Umbilical venous pulsatility and volume blood flow in complicated pregnancies: Correlation with the umbilical artery blood velocity waveforms

EUROPEAN JOURNAL OF

~ LTFIiI~II©~NII) European Journal of Ultrasound 2 (1995) 51-56

Clinical report

Umbilical venous pulsatility and volume blood flow in complicated pregnancies: correlation with the umbilical artery blood velocity waveforms Krzysztof Preis, Saemundur Gudmundsson*, Karel Marsal Department of Obstetrics and Gynaecology, University of Lurid, Maim6 General Hospital, S-21401 Malmt. Sweden

Received 10 April 1994; revision received 13 October 1994;accepted 29 October 1994

Abstract The purpose of this retrospective work was to evaluate Doppler recorded umbilical venous volume blood flow in complicated pregnancies with abnormal umbilical venous pulsatility. During 1632 examinations abnormal pulsatility was found in 14 fetuses having normal volume flow. There were four perinatal deaths, all in pregnancies with absent blood velocity in the umbilical artery and abnormal umbilical venous pulsatility, suggesting that measurements of umbilical venous blood velocity should be included in the surveillance of pregnancies with absent diastolic blood velocity. Keywords: Doppler ultrasound; Umbilical vein pulsation; Volume blood flow measurement; Umbilical artery and peri-

natal outcome

1. Intrmluetion Doppler ultrasonography of fetal arterial blood velocity has become a routine part of clinical surveillance in complicated pregnancies in recent years. Fetal venous blood velocity recording has more recently been evaluated and found to yield important clinical information on fetal condition. Abnormal umbilical venous pulsatility has been reported to occur in cases of cord occlusion (Utsu et al. 1991), fetal heart failure (Gudmundsson et al. * Corresponding author.

1991), or imminent fetal asphyxia (Lingman et al. 1986a; Rizzo et al. 1992a). Volume blood flow in the umbilical vein and the fetal aorta, the variables chiefly used during the early days of Doppler ultrasonography at our unit, were subsequently found to be of limited clinical value in complicated pregnancies. Recordings tended to yield values within normal reference values, despite the presence of signs of increased placental vascular resistance (Laurin et al. 1987). Doppler volume blood flow measurements are now only used at our unit to evaluate fetal circulation in fetuses with ar, rhythmia and in pregnancies complicated by Rh-

0929-8266/95/$09.50 © 1995 ElsevierScienceIreland Ltd. All rights reserved SSDI 0929-8266(94)0008l-N

52

K. Preis et al./ European Journal of Ultrasound 2 (1995) 51-56

isoimmunisation. Instead, Doppler recordings of fetal arterial blood velocity waveforms are currently being used for routine fetal surveillance. As volume blood flow in fetuses with umbilical venous pulsatilty had never been evaluated, we retrospectively analysed our findings in pregnancies characterised by this abnormal blood velocity pattern to ascertain whether fetal umbilical venous volume blood flow might be a predictor of pregnancy outcome.

2. Materials aml metheds Data from a total of 1632 Doppler ultrasound recordings of umbilical venous volume blood flow, performed at our unit during the 6-year period, 1987-1992, were screened for signs of abnormal umbilical venous pulsatility. The main indications for Doppler ultrasonography were: intrauterine growth retardation, pre-eclampsia, diabetes, third trimester haemorrhage, post-term pregnancy, decreased fetal movements, Rh-isoimmunisations, or fetal arrhythmia. Umbilical artery and vein blood velocities were recorded with a 2-MHz pulsed Doppler ultrasound instrument (Alfred, Ving-Med A/S, Oslo, Norway) combined with a 3.5-Ml-lz real-time linear array ultrasound scanner (ADR, Model 2130, Advanced Diagnostic Research Corp, Tempe, AZ) as described by Eik-Nes et al. (1984). A 100-Hz high-pass filter was used to remove interfering signals from slow-moving tissues in the path of the Doppler beam. The quality of signals was monitored from the Doppler shift spectrum displayed on a oscilloscope (Hewlet-Packard, Colorado Springs, CO). Output signals of maximum velocities were recorded on a polygraph and stored in a microcomputer (ABC 806, Luxor, Motala, Sweden) with a curve-fitting program for waveform analysis. The free floating part of the umbilical cord was visualised in the araniotic fluid, the sample volume positioned and the umbilical artery flow velocity waveforms recorded. If the end-diastolic blood velocity was absent, then the blood velocity pattern was reproduced at three different angles, the waveforms with the greatest diastolic blood velocity being accepted for analysis. Intra-abdominal

umbilical vein diameter was measured using the method of Eik-Nes et al. (1984), the value obtained being the mean for 10 frozen vessel ultrasound images. The insonation angle (between the Doppler ultrasound beam and the vessel) was always 45 °. Volume blood flow ({2) was calculated (in ml/min) using the formula: Q = (.

V cos 45°

2.7)

xd2 4

where V is the mean blood velocity (cm/s), d the vessel diameter (cm), and 1/cos 45 ° the factor used to correct recorded velocity for the insonation angle. As mean blood velocity in the umbilical vein is overestimated when the high-pass filter is used, values were corrected using the constant 2.7, according to Eik-Nes et al. (1984). Fetal weight was estimated using the formula proposed by Persson and Weldner (1986): fetal w e i g h t = B P D 1'321 X A D 1"s33 X 10 -2.830

where BPD is biparietal diameter, and AD abdominal diameter. Umbilical venous blood flow per kilogram of fetal weight was calculated and related

:~.~:--I~ ~ t , Z ~ , l . ~:~,..~: ! ' . ' ; I - : £ ; L z ' : t : :" :: ~ .i-.~

....

.... - : : : i : : : ! } - : : : ~ - :

....

: ~ ~..:t

-.~ ~1.- :..i _ _ ~ . ~ _ - : ~ .~__ . ~'.L. :'-2_: .-.~: 7 7 . : " / : - : " ~ ' : ' ~ P . - ~1" - "

II ....

: ~ ,.~

..... L : ~ = I ! ~:~

• :r:~F:

[:-:~ -

~-

!.-,

Fig. 1. Doppler ultrasound recordings of maximum blood velocity waveforms in the intra-abdominal part of the umbilical vein. Top: normal blood velocity recording. Bottom: blood velocity recording showing abnormal heart-synchronous pulsations. The horizontal axis expressing time in s and the vertical axis blood velocity in m/s.

53

K. Preis et al./ European Journal o f Ultrasound 2 (1995) 51-56

to normal reference values (Lingman and Marsal 1986b). Blood velocity tracings in the umbilical vein (UV) were analysed for presence of pulsations. Abnormal pulsations were defined as a decrease in velocity by more than 15% from the basal state. Umbilical artery blood velocity waveforms were analysed for pulsatility index (PI) according to Gosling et al. (1971). The blood velocity waveform pattern in the umbilical artery was used to classify the cases according to four blood flow classes (BFC) according to Laurin et al. (1987) and defined as: normal BFC, a PI within normal limits; BFC 1, positive diastolic blood velocity and a PI > mean + 2 S.D.; BFC 2, absent end-diastolic blood velocity; and BFC 3, absent diastolic blood velocity throughout diastole or reversed blood flow. The reference values of Gudmundsson and Marsal (1988) for umbilical artery pulsatility index were used as reference. Attendant clinicians were informed of the umbilical artery waveform analysis, but not of the presence of the abnormal venous pulsatility or the results of volume blood flow measurement. Outcome of pregnancy was evaluated in terms of gestational age at delivery, whether the neonate was small for gestational age (birth weight below the mean - 2 S.D. o f the normal Maim6 population according to Persson and Weldner (1986)), and perinatal mortality. Fisher's exact test was used for statistical evaluation of the results.

Table 2 The relationshipbetweenumbilicalvenouspulsatilityand mortality in all pregnancies in the BFC 3 subgroup Umbilical venous Survival pulsatility

Mortality

Absent Present

I 4

12 2

Differencebetween groups: P < 0.05.

the 6-year period, in all 14 of which values for relative umbilical venotis volume blood flow were within normal reference limits. There were four perinatal deaths in this group o f fetuses, one in utero and three during the neonatal period. The distribution of abnormal umbilical venous pulsatility and mortality by BFC is given in Table I. Of the 1632 pregnancies, 20 were in the subgroup BFC 3. The relationship between umbilical venous pulsatility and mortality in cases of BFC 3 is given in Table 2. Table 3 gives a more detailed description of the pregnancies with abnormal pulsations in the intra-abdominal part of the umbilical vein. Two of the fetuses died in-utero, one being a twin that was delivered more than 3 weeks later. 4. Discussion

3. Reselts

At retrospective analysis, abnormal umbilical venous pulsatility was observed in 14 cases during

Table 1 Distribution of intra-abdominal umbilical venous pulsatility and perinatal mortality by blood flow class (BFC) BFC

Umbilical vein puisatility (n)

Perinatalmortality (n)

Normal

4

0

1

0

0

2 3

4 6

0 4

Absent end-diastolic blood velocity throughout diastole or reversed blood velocity in the umbilical artery (i.e. BFC 3) is an accepted sign of a severely compromised fetus at high risk of morbidity and mortality (Hacket et al. 1987; Laurin et al. 1987; Johnstone et al. 1988). The presence of abnormal umbilical venous pulsatility has also been reported to be associated with poor outcome of pregnancy (Lingman et al. 1986a; Gudmundsson et al. 1991; Rizzo et al. 1992a). Normally, umbilical venous blood velocity is even and without pulsations. In the present study umbilical venous blood velocity was classified according to BFC (Table 1) and perinatal mortality was mainly related to the subgroup BFC 3 (4/6 cases), suggesting abnormal umbilical venous pulsatility as an ominous sign in a

54

K. Preis et al. /European Journal of Ultrasound 2 (1995) 51-56

Table 3 Pregnancieswith abnormal intra-abdominal umbilicalvenous(UV) pulsations in relationship umbilical artery blood flowclass (BFC) and outcome of pregnancy Gestational age (weeks + days) at

Complications of pregnancy BFC Mode of delivery Birthweight (g)

Apgar score

Days in the NICU

Diabetesmeilitus Fetal arrythmia SuspectedIUGR Post-termpregnancy SuspectedIUGR SuspectedIUGR Fetal hydrothorax SuspectedIUGR SuspectedIUGR Twins,growth retardation Diabetes,growth retardation SuspectedIUGR AbnormalCTG SuspectedIUGR

9+9+10 9+10+10 9+!0+10 9+ 10+10 8+10+10 7+9+10 5+5+7 9+10+10 9+9+10 0+0+0 8+9+10 0+0+0 8+10+10 9+10+10

3 0 0 0 8 18 11 0 19 a 6a a 0 20a

Examination Delivery 32+1 34+5 38+6 42+0 36+5 36+4 31+0 37+3 35+2 33+6 29+6 27+0 36+0 29+2

38+6 39+6 39+4 43+0 36+6 37+5 31+5 38+0 35+2 37+2 29+6 27+0 36+0 29+2

0 0 0 0 2 2 2 2 3 3 3 3 3 3

Vaginal 3180 Vaginal 3950 Vaginal 2940 Cesareansection 4060 Cesareansection 2115 Cesareansection 2040 Cesareansection 2320 Cesareansection 2400 Cesareansection 1750 Cesareansection 1050 Cesareansection 940 Vaginal 400 Cesareansection 2200 Cesareansection 815

Abbreviations: IUGR, intra-uterine growth retardation; CTG, cardiotocograph; NICU, neonatal intensive care unit.

aPerinatal or neonatal mortality.

compromised fetus, and might thus be a valuable clinical marker. By contrast, umbilical venous volume blood flow in fetuses with abnormal venous pulsatility was normal in all BFC subgroups. This finding, which may have been due to fetal capacity for circulatory compensation, was consistent with previous findings by our group when measuring umbilical volume blood flow i n complicated pregnancies (Laurin et al. 1987). Fetal lamb studies have also shown that umbilical venous blood flow can be maintained during hypoxia (Paulick et al. 1991), which might be explained by increased fetal blood pressure. Umbilical venous flow pulsatility has been found in normal first trimester pregnancies, disappearing between the 9th and 12th weeks of gestation (Rizzo et al. 1992b), its disappearance having been suggested to be due to the development of the ductus venosus as a pressure filter between the umbilical and fetal central venous circulation. The diameter of the human ductus venosus is normally half that of the umbilical vein (Edelstone 1980).

The presence of an anatomical sphincter between the umbilical vein and the ductus venosus has been reported in fetal lamb (Chacko and Reynolds 1956), which might explain the lack of transmission of inferior vena cava blood velocity pressure waveforms to the umbilical vein. Blood flow through the ductus venosus is known to increase during hypoxia, which also increases the blood flow through the foremen ovale and to the upper part of the body (Beherman et al. 1970; Chohn et al. 1974). The inferior vena cava (IVC) blood velocity is normally pulsatory, reflecting central venous pressure. Transmission of IVC reverse flow into the umbilical vein, corresponding to atrial contraction, wight be the sign of increased central venous pressure due to a failing fetal heart, as has been suggested in reports on fetuses with non-immune hydrops (Tulzer et al. 1994). Presumably, the increase in central venous pressure rise exceeds the regulatory capacity of the ductus venosus, resulting in umbilical vein pulsations synchronous with the fetal heart beat. Different types of umbilical cord venous blood

K. Preis et al. /European Journal of Ultrasound 2 (1995) 51-56

flow pulsatility have been reported to occur: during systole due to cord occlusion (Utsu et al. 1991), and in end-diastole during fetal heart failure or imminent fetal asphyxia (Lingman et al. 1986a; Gudmundsson et al. 1991). In the present study, recordings were only obtained from the intraabdominal part of the umbilical vein. In a recent publication of venous blood velocity during 90 min of hypoxia in a chronic fetal lamb model, abnormal venous pulsatility in the intra-abdominal part of the vein was seen as an early sign of hypoxia unrelated to fetal blood pH (Gudmundsson et al. 1993a). Umbilical venous blood velocity in the cord, however, remained normal throughout the study (Gudmundsson e t a l . 1993a). In another study of umbilical venous blood velocities in 19 human fetuses with absent end-diastolic blood velocities in the umbilical artery, cases with abnormal venous pulsatility in the cord were associated with poor perinatal outcome (Gudmundsson et al. 1993b). This suggests that abnormal umbilical pulsatility in the intra-abdominal part of the vein might be an early sign of hypoxia, and pulsatility in the free floating cord a late sign of hypoxia with poor prognosis. In the present study, abnormal umbilical venous pulsatility may have represented a milder or a temporary form of fetal compromise among the survivors in the normal BFC and BFC 2 subgroups (n = 10), but a more severe form of compromise in fetuses in the BFC 3 subgroup (Table 1) with pulsations that might have extended into the cord. Unfortunately, however, umbilical venous blood velocities were not recorded in these cases.

Acknowledgement This work was supported by grants from the Medical Faculty at the University of Lund.

References lkherman RE, Lees MH, Peterson EN, DeLannoy CW, Seeds AE. Distribution of the circulation in the normal and asphyxiated fetal primate. Am J Obstet Gynecol 1970; 108: 956-69. Chacko AW, Reynolds SRM. Embryonic development in the human sphincter of the ductus venosus. Anat Rec 1956; 115: 151-173.

55

Chohn HE, Sacks EJ, Heymann MA, Rudolph AM. Cardiovascular responses to hypoxemia and acidemia in fetal Iambs. Am J Obstet Gynocol 1974; 120: 817-24. Eik-Nes S, Marsal K, Kristoffersen K. Methodology and basic problems related to blood flow studies in the human fetus. Ultrasound Med Biol 1984; 10: 329-337. Edelstone DI. Regulation of blood flow through the ductus venosus. J Dev Physiol 1980; 2: 219-238. Gosling RG, Dunbar G, King DH, Side CD, Woodcoock JP, FitzGerald DE, Keates JS, MacMillan D. The quantitative analysis of occlusive peripheral arterial disease by nonintrusive ultrasonic technique. Angiology, 1971; 22: 52-55. Gudmundsson S, Marsal K. Umbilical and uteroplacental blood flow velocity waveforms in normal pregnancy - - a cross-sectional study. Acta Obstet Gynecol Scand 1988; 67: 347-54. Gudmundsson S, Huhta JC, Wood DC, Tulzer G, Cohen AW, Weiner S. Venous Doppler in the fetus with non-immune hydrops. Am J Obstet Gynecol 1991; 164: 33-37. Gudmundsson S, Gunnarsson G, H6keb~rd KH, Kjellmer l, Marsal K. Fetal lamb ductus venosus and umbilical venous blood velocity during hypoxia. J Maternal-Fetal Invest 1993a; 3: 197. Gudmundsson S, Tulzer G, Huhta JC, Marsal K. Venous Doppler velocimetry in fetuses with absent end-diastolic blood velocity in the umbilical artery. J Maternal-Fetal Invest. 1993b; 3: 196. Hacket G, Campbell S, Gamsu H, Chohen-Overbeck T, Pearce JMF. Doppler studies in growth retarded fetuses predict neonatal death, necrotising enterocolitis and haemorrhage. Br Med J 1987; 294: 13-16. Johnstone FD, Haddad NG, Hoskins P, McDicken W, Chambers S, Muir B. Umbilical artery Doppler flow velocity waveform: the outcome of pregnancies with absent end diastolic flow. Eur J Obstet Gynecol Reprod Biol 1988; 28: 171-178. Laurin J, Lingman G, Marsai K, Persson PH. Fetal blood flow in pregnancies complicated by intrauterine growth retardation. Obstet Gynecoi 1987; 69: 895-902. Lingman G, Laurin J, Marsal K. Circulatory changes in fetuses with imminent asphyxia. Biol Neonate 1986a; 49: 66-73. Lingman G, Marsal K. Fetal central blood circulation in the third trimester of normal pregnancy. Longitudinal study. I. Aortic and umbilical blood flow. Early Human Dev 1986b; 13: 137-150. Paulick RP, Meyers RL, Rudolph CD, Rudolph AM. Umbilical and hepatic venous responses to circulating vasoconstrictire hormones in fetal lamb. Am J Physiol 1991; 260: 1205-1213. Persson PH, Weldner BM. Intrauterine weight curves obtained by ultrasound. Acta Obstet Gynaecol Scand 1986; 65: 169-173. Rizzo (3, Arduini D, Romanini C. Inferior vena cava velocities in appropriate and small for gestational age fetuses. Am J Obstet Gynecol 1992a; 166: 1271-1280. Rizzo G, Arduini D, Romanini C. Umbilical vein pulsations: a physiologic finding in early gestation. Am J Obstet Gynecol 1992b; 167: 675-677.

56

K. Preis et al. /European Journal of Ultrasound 2 (1995) 51-56

Tulzer G, Gudmundsson S, Huhta JC, Wood DC, Cohen AW, Weiner S. Cardiovagular Doppler in the fetus with nonimmune hydrops. Ultrasound Obstet Gynecoi 1994; 4: 279-283.

Utsu M, Makio A, Narita K, Maeda K. Sonosraphic detection of pathological hypertondon of umbilicalcord and its blood flow waveform by pulsed Doppler technique. J Maternal Fetal Invest 1991; I: 109.