Uterine and umbilical artery velocimetry in pre-eclampsia

Acta Obstet Gynecol Scand 1998; 77: 614–619 Copyright C Acta Obstet Gynecol Scand 1998

Printed in Denmark – all rights reservedActa Obstetricia et

Gynecologica ScandinavicaISSN 0001-6349

ORIGINAL ARTICLE

Uterine and umbilical artery velocimetry inpre-eclampsiaKRISTEL VAN ASSELT, SAEMUNDUR GUDMUNDSSON, PELLE LINDQVIST AND KAREL MARSAL

From the Department of Obstetrics and Gynecology, University of Lund, University Hospital MAS, Malmo, Sweden

Acta Obstet Gynecol Scand 1998: 77: 614–619. C Acta Obstet Gynecol Scand 1998

Background. The aim of the present study was to evaluate whether Doppler velocimetry ofthe placental circulation can predict adverse outcome of pregnancies complicated by pre-eclampsia and whether there is a correlation between maternal blood pressure, proteinuriaand placental vascular resistance.Material and methods. One hundred and eight pregnant women with pre-eclampsia were fol-lowed and examined by Doppler velocimetry of the uterine arteries. The presence of a notchand the mean pulsatility index (PI) in the two arteries were recorded. The velocity waveformsin umbilical arteries were also evaluated. The Doppler velocimetry results were related to theperinatal outcome, maternal blood pressure and proteinuria.Results. Abnormal arterial blood velocity waveforms on both sides of the placenta weresignificantly correlated with a shorter gestational age at delivery, lower birthweight, increasedcesarean section rate and more frequent admissions to the neonatal intensive care unit. Bilat-eral rather than unilateral uterine artery notches were predictive of poor perinatal outcome.The combination of umbilical and uterine artery waveform results was the best predictor ofadverse outcome. The uterine artery velocimetry was, however, not related to maternal bloodpressure or the degree of proteinuria.Conclusions. Abnormal velocity waveforms in the uterine and umbilical arteries have clinicalsignificance in pregnancies complicated by pre-eclampsia and predict adverse outcome ofpregnancy, especially the fetal growth restriction and need for operative interventions duringlabor and delivery.

Key words: Doppler velocimetry; notch; perinatal outcome; pre-eclampsia; pulsatility index:umbilical artery; uterine artery

Submitted 28 October, 1997Accepted 6 December, 1997

Approximately 8–10% of pregnancies in primigra-vidas are complicated by pre-eclampsia or preg-nancy induced hypertension (PIH), with increasedmaternal and perinatal mortality and morbidity(1–3). The etiology of pre-eclampsia is still notcompletely known. Several theories have been pro-posed concerning for example possible genetic sus-ceptibility (4), and an imbalance of prostacyclinand tromboxane (5). There is an indication that

Abbreviations:PI: pulsatility index: NICU: neonatal intensive care unit; SGA:small for gestational age newborns; MAP: mean bloodpressure.

C Acta Obstet Gynecol Scand 77 (1998)

the maternal immune system plays an importantrole (6). Several patho-physiological mechanismswere described, the main underlying abnormalitybeing general vasoconstriction and increased vas-cular sensitivity to pressor peptides and amines.Vasoconstriction leads to hypertension, especiallyto elevated diastolic blood pressure. Tissue damageoccurs as a consequence of the vasoconstrictionand the activation of coagulation system in severalorgans, e.g. the kidneys and liver. Proteinuriamight be a marker of tissue damage (7).

The uteroplacental blood flow increases tenfoldduring pregnancy (8, 9). This increase in bloodflow is facilitated by dilatation of the uteroplacen-

Doppler velocimetry in pre-eclampsia 615

tal vessels (10). One of the main features of pre-eclampsia is an abnormal placentation by inad-equate trophoblastic invasion of the maternalspiral arteries. The dilatation of the spiral arteriesis therefore halted and blood flow supply reduced(11, 12).

Doppler examination makes it possible to recordnon-invasively the blood flow velocity waveforms(FVW) of the uterine and umbilical arteries. TheDoppler method has been found clinically usefulin predicting adverse outcome of pregnancy inhigh-risk pregnancies, especially in cases of sus-pected intra-uterine growth retardation (14, 15).An early diastolic notch in the uterine artery bloodvelocity waveform is typical for an increased utero-placental vascular resistance, but can be a physio-logical finding before 26 weeks of gestation (13).

The aim of the present study was to evaluatewhether Doppler velocimetry of the placental cir-culation could predict adverse outcome in preg-nancies complicated by pre-eclampsia and to inves-tigate whether a correlation exists between ma-ternal blood pressure, proteinuria and increasedplacental vascular resistance.

Material and methods

A total of 108 pregnant women were enrolled inthis study. All women were referred to the Dopplerultrasound laboratory for fetal evaluation becauseof pre-eclampsia which was defined as: severe pre-eclampsia (systolic blood pressure Ø160 mmHgand diastolic Ø110 mmHg and/or proteinuria ofπ3 (Ø3.0 g/L) (Redia-test, Boehringer MannheimGmbH, Mannheim, Germany)) or mild pre-ec-lampsia (systolic blood pressure 145–155 mmHgand diastolic 90 to 105 mmHg and proteinuria π1or π2 (±0.3 and ∞3.0 g/L). Eighty out of 108women had mild pre-eclampsia and twenty-eightsevere pre-eclampsia. All women had a singletonpregnancy.

Blood pressure and proteinuria were measuredat the same time as the last Doppler ultrasoundexamination before delivery. The mean bloodpressure (MAP) was defined as systolic bloodpressure π2 diastolic blood pressure/3. Gestationalage was ascertained in all patients by routine ultra-sound examination at 18 weeks of pregnancy. Theplacenta location was determined during the rou-tine ultrasound examination at 32 weeks of ges-tation and was classified as either mainly unilateralor central including fundal, anterior and posterior.

Doppler examinations were performed with anAcuson 128 XP duplex scanner with pulsed andcolor Doppler options using 3.5 MHz transducerand 125 Hz high-pass filter. Recordings from theumbilical artery were obtained from a free-floating


central part of the cord during absence of fetalbreathing and body movements. Both uterine ar-teries were located by color Doppler imaging andthe sample volume placed in the vessels cranial tothe crossing of the iliac arteries.

The obtained blood velocity waveforms wereanalyzed for Pulsatility Index (PI) according toGosling et al. (16). Three subsequent heart cycleswere analyzed and PI values were related to nor-mal reference values for umbilical and uterine ar-teries (15, 17). Mean PI of both uterine arteries±1.20 was considered abnormal. Abnormal um-bilical artery PI values were those above the meanπ2 s.d. for gestational age.

The results of the last examination before deliv-ery were correlated to perinatal outcome char-acterized by gestational age at birth, birthweight,birthweight deviation in percent from the mean ofthe normal population, placental weight, mode ofdelivery, Apgar score at 1 and 5 min of life, inci-dence of admission to the neonatal intensive careunit (NICU) as well as umbilical cord arterial andvenous blood pH. Small for gestational age (SGA)newborns were defined as a birthweight belowmean ª2 s.d. of the Scandinavian population (18).

Fisher’s exact test, Student’s t-test and oddsratio with confidence interval were used for stat-istical analysis, p∞0.05 being regarded as signifi-cant. Spearman rank correlation coefficient wasused for the analysis of relationship between thedegree of proteinuria and uterine artery PI andmean arterial pressure.

Results

Patient characteristics according to the type of pre-eclampsia are given in Table I. Although the uter-

Table I. Patient characteristics and results of Doppler velocimetry. Median(range), numbers or percentages are given

Type of pre-eclampsia

Severe Mild p value

Number 28 80Gestational age at the last 37 (27-42) 39 (27-42) 0.02examination (weeks) (range)Primiparity 23 (82%) 49 (61%) 0.04Placenta location

unilateral 5 (18%) 22 (28%) NScentral 23 (82%) 58 (72%) NS

Uterine artery notchabsent 12 (43%) 50 (62%) NSbilateral 7 (25%) 12 (15%) NSunilateral 9 (32%) 18 (23%) NS

Abnormal uterine artery PI 9 (32%) 15 (19%) NS(±1.20)Abnormal umbilical artery PI 6 (21%) 11 (14%) NS(±meanπ2 s.d.)

PI: pulsatility index; NS: non-significant.

616 K. van Asselt et al.

Fig. 1. The mean pulsatility index (PI) in the two uterine arter-ies plotted against the degree of proteinuri.

ine artery PI showed a significant positive corre-lation to the degree of proteinuria at the time ofthe last Doppler examination (correl. coeff.Ω4.18;R2Ω0.29; p∞0.0001), the values overlapped greatlybetween different goups (Fig. 1). No relationshipwas found between the uterine artery PI and themean maternal blood pressure at the time of exam-ination.

The median gestational age at the last examin-ation was 37 weeks (range 25–42) and at delivery38 weeks (range 25–42 weeks). The median timeinterval between examination and delivery was 3.5days (range 0–25). There were 81 placentas cen-trally located in the uterus and 27 were mainly uni-lateral. In cases of unilateral placenta, the meanuterine artery PI on the placental side was0.85∫0.42 (∫s.d.; range 0.27 to 2.43), and of thenon-placental side 1.24∫0.65 (range 0.44 to 2.98).

Outcome of pregnancy for patients with abnor-mal uterine (nΩ24) and umbilical artery (nΩ17) PI

Table II. Perinatal outcome in relation to the results of umbilical and uterine artery Doppler velocimetry in 108 pregnant women with pre-eclampsia. Numbers,percentages and mean ∫s.d. are given

Uterine artery PI: Normal Abnormal Normal Abnormal

Umbilical artery PI: Normal Normal p-value* Abnormal p-value* Abnormal p-value

Number 76 15 8 9

Gestational age (weeks) 38.6∫2.5 36.5∫2.5 0.005 36.6∫3.3 NS 31.7∫5.1 0.0005Birthweight (g) 3352∫734 2472∫671 0.0005 2394∫795 0.025 1351∫774 0.0005B-weight deviat. (%) 0.1∫14.7 ª16.6∫12.1 0.0005 ª20.9∫13 0.0005 ª34.6∫11.5 0.0005SGA (Æmean - 2 s.d.) 4 5 0.006 2 NS 7 0.0001Placental weight (g) 632∫173 441∫86 0.0005 426∫92 0.0005 383∫166 0.0005Cesarean section 23 8 NS 5 NS 8 0.002NICU admission 12 5 NS 5 0.008 8 0.0001

PI: pulsatility index; SGA: small for gestational age i.e. birthweight below the mean - 2 s.d. of normal population; NICU: neonatal intensive care unit; NS: non-significant. * Ω compared with cases with normal blood velocity on both sides of the placenta.


is given in Table II. A significantly shorter ges-tational age at delivery (p∞0.01), lower birthweight(p∞0.0025) and higher birthweight deviation(p∞0.0005), more SGA newborns (p∞0.03) andmore frequent admissions to the NICU (p∞0.03)were seen in the group with abnormal PI in bothuterine and umbilical arteries when compared withcases with abnormal PI on one side of the placentaor with normal PI on both sides (Table II).

The perinatal outcome in relation to the occur-rence of a notch in the uterine arteries is given inTable III. When compared with cases with normaluterine artery blood velocity, the likelihood of de-livering a SGA newborn was increased eight timesin the presence of a unilateral notch and ten timesin cases with bilateral notch (Table III). In the sub-group with bilateral notches, there was a 4–5 timesincreased likelihood of cesarean section and admis-sion to the NICU. No relationship was found be-tween increased placental vascular resistance andlow Apgar score or pH at delivery.

Discussion

In the present study, umbilical artery and uteropla-cental Doppler velocimetry was evaluated in re-lation to the perinatal outcome in pregnanciescomplicated by pre-eclampsia. Abnormalities oneither side of the placenta were correlated to anunfavorable outcome of pregnancy (Tables II, III).When comparing the groups with signs of in-creased vascular resistance on one side of the pla-centa only, with the group with abnormal vascularresistance on both sides of the placenta, the ad-verse outcome of pregnancy was most frequent inthe latter group.

Proteinuria is a marker of tissue damage in pre-eclampsia. A significant relationship was found be-tween the degree of proteinuria and uterine arteryPI, but no association was found between mean


Table III. Perinatal outcome according to the occurrence of uterine artery notch. Mean∫s.d. and numbers are given

Notch

Odds ratio Odds ratioabsent unilateral p-value (95% confidence interval) bilateral p-value (95% confidence interval)

Number 62 27 19Gestational age (weeks) 38∫3 37∫3 NS - 35∫4 0.0005 -Birthweight (g) 3358∫875 2755∫784 0.0025 - 2133∫761 0.0005 -Birthweight deviation (%) 0.3∫17 ª12∫15 0.0025 - ª21∫13 0.0005 -SGA newborns 4 10 0.005 8.5 (2.7ª27) 8 0.0008 10.6 (3.2ª35.2)Placenta weight (g) 639∫187 516∫136 0.0005 - 427∫106 0.0005 -

Cesarean section 21 11 0.01 1.3 (0.5ª3.2) 13 0.009 4.2 (1.5ª12.2)NICU admissions 12 6 NS 1.2 (0.4ª3.6) 10 0.007 4.6 (1.6ª13.3)

SGA: small for gestational age i.e. birthweight below the mean - 2 s.d. of normal population; NICU: neonatal intensive care unit;NS: non-significant. The p-values and odds ratio describe the significance of difference as compared with the subgroup with absent notches.

maternal arterial pressure and uterine artery PI.Some of the more severe pre-eclampsia patientswere on antihypertensive medication (pindolol),which might have decreased the blood pressurewithout changing placental vascular resistance orthe degree of protein leakage in the urine andtherefore might have masked the possible relation-ship between uterine artery vascular resistance andmaternal blood pressure.

Biopsies from the placental bed during cesareansection have shown that the ingrowth of cytotro-phoblast into the sub-placental arteries is less ad-vanced in cases complicated by pre-eclampsia andIUGR than in normal pregnancies. In normalpregnancies the sub-placental arteries can be trans-formed to flaccid non-contractile channels as faras into the central part of the myometrium (19,20). The change in the sub-placental vessels is morepronounced under the central part of the placentathan in the periphery. The lack of transformationof the sub-placental vessels might cause decreasedplacental perfusion, and also a release of some yetunknown agent which increases maternal bloodpressure in order to maintain placental blood flow.This agent has never been found, but the fact thatthe disease is cured by removal of the placenta doessuggest it strongly.

The first reports on uteroplacental Dopplervelocimetry in high-risk pregnancies reported lowsensitivity for the prediction of SGA newborns (29 to 39%) (21–24). Arcuate artery blood velocityrecording was used in these studies in order to pre-dict uteroplacental vascular resistance. As theblood velocity waveforms were obtained blindlyfrom the sub-placental myometrium, a recordingmight sometimes have been obtained from spiralarteries distal to the vascular narrowing, in the di-lated part of the vessel, wrongly giving the im-pression of normal peripheral vascular resistanceas has been described by Gudmundsson and Mar-


sal (25). Focusing on the main uterine arteries hasgreatly improved the predictive value of the ar-terial blood velocity waveform giving sensitivitiesof SGA newborns between 43 to 78% in high-riskpregnancies (13, 15, 26, 27).

The results from the present study showed thatonly 24 cases had an abnormal uterine artery PI(22%); 32% in severe and 19% in mild pre-eclamp-sia groups. The corresponding percentages for theumbilical artery velocimetry were 14%, 18% and13%, respectively. A notch in one or both uterinearteries was, however, more frequent, (46 cases,43%). Although a uterine artery notch is morecommon in pre-eclamptic patients than an abnor-mal PI, the predictive value of an early diastolicnotch seems to be inferior to an increased uterineartery PI with regard to abnormal outcome. Thesensitivity of abnormal uterine artery PI for cesar-ean section delivery was 71% in the present study.The sensitivity for a unilateral uterine artery notchwas 52% and for a bilateral notch 68%. The corre-sponding figures for prediction of SGA-newbornswere 50%, 30% and 42%, respectively. These resultsare similar to findings by Hofstaetter et al. (15)studying a mixed group of high-risk pregnancies,although the sensitivities in the present study wereslightly higher.

An early diastolic notch can be a physiologicfinding till 24–26 gestational weeks. In the presentstudy, only two women had their last examinationperformed before 26 completed weeks of gestation.Screening for uterine artery notches in mid-ges-tation has been reported with high sensitivity foradverse perinatal outcome later in gestation (28,29). Bower et al. (30) recommended a two-stagescreening of notches in the uterine arteries. Firstat 18–22 weeks of gestation and then at 24 weeks,implying that abnormal blood velocity waveformsin the uterine artery after that time were highlypredictive of adverse outcome of pregnancy. Other

618 K. van Asselt et al.

reports have been more sceptical on the use ofscreening, only half of the cases that developedpre-eclampsia or delivered a SGA infant were iden-tified. The best results gave a 33% positive predic-tive value for either pre-eclampsia or SGA (31). Asonly 43% of the pre-eclamptic pregnancies in thepresent study had notches in the uterine arteries,screening for pre-eclampsia before 26 weeks of ges-tation might therefore have unacceptably low sen-sitivity and a high number of false-negative casesfor a general population screening.

Previous reports have shown that abnormaluterine artery vascular resistance can be found in15% to 64% of cases complicated by pre-eclamp-sia or PIH (32–36). Differences in gestational ageat the time of examination might be one factorexplaining the large variation, but differences inblood velocity waveform parameter used foranalysis (S/D-ratio or PI), in Doppler techniqueused, and populations might also be involved.

There has been a disagreement on where tolook for uterine artery abnormalities – eitherunilaterally, bilaterally, on the placental or on thenon-placental side of the placenta (15, 32, 36).Kofinas et al. (36) concluded that the uterine ar-tery PI on the placental side was the best predic-tor of poor perinatal outcome. In contrast Gon-ser et al. (37) found the uterine artery on thenon-placental side to be a better predictor ofperinatal outcome. Hofstaetter et al. (15) re-ported that the mean PI of both uterine arteriesPI had the best perinatal predictive value, fol-lowed by PI on placental side. The PI on thenon-placental side was the worse predictor ofoutcome. The number of unilateral placentas inthe present study was 27, which is too small formaking conclusions on the choice of differentplacental sites. The mean of both uterine arteryPI was therefore chosen for analysis.

The abnormal umbilical artery blood velocitywaveform was in the present study a strong pre-dictor of adverse perinatal outcome (Table II),which is in agreement with previous publications(25, 32).

In conclusion, abnormal vascular resistance inthe uterine and umbilical arteries were related toadverse outcome of pregnancies in cases compli-cated by pre-eclampsia. Abnormal blood velocitywaveforms on both sides of the placenta weresignificantly related to adverse outcome of preg-nancy characterized by premature delivery, fetalgrowth restriction, more frequent cesarean sec-tions and higher incidence of admissions to theNICU. Utero and fetoplacental blood veloci-metry might therefore be of clinical value in rou-tine surveillance of pregnancies complicated bypre-eclampsia.


Acknowledgments

This study was supported by the Medical Faculty, Universityof Lund, the Swedish Society of Medicine, the Swedish MedicalResearch Council (grant no. 5980), and University HospitalMalmo Research Funds.

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Address for correspondence:

Saemundur Gudmundsson, M.D., Ph.D.University of LundDepartment of Obstetrics and GynecologyUniversity Hospital MASS-205 02 MalmoSweden

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Uterine and umbilical artery velocimetry in pre-eclampsia