Antenatal Fetal Surveillance (1)

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Antenatal fetal surveillance
Peter Malcus
Purpose of review Antenatal fetal surveillance is a field of increasing importance in modern obstetrics, especially as results in perinatal care have recently made dramatic progress. It is an evolving field, and it is no longer acceptable just to wait and see when problems arise in pregnancy. During the past few decades many studies have shown that antenatal surveillance in unselected populations is of little value. However, high-risk patients benefit from antenatal fetal surveillance, especially women with pregnancy problems associated with intrauterine growth restriction. Recent findings This review shows that modern antenatal fetal surveillance is based on fetal heart rate monitoring, ultrasound biometry and amniotic fluid assessment, Doppler blood flow studies of fetal and uteroplacental circulation, and an evaluation of biophysical fetal parameters. Summary Used in combination these methods lead to improvements in fetal morbidity and mortality. The aim of future research should be to minimize the risks of fetal morbidity and mortality further by the optimal timing of delivery. Better organization of healthcare systems may improve our ability to identify at-risk patients during pregnancy. There is potential to improve the specificity of fetal surveillance tests, e.g. better methods of biometry and amniotic volume estimation with three-dimensional ultrasound and measurements of subcutaneous tissue. Improved knowledge of fetal physiology can be gained from research on fetal circulation with Doppler studies. Computer analysis of the fetal heart rate can increase the specificity of that test, and artificial neural networks may enhance the ability to evaluate the optimal use of integrated testing. Keywords amniotic fluid volume, antenatal fetal surveillance, biophysical profile, Doppler blood flow, fetal heart rate monitoring, ultrasound biometry
Curr Opin Obstet Gynecol 16:123–128.
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Abbreviations AFI BPP CTG FHR IUGR NST SGA
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amniotic fluid index biophysical profile cardiotocography fetal heart rate intrauterine growth restriction non-stress test small for gestational age

2004 Lippincott Williams & Wilkins 1040-872X

Introduction
Antenatal fetal surveillance is a field of increasing importance in modern obstetrics. This surveillance may concern control of the fetal heart rate (FHR) either electronically or by listening using older methods. It may be an ultrasound assessment of fetal weight or amniotic fluid volume and fetal behaviour, or it may be a Doppler evaluation of the fetoplacental or uteroplacental circulation. In the low-risk population these tests all show low sensitivity, specificity, positive and negative predictive values for fetal and neonatal morbidity and mortality, with low cost–benefit values when applied. The identification of at-risk pregnancies and their surveillance are currently of high priority in most societies. In a recent report, Ku ¨ nzel and Misselwitz [1 .] showed, in a large retrospective study between 23 and 42 weeks of gestation, that fetal antepartum death can be substantially reduced if available methods for fetal surveillance are aimed at detecting the signs of fetal oxygen deprivation at an early stage. The authors identified significant risk factors, such as social burden, diabetes mellitus, maternal age and maternal smoking, from the medical history in more than 50% of cases with antenatal fetal death. Bobby [2] advocated multiple assessment techniques to evaluate antepartum fetal risks, including FHR monitoring performed as a nonstress test (NST), the contraction stress test, an assessment of amniotic fluid volume, evaluation of fetal behaviour – biophysical profile (BPP), and Doppler assessment of fetal blood flow. An early diagnosis of the fetal state is based on information about the fetus from many perspectives of physiology and pathophysiology in different organ systems. Although surveillance has become more precise and reliable, there is still a need for an improvement of the existing diagnostic methods and the incorporation of new knowledge about these methods. Fetal circulation and neurology are of crucial importance, and an evaluation of the heart action with computerized cardiotocography (CTG) may give better information about the fetus in the antenatal period.
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2004 Lippincott Williams & Wilkins.

Department of Obstetrics and Gynecology, University Hospital Lund, Lund University, Lund, Sweden Correspondence to Peter Malcus, MD, PhD, Department of Obstetrics and Gynecology, University Hospital Lund, Lund University, S221 85 Lund, Sweden Tel: +46 46 171000, 172509; fax: +46 46 157868; e-mail: [email protected] Current Opinion in Obstetrics and Gynecology 2004, 16:123–128

DOI: 10.1097/01.gco.0000124167.64477.b6

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Information from Doppler examinations at increasingly lower gestational ages and from additional vascular beds teaches us more about fetal physiology both in normal and abnormal pregnancies. The combined approach with Doppler studies, antenatal computerized CTG and the BPP, the latter widely used in the United States, will probably improve our understanding of fetal pathophysiology even more in the future. This article will cover fetal surveillance in the period from 24 full gestational weeks to term, and will therefore deal with Doppler studies, fetal biophysical parameters, antenatal fetal heart monitoring and amniotic fluid volume. The overwhelming number of fetuses at risk of compromise are those with problems related to fetal growth restriction. Indications for fetal surveillance and appropriate tests will be discussed. Intrapartum fetal surveillance is not in the scope of this review, nor will it discuss fetal normality, screening for Down’s syndrome, fetal malformations, etc.

Intrauterine growth restriction
Intrauterine growth restriction (IUGR) is one of the most important clinical problems in perinatal medicine. It may express the fetal answer to a poorly functioning and sick placenta in many at-risk pregnancies, e.g. pre-eclampsia, other hypertensive disorders of pregnancy, multiple gestation and infectious or haemorrhagic insults to the placenta. The pathophysiology of IUGR is complex, and the knowledge of background factors is still incomplete. The reasons for IUGR may include vasculopathy at a very early stage of pregnancy, inflammatory response, alterations in feto–maternal cell traffic, or may depend on the defect regulation of placental and fetal development as a result of an abnormal interaction of growth factors and hormones in the maternal or fetal blood. The different modalities of the pathophysiological explanations of IUGR were recently reviewed by Mars ˇa ´ l [3 . .]. IUGR is associated with increased perinatal mortality and morbidity and is a common cause of premature delivery. It is not always easy to decide whether a fetus is small for gestational age (SGA) as a result of genetic imprinting or if it suffers from placental insufficiency. When a suspicion of IUGR is at hand it is important to apply biometric variables as early as possible in pregnancy, and to follow the development with serial and repeated investigations. The best way of assessing fetal size is by ultrasonic biometry. In recent years, the traditional method of ultrasonic biometry, with formulas for biparietal diameter, abdominal diameter or circumference and femur length has been challenged by threedimensional measurements and measurements of fetal subcutaneous tissue. These methods seem to improve the accuracy of fetal size calculations [4]. Fat volumetric measurements, however, may have applications mostly in the late third trimester and in diabetic pregnancies to assess glycemic control. For the SGA fetus in the second

and early third trimester, subcutaneous measurements will probably be less valuable [5 .]. Fractional soft tissue volume measurements using individualized growth charts in the premature fetus may possibly improve the detection and monitoring of early SGA fetuses, as recently reported [6,7]. Various definitions and cut-off values are used for the diagnosis of the SGA fetus. Most often it is defined as a fetus with a calculated weight below the 10th centile, or below the population mean minus 2 standard deviations. In our setting, two routine ultrasound scans are offered in pregnancy: at 18 weeks for dating and at 32 weeks for fetal growth estimation. Fetometry is performed with a formula including the biparietal diameter, abdominal diameter and femur length, and has a standard deviation of estimation error of 7% [8]. The detection rate for SGA (population mean minus 2 standard deviations) in our pregnant population was approximately 75% over the past 5 years with this programme. It should be compared with neighbouring centres, at which only one routine ultrasound scan is offered at 18 weeks for dating, and additional scans are carried out only on medical indication or in recognized at-risk pregnancies, in which the detection rate of SGA is approximately 50% (J. Molin, J. Laurin, N.O. Sjo ¨ berg, P. Lindqvist, unpublished data, in manuscript). As soon as the suspicion of SGA is confirmed, fetal surveillance with additional dynamic testing of fetal circulation, placental function, and fetal behaviour should be started and the fetus followed longitudinally. A multiple pregnancy carries special difficulties. The proportion of twin pregnancies with discordant growth of more than 25% is similar in mono and dichorionic twins, but morbidity and mortality are higher in the latter group [9]. Twin pregnancies should therefore be supervised with repetitive and longitudinal fetometry from the late second and early third trimester regardless of chorionicity. An evaluation of fetal growth in twin pregnancies often becomes troublesome, mainly because of the problem of ‘crowding’.

Cardiotocographic surveillance in the antenatal period: the non-stress test
Reflecting cardiorespiratory regulation of fetal heart performance, the NST has over the years, since its introduction during the 1970s, continued to be one of the cornerstones in fetal surveillance. The purpose of the test is an attempt to reduce the incidence of fetal compromise as a result of placental insufficiency and hypoxia. It is used in virtually all situations to assess fetal condition when complications in pregnancy arise. The classification of the NST has not been substantially changed since it came into use. The normal test was defined as a reactive pattern that required a minimum of two accelerations (15 beats per minute increase from the baseline during 15 s) during a 20 min test. The

Antenatal fetal surveillance Malcus 125

discussion about the NST is now more about how long the test period should be, how often and at what intervals it should be performed. A trace, reactive after 10–20 min, is generally regarded as sufficient for normality [10]. In some reports it has been advocated that the NST continues for up to 2 h before a non-reactive test is finally confirmed. The predictive value of a non-reactive NST is poor when outcome parameters such as fetal death and fetal distress during labour are used. A reactive test can be expected to impose a 10-fold lower risk of intervention for fetal distress during labour than a pregnancy with a non-reactive test [11]. However, in 1987 Bochner et al. [12] had already shown, in postdate pregnancies, that only 20–30% in a group of fetuses with non-reactive NST might undergo operative intervention for fetal distress, giving a specificity of less than 50% for the non-reactive NST. From the beginning, NST was applied only in pregnancies from 32 weeks and onwards. With the present ability to save preterm fetuses of increasingly lower gestational age, FHR monitoring and interpretation before 30 weeks are important. The pattern of CTG undergoes physiological changes during gestation. With increasing fetal maturity, the parasympathetic nervous system influences FHR patterns to a maturation of reactivity and a decline of the baseline heart rate. In the preterm period, short-term baseline variability is particularly difficult to assess and the variety of cardiotocographic patterns antepartum is vast. With computerized CTG, developed by Dawes and coworkers [13,14], the ability of the NST to diagnose fetal hypoxia by reduced short-term variability in the antepartum period has been shown to increase. Unfortunately, no controlled randomized trials have been performed during recent years to evaluate computerized CTG compared with standard CTG in relation to fetal outcome. Studies comparing computerized CTG with Doppler blood flow have recently been performed. They will be discussed later.

studies that it has a good negative predictive value for fetal death [16]. As a basis for our understanding of fetal physiology from different aspects, cardiorespiratory control, neurological adaptation and testing of the fetoplacental function, fetal movements, breathing and amniotic fluid volume may serve as a good complement to other testing modalities in the compromised, especially growth-restricted preterm fetus, as evaluated in a very interesting recent review article by Bocking [17 . .]. The validity of automatic cardioactographs was recently tested, and the authors found false positive detection of fetal movements, particularly in the preterm period. Caution is recommended in including actograph results in the interpretation of difficult FHR traces [18 . .]. Ultrasound examination still seems to be more valid to assess fetal movements.

The amount of amniotic fluid
There is a positive correlation between amniotic fluid volume and neonatal morphometry. Despite this, the positive likelihood ratios for the prediction of skinfold thickness below the 10th centile are low, indicating that the test is only rarely useful as a marker for IUGR. The two most often used markers of amniotic fluid volume, the amniotic fluid index (AFI) and the single deepest pocket, have not proved to be correlated to the actual amniotic fluid volume, although the tests have used amniocentesis with dye-dilution and spectrophotometry. There is, however, evidence that this gold standard for volume calculation is inaccurate [19]. Despite this, a large systematic meta-analysis [20] found that an antepartum AFI of 5 cm or less was associated with an increased risk of a low Apgar score less than 7 at 5 min [relative risk (RR) 5.2; 95% confidence interval (CI) 2.4–11.3], but not with neonatal acidosis. Earlier studies have shown a correlation between ultrasound evaluated reduced liquor volume and increased perinatal mortality compared with controls with a normal liquor volume. Magann et al. [21 .] have recently shown that the technique of measuring AFI and the single deepest pocket to the umbilical cord is better than through the cord to assess oligohydramnios, but the accuracy is equal for both methods in pregnancies with normal or high amniotic fluid volumes. Magann et al. [22 .] showed in another interesting recent study that both techniques were useful for predicting variable decelerations, low Apgar scores and caesarean delivery for fetal distress.

Fetal biophysical parameters
FHR changes may only represent the current cardiorespiratory status of the fetoplacental unit and not reflect chronic placental reserves. The integration of aspects of fetal behaviour, such as fetal gross body movements, fetal breathing movements and fetal tone, together with the NST and the amount of amniotic fluid in the testing of fetal well-being, constitute the BPP. The BPP described by Manning [15] is widely used especially in the United States for antepartum fetal surveillance. The test is, however, time consuming and impractical and may not be regarded as an instrument suited for fetal surveillance in unselected populations. BPP has not been shown to improve perinatal outcome, but sufficient data do not exist to rule out its definitive value. BPP has only been tested in high-risk pregnancies, and from these there is evidence from uncontrolled observational

Doppler examinations of fetal and placental circulation
Doppler examinations have given new knowledge about fetal circulatory physiology in health as well as in fetuses compromised by chronic hypoxia because of placental insufficiency. A large number of controlled, randomized, non-randomized and observational Doppler studies have shown that a blood flow investigation of the fetoplacental

126 Maternal–fetal medicine

circulation is of little value in the unselected low-risk pregnancy. During the past few decades, an extensive number of studies have shown that an absence of diastolic flow in the umbilical artery flow velocity waveform is the most decisive feature of the waveform for fetal compromise in high-risk pregnancies. Metaanalyses have indicated that umbilical artery Doppler surveillance of at-risk pregnancies is of great importance, especially in pregnancies associated with growth restriction [23,24]. Westergaard et al. [25] recently showed that umbilical artery Doppler applied in high-risk pregnancies significantly lowered perinatal mortality by 34%, and the need for the induction of delivery and the emergency caesarean section rate by 22%. Studies of other vascular beds in the fetus, including the cerebral circulation and the central arterial and venous systems, have increased the knowledge of compensatory and adaptive mechanisms [26 . .–28 . .] and the time sequence of circulatory changes in the fetus subjected to hypoxia and severe growth restriction. In a prospective observational study by Ferrazzi et al. [29 . .] on severely growth-restricted fetuses, early signs of fetal morbidity occurred in the umbilical and cerebral arteries, whereas late changes included reversed umbilical artery flow and abnormal changes in the ductus venosus, aortic and pulmonary outflow tracts. The time interval between early (15–16 days before delivery) and late changes (4–5 days before delivery) was significantly different, and late changes were significantly associated with perinatal death. The decision and timing to deliver were based on a non-reactive computerized FHR trace. The investigation of uteroplacental circulation has added knowledge of how to identify at-risk patients for the future development of pre-eclampsia and fetal growth restriction during pregnancy by the identification of increased flow resistance and a ‘notch’ of the uterine artery waveform in the second trimester [30,31 .]. Abnormal uterine artery flow is considered to be a sign of placental maldevelopment in early pregnancy.

correlation to risks for the fetus. An attempt was made to combine data in a low-risk population from ultrasound biometry, amniotic fluid index and umbilical artery Doppler in a multivariable analysis by Bachmann and coworkers [32 .]. The authors could not find any significant increase in the prediction of IUGR with this artificial neural network approach, and concluded that such an analytical technique is interesting, but demands sample sizes that are correlated both to the prevalence of the condition and the number of variables studied. Their study was not sufficient in this respect. Hod and Kerner [33 .] described and reviewed telemedicine as a first-line surveillance opportunity for at-risk pregnancies based on the teletransmission of FHR, fetal movement and uterine contraction monitoring. This could be an option for pregnant women at a remote distance from specialists and referral centres. The small studies that have been performed are promising, and need to be followed by larger randomized studies. After the identification of the pregnant woman at risk, an evaluation of fetal movements [34 .], the NST, combined with Doppler assessment of fetal, fetoplacental and uteroplacental blood flow, seems to be the most effective way of exclusion or verification of whether the fetus is at risk of chronic or acute hypoxia. In the preterm and especially the extreme preterm period before 28 weeks of gestation, the centralization of preterm risk pregnancies is necessary to centres where advanced fetal surveillance, including an evaluation of the central arterial and venous circulation, computerized CTG and biophysical profile is well established. High-risk conditions other than IUGR, e.g. diabetes mellitus and multiple pregnancy, also benefit from the integration of tests for fetal surveillance. In poorly controlled diabetic mothers, the fetus suffers the risks of hypoxia, acidosis and growth restriction. They have the same pattern of abnormal umbilical artery Doppler and FHR patterns as other pregnancies affected by IUGR, as reviewed by Maulik et al. [35 .]. In an observational pilot study, Wong et al. [36 .] showed significantly impaired fetal heart compliance and preload in metabolic poorly controlled diabetic pregnancies expressed by significantly elevated HbA1c values. Multiple pregnancy is associated with an increased risk of fetal abnormalities, prematurity, discordant growth of the fetuses and growth restriction of one or both fetuses. In the monochorionic twin pregnancy there is also a substantial risk of twin-to-twin transfusion syndrome of approximately 10–20%. Giles and coworkers [37 . .] recently published the results from the Doppler Assessment in Multiple Pregnancy study. It compared fetal surveillance with biometry with or without umbilical

The integration of tests for antenatal fetal surveillance
Our knowledge of fetal pathophysiology is increasing steadily. New methods for fetal surveillance in at-risk pregnancies have a tendency to be regarded as the one and only test when they are first applied. Tests have often not been evaluated in all the steps needed to constitute a good diagnostic test before they are taken into clinical use. As this review has shown, there is not one test that gives a complete and full explanation of fetal pathophysiology in the pregnancy at risk. We have to use modalities that attack the possibility to detect fetal hypoxia from different physiological aspects. Therefore, it is important to integrate all present knowledge in a test battery that is well proved for its

Antenatal fetal surveillance Malcus 127

artery Doppler velocimetry. A total of 529 women were randomly assigned and there were no statistically significant differences in antenatal, delivery, perinatal or neonatal outcomes. Both groups had unexpectedly low fetal mortality rates. In the Doppler group there were no unexplained intrauterine fetal deaths versus three in the non-Doppler group (non-significant). Earlier, smaller both randomized and non-randomized studies have indicated the reduction in fetal mortality when including Doppler studies in the surveillance of twin pregnancies [38,39]. During the past year, studies concluded that Doppler velocimetry was superior to the NST [40 .], or the contraction stress test in the case of a non-reassuring NST [41 .] for the detection of fetal distress and adverse fetal outcome, respectively. In an excellent review this year, Baschat [42 . .] pedagogically advocated the combined testing of highrisk pregnancies with Doppler velocimetry and biophysical parameters. Baschat and coworkers [43] have shown that the combination of BPP and multivessel arterial and venous Doppler is better in the prediction of perinatal mortality, acaedemia at birth and major neonatal morbidity than either modality alone. The timing of delivery is probably better indicated with the combination of tests, and especially in the preterm period it is of crucial importance that timing is adequate. The time sequence for parameters to indicate the deterioration of fetal health has also been described and evaluated in a study by Hecher et al. [44], which showed that the pulsatility index of ductus venosus and short-term FHR variation are important. The optimal time for delivery before 32 weeks of gestation should be if one of these parameters becomes persistently abnormal. Our own experience is that these changes are coincidental with or even preceded by retrograde flow velocities in the umbilical artery and with pulsations in the umbilical vein.

measurements. In case IUGR and placental insufficiency are diagnosed, fetal surveillance should continue with serial individualized controls. They should comprise biometry with an evaluation of the amount of amniotic fluid and preferably also an objective assessment of fetal body and maybe breathing movements, CTG and extended blood flow studies of the cerebral, central venous and arterial circulation. Although our knowledge is steadily increasing, there is still potential for improvement in terms of refined methods and prophylactic measures.

References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as: . of special interest .. of outstanding interest Ku ¨ nzel W, Misselwitz B. Unexpected fetal death during pregnancy: a problem of unrecognized fetal disorders during antenatal care. Eur J Obstet Gynecol Reprod Biol 2003; 110 (Suppl):86–92. An interesting large retrospective cohort study clearly indicating what should be regarded as a significant high-risk pregnancy. 2 3 Bobby P. Multiple assessment techniques evaluate antepartum fetal risks. Pediatric Ann 2003; 32:609–616. 1

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Mars ˇa ´ l K. Intrauterine growth restriction. Curr Opin Obstet Gynecol 2002; 14:127–135. This is a comprehensive and very educational review of the current knowledge about the different aspects of the pathogenesis of IUGR. 4 5 Schild RL, Fimmers R, Hansmann M. Fetal weight estimation by threedimensional ultrasound. Ultrasound Obstet Gynecol 2000; 16:445–452.

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Schwartz J, Galan H. Ultrasound in assessment of fetal growth disorders: is there a role for subcutaneous measurements? Ultrasound Obstet Gynecol 2003; 22:329–335. A well balanced and critical review of the advantages and pitfalls of subcutaneous fat measurements of different body compartments, and the ability of this technique to detect true IUGR. 6 Lee W, Detert R, McNie B, Romero R. Fractional thigh volume: a new soft tissue for fetal growth assessment. Ultrasound Obstet Gynecol 2003; 22 (Suppl 1 P197):123. Larciprete G, Valensise H, Vasapollo B, et al. Ultrasound determined fetal subcutaneous tissue thickness (SCTT) for a birthweight prediction model. Ultrasound Obstet Gynecol 2003; 22 (Suppl 1 P200):124. Persson P-H, Weldner B-M. Intra-uterine weight curves obtained by ultrasound. Acta Obstet Gynecol 1986; 65:169–173. Victoria A, Mora G, Arias F. Perinatal outcome, placental pathology and severity of discordance in monochorionic and dichorionic twins. Obstet Gynecol 2001; 97:310–315.

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Conclusion
Fetal antenatal surveillance starts with the problem of the identification of the at-risk pregnancy. According to reports, more than 50% of risk factors can be found in a maternal history of social burden, maternal smoking, health problems such as diabetes and probably heredity or a history of hypertension or pre-eclampsia. These factors all impose an increased risk of IUGR and prematurity. Methods for the detection of SGA are rather imprecise, but include the serial measurements of the symphys-fundal height or ultrasound biometry, the later presumably the better. When SGA is suspected, an evaluation of fetal status should be performed from different aspects of fetal physiology, including FHR monitoring with NST, maternal counting of fetal movements, umbilical and uterine artery Doppler flow

10 Schifrin B, Foye G, Amato J, et al. Routine fetal heart rate monitoring in the antepartum period. Obstet Gynecol 1979; 54:21–25. 11 Paul R, Miller D. Nonstress test. Clin Obstet Gynecol 1995; 38:3–10. 12 Bochner CJ, Medearis AL, Davis J, et al. Antepartum predictors of fetal distress in post-term pregnancy. Am J Obstet Gynecol 1987; 157:353–358. 13 Dawes GS, Moulden M, Redman CWG. Short-term fetal heart rate variation, decelerations, and umbilical flow velocity waveforms before labor. Obstet Gynecol 1992; 80:673–678. 14 Dawes GS, Moulden M, Redman CWG. System 8000. Computerized antenatal FHR analysis. J Perinat Med 1991; 19:47–51. 15 Manning FA. Dynamic ultrasound-based fetal assessment: the fetal biophysical score. Clin Obstet Gynecol 1995; 38:26–44. 16 Dayal AK, Manning FA, Berck DJ, et al. Fetal death after normal biophysical profile score: an eighteen-year experience. Am J Obstet Gynecol 1999; 181:1231–1236.

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17 Bocking AD. Assessment of fetal heart rate and fetal movements in detecting oxygen deprivation in-utero. Eur J Obstet Gynecol Reprod Biol 2003; 110:108–112. A very good review of the basics and physiology of the consequences of oxygen deprivation on FHR and other biophysical parameters. 18 De Wit AC, Nijhuis JG. Validity of the Hewlett–Packard actograph in detecting fetal movements. Ultrasound Obstet Gynecol 2003; 22:152–156. A critical and very relevant study evaluating the automatic actograph assessment of fetal movements in comparison with objective supervision with ultrasound. 19 Brans YW, Andrew DS, Dutton EB, et al. Dilution kinetics of chemicals used for estimaton of water content of body compartments in perinatal medicine. Pediatr Res 1989; 25:377–382. 20 Chauhan SP, Sanderson M, Hendrix NW, et al. Perinatal outcome and amniotic fluid index in antepartum and intrapertum periods: a meta-analysis. Am J Obstet Gynecol 1999; 181:1473–1478.

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32 Bachmann LM, Khan KS, Ogah J, Owen P. Multivariable analysis of tests for the diagnosis of intrauterine growth restriction. Ultrasound Obstet Gynecol 2003; 21:370–374. Although too small a sample size, this is an interesting test study of multivariable analysis for risk estimation in perinatal medicine. It may serve as a model for future research. 33 Hod M, Kerner R. Telemedicine for antenatal surveillance of high-risk pregnancies with ambulatory and home fetal heart rate monitoring: an update. J Perinat Med 2003; 31:195–200. This update reviews the concept of home FHR monitoring of high-risk pregnancies. A technique that may be well suited, especially for patients at a remote distance from referral centres. 34 Korzun P, Dubiel M, Kudla M, Gudmundsson S. Doppler velocimetry for predicting outcome of pregnancies with decreased fetal movements. Acta Obstet Gynecol Scand 2002; 81:926–930. This study describes the relevance of the maternal perception of decreased fetal movements and a possible relationship with combined abnormal umbilical and uterine artery Doppler velocimetry. 35 Maulik D, Lysikiewicz A, Sicuranza G. Umbilical artery Doppler sonography for fetal surveillance in pregnancies complicated by pregestational diabetes mellitus. J Maternal Fetal Neonatal Med 2002; 12:417–422. An interesting article that stresses the value of individualized management and umbilical artery Doppler surveillance in pregnant women with type I diabetes, especially those with vasculopathy. 36 Wong SF, Chan FY, Cincotta RB, et al. Cardiac function in fetuses of poorly controlled pre-gestational diabetic pregnancies: a pilot study. Gynecol Obstet Invest 2003; 56:113–116. An interesting study illustrating that poor diabetes control may have negative effects on fetal cardiac function, and is therefore of importance for diabetes care in pregnancy.

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21 Magann EF, Chauhan SP, Washington W, et al. Ultrasound estimation of amniotic fluid volume using the largest vertical pocket containing umbilical cord: measure to or through the cord? Ultrasound Obstet Gynecol 2002; 20:464–467. This excellent article discusses the controversy of the measurement techniques of amniotic fluid volume with ultrasound.

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22 Magann EF, Chauhan SP, Bofill JA, et al. Comparability of the amniotic fluid index and single deepest pocket measurements in clinical practice. Aust NZ J Obstet Gynaecol 2003; 43:75–77. This is an interesting study that discusses the different techniques of assessing amniotic fluid volume with ultrasound, and correlates their predictive value for fetal distress. 23 Giles WB, Bisits AM. Clinical use of Doppler ultrasound in pregnancy: information from 6 randomized trials. Fetal Diagn Ther 1993; 8:247–255. 24 Alfirevic Z, Neilson JP. Doppler ultrasound in high-risk pregnancies: systematic review with meta-analysis. Am J Obstet Gynecol 1995; 172:1379–1387. 25 Westergaard HB, Langhoff-Roos J, Lingman G, Marsa ´ l K. A critical appraisal of the use of umbilical artery Doppler ultrasound in high-risk pregnancies: use of meta-analyses in evidence-based obstetrics. Ultrasound Obstet Gynecol 2001; 17:466–467.

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37 Giles W, Bisits A, O’Callaghan S, et al. The Doppler assessment in multiple pregnancy randomized controlled trial of ultrasound biometry versus umbilical artery Doppler ultrasound and biometry in twin pregnancy. Br J Obstet Gynaecol 2003; 110:593–597. An important large randomized twin study that gives the information that close surveillance with biometry with or without Doppler is equally good at preventing fetal mortality in twins. 38 Johnstone FD, Prescott R, Hoskins P, et al. The effect of introduction of umbilical artery Doppler recordings to obstetric practice. Br J Obstet Gynaecol 1993; 100:733–741. 39 Jensen OH. Doppler velocimetry in twin pregnancy. Eur J Obstet Gynecol Reprod Biol 1992; 45:9–12.

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26 Hofstaetter C, Gudmundsson S, Hansmann M. Venous Doppler velocimetry in the surveillance of severely compromised fetuses. Ultrasound Obstet Gynecol 2002; 20:233–239. A very interesting prospective study that shows the importance of fetal venous flow changes as an indicator of fetal heart decompensation. 27 Baschat AA, Gembruch U, Weiner CP, Harman CR. Qualitative venous Doppler waveform analysis improves prediction of critical perinatal outcomes in premature growth-restricted fetuses. Ultrasound Obstet Gynecol 2003; 22:240–245. A well performed study indicating that the prediction of critical perinatal outcome is improved when qualitative venous and umbilical artery waveform analysis is combined. 28 Ma ¨ kikallio K, Jouppila P, Ra ¨ sa ¨ nen J. Retrograde aortic isthmus net blood flow and human fetal cardiac function in placental insufficiency. Ultrasound Obstet Gynecol 2003; 22:351–357. A very interesting study that confirms earlier experimental animal studies regarding the role of the aortic isthmus as an indicator of decreased oxygen supplies to the coronary and cerebral circulations in placental insufficiency.

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40 Williams KP, Farquharson DF, Bebbington M, et al. Screening for fetal wellbeing in a high-risk pregnant population comparing the nonstress test with umbilical artery Doppler velocimetry: a randomized controlled study. Am J Obstet Gynecol 2003; 188:1366–1371. A well performed randomized study showing that umbilical artery Doppler has a better predictive value for operative delivery for fetal distress than the NST, which confirms the results from earlier studies. 41 Figueras F, Martı´nez JM, Puerto B, et al. Contraction stress test versus ductus venosus Doppler evaluation for the prediction of adverse perinatal outcome in growth-restricted fetuses with a non-reassuring non-stress test. Ultrasound Obstet Gynecol 2003; 21:250–255. This study in growth-restricted fetuses, however small, shows that ductus venosus Doppler evaluation in fetuses with haemodynamic redistribution has no benefit of contraction stress test in case there is an abnormal NST in the prediction of adverse perinatal outcome.

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29 Ferazzi E, Bozzo M, Rigano S, et al. Temporal sequence of abnormal Doppler changes in the peripheral and cerebral circulatory systems of the severely growth-restricted fetus. Ultrasound Obstet Gynecol 2002; 19:140–146. This well performed study gives excellent information about the sequential Doppler changes in the severely compromised fetus. 30 Papageorghiou AT, Yu CKH, Bindra R, et al. Multicenter screening for preeclampsia and fetal growth restriction by transvaginal uterine artery Doppler at 23 weeks of gestation. Ultrasound Obstet Gynecol 2001; 18:441–449.

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42 Baschat AA. Integrated testing in growth restriction: combining multivessel Doppler and biophysical parameters. Ultrasound Obstet Gynecol 2003; 21:1–8. An excellent review with solid data about the combination of multivessel Doppler studies and other biophysical variables for the surveillance of fetal growth restriction. 43 Baschat AA, Gembruch U, Weiner CP, Harman CR. Combining multi-vessel Doppler and biophysical profile scoring improves prediction of critical outcomes in fetal growth restriction. Am J Obstet Gynecol 2003; in press. 44 Hecher K, Bilardo CM, Stitger RH, et al. Monitoring of fetuses with intrauterine growth restriction: a longitudinal study. Ultrasound Obstet Gynecol 2001; 18:564–570.

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31 Papageorghiou AT, Yu CKH, Cicero S, et al. Second-trimester uterine artery Doppler screening in unselected populations: a review. J Maternal Fetal Neonatal Med 2002; 12:78–88. This is a good review of the many studies that have been performed regarding the capability of uterine artery flow velocimetry to indicate risk for pregnancy complications.

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