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Increased uterine artery vascular impedance is related to adverse outcome of pregnancy but is present in only one-third of late third-trimester pre-eclamptic women

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Increased uterine artery vascular impedance is related to adverse outcome of pregnancy but is present in only one-third of late third-trimester pre-eclamptic women
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  Ultrasound Obstet Gynecol   2005;  25 : 459–463Published online in Wiley InterScience (www.interscience.wiley.com).  DOI:  10.1002/uog.1895 Increased uterine artery vascular impedance is relatedto adverse outcome of pregnancy but is present in onlyone-third of late third-trimester pre-eclamptic women H. LI, H. GUDNASON, P. OLOFSSON, M. DUBIEL and S. GUDMUNDSSON University of Lund, Department of Obstetrics and Gynecology, Malm¨ o University Hospital, Malm¨ o, Sweden KEYWORDS : blood flow; Doppler, growth restriction; placenta; pre-eclampsia; pregnancy; ultrasound ABSTRACT Objective  Signs of increased uterine artery vascularimpedance in mid-gestation are strongly related to pre-eclampsia later in pregnancy. Whether this is true for thelate third trimester is, however, unclear. The aim of the present study was to analyze the frequency of increased uterine artery vascular impedance in the third trimester,and its relationship to abnormal umbilical artery Dopplerand adverse outcome of pregnancy.  Methods  This was a retrospective study of uterine and umbilical artery Doppler velocimetry in 570 pregnanciescomplicated by pre-eclampsia. The managing clinicianwas informed only about the umbilical artery flow.The Doppler recordings were related to severity of pre-eclampsia, prematurity, fetal growth restriction, and ratesof Cesarean section and admission to neonatal intensivecare.  Results  Increased umbilical artery vascular impedancewas seen in 59 cases (10.4%), seven having absent orreversed end-diastolic flow. Uterine artery notching wasseen in 145 cases (25%), 88 (15%) having bilateral notches. Either increased uterine artery pulsatility index(PI) or notching, or both, were seen in 207 women(36.3%). In 108 women with severe pre-eclampsia, 38(35.2%) had uterine artery notching. Signs of increased uteroplacental vascular impedance were more common insevere than in mild pre-eclampsia (57.4% vs. 31.4%),in premature than in term pregnancies (70.9% vs.28.4%), and were more prevalent than abnormality inthe umbilical artery (36.3% vs. 10.4%). Conclusion  Only one-third of pre-eclamptic casesshowed signs of increased uterine artery vascularimpedance in the third trimester. However, signs of increased vascular impedance were much more frequent in the uterine than in the umbilical arteries and werestrongly related to adverse outcome of pregnancy. Copy-right   © 2005 ISUOG. Published by John Wiley & Sons,Ltd. INTRODUCTION Doppler ultrasound has become a valuable tool inthe evaluation of the fetal and placental circulationand in the prediction of pregnancy outcome. Increasedplacental vascular impedance is frequently related tofetal growth restriction 1 , 2 . Umbilical artery Dopplervelocimetry is presently used in many centers for fetalsurveillance in pregnancies complicated by pre-eclampsiaand intrauterine growth restriction (IUGR). Dopplerinformation has been found to reduce the number of emergency operations, hospital admissions, and daysin hospital for both mother and newborn in cases of suspected IUGR 3 .Uterine artery Doppler evaluation provides importantinformation on the normal physiological transforma-tion of subplacental arteries. The transformation of the spiral and radial arteries is normally complete at20 to 24 weeks of gestation 4 . Uteroplacental vascularimpedance decreases gradually during vessel transforma-tion, but is fairly stable after 24 weeks of gestation 5–7 .Increased uteroplacental vascular impedance at 24 weeksof gestation is strongly related to the development of pre-eclampsia and/or IUGR later in pregnancy 8 , 9 . Thepredictive value of high uterine vascular impedance in thelate third trimester is, however, unclear.The aim of the present study was to investigate thefrequency of abnormal uterine artery Doppler and its Correspondence to:  Dr S. Gudmundsson, Department of Obstetrics and Gynecology, Malm ¨o University Hospital, S-205 02 Malm ¨o, Sweden(e-mail: saemundur.gudmundsson@obst.mas.lu.se) Accepted: 27 January 2005 Copyright © 2005 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER  460  Li et al. implication in third-trimester pregnancies complicated bypre-eclampsia. METHODS A retrospective analysis was performed on 570 womenadmitted to hospital for pre-eclampsia over a 7-yearperiod (1994–2000). All women gave their informedconsent for the study, which was approved by the localethics committee.The median maternal age was 30 (range, 17–46)years. Uterine and umbilicalartery Doppler velocimetry isroutinelyperformedatourunitinallpregnanciesadmittedforpre-eclampsia,unlesstheydeliversoonafteradmissionor are diagnosed when in labor. Patients admitted witheclamptic fits, HELLP syndrome or those admitted duringnight duties or weekends were excluded. Pre-eclampsiawas defined as a blood pressure ≥ 140/90 mmHg andpresence of proteinuria of  ≥ 0 . 3 g/L or a 1 +  urinedipstick on two occasions at least 12 h apart and atrest. Mild pre-eclampsia was defined as a systolic bloodpressure of 145–155 mmHg and a diastolic pressure of 90–105 mmHgandproteinuria + 1or + 2( ≥ 0 . 3 g/Land < 3 . 0 g/L). Severe pre-eclampsia was defined as a systolicblood pressure ≥ 160 mmHg and diastolic ≥ 110 mmHgand proteinuria of  + 3 ( ≥ 3 g/L).The blood flow measurements were performed with anAcuson 128 XP and Sequoia (Siemens/Acuson, MountainView, CA, USA) duplex scanner with pulsed and colorDoppler option. The uterine artery blood velocity wasrecorded from both uterine arteries after the vesselswere identified by color flow mapping in an obliquescan with the sample volume placed in the artery justcranial to the anatomical crossing of the external iliacartery. Three even blood flow velocity waveforms wererecorded and analyzed for pulsatility index (PI) accordingto Gosling  et al  . 10 as a marker of vascular impedance. Anincreased uterine artery vascular impedance was definedas a mean PI  > 1 . 20 2 . Presence of an early diastolic notchin the uterine blood velocity spectrum, as a marker of uteroplacental vessel wall compliance, was also noted asdescribed by Campbell  et al  . 11 . The uterine artery bloodflow velocity waveform spectrum was classified into fiveuterine artery scores (UAS) according to Gudmundsson et al  . 2 (Table 1). Abnormal uterine artery Doppler wasdefined as UAS  > 0.The umbilical artery Doppler flow spectrum wasrecorded from a free-floating central part of the umbilicalcord. The mean of three even blood velocity waveformswere analyzed for PI and related to reference values 12 .An absent or reversed end-diastolic flow velocity (ARED)was noted. The waveform pattern was classified intoblood flow class (BFC) according to Gudmundsson  et al  . 2 (Table 1). The UAS and the BFC were combined toform a placental score (PLS) as an expression of thegeneral placental vascular resistance: PLS = BFC + UAS,with scores ranging from 0 to 7 2 .Serial Doppler examinations were usually performedat intervals of less than 3 weeks. Only the results of the Table 1  Definitions of the uterine artery score (UAS) system andumbilical artery blood flow classes (BFC) Score/Class Definition UAS 0 Normal blood flow velocity waveforms in bothuterine arteries1 One abnormal parameter (high PI ( > 1.2) or adiastolic notch) present2 Two abnormal parameters present3 Three abnormal parameters present4 Four abnormal parameters present (bilateralnotch and high PI)BFC 0 Normal umbilical artery blood flow velocitywaveforms1 PI between + 2 and + 3 SD above the mean2 PI  > + 3 SD above the mean but forward flowin diastole3 Absent or reversed end-diastolic flowPI, pulsatility index. last examination were used for analysis. The managingclinicianwasinformedabouttheumbilicalarteryDopplermeasurements, but not those of the uterine artery. Themedian gestational age at the last examination was 38(range, 28–43) completed weeks and at delivery 39(range, 28–43) weeks. The median time interval fromthe last Doppler examination to delivery was 1 (range,1–15) day. Parity, gestational age at last ultrasound,gestational age at birth, birth weight, weight deviationfrom the gestational age-adjusted mean birth weight inthe population, placental weight, Apgar score at 1, 5and 10 min, small-for-gestational age (SGA) newborns,prematurity (birth  < 37 completed weeks), and Cesareansection, were all recorded. SGA was defined as a birthweight below mean − 2 SD of the local population 13 .Descriptive statistics in terms of mean and SDwere calculated. Comparison of means and trendswere performed with Spearman’s rank correlation withthe statistical computer program MedCalc ® version6.00.014 (MedCalc Software, Mariakerke, Belgium).Receiver–operating characteristics (ROC) curves weredrawn for each diagnostic index or score to evaluateits ability to discriminate the likelihood of developingadverse perinatal outcome 14 . The area under the curveand 95% confidence intervals (CI) were also calculatedusing the MedCalc software. If the lower limit of the CIfor the area under the ROC curve was more than 0.5, thediagnostictestwasconsideredtobeabletopredictadverseperinatal outcome 15 , 16 . The optimal cut-off for each scorewas also calculated by the computer program, giving avalue with highest accuracy (minimal false-negative andfalse-positive results). RESULTS Of the 570 pregnant women with pre-eclampsia, 383were nulliparae (67.2%). An increased umbilical arteryvascular impedance was found in 59 cases (10.4%), 7 of them having ARED. Uterine artery Doppler velocimetry Copyright © 2005 ISUOG. Published by John Wiley & Sons, Ltd.  Ultrasound Obstet Gynecol   2005;  25 : 459–463.  Pre-eclampsia and uterine Doppler  461 Table 2  Uterine artery score (UAS) and umbilical artery blood flow class (BFC) in 570 pre-eclamptic pregnancies UASBFC 0 1 2 3 4 Total (%) 0 347 65 64 27 8 511 (89.6)1 10 7 7 7 4 35 (6.1)2 6 3 4 1 3 17 (3.0)3 0 1 4 0 2 7 (1.2)Total (%) 363 (63.7) 76 (13.3) 79 (13.9) 35 (6.1) 17 (3.0) Table 3  Perinatal outcome in relation to the uterine artery score (UAS) system UASParameter 0 1 2 3 4  P Total  n  363 76 79 35 17Nulliparous  n  (%) 249 (69) 49 (64) 51 (65) 25 (71) 9 (53) NSSevere pre-eclampsia  n  (%) 46 (13) 20 (26) 20 (25) 12 (34) 10 (59)  < 0 . 0001 Gestational age at delivery (weeks, mean ± SD)  39 . 2 ± 1 . 9 37 . 0 ± 3 . 2 36 . 7 ± 3 . 9 35 . 6 ± 3 . 9 31 . 9 ± 5 . 0  < 0 . 0001 Birth weight (g, mean ± SD)  3548 ± 824 2765 ± 845 2630 ± 891 2318 ± 667 1528 ± 905  < 0 . 0001 Weight deviation from mean (%)  0 . 18 ± 15  − 8 . 77 ± 12  − 11 . 15 ± 13  − 17 . 03 ± 14  − 22 . 54 ± 12  < 0 . 0001 Cesarean section  n  (%) 94 (26) 29 (38) 33 (42) 22 (63) 12 (71)  < 0 . 0001 Delivery  < 37  weeks  n  (%) 34 (9) 21 (28) 29 (37) 20 (57) 13 (76)  < 0 . 0001 Delivery  < 34  weeks  n  (%) 6 (2) 12 (16) 13 (16) 6 (17) 9 (53)  < 0 . 0001 SGA newborn  n  (%) 25 (7) 10 (13) 16 (20) 11 (31) 8 (47)  < 0 . 0001 NICU admission  n  (%) 9 (2) 2 (3) 8 (10) 6 (17) 4 (24)  < 0 . 0001 NICU, neonatal intensive care unit; NS, non-significant; SGA, small-for-gestational age. Spearman’s rank correlation analysis was used forstatistical analyses. Table 4  Receiver–operating characteristic analyses of placental indices and scores in relation to prediction of a small-for-gestational age(SGA) newborn and premature birth ( < 37  weeks) Area under the curve 95% CI Optimal cut-off Sensitivity Specificity SGAMean uterine artery PI 0.861 0.781–0.921  > 2.33 0.89 0.87Umbilical artery PI 0.746 0.708–0.781  > 1 0.65 0.77PLS 0.744 0.706–0.780  > 0 0.73 0.66UAS 0.682 0.642–0.720  > 0 0.62 0.68BFC 0.677 0.637–0.716  > 0 0.41 0.94PrematurityMean uterine artery PI 0.839 0.755–0.903  > 2.08 0.82 0.80Umbilical artery PI 0.824 0.790–0.854  > 0.97 0.73 0.80PLS 0.777 0.741–0.811  > 0 0.76 0.70UAS 0.748 0.710–0.783  > 0 0.71 0.73BFC 0.635 0.594–0.675  > 0 0.32 0.95BFC, blood flow class; CI, confidence interval; PLS, placental score; UAS, uterine artery score. revealed that 145 women (25%) had diastolic notching,88havingbilateralnotches.TherelationshipbetweenUASand BFC is given in Table 2. There were 62 cases withuterine artery PI  > 1 . 20 as the only sign of increasedvascular impedance, 14 having bilateral increased PIwithout notching. Signs of increased vascular impedancewere frequently seen on only one side of the placenta; 164cases on the maternal side and 16 on the fetal side of theplacenta.Women delivering before 34 weeks of gestation hadthe highest frequency of increased uterine artery vascularimpedance, this occuring in 40/46 (87%) cases. Thecorresponding figures for premature birth ( < 37 weeks)were83/117(70.9%)and129ofthe453termpregnancies(28 · 4%) had increased uterine artery impedance. Eighty-two of the 117 premature cases (70%) were delivered byCesarean section due to worsening fetal and/or maternalcondition. Forty (34%) of the premature cases were SGAat birth and 23 cases (20%) were admitted for neonatalintensive care.In 108 women with severe pre-eclampsia, 38 (35.2%)had uterine artery notching. Signs of an increased Copyright © 2005 ISUOG. Published by John Wiley & Sons, Ltd.  Ultrasound Obstet Gynecol   2005;  25 : 459–463.  462  Li et al. 0102030405060708090100PLS0 1 2 3 4 5 6 7    F  r  e  q  u  e  n  c  y   (   %   ) Figure 1  Frequency of premature birth ( < 37  weeks) ( ž ),small-for-gestational age newborns (  ) and Cesarean section (  )according to placental score (PLS). uteroplacental vascular impedance were more commonin severe than in mild pre-eclampsia (57.4% vs. 31.4%, P  <  0 . 0001), and were more prevalent than abnormalityin the umbilical artery (36.3% vs. 10.2%,  P  <  0 . 0001).There was no difference in PLS between nulliparous andparous women.Abnormal uteroplacental blood flow velocity wassignificantly related to adverse outcome (Table 3). Thefrequency of Cesarean delivery was 190/570 (33.3%).The greater the vascular impedance in the uterine arteries,the greater the frequency of complications (Table 3).Umbilical and uterine artery PI and the three placentalscore systems were compared with ROC analyses relativeto SGA newborns and premature birth. The uterine arteryPI was the best indicator of adverse outcome, followed byumbilical artery PI. Regarding the score systems, the PLSwasthebestindicatorofadverseoutcome,followedbytheUAS system (Table 4). Figure 1 illustrates the relationshipbetween PLS and three outcome variables: prematurebirth, an SGA newborn and delivery by Cesarean section.There were only two cases with a PLS of 7, one died in utero  at 23 weeks of gestation and was deliveredvaginally. There was only one other perinatal death, acase diagnosed with mild pre-eclampsia at 42 weeks of gestation.Placentalbloodflowwasnormal(PLS0).Laborwas induced. The fetus showed signs of asphyxia duringinduction and was delivered by emergency Cesareansection. The infant weighing 3560 g was stillborn. DISCUSSION This study shows that in pre-eclamptic third-trimesterpregnancies only 25% of cases have uterine artery notch-ing. Even in severe pre-eclampsia, uterine artery notchingwas recorded in only 35% of cases. Abnormal uterinearteryvelocimetrywasmorefrequentinpregnanciesdeliv-eredprematurely,87%  < 34 weeksand71% < 37 weeks.A strong correlation was seen between increased uter-ine artery vascular impedance and adverse outcome of pregnancy.Abnormal uterine artery blood flow was more commonthanabnormalumbilicalarterybloodflow,36%vs.10%.A strong correlation was seen between increased uterineartery vascular impedance and vascular impedance in theumbilical artery. PI in the uterine and umbilical arterieshad higher predictive values for SGA and premature birththan did UAS or PLS (Table 4).Most of the previous uterine artery Doppler studieshave addressed the relationship between mid-gestationscreening and outcome of pregnancy. Abnormal uterineartery blood flow velocity waveforms have been reportedtohaveahighsensitivityforthepredictionofdevelopmentof IUGR and/or pre-eclampsia later in pregnancy 8 . Theresults of the present study confirm our previous study 17 ,but are in conflict with the results reported by Frusca et al  . 18 . In the latter study, 88% of cases with pre-eclampsia had abnormal uterine artery blood flow. Webelieve that the different results are due tomethodologicaldifferences with a selection of more severe cases of hypertension and a different definition of abnormaluterine artery flow in the study by Frusca  et al  . 18 . Joern  et al  . 19 examined uterine artery blood flowvelocity in 102 pregnancies complicated by HELLPsyndrome. An increased vascular impedance was presentin as many as 95% of cases. This and our results indicatethat the most severe and the most premature cases aremore likely to have abnormal uterine artery Doppler.In our study, the frequency of abnormal uterine arteryblood flow velocity was 87% in pregnancies deliveredbefore 34 weeks,71% inthose deliveredbefore 37 weeks,but only 28% in term pregnancies. The severity of pre-eclampsia was also more frequent in the preterm cases.In the present study only 21% of women deliveredbefore37completedweeks,andonly8%before34 weeks.Since this was a hospital based cohort study, the vastmajority of pregnancies complicated by pre-eclampsiain the city of Malm ¨o were included. However, someof the cases admitted and delivered the same day orduring weekends were not included. Some of the mostsevere cases may therefore have been missed as theywere delivered promptly. Cases with mild pre-eclampsia,diagnosedonlaboradmission,mayalsohavebeenmissed.The study material is thus a good representation of thetotal population.In a study by Vergani  et al  . 20 on pregnancies suspectedof having IUGR after 34 weeks of gestation, only 37%had abnormal uterine artery Doppler. Abnormal uterineartery blood velocity was also related to adverse outcomeof pregnancy.Thenormalphysiologicaltransformationofthesubpla-cental vessels is complete at 24 weeks of gestation. Con-sequently, uterine artery vascular impedance decreasesuntil 24 weeks of gestation as a reflection of vesseltransformation 21 , 22 . In normal pregnancy after 24 weeksof gestation, uterine artery vascular impedance remainsalmostunchangedfortheremainderofgestation 5–7 .Sore-garoli  et al  . 23 performed uterine artery Doppler screeningat 24, 28–30, and 32–34 weeks and reported that abnor-mal uterine artery flow velocity waveforms recorded at24 weeks had normalized in 49% of cases at 34 weeks.This phenomenon may support our findings, suggestinga lower sensitivity of abnormal uterine artery Doppler Copyright © 2005 ISUOG. Published by John Wiley & Sons, Ltd.  Ultrasound Obstet Gynecol   2005;  25 : 459–463.  Pre-eclampsia and uterine Doppler  463 in late third-trimester pre-eclamptic pregnancies. Uter-ine artery blood flow abnormalities recorded in the latesecondtrimestermaythusdisappearinthethirdtrimester. ACKNOWLEDGMENTS This study was supported by grants from the MedicalFaculty, University of Lund, the Swedish Society of Medicine,andtheUniversityHospital,Malm ¨o.Mss.LenaBerg, Emma Nilsson, Maria Nilsson, and Pia Soikkeliare gratefully acknowledged for performing the Dopplerrecordings. REFERENCES 1. Gudmundsson S, Marsal K. Blood velocity waveforms in thefetal aorta and umbilical artery as predictors of fetal outcome. Am J Perinatol   1991;  8 : 1–6.2. Gudmundsson S, Korszun P, Olofsson P, Dubiel M. A newscore indicating placental vascular resistance.  Acta Obstet Gynecol Scand   2003;  82 : 807–812.3. Almstrom H, Axelsson O, Cnattingius S, Ekman G, Mae-sel A, Ulmsten U, Arstrom K, Marsal K. Comparison of umbilical-artery velocimetry and cardiotocography for surveil-lance of small-for-gestational-age fetuses.  Lancet   1992;  340 :936–940.4. Brosens I, Robertson WB, Dixon HG. 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Multicenter screening for pre-eclampsia and fetalgrowth restriction by transvaginal uterine artery Doppler at23 weeks of gestation.  Ultrasound Obstet Gynecol   2001;  18 :441–449.10. Gosling RG, Dunbar G, King DH, Newman DL, Side CD,Woodcock JP, Fitz-Gerald DE, Keates JS, MacMillian D. Thequantitative analysis of occlusive peripheral arterial diseaseby a non-intrusive ultrasound technique.  Angiology  1971;  22 :52–55.11. Campbell S, Diaz-Recasens J, Griffin DR, Cohen-Overbeek TE,Pearce JM, Willson K, Teague MJ. New Doppler technique forassessing utero-placental blood flow.  Lancet   1983;  1 : 675–677.12. Gudmundsson S, Mars ´al K.Umbilicalartery and uteroplacentalblood flow velocity waveforms in normal pregnancy – a cross-sectionalstudy. ActaObstetGynecolScand  1988; 67 :347–354.13. Marsal K, Persson PH, Larsen T, Lilja H, Selbing A, Sultan B.Intrauterine growth curves based on ultrasonically estimatedfoetal weights.  Acta Paediatr  1996;  85 : 843–848.14. 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Vergani P, Roncaglia N, Andreotti C, Arreghini A, Teruzzi M,Pezzullo JC, Ghidini A. Prognostic value of uterine arteryDoppler velocimetry in growth-restricted fetuses delivered nearterm.  Am J Obstet Gynecol   2002;  187 : 932–936.21. den Ouden M, Cohen-Overbeek TE, Wladimiroff JW. Uterineand fetal umbilical artery flow velocity waveforms in normalfirst trimester pregnancies.  Br J Obstet Gynaecol   1990;  97 :716–719.22. Kaminopetros P, Higueras MT, Nicolaides KH. Doppler studyof uterine artery blood flow: comparison of findings in the firstand second trimesters of pregnancy.  Fetal Diagn Ther  1991;  6 :58–64.23. Soregaroli M, Valcamonico A, Scalvi L, Danti L, Frusca T.Late normalisation of uterine artery velocimetry in high-riskpregnancy.  EurJObstetGynecolReprodBiol  2001; 95 :42–45.Copyright © 2005 ISUOG. Published by John Wiley & Sons, Ltd.  Ultrasound Obstet Gynecol   2005;  25 : 459–463.
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