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Clinical significance of uterine artery blood flow velocity waveforms during provoked uterine contractions in high-risk pregnancy

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Clinical significance of uterine artery blood flow velocity waveforms during provoked uterine contractions in high-risk pregnancy
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  Ultrasound Obstet Gynecol   2004;  24 : 429–434Published online in Wiley InterScience (www.interscience.wiley.com).  DOI:  10.1002/uog.1708 Clinical significance of uterine artery blood flow velocitywaveforms during provoked uterine contractions inhigh-risk pregnancy H. LI*†, S. GUDMUNDSSON* and P. OLOFSSON* Departments of Obstetrics and Gynecology,  * Malm¨ o University Hospital, University of Lund, Malm¨ o, Sweden and   † No. 2 Clinical Hospital, China Medical University, Shenyang, People’s Republic of China KEYWORDS : contraction; Doppler; flow; labor; oxytocin; pregnancy; resistance; uterine ABSTRACT Objective  To determine whether, in a group of high-risk pregnanciesundergoinganoxytocinchallengetest(OCT),uterine artery Doppler velocimetry will identify fetuses at risk of distress during the provoked contractions.  Methods  Bilateral uterine artery Doppler velocimetrywas performed simultaneously with electronic fetal heart rate (FHR) recordings in 67 high-risk pregnanciessubjected to an OCT. Flow velocity waveforms (FVWs)wereclassifiedaccordingtopulsatilityindex(PI),presenceof diastolic notching and a novel classification of FVW shapes. The OCT was classified as negative (normal) or positive (late FHR decelerations). Only OCT-negativecases were allowed a trial of vaginal delivery. Non- parametric statistical methods were used to test fordifferences between the OCT groups.  Results  There was no difference in prevalence of high PI or diastolic notching in OCT-positive (  n = 10) and OCT-negative (  n = 57) cases at basal (resting) measurementsor between uterine contractions in either uterine artery(  P ≥ 0 . 3). During contractions the PI could not be used for assessment due to the biphasic shape of the FVWs,but there was no difference in distribution of FVW classes between the groups in either the placental side(  P ≥ 0 . 3) or contraplacental side (  P ≥ 0 . 6) uterine artery.No significant associations between PI or FVW classdistribution and birth asphyxia or operative delivery forfetal distress in labor were found (  P ≥ 0 . 1). Conclusions  During uterine contractions there is nodifference in uterine artery FVW pattern between OCT- positive and OCT-negative cases. Recording of uterineartery FVWs during the OCT seems to be of limited clinical relevance. Copyright   ©  2004 ISUOG. Published by John Wiley & Sons, Ltd. INTRODUCTION Together with intrapartum fetal heart rate (FHR)recordings, Doppler velocimetry of uteroplacental andumbilicoplacental blood flow during uterine contractionsis a means of identifying fetuses at risk of fetal distress inlabor. In fetuses with an intact defense against hypoxia,umbilical artery vascular flow resistance does not changeduring contractions 1–5 , whereas an increased vascularflow resistance during contractions indicates a defectiveability to cope with anaerobic stress 6 . In accordance withthis,Olofsson et al  . 7 foundapositive(abnormal)outcomeof the oxytocinchallenge test (OCT) tobe associatedwithan increased umbilical artery pulsatility index (PI).In contrast to umbilical artery flow resistance, theuterine artery flow resistance increases strongly duringcontractions 2 , 4 , 8 , 9 , and there is evidence that the increaseis more marked in cases of an insufficient placentalfunction. In a study on uterine and umbilical circulationsduring the OCT, the increase of uterine artery PI washigher in cases of a positive OCT, reflecting placentalinsufficiency, than in cases of a negative OCT 7 . Theaim of the present study was to investigate the potentialclinicalvalueofuterinearteryDopplervelocimetryduringuterine contractions in a series of high-risk pregnanciesundergoing the OCT. METHODS Sixty-seven women with singleton pregnancies  ≥ 36completed weeks’ gestation were subjected to an OCT onthe following clinical indications: 55 because of suspectedintrauterine growth restriction (IUGR) (nine also withpre-eclampsia), two with prolonged pregnancy, two witholigohydramnios, five with decreased fetal movements, Correspondence to:  Dr P. Olofsson, Department of Obstetrics and Gynecology, Malm ¨o University Hospital, S-205 02 Malm ¨o, Sweden(e-mail: per.olofsson@obst.mas.lu.se) Accepted: 20 April 2004 Copyright © 2004 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER  430  Li et al. and because of a poor obstetric history in three women.The indication to perform an OCT was the managingobstetrician’s uncertainty about the optimal time andmode of delivery, and a high umbilical artery PI was thenan additional indication in 20 cases. The procedure of performing simultaneous recordings of FHR and Dopplerevaluation of flow velocity waveforms (FVWs) duringthe OCT was approved by the Lund University ResearchEthics Committee and all participating women gave theirinformed consent.Theprocedureprotocolhasbeendescribedpreviously 7 .Basal (resting) Doppler blood flow measurements wereperformed immediately prior to the OCT. Women withabsent or reversed diastolic umbilical artery flow weredelivered by Cesarean section and not included inthe study. To mimic labor contractions, an oxytocininfusion was started and the infusion rate increasedstepwise until three uterine contractions per 10-minperiodoccurred.Dopplervelocimetrywasthenperformedduring contractionsandrelaxations andthe FHR patternsinterpreted relative to contractions. The OCT wasclassified as normal (negative) or pathological (positive)according to Freeman 10 . In cases of a positive OCT, aCesarean section was performed the same day. When theOCT was negative, labor was induced or spontaneouslabor awaited. The median time from OCT to deliverywas 1 (range, 0–21) days.AnAcuson128XP(Acuson,MountainView,CA,USA)Doppler ultrasound machine equipped with pulsed andcolor Doppler options (3.5- and 5-MHz transducers)was used during the first part of the study and anAcuson Sequoia 512 (Acuson) with a 6C2 multiHertzprobe (step-less from 2.5 to 6 MHz) in the secondpart of the study. The iliac and uterine arteries wereidentified with Doppler color flow mapping and uterineartery FVWs recorded by Doppler velocimetry at aninsonation angle  < 25 ◦ just cranial to the crossing withthe external iliac artery 11 . To ensure that the Dopplershift sampling volume was maintained in the uterineartery during the procedure, rapid switches betweenvelocimetry and color flow mapping were performed. Allrecordings were videotaped for later analysis. The meanPI 12 was calculated from three consecutive waveformsobtained prior to OCT (basal measurements) and duringuterine relaxation between contractions, and during thepeak of contractions. The results of OCT and basalumbilical artery Doppler velocimetry were disclosed tothe managing obstetrician, but uterine artery recordingsbefore or during the OCT were not used for clinicalguidance.During basal conditions and uterine relaxations theuterine artery PI was classified as normal when withinmean  ± 2 SD, i.e. between 0.41 and 1.19, and as highwhen  ≥ 1.20 according to reference values 11 . ‘Diastolicnotching’oftheFVW 13 wasassessedvisuallyasabiphasicshape of the waveform in diastole where the velocityduring the nadir of the ‘notch’ was lower than the peakvelocity of the diastolic phase.For basal measurements PI and presence or absence of diastolic notching were considered and classified as partof the uterine artery scoring (UAS) system according toHernandez-Andrade  et al  . 14 , namely Score 0: no notchingor high PI in any uterine artery; Score 1: notching orhigh PI unilaterally; Score 2: two signs of notching and/orhigh PI present; Score 3: three signs of notching and highPI present and Score 4: notching and high PI presentbilaterally in the uterine arteries.We have recently described and classified 11 differentshapes of FVWs occurring during uterine contractions,including biphasic and reversed flows 15 . The base forthe classification system is the time-averaged mean flowvelocityrecordedovertheheartcycle( V  mean ).Incasesofapredominantly reversed diastolic flow, i.e. with a negative V  mean  value, calculation of PI is not relevant, and in caseswith biphasic or reversed flow identification of diastolicnotches is also irrelevant.To enhance the understanding and statistical analysesof FVWs obtained during contractions the 11 wave-form shapes were condensed to five classes (Table 1):(1) maintained forward flow during both systole anddiastole; (2) forward systolic and absent diastolic flow;(3) forward systolic and reversed diastolic flow (biphasicflow); (4) absent systolic and diastolic flow and (5) bothsystolic and diastolic flow reversed 15 .The placental position was determined by ultrasono-graphy and classified as central when its mass was equallypositioned between the right and left sides (irrespective of its anteroposterior or fundal position), and lateral when > 75% of the mass was asymmetrically positioned 16 .In cases of a laterally positioned placenta, the PI valueobtained from the ipsilateral uterine artery during basalconditionswaschosentobestrepresenttheuteroplacentalcirculation. In cases of a centrally positioned placenta theartery with the lowest PI was chosen to best represent theplacenta.TheuterinearteryFVWrecordingswerecomparedwithregard to the OCT result (positive or negative), operativedelivery for fetal distress (ODFD) in cases of negativeOCT (abdominal, ventouse or forceps delivery due toabnormal FHR tracings) and birth asphyxia (defined as a5-min Apgar score  < 7 and/or umbilical cord arterial pH < 7.10 and/or venous pH  < 7.15).Appropriate-for-gestational age (AGA) was defined asa birth weight within mean ± 2 SD, small-for-gestationalage (SGA) as  ≥ 2 SD below the mean, and large-for-gestational age (LGA) as ≥ 2 SD above the mean 17 . Statistical analysis The Chi-square test and Fisher’s exact test wereused for comparison of categorical variables, and theMann–Whitney  U  -test and Kruskal–Wallis test forcomparison of cross-sectional, non-paired, continuousvariables.Valuesare reportedas mean ± SD.A two-tailed P  value  < 0.05 was considered significant. Statistics wereperformedwithStatView ® (SASInstitute,Cary,NC,USA) Copyright © 2004 ISUOG. Published by John Wiley & Sons, Ltd.  Ultrasound Obstet Gynecol   2004;  24 : 429–434.  Uterine flow during OCT   431 Table 1  Classification of flow velocity waveforms (FVWs) recordedby Doppler velocimetry in the uterine arteries during contractions FVW patterns Class Description 1 Maintained forwardflow during bothsystole and diastole2 Forward systolic andabsent diastolicflow3 Forward systolic andreversed diastolicflow4 Absent flow over thewhole heart cycle5 Both systolic anddiastolic flowreversed andMedCalc ® (MedCalcSoftware,Mariakerke,Belgium)computer software. RESULTS The OCT was positive in 10 (15%) and negative in 57(85%) cases. During basal Doppler flow measurementsuterine artery FVWs were obtained from both uterinearteries in all cases; during the OCT FVWs were recordedfrom the ipsilateral (placental side) uterine artery in 63cases and from the contralateral (contraplacental side)artery in 60 cases. In one OCT-positive case FVWs werenot obtained from the placental side uterine artery duringthe OCT, and in another OCT-positive case from thecontraplacental side artery.Due to the small number of OCT-positive cases,for comparisons of UAS and of FVW classes duringcontractions the different scores and classes had to bemerged to allow statistical analyses with the Chi-squaretest at a degree of freedom  > 1. Even then, the numberof cases for comparison were occasionally too few forthe Chi-square test (number  < 5 in merged classes), andthe analyses were then performed with Fisher’s exact testwith merging of rows at different levels in 2 × 2 tables(e.g. FVW Class 1 compared with Classes 2–5, Classes1–2 compared with classes 3–5, etc.).There wasnodifferenceinUASfor basalmeasurementsbetween the OCT groups (Fisher’s exact test on mergeddata,  P ≥ 0 . 2, table not shown). Uterine artery FVWclasses relative to the OCT results are shown in Table 2.Nostatisticallysignificantdifferenceswerefoundbetweenthe positive and negative OCT groups in either uterineartery for measurements obtained during basal conditionsor during relaxation. In the placental side artery onlyFVW Class 2 and Class 3 flows were recorded in theOCT-positive group, whereas for OCT-negative casesClass 1 and Class 5 flow were also recorded.During basal conditions the PI was not significantlydifferent in the OCT-positive group compared withthe OCT-negative group in either the placental side(0 . 83 ± 0 . 25 vs. 0 . 70 ± 0 . 21; Mann–Whitney  U  -test, P = 0 . 1) or the contraplacental side (1 . 07 ± 0 . 51 vs.0 . 97 ± 0 . 42; Mann–Whitney  U  -test,  P = 0 . 6) uterineartery. Similarly, during relaxations there were nodifferences between the groups (0 . 75 ± 0 . 21 vs. 0 . 70 ± 0 . 18; Mann–Whitney  U  -test,  P = 0 . 5, and 0 . 96 ± 0 . 37vs. 0 . 95 ± 0 . 37; Mann–Whitney  U  -test,  P = 0 . 9). Dueto the biphasic FVW pattern in the majority of cases(Table 2) the PI could not be calculated during uterinecontractions.Three cases of ODFD in labor occurred in theOCT-negative group. In comparison with cases withoutODFD ( n = 54) the uterine artery PI was not significantlydifferent in either artery, nor from basal measurements(Mann–Whitney  U  -test,  P = 0 . 1, 0.3) nor from measure-ments during uterine relaxations (Mann–Whitney  U  -test, P = 0 . 1, 0.3). No difference in FVW class distributionwas found during uterine contractions (Fisher’s exact teston merged data,  P ≥ 0 . 2). Copyright © 2004 ISUOG. Published by John Wiley & Sons, Ltd.  Ultrasound Obstet Gynecol   2004;  24 : 429–434.  432  Li et al. Table 2  Uterine artery flow velocity waveforms classes (see Table 1) relative to the result of the oxytocin challenge test * ParameterOCT-negative(  n = 57  †  )OCT-positive(  n = 10 ‡  ) Significance of differenceBasal measurements Placental side arteryNormal PI, no notching 15 4Normal PI, notching 38 5  High PI:  P = 0 . 6 High PI, no notching 3 0 Notching:  P = 0 . 7 High PI, notching 1 1Contraplacental side arteryNormal PI, no notching 15 4Normal PI, notching 29 2  High PI:  P = 0 . 3 High PI, no notching 1 0 Notching:  P = 0 . 5 High PI, notching 12 4 During uterine contractions Placental side arteryClass 1 16 0Class 2 7 2Class 3 25 7  P ≥ 0 . 3§ Class 4 0 0Class 5 6 0Contraplacental side arteryClass 1 8 0Class 2 9 3Class 3 29 6  P ≥ 0 . 6§ Class 4 1 0Class 5 4 0 During uterine relaxations Placental side arteryNormal PI, no notching 16 4Normal PI, notching 36 5  High PI:  P = 1 . 0 High PI, no notching 1 0 Notching:  P = 0 . 5 High PI, notching 1 0Contraplacental side arteryNormal PI, no notching 12 3Normal PI, notching 32 4  High PI:  P = 0 . 6 High PI, no notching 1 0 Notching:  P = 0 . 7 High PI, notching 6 2Statistics with Fisher’s exact test.  * Values are number of cases.  † Flow velocity waveforms not obtained during the oxytocin challenge test(OCT) from three OCT-positive cases in the placental side uterine artery and in six cases from the contraplacental side artery.  ‡ Flow velocitywaveforms not obtained during the OCT from one OCT-positive case in the placental side uterine artery and in another case from thecontraplacental side artery.  § Rows merged to allow statistical comparisons (see text). PI, pulsatility index. (NB. For definition of high PI andnotching see text.) Birth asphyxia was diagnosed in four cases, oneof them OCT-positive and three OCT-negative. Incomparison with cases without birth asphyxia ( n = 63)no statistically significant differences were found for PI ineither artery at basal measurements (Mann–Whitney  U  -test,  P = 0 . 1, 0.3) or during relaxations (Mann–Whitney U  -test,  P = 0 . 5, 0.5) or for FVW classes recordedduring contractions (Fisher’s exact test on merged data, P = 1 . 0 ≥ 0 . 3).During basal conditions there was no differencein PI between the SGA group ( n = 37) comparedwith the AGA group ( n = 29) or LGA group ( n = 1)(Kruskal–Wallis test,  P = 0 . 2 for placental side artery,0.6 for contraplacental side artery). During uterine relax-ations the PI in the placental side uterine artery inthe SGA group was higher than that in the AGAgroup and that in the LGA case (SGA = 0 . 76 ± 0 . 20,AGA = 0 . 66 ± 0 . 16, LGA = 0 . 54; Kruskal–Wallis test, P = 0 . 049; Mann–Whitney  U  -test for SGA vs. AGA, P = 0 . 02), but no difference was found in the contrapla-cental side uterine artery (Kruskal–Wallis test,  P = 0 . 3).No significant difference in FVW classes between SGAand AGA was found for recordings during uterine con-tractions (Fisher’s exact test on merged data,  P ≥ 0 . 09 forthe placental side artery,  P ≥ 0 . 1 for contraplacental sideartery). DISCUSSION Duetomethodologicalproblems,adynamicevaluationof the uterine circulation with Doppler velocimetry duringuterine contractions has gained little attention amongresearchers. The fact that blood FVWs recorded in theuterine artery represent downstream flow impedance not Copyright © 2004 ISUOG. Published by John Wiley & Sons, Ltd.  Ultrasound Obstet Gynecol   2004;  24 : 429–434.  Uterine flow during OCT   433 only in the placental bed but also in parts of the uterusand vagina not involved in the placental circulation hasbeen regarded a major confounder against the use of uterine artery blood flow analysis in clinical practice.Flow recordings more distally in the uterine arterialtree only partly represent the uteroplacental circulation.Another confounding factor is that the blood supplyto the upper parts of the uterus may be conveyedthrough anastomoses with branches of the ovarianarteries. Nevertheless, abnormal uterine artery Dopplervelocimetry has proved to be able to identify cases atincreasedriskofdevelopingcomplicationsassociatedwithimpaired placental development and function 11 , 14 , 18–20 .Although this concept is disputed 21 , we hypothesized thata dynamic evaluation of the uterine circulation duringcontractions would reflect the fetus’ ability to cope withanaerobic stress.Dynamic uterine artery blood flow changes might havea different etiology andimpact onoutcome measuresthanchronic flow changes, and our study findings could notconfirm the hypothesis of a clinical value of uterine arteryDoppler velocimetry during contractions. Although therewas a tendency towards a higher uterine artery vascularflow resistance in the placental side uterine artery inOCT-positive cases compared with OCT-negative casesduring basal conditions, Doppler flow recordings duringuterine contractions and relaxations revealed no furtherdifferences between the groups. This was valid also forthe presence of diastolic notching and high PI duringbasal conditions and relaxations. Furthermore, FVWsrecorded in cases requiring ODFD or suffering birthasphyxia showed no difference in pattern compared withcases without these complications. However, the indexcase sample sizes were small and did not allow for safeconclusions in these matters.The only significant finding in the present study wasa higher placental side uterine artery PI in SGA casescompared with AGA and LGA cases during uterinerelaxations. There was also a tendency towards differentFVW patterns recorded during uterine contractions, withthe more severe biphasic flow patterns more commonlyrecorded in SGA than in AGA cases. During basalmeasurements no significant difference was found ineitherartery.Thesefindings mightrepresent placentalandplacental bed lesions functionally revealed only duringuterine contractions. In a previous small study, Olofsson et al  . 7 found a lower uterine artery PI in SGA casesand speculated that blood is shunted from the uterinearterial circulation to uterine veins due to obliterationof uteroplacental vessels, but this hypothesis was notsupported by the present results.The functionalreserve capacity of the placenta in IUGRis thought to be predicted by umbilical artery Dopplerflow velocimetry 22 and revealed by the OCT 10 , 23–25 . In aprevious study of IUGR fetuses we found partial supportfor this hypothesis: in cases of high umbilical arteryvascular flow resistance the OCT was positive twice asoften as in cases with normal flow, but in OCT-negativecases uneventful vaginal delivery was equally commonin the two groups 26 . Similarly, it has been claimed thatumbilical artery Doppler velocimetry has a limited valuein predicting development of fetal distress in labor 27–29 .In the present study the question was, however, to whatextent a placental circulatory dysfunction affecting thefetus is reflected by any dynamic uterine artery blood flowchanges during the OCT. During uterine inertia, a highuterine artery vascular flow resistance correlates withplacental bed spiral artery pathology 30 , 31 but not withplacental histopathology 31 . Conversely, a high umbilicalartery flow resistance correlates with placental pathologybut not with placental bed spiral artery pathology 31 .Thus, uterine artery Doppler velocimetry may be a too‘remote’ and diffuse tool to test the placental reservecapacityandrevealcaseswithslighttomoderateplacentalinsufficiency.InarecentstudyonuterinearteryFVWshapesrecordedduring uterine contractions we found significant differ-ences between waveform patterns recorded during theOCT and during spontaneous labor 15 . Reversals of flowdirection were more common during oxytocin-provokedcontractions than during spontaneous contractions. Thisfinding might have a clinical implication and is worth fur-ther exploration. Recordings of the uterine artery FVWsduring the OCT, with the aim of revealing imminent fetaldistress, is an issue that needs to be further elucidatedin larger studies and in comparison with uncomplicatedcases. ACKNOWLEDGMENTS This study was supported by grants from Region Sk˚aneand Sydv ¨astra Sk˚anes sjukv˚ardsdistrikt. Mss Lena Berg,Maria Nilsson, Pia Soikkeli and Ann Thuring-J ¨onsson aregratefully acknowledged for expert technical assistance. REFERENCES 1. Stuart B, Drumm J, FitzGerald DE, Duignan NM. Fetal bloodvelocity waveforms in uncomplicated labour.  Br J Obstet Gynaecol   1981;  88 : 865–869.2. Fleischer A, Anyaegbunam AA, Schulman H, Farmakides G,Randolph G. Uterine and umbilical artery velocimetry duringnormal labor.  Am J Obstet Gynecol   1987;  157 : 40–43.3. Fairlie FM, Lang GD, Sheldon CD. Umbilical artery flowvelocity waveforms in labour.  Br J Obstet Gynaecol   1989; 96 : 151–157.4. Brar HS, Platt LD. Reverse end-diastolic flow velocity onumbilical artery velocimetry in high-risk pregnancies: anominous finding with adverse pregnancy outcome.  Am J Obstet Gynecol   1988;  159 : 559–561.5. Murakami M, Kanzaki T, Utsu M, Chiba Y. Changes in theumbilical venous blood flow of human fetus in labor.  NipponSanka Fujinka Gakkai Zasshi  1985;  37 : 776–782.6. Damron DP, Chaffin DG, Anderson CF, Reed KL. Changes inumbilical arterial and venous blood flow velocity waveformsduring late decelerations of the fetal heart rate.  Obstet Gynecol  1994;  84 : 1038–1040.7. Olofsson P, Thuring-J ¨onsson A, Mars ´al K. Uterine and umbil-ical circulation during the oxytocin challenge test.  Ultrasound Obstet Gynecol   1996;  8 : 247–251.8. Janbu T, Koss KS, Nesheim BI, Wesche J. Blood velocities inthe uterine artery in humans during labour.  Acta Physiol Scand  1985;  124 : 153–161.Copyright © 2004 ISUOG. Published by John Wiley & Sons, Ltd.  Ultrasound Obstet Gynecol   2004;  24 : 429–434.
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