It is desit- able to identify the growth-retarded from the small but healthy fetus, so that management of the at-risk preg- nancy can be targeted appropriately With ultrasound, it has become possible to assess the structure and growth of the fetus, and monitor its response to adverse conditions in utera. The introduction of Doppler ultrasound has allowed the fetal circulation to be examined*’. A failure of placental development can be identified by observing the level of resistance in the umbilical arteries*’, and, by examining the fetal aorta and cerebral vessels, it is possible to monitor the response of the fetal circulation to hypoxia and acidemia"? The primary response observed with fetal Doppler is the brain-sparing effect. ie, blood is preferentially sup- plied to the fetal heart, adrenal glands and brain, at the expense of the rest of the body, which has been demon- strated in both animal! and human" studies. More severe changes in the fetal systemic circulation, in par ticular the loss of end-diastolic frequencies in the fetal aorta, are closely correlated with the development of acideria!® and an increase in neonatal morbidity", while increased pulsatility in the venous circulation reflects cardiac compromise secondary to an increased after- load Confirmation of the progression from hypoxia to heart failure (as evidenced by an abnormal fetal heart rate pattern) has been documented’. Although Doppler velocimetry changes in individual vessels have been shown to be abnormal in the growth-retarded fetus'™", comparison of changes in the fetal cerebral citculation with changes in the systemic circulation or the umbilical arteries has been shown to be of more promise as a predictor of the condition of the fetus"™”. Because of the potential for this technique, reference ranges for fetal Doppler indices have been published for several vessels", The introduction of color Doppler imaging has focused attention on three arterial vessels: the umbilt- cal arteries, the fetal middle cerebral arteries, and the thoracic aorta The aim of this study was to create reference ranges for indives derived from the fetal vessels that are in current use, to examine the relationship between fetal Doppler indices and a complicated outcome to preg nancy, in particular the development of PPILI, the birth ofa small-for gestational-age baby, or a combination of these problems. The measurements are also combined as, ratios or products to examine whether these indices may more clearly delineate the relationship between fetal hemodynamic changes and compromise in utero, METHODS AND MATERIALS A total of 167 uncomplicated pregnancies with a term delivery of an appropriately grown baby were used (0 define the normal range. The study group was made up of 123 high-risk pregnancies. The indications for referral 20 Ultrasound in Obstetrics and Gynecology Harrington et al. included suspected SGA fetus, oligohydramnios, ahnor- mal vterine artery Doppler studies (persistent notching), hypertension, or a poor obstetric history. Multiple preg- nancies. and any fetus with a structural or chromosomal anomaly. were not included in the study. Informed consent was obtained from each patient. The investigations were performed using an Acuson 128 (Mountain View, California) with 3.5- and 5-MIlz linear transducers. The patients were allowed to rest for 10-15 min in a scmi-recumbent position prior to commencing, the ultrasound investigation. Fetal biometry, including, the abdominal circumference (AC) was performed it tially, Umbilical artery Doppler flow velocity waveforms were obtained from a free loop of cord, and measure- ments taken when a clear waveform was acquired in the absence of fetal breathing or body movement. The pulsatility index (PI) was measured, and the presence or absence of end-diastolic frequencies was noted. The PI wwas used as it continues to reflect changes in resistance with progressive absence of end-diastolic frequencies or reverse flow, and the values are normally distributed in the third trimester". The thoracic aorta was visualized in a longitudinal view of the fetus, The transducer was tilted so that an angle of 60° or less was created between the beam and the aorta, The Pl and time-averaged velocity (TAV) were measured, and the presence or absence of end-diastolic frequencies noted. ‘The TAV was calculated using the peak velocity envelope. To obtain measurements. from the middle cerebral artery (MCA), the transducer was positioned so that the sphenoid bones were seen in a transverse view of the fetal head. The MCA conveniently courses along the wing of the sphenoid bone, and can readily be seen when color Doppler is applied. The Pl and TAV were recorded, The results were not revealed to clinicians or patients, and no action was taken on the basis ofthe fetal Doppler findings. Outcome variables included gestational age at delivery, the development of PPIH, and delivery of an SGA (© 10th centile) baby. PPIH was defined as two recordings of 2 90 mmHg diastolic pressure, or one read ing of > 110 mmHg, in the presence of > 300) mg pro teinuria in 24 h. The definition of small for gestational age at birth was based on charts currently in use at our hospitat”. The outcome for each pregnancy was obtained by examining the labor ward records, and neonatal intensive care unit records where appropriate. Where the outcome was unclear, the individual case notes were examined. The outcome is unknown in two high-risk cases, leaving 123 pregnancies available for analysis, The complicated pregnancies were divided into five outcome categories (Table 1): normal (n = 167), PPIH only (n= 13), SGA only (n= 55), and PPIH + SGA (7 = 37), and 18 other pregnancies that did not fit any of the above categories, which were excluded from the analysis. This group is comprised of women that delivered spontaneously before 37 weeks with an appro- priately grown baby, or required delivery by Cesarean section for reasons other than PPIH, SGA, of evidence of fetal compromise (abnormal fetal heart rate pattern. Fetal circulation in complicated pregnancies Table 1 The outcome of the 290 pregnancies that were inves tigated in this study Pregnancy outcome Number of cases ‘Normal 167 PPI 1B SGA 55 PPIH + SGA EY Other IR PPIH, pre-eclampsia/proteinutic pregnancy-induced hypert sion, with an appropriately grown baby; SGA, delivery of a smail-for-gestational-age (< 10th centile) baby. with no evi- dence of PPIH; PPIH + SGA, development of PPIH and the delivery of an SGA hahy; Other, a group of pregnancies that did not have a noma outcome, but did wot qualify for the subgroups used in this analysis Pregnancies complicated by pre-eclampsia that resulted im the delivery of an appropriately grown tetus were allocated into the PPIH only group: pregnancies that were complicated by the delivery of an SGA baby, but had no evidence of pre-eclampsia were placed in the SGA. only group; and pregnancies complicated by pre-eclamp= sia and an SGA baby were placed in the PPIH + SGA. ‘group. The division of pregnancies with a complicated outcome into these three categorics allowed us to ex ‘amine the differences in the relationship between fetal Doppler in preeclampsia with or without the added complication of an SGA fetus. Furthermore, as the etiology of smallness is diverse, all SGA fetuses would not be expected to demonstrate alteration in their fetal hemodynamics consistent with hypoxia, whereas most, i not all, of the PPIH + SGA fetuses are likely to suffer some degree of placental insufficiency and hypoxia. ‘These three groups therefore allow us to examine the hemodynamic response of the fetus in conditions which frequently state a common etiology. The statistical computer package SPSS” was used for data processing and analysis of variance. Grostat”® was used for the construction of the normal ranges and ‘computation of normal scores. This program models the normal data for a test in stages. First, the data are arranged in order of gestational age. Then, using a box comprising the first 10% of the data, a series of centiles 58 estimated for the observations in their box at their median age (after making a linear adjustment for age) In this application, up to seven centiles were estimated G10, 25, 50. 75, 90 and 97), The box is then moved one step by dropping one observation and including the next largest observation not already included. Then a set of centiles are estimated corresponding to the new median gestational agc of the box. The process is repeated until the box finally covers the last 10% of observations. In this way, a set of ‘raw’ centiles are computed covering 90% of the data, The raw centiles are then smoothed by fitting a polynomial in gestational age a, a’, etc., and in the standard normal deviate > and =. Terms combining powers of @ and 2 are also included. Thus the S0th centile, Which corresponds to = = 0, is modelled by the terms of Harrington et al the polynomial that only involve a. If the data are normally distributed with SD constant, all the centiles can be modelled by including a term bz, where b is the standard deviation (SD). By including a term in a’z in the polynomial, changes in SD with age can be modelled Terms in = moctel skewness in the data and changes in skewness with age can also be modelled, Fitting is by least squares, and all stages are imple- mented in Grostat. In addition, after the centiles have been modelled, normal scores (2) can be computed for test results. Special procedures must be implemented when observations are well outside the normal range”. Various methods of assessing goodness of fit are availa- ble (Ayatolli, Cole and Matthews, personal communica- tion), but conventional methods used in conjunction with. least square fitting are not appropriate because raw centile data points are correlated. By plotting the normal z-scores by age against normal centiles and by tests of normality of these 2-scores, it 1s possible to picture the goodness of fit (see Figures 9 and 10) Reference ranges were created using all the observa- tions on the normal infants so that the whole period after 22 weeks’ gestation was covered. The use of multiple observations on these normal pregnancies does not invalidate the normal ranges, because the charts are built up from the raw centiles, spanning a limited range of gestational ages which rarely include more than one observation per fetus; less than 5% of the repeated measures on the normals form the normal group. =-scores of the last observations made before delivery were calculated for each of the vessel measurements and measurement ratios, in the normal, PPIH and SGA subgroups. These data were then used to calculate an F-value (degrees of freedom) to investigate the amount of intergroup variance for each particular measurement. The z-scores und analysis of variance provide com- plementary information about changes seen in the differ ent study groups, RESULTS Figures 18 display the normal ranges for eight test ‘measurements and the last observation for each of the three study groups. The coefficients of the equations detining these ranges and an explanatory note are given in the Appendix. Gioodness of fit of these charts to the ‘normal data is illustrated in Figures 9 and 10. Figure 9 shows the =-scores of the normal data in relation to the normal centiles. It can be seen that the data points are symmetrically spread about the meant (2-0) for the whole range of gestational ages, except possibly for a small concentration of points around 35-36 weeks’ ge- station. Five (2.0%) of the 246 points lic below the first centile and four (1.6%) lie above the 99th eentile, Figure 10 shows that, taken asa whole, the 246 normal scores are accurately distributed The :-score from the mean for the normal population and each of the complicated outcome groups is presented in Table 2. The values for the abdominal circumfer- ence (AC) are included for comparison. The degrees of Ultrasound in Obstetries and Gynecology 24 Feral circulation in complicated pregnancies Harrington et al BSE aE 4 Ease 7s * 4d o¢ g 5 5 3 z gus § z 3 5, 3 = os cbt tats tat iit obit iititit 24 26 2 3 HA 0 22 2S 26 WS 303 B36 BW Gestational age (weeks) Gestational age (weeks) Figure 1 List umbilical aatery pulsaility indea (PD) values Figure 2 Last snide cerebral artery Pl values obtain before obtained before delivery in the three groups of patients studied, plotted on reference ranges derived from pregnancies with a normal outcome. , PPIH only; X, SGA only: I, PPIH 1 SGA delivery in the three groups of patients studied, plotted on reference ranges derived from pregnancies with a normal out- come. 0, PPIH only; X, SGA only; Ml, PPIT | SGA oS Fea aaa aa aT TT pe Rae en a cia we 4 as Mile cerebrel artery TAY (cms) obbetidetititetitititite 20 22 24-26 28 1 324 36 38 40-42 4 Gestational age (works) Figure 3 Tast middle cerebral artery time-averaged velocity (TAY) values obtained before delivery it the three groups of patients studied, plotted on reference ranges derived from pregnancies with a normal outcome. ©. PPIH only: X. SGA, only: M, PPIH | SGA 23 “Thoracie aorta PL stitetititotetitatite 5 out 2022-24 26 28 30 32 34 36 38 A) AD 44 Gestational age (weeks) Figure 4 Last middle cerebral artery PI values obtained before Uslivery in the three yroups of patients studied, plotted on reference ranges derived from pregnancies with @ normal out- come. 0. PPIH only: X. SGA only: ML PPIH + SGA Table 2 The result of the last measurement before delivery, expressed as the standard deviation from normal for each group. The rmumber of observations for any particular test is displayed in parentheses Test Normal PPIH SGA PPI + SGA Rat) pevalue Ac “0.11109) 0.883) =197145) 2.1736) 35.8(3,199) 0.0001 UAPL ~0.15(137) 0.52113) 145(53) 21307) 25.2(3.256 0.0001 MCA PI 0.08142) -0.88(13) 1.33449) 0437) 48.7(3,237) 0.0001 MCA TAY 0.05(142) 161113) 0.68449) 17907) 21.4(3,237) 0.0001 AO PI 0.03(141) 0.7813) 1.0350) 1.68(37) 140,237) 0.0001 AOTAV 0.071139) 10913) 112449) -0.77(34) 13.1231) 0.0001 UA PUMCA PL 0.11(142) L18(13) 3.049) 3.9937) 42.6(3.237) 0.0001 MCA PAO PI 0.08142) 0.9913) 1.50(49) -2.33(37) $8,403,235) 0.0001 MCA PI'AOTAV —_0.10(138) 1.5013) 2.45041) 3.1829) 38.63,323) 0.0001 PPIH, pre-eclampsia/proteinuric pregnancy-induced hypertension, with an appropriately grown baby; SGA, delivery of small-for-gestational-a (© 10th centile) baby, with no evidence of PPIH, PPIH * SGA, developinent of PPIH and the delivery ‘of an SGA baby: UA Pl, umbilical artery pulsatility index (PI); MCA, middle cerebral artery; TAY, time-averaged velocity; AO, aorta; AC, abdominal circumference 22 Ultrasound in Obstetrics and Gynecology Fetal circulation in complicated pregnancies 0 7° aa > a

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