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Uterine artery score and perinatal outcome

Uterine artery score and perinatal outcome
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  438 ORIGINAL PAPER Ultrasound Obstet Gynecol 2002; 19 : 438–442 BlackwellScience,Ltd Uterine artery score and perinatal outcome E. HERNANDEZ-ANDRADE * , J. BRODSZKI * , G. LINGMAN * , S. GUDMUNDSSON†, J. MOLIN† and K. MAR S ÁL * * Department of Obstetrics and Gynecology, Lund University Hospital, Lund, Sweden and † Department of Obstetrics and Gynecology, Malmö University Hospital, University of Lund, Sweden KEYWORDS :Doppler ultrasound, High-risk pregnancy, Perinatal outcome, Uterine artery velocity waveform ABSTRACT Objective To evaluate a modified uterine artery score based on the pulsatility index and presence or absence of notching in the Doppler velocity waveform recorded from both uterinearteries in relation to the perinatal outcome.  Methods A retrospective analysis was performed in 741third-trimester high-risk pregnancies. The uterine arteryscore was constructed assigning one point to each abnormal  parameter—high pulsatility index and presence of notch— thus ranging from 0 (normal findings in both uterine arteries)to 4 (notch and high pulsatility index in both uterine arteries).In a subgroup with lateral placenta (  n = 359), two definitionsof abnormal pulsatility index were compared. In the uniformuterine artery score, a pulsatility index > 1.20 in both uterinearteries was considered abnormal, disregarding the placental location; in the subgroup with lateral placenta, the high pulsatility index was defined as > 1.00 on the placental sideand > 1.40 on the non-placental side.  Results Receiver-operating characteristic curves did not reveal any difference in the diagnostic capacity between the group with a uniform uterine artery score and the subgroupwith lateral placenta (  P = 0.54). In the total material, the oddsratios and linear regression analysis showed an increased riskfor an adverse perinatal outcome with increasing uterineartery score (  P < 0.01). At a uterine artery score > 2, therewas a significantly increased risk for operative delivery forfetal distress, neonatal intensive care unit admission, 5-minApgar score < 7, preterm delivery and delivery of a small-for- gestational age fetus. Conclusion In high-risk third-trimester pregnancies, Dopplervelocity waveforms of the uterine arteries can be evaluated using the uterine artery score disregarding the placental location. The uterine artery score possesses a high predictivevalue regarding adverse perinatal outcome. INTRODUCTION Analysis of the flow velocity waveform recorded withDoppler ultrasound from the uterine artery in the second andthird trimesters of gestation has been proposed as a diag-nostic test predicting an adverse perinatal outcome in high-risk pregnancies 1 . With the advent of color Doppler imaging,enabling a clear identification of the uterine artery, many of the practical problems in obtaining a good quality signal havebeen circumvented and the reproducibility of Doppler resultsimproved 2 . The pulsatility index (PI), resistance index (RI)and presence of an early diastolic notch are the parametersmost often used for evaluation of the uterine artery velocitywaveform 3–5 . Recently, a uterine artery score (UAS) based onthe combination of RI value and the presence or absence of notching in the blood velocity waveform of the uterine arteryhas been proposed as a potentially useful test for surveillanceof fetal health in pregnancies with growth-restricted fetusesand/or pregnancy induced hypertension 6 . The UAS wasbased on signals obtained from both sides of the uterinecirculation and different RI cut-off values were used for theplacental and non-placental sides.The aim of the present retrospective study was to evaluatea modified UAS based on the uniform PI value for both uter-ine arteries in relation to the perinatal outcome and compareit with a UAS taking placental site into account. METHODS A retrospective analysis was performed in a group of 741high-risk pregnant women referred for Doppler examinationbecause of the following indications: pregnancy-inducedhypertension defined as a systolic and/or diastolic bloodpressure increase of at least 30 and 15 mmHg, respectively,after 20 weeks of gestation, or pre-eclampsia (blood pressure ≥  140/90 mmHg and proteinuria) ( n  = 148), suspected Correspondence: Dr E. Hernandez-Andrade, Department of Obstetrics and Gynecology, Lund University Hospital, SE 221 85 Lund, Sweden (e-mail: Accepted 20-12-01  Ultrasound in Obstetrics and Gynecology 439 Uterine artery score and perinatal outcomeHernandez-Andrade et al. intrauterine growth restriction (fetal weight > 2 SD below theexpected mean of reference population) ( n  = 127), vaginalbleeding ( n  = 77), preterm labor (regular uterine activitybefore 37 weeks of gestation and effacement of the uterinecervix) ( n  = 119), oligohydramnios (amniotic fluid index< 50 mm) ( n  = 113), prolonged pregnancy ( ≥  42 completedweeks of gestation) ( n  = 85), and others, e.g. previous historyof perinatal death, pregnancy-induced hypertension orintrauterine growth restriction, or decreased fetal movementsin the present pregnancy ( n  = 105). More than one mainindication was noted in 33 cases. The median age of thewomen was 29 years (range, 16–46), the median gestationalage at Doppler examination was 38 + 6 weeks (range, 25 + 6to 43 + 1), 38% of the women were nulliparas.Pulsed-wave Doppler ultrasound examination of the uterinearteries supported by directional color Doppler was performedwith a real time scanner (Acuson 128-XP/10, Mountain View,CA, USA) equipped with a 3.5-MHz probe. A 125-Hz high-passfilter was used to eliminate signals from slowly moving tissues.The uterine arteries were located in an oblique plane of thepelvis and the Doppler signals sampled 1 cm cranial to thecrossing point with the external iliac artery. Three consecutivecycles were evaluated in the absence of maternal breathingmovements. The PI was calculated according to Gosling et al  . 7 , and the presence of a notch was assessed subjectivelyby an experienced examiner according to Bower et al  . 8 . Onlythe last Doppler evaluation before delivery was consideredfor the UAS calculation. The results of Doppler examinationof uterine arteries were not made available to the cliniciansand, thus, not used in the clinical management of patients.The UAS was constructed by assigning the PI value andassessing the presence or absence of notching in both uterinearteries. A value of 1 was assigned for a high PI or for the pres-ence of a notch. The values of the UAS ranged from 0 to 4,depending on the number of altered parameters. Cut-off valuesfor the definition of high PI were based on the previous reportof our group 2 . Uniform uterine artery score (UAS uniform)was based on a PI value > 1.20, defined as abnormal for bothsides of the uterine circulation disregarding the placentallocation. In a subgroup of 359 pregnancies, a differentiateduterine artery score based on a clear lateral placental location(UAS LP) was calculated with an abnormal PI value of > 1.00for the placental side, and > 1.40 for the non-placental side.In this subgroup, the predictive capacities of the two scoreswere compared.Adverse perinatal outcome was defined as the presence of at least one of the following: perinatal death ( n  = 6), operat-ive delivery for fetal distress (ODFD) indicated by an abnormalcardiotocographic trace (bradycardia < 100 bpm, and/orlate decelerations, and/or low variability) and/or fetal scalppH value < 7.20 ( n  = 192), preterm delivery (< 37 weeksof gestation) ( n  = 117), Apgar score < 7 at 1 ( n  = 55) or5 min ( n  = 12), pH value of the umbilical venous blood< 7.20 ( n  = 68), pH value of the umbilical arterial blood< 7.10 ( n  = 52), admission to the neonatal intensive careunit (NICU) ( n  = 182) and birth weight small-for-gestationalage (SGA) (> 2 SD below the expected weight at the time of delivery) ( n  = 96). More than one perinatal complicationwas found in 208 cases.In the UAS group ( n  = 741), descriptive statistics, oddsratios with 95% confidence intervals and logistic regressionwere used for statistical analysis. In the subgroup with later-alized placenta ( n  = 359), receiver-operating characteristicscurves (ROC) were constructed for the UAS LP and UASuniform, respectively, and the optimal cut-off points wereselected. Differences between the areas under the ROCcurves were tested with chi-squared test. The predictivecapacity of both UAS was evaluated in terms of sensitivity,specificity, and positive and negative predictive values. A P -value < 0.05 was considered significant. RESULTS Odds ratios for adverse perinatal outcome in relation to UASvalues are shown in Table 1. The risk increased with increas-ing value of the UAS ( P  < 0.01).Table 2 shows the distribution of UAS values in the sub-group of 359 fetuses. There was no significant differencebetween the distribution of the UAS uniform and UAS LP( P  = 0.54). Sensitivity, specificity and predictive values forthe two UAS are given in Table 3; no differences between thetwo UAS were found. According to the ROC curves, the bestdiagnostic performance was with a score of ≥  2 for bothscores. With this cut-off level, the UAS uniform and the UAS Table 1 Odds ratios for uterine artery score (UAS) with uniform pulsatility index cut-off level with regard to the adverse perinatal outcome   Table 2 Distribution of the two uterine artery scores (UAS) in the subgroup with lateral placental location   UAS valueTotal (  n  )Adverse outcome (  n  )Odds ratio (95% CI) 03891421.011881281.64 (1.00–2.70)2103761.86 (1.00–3.54)350424.03 (1.77–10.32)41111 ∞  (3.20– ∞ )Total741399Linear regression analysis showed a significant trend ( P  < 0.01). UAS, uterine artery score using uniform definition of abnormal pulsatility index (PI) for both uterine arteries (PI > 1.20). For the definition of the adverse outcome see the text. CI, confidence interval. UAS valueUAS uniformUAS lateral placenta n % n % 018451.219855.218022.37019.424813.44913.733610.1277.64113.0154.1Total359100359100 χ 2  = 3.09; P  = 0.54. UAS uniform, uterine artery score using uniform definition of abnormal pulsatility index (PI) for both uterine arteries (PI > 1.20); UAS lateral placenta, uterine artery score using different definitions of abnormal PI values for the placental (PI > 1.0) and non-placental uterine arteries (PI > 1.40).  Uterine artery score and perinatal outcomeHernandez-Andrade et al. 440 Ultrasound in Obstetrics and Gynecology LP had similar sensitivity, 32.0% and 31.2%, and similarfalse-positives rates, 17.2% and 14.3%, respectively. No dif-ference between the two ROC curves was found ( P  = 0.49).For the total group with UAS ≥  2, there was a significantrisk of operative delivery for fetal distress, NICU admission,5-min Apgar score < 7, preterm delivery and SGA (Figure 1). DISCUSSION Maternal blood supply to the uterus is crucial for fetalwell-being, and low resistance to flow in the uterine arteriesis important for the maintenance of adequate placental per-fusion. Increased resistance to flow can be traced by Dopplervelocimetry in the uterine arteries. The scoring system pro-posed by Sekizuka et al  . 6  evaluates in a simple way the uterineartery waveform characteristics, high score values beingassociated with abnormal fetal outcome. In their scoringsystem, the cut-off RI values were based on the placentallocation. Using the same principle, we compared and testeda modified uterine artery score based on a uniform cut-off PI value for both uterine arteries (UAS uniform) and a differ-entiated uterine artery score based on cut-off values related tothe placental location (UAS LP). PI was used by us instead of RI,because PI describes the shape of the velocity waveform muchbetter, as it includes the area below the curve into the formula 9 .In the present study, it was possible to clearly locate theplacenta in one side of the uterus in 48% of the cases (359/ 741). In contrast, UAS uniform could be calculated in all 741cases. Placental location is not always possible to one side of the uterus as nearly 60% of placentae are located centrally inuncomplicated pregnancies 10 . Zimmermann and colleagues 4 have suggested that, in order to establish the Doppler wave-form parameters when estimating the placental location, thelowest value of the two uterine arteries should be consideredas the placental value. Other authors mentioned that theslight tendency of laterality in central placentae might beused to define the placental side location; however, in 40%of complicated pregnancies it was still not possible to estab-lish a side tendency in the placental location 11 . North andcoworkers 12  have reported a placental location in compli-cated pregnancies to be 35% on the left side, 34% on the rightside and 31% in the middle of the uterus. In their study, fordefinition of the normal Doppler parameters in cases withcentrally located placentae, a mean RI value of both uterinearteries was used.In our study, the group with UAS of 1 had a greater riskof adverse outcome than the group with normal uterine cir-culation (Table 1). One abnormal parameter in the uterineDoppler waveform as a marker of risk has been mentionedbefore by Hofstaetter et al  . 2 . They found the unilateral notchto be a better predictor of the perinatal outcome than the uni-lateral high PI. In other studies, high resistance on one side of the uterine circulation, represented by a high PI value, hasbeen associated with an increased risk of complications 13,14 .Conversely, Zimmermann et al  . 4  described a similar pre-valence of unilateral notching in high-risk pregnancies as inuncomplicated pregnancies, and Frusca and coworkers 15 found in selected high-risk pregnancies with a unilateraldiastolic notch a similar probability for an adverse perinataloutcome as among those with normal uterine circulation.The present study suggests that in the integrated system of UAS, an increased risk in pregnant women is identified evenat the level of UAS of 1, the most effective cut-off being UASof 2.The presence of unilateral or bilateral notches at 24–26 weeks in normal population has been associated with ahigh probability for developing intrauterine growth restric-tion and pre-eclampsia 16 . In high-risk pregnancies, this riskincreases up to 60% at this gestational age 17 . There seems tobe an agreement that uterine artery notch persisting after26 weeks of gestation should be considered a risk factor Tae 3 Diagnostic capacity o te two uterine artery scores (UAS) in preiction o averse perinata outcome   UAS uniformUAS lateral placenta ≥  1  ≥  2  ≥  3  ≥  4  ≥  1  ≥  2  ≥  3  ≥  4 Sensitivity (%)54.632.017.74.851.731.214.25.8Specificity (%)61.182.894.710067.785.793.998.4Positive predictive value (%)70.275.785.110072.076.976.189.6Negative predictive value (%)44.542.040.736.445.442.539.438.0UAS uniform, uterine artery score using uniform definition of abnormal pulsatility index (PI) for both uterine arteries (PI > 1.20); UAS lateral placenta, uterine artery score using different definitions of abnormal PI values for the placental (PI > 1.0) and non-placental uterine arteries (PI > 1.40). For the definition of adverse outcome see the text. Figure 1 Odds ratios and 95% confidence intervals for perinatal complications according to the values of the uterine artery score (UAS 1–4) as compared with the UAS of 0 (odds ratio, 1.0). NICU, neonatal intensive care unit; Umb V, umbilical vein; Umb A, umbilical artery; ODFD, operative delivery for fetal distress; PNM, perinatal mortality; SGA, small-for-gestational age.  Ultrasound in Obstetrics and Gynecology 441 Uterine artery score and perinatal outcomeHernandez-Andrade et al. for adverse pregnancy outcome. In our study group, onlyone case was included before 26 weeks (25 + 6 weeks) of gestation, most cases being examined during the last monthof gestation.In several reports, bilateral notching was associated withan increased probability of perinatal complications 4,18–20 .Park et al  . 21  have shown a positive predictive value of 90%when both a notch and a high systolic/diastolic ratio werefound and Thaler et al  . 5  reported an increased rate of ODFD,NICU admission and abnormal fetal heart rate (FHR) inlabor in pregnant women with an increased RI in both uterinearteries as compared with those with normal circulation. Ina high-risk population the presence of unilateral or bilateralnotches after 24 weeks of gestation has been associated witha 60% possibility of developing an adverse perinatal outcome.According to our results, a UAS of 2 was associated with a1.86 times increased risk for an adverse perinatal outcomeas compared with UAS of 0 (Table 1). Similarly, a UAS of 3 or 4 indicated at least a 1.77 times higher risk of adverseperinatal outcome. These results are in accordance with thoseof other authors who reported a sensitivity of 21%, specificityof 99% and positive predictive value of 92% when notchesand high resistance were found in both uterine arteries 22 .Comparable results have also been reported by our grouppreviously 2 .In the srcinal report by Sekizuka et al  . 6  on 89 patients,a UAS ≥  3 was reported to have a sensitivity, specificity andpositive predictive value of 74.5, 84.2 and 86.4%, respect-ively. The differences in the diagnostic capacity of thesrcinally reported score and the UAS modified by us can beprobably explained by different populations and definitionsof outcome.Using evaluation with ROC curves we have found theUAS ≥  2 to be the optimal definition of abnormal UAS for theprediction of adverse perinatal outcome and selection of arisk group for further close surveillance. In the group with aUAS < 2, fewer controls might be necessary, making the sur-veillance of high-risk pregnancies more efficient. Naturally,this suggestion should be tested prospectively.Risk estimation evaluated by means of odds ratios showedan increased risk for 5-min Apgar score < 7, ODFD, NICUadmission, SGA and preterm delivery when the UAS was ≥  2,indicating that the fetal well-being is affected by impaireduterine circulation (Figure 1). In the case of preterm deliveryand ODFD, it could be argued that they are related to a false-positive estimate of risk. However, as the uterine velocimetrywas not used for clinical decision-making, some other alteredparameters of the fetal well-being were already present atthe moment of the obstetric decision. The lack of a significantassociation between UAS and the ‘strong’ markers of adverseperinatal outcome (cord pH values and perinatal mortality)is frequently observed when correlations are attemptedbetween these markers and antenatal Doppler parametersand is probably due to clinical interventions consequenton umbilical artery velocimetry and FHR monitoring inlabor 21,22 .In conclusion, our results show that a UAS evaluating PIand the presence or absence of a notch irrespective of theplacental location is comparable with a UAS that takes theplacental location into account. The UAS uniform makesevaluation of the uterine artery velocimetry in the thirdtrimester of pregnancy simple, eliminating the difficulty of establishing a clear placental location, and shows a goodcorrelation with the perinatal outcome of complicatedpregnancies. The modified UAS concept should be nowtested in prospective clinical studies. ACKNOWLEDGMENTS The professional help in performing the uterine arteryDoppler examination by Ms Lena Berg, Maria Nilsson, PiaSoikkeli and Ann Thuring-Jönsson is gratefully acknow-ledged. Edgar Hernandez-Andrade was supported by theMexican National Council for Science and Technology(CONACyT) and the National Institute of Perinatal Medi-cine (INPer) in Mexico City. The study was supported by theSwedish Medical Research Council (grant number 5980). REFERENCES 1Campbell S, Diaz-Recasens J, Griffin D, Cohen-Overbeek T,Pearce J, Wilson K, Teague M. New Doppler technique for assessingutero-placental blood flow. Lancet   1983; i: 675–72Hofstaetter C, Dubiel M, Gudmundsson S, Mar s ál K. Uterine arterycolor Doppler assisted velocimetry and perinatal outcome. ActaObstet Gynecol Scand   1996; 75: 612–93Morris J, Fay R, Ellwood D. 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